Surg Endosc (1997) 11: 12131215

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Minimally invasive surgical biopsy confirms PET findings in esophageal cancer

J. D. Luketich, P. Schauer, K. Urso, D. W. Townsend, C. P. Belani, C. Cidis Meltzer, P. F. Ferson, R. J. Keenan
University of Pittsburgh Medical Center, 300 Kaufmann Building, 3471 Fifth Avenue, Pittsburgh, PA 15213, USA Received: 6 December 1997/Accepted: 14 January 1997

Abstract. This report describes our initial experience using positron emission tomography (PET) scanning in esophageal cancer patients. In two patients PET identified distant metastatic disease missed by conventional staging. Laparoscopic biopsy provided histological confirmation of metastases. In the third patient, locoregional lymph nodes were identified by PET and confirmed by surgical staging. In this preliminary report, PET appears to be a promising new noninvasive modality for staging patients with esophageal cancer. Key words: Esophageal Cancer Positron emission tomography (PET) Thoracoscopy Laparoscopy

the T3 vertebral body and the sacroiliac region of the pelvis and an unsuspected liver metastasis. The presence of metastases was confirmed through laparoscopic biopsy. Surgical resection of the esophagus was not undertaken. Subsequently the patient developed a T3 radiculopathy and died of extensive metastatic disease 3 months later.

Case 2
A 64-year-old male was diagnosed with adenocarcinoma of the distal esophagus. CT scans of the chest and abdomen and a bone scan were negative for metastases. Endoscopic ultrasound revealed enlarged periesophageal and gastrohepatic lymph nodes. A PET scan was ordered to evaluate the extent of disease. The PET scan (Fig. 2) revealed foci of increased FDG uptake in the distal esophagus, periesophageal, and gastrohepatic lymph regions, consistent with a primary tumor and lymph node metastases. Biopsies taken at video-assisted thoracoscopic and laparoscopic staging procedures confirmed metastases to these lymph nodes. The patient was entered into a taxol-platinum neoadjuvant protocol.

Positron emission tomography (PET) is an imaging technology that can be used to assess tissue metabolism. The increased metabolic demands of tumors can be visualized through increased focal uptake of the positron-emitting tracer 18F-fluorodeoxyglucose (FDG). The distribution of FDG has been used to distinguish benign from malignant tissue in various types of cancers [4, 16]. This report describes the results of PET scanning in three patients with esophageal cancer.

Case 3
A 66-year-old male diagnosed with esophageal cancer underwent a transhiatal esophagectomy, gastric pull-up, and a neck anastamosis 6 months before presenting to our clinic with complaints of dysphagia and a single palpable left cervical lymph node. Metastatic esophageal cancer was confirmed by a fine-needle aspirate of the lymph node, and CT scans of the neck and chest showed no other disease. A PET scan was performed to assess the extent of metastatic recurrence. The PET image (Fig. 3) showed multiple foci of increased uptake of FDG in the cervical and supraclavicular nodes which were confirmed by fine-needle aspirate as sites of metastasis. Palliative radiotherapy was successful in relieving dysphagia.

Case reports

PET methods
Each patient was requested to fast after midnight the evening prior to the PET study. PET imaging was performed on the ECAT ART tomograph (CTI/Siemens PET Systems; Knoxville, TN), located in the UPMC PET Facility. An intravenous injection of 68 mCi of FDG was administered followed by a 45-min delay for tracer uptake, prior to whole-body imaging at six bed positions. Images were evaluated for regions of focally increased uptake relative to adjacent tissues and compared with CT scans for anatomic correlation.

Case 1
A 59-year-old male was diagnosed with localized adenocarcinoma of the distal esophagus and received neoadjuvant chemotherapy. Prior to esophagectomy, restaging including chest and abdominal CT and a bone scan which were negative for distant metastatic disease. A PET scan was performed to evaluate possible distant metastatic disease prior to surgery. The PET scan (Fig. 1) demonstrated unsuspected bone metastases to

Correspondence to: J. D. Luketich

Discussion Patients with esophageal cancer are frequently diagnosed late in the course of their disease, and up to 50% already

1214

Fig. 1. A PET scan (A) showing three sites of metastatic disease: (a) a thoracic vertebral metastasis, (b) a liver metastasis that was not seen on the abdominal CT scan, and (c) a sacroiliac bone metastasis. The bone scan (B) did not detect either of the two bone metastases. Fig. 2. A PET scan demonstrating periesophageal and gastrohepatic lymph node metastases in addition to the primary esophageal cancer. Fig. 3. A PET scan demonstrating multiple bilateral cervical lymph node metastases from esophageal cancer.

have metastatic disease at presentation. For those with metastatic disease, the outcome is extremely poor: Most patients die within 6 months. For apparently localized disease, surgical resection alone has been the traditional approach when

there is a potential for complete resection [2, 7, 8]. Unfortunately, surgery alone results in 5-year survival rates of only 2030% in most series, and many patients develop distant metastases within 6 months to 1 year. This suggests

1215

that clinically occult metastases were present at initial presentation. Recently, minimally invasive surgical staging has been employed to more accurately evaluate the extent of locoregional disease and to rule out clinically occult sites of metastases. Positron emission tomography (PET) scanning may facilitate the staging of esophageal cancer. Preliminary reports on the use of PET scanning in patients with nonsmall cell lung cancer (NSCLC) are encouraging [5]. Up to 90% sensitivity and specificity have been reported in the detection of mediastinal lymph nodes in NSCLC using PET. However, a false-positive rate of between 13 and 20% has been noted in some series, and the ultimate role of PET in staging NSCLC continues to be evaluated [1, 3]. Our results suggest PET scanning could play an important role as a noninvasive staging modality in patients with esophageal cancer. In this report, PET accurately detected local or distant unsuspected metastatic disease in all three patients. CT scans, bone scans, and endoscopic ultrasound failed to detect lymph node involvement in two patients and liver and bone metastases in one patient. The accurate detection of locoregional or distant metastases contributed significantly to the management of their disease. These preliminary results suggest that PET scanning may play a role in the noninvasive staging of patients with esophageal cancer and may provide targets for minimally invasive surgical biopsy.

References
1. Chin R, Ward R, Keyes JW, Choplin RH, Reed JC, Wallenhaupt S, Hudspeth AS, Haponik EF (1995) Mediastinal staging of non-small cell lung cancer with positron emission tomography. Am J Respir Crit Care Med 152: 20902096 2. Lerut T, DeLeyn P, Coosemans W, Van Raemdonck D (1992) Surgical strategies in esophageal carcinoma with emphasis on radical lymphadenectomy. Ann Surg 216(5): 583590 3. Patz EF, Lowe VJ, Goodman PC, Herndon J (1995) Thoracic nodal staging with PET imaging with FDG in patients with bronchogenic carcinoma. Chest 108(6): 16171621 4. Scott WJ, Schwabe JL, Gupta NC, Dewan NA, Reeb SD, Sugimoto JT (1994) Positron emission tomography of lung tumors and mediastinal lymph nodes using F-18-fluorodeoxyglucose. Ann Thorac Surg 58: 698703 5. Valk PE, Pounds TR, Hopkins DM, Haseman MK, Hofer GA, Greiss HB, Meyers RW, Lutrin CL (1995) Staging non-small cell lung cancer by whole body PET imaging. Ann Thorac Surg 60: 15731582 6. Wahl RL, Hutchins G, Buchsbaum D, Liebert M, Grossman HB, Fisher S (1991) F-18-2-deoxy-fluoro-D-glucose (FDG) uptake in human tumor xenografts: feasibility studies for cancer imaging with PET. Cancer 67: 15441550 7. Watson A (1994) Operable esophageal cancer: current results from the West. World J Surg 18: 361366 8. Zhang DW, Cheng GU, Huang GJ, Zhang RG, Liu XY, Mao YS, Wang YG, Chen SJ, Zhang LZ, Wang LJ, Zhang DC, Yang L, Meng PJ, Sun KL (1994) Operable squamous esophageal cancer: current results from the East. World J Surg 18: 347354

Surg Endosc (1997) 11: 11891193

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Video-assisted thoracoscopic treatment of spinal lesions in the thoracolumbar junction

T. J. Huang,1 R. W. W. Hsu,1 H. P. Liu,2 K. Y. Hsu,1 Y. S. Liao,1 H. N. Shih,1 Y. J. Chen1
Department of Orthopedic Surgery1 and Thoracic and Cardiovascular Surgery,2 Chang Gung Memorial Hospital, Chang Gung Medical College, Taipei, Taiwan, R.O.C. Received: 6 February 1997/Accepted: 8 April 1997

Abstract Background: The endoscopic treatment of spinal lesions in the thoracolumbar junction (T11L2) poses a great challenge to the surgeon. From November 1, 1995 to December 31, 1996, we successfully used a combination of videoassisted thoracoscopy and conventional spinal instruments to treat 38 patients with anterior spinal lesions. Twelve of them had lesions in the thoracolumbar junction. Methods: The so-called extended manipulating channel method was used to perform vertebral biopsy, discectomy, decompressive corpectomy, interbody fusions, and/or internal fixations in these patients. The size of the thoracoscopic portals was greater than usual in order to allow conventional spinal instruments and a thoracoscope to enter the chest cavity freely and be manipulated by techniques similar to those used in standard open surgical procedures. In this series, the procedures were performed by using either a three-portal approach (2.53.5 cm) or a modified two-portal technique involving a 56 cm larger incision and a small one for introducing the scope. Results: None of the operations resulted in injury to the great vessels, internal organs, or spinal cord. The total time for the operation ranged from 1.5 to 4.5 h (average, 3); and the total blood loss ranged from 50 to 3000 cc (average, 1050). One patient was converted to an open procedure due to severe pleural adhesion. Complications included two instances of transient intercostal neuralgia, one superfical wound infection, and one residual pneumothorax. Conclusions: The video-assisted technique with the extended manipulating channel method presented in this re-

port simplifies thoracoscopic spinal surgery in the thoracolumbar junction and makes it easier. It avoids division of the diaphragm, removal of the rib, and wide spread of the intercostal space, and it allows greater control of intraoperative vessel bleeding. Using this technique, the number of portals required during the procedure can be reduced. In addition, the technique reduces the endoscopic materials required, thus lowering overall cost. It is an effective and promising approach. Key words: Video-assisted thoracoscopic surgery Thoracolumbar junction Spinal lesions

Presented in part at the first combined meeting of the Leading European Spine Society, Zurich, Switzerland, 1619 October 1996; the third combined meeting of spinal and pediatric sections of West Pacific Orthopedic Association, Kochi, Japan, 58 November 1996; and the first Asian Pacific Workshop on Minimally Invasive Thoracic Surgery, Hong Kong, 2123 November 1996. Correspondence to: T. J. Huang, Department of Orthopedic Surgery, Chang Gung Memorial Hospital, Chang Gung Medical College, No. 5, Fu-Hsing St. 333, Kweishan, Taoyuan, Taiwan, R.O.C.

Standard open surgery techniques for spinal lesions in the thoracolumbar junction (T11L2) usually require division of the diaphragm, resection of the rib, and wide spreading of the surgical wounds. These procedures may result in increased pain, prolonged postoperative rehabilitation, extensive scarring, and longer hospitalization [5, 6, 8, 11]. Endoscopic procedures are widely used in peripheral joints, as well as thoracic, urologic, gynecologic, and general surgery. The use of thoracoscopy to treat spinal lesions is a relatively recent development [7, 8, 12, 13]. Among the variety of video-assisted thoracoscopic spinal procedures that have been reported are biopsy, discectomy, anterior releasing procedures in scoliosis surgery, decompressive corpectomy, interbody fusion, and internal instrumentation [1, 7, 8, 1113]. However, when this technique is used, many problems and complications can develop due to the limited trocar spaces and lack of suitability of endoscopic instruments [1, 68, 12, 13]. Problems are particularly likely to arise when the lesions are located in the thoracolumbar junction. Under one-lung ventilation, the high-riding diaphragm may occlude the lesion site; therefore, additional portals and special endo-equipment are needed to facilitate exposure. As many as four, five, or even more portals are common in these procedures [1, 8, 12, 13].

1190 Table 1. Clinical data for 12 patients with lesions involving the thoracolumbar function (T11L2) Case no. 1 2 3 4 5 6 7 8 9 10 11 12
a

Sex F M M M F F M F F M M F

Age (yr) 40 73 52 75 66 38 45 65 34 64 24 43

Final diagnosis (level) Thoracic disc herniation (T11T12) Metastatic hepatoma (T11) Acute burst fracture (T11) Metastatic laryngeal Ca (T12) Metastatic adenoca, unknown primary (T12) Metastatic breast Ca (T11) Metastatic renal cell Ca (T11) Metastatic adenoca, unknown primary (T11) Neglected old burst fracture (L1) Osteoporotic burst fracture Ankylosing spondylitis with discitis (T10T11) Metastatic adenoca, unknown primary (L1)

Operative proceduresa 2 Conversion to open 3 + 4a + 5 3 + 4b 3 + 4b + 6 3 + 4b + 6 3c 1 3 + 4a + 5 + 6 3 + 4b + 5 3 + 4a + 5 3 + 4c + 5

Total operating time (h)b 3.5 4.5 2.5 3.0 3.0 2.0 1.5 4.0 2.5 3.5 3.5

Total blood loss (cc) 400 1,000 1,500 650 1,300 3,000 50 1,200 500 450 1,500

Incisions in chest (no.) Lt (3) Lt (3) Rt (3) Rt (3) Rt (3) Rt (3) Rt (3) Lt (2) Lt (2) Lt (2) Lt (2)

operative procedures: 1, biopsy; 2, discectomy; 3, corpectomy; 4, interbody fusion: a (autograft), b (allograft), and c (polymethylmethacrylate); 5, anterior instrumentation (Reduction-Fixation fixator system, Trifix, San Leandro, CA, USA); 6, posterior instrumentation (Harrington rodding techniques). total operating time: not including posterior procedures. c partial corpectomy only.
b

We report a new approach that uses the so-called extended manipulating channel method [2] to treat spinal lesions located in the thoracolumbar junction endoscopically. This method allows for the use of a combination of videoassisted thoracoscopy and conventional spinal instruments during surgery. The series presented here comprises 12 patients. Patients and methods
From November 1, 1995 to December 31, 1996, we used video-assisted thoracoscopic surgery (VATS) to treat 12 patients with anterior spinal lesions in the thoracolumbar junction (T11L2) (Table 1). There were six women and six men; their ages ranged from 24 to 75 years (average, 52). The patients and their families were informed that an open thoracotomy might be necessary if video-thoracoscopic surgery was not successful. The location of the pathology in the involved vertebra often determines the approach. In this series, either a right- or left-sided approach was feasible. For lesions involving the L1 body or L1L2 disc, we prefer a left-sided approach because the aorta is located just left to the midline and more space is available next to the vertebral surface. Using the so-called extended manipulating channel method [2], the number of incisions was usually sufficient using either a three-portal (Fig. 1) or a modified twoportal technique (Fig. 2). Fig. 1. Video-assisted thoracoscopic surgery for spinal lesions in the thoracolumbar junction (T11L2) using the so-called extended manipulating channel method with a three-portal approach (2.53.5-cm incision wounds). Fig. 2. A modified two-portal approach for lesions in the thoracolumbar junction (T11L2) using an extended manipulating channel measuring 56 cm and a small incision (2.5 cm) for introducing the thoracoscope.

Case illustration
A 24-year-old man (case 11) suffered from ankylosing spondylitis of >6 years duration. Due to severe hip pain and flexion deformity, he underwent bilateral total hip replacements 3 years earlier. He presented to us with progressive mid-back pain of 3 months duration and urine retention of 1 weeks duration. Plain radiographs demonstrated irregular and sclerotic changes at the bony endplates adjacent to the T10T11 disc space (Fig. 3). The urodynamic study revealed a detrusor hyporeflexia, and the magnetic resonance imaging (MRI) showed a widening and decreased signal intensity of the T10T11 disc, with mild cord compression at that level (Fig. 4). Prior to the operation, video-assisted thoracoscopic discectomy, interbody fusion, and internal fixation were chosen as the course of treatment. Under general anesthesia and following intubation with a double-lumen endotracheal tube, the patient was put in the right lateral decubitus position. The operative table was flexed to open the flank region. Skin was draped and prepped for a posterolateral thoracotomy, so that in the event of intraoperative complication or if thoracoscopic surgery was not possible the procedure could be converted. With selective collapse of the left lung, the

chest was entered carefully through a stab incision. The initial trocar incision was located at the seventh intercostal space (ICS) along the anterior axillary line. An 11-mm trocar was used to introduce the operating thoracoscope (0, 10 mm; Stryker, Kalamazoo, MI, USA). The lesion site was identified and displayed on the video monitor. Then a larger manipulating channel measuring 56 cm in length was created under the guidance of the scope; it was made at the level or slightly behind the posterior axillary line at the T9T10 ICS (Fig. 2). The diaphragm was grasped and pushed down gently with a traditional sponge forceps (9.5, Foster type; Edward Weck, Research Triangle Park, NC, USA) that had been introduced through the manipulating channel. The lung was also removed from the lesion site with the sponge forceps.

1191

Fig. 3. Case 11. A plain antero-posterior radiograph of a 24-year-old man with ankylosing spondylitis and discitis at the level of T10T11. Fig. 4. Case 11. Magnetic resonance imaging of a 24-year-old man with ankylosing spondylitis and discitis at the level of T10T11. MRI revealed a widening and decreased signal intensity of the T10T11 disc and slight cord compression. Fig. 5. Case 11. A 24-year-old man with ankylosing spondylitis and discitis (T10T11). A: Antero-posterior and B: lateral radiographs taken after video-assisted thoracoscopic discectomy, interbody fusion with left iliac strut grafting, and internal fixation with the Reduction-Fixation fixator system.

The thoracoscope helped us to identify the lesion and establish its proximity to the aorta. The lesion site was ascertained by a C-arm intensifier. The intercostal arteries and veins were isolated using Debakey right angle forceps (10; Edward Weck) and ligated with hemoclips. The discectomy at the T10T11 level was then carefully performed under video monitoring using conventional disc rongeurs (8; Cushing type; Lawton, Tuttlingen, Germany) and elongated bone curettes (15; Howmedica, Rutherford, NJ, USA). With selective use of a 0 or 30 thoracoscope, the discectomy was performed posteriorly and down to the epidural space. Through another incision, a 2 2 1.2 cm3 tricoctical iliac bone graft was

harvested from the left iliac crest. The graft was inserted and applied between the 10th and 11th thoracic vertebrae using a conventional bone impactor (12; Trauma-fix; AST, San Leandro, CA, USA). After that, a guide pin was introduced through the manipulating channel into the anterolateral aspect of the vertebral body. The direction of the pin was checked by a C-arm intensifier, and a vertebral screw was then inserted with a screw-holding device. The position and depth of the screw were checked again by the C-arm intensifier at the 10th and 11th instrumented vertebrae. A length of titanium plate (Reduction-Fixation fixator system; Trifix, San Leandro, CA, USA) was applied. The sandwich con-

1192 figuration of the two square-shaped washers between the screw and plate allows a variable angle anchorage. Upon completion of the procedure, a nut was loaded and tightened on top of the screw head (Fig. 5). Once hemostasis was assured, a single 32-F chest tube was inserted through the incision site at the anterior axillary line and guided under direct visualization to the apex of the chest. During completion of the procedure, the incision wounds were closed in layers using 3-0 nylon and an interrupted suture. A chest radiograph was taken immediately after the operation to make sure the lung was reinflated. The chest tube was removed on the 3rd postoperative day. The patient wore a protective Taylor-Knight brace for a period of 3 months.

Results The total time for the operation ranged from 1.5 to 4.5 h (average, 3); the total blood loss ranged from 50 to 3000 cc (average, 1050). The average number of portals made during the procedures was less than three (Table 1). There were no injuries to great vessels or visceral organs, and no further neurological deterioration was caused by the procedure. One patient (case 2) was converted to an open procedure due to a severe pleural adhesion from a previous hepatectomy procedure. Complications included two cases of transient intercostal neuralgia, one residual pneumothorax after chest tube removal, and one superficial wound infection. One patient (case 7) had massive bleeding (3000 cc) during the operation due to a metastatic renal cell carcinoma, so the procedure was limited to partial corpectomy only. Six patients had their surgery via a right-sided approach; the other six had a left-sided one.

Discussion Since its use was first reported for the treatment of a variety of thoracic lesions, VATS has become widespread [5]. Many procedural refinements and improvements in video optics and instrumentation have been developed since the initial report. VATS has only recently been applied in such thoracic spine procedures as biopsy, discectomy, anterior releases in scoliotics, decompressive corpectomy, and internal instrumentations [1, 7, 8, 1113], so most spine surgeons are still somewhat unfamiliar with the technique. Although in some respects VATS is superior to open thoracotomy [3, 4, 6, 9, 10], it also has some disadvantages. First, the technique requires a learning curve to acquire the handeye coordination necessary to perform remote bone and soft-tissue dissection, as well as to establish proper orientation under the angled endoscope [1, 13]. Second, successful one-lung ventilation is required for the operation. The complete assistance of an experienced anesthesiologist is a prerequisite for proper ventilation. Third, high riding of the dome of the diaphragm to the eighth ICS may occur while the lung is collapsed [8]. Therefore, the initial portal for introducing the thoracoscope must be made at the sixth or seventh ICS. Fourth, many spinal lesions, including trauma cases, frequently occur in the thoracolumbar junction (T11 L2). It is far more difficult and a technically demanding to perform endoscopic surgery in this sensitive location. The traditional trocar method in VATS surgery is timeconsuming and fraught with difficulties in manipulating the instruments. Many problems arise due to limited trocar space and a lack of suitable endoscopic equipment. In this series, we used a technique known as the extended ma-

nipulating channel method. This method allowed us to use a combination of video-assisted thoracoscopy and conventional spinal instruments [2]. Using this approach, the instruments can be passed freely through the channels and manipulated in ways similar to the techniques familiar to surgeons accustomed to standard open procedures. In the thoracolumbar junction (T11L2), the endoscopic technique is complicated by the high riding of the dome of the diaphragm. With the VATS approach, the spine can be accessed as far as the T12L1 disc space. Although endoscopic T12 corpectomy is no more difficult to perform than an open procedure, additional portals are required for the diaphragms retraction [8]. Therefore, a total of four, five, or more incisional wounds must be made [1, 8, 13]. Anatomically, the diaphragm originates in three locations: a sternal, a costal, and a vertebral part arise by means of crura and from the arcuate ligaments. The right crus arises from the sides of the bodies of L1L3; the left crus arises from the sides of L1 and L2 bodies. The medial arcuate ligament extends from the side of L2 body to the tip of the transverse process of the first lumbar vertebra. The lateral arcuate ligament extends from the tip of the transverse process of the L1 vertebra to the lower border of the 12th rib. Therefore, both the crura and arcuate ligaments of the diaphragm are inserted below the T12L1 disc space. When the lesion is located above the T12L1 disc, it is usually unnecessary to dissect the diaphragm. However, in lesions below the T12L1 disc, the spine is surrounded by the diaphragmatic crura, arcuate ligaments, and psoas muscles. This lower location of the lesion may increase technical difficulties for the surgeon when VATS is used and the instruments are manipulated from the diaphragm above the lesion. Regan and Ben-Yisbay recommend a combined thoracoscopic and laparoscopic method to approach lesions below the T12L1 disc [12]. However, because of the potential hazard of penetration of the peritoneum, this approach requires both the exploration and transection of the diaphragm [12]. In this paper, we have reported the successful use of a combination of video-assisted thoracoscopy and conventional spinal instruments to perform endoscopic spine surgery at the thoracolumbar junction (T11L2). Our technique decreases the number of portals required for the procedure. Using the extended manipulating channel method, we found that either a three-portal or a modified two-portal approach was sufficient. This technique makes thoracoscopic spinal surgery simpler and easier in this region. In most cases, there is no need to transect the diaphragm. For lesions below the T12L1 disc level, the diaphragm can be detached easily from its lumbar origins, the crura, and the arcuate ligaments following ligation of the segmental vessels. We have no experience with Regan and Ben-Yisbays combined laparoscopic method [12]; however, it seems less likely to compromise the surgical objective in our patients. In addition, very few endoscopic materials were required for the procedure, resulting in a reduction of overall costs. References
1. Dickman CA, Rosenthal D, Karahalios DG, Paramore CG, Mican CA, Apostolides PJ, Lorenz R, Sonntag VKH (1996) Thoracic vertebrectomy and reconstruction using a microsurgical thoracoscopic approach. Neurosurgery 38: 279293

1193 2. Huang TJ, Liu HP, Liao YS, Hsu KY, Hsu RWW (1996) Videoassisted thoracoscopic surgery for the spine: preliminary results. Proc J Endosc Laparosc Surgeons Asia 2: s3334 3. Kaiser LR, Bavaria JE (1993) Complications of thoracoscopy. Ann Thorac Surg 56: 796798 4. Landreneau RJ, Mack MJ, Mazelhjg SR (1992) Video-assisted thoracic surgery: basic technical concepts and intercostal approach strategies. Ann Thorac Surg 54: 800807 5. Lewis RJ, Caccavale RJ, Sisler GE (1991) Special report: videoendoscopic thoracic surgery. NJ Med 88: 473475 6. Liu HP, Chang CH, Lin PJ, Hsieh HC, Chang JP, Hsieh MJ (1994) Video-assisted thoracic surgery. The Chang Gung experience. J Thorac Cadiovasc Surg 108: 834840 7. Mack MJ, Regan JJ, Bobechko WP, Acuff TE (1993) Application of thoracoscopy for diseases of the spine. Ann Thorac Surg 56: 736738 8. McAfee PC, Regan JR, Zdeblick T, Zuckerman J, Picetti GD, Heim S, Geis WP, Fedder IL (1995) The incidence of complications in endoscopic anterior thoracolumbar spinal reconstructive surgery. A prospective multicenter study comprising the first 100 consecutive cases. Spine 14: 16241632 McCormack PM, Martini N (1979) The changing role of surgery for metastatic pulmonary metastasis. Ann Thorac Surg 28: 139145 Miller JI, Hatcher CR Jr (1978) Thoracoscopy: a useful tool in the diagnosis of thoracic disease. Ann Thorac Surg 26: 6872 Regan JJ, Mack MJ, Picetti GD (1995) A technical report on videoassisted thoracoscopy in thoracic spinal surgerypreliminary description. Spine 20: 831837 Regan JJ, Ben-Yisbay A (1995) Thoracolumbar discectomy. In: Regan JJ, McAfee PC, Mack MJ (eds) Atlas of endoscopic spine surgery. Quality Medical Publishing, St Louis Rosenthal D, Sutterlin CE III, Corbin TP, Connolly J, Yuan HA, Kolata RJ, Clem MF, Regan JJ, Mack MJ (1995) Newer applications of spinal instrumentation. In: Regan JJ, McAfee PC, Mack MJ (eds) Atlas of endoscopic spine surgery. Quality Medical Publishing, St Louis

9. 10. 11.

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13.

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The author replies

It is true that the TAPP and Shouldice techniques differ significantly. Their similarities are limited to their goal, namely, to cure groin hernias surgically. The differences comprise the anesthesia, the anatomic approach, the technique itself, the materials used, the difficulty, the cost, andin our handsthe results. However, a new technique should be compared to the gold standard whichin Switzerlandsurely is the Shouldice procedure. The aim of the study was to compare the results of both techniques in the hands of the same surgeons. It could not be to show the superiority of one technique over the other. In that case the results would have been biased. In fact, to tell the truth, I initially doubted very much that the results would be in favor of laparoscopy. The reason for this was that we quickly realized how difficult the TAPP procedure is and that the learning curve takes longer than we first assumed. The complication rate has dropped since, as have the operating times and thus the costs. The early recurrence rate has been low in the laparoscopic group from the beginning [9]. Open tension-free hernia repairs indeed give promising results. Where these techniques are established it seems reasonable to compare them to the laparoscopic procedure. The common feature being the use of prostheses to reinforce the groin, the comparison will be between an anterior approach with the mesh in onlay position [4] or in a sublay position [3] with a second onlay mesh as reinforcement [6] and the laparoscopic posterior sublay approach ultimately referring to the Stoppa technique [7] either transabdominally or extraperitoneally. The solely onlay open technique will be prone to miss associated femoral components, which should theoretically not be the case in the transinguinal preperitoneal approach either with or without onlay reinforcement. The difference compared to the laparoscopic technique will be that the latter allows a visual control of the whole inguinal floor and thus a precise diagnosis of all hernias including the very rare obturator hernia [2, 8]. The placement of the mesh occurs under vision and even very large meshes of 15 13 cm, e.g., can be placed without folds and fixed securely, which I find more difficult to achieve in the transinguinal approach. I wonder, too, whether a double buttress onlay-sublay technique does not stiffen the abdominal wall too much and cause some discomfort to the patient.

The pain the patients experience postoperatively determines the moment when they resume their usual activities, as most patients do not strain a painful groin even when encouraged to do so. I have no doubt that open tension-free techniques are less painful than a conventional herniorrhaphy. There still seems, however, to remain a difference in favor of laparoscopy, especially when perioperative exercise testing is used as an adjunct to return to work in the comparison of methods [5]. The Shouldice Clinic [1] has shown that the key to preventing technical errors with an anterior approach is experience. We must assume that this will be the case for laparoscopic techniques, too. To restrict laparoscopy to difficult cases like recurrences and bilateral hernias may be dangerous, as it needs a lot of experience to perform a perfect laparoscopic procedure in these cases. The ease of repair, low cost, low complication rate, and short time of rehabilitation strongly favor open tension-free methods. The ultimate standard by which any hernioplasty is judged will nevertheless be the recurrence rate, for in the end the incidence of recurrence determines the true cost of the procedure [2]. If we assume that open tension-free hernioplasties give the same or better results than the laparoscopic techniques we will need many more trials with large numbers of patients and at least 2-year results to get the answer, as most recurrencies in hernioplasties occur within the first 2 years [2]. It will be of uttermost importance to have a high percentage of clinical follow-up of the patients of more than 90% in order to validate these studies. Hernia centers all over the world seem ideally suited to perform this task.

References
1. Ben David R (1989) New techniques in hernia repair. World J Surg 13: 522531 2. Felix EL, Michas CA, Gonzalez MH Jr (1997) Laparoscopic hernioplasty: why does it work? Surg Endosc 11: 3641 3. Gilbert AI (1991) Inguinal hernia repair: biomaterials and sutureless repair. Perspect Gen Surg 2: 113129 4. Lichtenstein IL, Shulman AG (1974) Ambulatory outpatient hernia surgery, including a new concept, introducing tension-free repair. Int Surg 71: 17

1231 5. Payne JH Jr, Grininger LM, Izawa MT, Podoll EF, Lindahl PJ, Balfour J (1994) Laparoscopic or open inguinal herniorrhaphy? A randomized prospective trial. Arch Surg 129: 973981 6. Rutkow IM (1994) Open tension-free mesh plug versus laparoscopic groin herniorrhaphy: economic practicalities. In: Bu chler MW, Farthmann EH (eds) Laparoscopic hernia repair: a new standard? Progress in Surgery vol 21. Karger, Basel Freiburg Paris London New York, pp 105112 7. Stoppa R (1989) The treatment of complicated groin and incisional hernias. World Surg 23: 545554 8. Tschudi J, Wagner M, Klaiber Ch (1993) Laparoskopische Operation einer incarcerierten Obturatoriushernie mit assistierter Darmresektion. Chirurg 64: 827828 9. Tschudi J, Wagner M, Klaiber Ch, Brugger JJ, Frei E, Kra henbu hl L, Inderbitzi R, Hu sler J, Hsu Schmitz S (1996) Controlled multicenter trial of laparoscopic transabdominal preperitoneal hernioplasty vs Shouldice herniorrhaphy: early results. Surg Endosc 10: 845847

J. Tschudi
Bahnhofstr. 39 CH-2502 Biel Switzerland

Letters to the editor

Surg Endosc (1997) 11: 12241225

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Tumor dissemination during laparoscopic cholecystectomy for gallbladder carcinoma

Port site and peritoneal tumor seeding is a lethal complication following laparoscopic cholecystectomy (LC) for gallbladder carcinoma. Since the first report by Drouard et al. [4] in 1991, many other cases of seeding have been published. The number of previous articles appearing in Surgical Endoscopy [2, 3, 5, 8, 1012, 14, 15] suggests that readers of the journal are very interested in this problem. We attempt here to obtain answers from the literature as to whether LC promotes tumor seeding more than open cholecystectomy, and by what mechanisms. The true incidence of port site and peritoneal seeding after LC for gallbladder cancer is not known, as cases without this complication typically are not reported. Only a few small studies allow an estimate of incidence. Wibbenmeyer et al. [16] reported that three of six patients undergoing LC for unsuspected cancer developed seeding. Fong et al. [6] reported that four of 10 patients with laparoscopically resected cancer developed tumor implants from seeding soon after LC. Sandor and associates [12] reported that two of three patients undergoing LC for unsuspected cancer developed port site recurrences. In our experience, one of two LC patients with unsuspected cancer developed peritoneal seeding (unpublished data). Considering these four small series, the incidence of tumor seeding after LC is considerable. In contrast, we previously have reported that none of 98 patients with unsuspected gallbladder carcinoma developed wound metastases after open cholecystectomy [13]. A recent study in rats [9] revealed that port site seeding occurred more frequently after laparoscopic tumor manipulation than after an open procedure; seeding developed equally in contaminated ports from which a tumor-laden instrument was withdrawn and clean ports from which a tumor-free laparoscope was retrieved. Clinically, also, seeding may occur at ports which had no evident contact with tumor [8, 9]; pneumoperitoneum with carbon dioxide may explain seeding at apparently clean port sites [2, 9]. Another unresolved question is whether laparoscopic resection could enhance hematogeneous or lymphatic dissemination. Fong et al. [6] and Nishizaki et al. [10] have reported hepatic metastases appearing soon after LC. Finally, many anecdotal reports of seeding after LC have omitted critical information such as the incidence of cancer in the surgeons LC experience, the incidence of seeding in their cancer cases, the TNM stage [1, 7] of the tumor, whether bile spillage occurred, and whether a gallbladder bag was used. The follow-up period also is short in most reports. Future authors should ensure that such data is included, especially since prospective randomized trials regarding this complication are largely precluded by ethical issues and tumor rarity. In conclusion, LC risks tumor dissemination more than open cholecystectomy, not only by direct contact but also by metastatic spread. Well-documented clinical reports and well-designed animal studies are needed to better understand this lethal complication.

References
1. Beahrs OH, Henson DE, Hutter RVP, Kennedy BJ (eds) (1992) Manual for staging of cancer. 4th ed. JB Lippincott, Philadelphia 2. Birkett DH (1995) Spilled cells, spilled clips, spilled stones: new problems or old challenges. Surg Endosc 9: 269271 3. Copher JC, Rogers JJ, Dalton ML (1995) Trocar-site metastasis following laparoscopic cholecystectomy for unsuspected carcinoma of the gallbladder: case report and review of the literature. Surg Endosc 9: 348350 4. Drouard F, Delamarre J, Capron J (1991) Cutaneous seeding of gallbladder cancer after laparoscopic cholecystectomy. N Engl J Med 325: 1316 5. Ferzli GS, Daou R (1994) Laparoscopic cholecystectomy and gallbladder cancer. Surg Endosc 8: 1357 6. Fong Y, Brennan MF, Turnbull A, Colt DG, Blumgart LH (1993) Gallbladder cancer discovered during laparoscopic surgery: potential for iatrogenic tumor dissemination. Arch Surg 128: 10541056 7. Hermanek P, Sobin LH (eds) (1992) UICC TNM classification of malignant tumours. 4th ed. 2nd rev. Springer-Verlag, Berlin 8. Jacobi CA, Keller H, Mo nig S, Said S (1995) Implantation metastasis of unsuspected gallbladder carcinoma after laparoscopy. Surg Endosc 9: 351352 9. Mathew G, Watson DI, Rofe AM, Baigrie CF, Ellis T, Jamieson GG (1996) Wound metastases following laparoscopic and open surgery for abdominal cancer in a rat model. Br J Surg 83: 10871090 10. Nishizaki T, Matsumata T, Hashizume M, Maeda T, Otsuka K, Sugimachi K (1994) Hepatic metastasis after laparoscopic cholecystectomy for polypoid gallbladder cancer followed by radical surgery. Surg Endosc 8: 14361438 11. Sailer M, Debus S, Fuchs KH, Thiede A (1995) Peritoneal seeding of gallbladder cancer after laparoscopic cholecystectomy. Surg Endosc 9: 12981300

Correspondence to: Y. Shirai

1225 12. Sandor J, Ihasz M, Fazekas T, Rego ly-Me rei J, Batorfi J (1995) Unexpected gallbladder cancer and laparoscopic surgery. Surg Endosc 9: 12071210 13. Shirai Y, Yoshida K, Tsukada K, Muto T (1992) Inapparent carcinoma of the gallbladder: an appraisal of a radical second operation after simple cholecystectomy. Ann Surg 215: 326331 14. Targarona EM, Pons MJ, Viella P, Tr as M (1994) Unsuspected carcinoma of the gallbladder: a laparoscopic dilemma. Surg Endosc 8: 211213 15. Wade TP, Comitalo JB, Andrus CH, Goodwin MN Jr, Kaminski DL (1994) Laparoscopic cancer surgery: lessons from gallbladder cancer. Surg Endosc 8: 698701 16. Wibbenmeyer LA, Wade TP, Chen RC, Meyer RC, Turgeon RP, Andrus CH (1995) Laparoscopic cholecystectomy can disseminate in situ carcinoma of the gallbladder. J Am Coll Surg 181: 504510

Y. Shirai T. Ohtani K. Hatakeyama

Department of Surgery Niigata University School of Medicine 1 Asahimachi-dori Niigata City 951 Japan

Surg Endosc (1997) 11: 11501152

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Ambulatory laparoscopic fundoplication

M. A. Milford, T. A. Paluch
Department of Surgery, Kaiser Foundation Medical Center, 4647 Zion Avenue, San Diego, CA 92120, USA Received: 1 April 1996/Accepted: 29 May 1997

Abstract Background: Increasingly larger series of laparoscopic fundoplications (LF) are being reported. A well-documented advantage of the laparoscopic approach is shortened hospital stay. Most centers report typical lengths of stay (LOS) for LF of 23 days. Our success with LF with a LOS of 1 day led to an attempt at performing LF on an ambulatory basis. Methods: Sixty-one consecutive patients with appropriate criteria for LF underwent surgery at our institution. Patients were counseled by the authors as to the usual postop course and progression of diet. All patients received preemptive analgesia (PEA) consisting of perioperative ketorolac and preincisional local infiltration with bupivicaine. Anesthetic management included induction with propofol, high-dose inhalational anesthetics, minimizing administration of parenteral narcotics, and avoidance of reversal of neuromuscular blockade. Immediate postop pain management included parenteral ketorolac and oral hydro- or oxycodone. All patients were given oral fluids and soft solids after transfer from the recovery room to the postoperative observation unit. Two patients were excluded from ambulatory consideration due to excessive driving distance from our hospital. Another two were hospitalized for observation after experiencing intraoperative technical problems. Results: Of 57 patients in whom same-day discharge was attempted, there were three failures requiring overnight hospitalization: All were due to pain and nausea; one patient also suffered transient urinary retention. There were no adverse outcomes related to early discharge, and there were no readmissions. One patient returned to the emergency room after delayed development of urinary retention. Median time from conclusion of operation to discharge was less than 5 h. No patients expressed dissatisfaction with early discharge on follow-up interview. Conclusions: LF can be safely performed as an ambulatory procedure. Analgesic and anesthetic management should be tailored to minimize nausea and provide adequate pain control.

Key words: Laparoscopic fundoplication Ambulatory surgery Preemptive analgesia Propofol Ketorolac Bupivicaine

Minimally invasive surgical techniques have created a revolution in the management of gastroesophageal reflux disease (GERD). The ability to combine the time-tested efficacy and durability of total and partial fundoplications with the more rapid recovery afforded by laparoscopic techniques is at the cornerstone of this change. As increasingly larger series of laparoscopic fundoplications (LF) are reported, a clear and favorable picture of both outcomes and costs is emerging. Although the cost of surgical therapy hinges on many variables, length of hospital stay (LOS) is a prime contributor. Published American series of LF, ranging upward to nearly 300 patients, have reported average LOS of 24 days [3, 4]. Against concurrent controls, this would appear to afford a greater than 5-day improvement in LOS compared with fundoplication via laparotomy [6]. In our own series of LF, a gradual evolution in analgesic and anesthetic techniques combined with improving patient care strategies resulted in a more predictable recovery and progressively shorter LOS. This was accomplished without compromise in safety, efficacy, or patient satisfaction. After first establishing a consistent and reproducible experience with overnight hospitalization for LF, we embarked on a trial of same-date discharge, i.e., true ambulatory surgery. Patients and methods
From May 1995 to January 1997, a consecutive series of 61 patients with documented GERD were referred from our Gastroenterology Unit for LF by the authors. The patients, 26 women and 35 men, ranged in age from 30 to 77 years, with a median of 47 years. Only one patient was over 65 years of age. Age distribution is shown in Fig. 1. The women ranged in weight from 56 to 109 kg (123240 pounds), with Body Mass Indices (BMI) (calculated as weight in kilograms, divided by height in meters, squared) ranging from 23.9 to 38.1. The men ranged from 68 to 130 kg (150286 pounds), with BMI ranging from 23.4 to 37.7. BMI distribution for all patients is shown in Fig. 2. All had met criteria for operability on the basis of endoscopically documented esophagitis, and dependence upon omepra-

Correspondence to: M. A. Milford

1151 Table 1. Standard ambulatory surgery discharge criteria at Kaiser Foundation Medical Center, San Diego Medical: Alert and oriented Vital signs stable No evidence of active bleeding Ambulation without nausea or dizzyness Tolerating oral fluids well Free of excessive pain Able to void Social: Escort available to transport patient to home Home care instructions explained, copy given Patient/family verbalized understanding of home care instructions

Fig. 1. Age distribution of 61 consecutive patients undergoing laparoscopic fundoplication.

Fig. 2. Body Mass Index distribution of the same 61 patients.

zole (Prilosec) for symptom control. Esophageal motility was routinely assessed by preoperative esophageal manometry. In 51 patients, esophageal body motility was normal, and laparoscopic Nissen fundoplication was performed. In 10 patients, esophageal motility was diminished, and partial (modified Toupet) fundoplication was performed. Patients were not excluded from operative candidacy due to age, weight, or prior upper abdominal operative history. Comorbidities were relatively rare, although seven patients (11%) were under treatment for asthma/reactive airway disease. Patients were counseled regarding the common postoperative experience, anticipated hospitalization period, and criteria and conditions for discharge. All patients were agreeable to this approach. Patients were electively admitted for same-day surgery approximately 2 h prior to anticipated anesthetic induction. Preoperative parenteral metoclopramide (Reglan) was administered as prophylaxis against aspiration. In the operating room, all patients received a standard combination of agents as preemptive analgesia (PEA), after anesthetic induction. All were administered a total of 50 ml of bupivicaine (Marcaine) with epinephrine, a long-acting local anesthetic, at the five pre-marked port sites, by the operating surgeon. Patients also received a preincisional dose of 30 mg of parenteral ketorolac (Toradol), a nonsteroidal antiinflammatory drug (NSAID) that has shown analgesic effects comparable to that of commonly used doses of narcotics. This was followed in most cases by another identical dose at the time of fascial closure. Adults greater than 65 years of age received half of this dose. Anesthetic technique was tailored to minimize immediate postoperative anesthetic side effects Propofol (Diprivan) was used as the induction agent, in contrast to barbiturates, which have some nausea-inducing properties. Isoflurane (Forane) was used, without nitrous oxide, for maintenance of anesthetic depth. Fentanyl (Sublimaze), a short-acting parenteral narcotic, was selectively used to complement the inhalation agent, but in minimal doses. Intermediate-acting neuromuscular relaxants such as vecuronium (Norcuron) were utilized in order to avoid the use of neuromuscular reversal regimens and their autonomic side effects. An orogastric tube was utilized in the first half of the procedure only, and it was not replaced after construction of the fundoplication. Urinary catheters were not utilized. The procedure was performed with the patient in modified lithotomy, reverse Trendelenburg position. A standard five-puncture technique was used, typically with 1012-mm ports. In 51 patients, a (360) sutured

Nissen-style fundoplication was created, 2.0 cm long. In 10 patients, a partial (270) modified Toupet-style fundoplication was created using interrupted sutures and Teflon felt pledgets. The fundoplications were constructed over a 60-French (Maloney) dilator. In all instances, the dilators were placed by the assisting surgeon under strict video observation. The short gastric vessels were divided by either laparoscopic intestinal stapling devices or by use of an ultrasonic scalpel. Crural closure was routinely performed. Fascia was routinely closed at 10- and 12-mm sites. An attempt was made to evacuate all CO2 at the conclusion of the procedure. Additional planned procedures were performed as medically or technically indicated. Seven patients, with histories of prior upper laparotomies, underwent adhesiolysis/enterolysis to allow exposure of the left upper quadrant. One of these patients had previously undergone an (open) Nissen fundoplication, which had failed. Two patients underwent synchronous cholecystectomy. One patient each underwent paraesophageal hernia repair with prosthetic mesh and incisional hernia repair. In the recovery room, standard monitoring and techniques were utilized. Parenteral narcotics and antiemetics were used as needed under the direction of the supervising anesthesiologist. Once directed to the postoperative observation unit, patients were offered liquids and soft solids by mouth. Analgesics were provided, when needed, in the form of parenteral ketorolac and/or oral hydrocodone or oxycodone. Once diet and oral analgesic tolerance were demonstrated, patients were required to meet standard criteria prior to consideration for discharge. Discharge criteria are itemized in Table 1. Patients were routinely contacted by telephone on the day after operation by a registered nurse experienced in perioperative care. Patients were routinely seen back in the office within 10 days.

Results Of the 59 patients who were considered ambulatory candidates at the outset of the procedure, two were admitted to hospital after operation for technical reasons. One suffered a splenic capsular tear, which required additional hemostatic maneuvers. The other suffered an esophageal tear from passage of the Maloney dilator. This patient had a history of prior stricture and dilatation, which may have contributed to this problem. Both problems were corrected laparoscopically, and both patients were discharged uneventfully on the following day. No other complications occurred. No patients were converted to laparotomy. No difficulties with hemostasis were ascribed to the use of ketorolac. Mean operating time for all 61 patients was 87 min (1 h, 27 min), ranging from 53 to 160 min. Of the 57 patients who were directed to the postoperative observation unit, 54 (95%) successfully met discharge criteria that date and left hospital at a median interval of 290 min (4 h, 50 min) after completion of operation (range 140607 min). In this group, 21 patients (39%) required no additional parenteral narcotic after leaving the operating room. An additional 24 patients (44%) required 1.0 mg or

1152

less of parenteral hydromorphone (Dilaudid), which was administered in the recovery room. Only 12 patients (22%) requested antiemetic agents while in the recovery room. Their complaints of nausea did not recur in the observation area, prior to discharge. Three patients failed to meet discharge criteria, all due to complaints of unresolved nausea and inadequate pain control. One of these patients, a 50year-old man, also had initial urinary retention, which resolved after a single catheterization. All three patients required additional doses of both ketorolac and Dilaudid for adequate analgesic effect. All three were improved and able to be discharged on the following day. Patients who failed to meet discharge criteria did not differ from those who did in regard to length of operation, age, obesity, or extent of procedure (fundoplication alone vs fundoplication with additional procedures). No patients required readmission after successfully meeting discharge criteria. Only one patient, a 56-year-old man, returned to office or emergency room for unanticipated postoperative problems during the follow-up period, this being due to delayed presentation of urinary retention. At scheduled clinic follow-up, no patients expressed any dissatisfaction with the conduct of their postoperative care or their readiness for discharge. Discussion Many series of LF have recently been published, attesting to the popularity of this approach. Excellent records of safety and efficacy have been established, paralleling that of the open procedure. Typically, however, little detail is provided regarding analgesic or anesthetic methods or dietary progression. As a result, it is unclear why LF patients have significantly longer hospital stays than other laparoscopic procedures currently performed on an ambulatory basis, such as cholecystectomy. In our own series of LF, dating to 1993, early cases were managed with emphasis on those mechanical aspects of postoperative care that might minimize the potential for nausea, retching, and/or gastric distension. As a consequence, patients were subjected to a mandatory period of nasogastric tube decompression and bowel rest. These measures were largely ineffective, however, in prevention or treatment of complaints of nausea. As a result, neurolepticclass antiemetics were commonly prescribed, which then contributed to sedation and lethargy. In contrast, during this same period, it was observed that nausea and failure of dietary tolerance were rare in those patients who had postoperative analgesia with parenteral ketorolac rather than traditional parenteral narcotics. This suggested that medication side effects, rather than ileus or gastroparesis, contributed to these complaints, which is consistent with the known sideeffect profiles of the two respective classes of analgesic (NSAID vs opiate). Additionally, patients who had received preincisional ketorolac required less total analgesic than those who received it after operation was complete, suggesting what has been termed a preemptive effect [7].

Preemptive analgesia is a concept that has not yet gained widespread clinical acceptance. There is ample laboratory evidence to show that noxious stimuli, even when experienced under general anesthetic, create alterations in peripheral and spinal cord pathways that heighten the sensitivity of these channels to pain [8]. If these stimuli are blocked, the subsequent pain experienced when conscious may be lessened. Ketorolac and bupivicaine appear to be ideal agents for PEA in an ambulatory setting, since the former has systemic efficacy comparable to potent narcotics, but with lessened propensity for nausea, and both have durations of action sufficient to cover the time from incision to postoperative observation unit. Ketorolac has been shown to have clinically measurable preemptive analgesic effect in prospective studies on both total hip replacement [2] and hysterectomy patients [5]. Similarly, the use of preincisional vs postincisional bupivicaine has been shown to lessen early postoperative analgesic requirements in pediatric hernia patients [1]. Once ketorolac/bupivicaine PEA was adopted as our standardized technique for pain management, the rarity of nausea led to the abandonment of postoperative nasogastric tubes and progressively earlier feeding. The final step in the transition from overnight hospitalization to true ambulatory status was minimizing both length of recovery and side effects from anesthesia, particularly within the first 6 h after the operation concluded. We empirically selected a scheme that minimizes or excludes those agents with prolonged, emetogenic and/or adverse autonomic activities. The resulting series of patients shows consistently shorter LOS than previously reported series. We believe that this combination of preoperative counseling, ketorolac-bupivicaine PEA, and a tailored anesthetic method is a simple, effective, and reproducible technique. The resulting improvement in patient comfort and functional status has led to a significant reduction in hospital stay for laparoscopic fundoplication. References
1. Dahl V, Raeder JC, Erno PE, Kovdal A (1996) Pre-emptive effect of pre-incisional versus post-incisional infiltration of local anesthesia on children undergoing hernioplasty. Acta Anesth Scand 40: 847851 2. Fletcher D, Zetlaoui P, Monin S, Bombart M, Samii K (1995) Influence of timing on the analgesic effect of intravenous ketorolac after orthopedic surgery. Pain 61: 291297 3. Hinder RA, Filipi CJ, Wetscher G, Neary P, DeMeester TR, Perdikis G (1994) Laparoscopic Nissen fundoplication is an effective treatment for gastroesophageal reflux disease. Ann Surg 220: 472483 4. McKernan JB, Champion JK (1995) Laparoscopic antireflux surgery. Am Surg 61: 530536 5. Parke TJ, Lowson SM, Uncles DR, Daugherty MO, Sitzman BT (1995) Pre-emptive versus post-surgical administration of ketorolac for hysterectomy. Eur J Anaesth 12: 549553 6. Peters JH, Heimbucher J, Kauer WKH, Incarbone R, Bremmer, DeMeester TR (1995) Clinical and physiologic comparison of laparoscopic and open Nissen fundoplication. J Am Coll Surg 180: 385392 7. Wall PD (1988) The prevention of postoperative pain. Pain 33: 289290 8. Woolf CJ (1989) Recent advances in the pathophysiology of acute pain. Br J Anesth 63: 139146

Editorial
Surg Endosc (1997) 11: 11431144

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Day-case (ambulatory) laparoscopic surgery

Let us sing from the same hymn sheet
This issue of Surgical Endoscopy contains three reports on ambulatory laparoscopic surgery: two on laparoscopic cholecystectomy and one on laparoscopic fundoplication. There have been a number of reports on ambulatory LC with the majority verdict based on these reports, including the two published in the current issue, being in favor of same-day discharge for the majority of patients [16]. The substantial reduction in hospital charges is self-evident. The seminal question centers on the safety of such an approach, especially if careful selection of patients for ambulatory care is not practiced. A minority has been criticized [7] for advising caution against outpatient cholecystectomy on the sensible but unproven assumption that day-case discharge will inevitably lead to occasional delays in the diagnosis and management of postoperative complications [8]. The report on ambulatory laparoscopic fundoplication is the first of its kind and merits special consideration [9]. Although there can be no argument about the substantial savings from the widespread practice of ambulatory laparoscopic surgery, we shall never be able to document its safety unless we conduct and participate in prospective randomized studies comparing day-case laparoscopic surgery versus short stay (overnight) practice. There are also certain considerations that require clarification and agreement for us to ensure that in addressing this important change in surgical practice, we are singing from the same hymn sheet. charge in 24 hours. Perhaps future reports on the subject should specifically indicate the patients who for any reason required an overnight stay in the hospital. Anaesthesia/gasless techniques Many surgeons may not be fully aware of the need for specialized anaesthetic techniques and the importance of preemptive analgesia (PEA), particularly in the prevention of postoperative nausea and vomiting that have been developed for day-case surgery. In this and other respects, the report by Milford and Paluch on Ambulatory Laparoscopic Fundoplication [9] is both instructive and exemplary. There is good evidence, which is strengthened by this report, that avoidance of opiate administration by PEA virtually abolishes the postoperative complaints of nausea and vomiting that preclude oral intake of fluids soon after the operation. There is, however, a need for standardization of both anaesthetic and preemptive analgesic techniques used for ambulatory laparoscopic surgery and perhaps the E.A.E.S. and SAGES ought to set up a consensus conference on this subject with active involvement of expert anaesthesiologists. My impression on reading the literature on the subject is that various techniques are used in different institutions. Gasless and abdominal wall lift techniques have been shown to reduce postoperative nausea and vomiting and CO2 narcosis [10, 11]. This approach merits serious consideration. Selection of patients Some surgeons believe that comorbid disease, old age, and physical status do not preclude safe ambulatory surgery. This assumption is largely based on retrospective reports that ignore the precise definition of day-case (ambulatory) surgery. There is no doubt, at least in my mind, that these higher-risk patients require a longer period of observation after their surgery. Indeed, many can often be discharged early after an overnight stay and within 24 hours, but, by definition, this is not ambulatory surgery. Patients related factors go beyond comorbid factors and old age, and include home support, distance and access between the patients home and the hospital, personality type, and regional environment. Day-case discharge of an otherwise fit patient who

Nomenclature One has to raise this issue even at the risk of sounding pedantic. Ambulatory surgery, day-case surgery, and outpatient surgery are terms used synonymously on both sides of the Atlantic. By definition, certainly in the National Health Service in the United Kingdom, the terms mean that the patient is discharged during the same day. This is not equivalent to a stay of less than 24 hours in a hospital. Thus if a patient has an operation (laparoscopic or otherwise) on the afternoon of a certain day and is discharged next morning (well within 24 hours), the overnight stay excludes the patient from being categorized as an ambulatory, day-case, or outpatient. It is obvious from at least two of the reports in the current issue and others reported previously that this standard definition of ambulatory (day-case) care is not adhered to, and indeed, one report specifically refers to dis-

1144

lives alone in a region where the winters are harsh, the days are short, and the roads are often impassable after heavy snowfalls cannot be regarded as an exercise of good clinical judgment. Perhaps colleagues who live and practice in warmer and kinder environments never encounter this situation; they are blessed even though they may not be aware of it. Ambulatory discharge criteria The standard ambulatory discharge medical and social criteria at the Kaiser Foundation Medical Center, San Diego, quoted in the article by Milford and Paluch, seem fine but, in my view, require fine tuning. It is not clear from this and other reports as to who is responsible (by documented signature) for the ambulatory discharge of these patients when all these criteria are met. Free of excessive pain worries me as being insufficiently precise and the legal profession would have a field day in the event of an adverse outcome. A more objective assessment based on a linear analogue scale should be agreed upon. Follow-up If surgeons are convinced that patients can be discharged safely as day cases after laparoscopic surgery, and the vast majority of patients obviously do well at considerable cost savings to the hospital, why is it necessary that they are all seen at the office ten days later? The point is that if we are to change drastically our surgical practice, why should we not also consider changes in the follow-up policy, especially in this digital age with unsurpassed means of efficient, in-

expensive, and real time communication between patient and surgeon or his staff?

References
1. Arregui ME, Davis CI, Arkush A, Nagan RF (1991) In selected patients outpatient cholecystectomy is safe and significantly reduces hospitalization charges. Surg Laprosc Endosc 1: 240245 2. Reddick EJ (1992) Laparoscopic cholecystectomy in free-standing outpatient centres. J Laparoendosc 2: 6567 3. Llorente J (1992) Laparoscopic cholecystectomy in the ambulatory setting. J Laparoendosc 2: 2326 4. Voitk AJ (1996) Routine outpatient laparoscopic cholecystectomy. Can J Surg 6: 262265 5. Hargreaves R (1996) Is outpatient laparoscopic cholecystectomy wise? (letter) Surg Endosc 10: 950 6. Saunders CJ, Leary BF, Wolfe BM (1995) Is outpatient laparoscopic cholecystectomy safe? Surg Endosc 9: 12631268 7. Voyles R, Berch BR (1997) Selection criteria for laparoscopic cholecystectomy in an ambulatory care setting. Surg Endosc 11: 11451146 8. Voitk AJ (1997) Is outpatient cholecystectomy safe for the higher-risk elective patient? Surg Endosc 11: 11471149 9. Milford MA, Paluch TA (1997) Ambulatory laparoscopic fundoplication. Surg Endosc 11: 11501152 10. Koivusalo A-M, Kellokumpu I, Lindgren L (1997) Postoperative drowsiness and emetic sequelae correlate to total amount of carbon dioxide during laparoscopic cholecystectomy. Surg Endosc 11: 4244 11. Koivusalo A-M, Kellokumpu I, Lindgren L (1996) Gasless laparoscopic cholecystectomy: comparison of postoperative recovery with conventional technique. Br J Anaesth 77: 576580

A. Cuschieri
Department of Surgery Ninewells Hospital and Medical School Dundee DD1 9SY, UK

Surg Endosc (1997) 11: 12281229

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Laparoscopic vs open hernioplasty

Which open technique for a correct comparison of outcomes?
We read with interest the article by J. Tschudi et al. entitled Controlled multicenter trial of laparoscopic transabdominal preperitoneal hernioplasty vs Shouldice herniorrhaphy: Early Results, published in the August 1996 issue of Surgical Endoscopy [13]. Patients treated by the open technique left the hospital later (6.3 vs 4.9 days), had more postoperative complications (26 vs 16%), and had double the rate of recurrence (4.6 vs 2.3%) experienced by patients treated by laparoscopy. Moreover, the open technique caused more postoperative pain and more delayed return to full work and usual activities. If the main aim of the authors was to demonstrate the superiority of laparoscopic transabdominal preperitoneal hernioplasty (LTAPPH) compared to the Shouldice herniorrhaphy, we do believe that they reached their goal, supported by the same conclusion reached by other similar randomized studies [6, 11]. If, on the other hand, the aim was to demonstrate the superiority of LTAPPH compared to open hernioplasty, we do not agree with the authors. We do think that it is not correct at all to compare LTAPPH to an open repair such as the Shouldice technique. Relying solely on the traditional open techniques, the advocates of laparoscopic hernia repair concluded that this offers a better outcome (less postoperative pain, shorter recovery period, and lower recurrence rate) [2]. This comparison is not appropriate, a more suitable approach to the problem being to compare it to a modern, tension-free and prosthetic repair such as the Lichtenstein repair [1], the Gilbert sutureless technique [5], and the Rutkow-Robbins mesh-plug repair [9]. The results of these techniques are significantly better than those recorded in a recent multicenter trial on LTAPPH [4]namely, a lower overall rate of complications, a lower rate of postoperative admissions, a lower rate of recurrence, and lower costs. Recently, a prospective randomized trial demonstrated the superiority of open plug repairs (Gilbert and RutkowRobbins) compared to LTAPPH [3]. Actually, the latter took longer operative time, required more postoperative admissions, showed the same rate and length of postoperative pain/discomfort, and was more expensive than the former. Patients undergoing LTAPPH returned to full work 4 days sooner than did patients submitted to open repair, but both groups were unusually quick to resume normal working activities compared to the commonly held notion of a 4week recuperation for hernia repair. The evidence that LTAPPH enables patients to return earlier to work could appear more theorethical than actual when comparing it with tension-free open repairs. Moreover, determinants of return to work are strongly subjective and influenced by the attitudes of patients, surgeons, and general practitioners. For example, in a recently reported randomized single-blind comparison of laparoscopic vs small-incision open cholecystectomy, in which patients were left free to decide their own time off-work, all the patients returned to work at the same time [7]. We are not surprised at all that LTAPPH induced less pain than the Shouldice technique in the study by Tschudi et al. This appears quite obvious when the comparison is made with techniques under tension with division of the hernial sac, because such maneuvers are the main determinants of postoperative pain [10]. Moreover, the degree of postoperative pain is very difficult to measure, and current criteria (postoperative consumption of analgesics, visual analogue scales, time off-work) appear unsufficient to cover the tremendous variations among different subjects. Anyway, in our personal series of about 700 open tension-free hernia repairs, only few patients required a mild analgesic during the first 10 postoperative h, prolonged administration having been anedoctal. In any case, less pain and more rapid resumption of working activities cannot overcome the disadvantages of LTAPPH: the need for general anesthesia, higher rate of postoperative complications, especially major ones, longer and difficult training, higher costs. Concerning laparoscopic hernia repair, on one hand, Rutkow [8] stated that simply because an operation can be done laparoscopically does not mean that is necessarily the most expedient method. On the other hand, Swanstrom [12] recently concluded that laparoscopic repair can be emphasized for bilateral hernias, recurrent hernias and, rarely, for patients undergoing unilateral, first-time hernia repairs who absolutely must resume normal activity at the earliest possible moment. We do agree that there is a place for laparoscopic hernioplasty in the treatment of groin hernia, but its indications should be determined by a careful and controlled comparison with prosthetic tension-free open hernioplasty. References
1. Amid PK, Shulman AG, Lichtenstein IL (1993) Critical scrutiny of the open tension-free hernioplasty. Am J Surg 165: 369371

1229 2. Amid PK, Shulman AG, Lichtenstein IL (1994) A critical comparison of laparoscopic hernia repair with Lichtenstein tension-free hernioplasty. Med J Aust 161: 239240 3. Brooks DC (1994) A prospective comparison of laparoscopic and tension-free open herniorraphy. Arch Surg 129: 361366 4. Fitzgibbons RJ, Camps J, Cornet DA (1995) Laparoscopic inguinal herniorrhaphy. Results of multicenter trial. Ann Surg 221: 313 5. Gilbert AI (1992) Sutureless repair of inguinal hernia. Am J Surg 163: 331335 6. Maddern JG, Rudkin G, Bessel JR, Devitt P, Ponte L (1994) A comparison of laparoscopic and open hernia repair as a day surgical procedure. Surg Endosc 8: 14041408 7. Majeed AW, Troy G, Nicholl JP, Smythe A, Reed MWR, Peacock J, Johnson AG (1996) Randomized prospective single-blind comparison of laparoscopic versus small-incision cholecystectomy. Lancet 347: 989994 8. Rutkow IM (1995) Open tension-free mesh plug versus laparoscopic herniorrhaphy: economic practicalities. Prog Surg 21: 105112 9. Rutkow IM, Robbins AW (1995) Mesh plug hernia repair: a follow up report. Surgery 117: 597598 10. Smedberg SGC, Broome AEA, Gullmo A (1984) Ligation of the hernial sac? Surg Clin North Am 64: 299306 11. Stoker DL, Spiegel H, Alter DJ, Singh R, Wellwood JM (1994) Laparoscopic versus open inguinal hernia repair: randomised prospective trial. Lancet 343: 12431245 12. Swanstrom LL (1996) Laparoscopic herniorrhaphy. Surg Clin North Am 76: 483491 13. Tschudi J, Wagner M, Klaiber CH, et al (1996) Controlled multicenter trial of laparoscopic transabdominal preperitoneal hernioplasty vs Shouldice herniorrhaphy. Early results. Surg Endosc 10: 845847

P. Negro F. Gossetti M. Catarci

2nd Surgical Clinic, University of Rome La Sapienza and Hernia Center of Rome V.le del Policlinico, 155 00161 Rome Italy

Surg Endosc (1997) 11: 1227

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

The author replies

We thank Dr. Zornig, Hamburg, Germany, for his interest in our recent article. The following topics were addressed in his letter. First he criticizes us in the laparoscopic procedures for neglecting local ulcer excision and describes that as a compromise of surgical standard. Regarding this point, we have to admit that the paper in Surgical Endoscopy really reflects our initial experience with laparoscopic ulcer closure. At the very beginning we were not yet able to completely excise an ulcer and close the duodenal wall. Today in 1997 this technique would of course be feasible; still, we would perform only simple closure of the ulcer today. The next topic addresses the problem of carbon dioxide pneumoperitoneum in patients with severe peritonitis and long interval between onset of peritonitis and treatment. Unfortunately, in our cases we are not able to document the exact time spent between the onset of peritonitis and surgical intervention. However, the concerns which are uttered by Dr. Zornig do not seem to translate into a clinical disadvantage for the patient. In their study (Surg. Endosc. 1995;9:898901) Bo chle and Zornig show that in rats a pneumoperitoneum aggravates the extent and severity of peritonitis when the interval between ulcer perforation and pneumoperitoneum is longer than 12 h. On the other hand, Gurtner (British Journal of Surgery 1995;82:844848) could not prove an adverse defect of carbon dioxide pneumoperitoneum on bacteremia and endotoxemia in a rabbit model. Parallel to the latter findings, clinically relevant disadvantages for the patients have, to our mind, not yet been proven. The distribution of patients to the treatment groups was also addressed. Of course, the intention to treat principle has to be followed. However, our number of patients was rather small, so we put the three conversion patients the conventional closure group. On the other hand, when these patients were calculated in the laparoscopic group (as was done in the paper), the rate of uncomplicated causes dropped to 43% of the patients (page 832). We agree with the authors that further sound experimental and clinical data focusing on the risk of laparoscopic management of peritonitis are needed. However, a further important piece of evidence has been collected by the study of Lau and others in the Annals of Surgery (1996;224:131 138). The authors report findings similar to those we have shown in our preliminary paper in Surgical Endoscopy.

E. Eypasch
2nd Department of Surgery University of Cologne Ostmerheimer Strae 200 51109 Ko ln Germany

Surg Endosc (1997) 11: 12161217

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

First trimester of pregnancy laparoscopic procedures

B. S. Schwartzberg, J. A. Conyers, J. A. Moore
Department of Surgery, Rose Medical Center, 4500 East 9th Avenue, Suite 710, Denver, CO 80220, USA Received: 25 March 1996/Accepted: 24 January 1997

Abstract. Laparoscopic procedures are being performed during pregnancy with increasing frequency; however, few first-trimester operations have been published. Two firsttrimester procedures are here reported, both performed with uneventful recoveries. Key words: Laparoscopy Pregnancy Appendectomy Cholecystectomy Twins

First-trimester pregnancy laparoscopic procedures remain controversial due to the potential impact of carbon dioxide pneumoperitoneum on fetal organogenesis. Traditional first-trimester open procedures are, however, associated with a fetal loss of 1.1% with appendectomy [7] and 12% with cholecystectomy [3]. Initial first-trimester laparoscopic reports have been encouraging [2, 4, 5, 8]. The operations have been successfully accomplished without fetal loss and subsequent delivery of healthy normal infants. We would like to present two first-trimester cases, an appendectomy and cholecystectomy, the second involving a twin pregnancy. Case reports Case report I
A 30-year-old woman (gravida 3, para 1, abortus 1) presented at 8 weeks of gestation with sudden acute right lower quadrant pain. Her medical history was pertinent for recurrent symptomatic Crohns disease. Physical examination revealed a temperature of 99.0F and significant localized abdominal pain. WBC was 4,600/mm3. Appendicitis was the primary preoperative diagnosis. Surgical options were discussed. These included either a standard open surgical approach with known organogenesis anesthetic risk and a 2% risk of fetal loss, or a laparoscopic approach which could

provide a more complete diagnostic evaluation, treatment, and quicker recovery, but with less known risk of organogenesis and fetal loss as a result of carbon dioxide pneumoperitoneum. Informed consent was obtained for laparoscopy. ASA class was 3E. Cefotetan was given as antibiotic prophylaxis. Sequential compression stockings were placed. Laparoscopy was initiated following general endotracheal anesthesia (GETA) using propofol, succinylcholine, fentanyl, mivacurium, and isoflurane. A Hassan port was placed with an open cutdown technique due to previous abdominal procedures. Pneumoperitoneum was maintained with carbon dioxide for an average intraabdominal pressure of 15 mmHg and an endtidal carbon dioxide of 2833 mmHg. O2 saturation was 9699%. Arterial gases were not obtained. Laparoscopy revealed a recent right ovarian cyst rupture. Active Crohns disease was not noted. The appendix was removed via a suprapubic port placed under direct vision. It was normal on final pathology. The procedure lasted 1 h. Transvaginal ultrasound fetal evaluation performed preoperatively and 48 h postoperatively documented a continued viable intrauterine pregnancy. Droperidol, ketorolac, morphine, and acetaminophen were given in the initial postoperative period. The patient was transitioned to oral oxycodone and hydrocodone. The patient was discharged on the 1st postoperative day. She had an uneventful pregnancy and delivered at 37 weeks gestation by elective cesarean section. The baby was healthy, weighing 7 lb 0 oz and having Apgar scores of 7 at 1 min and 9 at 5 min. Mother and child enjoy good health.

Case report II
A 31-year-old woman (gravida 6, para 3, abortus 2) was referred at 8.5 weeks gestation with symptomatic cholelithiasis. This was causing nausea and weight loss, threatening her twin pregnancy. She was afebrile with only minimal right upper quadrant pain. Laboratory values were normal. Multiple gallstones were documented by ultrasound. Informed consent included discussion of open surgical technique, with known anesthetic risk and 10% risk of fetal loss, or a laparoscopic approach with benefits of a short procedure and quick recovery but with less known risk of effect of carbon dioxide pneumoperitoneum on organogenesis or fetal loss. ASA class was 3, cefotetan was administered, and pneumatic stockings were placed preoperatively. GETA was initiated using fentanyl, thiopental, atracurium and isoflurane. Laparoscopic cholecystectomy was performed using a Veress needle to create a pneumoperitoneum (average insufflation 12 mmHg, O2 saturation 9699%; average endtidal CO230 mmHg). Arterial gases were not obtained. A cholangiogram was not performed as the biliary anatomy was straightforward; the procedure took 0.5 h. Postoperative medications were droperidol, demerol, and hydrocodone. Preoperative and 48-h postoperative transvaginal ultrasound fetal evaluation was unremarkable. The patient was discharged on the 2nd postoperative day; her appetite improved and she gained 30 lb over the next 23 weeks. An emergency cesarean section was performed at 31 weeks gestation for a bleeding placenta previa. Twin A was born weighing 3 lb 15 oz and had Apgar scores of 7 at 1 min and 8 at 5 min. He required ventilator support

Presented at the 5th World Congress of Endoscopic Surgery of the Society of American Gastrointestinal Endoscopic Surgeons (SAGES), Philadelphia, Pennsylvania, USA, 1317 March 1996 Correspondence to: B. S. Schwartzberg

1217 for 1 week following delivery. Twin B, weighing 4 lb 0 oz, had Apgar scores of 7 at 1 min and 8 at 5 min and needed continuous positive airway pressure after birth. All are now well.

Discussion Pregnancy is no longer considered an absolute contraindication to laparoscopic procedures. Laparoscopy is now being used cautiously for nonobstetrical emergent and urgent indications despite potential adverse complications. Although most frequently performed in the second trimester, first-trimester-pregnancy operations have been reported. First-trimester gynecologic procedures have included treatment of adnexal torsion [5], and treatment of an ectopic pregnancy complicating a concomitant intrauterine one (B. Albrecht, personal communication). Laparoscopy was also used to diagnose appendicitis in first-trimester patients [8]. Open appendectomies were then successfully performed. A first-trimester laparoscopic appendectomy is now being described. Three cases of first-trimester laparoscopic cholecystectomies have been published, including one successfully treating acute cholecystitis [2, 4, 6]. Increased fetal loss has been reported following nonobstetric second- and third-trimester laparascopic procedures [1]. Abnormal fetal organogenesis has not been observed. Most surgeons employed a Veress needle for firsttrimester insufflation. Intraoperative fetal monitoring was not performed during the first trimester, although transvaginal ultrasound fetal heart monitoring could be used after approximately 8 weeks gestation. End-tidal carbon dioxide measurements were used to monitor maternal, and thereby indirectly fetal, carbon dioxide levels during each procedure. More precise arterial gas monitoring was not utilized.

The abnormal fetal heart rhythms and excessive maternal end-tidal carbon dioxide levels which would mandate laparoscopic procedure termination have yet to be determined. During the first trimester of pregnancy laparoscopic procedures may have undetermined complications; however, most initial case reports reveal safe outcome. Long-term safety needs to be established. Further study should include both experimental animal models to better understand the fetal physiologic effects of laparoscopy and formation of a laparoscopy-in-pregnancy registry.

References
1. Amos JD, Schorr SJ, Norman PF, Poole GV, Thomae KR, Mancino AT, Hall TJ, Scott-Conner CEH (1996) Laparoscopic surgery during pregnancy. Am J Surg 171: 435437 2. Chandra M, Shapiro SJ, Gordan LA (1994) Laparoscopic cholecystectomy in the first trimester pregnancy. Surg Laparosc Endosc 4: 6869 3. Curet MJ, Allen D, Josloff RK, Pitcher DE, Curet LB, Miscall BG, Zucher KA (1996) Laparoscopy during pregnancy. Arch Surg 131: 546551 4. Elerding SC (1993) Laparoscopic cholecystectomy in pregnancy. Am J Surg 165: 625627 5. Garzarelli S, Mazuca N (1994) One laparoscopic puncture for treatment of ovarian cysts with adnexal torsion in early pregnancy. A report of two cases. J Reprod Med 39: 985986 6. Hart RO, Tamadon A, Fitzgibbons RJ, Fleming A (1993) Open laparoscopic cholecystectomy in pregnancy. Surg Laparosc Endosc 3: 13 16 7. Mazze RI, Kallen B (1991) Appendectomy during pregnancy: a Swedish registry study of 778 cases. Obstet Gynecol 77: 835840 8. Spirtos NM, Eisenkop SM, Spirtos TW, Poliakin RI, Hibbard LT (1987) Laparoscopya diagnostic aid in cases of suspected appendicitis. Its use in women of reproductive age. Am J Obstet Gynecol 156: 90009094

Surg Endosc (1997) 11: 12061208

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Laparoscopic cecal ligation and puncture in the rat

Surgical technique and preliminary results
R. Berguer,1 A. Alarcon,2 S. Feng,1 C. Gutt3
1 2

Department of Surgery, University of California Davis Medical Center, 4301 X. Street, Room 2310, Sacramento, CA 85917, USA Central University of Ecuador, Calle Sodiro y 12 de Octubre, Quito, Ecuador 3 Johann-Wolfgang-Goethe Universitat Frankfurt, Theodor-Stern-Kai 7, 60590 Frankfurt, Germany Received: 3 July 1996/Accepted: 7 January 1997

Abstract Background: We describe a technique of laparoscopic cecal ligation and puncture (CLP) in the rat analogous to open CLP which may facilitate the study of minimally invasive surgery (MIS) and peritonitis. Methods: Forty-four rats were randomized to either laparoscopic or open CLP and their 3-day mortality was recorded. Autopsies were performed for peritoneal fluid cultures, measurement of the length of ligated cecum, and scoring of the degree of cecal necrosis. Results: Laparoscopic CLP required slightly longer operating times compared to open CLP (average 15.6 vs 13.1 min, p 0.002). Three-day postoperative mortality was 36.4% and 22.7% for open and laparoscopic CLP, respectively (p NS). There were no differences in the length of ligated cecum or the cecal necrosis score between the open and laparoscopic CLP groups. Conclusion: Laparoscopic CLP is feasible and produces a fecal peritonitis with similar characteristics to those of traditional open CLP. Key words: Laparoscopy Cecal ligation and puncture Peritonitis Rats

would be facilitated by the development of a good MIS animal model of peritonitis. Cecal ligation and puncture (CLP) is a simple and widely used model of severe peritonitis [11, 15]. We have adapted the technique of open CLP to our rat model of laparoscopic surgery [3, 4] and herein report our preliminary results with this technique.

Methods
The research protocol was approved by the Animal Care and Use Committee at the University of California Davis. Male Lewis rats weighing 250300 g (Charles River Laboratories) were housed individually in plastic cages and fed standard rat chow. Rats were not fasted prior to CLP so as to maintain the maximum amount of stool in the gastrointestinal tract. Following CLP rats were given ad lib water and rat chow. No antibiotics or pain medications were administered to avoid confounding effects on immune function. Animals who died during the first 3 postoperative days were stored at 20C in plastic bags until necropsy on day 4. On postoperative day 4 all surviving animals were euthanized by CO2 inhalation per AALAC guidelines and necropsies were performed on all animals. At necropsy, the peritoneal cavity was examined and the gross appearance of the cecum was graded as Normal, Red, or Black/gray (authors classification). In order to assess the adequacy of the laparoscopic placement of the cecal ligature, the distance from this ligature to the tip of the necrotic cecum was measured in all animals. In animals that survived to postoperative day 4, necropsy also included a swab of peritoneal fluid for aerobic and anaerobic culture. Rats were anesthetized with 1.52.0% isoflurane and 50% nitrous oxide at gas flow rates of 2 l/min via tight-fitting masks in order to provide rapid induction and reversal of anesthesia without the need for intraperitoneal injection. The animals body temperature was monitored with a rectal probe and maintained between 37 and 38C during surgery with an electric heating pad. Five ml per 100 g body weight of 0.9% saline fluid resuscitation was given subcutaneously in the neck to all animals prior to awakening. Our laparoscopic surgical technique used a specialized small-animal operating table (Kaps Co., Frankfurt, Germany) (Fig. 1) with an attached flexible arm to hold the laparoscope. Rats were placed supine on the operating table over an electric heating pad and with the head and anesthesia mask facing the surgeon. The abdomen was shaved, sprayed with 70% isopropyl alcohol, and covered with a sterile paper drape. All instruments were sterilized in solution and cleansed with 70% isopropyl alcohol.

The application of minimally invasive surgery (MIS) techniques to a wide variety of operations has demonstrated that this technique causes less postoperative pain, a more rapid recovery [1, 12], and possibly less stress-induced postoperative immune impairment than open surgery [2, 5, 8, 13, 14], although the evidence for the latter remains controversial [11]. The study of potential benefits of MIS in the treatment peritonitis as well as the understanding of the host reaction to visceral perforation at the time of laparoscopy
Correspondence to: R. Berguer

1207

Fig. 1. The small-animal laparoscopic operating table (Kaps Co., Frankfurt, Germany) allows the operator or an assistant to move the table, rather than the laparoscope, in order to change the surgeons view.

Fig. 2. Kaplan-Meier survival curves for rats undergoing laparoscopic or open cecal ligation and puncture (n 22 for each group). The differences in survival between the two groups are not statistically significant by the log-rank test. open, ..... laparoscopy.

We employed a 2.9-mm arthroscopic sheath with a blunt obturator (Dyonics Inc., Andover, MA) held by the flexible arm on the operating table and introduced into the abdomen via a 2-mm subxyphoid midline abdominal puncture. A 2.7-mm-diameter 30 wide-angle arthroscope (Dyonics Inc.) was inserted through the sheath into the peritoneal cavity and connected to a laparoscopic light source and video camera (Karl Storz Endoscopy, Germany) to visualize the peritoneal cavity on a 13-inch color video monitor (Sony Corp., Japan). We created a 23 mmHg CO2 pneumoperitoneum using a standard laparoscopic insufflator (Karl Storz Endoscopy, Germany) connected to the side port of the arthroscopic sheath. Micro-alligator forceps (Weck Endoscopy, Largo, FL) were placed directly into the peritoneal cavity through right and left abdominal wall punctures for dissection and knot tying. The cecum in the rat is large and easy to identify and usually lies in the left lower abdomen with the ileocecal junction nearest the surgeon when viewed from a cephalad direction. The ileocecal peritoneal reflection is divided bluntly to free the tip of the cecum for ligation. A 3-cm 4.0 silk ligature is inserted into the peritoneal cavity through the lumen of an 18-gauge needle which is introduced and left in alongside the left-sided forceps. The ligature is grasped from the inside with the right-sided forceps and placed around the tip of the cecum as near to the ileocecal junction as possible. Using two-handed intracorporeal knot-tying technique, a surgeons knot and two more squared throws were used to ligate the cecum. The tip of the same 18-gauge needle is then easily used to puncture the antimesenteric surface of the cecum distal to the ligature in three different locations. At the end of the procedure the instruments, needle, and the arthroscope are removed and the three abdominal wall puncture sites are closed with skin staples (Davis and Geck, Danbury, CT). For the purpose of exact comparison 44 rats were randomized to either laparoscopic CLP or open CLP. Open CLP was carried out via a 4-cm midline incision using the same steps and instruments as described for the laparoscopic approach. Statistical comparison of the length of ligated cecum and operative times was performed by Students t-test. The comparison of the cecal necrosis score and the number of positive peritoneal cultures was performed by chi-square analysis. The survival rats for the two groups were compared using a Kaplan-Meier survival curve and the log-rank test. Statistical significance was set at p < 0.05.

ligated cecum, the cecal necrosis score, or the number of positive peritoneal cultures between the two groups (Table 1).

Discussion Laparoscopic surgery in the rat is gaining wider acceptance among MIS researchers [57, 10, 14]. Our animal model of peritonitis induced by laparoscopic surgery is simple and effective and may be most useful for the study of effects of bowel injury at the time of laparoscopy. This model may also allow a comparison of the stress and immune responses to peritonitis with and without a laparotomy incision. Our technique is based on previously reported open methods [15] except that we dont milk the stool into the cecum. In order to maintain uniformity of technique between laparoscopic and open CLP we used the same laparoscopic instruments, dissection technique, and knot-tying methods during both procedures. The adequacy of our CLP technique is attested to by the similar mortality, length of cecal ligation, and cecal necrosis score compared to open CLP. Several technical tips may be of help to other investigators interested in performing laparoscopic CLP. The surgeon needs to be careful not to cause bleeding from tearing small surface vessels on the cecum during the blunt division of the ileocecal ligament. Passing the ligating silk suture through the abdominal wall through a needle avoided the need to remove an instrument to introduce the ligature during the operation and therefore the need for trocars. By passing the needle along the left-sided instrument we avoided an additional abdominal wall puncture and the tip of the needle remained ready for cecal puncture as soon as the ligature was tied. There is no need to trim the ends of the silk ligature.

Results There were no intraoperative deaths or differences in body weight or rectal temperature between animals undergoing laparoscopic or open CLP. Laparoscopic CLP required slightly longer operating times than open CLP (average 15.6 vs 13.1 min, p 0.002). The 3-day postoperative mortality was 36.4% for open CLP and 22.7% for laparoscopic CLP (Fig. 2, p NS). There were no differences in the length of

1208 Table 1. The gross appearance and length of ligated cecum at necropsy in rats 4 days following laparoscopic or open CLP; NS nonsignificant Laparoscopic CLP Length of cecal ligation (mm) Cecum normalb Cecum redb Cecum black/grayb (+) peritoneal cultureb
a b a

Open CLP 13.1 3 10 4 10 NS NS NS NS NS

15.6 5 6 4 10

Group average. Number of animals.

References
1. (1993) National Institutes of Health consensus development conference on gallstones and laparoscopic cholecystectomy. Am J Surg 165: 390396 2. Allendorf J, Kayton M, Libutti S, Trokel M, Whelan R, Treat M, Nowygrod R, Bessler M (1994) The effect of laparotomy versus insufflation on tumor establishment and growth. Surg Endosc 8: S38 3. Berguer R, Gutt C, Stiegmann GV (1993) Laparoscopic surgery in the rat. Description of a new technique. Surg Endosc 7: 345347 4. Berguer R, Gutt CN (1994) Laparoscopic colon surgery in a rat model: a preliminary report. Surg Endosc 8: 11951197 5. Bouvy ND, Marquet RL, Hamming JF, Jeekel J, Bonjer HG (1996) Laparoscopic surgery in the rat: beneficial effect on body weight and tumor take. Surg Endosc 10: 490494

6. Crane LH, Martin L (1991) In vivo myometrial activity in the rat during the oestrous cycle: studies with a novel technique of video laparoscopy. Reprod Fertil Dev 3: 185199 7. Filmar S, Gomel V, McComb PF (1987) Operative laparoscopy versus open abdominal surgery: a comparative study on postoperative adhesion formation in the rat model. Fertil Steril 48: 486489 8. Griffith J, Everitt N, Curley P, McMahon M (1993) Laparoscopic versus open cholecystectomyreduced influence upon immune function and the acute phase response. Surg Endosc 7: 123 9. Johnson D, Spencer M, Cerra F, Constatidides F, Tothenberger D, Madoff R (1994) Laparoscopic versus open colectomy. A comparative study of the systemic stress response. Surg Endosc 8: S37 10. Kayton M, Morales A, Chen M, Treat M, Nowygrod R (1994) Laparoscopic surgery in the rat: a model for teaching laparoscopic suturing techniques. Surg Endosc 8: 264 11. Martinell S, Falk A, Haglund U, Myrvold H (1985) Peritonitis and septic shockan evaluation of two experimental models in the rat. Eur Surg Res 17: 160166 12. Troidl H, Spangenberger W, Langen R, al-Jaziri A, Eypasch E, Neugebauer E, Dietrich J (1992) Laparoscopic cholecystectomy: technical performance, safety and patients benefit. Endoscopy 24: 252261 13. Trokel M, Allendorf J, Treat M, Whelan R, Nowygrod R, Bessler M (1994) Inflammatory response is better preserved after laparoscopy vs laparotomy. Surg Endosc 8: S30 14. Trokel MJ, Bessler M, Treat MR, Whelan RL, Nowygrod R (1994) Preservation of immune response after laparoscopy. Surg Endosc 8: 13851387; discussion 13871388 15. Wichterman KA, Baue AE, Chaudry IH (1980) Sepsis and septic shock: a review of laboratory models and a proposal. J Surg Res 29: 189201

News and notices

Surg Endosc (1997) 11: 12321234

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

New Address for the European Association for Endoscopic Surgery (E.A.E.S.)
Effective January 1, 1997, the new correspondence, telephone, and fax numbers of the E.A.E.S. office are: E.A.E.S. Office, c/o Mrs. Ria Palmen Luchthavenweg 81 Unit 1.42 5657 EA Eindhoven The Netherlands or: P.O. Box 335 5500 AH Veldhoven The Netherlands Tel: +31 40 2525288 Fax: +31 40 2523102

Essentials of Laparoscopic Surgery Surgical Skills Unit University of Dundee Scotland, UK

Under the direction of Professor A. Cuschieri the Surgical Skills Unit is offering a three-day practical course designed for surgeons who wish to undertake the procedures such as laparoscopic cholecystectomy. This intensely practical program develops the necessary operating skills, emphasizes safe practice, and highlights the common pitfalls and difficulties encountered when starting out. Each workshop has a maximum of 18 participants who will learn both camera and instrument-manipulation skills in a purpose-built skills laboratory. During the course there is a live demonstration of a laparoscopic cholecystectomy. The unit has a large library of operative videos edited by Professor Cuschieri, and the latest books on endoscopic surgery are on display in our Resource area. Course fee including lunch and course materials is $860. For further details and a brochure please contact: Julie Struthers, Unit Co-ordinator Surgical Skills Unit Ninewells Hospital and Medical School Dundee DD1 9SY Tel: +44 382 645857 Fax: +44 382 646042

Volunteer Surgeons Needed Northwestern Nicaragua Laparoscopic Surgery Teaching Program, Leon, Nicaragua
Volunteer surgeons are needed to tutor laparoscopic cholecystectomy for this non-profit collaboration between the Nicaraguan Ministry of Health, the National Autonomous University of Nicaragua, and Medical Training Worldwide. The program consists of tutoring general surgeons who have already undergone a basic laparoscopic cholecystectomy course. Medical Training Worldwide will provide donated equipment and supplies when needed. For further information, please contact: Medical Training Worldwide Ramon Berguer, MD, Chairman Tel: 707-423-5192 Fax: 707-423-7578 e-mail: berguer.r@martinez.va.gov

Advanced Endoscopic Skills Surgical Skills Unit University of Dundee Scotland, UK

Each month Professor Cuschieri Surgical Skills Unit offers a 412 day course in Advanced Endoscopic Skills. The course is intensely practical with hands on experience on a range of simulated models. The program is designed for experienced endoscopic surgeons and covers advanced dissection techniques, extracorporeal knotting techniques, needle control, suturing, internal tying technique, stapling, and anastomotic technique. Individual workstations and a maximum course number of 10 participants allows for personal tuition. The unit offers an extensive collection of surgical videos and the latest books and publications on endoscopic surgery. In addition, participating surgeons will have the opportunity to see live advanced laparoscopic and/or thoracoscopic procedures conducted by Professor Cuschieri and his team. The course is endorsed by SAGES. Course fee including lunch and course materials is $1850. For further details and a brochure please contact: Julie Struthers, Unit Co-ordinator Surgical Skills Unit Ninewells Hospital and Medical School Dundee DD1 9SY Tel: +44 382 645857 Fax: +44 382 646042

Fellowship in Minimally Invasive Surgery George Washington Medical Center Washington, DC USA
A one-year fellowship is being offered at the George Washington University Medical Center. Interested candidates will be exposed to a broad range of endosurgical Education and Research Center. Active participation in clinical and basic science research projects is also encouraged. For further information, please contact: Debbie Moser 202-994-8425 or, send curriculum vitae to: Dr. Jonathan M. Sackier Director, Washington Institute of Surgical Endoscopy George Washington University Medical Center Department of Surgery 2150 Pennsylvania Avenue, N.W. 6B-417 Washington, DC 20037, USA

The Practical Aspects of Laparoscopic Fundoplication Surgical Skills Unit University of Dundee Scotland, UK
A three-day course, led by Professor Cuschieri, designed for experienced laparoscopists wishing to include fundoplication in their practice. The

1233 course covers the technical details of total and partial fundoplication using small group format and personal tuition on detailed simulated models. There will be an opportunity to observe one of these procedures live during the course. Maximum course number is six. Course fee including lunch is $1850. For further details and a brochure please contact: Julie Struthers, Unit Co-ordinator Surgical Skills Unit Ninewells Hospital and Medical School Dundee DD1 9SY Tel: +44 382 645857 Fax: +44 382 646042 tomy (May 1516, August 1112, November 1011, 1997); Laparoscopic colon and rectal surgery (June 2021, September 1516, December 45, 1997). Also, courses for operating room nurses and technicians will be run on a monthly basis and personal instruction and preceptorship is available. For further information, please call: Debbie Moser Washington Institute of Surgical Endoscopy 2150 Pennsylvania Avenue, N.W. Washington, DC 20037 Tel: 202-994-9425

Courses at the Royal Adelaide Centre for Endoscopic Surgery

Basic and Advanced Laparoscopic Skills Courses are conducted by the Royal Adelaide Centre for Endoscopic Surgery on a regular basis. The courses are limited to six places to maximize skill development and tuition. Basic courses are conducted over two days for trainees and surgeons seeking an introduction to laparoscopic cholecystectomy. Animal viscera in simulators is used to develop practical skills. Advanced courses are conducted over four days for surgeons already experienced in laparoscopic cholecystectomy who wish to undertake more advanced procedures. A wide range of procedures are included, although practical sessions can be tailored to one or two procedures at the participants request. Practical skills are developed using training simulators and anaesthetised pigs. Course fees: $A300 ($US225) for the basic course and $A1,600 ($US1,200) for the advanced course. For further details and brochure, please contact: Dr. D. I. Watson or Professor G. G. Jamieson The Royal Adelaide Centre for Endoscopic Surgery Department of Surgery Royal Adelaide Hospital Adelaide SA 5000 Australia Tel: +61 8 224 5516 Fax: +61 8 232 3471

Call for Abstracts Society of American Gastrointestinal Endoscopic Surgeons (SAGES) 1998 Annual Meeting April 14, 1998 Seattle, WA, USA
Abstract deadlines: Oral and Poster abstracts: September 12, 1997 Video Submissions: September 18, 1997 For further information, or to obtain an abstract form, please contact: SAGES Program Committee Society of American Gastrointestinal Endoscopic Surgeons Suite #3000 2716 Ocean Park Boulevard Los Angeles, CA 90405 Tel: (310) 314-2404 Fax: (310) 314-2585 e-mail: SAGESMail@AOL.com

Advanced Laparoscopic Suturing and Surgical Skills Courses MOET Institute San Francisco, CA, USA
Courses are offered year-round by individual arrangement. The MOET Institute is accredited by the Accreditation Council for Continuing Medical Education (ACCME) to provide continuing medical education for physicians and designates these CME activities for 2040 credit hours in Category 1 of the Physicians Recognition Award of the American Medical Association. These programs are also endorsed by the Society of Gastrointestinal Endoscopic Surgeons (SAGES). For further information, please contact: Wanda Toy, Program Administrator Microsurgery & Operative Endoscopy Training (MOET) Institute 153 States Street San Francisco, CA 94114, USA Tel: (415) 626-3400 Fax: (415) 626-3444

Second Asian Pacific Symposium and Workshop on Minimally Invasive Thoracic and Cardiac Surgery December 911, 1997 Taipei, Taiwan
The main themes are updates and live operative demonstrations of thoracoscopy and video-assisted thoracic surgery, minimally invasive cardiac surgery, and thoracoscopic spine surgery. For further information, please contact: Hui-Ping Liu, MD Division of Thoracic and Cardiovascular Surgery Chang Gung Memorial Hospital 199 Tun-Hwa N Rd. Taipai, Taiwan 10591 Tel: 866-3-3281200 Fax: 866-3-3285818

Courses at WISE Washington Institute for Surgical Endoscopy Washington, DC, USA
The Washington Institute of Surgical Endoscopy is pleased to offer the following courses: Laparoscopic antireflux and hiatal hernia surgery (July 1415, 1997); Laparoscopic management of the common bile duct and difficult cholecystec-

Colorectal Disease in 1998 February 1921, 1998 Fort Lauderdale, FL, USA Symposium Director: Steven D. Wexner, MD
Cleveland Clinic Florida presents its ninth annual postgraduate course. Provides an intensive, in-depth, analytical review of all aspects of colorectal disease, including laparoscopy; colorectal carcinoma screening and

1234 genetics, inflammatory bowel disease; and pouch surgery. There will be a review of both basic and advanced principles of diagnosis and management of disease. Video techniques will be shown as well. The faculty is internationally represented and includes leading experts in the field. Simultaneous Spanish and Italian translation is available. For more information, please contact: Cleveland Clinic Florida Department of Education 2950 West Cypress Creek Road Fort Lauderdale, FL 33309-1743 Tel: 800-359-6101, ext. 6066 Fax: 954-978-5539 original and non original scientific reports; and a world expo of new technology in surgery. For further information, please contact: Congress Secretariat: Studio EGA Viale Tiziano, 19 00196 Rome, Italy Tel: +39 6 322-1806 Fax: +39 6 324-0143

Tenth International Conference of the Society for Minimally Invasive Therapy September 35, 1998 London, England
Host Chairman: Mr. J. Wickham For further information, please contact: The Society for Minimally Invasive Therapy 2nd Floor, New Guys House Guys Hospital St. Thomas Street London, SE1 9RT, England Tel: +44 (0)171 955 4478 Fax: +44 (0)171 955 4477 email: j.wickham@umds.ac.uk

6th World Congress of Endoscopy Surgery Roma 98 6th International Congress of European Association for Endoscopic Surgery June 36, 1998 Rome, Italy
The program will include: the latest, original high quality research; symposia; plenary lectures; abstract presentations (video, oral, and posters); EAES and SAGES postgraduate courses, OMED postgraduate course on therapeutic endoscopy; working team reports; educational center and learning corner; meeting of the International Society of Nurses and Associates;

Surg Endosc (1997) 11: 11981201

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Needle and trocar injury during laparoscopic surgery in Japan

M. Hashizume, K. Sugimachi, Study Group of Endoscopic Surgery in Kyushu, Japan
Department of Surgery II, Faculty of Medicine, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka, 812-82, Japan Received: 10 February 1997/Accepted: 22 May 1997

Abstract Background: With the growth and sophistication of laparoscopic surgery, increased attention is now being focused on safety and complications. Methods: In an attempt to address questions regarding the safety of laparoscopic surgery, a retrospective study of the time period from January 1991 to December 1995 was conducted by the Study Group of Endoscopic Surgery in Kyushu, Japan. Results: The response rate was 84.4% (152 of 180 hospitals). During the last 5 years 17,626 patients underwent endoscopic operations and 87.5% (15,422 patients) had laparoscopic surgery while 12.5% (2,204 patients) underwent thoracoscopic surgery. In 96.6% of the hospitals a minimal open laparotomy was used. Among the various operations, a cholecystectomy was performed in the largest number of patients (13,787). The total number of complications was 415 (2.7%), of which 156 (37.6%) were related to needle or trocar insertion. Visceral injury was found in 22 patients (0.14%): major vessel injury in 10, gastrointestinal tract injury in 11, and liver injury in one patient. Abdominal wall injury was seen in 79 patients (0.52%), bleeding in 70 (0.46%), and a hernia in 9 (0.06%). Extraperitoneal insufflation occurred in 55 patients (0.36%). There was no mortality. The complication rate significantly decreased year by year after the use of laparoscopic surgery began. Conclusions: The most common complications of laparoscopic surgery are related to needle and trocar insertion. These are preventable by placement under direct vision with verification of the intraperitoneal location of the needle and trocar. Key words: Trocar injury Complication Laparoscopic surgery

Having achieved vast acceptance following its pioneering phase, minimally invasive surgery is now exerting a substantial impact on the world of medicine. The use of laparoscopy as an alternative to open surgery continues to grow dramatically. Along with its growth and sophistication, however, has also come an intensified focus on the need to prevent laparoscopic complications [3, 5, 6, 21]. The potential complications of laparoscopic surgery include those resulting from the insertion of the needle and trocar, the creation of the pneumoperitoneum, the positioning of the patient, and the insertion and manipulation of the instruments [2, 18, 22]. In an attempt to address questions regarding the safety of laparoscopic surgery, a retrospective study of the time period from January 1991 to December 1995 was conducted by the Study Group of Endoscopic Surgery in Kyushu, Japan. Materials and methods
In November 1995, we mailed a questionnaire to 180 hospitals that are members of the Study Group of Endoscopic Surgery in Kyushu, Japan. The respondents involved in the collection of data were chiefs of departments of the hospitals and the data were collected from medical records. The questions referred to the frequencies with which laparoscopic procedures were carried out during the period of January 1991 to December 1995 and also to the frequency of complications. The analysis of complication related to needle and trocar insertion was conducted on patients who underwent laparoscopic surgery. The patients who underwent thoracoscopic surgery or transanal endoscopic microsurgery (TEM) were excluded from this study. In addition, the preventive measures taken to avoid complications were evaluated.

Results The Study Group survey generated a response rate of 84.4% (152/180). In five (3.3%) of the 152 hospitals that participated in the survey, only thoracoscopic operations were performed. Between January 1991 and December 1995, 17,626 patients were registered; 87.5% (15,422 patients) of the total number of patients underwent laparoscopic surgery while 12.5% (2,204 patients) had thoracoscopic surgery. In all of the hospitals except three, the total number of lapa-

Presented in part at the postgraduate course of the 5th World Congress of Endoscopic Surgery, Philadelphia, Pennsylvania, USA Correspondence to: M. Hashizume

1199 Table 1. Type of laparoscopic operations Cholecystectomy Repair of inguinal hernia Colectomy Choledochotomy Transanal endoscopic microsurgery (TEM)a Partial gastrectomy Release of ileus Splenectomy Repair of duodenal perforation Appendectomy Drainage of hepatic cyst Hepatectomy Vagotomy Resection of pancreas Repair of esophageal hernia Esophagectomy Others Total
a

Table 2. Complications related to needle and trocar insertion 13,787 541 197 150 143 113 99 80 57 44 14 8 6 5 5 2 171 15,422 Complication Abdominal wall injury Bleeding Hernia Visceral injury Major vessel Gastrointestinal tract Liver Extraperitoneal insufflation Total n 79 70 9 22 10 11 1 55 156/ 15,279 % 0.52 0.46 0.06 0.14 0.07 0.07 0.01 0.36 1.02

In this study, 143 patients who underwent TEM were excluded from the analysis of complication related to needle and trocar insertion.

roscopic operations performed was under 500 cases. In three hospitals more than 1,000 cases were reported. Table 1 shows the type of operations performed. The great majority of these operations were laparoscopic cholecystectomies (13,787, 89.4%). The mortality rate was zero. TEM was performed in 143 patients and was excluded from this study. The total complication rate was 2.7% (415/ 15,279). The insertion of needle or trocar was responsible for 156 injuries during laparoscopy (Table 2). Of these complications, 79 patients had early and late abdominal wall injuries, 22 patients had visceral injuries, and 55 patients experienced extraperitoneal insufflation. In 142 (96.6%) of the 147 hospitals in the Study Group open laparoscopy was performed (except during the 1st year, when endoscopic surgery had just started); only five hospitals still used the Veress needle to establish a pneumoperitoneum.

Fig. 1. Rate of vascular injury.

Gastrointestinal tract injury Gastrointestinal tract injury occurred in 23 patients. The incidence of gastrointestinal tract injury related to trocar insertion was 0.07% (11 patients) (Fig. 2). The small intestine was injured in 10 patients and the large intestine in one patient. Injury was caused by insertion of the primary trocar in seven patients (63.6%) and the secondary trocar in four patients. No intestinal injuries were related to insertion of the Veress needle. A laparotomy was required in two patients and all injuries were successfully sutured. Figure 2 shows the rate of gastrointestinal tract injury each year after starting endoscopic surgery. The incidence of gastrointestinal tract injury decreased over time.

Vascular injury Vascular injury occurred in 152 patients (Fig. 1), but major vascular injury related to needle and trocar insertion occurred in only 10 patients (0.07%). The aorta was injured in one patient, the left common iliac artery in one patient, right common iliac artery in three patients, the gastroepiploic artery in one patient, the epigastric artery in one patient, the retroperitoneal vessel in one patient, and the superior mesenteric artery in two patients. The mechanism of injury involved insertion of the primary trocar in seven patients (70%) and insertion of the Veress needle in two patients (20%). Injury was due to placement of the secondary trocar in one patient. A laparotomy was required in nine of 10 patients with vascular injury. Suturing was done in five patients, ligation in two patients, electrocoagulation in one patient, and tamponade in one patient. Only one patient required no treatment for the bleeding. Figure 1 shows the complication rate of vascular injury every year after starting endoscopic surgery. The incidence of vascular injury was the highest in the 1st year but thereafter gradually decreased.

Bleeding from the abdominal wall Bleeding from the abdominal wall, which was the most common complication, was always caused by trocar insertion and occurred in 70 patients (0.46%). The most frequent sources of hemorrhage were the superficial epigastric, inferior epigastric, and muscular abdominal wall vessels. In 69 patients the bleeding was from the secondary trocar sites. A laparotomy was required in four patients. Suture ligature of the bleeding vessels was done extracorporeally in 20 patients and intracorporeally in three patients. Electrocoagulation was done externally in 14 patients and laparoscopically in two patients. Tamponade with the use of a Foley balloon catheter was successfully applied in one patient. Bleeding from the abdominal wall spontaneously ceased during operation without any specific treatment in 30 pa-

1200

Fig. 2. Rate of gastrointestinal tract injury.

Fig. 3. Rate of bleeding from the abdominal wall.

tients. The rate of bleeding from the abdominal wall decreased with experience (Fig. 3).

Primary late abdominal wall complications Hernia formation occurred as a late abdominal wall complication in nine patients (0.06%). Hernias were found at the umbilical site of the primary trocar in seven patients and at an extraumbilical site in two patients. All hernias were associated with a port site larger than 10 mm in size. A laparotomy was required in five patients and suture repair was performed in nine patients. One hernia was repaired laparoscopically with the use of a mesh. The incidence of postoperative hernia by each year is shown in Fig. 4.

Fig. 4. Rate of postoperative hernia.

Table 3. Complications related to pneumoperitoneum

Complications related to pneumoperitoneum The complication rate related to the pneumoperitoneum was 0.48% (Table 3). Subcutaneous emphysema was the most common of these complications. In 54 of 55 patients in whom subcutaneous emphysema was found no specific treatment was necessary. In the remaining patient, evacuation of the gas by manual pressure on the abdominal wall was done.

Complications Subcutaneous emphysema Right shoulder or back pain Pneumothorax Hypercarbia Vagotonia Oliguria Pulmonary infarction CO2 gas embolism Total

n 55 6 4 3 2 1 1 1 73/ 15,279

% 0.36 0.04 0.03 0.02 0.01 0.01 0.01 0.01 0.48

Discussion The insertion of the Veress needle or trocars is responsible for a substantial number of injuries during laparoscopy. It has been reported that the complication rate of Veress needle or trocar insertion during closed laparoscopy is approximately 0.20.3% [14]. The modern technique of open laparoscopy was first popularized by Hasson in 1974 [8]. The primary advantage of this technique is that access to the peritoneal cavity is gained under direct vision. Therefore, bowel and vascular injuries should be virtually nonexistent [4, 13, 16]. However, bowel injuries still occur at the same rate using this technique. Of our Study Group members, 96.6% changed their method of establishing a pneumoperitoneum from the closed method to an open laparoscopic technique in order to increase patient safety during endoscopic surgery. The rate of complications related to needle and trocar insertion subsequently decreased as the surgeons experience performing endoscopic surgery increased. Vascular injuries, which occur in 0.10.6% of all patients, may involve abdominal wall vessels, major retroperitoneal vessels, or other intraabdominal vessels [1, 14, 15]. Injury to the major retroperitoneal vessels such as the aorta, inferior vena cava, and iliac artery or vein has a mortality rate of 9% [4]. Major vascular injuries occur in about 0.030.06% of the patients [17, 18, 20]. Injury to a major vessel is the second most common cause of death during laparoscopy, following anesthesia. A delayed diagnosis is common in such fatalities. The mechanism of injury involves the Veress needle in approximately two-thirds of all such cases and the insertion of the primary trocar in one-third of cases. Our study also showed that in nine of 10 patients the major

1201

vascular injury was associated with the Veress needle and the primary trocar. In nine of 10 patients an open laparotomy was required to control bleeding. The best management of major vascular injury is prevention. The proper technique of Veress needle insertion and verification of an intraperitoneal location are the two most important steps [4]. If an injury occurs, the Veress needle should be left in place and an immediate laparotomy should then be performed to obtain vascular control. Injuries to the vessels of the abdominal wall are a frequent source of morbidity, occurring in 0.256.0% of cases [14, 15]. Bleeding from abdominal wall vessels is usually manifested by troublesome oozing around the trocar, either internally or externally. In 30 of the 70 patients with bleeding from the abdominal wall, the bleeding spontaneously ceased during the operation after merely applying pressure with the trocar on the abdominal wall. Other initial methods of management include tamponade with a Foley balloon catheter or a lever to apply pressure to the posterior aspect of the anterior abdominal wall. Coagulation or ligation of the bleeding point externally or internally with a laparoscopic approach is an alternative method. Finally, if all such methods fail, a laparotomy should be done to stop the bleeding. Injuries to the abdominal wall vessels may also be avoided in thin patients by transillumination and by inspection of the abdominal wall prior to trocar insertion. The complications of gastrointestinal injury are second only to hemorrhage in frequency. Half of the gastrointestinal tract injuries during operation are due to trocar insertion. The incidence in large series has been reported to range from 0.06 to 0.4% [7, 912, 15, 19, 20] and has been associated with a relatively high mortality rate of 5%. The injuries most frequently involve the small intestine, followed by the colon, duodenum, and stomach [6]. These injuries are often unrecognized at the time of the laparoscopic procedures and are usually only detected later when the patient presents with peritonitis, sepsis, or intraabdominal abscess. The incidence of gastrointestinal tract injury was the highest in the 1st year after starting endoscopic surgery, but the incidence of such injuries has substantially decreased as the experience of the surgeons performing endoscopic surgery has increased. The predominate late abdominal wall complication following laparoscopic surgery is hernia formation. Herniation through laparoscopic entry sites is uncommon, with an incidence of less than 0.1% [2]. It is possible that this complication has been underreported. Boike et al. [2] offered several guidelines that may reduce the occurrence of this complication. The surgeon should use smaller trocars (5 mm), if possible. The use of trocar anchoring devices such as fascial screws may increase the risk of herniation by widening the fascial defect. When ports larger than 10 mm are used an attempt should thus be made to suture the defect. If the surgeon elects not to close these incisions, then recommendations include the use of Z-track placement of trocars and the slow release of the pneumoperitoneum with direct visualization of the trocar removal to ensure that the bowel is not drawn into the abdominal wall. Selected cases of herniation may also be managed laparoscopically. In conclusion, the complications related to needle and

trocar insertion are preventable by placement under direct vision. Laparoscopic surgery is safe and effective when proper techniques are utilized.
Acknowledgments. We wish to express our heartfelt thanks to Drs. Shinichiro Migo and Kouji Tsugawa for their kind help in the statistical treatment of the data collected in this study.

References
1. Begqvist D, Bergqvist A (1987) Vascular injuries during gynecologic surgery. Acta Obstet Gynecol Scand 66: 1923 2. Boike GM, Miller CE, Spirtos NM, Mercer LJ, Fowler JM, Summitt R, Orr JW (1995) Incisional bowel herniations after operative laparoscopy: a series of nineteen cases and review of the literature. Am J Obstet Gynecol 172: 17261733 3. Deziel DJ (1994) Avoiding laparoscopic complications. Int Surg 79: 361364 4. Deziel DJ, Millikan KW, Economou SG, Doolas A, Ko S-T, Airan MC (1993) Complications of laparoscopic cholecystectomy; a national survey of 4,292 hospitals and an analysis of 77,604 cases. Am J Surg 165: 914 5. Dubelman A (1994) Complications of laparoscopic surgery: surgical and anesthetic considerations. Semin Laparosc Surg 1: 219222 6. Flowers JL, Zucker KA, Bailey RW (1994) Complications. In: Ballantyne GH, Leahy PF, Modlin IM (eds) Laparoscopic surgery. Chapter 8, WB Saunders, Philadelphia, pp 7794 7. Grainger DA, Soderstrom RM, Schiff SF, Glickman MG, DeCherney AH, Diamond MP (1990) Ureteral injuries at laparoscopy; insight into diagnosis, management and prevention. Obstet Gynecol 75: 839843 8. Hasson HM (1974) Open laparoscopy: a report of 150 cases. J Reprod Med 12: 234238 9. Henning H (1985) The Dallas report in laparoscopic complications. Gastrointest Endosc 31: 104105 10. Ilter T, Bolukoglu MA, Musoglu A (1986) Complication rates of diagnostic laparoscopy. Gastrointest Endosc 32: 126 11. Kleppinger RK (1977) Laparoscopy at a community hospital: an analysis of 4300 cases. J Reprod Med 19: 353363 12. Krebs HB (1986) Intestinal injury in gynecologic surgery: a ten year experience. Am J Obstet Gynecol 155: 509514 13. Larson GM, Vitale GC, Casey J, Evans JS, Gilliam G, Heuser L, McGee G, Rao M, Scherm MJ, Voyles CR (1991) Multipractice analysis of laparoscopic cholecystectomy in 1,983 patients. Am J Surg 163: 221226 14. Loffler FD, Pent D (1975) Indications, contraindications, and complications of laparoscopy. Obstet Gynecol Surg 30: 407427 15. McDonald PT, Rich NM, Collins GJ, Andersen CA, Kozloff L (1978) Vascular trauma secondary to diagnostic and therapeutic procedures: laparoscopy. Am J Surg 135: 651655 16. The Southern Surgeons Club. (1991) A prospective analysis of 1518 laparoscopic cholecystectomies. N Engl J Med 324: 10731078 17. Minz M (1977) Risks and prophylaxis in laparoscopy: a survey of 100,000 cases. J Reprod Med 18: 269272 18. Nordestgaaard AG, Bodily KC, Osborne RW Jr, Buttorff JD (1995) Major vascular injuries during laparoscopic procedures. Am J Surg 169: 543545 19. Peterson HB, Hulka J, Phillips JM (1990) American Association of Gynecologic Laparoscopists 1988 membership survey on operative laparoscopy. J Reprod Med 35: 587589 20. Riedel HH, Lehmann-Willenbrock E, Conrad P, Semm K (1986) German pelviscopic statistics for the years 19781982. Endoscopy 18: 219222 21. Riedel HH, Willenbrock EL, Mecke H, Semm K (1989) The frequency distribution of various pelviscopic (laparoscopic) operations, including complications rates: statistics of the Federal Republic of Germany in the years 19831985. Zentralbl Gynakol 111: 7891 22. Yuzpe AA (1990) Pneumoperitoneum needle and trocar injuries in laparoscopy. A survey on possible contributing factors and prevention. J Reprod Med 35: 485490

Surg Endosc (1997) 11: 11941197

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Diagnostic ultrasound of acute colonic diverticulitis by surgical residents

A. Zielke,1 C. Hasse,1 Th. Bandorski,1 H. Sitter,2 P. Wachsmuth,1 R. Grobholz,1 M. Rothmund1
1

Department of General Surgery and 2Institute of Theoretical Surgery, Philipps-University of Marburg, Baldinger Strasse, P.O. Box 100, 35043 Marburg, Germany Received: 3 October 1996/Accepted: 9 May 1997

Abstract Background: Recent studies have documented the feasibility of ultrasonography (US) to diagnose acute colonic diverticulitis (ACD). This prospective observational trial determined the sonomorphology of ACD and evaluated the diagnostic accuracy of routine US performed on admission by surgeons in training. Methods: Fifty-seven consecutive patients with a confirmed episode of ACD were entered into this study, and the sonomorphology of the involved colon was assessed. US findings were compared to the results of the clinical evaluation and correlated to the clinicopathological outcome. Results: The sonomorphology of ACD was characterized by segmental inflammatory transformation of the colon averaging 9.9 3.2 cm (range, 620) in length and visualized as target phenomena of a mean 3.5 0.8 cm (range, 2.44.8) width. Targets were caused by hypoechogenic thickening of the colonic wall of an average 7.7 2.6 mm (range, 418). In 40% of cases, a hyperechogenic halo representing peridiverticulitis (average width, 2.3 0.6; range, 1.23 cm) was noted. Diverticula were seen in almost half of the cases. Of the 57 cases with confirmed ACD, the diagnosis was made by US in 48, for a global accuracy of 84.2%. US was false negative in nine patients, suggesting perforated appendicitis in five cases and acute appendicitis in one (the final diagnoses were perforated sigmoid diverticulitis in five cases and cecal diverticulitis in one case). In three patients, US was nondiagnostic. Conclusion: In the hands of sonographically trained surgeons, ultrasound is a useful modality to image acute colonic diverticulitis. US reveals diagnostic sonomorphology in most cases of ACD and therefore facilitates early confirmation of the diagnosis and assessment of severity. Key words: Ultrasound Acute colonic diverticulitis

Ultrasound (US) is a new method for imaging acute colonic diverticulitis (ACD) [10, 14, 16]. If performed by an expert sonographer, it can be very accurate in establishing the diagnosis [13]. However the diagnostic sonomorphology of ACD is not yet fully established. Moreover, it is unclear whether surgeons trained in US imaging can successfully utilize the method to diagnose ACD. We therefore studied the sonomorphology as well as the overall diagnostic accuracy of routine ultrasonography performed by surgeons in training in patients with confirmed episodes of ACD.

Patients and methods

Over a 4-year period, all patients admitted to the surgical clinic with a possible diagnosis of acute colonic diverticulitis underwent US evaluation and were entered into this study. Patients with generalized peritonitis requiring emergent surgery were excluded. Only those patients in whom the diagnosis of ACD was proven by either surgery or at least one established diagnostic modality other than US were accepted for analysis. Ultrasound was performed on admission, after the physical examination. Eleven surgeons in training (2nd- to 6th-year residents) were involved in this study; all of them had received standardized training in abdominal ultrasound, as described in detail elsewhere [6]. Training included an average of 400 supervised investigations of the abdomen, as well as an introduction to the method of graded compression [6]. Graded compression refers to a technique of handling the ultrasound probe in a way closely resembling that of a surgeons palpating hands during physical examination: Gentle compression graded by the patients tolerance for pain is applied with the probe, which is then slowly moved. Compression of the abdominal wall reduces the distance between the transducer and bowel, displaces gas and intraluminal residue, interposing bowel or mesentery and eliminates (or at least reduces) interfaces. Graded compression was also used in the area of greatest abdominal tenderness. The US investigator was chosen arbitrarily and had supplied with the details of the clinical indications for the study. For the purpose of this study, individual investigators were asked to deliver a definite diagnosis. Sonograms were interpreted immediately at the time of the procedure, and there was no supervision until a definite ultrasonographic diagnosis was established. Patients were scanned using commercially available electronic realtime scanners (3.5- and 5.0-MHz transducers; Siemens SL100, Erlangen, Germany). Visualization of a hypoperistaltic segment with hypoechogenic mural thickening, presenting as a poorly compressible target in transverse view, was considered diagnostic of acute diverticulitis and thus recorded as

Offprint requests to: C. Hasse Correspondence to: A. Zielke

1195

Fig. 1. Transverse section in the left lower quadrant exemplifying postinflammatory sigmoid diverticulosis. Note the target pattern of the sigmoid colon, revealing marked hypoechogenicity of the wall. Five concentric layers of the bowel wall can be readily identified: The innermost bright layer is produced by residue and air present within the lumen of the colon (1); the next layer is representative of the mucosa (2); the next bright layer represents an interface between mucosa and muscularis (3); the hypoechogenic outer layer represents the muscularis (4); the next bright layer [(5) appreciated between 6 and 9 h] is yet another interface between muscularis and serosa. To the right of the target pattern, at 5 h, a small grape-like structure with a central hyperechogenic reflection and faint dorsal acoustic shadowing represents a noninflamed diverticulum.

Fig. 2. Transverse section in the left lower quadrant in a case of uncomplicated acute sigmoid diverticulitis. Acute diverticulitis is characterized by an asymmetric inflammatory target pattern of the sigmoid colon (T) caused by hypoechogenic thickening of the wall, narrowing of the lumen, and decreased peristalsis in dynamic view. To the right of the target, at 3 h, a tubular structure with a bright apical reflection represents an inflamed diverticulum (D). It is surrounded by a hyperechogenic mass of homogenous sonolucency, which is caused by inflammatory edema of the pericolic fat and indicates peridiverticulitis (hyperechogenic halo, H).

a positive finding. Nonvisualization of such a segment was regarded as a negative result. The largest diameter of the segment, its length, and mural thickness were measured by calipers. Diverticula, peridiverticulitis, and other signs of diverticulitis were recorded. To assess the clinical utility of US in ACD, patients were allocated into one of the following three clinical categories after the physical examination: group A, highly likely for diverticulitis; group B, equivocal diagnosis of acute diverticulitis pending further investigation; group C, highly unlikely for diverticulitis. This allowed for a grading of the clinical suspicion of ACD. US results were compared to those obtained during the clinical evaluation and correlated to the discharge diagnoses of the respective patients.

Results We evaluated 57 patients with a confirmed episode of ACD. This group was comprised of 31 female patients with a mean age of 64.9 years (range, 3589) and 26 male patients with a mean age of (2181) 55.6 years (m/f ratio, 1:1.2). The sigmoid colon was the most common site of acute diverticulitis (47/57; 82.4%). Involvement of the descendent colon and left colonic flexure was found in eight cases

(14.1%). The cecum and ascending colon accounted for two cases (3.5%). The final diagnosis of ACD was confirmed by radio-opaque enemas in 29 patients (50.8%), surgery in 21 patients (36.9%), colonoscopy in six patients (10.5%), and computed tomography in one patient (1.8%), respectively. Overall, 28 patients underwent operative interventions during the same hospital stay; ACD was confirmed in all cases. During US evaluation ACD was characterized by hypoechogenic thickening of the wall of an average 7.7 2.6 mm (range, 418) accompanied by luminal narrowing and hypoperistalsis of the involved colonic segment during dynamic view. This region was usually appreciable as a poorly compressible segmental target pattern in transverse view and a rigid tubular structure displaying multiple hypoechogenic strata in longitudinal view. The average width and length of the inflamed segments were 3.5 0.8 cm (range, 2.44.8) and 9.9 3.2 cm (range, 620). In 19 of 48 (39.6%) cases of ACD with a true positive US investigation, a hyperechogenic halo of an average width of 2.3 0.56 cm (range, 1.23) was noted (Figs. 14). Diverticula were seen with a frequency of 47.9%. Abscesses were present in 11 patients and visualized by US in nine; they ranged from

1196

Fig. 3. Transverse section in the left lower quadrant in a case of complicated sigmoid diverticulitis. Note the target pattern of the sigmoid colon with asymmetric hypoechogenic thickening of the wall (T). A small irregular hypoechogenic target with a central air reflection, visualized at 5 h represents an inflamed diverticulum (D). It is surrounded by a hypoechogenic halo (shaded area). A well-confined abscess of 2 1 cm can be seen to the right of the diverticulum (A).

2 4 to 12 3 cm (Fig. 3). Enterovesicular fistulas were apparent in two patients; neither was detected by US. One enterocutaneous fistula was correctly diagnosed by US (Table 1). US made the diagnosis of ACD in 48 of the 57 cases with proven diverticulitis, for an accuracy of 84.2%. False negative results of US were recorded in nine cases (15.8%). The false diagnosis of complicated acute appendicitis was made in five patients; in these cases, the inflamed sigmoid colon was found displaced to the right lower abdominal quadrant. All of these patients underwent surgery for signs of localized peritonitis. Four patients received two-stage sigmoid colectomies and appendectomy for perforated sigmoid diverticulitis, and one patient underwent one-stage sigmoid colectomy without appendectomy. Another case concerned a patient with an inflamed solitary cecal diverticulum and confined local peritonitis, which was also misdiagnosed as acute appendicitis. This patient underwent appendectomy and local resection of the cecal diverticulum. The remaining three cases involved a group of clinically mildly affected patients; in these cases, diagnosis of uncomplicated ACD was made by water-soluble contrast enemas in two patients and CT scanning in one patient, respectively. Based on the results of the clinical evaluation on admission, the immediate clinical diagnosis of an ACD was made

Fig. 4. Transverse section in the left lower quadrant in a case of perforated sigmoid diverticulitis with advanced local peritonitis. Note the faintly visible, poorly defined hypoechogenic target pattern of the sigmoid colon (T), which is surrounded by a noncompressible zone of increased echogenicity. The inflammatory pseudo-tumor has attained a diameter of 7.5 cm and shows evidence of the spread of inflammation to pericolic fat and mesentery. Close to the abdominal wall, the halo is divided by multiple hypoechogenic strata, representing fluid collections between the different layers of edematous epiploic appendices, mesenteric, and pericolic fat (onion-skin appearance).

in 29 of 57 patients, for a diagnostic accuracy of 50.8%. Of the six patients who appeared clinically very unlikely for ACD, five cases were misdiagnosed as acute appendicitis and one case as nonspecific acute abdominal pain. All other patients were classified as clinically equivocal cases, including five patients who eventually required emergency surgery for complicated ACD. Overall, of the 28 patients who underwent surgery for ACD, the indication for a laparotomy was clinically evident in 12 cases, including the five patients who were misdiagnosed as acute appendicitis. US identified all cases that subsequently underwent operative therapy although, as already pointed out, six cases were misinterpreted as acute appendicitis. While US and CT were always performed at the day of admission, colonoscopies were performed after a median 3.5 days (mean, 7.7 3.5; range, 028), and water-soluble contrast enemas were done at a median 6 days (mean, 6.7 5.4; range, 228) after admission. Discussion Ultrasound (US) is increasingly used by surgeons in the initial evaluation of the patient with acute abdominal pain

1197 Table 1. Sonomorphology of acute colonic diverticulitis Finding Wall thickness Target width Segment length Hyperechogenic halo Average (mm) 7.7 2.6 35 8 99 32 23 5.6 Range (mm) 418 2448 60200 1230

[2, 6, 11]. This study establishes that surgeons trained in ultrasound imaging can effectively use this method to diagnose acute colonic diverticulitis (ACD). Computed tomography constitutes the current gold standard imaging modality in complicated diverticulitis [1, 9]. Like CT, US imaging allows the physician to define the extent of extramucosal inflammation and identify sequelae of ACD, such as perforation and abscess, without intraluminal procedures or contrast extravasation. The colon was relatively easy to access by US because of its close proximity to the abdominal wall and its size. The inflamed segments usually attained a considerable size; they averaged 3.5 9.9 cm in this study. The diagnostic sonomorphology of ACD established during this study was similar to that reported by other authors [13, 14, 16]. Besides some rather unspecific criteria of inflammatory bowel disease, such as thickening of the colonic wall to 418 mm, lack of compressibility, and hypoor aperistalsis, we observed a number of more specific signs, such as diverticula (50%), local abscesses (20%), and fluid collections or fistulas (5%). Inflamed diverticula ordinarily were visualized as grape-like hypoechogenic structures, surrounded by an often double contoured wall. They frequently displayed bright acoustic reflexes caused by trapped air and feces. With extensive disease, hyperechogenic halos surrounding the involved colonic segment were noted; in addition, there was a lack of synchronous movement with breathing. This finding, which was considered an ultrasonographic sign of peridiverticulitis, was noted in some 40% of patients. Although no single sonographic criterion was considered diagnostic, it was evident from this study that visualization of an inflammatory target sign in the left lower quadrant, together with hyperechogenic halo and diverticula, is highly suggestive of ACD in a symptomatic patient. Consequently, the 84% accuracy of this study for the sonographic diagnosis is quite comparable to the results from three other prospective trials published by recognized experts in the field of ultrasonography, who reported an overall accuracy of 8298%, sensitivity of 8498%, and a specificity of 8096% [4, 12, 15]. One potential pitfall, however, is the clinical presentation of right-sided colonic diverticulitis, which is either caused by a solitary cecal diverticulum or a displaced sigmoid colon. Both conditions may be impossible to distinguish from acute appendicitis. This presentation accounted for five false clinical diagnoses and six false US results. Previous studies did not comment on this particular difficulty; therefore, this problem may have been a reflection of

lack of experience [6, 9]. CT may be a better alternative in these circumstances. Not unexpectedly, the accuracy for the clinical diagnosis of ACD was low, but this problem is well documented in the literature [10, 16]. The clinical diagnosis is rarely more accurate than 75% [3, 5]. However, assessing the site and severity of the disease is important, particularly in complicated diverticulitis, since the outcome largely depends on a timely diagnosis [7, 8]. The routine use of CT is hampered by its own restrictionsmainly limited availability and high cost [1, 9]. Use of colonoscopy and radio-opaque enema is also limited, due to the increased frequency of complications in ACD. Therefore, they cannot always be employed immediately; the resulting diagnostic time lag of several days was also found in the present study. Based on the results of this study, it appears that US imaging is a fast, feasible, and effective diagnostic modality for patients in whom ACD is suspected. US imaging facilitates early confirmation of ACD and permits rational management decisions to be made. Whether or not US will alter the surgical management of these patients remains to be seen. References
1. Ambrosetti P, Robert J, Witzig JA, Mirescu D, deGautard R, Borst F, Rohner A (1992) Incidence, outcome and proposed management of isolated abscesses complicating acute left sided colonic diverticulitis: a prospective study of 140 patients. Dis Col Rec 35: 10721076 2. Davies AH, Mastoraku I, Cobb R, Rogers C, Lindsell D, Mc. Mortensen NJ (1991) Ultrasonography in the acute abdomen. Br J Surg 78: 11781180 3. Dawson JL, Harrow I, Roxburgh RA (1965) Diverticulosis coli complicated by diffuse peritonitis. Br J Surg 52: 354357 4. Federmann G (1989) Sonographie in der Diagnostik der akuten Kolondivertikulitis. Chirurg 60: 415416 5. Hiltunen KM, Kolehmainen H, Vuorinen T, Matikainen M (1991) Early water-soluble contrast enema in the diagnosis of acute colonic diverticulitis. Int J Colorecal Dis 6: 190192 6. Klotter HJ, Zielke A, Niess C, Sitter H, Rothmund M (1992) Sonographie beim akuten abdominellen Notfall. Chirurg 63: 597605 7. Kronborg O (1993) Treatment of perforated sigmoid diverticulitis: a prospective randomized trial. Br J Surg 80: 505507 8. Krukowski ZH, Matheson NA (1984) Emergency surgery for diverticular disease complicated by generalized and fecal peritonitis: a review. Brit J Surg 71: 921927 9. McKee RF, Deignan RW, Krukowski ZH (1993) Radiological investigation in acute diverticulitis. Brit J Surg 80: 560565 10. Parulekar SG (1985) Sonography of colonic diverticulitis. J Ultrasound Med 4: 659666 11. Paterson-Brown S, Vipond MN (1990) Modern aids to clinical decision-making in the acute abdomen. Br J Surg 77: 1318 12. Puylaert JBCM, Rutgers PH, Lalisang RI, deVries BC, van der Werft SDJ, Do rr JPJ, Block RAPR (1987) A prospective study of ultrasonography in the diagnosis of appendicitis. N Engl J Med 317: 666669 13. Schwerk WB, Schwarz S, Rothmund M (1992) Sonography in acute colonic diverticulitis: a prospective study. Dis Col Rectum 35: 1077 1084 14. Townsend RR, Jeffrey RB, Laing FG (1989) Cecal diverticulitis differentiated from appendicitis using graded compression sonography. AJR 152: 12291230 15. Verbanck J, Lambrecht S, Rutgeers L, Ghillebert G, Buyse T, Naesens M, Tytgat H (1989) Can sonography diagnose acute colonic diverticulitis in patients with acute intestinal inflammation? A prospective study. J Clin Ultrasound 17: 661666 16. Wilson SR, Toi A (1989) The value of sonography in the diagnosis of acute diverticulitis of the colon. AJR 154: 11991202

Case reports
Surg Endosc (1997) 11: 12091212

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Laparoscopically assisted abdominoperineal resection and simultaneous total anorectal reconstruction with electrostimulated static-dynamic graciloplasty
E. Cavina, M. Seccia, M. Chiarugi, P. Banti, G. Zocco
Emergency Surgery Unit, Department of Surgery, Ospedale Santa Chiara, Via Roma 67, 56100 Pisa, Italy Received: 1 July 1996/Accepted: 19 November 1996

Abstract. Bilateral electrostimulated graciloplasty, performed in a static-dynamic configuration around a perineal colostomy (total anorectal reconstructionTAR), has been proven a reliable way to restore continence in patients who undergo to abdomino perineal resection (A.Pe.R.) of the anorectum for lower rectal cancer. In selected cases, laparoscopically assisted TAR can significantly improve body-image preservation and aesthetic results. A 33-yearold woman affected by lower rectal cancer was submitted to laparoscopic-assisted A.Pe.R and TAR with simultaneous bilateral graciloplasty; a suprapubic median mini-access was adopted to fully mobilize the mesorectum in absence of pneumoperitoneum. A subcutaneous pulse generator and special electrodes were also implanted to chronically electrostimulate the graciloplasty. In spite of postoperative bleeding which required a blood transfusion, postoperative outcome was satisfactory; electrostimulation was started on the 10th postoperative (p.o.) day and the patient was discharged on the 17th p.o. day. Two months after TAR, level II continence (N.S. Williams Scale) was achieved. In selected cases, laparoscopically assisted A.Pe.R. and TAR can be safely adopted to preserve body image and quality of life, avoiding at the same time a large abdominal approach and a permanent abdominal colostomy. Key words: Rectal cancer Graciloplasty Laparoscopy Sphincter reconstruction Electrostimulation Neosphincter

Total Anorectal Reconstruction (TAR) was adopted in a young woman affected by lower rectal cancer with the aim of avoiding both a large abdominal approach and a perma-

Correspondence to: E. Cavina

nent abdominal colostomy; technique and a preliminary follow-up study are presented. Recent literature reviews on laparoscopic vs open colon surgery state that the laparoscopy has become an acceptable alternative for the treatment of a variety of colorectal disorders and at the same time that in conclusion, these were no statistically significant differences in costs or outcome between laparoscopic and open colorectal procedures [24]. As far as oncological safety of laparoscopic surgery is concerned, potential hazards of tumor recurrences at laparoscopic port sites are highlighted by many recent reports, even though the effectiveness and statistical significance of this phenomenon are controversial [1, 5, 8, 10, 1315, 22, 25, 34]. In spite of that, the total number of colorectal laparoscopic or laparo-assisted procedures is growing and thousands of cases are collected in international registers [3, 4, 9, 11, 12, 16, 17, 20, 21, 23, 26, 28, 30, 33, 35, 36]. As of March 1996, the Italian national register Societa ` Italiana di Chirurgia Endoscopica (S.I.C.E.) reported 664 VLCs; 28.7% (190 VLCs) were carried out for rectal cancer and 8% (53 VLCs) consisted in A.Pe.R. Presumably, in the near future, more detailed guidelines allowing performance of better laparoscopic or laparoassisted colorectal surgery will be available; standardized protocols for patient enrollment, oncological risk evaluation, and an effective comparison vs open surgery (costs, aesthetic results, quality of life, postoperative discomfort, complication rates, etc.) will also be better defined. Keeping these prospects in mind, our initial enthusiasm in performing colorectal laparoscopic surgery has been reduced, and this approach is now submitted to a prudent and strict selection, with the exclusion of all cases presenting high risk of tumor recurrence, in particular at port sites. Concerning the aesthetic aspects, it has recently been affirmed that in the young patients the improved cosmetic results after laparoscopic surgery may play a significant role [36].

1210

Since 1991 to date, our laparoscopy experience has mainly been based on biliary tract diseases (1,113 cases). Colorectal laparoscopy surgery was limited to 31 cases, the majority of which were treated for right colonic cancer; in all these cases, lymphoadenectomy was carried out in the absence of pneumoperitoneum. The management of the reported case was inspired by the contemporary necessity of a correct oncologic approach and the restoration of sphincteric function, giving to a 33year-old woman the possibility of a good quality of life together with aesthetic benefits. Continence restoration was based on the same technique of TAR performed during a 10-year experience in which 99 electrostimulated graciloplasties were wrapped around a perineal colostomy in static-dynamic fashion. During this experience, good continence rates ranged from 70 to 87% depending on stimulation protocols and devices (short-term/chronic stimulation), and no significant differences were observed in early and 5-year mortality rates between this technique and A.Pe.R. [7]. Materials and methods
In February 1996, a 33-year-old woman was admitted to our unit for surgical treatment of a lower rectal adenocarcinoma. Previous outpatient studies (endoscopy, endorectal sonography, pelvic CAT scan) demonstrated the presence of a 2 4 cm tumor involving the posterior wall of the rectum, 1 cm above the anal verge. No extramural spreading or metastases were observed with either CAT or US evaluation. Combined chemo- and radiotherapy (fluorouracil [5FU]45 Gy) was then carried out by the Oncology Unit of our institution, obtaining a tumor size reduction of 50%. Preoperative staging was T2N0M0, confirmed by specimen examination (T0N0MxGrading 2/4, B1 Astler-Coller system stage).

Fig. 1. Postoperative view of the abdomen.

Right gracilis wrap configured in a clockwise , simulating the anal sphincter Both muscle bellies sutured to landmarks previously placed on the levators-ani insertions Gracilis tendons fixed to subcutaneous fascia, to avoid excessive tension around the perineal colostomy

Electrostimulation
Electrostimulation device implant was carried out as the final step of the procedure once all incisions were sutured, muscle relaxant administration was suspended, and gentamicin was locally flushed. Platinum-iridium electrodes (model 4300 Implantable Unipolar Leads; Medtronic Interstim, Kerkrade, The Netherlands) were placed on each muscle, following a combined technique of over-the-nerve and intramuscular implant. After the main nerve identification, carefully avoiding any direct damage, the proximal part (1.5 cm) of each exposed electrode was fixed to the perineural, while the remaining part (2.5 cm) was inserted into the muscle perpendicular to its longitudinal axis. Both electrodes were connected to a quadripolar Implantable Pulse Generator (Itrel II IPG, model, 7424; Medtronic Interstim, Kerkrade, The Netherlands) placed in a subcutaneous abdominal pocket; basal stimulation parameters were then recorded and incisions were sutured. Intraoperative full contraction was obtained at 0.8 V amplitude and 315 impedance, recorded 90 minutes after the last muscle-relaxant administration.

Technique
After bowel preparation (iso-osmotic laxative solution) and antibiotic prophylaxis (cephalosporin), the patient was submitted to VL approach through four ports placed as shown in Fig. 1; intraoperative US evaluation (laparoscopic ultrasound probe 6.57.5 MHzEsaote Biomedica, Genova, Italy) excluded liver, pre-aortic, and pelvic involvement, confirming the existence of gallbladder microlithiasis. After inferior mesenteric vein section, transverse colon, splenic flexure, descending colon, and sigma were fully mobilized and the inferior mesenteric artery (IMA) resected at its origin. Pre-aortic lymphoadenectomy was then extended from above this point down to the presacral space; laparoscopic cholecystectomy was also carried out [18, 19, 29, 32, 38]. Through a median suprapubic mini-access (9 cm in length), open surgery was then started, pursuing the following steps: A preliminary, accurate examination of the mobilized colon to evaluate the adequacy of its vascular supply and length in order to lower it to the perineal floor Proximal colonic stump section and blunt mobilization of the rectum Dissection of the mesorectum, rectum, and lateral pedicles from the lower pelvic floor and the vagina The subsequent perineal resection was then accomplished according to the classic Miles procedure and suture landmarks were placed on the levators-ani insertions to allow the neosphincter anchoring. The colon was then lowered to the perineal floor where it was left closed with a Foley catheter inserted into the lumen; no diversionary procedures were applied. According to our previously described static-dynamic draft, bilateral graciloplasty was carried out as follows [7]: Full mobilization of both muscles through three segmental incisions Left gracilis wrapped behind the perineal colonic stump, reproducing the puborectalis sling function (Fig. 2)

Results Postoperative course was complicated by consistent bleeding which probably originated from colonic dissection surfaces; after clinical and ultrasound monitoring the complication was conservatively treated. Nevertheless, a transfusion of two blood units was needed [6, 27]. In spite of that, the succeeding postoperative (p.o.) course was uneventful. Colonic stump was resected on the 3rd p.o. day and a colocutaneous suture was carried out under local anesthesia on the 5th p.o. day. Hospital length of stay was 17 days. Electrostimulation was started on the 10th p.o. day for 6 h and progressively increased to 24 h; stimulation parameters were then assessed to allow an acceptable continence even during the first training period of cyclic (on/off) stimulation. According to previous studies [2, 31, 37], a chronic stimulation protocol was then carried out with the following parameters: amplitude: 1.8 V, frequency: 25 pps, on/off ratio: 0.1/1.2 s. Four weeks after starting electrostimulation,

1211

Fig. 2. Static-dynamic graciloplasty model: both gracilis muscles are wrapped around the perineal colostomy (C). The deeper wrap mimics the puborectalis sling function, passing behind the colonic stump (B), while the second wrap (A), circularly surrounds the colon.

no deviation from the protocol is noted and patient continence is classified as II of the Williams modified Scale. The electromanometry (EMM) study performed in IPG-ON mode shows MRP and MVP values of 60 mmHg and 80 mmHg, respectively; dynamic vector volumetry confirms homogeneous pressure areas corresponding to the transposed muscles.

References
1. Alexander EJT, Jaques BC, Mitchell KG (1993) Laparoscopically assisted colectomy and wound recurrence (letter). Lancet 341: 249250 2. Baeten CGMI, Konsten J, Spaans F, Visser R, Bourgeois AMMC, Wagenmakers AJM, Soeters PB (1994) Dynamic graciloplasty for treatment of faecal incontinence. Lancet 338: 9: 11631165 3. Beart R (1994) Laparoscopic colectomy: status of the art. Dis Colon rectum 37 (Suppl): S47S49 4. Benitez LD, Plasencia G, Viamonte M, Jacobs M, Edelman DS (1996) Laparoscopic assisted colectomy: a retrospective review. Surg Endosc 10: 223 (Abstract) 5. Bouvy ND, Marquet RL, Jeekel H, Bonjer J (1996) Gasless laparoscopy versus CO2 pneumoperitoneum in relation to the development of abdominal wall metastases. Surg Endosc 10: 210 (S154) 6. Breton G, Pomp A, Gagner M (1996) Complications related to laparoscopic surgery for intestinal obstruction. Surg Endosc 10: 211 (S155) 7. Cavina E (1996) Outcome of restorative perineal graciloplasty with simultaneous excision of the anus and rectum for cancer. Dis Colon Rectum 39 (2): 19 8. Cirocco WC, Schwartzman A, Golub RW (1994) Abdominal wall recurrence after laparoscopic colectomy for colon cancer. Surg 116: 842846 9. Fielding G, Stitz R, Nathanson L, Lumley J, Rhodes M (1996) Laparoscopic assisted colorectal surgery. Surg Endosc 10: 211 (S158) 10. Fielding G, Stitz R, Nathanson L, Lumley J, Rhodes M, Bailey I (1996) Laparoscopic assisted colectomy for malignant disease. Surg Endosc 10: 231 (Abstract) 11. Fowler DL, White SA, Anderson CA (1995) Laparoscopic colon resection: 60 cases. Surg Laparosc Endosc 5: 468471 12. Franklin ME, Ramos R, Rosenthal D, Schuessler W (1993) Laparoscopic colonic procedures. World J Surg 17: 5156 13. Fusco MA, Paluzzi MW (1993) Abdominal wall recurrence after laparoscopic assisted colectomy for adenocarcinoma of the colon. Dis Colon Rectum 36: 858861 14. Jacquet P, Sugarbaker P (1996) Wound recurrence after laparoscopic colectomy for cancer: new rationale for intraoperative intraperitoneal chemotherapy. Surg Endosc 10: 295296 15. Jawad MZA (1996) Abdominal wall recurrence after laparoscopically assisted colon resection for malignant tumors. Surg Endosc 10: 237 (Abstract) 16. Kim HC, Geis WP (1996) Laparoscopic assisted colon surgery by a single surgeon: techniques and results. Surg Endosc 10: 240 (Abstract) 17. Lacy Am, Garc `a-Valdecasas JC, Pique JM, Delgado S, Campo E, Bordas JM, Taura ` P, Grande L, Fuster J, Pacheco JL, Visa J (1995)

Discussion We believe that in the described case, as in future VLassisted procedures, a correct preoperative staging and a laparoscopic intraoperative US are mandatory to evaluate risks of recurrence and the feasibility of a laparoscopic procedure. Surgical maneuvers carried out in the upper peritoneal cavity preliminary to the pelvic dissection were acceptable from the oncological point of view and very useful for the subsequent open mini-access. The open mini-access allowed full pelvic control, reduced operation length, and permitted at the same time an approach to the mesorectum in the absence of pneumoperitoneum which decreased oncologic risks of contamination. The aesthetic aspect was particularly relevant in the reported case, due to the fact that open surgery would otherwise have led to a large median laparotomy and to a permanent abdominal stoma, with consequent severe impairment in quality of life and body-image; from this point of view, the final result was excellent (Fig. 1). Short-term (4 weeks) functional results anticipate a future continence in the best range of our previous results: at the moment colonic voiding is regular; a mini-enema is needed on alternate days; continence is reasonably acceptable (occasional leakage), and the patient uses a minipad per day for security. On the basis of this experience we can conclude that a laparoscopically assisted A.Pe.R with a simultaneous TAR is an appropriate and a safe continence-restoring procedure in selected cases.

1212 Short-term outcome analysis of a randomized study comparing laparoscopic vs open colectomy for colon cancer. Surg Endosc 9: 1101 1105 Larach SW, Salomon MC, Williamson PR, Goldstein E (1993) Laparoscopic assisted abdominoperineal resection. Surg Laparosc Endosc 3: 115118 Milsom JW, Marchesa P, Fazio VW (1996) Retroperitoneal mesenteric dissection in laparoscopic oncologic colorectal surgery. Surg Endosc 10: 210 (S153) Monson JRT, Darzi A, Declan Carcy P, Guillou PJ (1992) Prospective evaluation of laparoscopic-assisted colectomy in an unselected group of patients. Lancet 340: 831833 Monsons JRT, Hill ADK, Darzi A (1995) Laparoscopic colonic surgery. Br J Surg 82: 150157 Nduka CC, Monson JRT, Menzies-Gow N, Darzi A (1994) Abdominal wall metastases following laparoscopy. Br J Surg 81: 648652 Ota DM (1995) Laparoscopic colon resection for cancer. Surg Endosc 9: 13181322 Pfeifer J, Wexner SD, Reissman P, Bernstein M, Noguera JJ, Singh S, Weiss E (1995) Laparoscopic vs open colon surgery. Surg Endosc 9: 13221326 Ramos JM, Gupta S, Anthone GJ, Ortega AE, Simons AJ, Beart RW (1994). Laparoscopy and colon cancer. Is the port site at risk? A preliminary report. Arch Surg 129: 897899 Ramos JM, Beart RW Jr, Goes R, Ortega AE, Schlinkert RT (1995) Role of laparoscopy in colorectal surgery. Dis Colon Rectum 38: 494 501 Reissman P, Wexner SD, Cohen SM, Nogueras JJ, Jagelman DG (1994) Complications of laparoscopic colorectal surgery. Surg Endosc 8: 562 (Abstract) Rouffet F, May JM, Vacher B, Fingerhut A, Elhadad A, Flamant Y, Mathon C, Gainant A (1994) Curative resection for left colonic carcinoma: hemicolectomy vs segmental colectomy. Dis Colon Rectum 37: 651659 Schoucair A, Brouch H, Herold A (1994) Laparoscopic abdominoperineal rectum resection. Surg Endosc (Abstr 4th World Congr Endosc Surg Kyoto 1619 June 1994) 8: 508 Scoggin SD, Frazee RC, Snyder SK, Hendricks JC, Roberts JW, Symmonds RE, Smith RW (1993) Laparoscopic-assisted bowel surgery. Dis Colon Rectum 36: 747750 Seccia M, Menconi C, Balestri R, Cavina E (1994) Study protocols and functional results in 86 electrostimulated graciloplasties. Dis Colon Rectum 37 (9): 897904 Tanaka J, Ito M, Shindo Y, Kotanagi H, Koyama K (1996) Laparoscopically assisted resection of the lower rectum. Surg Endosc 10: 338340 Van Ye TM, Cattey RP, Lyle GR (1994) Laparoscopically assisted colon resection compares favorably with open technique. Surg Laparosc Endosc 4: 2531 Walsh D, Wattchow D, Wilson T (1993) Subcutaneous metastases after laparoscopic resection of malignancy. Aust N Z J Surg 63: 563 565 Wexner SD, Cohen SM, Johansen OB, Noguers JJ, Jagelman DG (1993) Laparoscopic colorectal surgery: a prospective assessment and current perspective. Br J Surg 80: 16021605 Wexner SD, Reismna P, Pfeifer J, Bernstein M, Geron N (1996) Laparoscopic colorectal surgery: analysis of 140 cases. Surg Endosc 10: 133136 Williams NS, Patel J, George BD, Hallan RI, Watkins ES (1991) Development of an electrically stimulated neoanal sphincter. Lancet 338 (9): 11661169 Wu JS, Fleshman JW (1996) Early experience with laparoscopic abdominal perineal resection. Surg Endosc 10: 267 (Abstract)

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Surg Endosc (1997) 11: 11471149

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Is outpatient cholecystectomy safe for the higher-risk elective patient?

A. J. Voitk
Department of Surgery, Suite 1840, The Salvation Army Scarborough Grace Hospital, 3030 Birchmount Avenue, Scarborough, Ontario, Canada M1W 3W3 Received: 26 December 1996/Accepted: 2 April 1997

Abstract Background: This study was done to determine the safety of outpatient cholecystectomy for the higher-risk patient. Methods: All patients over age 70 or with American Society of Anesthesiologists physical status classification of 3 or greater, from all 515 consecutive patients booked for elective cholecystectomy between April 1, 1994, and March 31, 1996, were reviewed. Results: Of 85 higher-risk patients, 77 were booked as outpatients. Sixty-one were successfully completed as outpatients, with no complications or readmissions related to their outpatient status. Of 24 admitted patients, 15 had specific indications for hospitalization. Nine were admitted for reasons of precaution. One of these developed a complication, possibly related to her inpatient status. The other eight could have been managed as outpatients. Conclusions: Outpatient cholecystectomy is safe for the higher-risk patient. Patients who recover uneventfully from surgery can be discharged without harmful effects. Precautionary hospitalization may be harmful. Key words: Laparoscopic cholecystectomy High-risk patient Ambulatory surgery Safety

Methods and patients

The Salvation Army Scarborough Grace Hospital is a 256-bed acute-care nonteaching hospital served by four general surgeons and located on the outskirts of a major urban center. All patients booked for elective cholecystectomy by all four surgeons between April 1, 1994, and March 31, 1996, inclusive, were identified. Patients above age 70 or with an American Society of Anesthesiologists physical status classification of 3 (ASA 3) or higher were selected and the fate of those successfully treated as outpatients was reviewed in detail. All operations were done under general inhalation anesthesia. The operative technique and perioperative management have been described [11]. All patients were telephoned by a Day Surgery nurse the day after surgery and all were seen by the operating surgeon within 15 days of operation. For the purposes of this study, outpatient was defined as discharge on the day of surgery; overnight stay was considered admission to hospital, even if total stay was under 24 h. Probability was determined by the 2 test and significance assumed at the p < 0.05 level.

Results In the years under study 515 elective cholecystectomies were done, of which 85 were done on higher-risk patients. Age was a risk factor for 57 patients and comorbidity for 46; 18 patients had both risk factors. Cardiovascular disease was the sole or most significant contributor to ASA classification for 78% of the higher-risk patients. The incidence of acute cholecystitis, conversion, admission, readmission, or complication was not significantly different between these subsets. Average door-to-door time for outpatients was 6 h. The 28% admission rate of the higher-risk patients was significantly higher than the 12% admission rate of the

Outpatient cholecystectomy has been the standard of practice at the Salvation Army Scarborough Grace Hospital since 1994. Although it has been demonstrated repeatedly that neither old age nor comorbidity precludes safe outpatient surgery [2, 3, 68, 1113], some clinicians remain skeptical about the prudence of such practice for higher-risk patients [9]. Both age [1, 3, 14] and physical status [4, 5, 10] have been shown to be reliable predictors of surgical risk. To determine the safety of elective outpatient cholecystectomy for higher-risk patients, this paper examines the fate of all higher-risk patients at the Salvation Army Scarborough Grace Hospital during 2 years of routine outpatient cholecystectomy.

Table 1. Clinical characteristics of higher and lower-risk populations expressed as percent n Higher risk Lower risk p 85 430 n/a Male 34 21 p > 0.05 Acute chole 14 7 p > 0.05 Converted 6 3 p > 0.05 Admitted 28 12 p < 0.05

1148 Table 2. Clinical characteristics of higher-risk outpatients and higher-risk inpatients (expressed as percent) n Outpatients Admitted p 61 24 n/a >70 69 63 >0.05 ASA > 3 52 58 >0.05 >70 & ASA >3 20 25 >0.05 Male 41 17 >0.05 Acute chole 16 8 >0.05 Minor complications 26 17 >0.05 Conversions 0 21 <0.05 Readmissions 3 4 >0.05

lower-risk patients. The higher- and lower-risk populations are compared in Table 1. Of the 85 higher-risk patients, 77 were booked for outpatient cholecystectomy, which was successfully accomplished for 61. These 61 higher-risk outpatients encountered no problems related to outpatient status; 26% had minor complications and two readmissions (one patient came with abdominal pain 3 weeks later, was admitted, and had an ERCP; the other patient returned with a fractured hip 4 months postoperatively). The 24 admitted patients had a 17% minor complication rate and one readmission 3 weeks postoperatively for percutaneous drainage of a subphrenic abscess. Complication rates and readmission rates did not differ significantly between higher-risk outpatients and higher-risk admitted patients. Table 2 compares these groups: Both are essentially similar, except for a greater number of conversions in the admitted group. Sixteen patients, booked as outpatients, were admitted during the perioperative period. A specific reason for hospitalization became apparent for 12 patients: five were converted to open surgery, three needed intravenous antibiotics, and one each because of hypoxia, profound vomiting and social reasons. Four patients were admitted for precautionary reasons; none of these required any active intervention in hospital, all were discharged the next morning, and none had any readmissions or complications. A decision to admit had been made during the preoperative evaluation in the office for eight higher-risk patients. For three a specific indication for hospitalization was documented: unstable heart failure, anticipated further surgery, and social reason. Reason to admit was precautionary for the other five. One of these five developed pulmonary congestion a few hours after surgery, needing intravenous diuresis; she was discharged well the next morning. The other four did not need any active intervention in the hospital, were discharged the next morning, and had no readmissions or complications. Average length of stay was 2.7 days for patients admitted for specific indications and 1.1 days for those admitted for precautionary reasons (p < 0.05).

Discussion The complication rate for these 515 patients was refreshingly low, possibly because all operations were done by surgeons with extensive laparoscopic experience. The aim of this study was not to compare the overall results of these four surgeons to those of any other group but rather to assess the safety of routine outpatient surgery for the higherrisk patient. Both the increased conversion rate and hospital admission rate show that higher-risk outpatients did indeed have more complications than their lower-risk counterparts. However, the results clearly show that routinely booking

higher-risk patients as outpatients is safe. Although they have a higher complication rate, complications needing hospital admission become readily apparent during the 6-h period of observation accorded to outpatients. Patients who remain stable can be discharged without fear of delayed instability which might have been prevented by hospital admission, as there were no readmissions or complications related to outpatient status among higher-risk patients who had been discharged. Of nine higher-risk patients admitted as a precaution, eight needed no intervention and could have been treated as outpatients. The pulmonary congestion developed by one patient postoperatively was evident within hours and would have been detected readily had she been booked as an outpatient. Possibly her congestion could have been prevented had she been an outpatient. Intravenous fluids of outpatients are discontinued early to allow them to become mobile and leave. Since she was booked as a precautionary inpatient, intravenous fluids were continued and may have helped precipitate the congestion. Readmission rates were no different for higher or lower risk patients. Of all 515 cholecystectomies over the 2 years, the readmission rate was 2% and rate of return visits to Emergency 6%; review suggested that overnight admission may have prevented about one-quarter of the Emergency visits (<2% of all patients) and none of the readmissions. These data give no cause to doubt the wisdom of outpatient cholecystectomy and the findings presented do not support the concept that higher-risk patients fare better with routine admission to hospital. The opposite may be true, as suggested by the patient who developed pulmonary congestion: Hospitalization is an interventional treatment with its own complications. This study reports the fate of actual outpatients and is not an interpolation of inpatient results with speculation of what would happen had they been outpatients. Most of the patients of Saunders and co-workers seem to have been inpatients, proving that keeping patients in the hospital did not forestall the complications noted by them. Most of the minor complications documented Saunders and co-workers became evident 23 days after surgery and the more serious ones after 57 days. Since the standard for most surgeons who still keep their patients in hospital after laparoscopic surgery is a 12-day stay, the majority of complications could still go undetected at discharge. These patients have no suitable inpatient controls, as outpatient laparoscopic cholecystectomy, without selection because of medical status or risk, was routine for the authors institution during this study. However, since no complications or readmissions related to outpatient status were detected, it seems unlikely that a randomized controlled study could produce better results in the outpatient arm.

1149

Comparing these results to those of Saunders and coworkers, it seems that the question for a randomized controlled study to settle is not whether outpatient treatment is equally safe, but rather whether keeping patients in hospital promotes onset of complications.
Acknowledgments. The author is indebted to Ms. Diana Schouten and Dr. Robert A. Mustard for help with the statistical analyses, Ms. Sumi Ignatius for help with the records, and Dr. Remo Zadra for critical review of the manuscript.

References
1. Dawson B, Reed WA (1980) Anaesthesia for surgical outpatients. Can Anaesth Soc J 27: 409411 2. Federated Ambulatory Surgery Association Special Study 1 (1987) Alexandria, Virginia, Federated Ambulatory Surgery Association 3. Gold BS, Kitz DS, Leckey JH, Neuhaus JM (1989) Unanticipated admission to the hospital following ambulatory surgery. JAMA 262: 30083010 4. Keenan RL, Boyan CP (1985) Cardiac arrest due to anesthesia: a study of incidence and causes. JAMA 253: 23732377

5. Marx GF, Mateo CV, Orkin LR (1973) Computer analysis of postanesthetic deaths. Anesthesiology 39: 5458 6. Meridy HW (1982) Criteria for selection of ambulatory surgical patients and guidelines for anesthetic management: a retrospective study of 1553 cases. Anesth Analg 61: 921926 7. Natof HE (1980) Complications associated with ambulatory surgery. JAMA 244: 11161118 8. Natof HE (1984) Ambulatory surgery: patients with pre-existing medical problems. Ill Med J 166: 101104 9. Saunders CJ, Leary BF, Wolfe BM (1995) Is outpatient laparoscopic cholecystectomy wise? Surg Endosc 9: 12631268 10. Vacanti CJ, VanHouten RJ, Hill RC (1970) A statistical analysis of the relationship of physical status to postoperative mortality in 68,388 cases. Anesth Analg 49: 564568 11. Voitk AJ (1994) Outpatient cholecystectomy: implications for hospital utilization. Leadership Health Serv 3: 2123 12. Voitk AJ (1995) Routine outpatient cholecystectomy. Can J Surg 38: 262265 13. Voitk AJ (1996) Outpatient cholecystectomy. J Laparoendosc Surg 6: 7981 14. Wetchler BV (1988) Outpatient anesthesia. The geriatric outpatient. Probl Anesth 2: 128131

Original articles
Surg Endosc (1997) 11: 11451146

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Selection criteria for laparoscopic cholecystectomy in an ambulatory care setting

C. R. Voyles,1,2 B. R. Berch1,2
1 2

Surgical Clinic Associates, University of Mississippi, Jackson, MS, USA Department of Surgery, University of Mississippi, Jackson, MS, USA

Received: 1 April 1997/Accepted: 27 May 1997

Abstract Background: The ambulatory care center offers patient convenience and reduced costs after uneventful laparoscopic cholecystectomy. Methods: A prospectively accumulated database of 1,750 cholecystectomies performed by one surgeon in a hospital setting was analyzed to test criteria for ambulatory cholecystectomy. Proposed criteria included age less than 65, absence of upper abdominal operations, and elective operations in healthy patients at low risk for common bile duct stones. Results: Of 1,750 cholecystectomies, only 605 patients met all criteria for outpatient care. Discharge (from the inhospital setting) was accomplished within 24 h of operation in 92% (first 3 years) and 98% (last 4 years) of selected cases. Only one patient (0.2%, 1/605) was converted to an open procedure; another was readmitted 30 h postoperatively with hemorrhage from the liver bed. Conclusions: Laparoscopic cholecystectomy can be performed safely in an ambulatory care setting, given careful selection and education of patients and documented experience of the surgical team. Key words: Laparoscopic cholecystectomy Outpatient Ambulatory

In this study, we reviewed the prospectively accumulated data on 1,750 patients from a hospital setting in order to verify a strategy for identifying those patients appropriate for laparoscopic cholecystectomy in an ambulatory care facility with overnight stay capabilities. Materials and methods
From February 1990 through February 1997, 1,750 cholecystectomies were performed by a single surgeon. Data were compiled prospectively regarding age, sex, final diagnosis, enzyme levels, common bile duct (CBD) diameter by preoperative ultrasound, operation performed, postop stay, and complications. Criteria for the ideal patient were set by empirical methods: elective operations only; age less than 65; no significant underlying medical problems; no previous upper abdominal operations; no/low risk for common bile duct stones. The criterion of no/low risk was based on two preoperative studies: (1) maximum CBD diameter by preoperative ultrasound 5 mm and (2) normal biochemical studies (alkaline phosphatase, serum glutamic oxaloacetic transaminase, bilirubin, and amylase) [7]. The course of selected ideal patients was then evaluated for completed laparoscopic cholecystectomy, hospital stay 24 h, and avoidance of significant complications.

Results Of the 1,750 cholecystectomies performed, 10% were excluded from outpatient consideration because their cholecystectomy was performed incidental to other abdominal operations (Table 1). Another 25% were excluded because of emergencies (acute cholecystitis, suspected CBD stones, jaundice, pancreatitis, etc.), 19% because of age over 65, and 1% because of underlying medical problems or upper abdominal problems. Of the remaining 757 patients, onefifth were excluded because of elevated liver enzymes and/ or CBD dilatation. Therefore, the remaining sample of ideal patients included 605 of the 1,750 patients or 35% of the total number. Conversion from laparoscopic to open cholecystectomy was necessary in only one of 605 patients in order to better define the anatomy. One patient was discharged after 18 h, only to return with bleeding from the liver bed; transfusion and reoperation were required.

Laparoscopic cholecystectomy is the procedure of choice for symptomatic cholelithiasis; most patients are discharged from the hospital within 2448 h. Many procedures are currently being performed in ambulatory care centers [2, 4, 5]. However, the transition to the outpatient setting is acceptable only if the complication rate is quite low and the patients are reliably and safely discharged within 24 h.

Correspondence to: C. R. Voyles, 1421 North State Street 304 Jackson, MS 39202, USA

1146 Table 1. Reasons for exclusion (1,750 patients) Reason Incidental procedure Emergency Age >65 Complex medical problems Increased risk for CBD stones No. 170 446 356 21 152 Balance 1,580 (90%) 1,134 (65%) 778 (44%) 757 (43%) 605 (35%)

Table 2. Hospital stay 24 hours Years All electives All electives <65 All electives <65, no/low risk for stones 19901992 501/590 (85%) 370/406 (92%) 285/309 (92%) 19931996 488/544 (90%) 340/351 (97%) 289/296 (98%)

The analysis of postoperative stay was separated into two periods (19901992 and 19931996). The percentage of ideal candidates discharged in 24 h or less was higher in the most recent period with 98% of patients being discharged (Table 2). Reasons for hospitalization longer than 24 h included conversion to an open operation (one) and nausea (six). During the last year of the study, only 25% of the ideal patients were discharged the same day from the hospital setting. Overnight stay was often necessary because of late afternoon operations. Supported by this study, we have begun to perform laparoscopic cholecystectomy in an ambulatory care facility which has overnight capability. The facility charges for laparoscopic cholecystectomy are 30% less in the ambulatory care center (approximately $2,700 vs $4,000).

defined by normal liver enzymes and common bile duct diameter (5 mm). In the no/low risk patients, operative cholangiograms were not obtained as long as there were no signs of acute cholecystitis or cystic duct abnormality [7]. With a 7-year follow-up, there has been no clinical evidence of choledocholithiasis in over 800 patients judged to be at no/low risk and in whom operative cholangiograms were not obtained. Proponents of routine cholangiograms argue that 45% of patients have unsuspected stones in spite of preoperative studies. The discrepant findings must be explained by either false-positive studies or else clinically insignificant findings by the routine cholangiographers; less likely, our follow-up may have missed recurrent disease. While the controversy about routine cholangiography is likely to continue, all agree that the availability of cholangiography equipment is mandatory in both hospital settings and ambulatory care centers. The safety of laparoscopic cholecystectomy in selected patients in an ambulatory center has been supported by several studies. However, early surveillance with open communication is essential to reduce the risks associated with unrecognized complications. The progressively shortened facility stay must be offset by excellent patient teaching about the expected postoperative course and early office follow-up. In retrospect, the one patient who had a postoperative hemorrhage would have benefitted from a 48-h rather than a 24-h hospitalization. Increasing pain, nausea, or fever after the first postoperative day should be carefully evaluated since complications such as biliary leaks, intestinal injury, and hemorrhage may not be fully apparent within the first 24 h. As a caveat specific to most laparoscopic studies, the good results reported by many experienced surgeons in established laparoscopic centers may not be readily duplicated in less experienced centers [6]. Conclusion Given careful selection of patients, laparoscopic cholecystectomy can be safely performed in an ambulatory care setting. Our proposed criteria for patient selection is supported by an acceptably low complication rate and early discharge. References
1. Arregui ME, Davis CJ, Arkush A, Nagan RF (1991) In selected patients outpatient laparoscopic cholecystectomy is safe and significantly reduces hospitalization charges. Surg Laparosc Endosc 1: 240245 2. Farha GJ, Green BP, Beamer RL (1994) Laparoscopic cholecystectomy in a freestanding outpatient surgery center. J Laparoendosc Surg 4: 291294 3. Koo KP, Traverso LW (1996) Do preoperative indicators predict the presence of common bile duct stones during laparoscopic cholecystectomy? Am J Surg 171: 495499 4. Llorente J (1992) Laparoscopic cholecystectomy in the ambulatory surgery setting. J Laparoendosc Surg 2: 2326 5. Reddick EJ (1992) Laparoscopic cholecystectomy in freestanding outpatient centers. J Laparoendosc Surg 2: 6567 6. Southern Surgeons Club (1991) A prospective analysis of 1518 laparoscopic cholecystectomies. NEJM 324: 10731078 7. Voyles CR, Sanders DL, Hogan R (1994) Common bile duct evaluation in the era of laparoscopic cholecystectomy. Ann Surg 219: 744752 8. Zucker KA, Bailey RW, Gadacz TR, Imbembo AL (1991) Laparoscopic guided cholecystectomy. Am J Surg 161: 3644

Discussion Within the last decade, cholecystectomy has advanced from a 4- to 5-day hospitalization with the open procedure to a complete outpatient procedure for selected patients. The patient benefits of laparoscopic cholecystectomy in the ambulatory care setting include convenience and reduced costs [1, 2, 4, 5]. The benefits to the surgeon also include convenience, plus a more orderly operative schedule because disruptions are avoided that result from emergencies in the hospital setting [4, 5]. The benefits of convenience and reduced costs are real and laudable as long as patient safety is not compromised. Since conversion from a laparoscopic to an open procedure generally requires hospitalization, it is important to identify any preoperative risk factors that would increase the risk for an open procedure. Interestingly, the risk factors for conversions are the same factors that were originally judged to be relative contraindications to laparoscopic cholecystectomy [8]. These risk factors include advanced age, obesity, previous operations, pregnancy, and signs or symptoms of either acute cholecystitis or common bile duct stones. The accuracy of stratifying risk for common bile duct stones has been questioned by many investigators [3]. In our previous study, a no/low risk category of patients was

Surg Endosc (1997) 11: 12021205

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Laparoscopic Nissen fundoplication in children under 2 years of age

O. Zamir, R. Udassin, D. Seror, A. Vromen, H. R. Freund
Department of Surgery and Pediatric Surgery, Hadassah University Hospital Mount Scopus, and the Hebrew University-Hadassah Medical School, Jerusalem, 91240 Israel Received: 16 April 1997/Accepted: 30 June 1997

Abstract Background: Antireflux operations have been recommended for infants and children suffering from complications related to gastroesophageal reflux (GER). In recent years, the laparoscopic approach has been used increasingly for antireflux surgery in adult patients. This is our initial experience with Nissen fundoplication in infants and children under 2 years of age. Patients: We operated on 11 patients weighing between 3.0 and 10.0 kg. The main indications for surgery were GERinduced aspiration pneumonia and failure to thrive, in spite of intensive conservative treatment. All patients except one had an associated neurological abnormality, including six patients with familial dysautonomia. Results: All attempted operations were completed successfully laparoscopically, with only a few postoperative complications and acceptable short-term results. The clinical considerations and technical aspects unique to this specific group of patients are discussed. Conclusion: Laparoscopic Nissen fundoplication is feasible, safe, and effective, even in very small babies. Key words: Laparoscopy Fundoplication Infants and children Gastroesophageal reflux

was applied to various antireflux procedures in adults, including Nissen fundoplication. Recent reports suggested that Nissen fundoplication can be safely accomplished laparoscopically in most adult patients who need an antireflux operation, with acceptable morbidity and short-term results [2, 4, 5]. There have been a number of recent reports of laparoscopic fundoplication in children and adolescents [7 9, 11, 13]. In this report, we describe our experience with Nissen fundoplication in 11 infants and children who were <2 years of age at the time of operation. Some specific technical aspects and difficulties encountered in these small babies are discussed.

Patients Between October 1994 and November 1996 11 children (seven male and four female) <2 years of age (range, 324 months; mean, 12.2 months) underwent modified Nissen fundoplication at Hadassah University Hospital Mount Scopus. Their body weight at the time of operation ranged between 3.0 and 10.0 kg (mean, 7.2 kg). All children except one had associated abnormalities, mainly familial dysautonomia (six patients) or other neurological deficit (four patients). In all cases, conservative treatment was initially attempted; surgery was undertaken only after failure of all nonsurgical measures. The main complications leading to operation were recurrent lung infections and failure to thrive (Table 1). Three patients were transferred for surgery directly from the Department of Pediatrics following prolonged hospitalization for persistent vomiting and severe recurrent aspiration pneumonia. The indications for surgery, the preoperative work-up, and other relevant clinical details are shown in Table 1. During the study period, two babies with apparent delay in gastric emptying on barium meal or nuclear scan were excluded from the laparoscopic approach because this finding was considered an indication for pyloroplasty. In one patient with evidence of gastric emptying delay, laparoscopic procedure was employed, but pyloromyotomy was added at the end of the operation through a short supraumbilical incision. Two other babies underwent an open procedure because of their parents preference. The parents of all pa-

Gastroesophageal reflux (GER) may result in severe complications in infants and young children, including failure to thrive, recurrent aspiration pneumonia, apnea, asthma, and peptic stricture of the esophagus. The problem is especially common in neurologically impaired children. It has been widely accepted in recent years that even small children with severe symptomatic GER, including those with neurological impairment, may benefit from an antireflux operation such as Nissen fundoplication [3, 6, 10]. The very same conclusion was drawn for children with familial dysautonomia [12]. With advances in laparoscopic technique, this approach

Correspondence to: O. Zamir

1203 Table 1. Clinical data Age (mo) sex 24 Male 7 Female Weight (kg) 8.2 4.7 Associated disease Familial dysautonomia Familial dysautonomia Familial dysautonomia Familial dysautonomia Cerebral palsy Indication for surgery Recurrent pneumonia & apneic spells Aspirations, recurrent pneumonia & failure to thrive Recurrent pneumonia Recurrent pneumonia & failure to thrive Recurrent pneumonia & aspirations Recurrent pneumonia, aspirations, & asthma Aspirations & persistent vomiting Persistent vomiting, dehydration, & choking attacks Recurrent pneumonia Failure to thrive & recurrent pneumonia Failure to thrive & persistent vomiting Preoperative work-up Milk scan Milk scan Operation time (min) 200 195 Hospital stay (days) 10 17 Follow-up period (mo) 29 24

Procedure NF, G, App NF, G, App

9 Male

8.7

15 Male 11 Male 9 Female

8.8 7.4 7.7

pH study, barium meal, milk scan, esophagoscopy Milk scan Barium meal pH study, barium meal Barium meal Milk scan

NF, G, App

200

22

NF, G, App NF, G, App NF, G, App

265 225 225

8 9 9

20 16 16

6 Female 12 Male

4.9 8.3

Cerebral palsy & intractable seizures Familial dysautonomia Familial dysautonomia Microcephaly Methylmalonic acidemia & severe neurological deficit

NF, G, App

140

7 16

15 14

NF, G App, 185 pyloroplasty NF, G, App NF, G NF, G 190 210 270

19 Male 19 Female 3 Male

10.0 8.0 3.0

Milk scan pH study, barium meal, esophagoscopy Milk scan

7 7 7

11 9 5

NF, Nissen fundoplication; G, gastrostomy; App, appendectomy.

tients were given a detailed explanation of the laparoscopic procedure, and written consent was obtained in each case.

Surgical technique The procedure was performed under general endotracheal anesthesia with the child lying prone near the lower end of the operating table and the surgeon standing between the patients legs. A urethral catheter and a nasogastric tube were routinely inserted. A CO2 pneumoperitoneum was established using a Veress needle inserted through an infraumbilical incision. Pressures of 78 mm Hg only were used in the smaller babies and 12 mm Hg in larger children. An angled 30 10-mm scope was used in the larger children, while a 5-mm scope was used in three children weighing <5 kg. Four additional 5-mm ports were placed under direct vision and secured in place with a suture. A right lateral subcostal port was used for retraction of the liver anteriorly with a blunt grasper, and two ports, located one at each side of the camera port, were used for bimanual surgery. The fifth port was located on the left side for caudal traction of

the stomach and for traction of the esophagus, which was encircled with a tape following its mobilization. After placement of ports, the operating table was placed in a reverse Trendelenburg position. Pediatric 3.5-mm short instruments (Jarit Surgical Instruments, Inc, Hawthorne, NY, USA) and adult 5-mm instruments were used. The upper part of the gastrohepatic omentum and the phrenoesophageal ligament were first divided using curved bipolar coagulating scissors (Everest Medical, Minneapolis, MN, USA). The esophagus was mobilized using a blunt dissector. The plane of dissection could be identified clearly and mobilization was easily accomplished in these small children because of the minimal fat tissue present between the esophagus and the crura and in the hiatus. A short rubber sling was usually placed around the freed esophagus to facilitate its manipulation while expanding the retroesophageal space and during construction of the fundic wrap. In most cases, division of the short gastric vessels was not necessary. In two patients, partial division of the short gastric vessels was necessary to accomplish a tension-free wrap. One or two silk sutures were used to approximate the crura behind the esophagus.

1204

After passing the fundus behind the esophagus, the nasogastric tube was replaced by a bougie (1826 Fr) to assure a floppy fundoplication. A 23-cm long wrap was constructed using interrupted nonabsorbable sutures that were passed through both the stomach and the esophageal wall and tied with either extracorporeal or intracorporeal knotting technique. Special care was taken to avoid entrapment of the vagus nerves. Pledgets were used in seven cases. In all but two patients, appendectomy was also performed to avoid future confusion with the frequently occurring attacks of abdominal pain in these children. At the end of the procedure, a point on the anterior stomach wall suitable for gastrostomy was selected and pulled through the trocar site located in the left hypochondrium, which was slightly enlarged. A tube gastrostomy was fashioned, securing the stomach wall to the fascia with a few stitches. Since entrapment of omentum occurred postoperatively in two of our early cases, it is now our practice to close the fascia of all 10-mm ports as well as the 5-mm ports. All wounds were closed with subcuticular absorbable stitches.

Results All 11 attempted laparoscopic fundoplications were successfully completed as such. The mean operating time was 210 min (range, 140270 min). Because of their poor preoperative respiratory status, most patients needed aggressive pulmonary physiotherapy in an intensive care unit postoperatively, but only two patients required continuous mechanical ventilation for 2448 h after surgery. Enteral feeding was gradually started 24 days postoperatively. Nine children had a relatively smooth recovery and were discharged home in 710 days after surgery. In two children, entrapment of omentum in 5- and 10-mm ports wounds required surgical repair in the early postoperative period, prolonging their hospital stay to 16 and 17 days, respectively. The mean postoperative hospital stay was 9.6 days. In a follow-up period of 529 months (mean, 16.5 months), all patients reportedly stopped vomiting. Episodic nausea or retching persisted in two children with familial dysautonomia, apparently as part of their primary disease. Leakage around the gastrostomy tube occurred in two patients and was successfully treated on an ambulatory basis. Nine patients showed complete resolution of symptoms related to GER. Two patients required readmission to the hospital because of pulmonary infection. Barium study in both of them showed an intact fundoplication in an intraabdominal position, with no evidence of GER. We found no evidence of delayed gastric emptying in the postoperative follow-up period in any of our patients.

Discussion In recent years, laparoscopic Nissen fundoplication has been performed with increasing frequency in adult patients with symptomatic GER because it causes minimal trauma to the abdominal wall and supposedly eases patient recovery

[5]. Our initial experience demonstrates that Nissen fundoplication can be accomplished successfully and safely using the laparoscopic approach in very small babies suffering from severe GER. Infants and children who are candidates for antireflux procedure differ in many aspects from the adult population. In adults, GER is typically associated with hiatal hernia and is usually unrelated to any other abnormality. In children, on the other hand, there is usually no hiatal hernia, but clinically significant GER is often associated with neurological impairment, metabolic abnormality, or some other severe underlying disease. Therefore, even after successful surgical resolution of GER, these babies often remain very sick due to their primary disease. Many children undergoing antireflux operation are at increased risk because of chronic parenchymal lung damage due to recurrent episodes of pneumonia and because they are often severely malnourished. Operative risk is especially high in children with familial dysautonomia [1, 12]. Concomitant impairment of gastrointestinal motility is also unique to the pediatric population. In particular, impairment of the swallowing mechanism and delayed gastric emptying should be taken into account by the surgeon. Hence, when the swallowing mechanism is impaired, gastrostomy should be constructed for postoperative feeding or fluid administration to prevent persistent aspirations. Likewise, the surgeon should consider pyloroplasty when there is preoperative evidence of delayed gastric emptying [3]. In this case, we usually prefer an open procedure, although a pyloroplasty can be accomplished through a small laparotomy incision at the end of the laparoscopic procedure. This option was elected in one case in this series. There are several technical concerns in laparoscopic Nissen fundoplication that are unique to infants and small children. Because the operating space is very small, it is necessary to use specially designed short instruments and to handle them with great care. To prevent dislocation, the trocars need to be secured to the skin by stitches. The pneumoperitoneum should be maintained at pressures as low as 78 mm Hg. Elevation of pressure may cause difficulty in ventilation, with resultant hypercarbia. It is sometimes necessary to increase the pneumoperitoneum pressure temporarily, for example during suturing, and to immediately deflate the abdomen if expiratory CO2 increases or any difficulty in ventilation is encountered. Insufflation of a large volume of cold CO2 may cause hypothermia in small babies. Therefore, loss of the pneumoperitoneum must be kept to a minimum during surgery. At the same time, the minimal fat around the esophagus in these small babies and the absence of hiatus hernia make the definition of the dissection planes clearer. Thus, the dissection itself, including mobilization of the esophagus, identification of the vagus nerves, and construction of the fundic wrap are easier in small children than in adults. Furthermore, it is usually unnecessary to divide the short gastric vessels to achieve a tension-free wrap. Small children who need an antireflux operation often suffer from chronic lung disease, which makes them especially susceptible to postoperative lung complications. The laparoscopic approach seems to minimize these complications. The minimal trauma to the upper abdominal wall in this approach results in less impairment of respiration and

1205

minimizes the need for narcotics and sedatives postoperatively. Recent reports suggested that recovery was smoother following laparoscopic antireflux operations than after open procedures, with comparable short-term results [11, 13]. We conclude that laparoscopic Nissen fundoplication is feasible and safe in very small children and infants and that it appears to offer some advantages over the standard open technique. References
1. Beilin B, Maayan C, Vatashski E, Shulman D, Vinograd I, Aronson HB (1985) Fentanyl anesthesia in familial dysautonomia. Anesth Analg 64: 7276 2. Dallemagne B, Weerts JM, Jehacs C, Markiewicz S (1991) Laparoscopic Nissen fundoplication; preliminary report. Surg Laparosc Endosc 1: 138143 3. Fonkalsrud EW, Foglia RP, Ament ME, Berquist W, Vergas J (1989) Operative treatment of the gastroesophageal reflux syndrome in children. J Pediatr Surg 24: 525529

4. Geagea J (1991) Laparoscopic Nissens fundoplication; preliminary report on ten cases. Surg Endosc 5: 170173 5. Jamieson GG, Watson DI, Jones RB, Mitchel PC, Anvari MA (1994) Laparoscopic Nissen fundoplication. Ann Surg 220: 137145 6. Kazerooni NL, VanCamp J, Hirschi RB, Drongowski RA, Coran AG (1994) Fundoplication in 160 children under 2 years of age. J Pediatr Surg 29: 677681 7. Lloid DM, Robertson GSM, Jonstone JMS (1995) Laparoscopic Nissen fundoplication in children. Surg Endosc 9: 781785 8. Lobe TE, Schropp KP, Lunsford K (1993) Laparoscopic Nissen fundoplication in childhood. J Pediatr Surg 28: 358361 9. Meehan JJ, Georgeson KE (1996) Laparoscopic fundoplication in infants and children. Surg Endosc 10: 11541157 10. Randolph J (1983) Experience with the Nissen fundoplication for correction of gastroesophageal reflux in infants. Ann Surg 198: 579584 11. Szold A, Udassin R, Maayan C, Vromen A, Seror D, Zamir O (1996) Laparoscopic modified Nissen fundoplication in children with familial dysautonomia. J Pediatr Surg 31: 15601562 12. Udassin R, Seror D, Vinograd I, Zamir O, Nissan S (1992) Nissen fundoplication in the treatment of children with familial dysautonomia. Am J Surg 164: 332336 13. Zee van der DC, Bax NMA (1996) Laparoscopic Thal fundoplication in mentally retarded children. Surg Endosc 10: 659661

Surg Endosc (1997) 11: 11791182

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Minimally invasive treatment of acute biliary pancreatitis

F. Ricci, G. Castaldini, G. de Manzoni, G. Borzellino, L. Rodella, R. Kind
First Department of General Surgery, University of Verona, 37126 Verona, Italy Received: 23 September 1996/Accepted: 2 April 1997

Abstract Background: Stones of the common bile duct are the most important factor in acute pancreatitis (AP). Endolaparoscopic surgery plays a well-recognized role in the treatment of this pathology. Methods: From January 1992 to December 1995 we observed 62 cases of acute biliary pancreatitis (ABP). In 57 cases ( 93.4%) we proposed a minimally invasive treatment, based on performance of endoscopic retrograde cholangiopancreatography (ERCP) combined with endoscopic sphincterotomy (ES) and then of laparoscopic cholecystectomy (LC). Results: ERCP was attempted in emergency in 40/57 cases and successfully done in 34 cases. An ES was performed in all but two cases. In 51 patients we performed LC. The overall morbidity was 8.9% with no mortality. Conclusions: In the case of ABP early treatment can achieve the restoration of patency of the papilla, reducing the risk of associated cholangitis and the development of pancreatic necrosis. The cholecystectomy prevents the risk of relapse of ABP. Key words: Acute biliary pancreatitis Endoscopic retrograde pancreatography Laparoscopic cholecystectomy

istics of the patients or the dyshomogeneity of the diagnostic criteria adopted, on the other, it is undeniable that a substantial percentage of cases of AP defined as idiopathic are in actual fact due to the presence of microlithiasis or bile crystals [17, 22]. Thus, the relative incidence of biliary etiology would appear to be underestimated, so much so indeed that in our own experience such an etiology has been confirmed in 75% of the AP cases observed [3]. A number of investigators, moreover, believe that acute biliary pancreatitis (ABP) will relapse in 50% of cases within 6 months if the patient does not undergo a cholecystectomy [10, 1821, 28]. The development and increasingly widespread use of endolaparoscopic surgery has enabled us to propose a minimally invasive approach for this type of disease, according to a therapeutic protocol involving, first, the performance of emergency endoscopic retrograde cholangiopancreatography (ERPC) combined with endoscopic sphincterotomy (ES), and, once the acute attack has been resolved, laparoscopic cholecystectomy (LC). Particular concomitant pathological situations such as acute cholecystitis or an intraperitoneal fluid collection can also benefit from minimally invasive treatment by means of US-guided skin puncture. With a view to assessing the efficacy and validity of minimally invasive treatment we reviewed the data on patients admitted to our department for AP over the period from January 1992 to December 1995.

Acute pancreatitis (AP) is a disease of by no means negligible social importance with an annual incidence of approximately 10 cases/100,000 population [23, 25] and carries a mortality rate of around 10% [2, 15]. Stones of the common bile duct are undoubtedly the most important etiological factor in AP. On the basis of the data reported in the literature, biliary etiology is responsible for 5060% of cases of AP [2, 12, 25] with incidences ranging from 16 to 70% [20]. While, on the one hand, these variations reflect the different ethnic and cultural character-

Materials and methods

Over the period from January 1992 to December 1995 some 82 patients with a diagnosis of AP were admitted to the Verona University 1st Department of General Surgery. As regards the etiology of the AP, we observed alcohol abuse in 14 cases (17%), inflammatory or neoplastic disease of the duodenal papilla in four cases (4.9%), postoperative onset of AP in three cases (3.6%), and biliary etiology in 61 cases (74.4%). The diagnosis of ABP was based on medical history (established evidence of gallstones, previous episodes of biliary colic, absence of alcohol abuse), suggestive abnormalities in blood-chemistry tests (ALP > 250 IU/l, ALT > 100 IU/l, bilirubin > 25 mmol/l), and, at ultrasonography of the bile ducts, (lithiasis, microlithiasis, or bile sludge in the gallbladder, dilatation of the bile ducts, or choledocholithiasis). In the ABP cases, the patients were submitted to a minimally invasive

Correspondence to: F. Ricci, I Divisione Clinicizzata di Chirurgia, Ospedale Civile Maggiore, Piazzale Stefani, 1, 37126 Verona, Italy

1180 Table 1. ERCP findingsa Timing of ERCP Before 48 h After 48 hb

b

Predicted severity Mild Severe All cases Mild Severe All cases

CBDS 19/26 cases (73.1%) 7/8 cases (87.5%) 26/34 cases (76.5%) 8/17 cases (47%) 2/3 cases (66.6%) 10/20 cases (50%)

CBDD 16/26 cases (61.5%) 7/8 cases (87.5%) 23/34 cases (67.6%) 8/17 cases (47%) 1/3 cases (33.3%) 9/20 cases (45%)

Common bile duct stones (CBDS) and common bile duct dilatation (CBDD) related to severity of ABP and timing of ERCP b From the onset of symptoms

treatment according to a protocol involving the execution of an emergency ERCP combined with ES for the purposes of achieving early removal of the obstacle to pancreatic outflow. Once the acute attack had been resolved, the patient was kept in the department and a laparoscopic cholecystectomy was performed in order to prevent any relapse of AP. This treatment was possible in 57/61 cases of ABP ( 93.4%). The mean age of these patients was 52.1 years (range: 2486); in 19/57 cases (33.3%) the patients were aged > 70 years. The male/female ratio was 1.1:1. We used Ranson scores for a prognostic assessment: We thus observed mild AP (Ranson scores < 3) in 46/57 cases (80.7%) and severe AP (Ranson scores 3) in the other 11 cases (19.3%). Within the latter group we observed scores of 34 in eight cases (with a mean mortality rate of 16% according to Ranson), scores of 56 in two cases (reported mortality 40%), and a score of 7 in one case (reported mortality 100%). In the more clinically demanding cases, or when ultrasonography revealed the presence of intraabdominal fluid collections, an emergency abdominal CT scan was performed.

Results In our study we observed a biliary etiology of AP in 61/82 cases (74.4%). In 4/61 cases (6.5%) a pancreatic necrosectomy was performed with the positioning of multiple abdominal drains (one death). These patients were referred to our department from another hospital as a result of deterioration of their general condition. A mean period of 7 days (range: 411) had elapsed since onset of symptoms. We therefore excluded these four cases from our analysis. In 57/61 cases of ABP (93.4%) we examined the patient within only a few hours of onset of symptoms. It was thus possible to offer these patients the minimally invasive treatment described above. The ERCP was attempted in all 57 patients. In 40 cases (70.2%) the procedure was an emergency ERCP (within 48 h of onset of symptoms) and proved successful in 34 cases. The feasibility of the examination in emergency conditions was therefore 85%. In the remaining 17 cases the procedure was attempted after 48 h and proved successful in 15 cases (88.2% feasibility). In eight cases (three of which with a severe prognosis) the procedure failed at the first attempt. The causes of failure were the presence of substantial duodenal edema preventing visualization of the papilla (six cases), a bulky duodenal diverticulum (one case), and the onset of an allergic reaction to the iodinized contrast medium (one case). In five cases of duodenal edema, a second ERCP was successfully attempted after a mean interval of 8 days (range: 612). The remaining three patients, whose AP attack was mild, refused to repeat the examination and declined any further surgical treatment; they were treated with

medical therapy alone and discharged once the acute attack had been resolved. These patients are, of course, excluded from the analysis of the data on the cholangiographic study of the main bile duct and ES. In all, the ERCP was successful in 54/57 cases (94.7%). We observed the presence of common bile duct stones (CBDS) in 26/34 patients (76.5%) within 48 h and in 10/20 patients (50%) after 48 h. If we consider only the 11 patients with a severe prognosis, the respective percentages were 87.5% (7/8 patients) and 66.6% (2/3 patients). Dilatation of the common bile duct (CBDD) was observed in 23/34 patients (67.6%) within 48 h and in 9/20 patients (45%) after 48 h. In the cases with a severe prognosis, the respective values were 87.5% (7/8 patients) and 33.3% (1/3 patients). In particular, we observed CBDD without evidence of CBDS or edema of the papilla in six cases. In these patients, after execution of ES, we observed an out-gushing of dense bile (Table 1). The presence of papillary edema was observed in 13/54 cases (24%), five of whom had a severe prognosis. In six cases this finding was not associated with CBDD or CBDS. We performed ES in 52/54 cases (96.3%). The procedure was not performed in the other two cases, since, in one case, the papilla was broad enough, while, in the other case, we managed to perform only a pre-cut of the papilla, which, however, was sufficient to guarantee bile outflow. Extraction of choledochal stones by means of a Dormia basket was necessary in 38 cases and mechanical lithotripsy in five cases. In 15 cases a nasobiliary probe was positioned at the end of the procedure, so as to be able to perform a cholangiographic follow-up examination a few days later. In this phase we registered 7% morbidity (four cases of bleeding of the papilla). The mortality rate was nil. The results of laparoscopic cholecystectomy are shown in Table 2. The AP was accompanied by acute cholecystitis in four cases. These patients were submitted at entry to US-guided percutaneous cholecystostomy, with a rapid improvement in pain symptoms, leukocytosis, and hyperpyrexia. In three of the eight patients in whom ERCP failed at the first attempt owing to duodenal oedema, ultrasonography revealed an overdistended gallbladder with walls of normal thickness. In these cases we performed a US-guided percutaneous cholecystostomy and later a transcholecystic cholangiography documenting the presence of a papillary obstacle to bile outflow.

1181 Table 2. Results of laparoscopic cholecystectomy, performed in 51 cases Performed successfully Converted to open cholecystectomy Intraoperative cholangiography Performed during same hospital stay; mean interval from ERCP Performed during 2nd scheduled admission mean interval from ERCP Morbility Mortality 51/51 cases 0/51 cases 47/51 cases 34/51 cases 7.3 days (range 521) 17/51 cases 42 days (range 1865) 1/51 cases 0/51 cases 100% 0% 92.1% 66.6% 33.3% 1.9% 0%

In one case of acute necrotizing-hemorrhagic pancreatitis the CT scan performed at entry revealed a fluid collection occupying the right parietocolic sulcus. An 8-Fr drainage catheter was therefore positioned via a US-guided percutaneous route, enabling the collection to be drained off. Repeated US follow-up scans showed progressive reduction of the collection. In one last case, we observed a pancreatic collection located in the body-tail of the pancreas developing into a pseudocyst. This mass was responsible for pain in the left hypochondriac region associated with a sensation of nausea and vomiting due to gastric compression. After performance of an ERCP, combined with ES, had ruled out the existence of any communication between the pseudocyst and the pancreatic ductal system, the patient was submitted 51 days after the AP attack to US-guided percutaneous drainage of the pseudocyst with placement of a 7-Fr catheter. After discharge, the patient was followed up on an outpatient basis with repeated US scans. After 62 days, the drainage catheter was removed and the patient underwent laparoscopic cholecystectomy. The mean hospital stay for the entire treatment was 14.9 days (range: 737). This value was 12.7 days (range: 728) in cases of mild AP and 21.5 (range: 123) in cases of severe AP. All the patients were followed-up. No patient had relapse of ABP after a median follow-up of 6 months (range 654). Discussion We should make it clear right from the outset that in this study attention is focused on the group of 57 patients suffering from ABP and treated with wholly minimal invasive therapy: ERCP + ES percutaneous cholecystostomy or percutaneous drainage of peritoneal collections + laparoscopic cholecystectomy. An attack of ABP will occur in the course of time in roughly 48% of patients suffering from gallstone disease [1, 19, 20]. In actual fact, ABP is a nosological entity which is continually and progressively on the increase. In our own experience, we have observed a biliary etiology of AP in about 75% of cases (61/82 patients). Analysis of the literature shows that, whereas, on the one hand, the mild forms of ABP evolve favorably, in most cases with medical therapy alone [4, 7, 8], on the other, the severe forms are characterized by local and/or systemic complications. Mortality rates of 810% are still being reported today in AP populations [2, 12, 15].

ERCP combined with ES is today one of the mainstays in the treatment of ABP. However, there is no agreement among the various investigators as to the indications and actual efficacy of these procedures when performed in the emergency setting (within 48 h). A number of authors [1, 7, 16, 24] believe that this combination is indicated in the early phase only in the severe forms of ABP or in cases presenting associated cholangitis or CBDS, since ERCP + ES is by no means complication-free and the mild forms would not appear to benefit noticeably from the procedure. Other investigators [6, 13, 21, 27] stress the importance, both diagnostic and therapeutic, of ERCP + ES in cases of AP, regardless of the prognostic assessment. Some other authors [5, 14, 26] support the use of preoperative ERCP only selectively, based on persistent elevated pancreatic and/or liver enzymes or evidence of CBDS by ultrasonography. If these criteria are not met, it is possible to perform an LC with routine intraoperative cholangiography and, if necessary, laparoscopic CBD exploration, with stone retrieval through the cystic duct or saline flushing of the CBD. Our own feeling is that emergency ERCP (within 48 h) should be performed in all cases of AP of confirmed or strongly suspected biliary etiology. In our experience, the procedure proved successful in the emergency setting in approximately 85% of cases, revealing the presence of CBDS and dilation of the common bile duct in 76.5% and 67.6% of cases, respectively. An ES was performed in practically all cases. The approach in the early phase yielded a correct etiological diagnosis as well as ensuring that the patient received immediate therapy through cleansing of the main bile duct. These maneuvers, moreover, appear to be safe even in elderly patients, who, in our patient sample, account for 33.3% of the total. The overall morbidity rate we observed was 7% and the mortality rate nil. The execution of laparoscopic cholecystectomy, preferably performed in the course of the same hospital stay after resolution of the acute attack, permits definitive treatment of the disease, preventing recurrences of ABP. As we have already reported, the risk of relapse in patients with ABP is 50% of cases within 6 months of the first attack. The operation, which other authors do not regard as necessary after execution of an ES and which is now standardized in terms of surgical technique, does not take much longer to perform than in routine cases (90 min on average). Perioperative cholangiography, which we perform in 92.1% of cases, is a useful means of confirming both the anatomical picture and the clearing of the bile duct with good outflow at papillary level. The best results in terms of patient and socioeconomic

1182

benefit were achieved when the cholecystectomy was performed in the course of the same hospital stay, once the acute attack had been resolved (reversion of serum amylase and leukocytosis values to normal). US-guided transhepatic percutaneous cholecystostomy is indicated in cases of cholecystitis associated with ABP. This procedure affords a rapid improvement in the patients clinical course, thereby laying the foundations for performing the minimally invasive treatment [11]. Furthermore, after failure of ERCP, percutaneous cholecystostomy allows decompression of the bile ducts in cases where the gallbladder is overdistended. In these cases, too, the overdistention of the gallbladder is an indicator of the increased pressure of the bile ducts with a patent cystic duct, the latter being a sine qua non for effective transcholecystic drainage. Conclusions We think that in the presence of suspected or ultrasonographically confirmed ABP, treatment must be given as early as possible and must be aimed at achieving two primary objectives: 1. The restoration of patency of the papilla both in order to reduce the risk of associated cholangitis and in order to prevent and/or reduce the development of pancreatic necrosis 2. Treatment of the associated bile duct and gallbladder pathology to prevent the risk of relapse of ABP In light of this, in our opinion, the execution of a combined ERCP plus ES as early as possible, followed during the same hospital stay by a laparoscopic cholecystectomy, once the acute attack has been resolved, could modify the outcome of patients suffering from ABP. This approach should be further evaluated in prospective trials comparing other alternative treatments. References
1. Bedford RA, Howerton DH, Geenen JE (1994) The current role of ERCP in the management of benign pancreatic disease. Endoscopy 26: 113119 2. Blamey SL, Osborne H, Gilmour WH, ONeill J, Carter DC (1983) The early identification of patients with gallstone associated pancreatitis using clinical and biochemical factors only. Ann Surg 158: 574 578 3. Borzellino G, Ricci F, Veraldi D, Cordiano C (1995) Role of endolaparoscopic surgery in acute biliary pancreatitis. In: Lezoche E, Paganini AM, Bergi G (eds) Thoraco-laparoscopic and minimally invasive surgery. Milano, Italy, pp 145148 4. Bradley EL III (1993) A clinically based classification system for acute pancreatitis. Arch Surg 128: 586590 5. Canal DF, Broadie TA (1994) Results of laparocholecystectomy for the treatment of gallstone pancreatitis. Am Surg 60: 495499 6. Carr-Locke DL (1990) Acute gallstone pancreatitis and endoscopic therapy. Endoscopy 22: 180183

7. Carr-Locke DL (1992) Role of endoscopy in gallstone pancreatitis. Am J Surg 165: 519521 8. Cooperman AM, Siegel J, Neff R, Reddy S, Hammerman H (1991) Gallstone pancreatitis: combined endoscopic and laparoscopic approaches. J Laparoendosc Surg 1: 115117 9. Corfield AP, Cooper MJ, Williamson RCN, Mayer AD, McMahon MJ, Dickson AP, Shearer MG, Imrie CW (1985) Prediction of severity in acute pancreatitis: prospective comparison of three prognostic indices. Lancet 24: 403407 10. De Iorio AV, Vitale GC, Reynolds M, Larson GM (1995) Acute biliary pancreatitis. Surg Endosc 9: 392396 11. de Manzoni G, Furlan F, Guglielmi A, Brunelli G, Laterza E, Ricci F, Genna M, Borzellino G, Cordiano C (1992) Acute cholecystitis: ultrasonographic staging and percutaneous cholecystostomy. Eur J Radiol 15: 175179 12. Demmy TL, Burch JM, Feliciano DV, Mattox KL, Jordan GL (1988) Comparison of multiple-parameter prognostic systems in acute pancreatitis. Am J Surg 156: 492496 13. Fan ST, Lai ECS, Mok FPT, Lo CM, Zheng SS, Wong J (1993) Early treatment of acute biliary pancreatitis by endoscopic papillotomy. N Engl J Med 328: 228232 14. Graham LD, Burrus RG, Burns RP, Chandler KE, Barker DE (1994) Laparoscopic cholecystetomy in biliary pancreatitis. Am Surg 60: 40 43 15. Mann DV, Hershman MJ, Hittinger R, Glazer G (1994) Multicentre audit of death from acute pancreatitis. Br J Surg 81: 890893 16. Neoptolemos JP, Carr-Locke DL, London NJ, Bailey IA, James D, Fossard DP (1988) Controlled trial of urgent endoscopic retrograde cholangiopancreatography and endoscopic sphincterotomy versus conservative treatment for acute pancreatitis due to gallstones. Lancet 29: 979983 17. Neoptolemos JP, Davidson BR, Winder AF, Vallance D (1988) Role of duodenal bile crystal analysis in the investigation of idiopathic pancreatitis. Br J Surg 75: 450453 18. Neoptolemos JP, Stonelake P, Radley S (1993) Endoscopic sphincterotomy for acute pancreatitis. Hepatogastroenterology 40: 550555 19. Pellegrini CA (1993) Surgery for gallstone pancreatitis. Am J Surg 165: 515518 20. Ranson JHC (1982) Etiological and prognostic factors in human acute pancreatitis: a review. Am J Gastroenterol 77: 633638 21. Rhodes M, Armstrong CP, longstaff A, Cawthorn S (1993) Laparoscopic cholecystectomy with endoscopic retrograde cholangiopancreatography for acute gallstone pancreatitis. Br J Surg 80: 247 22. Ros E, Navarro S, Bru C, Garcia-Puge s A, Valderrama R (1991) Occult microlithiasis in idiopathic acute pancreatitis: prevention of relapses by cholecystectomy or ursodeoxycholic acid therapy. Gastroenterology 101: 17011709 23. Scuro LA, Cavallini G (1990) La patologia infiammatoria del pancreas. Luigi Pozzi (ed) Roma, Italy 24. Soper NJ, Brunt LM, Callery MP, Edmundowicz SA, Aliperti G (1994) Role of laparoscopic cholecystectomy in the management of acute gallstone pancreatitis. Am J Surg 167: 4251 25. Steinberg W, Tenner S (1994) Acute pancreatitis. N Engl J Med 330: 11981210 26. Targarona EM, Balague C, Viella P, Martinez J, Trias M (1994) Laparoscopic cholecystectomy for biliary pancreatitis. Br J Surg 81: 1694 1695 27. Uomo G, Galloro V, Rabitti PG, Marcopido B, Laccetti M, Visconti M (1991) Early endoscopic cholangiopancreatography and sphincterotomy in acute biliary pancreatitis: report of 50 cases. Ital J Gastroenterol 23: 564566 28. Winslet MC, Imray C, Neoptolemos JP (1991) Biliary acute pancreatitis. Hepatogastroenterology 38: 120123

Technique
Surg Endosc (1997) 11: 12211223

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Laparoscopic infrared imaging

W. W. Roberts,1 T. A. Dinkel,1 P. G. Schulam,1 L. Bonnell,2 L. R. Kavoussi1
1 2

Department of Urology, Brady Urological Institute, Johns Hopkins Medical Institutions, 4940 Eastern Avenue, Baltimore, MD 21224, USA Vipera Systems, Inc., 1464 Holcomb Road, Huntingdon Valley, PA 19006, USA

Received: 23 August 1996/Accepted: 14 October 1996

Abstract. A system was developed to determine the potential role of infrared imaging as a tool for localizing anatomic structures and assessing tissue viability during laparoscopic surgical procedures. A camera system sensitive to emitted energy in the midinfrared range (35 m) was incorporated into a two-channel visible laparoscope. Laparoscopic cholecystectomy, dissection of the ureter, and assessment of bowel perfusion were performed in a porcine model with the aid of this infrared imaging system. Inexperienced laparoscopists were asked to localize and differentiate structures before dissection using the visible system and then using the infrared system. Assessment of bowel perfusion was also conducted using each system. Infrared imaging proved to be useful in differentiating between blood vessels and other anatomic structures. Differentiation of the cystic duct and arteries and transperitoneal localization of the ureter were successful in all instances using the infrared system when use of the visible system had failed. This system also permitted assessment of bowel perfusion during laparoscopic occlusion of mesenteric vessels. These initial studies demonstrate that infrared imaging may improve the differentiation and localization of anatomic structures and allow assessment of physiologic parameters such as perfusion not previously attainable with visible laparoscopic techniques. It may thus potentially be a powerful adjunct to laparoscopic surgery. Key words: Thermography Laparoscopy Infrared

two-dimensional imaging of the operative field, and hand eye dissociation have limited its widespread adaptation for complex surgical procedures. Infrared imaging (also referred to as infrared thermography) is a technology that can potentially provide additional anatomic and physiologic information during laparascopic surgery. This study attempted to assess the utility of infrared thermography in a porcine model during laparoscopic surgery. Materials and methods System design
The infrared system consisted of a laparoscope measuring 15 mm in diameter and 30 cm in length. Within the laparoscope parallel visible and infrared channels transmitted images to visible and infrared electronic cameras, respectively. The cameras processed this information and relayed the data to a video mixer and then to a display monitor (Fig. 1). The infrared component of the system detected emitted energy in the midinfrared range, between 3 and 5 m, and was sensitive to gradations in temperature as small as one-tenth of one degree Centigrade. Warm areas appeared white and cooler areas appeared black when the image was displayed. This system was capable of displaying visible, infrared, blended, and composite images.

Animal studies
A porcine model was used for laparoscopic experimentation of the infrared imaging system. Three pigs were used for this study. After an adequate depth of anesthesia was achieved, a pneumoperitoneum was obtained in standard fashion and five working trocars were placed. A 15-mm trocar was placed supraumbilically and two 10-mm trocars were placed in the midclavicular line, one just subcostal and the other at the level of the anterior superior iliac spine. One trocar was placed in the posterior axillary line at the level of the umbilicus. After placement of all trocars, laparoscopic cholecystectomy, dissection of the ureter, and isolation of a segment of bowel were performed. Three inexperienced laparoscopists (junior residents) attempted to identify anatomic structures (cystic duct, cystic artery, and ureter) prior to dissection by visible inspection and then using the infrared camera. Additionally, bowel ischemia was assessed by three experienced laparoscopists. Mesenteric vessels were clipped and the bowel was imaged with both the visible and infrared systems. Room temperature saline, applied to the operative field via an irrigator/aspirator, was used as a contrast-enhancing agent.

Laparoscopy has resulted in significantly less postoperative morbidity when compared with traditional open approaches for many surgeries. This has led to an increasing demand for laparoscopic applications; however, lack of tactile feedback,

Correspondence to: L. R. Kavoussi

1222

Fig. 1. The 300 15 mm laparoscope contains two channels that transmit data to the visible and infrared cameras. The images are relayed to a video mixer and onto a monitor. This allows display of visible, infrared, composite, or blended images.

Results In all three pigs, inexperienced laparoscopists could independently identify the ureter, cystic duct (Fig. 2), and cystic artery (Fig. 3) using the infrared imaging system, prior to dissection, when these structures were not visibly apparent. Moreover, infrared imaging allowed assessment of tissue viability based upon degree of perfusion (Figs. 4, 5). This physiologic data was not apparent with a visible imaging system during surgery but could readily be discerned by all surgeons on the infrared images.

Discussion Thermography is a process of two-dimensionally mapping temperature differences by detecting the electromagnetic radiation emitted from a tissue or fluid that is warmer or cooler than its surroundings. Boltzmanns law states that the radiation (E) emitted by a body is proportional to the fourth power of its absolute temperature (T). The two variables are related by , the Stefan-Boltzmann constant. E T 4 As a result of this physical law, even slight temperature differences between adjacent areas will result in large differences in emitted radiation. This type of radiation is almost exclusively within the infrared portion of the electromagnetic spectrum, having wavelengths between 2 and 15 m. Visible light has shorter wavelengths, between 0.40 and 0.75 m. Special cameras have been designed to record infrared radiation emitted from the body. These cameras detect temperature gradients noninvasively and have been applied in wide-ranging areas of medicine as diagnostic devices, surgical instruments, and tools for measuring systemic temperatures [7]. The most well-publicized application of infrared thermography was breast cancer screening in the 1970s [2, 9]. Based on the premise that a cancerous focus would have a characteristic thermographic appearance, thermographs of a patients breasts were compared for symmetry. However, this technique failed because thermographic patterns of normal breasts are highly complex and attempts to compare

them resulted in cancer detection rates below 50% in some studies. However, in patients with known breast cancer, infrared thermography has proven useful in predicting tumor growth rates [3]. Other potential applications of this technology include diagnosing rheumatologic conditions [12], diagnosing carpal tunnel syndrome [11], assessing and monitoring coronary artery disease [5], evaluating uterine activity during labor [13], assessing herpes labialis infection during flareups [1], assessing brain activity [10], and documenting and characterizing skin-temperature changes due to many causes. Specific surgical applications include recoveryenhanced thermography for localization of cutaneous perforators in skin flaps [4], intraoperative assessment of internal mammary artery patency during coronary bypass procedures [6], and evaluation of cerebrovascular heat clearance during arteriovenous malformation repair [8]. This is the first reported use of infrared thermography in conjunction with laparoscopy. The principles upon which the system is based make use of temperature gradients between adjacent structures. Temperature differences within the body are slight so techniques are needed to accentuate these gradients. Recovery-enhanced thermography has been used in plastic surgery to identify cutaneous perforators. A region of skin is cooled by applying ice water and then infrared images of the area are taken as it rewarms. The vessels rewarm quickly and are distinguishable against a cooler background. We have applied this same technique to laparoscopic surgery. When room-temperature saline is used as an irrigant on the operative field, the whole field is cooled temporarily. As the field differentially rewarms, those structures, such as blood vessels, which rewarm quickly appear as white lines against a dark background. In this way vessels can be identified and differentiated from other tubular structures and ducts. A second application of this same concept involves filling the upper urinary system with room-temperature saline. The pelvis and ureter appear black against a warmer background which appears white. There are many other potential surgical applications for this system including localizing a ureteral stone during a ureterolithotomy by instilling room-temperature saline into the ureter to identify the level of obstruction. Assessment of perfusion is possible with infrared imaging at the time of the procedure, hours before visible alterations of the tissue are apparent. This may also be used to check the viability of a segment of bowel in patients who have suffered mesenteric ischemia or to provide a way to assess testicular blood flow during laparoscopic orchidiopexy. Cancerous or precancerous lesions could potentially be identified based upon their thermographic characteristics resulting from differential blood flow. The initial studies with this system are very promising; however, clinical applicability needs to be demonstrated. In doing so, several design modifications will be implemented. First, the diameter of the laparoscope needs to be decreased from 15 mm to 10 mm. Second, the combined infrared/ visible camera dimensions should be downsized to approach the dimensions of current visible cameras. Finally, a simple surgeon-controlled switch, which will allow rapid alternation between visible and infrared imaging, needs to be constructed.

1223

Figs. 2, 3. (far left and left, respectively) The gallbladder is in the upper lefthand corner of the pictures. The cystic duct and cystic vessels are contained within the pedicle (c). Infrared imaging clearly delineates the cystic duct, which appears dark, from the deep and superficial cystic arteries (a), which appear as white lines on either side of the cystic duct.

Figs. 4, 5. (far left and left, respectively) Using infrared imaging and room-temperature saline as a contrast-enhancing agent, a segmental mesenteric artery (a) appears as a thin white line. The bowel (b) perfused by that artery appears white. The segmental artery was clipped and a few minutes later the second infrared picture was taken. The segmental artery now appears dark, as does the bowel, suggesting a compromised blood flow. A clear line of demarcation is noted between the compromised and well-perfused regions of bowel.

The laparoscopic environment creates challenges for the surgeon because of lack of tactile feedback, two-dimensional imaging of the three-dimensional operative field, and handeye dissociation. Infrared imaging may help to overcome these challenges by providing additional information that previously was not available using visible imaging. This technology may decrease the risks associated with laparoscopic procedures as well as decrease costs by shortening operating time and thus has the potential to become a very powerful adjunct to laparoscopy.
Acknowledgment. This work was funded in part by a grant from the American Foundation for Urological Disease. We thank Leonard Bonnell, Dennis Leiner, and Thomas Brukilacchio of Vipera Systems, Inc., for providing their prototype Mid-Infrared Laparoscopic Imaging System.

4. Itoh Y, Arai K (1995) Use of recovery-enhanced thermography to localize cutaneous perforators. Ann Plast Surg 34: 507511 5. Lawson W, BenEliyahu D, Meinken L, Chernilas J, Novotny H, Cohn P, Dervan J (1993) Infrared thermography in the detection and management of coronary artery disease. Am J Cardiol 72: 894896 6. Mohr FW, Falk V, Philippi A, Autschbach R, Krieger H, Diegeler A, Dalichau H (1994) Intraoperative assessment of internal mammary artery bypass graft patency by thermal coronary angiography. Cardiovasc Surg 2: 703710 7. Nobell JJ (1992) Infrared ear thermometry. Pediatr Emerg Care 8: 5458 8. Okudera H, Kobayashi S, Toriyama T (1994) Intraoperative regional and functional thermography during resection of cerebral arteriovenous malformation. Neurosurgery 34: 10651067 9. Orel SG, Troupin RH (1993) Nonmammographic imaging of the breast: current issues and future prospects. Semin Roentgenol 28: 231 241 10. Shevelev IA, Tsicalov EN, Gorbach AM, Budko KP, Sharaev GA (1993) Thermoimaging of the brain. J Neurosci Methods 46: 4957 11. Tchou S, Costich JF, Burgess RC, Wexler CE (1992) Thermographic observations in unilateral carpal tunnel syndrome: report of 61 cases. J Hand Surg 17A: 631637 12. Thomas D, Siahamis G, Marion M, Boyle C (1992) Computerised infrared thermography and isotopic bone scanning in tennis elbow. Ann Rheum Dis 51: 103107 13. Yang W, Zhang N, Yang PPT, Lin ZZ (1993) Determination of uterine activity during labor by means of infrared thermography. J Biomech Eng 115: 254256

References
1. Biagioni PA, Lamey P (1995) Electronic infrared thermography as a method of assessing herpes labialis infection. Acta Derm Venereol (Stockh) 75: 264268 2. Blume SS (1993) Social process and the assessment of a new imaging technique. Int J Technol Assess Health Care 9: 335345 3. Head JF, Wang F, Elliott RL (1993) Breast thermography is a noninvasive prognostic procedure that predicts tumor growth rate in breast cancer patients. Ann N Y Acad Sci 698: 153158

Surg Endosc (1997) 11: 11531158

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Video-laparoscopic staging of gastric cancer

A prospective multicenter comparison with noninvasive techniques
F. Asencio,1 J. Aguilo ,2 J. L. Salvador,3 A. Villar,1 E. De la Morena,4 M. Ahamad,1 J. Escrig,3 J. Puche,4 2 V. Viciano, G. Sanmiguel,1 J. Ruiz1
1 2

Hospital Hospital 3 Hospital 4 Hospital

Arnau de Vilanova, Valencia, Spain de Xa tiva, Valencia, Spain General, Castello n, Spain Marina Alta, Denia, Spain

Received: 5 May 1996/Accepted: 10 March 1997

Abstract Background: The high proportion of gastric carcinomas present in an unresectable stage, together with the emergence of multimodal treatments, increases the usefulness of objective staging methods that avoid unnecessary laparotomies. Methods: A prospective evaluation of the accuracy of laparoscopy in the staging of 71 patients with gastric adenocarcinoma is presented. Serosal infiltration, retroperitoneal fixation, metastasis to lymph nodes, peritoneal and liver metastasis, and ascites were determined in the staging workup. Sensitivity, specificity, and predictive values were calculated and compared with those obtained with ultrasonography (US) and computed tomography (CT). Results: The diagnostic accuracy of laparoscopy in the determination of resectability was 98.6%. Consequently, over 40% of patients were spared unnecessary laparotomies. Laparoscopy yielded diagnostic indices superior to US and CT for all the tumoral attributes studied. Our technique permits accurate assessment and pathologic verification of liver and the peritoneal and retroperitoneal extent of tumor invasion in the majority of patients. Conclusions: Laparoscopy in gastric adenocarcinoma is a reliable technique that provides accurate assessment of resectability and stage, thus avoiding unnecessary laparotomies in patients in whom surgical palliation is not indicated. A stepwise diagnostic workup combining imaging and minimally invasive techniques is proposed.

Key words: Stomach Cancer Staging Laparoscopy Resectability

An original article by the Grupo Inter-Hospitalario Valenciano (G.I.H.V). Presented in part at the 19th ESMO Congress, Lisbon, Portugal, 1994 Correspondence to: F. Asencio, Plaza Mestre Ripoll 9 dcha. 28a, 46022 Valencia, Spain

Surgical therapy still represents the treatment of choice for patients with primary gastric adenocarcinoma, but surgery may have reached its limits concerning the rate of resectability, mortality, and survival. Most gastric carcinomas are currently diagnosed in advanced tumor stages, 1550% of patients being unresectable [1113]. The high morbidity (1323%) and mortality rates (1036%) after laparotomy in unresected patients, together with the new palliation techniques for malignant dysphagia in cancer of the proximal stomach, have given a priority to avoiding inappropriate surgery [8, 10, 11]. On the other hand, higher response rates to new antitumoral combinations referred to in the literature [1, 12, 22] implicitly question the usefulness of objective staging methods that facilitate the preoperative assignment of patients to multimodal treatments. Despite the introduction of ultrasonography (US), computed tomography (CT), and magnetic resonance, imaging methods lack sufficient accuracy when dealing with gastric cancer, and the surgeon often faces a wide discrepancy between preoperative and intraoperative staging. Thus, exploratory laparotomy continues to be the only reliable staging method for gastric cancer currently available. With the introduction of surgical videocelioscopy, this technique is increasingly being appreciated as a valuable staging technique in a variety of gastrointestinal cancers, and high accuracy in the detection of intraabdominal metastases has been reported [7, 9, 10, 20]. Our primary objective is to evaluate the efficiency and safety of surgical laparoscopy in the staging and determination of resectability of gastric cancer patients deemed resectable by conventional imaging techniques. Addition-

1154

ally, the staging ability of laparoscopy is compared with these diagnostic methods. Patients and methods Patients
Between July 1992 and March 1995, all patients with biopsy-proven gastric adenocarcinoma admitted to four public hospitals in the Valencian Community were eligible for the study. Obviously unresectable lesions and patients who presented bleeding or gastric outlet obstruction requiring bypass procedures were excluded. All patients gave their informed consent before final inclusion in the study. Seventy-six patients with presumably resectable lesions after the performance of conventional imaging were prospectively included. Ultrasonography was performed in all patients and dynamic contrast-enhanced CT was additionally performed in 37. The restricted use of CT depended exclusively upon availability in different centers. Laparoscopy was performed in these 76 patients. Five patients were excluded from further study since they were finally not operated on at our institutions and/or entered neoajuvant chemotherapy programs that could influence postoperative tumor staging. Thus, 71 patients (43 men and 27 women) remained evaluable throughout the study.

culated for the three diagnostic procedures evaluated (US, CT, and laparoscopy) in two-way contingency tables of frequencies of positive and negative results constructed as either true or false upon surgical and histologic evaluation. To determine the diagnostic capability of laparoscopy in the investigation of tumors located in the proximal stomach and particularly in its posterior surface, true and false diagnosis of serosal and retroperitoneal invasion have been compared between upper third and not upper third lesions by means of the chi square test with Yates continuity correction.

Results Patients ranged in age from 47 to 81 years (mean: 65.8). Tumors were located in the lower third of the stomach in 19 patients (27%), in the middle third in 21 (30%), in the upper third in 12 (17%), in two-thirds in 16 (22%), and in the whole stomach in three (4%). The distribution of tumors by final stage (UICC-1987) was as follows: stage Ia: three (4.2%); stage Ib: two (2.8%); stage II: nine (12.7%); stage IIIa: 12 (16.9%); stage IIIb: 10 (14.1%); stage IV: 35 (49.3%). The complications of laparoscopy were minimal and most patients were discharged after 1 or 2 days if the procedure was performed independently. After laparoscopic staging, laparotomy was discarded in 29 (40.8%) cases due to advanced disease not previously proven by the other preoperative tests. The main reasons were peritoneal metastasis in 16 patients, malignant ascites in 15, liver metastases in 12, Krukenberg tumor in two, and retroperitoneal fixation in eight. Most unresectable patients were affected by the coexistence of more than one of these findings. The other 42 patients were deemed resectable. In one of these patients resection was finally not feasible due to retroperitoneal fixation of the tumor. Thus, the resectability rate, that is, the proportion of patients effectively undergoing either radical or palliative gastrectomy, was 57.7% (41 out of 71); 83% of these patients underwent curative surgery (UICC Ro) while 17% had palliative operations. The diagnostic accuracy of laparoscopy in determination of resectability was 98.6% (70 out of 71 cases). Table 1 presents the correspondence of laparoscopic stage with final stage. The overall proportion of correctly diagnosed stages was 80% (57 accurate, 14 down-staging, and 0 up-staging). Laparoscopic diagnosis of a stage I/II tumor presented a positive predictive value (PPV) of 53.8%. When laparoscopy determined a stage III tumor, PPV increased to 85.7%. The laparoscopic diagnosis of a stage IV tumor was 100% accurate (PPV 100). Table 2 presents the diagnostic indices of laparoscopy, with their confidence intervals, in relation to the major attributes used in the staging workup of gastric cancer. Laparoscopy yielded a statistically significant relationship with true diagnosis for all these attributes studied independently (p < 0.05). Laparoscopic biopsy correctly identified 40 of 52 serosa-positive cases, with 12 false negatives (FN) and no false positives (FP), offering a sensitivity of 76.9% and a specificity of 100%, a positive predictive value (PPV) of 100%, and a negative predictive value (NPV) of 47.8%. Laparoscopic nodal biopsy correctly identified 30 of 48 node-positive cases, with 18 FN and no FP, offering a sensitivity of 62.5% and a specificity of 100%, a PPV of 100%, and an NPV of 33.3%.

Laparoscopic technique
Laparoscopy was performed with general anesthesia, either as an independent procedure or before laparotomy. A maximum of three ports was used (umbilical, right and left of the midline). The visible surfaces of the stomach, liver, diaphragm, omentum, and peritoneal surfaces were systematically explored in search of malignant deposits and ascites. A second port permitted the introduction of a palpation probe. The combined inspection and probing provided an estimate of the tumoral extension within the stomach. Enlarged lymph nodes were also explored. By elevating the liver, the undersurface and the hepatoduodenal ligament were inspected. These maneuvers were aided by elevating the head of the operating table. Access to the lesser sac was obtained after dissecting a small opening at the greater omentum near the greater curvature, as described elsewhere [3]. The posterior wall of the stomach and the relationship of the tumor to retroperitoneal structures (i.e., pancreas) were assessed, thus determining its resectability. Finally, the pelvic cavity was examined by elevating the foot end of the table. The following attributes were determined in the staging workup: anatomical localization of the tumor, serosal infiltration, tumor fixation, metastasis to lymph nodes, peritoneal and liver metastasis, and ascites. To reduce operative risks and time, laparoscopic obtention of serosal and nodal biopsies and inspection of retrogastric area were considered essential only if relevant for the fulfillment of the primary objective (global stage and resectability). Otherwise it was left to the surgeons consideration. Upon laparoscopic evaluation, patients were considered eligible for surgery when conditions for tumor resection were present.

Analysis
TNM staging was accomplished after the UICC classification (1987). To simplify laparoscopic evaluation, stage I and II have been unified in a single I/II stage since its preoperative discrimination has currently no influence in decision-making. For an objective interpretation, the tumoral attributes evaluated were considered as true positives only after being confirmed by histopathologic examination (laparoscopic/laparotomic biopsy or surgical specimen). Negative findings were only considered as true negatives if the absence of tumoral invasion was confirmed at laparotomy or in the resected specimen. With the intention of doing evaluation, equivocal, failed, or otherwiseunfulfilled requirements were considered as negatives for statistical analysis. Diagnostic indices (i.e., sensitivity, specificity, and predictive values of positive and negative tests) and their 95% confidence intervals were cal-

1155 Table 1. Correspondence of laparoscopic stage with final stage: positive predictive values (PPV) with 95% confidence intervals Laparoscopic stage I + II Correct Down-staging PPV 95% C.I. Total 14 (53.8%) 12 (46.2%) 53.8 33.473.4 26 (100%) III 12 (85.7%) 2 (14.3%) 85.7 57.298.2 14 (100%) IV 31 (100%) 0 100 99.8100 31 (100%) Total 57 (80%) 14 (20%)

71 (100%)

Table 2. Diagnostic indices and 95% confidence intervals for attributes of gastric cancer as assessed by laparoscopy and confirmed by histology or laparotomy Predictive value Attribute Serosa Infiltration* Lymph node Metastasis* Liver Metastasis* Peritoneal Metastasis* Retroperitoneal Infiltration* Ascites* * p < 0.05 Patients 63 57 56 60 54 66 Positives 52 48 14 18 14 15 Sensitivity 76.9 63.187.5 62.5 47.376.1 100 76.8100 88.9 65.398.6 57.1 28.982.3 100 78.2100 Specificity 100 71.5100 100 66.4100 100 91.6100 100 91.6100 100 91.2100 100 93.0100 Positive 100 91.1100 100 88.4100 100 76.9100 100 79.4100 100 63.1100 100 78.2100 Negative 47.8 26.869.4 33.3 16.554.0 100 91.6100 95.5 84.599.4 87.0 73.795.1 100 93.0100

Liver metastases were accurately detected in all 14 patients with confirmed hepatic metastases, with no FNs and no FPs, offering a sensitivity and a specificity of 100% and a PPV and an NPV of 100%. Peritoneal implants were correctly identified and biopsied by the laparoscope in 16 of the 18 patients with demonstrated peritoneal metastases, with two FNs and no FPs, offering a sensitivity of 88.9% and a specificity of 100%, a PPV of 100%, and an NPV of 95.5%. The presence of ascitic fluid was correctly identified in all 15 patients with confirmed ascites, with no FN and no FP, offering results of 100% in all diagnostic indices. Cytological analysis detected malignant cells in 13 cases and was negative in two. Laparoscopic evaluation of the lesser sac correctly identified eight of 14 cases with proven retroperitoneal extension of the tumor, with six FNs and no FP, offering a sensitivity of 57.1% and a specificity of 100%, a PPV of 100%, and an NPV of 87% in determining retroperitoneal invasion. Table 3 presents the diagnostic indices of computed tomography. CT only demonstrated a statistically significant relationship with true diagnosis in the assessment of ascitic fluid (p < 0.05), while the accuracy for hepatic metastasis did not reach this significance. The results of ultrasonographic staging only demonstrated a statistically significant association (p < 0.05) with true diagnosis in the detection of liver metastases, presenting a sensitivity of 38.5% and a specificity of 100%, a PPV of 100%, and an NPV of 84.3%. With the association of both scanning techniques (US + CT), the diagnostic yield for all the attributes studied was not statistically improved.

Tables 46 compare the diagnostic indices obtained with the three different tests for the detection of lymph node, liver, and peritoneal metastases. No statistical differences could be found in the laparoscopic detection of serosal and retroperitoneal invasion in relation to tumor location (upper third vs not upper third).

Discussion Laparoscopy has been evaluated in the management of patients with gastric cancer with somewhat conflicting results. This procedure has been limited, for the most part, to evaluation of visible hepatic or peritoneal metastasis [10, 13]. It has thus been suggested that laparoscopy cannot permit an accurate evaluation of anatomical tumor extension. A paucity of reports (except for Russian authors) describing the utilization of laparoscopy for preoperative evaluation of gastric carcinoma supports this belief [4, 7, 10, 13, 17]. Currently, technological developments in laparoscopy facilitate surgical manipulations in the abdomen that could increase its diagnostic capabilities in gastric malignancies. Some recent reports seem to confirm this point [2, 15, 18]. As determined solely on the basis of laparoscopic evaluation, resectability success rate was 98.6%, an appreciable improvement when compared with the rate of 57.7% using standard staging methods (US, CT), and thus, 40.85% of patients with presumably operable gastric cancer were spared unnecessary laparotomies. Similar results are obtained by other authors [10, 13, 17]. In our experience, using the technique described in this

1156 Table 3. Diagnostic indices and 95% confidence intervals for attributes of gastric cancer as assessed by computed tomography and confirmed by histology or laparotomy Predictive value Attribute Serosa Infiltration Lymph node Metastasis Liver Metastasis Peritoneal Metastasis Retroperitoneal Infiltration Ascites* * p < 0.05 Patients 34 33 30 32 32 33 Positives 29 27 7 10 10 10 Sensitivity 69.0 49.184.7 66.7 46.083.5 28.6 3.771.0 0.0 30.0 6.765.2 30.0 6.765.2 Specificity 60.0 14.797.7 66.7 22.395.7 100 85.2100 90.9 70.898.9 100 85.2100 Positive 90.9 70.898.9 90.0 68.398.8 100 15.8100 60.0 14.794.7 100 29.2100 Negative 25.0 5.557.2 30.8 9.161.4 82.1 63.193.9 74.1 53.788.8 76.7 57.790.1

Table 4. Diagnostic indices and 95% confidence intervals of the three tests for the detection of lymph nodes Predictive value Test Laparoscopy (*) US CT * p < 0.05 Patients 57 57 33 Positives 48 48 27 Sensitivity 62.5 47.376.1 15.2 6.328.9 66.7 46.083.5 Specificity 100 66.4100 88.9 51.799.7 66.7 22.395.7 Positive 100 88.4100 87.2 47.499.7 90.0 68.398.8 Negative 33.3 16.554.0 17.0 7.630.8 30.8 9.161.4

Table 5. Diagnostic indices and 95% confidence intervals of the three tests for the detection of liver metastasis Predictive value Test Laparoscopy (*) US* CT * p < 0.05 Patients 56 56 30 Positives 14 14 7 Sensitivity 100 76.8100 38.5 13.968.4 28.6 3.771.0 Specificity 100 91.6100 100 91.8100 100 85.2100 Positive 100 76.9100 100 47.8100 100 15.8100 Negative 100 91.6100 84.3 71.493.0 82.1 63.193.9

report, an accurate assessment of TNM stage can be obtained by laparoscopy. Nevertheless, laparoscopic diagnosis of a stage I/II tumor has little more than a 5050 chance of being correct (like flipping a coin, for instance). This diagnostic capability increases when a stage III tumor is detected (5798%) and yields absolute accuracy when laparoscopy identifies a stage IV tumor. The imperative of histologic confirmation for stage determination eliminates the incidence of errors due to up-staging. The technique performs best for the determination of liver and peritoneal metastases as well as for the detection of small amounts of ascitic fluid that can be collected for cytological examination. This accuracy decreases in the assessment of serosal affection and nodal infiltration. Nevertheless, the visually guided biopsy of these targets renders absolute specificity, thus permitting accurate decision mak-

ing in biopsy-positive cases. Similar experiences have been reported recently [19, 21]. The limitations of the technique are currently due to the presence of adhesions in the supramesocolic area (i.e., carcinoma of the gastric stump). Three patients could not be properly evaluated by laparoscopy due to internal adhesions of previous abdominal operations, including the single error in laparoscopic determination of resectability. When imaging techniques are revised in the literature [5, 11, 13, 17, 21], the high accuracy for liver metastases falls in the presence of small superficial lesions. This was the case in our study, since all patients presented presumably resectable lesions after conventional preoperative staging. Ozarda [16] has shown that 11% of patients with hepatic metastases fail to present them on the surface of the organ. These lesions will probably pass unseen by laparoscopy, as

1157 Table 6. Diagnostic indices and 95% confidence intervals of the three tests for the detection of peritoneal metastasis Predictive value Test Laparoscopy (*) US CT * p < 0.05 No. patients 60 60 32 No. positives 18 18 10 Sensitivity 88.9 65.398.6 6.3 0.230.2 0.0 Specificity 100 91.6100 100 91.6100 Positive 100 79.4100 100 Negative 95.5 84.599.4 73.7 60.384.5

well as by exploratory laparotomy, without the aid of intraoperative (or laparoscopic) ultrasonography [2]. Peritoneal metastases are almost undetectable by imaging techniques; and their presence usually precludes gastric resection. In our experience, both types of lesions were almost systematically detected by laparoscopy. The degree of posterior fixity of the tumors is described as difficult to assess by laparoscopic examination, most false-negative results being due to the posterior extension of the tumor [10, 13]. With the use of surgical laparoscopy, the technique described permits accurate assessment of the retroperitoneal extent of tumor invasion. Laparoscopy could also be an appropriate method by which to determine tumoral response to chemotherapy; conventional staging methods are currently inaccurate. Effectiveness of different therapeutic regimens could be more accurately compared, and current discrepancies could be thus obviated. The theoretical risk for tumor spreading after diagnostic laparoscopy reported in the literature [6] was accepted because all patients with positive biopsies underwent postoperative or neoadjuvant (excluded from analysis) chemotherapy treatments. Considering the invasive condition of laparoscopy, although clearly underutilized for gastric cancer staging, this procedure might not be practical for this purpose in all cases. Endoscopic ultrasound (EUS) is now regarded as most accurate in the preoperative determination of the degree of gastric wall infiltration [15, 18] and could play an important role in patient preselection for staging laparoscopy. A stepwise diagnostic workup combining imaging and minimally invasive techniques could be a reasonable approach for gastric cancer in the future, as recommended by Sendler [18]. After diagnosis by endoscopy and biopsy, imaging techniques (US/CT) and guided needle biopsies would represent the first line in staging. For patients without obviously advanced disease, further selection could be facilitated by EUS. Tumors regarded as T1T2 by EUS would undergo straight forward laparotomy. Considering that T3 tumors have 88% positive lymph nodes [14] and that the peritoneal cavity is an important failure site for patients who have either T3 or T4 lesions, this subgroup would be selected for staging laparoscopy.

thus obviating unnecessary laparotomies in patients in whom surgical palliation is not indicated. If evidence of inoperability is equivocal, accurate diagnosis of metastatic involvement requires histologic confirmation before a patient is denied potentially curative surgical treatment. In our experience, laparoscopic guided biopsies permit this confirmation in most patients. In addition, TNM staging could facilitate the assignment of patients to preoperative (neoadjuvant) treatment schedules in controlled studies or the assessment of tumoral response to multimodal antitumoral therapies. When compared with computerized tomography and ultrasound, laparoscopic diagnosis was superior in assessing all tumoral attributes tested in the study. The most convenient timing for staging laparoscopy (preoperative vs independent procedures) as well as the potential hazards of the method, such as free tumor cell implantation into the abdominal wall, should be determined with further experience.
Acknowledgments. Thanks are due to S. Pero, M.D., from the Valencian Institute for Studies in Public Health (IVESP), for his revision of the manuscript and for his scientific counseling.

References
1. Ajani J, Mansfeld P, Ota D (1995) Potentially resectable gastric carcinoma: current approaches to staging and preoperative therapy. World J Surg 19: 216220 2. Anderson D, Campbell S, Park K (1996) Accuracy of laparoscopic ultrasonography in the staging of upper gastrointestinal malignancy. Br J Surg 83: 14241428 3. Asencio Arana F (1994) Laparoscopic access to the lesser sac in gastric cancer staging. Surg Laparosc Endosc 4: 438440 4. Boliukh B, Alekseev V (1992) Exploratory laparoscopy in stomach cancer. Klin Khir 910: 5455 5. Colin-Jones D, Rosch T, Dittler H (1993) Staging of gastric cancer by endoscopy. Endoscopy 25: 3438 6. Cook T, Dehn T (1996) Port-site metastases in patients undergoing laparoscopy for gastrointestinal malignancy. Br J Surg 83: 14191420 7. Cuesta MA, Meijer S, Borgstein P (1992) Laparoscopy and assessment of digestive tract cancer. Br J Surg 79: 486487 8. Geoghegan JG, Keane TE, Rosenberg IL, Dellipiani AW, Peel AL (1993) Gastric cancer: the case for a more selective policy in surgical management. J R Coll Surg Edinb 38: 208212 9. Greene F (1992) Laparoscopy in malignant disease. Surg Clin North Am 72: 11251137 10. Gross E, Bancewicz J, Ingram G (1984) Assessment of gastric cancer by laparoscopy. Br Med J 288: 1577 11. Hallisey M, Allum W, Roginski C, Fielding J (1988) Palliative surgery for gastric cancer. Cancer 62: 440444 12. Kiyabu M, Leichman L, Chandrasoma P (1992) Effects of preoperative chemotherapy on gastric carcinoma. Cancer 70: 22392245

Conclusions Laparoscopic staging of gastric adenocarcinoma is a reliable technique that provides accurate assessment of resectability,

1158 13. Kriplani AK, Kaput BM (1991) Laparoscopy for pre-operative staging and assessment of operability in gastric carcinoma. Gastrointest Endosc 37: 441443 14. Maruyama K, Gunven P, Okabayashi K, Sasako M, Kinoshito T (1989) Lymph node metastases in gastric cancer. Ann Surg 210: 596 15. OBrien M, Fitzgerald E, Lee G, Crowley M, Shanahan F, OSullivan G (1995) A prospective comparison of laparoscopy and imaging in the staging of esophagogastric cancer before surgery. Am J Gastroenterol 90: 21912194 16. Ozarda A, Pickren J (1962) The topographic distribution of liver metastases: its relation to surgical and isotope diagnosis. J Nucl Med 3: 149152 17. Possik R, Franco E, Pires D, Wohnrath D, Ferreira E (1986) Sensitivity, specificity, and predictive value of laparoscopy for the staging of gastric cancer and for the detection of liver metastases. Cancer 58: 16 18. Sendler A, Dittler H, Feussner H, Nekarda H, Bollschweiler E, Fink U, et al. (1995) Preoperative staging of gastric cancer as precondition for multimodal treatment. World J Surg 19: 501508 Tognarelli B, Blanc P, Peray P, Galindo G, David XR, Rouillon JM (1993) The value of laparoscopy in the staging of digestive system cancers. Ann Gastroenterol Hepatol (Paris) 29: 229232 Warshaw A, Gu Z, Wittenberg J, Waltmann A (1990) Preoperative staging and assessment of resectability of pancreatic cancer. Arch Surg 125: 230233 Watt I, Stewart I, Anderson D, Bell G, Anderson J (1989) Laparoscopy, ultrasound and computed tomography in cancer of the oesophagus and gastric cardia: a prospective comparison for detecting intraabdominal metastases. Br J Surg 76: 10361039 Wilke H, Preusser P, Fink U (1990) New developments in the treatment of gastric carcinoma. Semin Oncol 17 (Suppl 2): 6170 Zakharov S, Kutepov V, Kalachev V (1988) Possibilities of laparoscopy in the diagnosis of disseminated cancer of the stomach. Klin Khir 5: 3738

19. 20. 21.

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Surg Endosc (1997) 11: 11831188

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Tailored augmentation of the lower esophageal sphincter in experimental antireflux operations

S. M. Freys, K. H. Fuchs, J. Heimbucher, A. Thiede
Department of Surgery, University of Wu rzburg, Josef-Schneider-Str. 2, D-97080 Wu rzburg, Germany Received: 29 January 1997/Accepted: 2 April 1997

Abstract Background: Modern upper GI function studies allow for the detection of several pathophysiological factors that contribute to gastroesophageal reflux disease. The information obtained can lead to therapeutic consequences in patients with an indication for a surgical intervention, i.e., an individualized choice of antireflux procedure according to the existing pathophysiologic defect. Methods: In an experimental study on mini-pigs the mechanical effect of four standardized antireflux operations (anterior and posterior 180 hemifundoplication, NissenDeMeester and Nissen-Rossetti 360 fundoplication) on the lower esophageal sphincter (LES) was investigated. It was the aim of the study to objectively determine the extent of changes in pressure and length parameters at the LES according to the performed antireflux procedure. Results: It could be demonstrated that different degrees of fundic wrap formation lead to a proportional mechanical effect at the LES according to the size of this wrap. Conclusion: Choosing a distinct type of fundoplication will allow for a tailored augmentation of the LES according to the individual functional defect. Key words: Gastroesophageal reflux disease Surgical therapy Antireflux operations Lower esophageal sphincter Experimental study

Gastroesophageal reflux disease (GERD) is a multifactorial process [5, 15]. The most important functional defect that seems to be involved concerns the high-pressure zone in the distal esophagus. This high-pressure zone functions as a reflux barrier which is in many publications nominated the lower esophageal sphincter (LES) [7, 31, 39]. The recent improvement and understanding in the pathophysiology of
Correspondence to: S. M. Freys

the disease [15, 29] as well as the establishment of laparoscopic techniques in GERD has made surgical therapy more attractive for patients [4, 5]. Surgical therapy focuses on the mechanical augmentation of the high-pressure zone in the distal esophagus. Even though a great variety of antireflux procedures have been developed over the past 2030 years it seems obvious that wrapping the fundus of the stomach in a total or a partial circumference around the high-pressure zone of the distal esophagus leads to an improvement of the reflux barrier function at the esophagogastric junction. This improvement can be observed with a full fundic wrap such as a Nissen fundoplication, with a partial fundic wrap such as the Belsey Mark IV procedure, with the positioning of an Angelchick antireflux procedure, and with a posterior gastropexy such as the Hill repair. The assessment of the functional changes comparing the postoperative manometric results is difficult since these operations are usually performed in different institutions on different patient populations by many surgeons. Some comparative studies, even randomized trials, have shown that there seems to be no difference in the mechanical effect on the antireflux barrier between full and partial wraps [23]; others have shown a stronger mechanical augmentation with a full fundoplication [8]. At present there is an ongoing controversial discussion over whether to tailor shape the mechanical augmentation of a defective LES by using, in some patients, a 360 fundoplication and in other patients a partial wrap [14, 20, 22]. The extent of the augmentation is not only important for the antireflux effect, since it may also cause side effects for the patients, especially postoperative bloating and persistent dysphagia [1]. The purpose of this study was to assess the mechanical action of different antireflux procedures in order to evaluate whether different principles of operative augmentation at the esophagogastric junction can lead to a modulation of the exerted mechanical effect in a standardized fashion. The answer to this question could be the basis for a discussion of whether it is useful to create a tailor-shaped augmentation of the LES according to the individual functional defect.

1184

Materials and methods Study protocol

Four antireflux procedures were performed on 28 mini-pigs (four groups of seven animals each). Immediately pre- and postoperatively and 2 months postoperatively an esophagogastroduodenoscopy and an esophageal manometry were performed. Surgery and investigations were performed in the Experimental Laboratory at the Department of Surgery of Wu rzburg University. The study protocol was approved and a written consent was given by the Committee on Animal Research of the Government of Unterfranken, Wu rzburg, according to the German Law on the Protection of Animals.

Selection and preparation of animals

Healthy mini-pigs with a body weight of 2362 kg were used. All animals underwent a veterinary examination prior to the study. The diet consisted of dry food and water. Three days prior to the investigations and operations the animals were fed with Fresubin (Fresenius, Inc.) and water, and finally on the last day only water was allowed. This standardized regimen allowed for an empty upper GI tract during the endoscopic investigations prior to manometry and operation. Immediately before the investigations the animals were sedated using a 600-mg i.m. injection of azaperon. All investigations and operations were performed under general anesthesia with intubation and ventilation (thiopental-natrium: 5 mg per kg bodyweight, N2O: 2.5 l per minute, O2: 0.65 l per minute). The animals were positioned and fixed in a supine position on an operation table.

Endoscopy
An endoscopic inspection of the upper GI tract was performed prior to any investigation and operation. A PQ 20 gastroscope (Olympus Inc.) was used. On the one hand, this investigation was performed to rule out any existing pathology, to check whether the upper GI tract was emptied, and postoperatively, to visually control the operative result. On the other hand, the endoscopy was used to position a guide wire in the stomach which then served as a path finder for the manometry probe used for esophageal manometry.

Esophageal manometry
All pre- and postoperative esophageal manometries were performed with a perfusion system according to a standardized protocol using the DeMeester criteria for characterization of the LES [13, 39]. Motility studies were performed using a water-perfused, low-compliance manometry system with a 170-cm five-channel catheter and an eight-channel catheter. The distance between channel openings was 5 cm in the five-channel catheter; in the eight-channel catheter the openings were on the same level. The perfusion was performed with distilled water at a rate of 0.5 ml per minute and channel. All investigations were recorded on a computerized system (Polygraf HR, Synectics, Inc., Frankfurt, Germany) and the analysis was performed with a commercially available software system (Polygram, Gastrosoft, Inc., Irvine, Texas, USA). During each motility study a station-tostation pull-through was performed with the five-channel catheter at a pace of 1 cm per 30 s. With this investigation the total length, the intraabdominal length, and the resting pressure of the LES were measured. The second part of each motility study consisted of a rapid motorized pull-through using the eight-channel catheter at a pace of 0.5 cm per second. This investigation allowed for the computerized calculation of the sphincter pressure vector volume using the above-mentioned software [30].

The laparoscopic access was equal in all operations using five trocars in the midabdomen: After establishment of the pneumoperitoneum using a Veress needle, a 10-mm optic was inserted via a left paraumbilical trocar. Four further 10-mm trocars were subsequently inserted into the abdomen under direct vision. The liver retractor was inserted through the right lateral trocar. The gastric fundus was then pulled laterocaudally using a grasping forceps through the left lateral trocar. The two other paramedian trocars were used for active operating instruments. Following a visual inspection the peritoneum and phrenicoesophageal membrane were incised and the LES was dissected from left to right, leading to a complete exposure of the anterior aspect of the sphincter. Subsequently the LES was dissected dorsally, allowing for a complete mobilization of the distal esophagus with careful identification of both vagal nerves. Before the performance of the actual fundoplication a posterior hiatoplasty was carried out in all cases using one nonabsorbable stitch. Thus, the dissection of the LES region was identical in all four procedures. During the anterior 180 hemifundoplication the fundic wrap was pulled to the right side in front of the distal esophagus. It was subsequently sutured to the left lateral aspect of the LES with a single stitch. Two further stitches were used for a fixation of the fundus at the LES, and finally, two stitches were performed to fixate the anterior aspect of the fundic wrap on the right crus of the diaphragm. During the posterior 180 hemifundoplication according to Toupet the dorsal part of the fundic wrap was pulled through behind the esophagus from left to right. This dorsal part of the fundic wrap was then sutured with two single stitches to the right crus of the diaphragm starting just above the hiatoplasty. The posterior wrap was additionally fixed with two single stitches each between the fundic wrap and the right as well as the left border of the LES. During the 360 fundoplication according to Nissen-DeMeester the dorsal part of the fundic wrap was pulled through behind the esophagus from left to right, creating a symmetric wrap of a dorsal and anterior fundic flap around the LES; then the short and floppy 360 wrap was positioned at the LES using the posterior and the anterior fundic flap by running a single U suture through both flaps and the right lateral aspect of the esophageal wall. In order to enforce this suture, 1-cm absorbable pledgets (Ethisorb) were used on each side of the fundic flaps underneath the stitches. During the 360 fundoplication according to Nissen-Rossetti a similar procedure was performed as during the Nissen-DeMeester version; however, in this case the wrap was longer, with four single stitches between the upper and the lower aspect of the fundus and two further single stitches between the anterior part of the fundic wrap and the anterior wall of the stomach. Nonabsorbable sutures (Seralene, Serag-Wiessner Inc., Naila, Germany) were used during all procedures. During the performance of the actual fundoplication a 9-mm tube was passed into the esophagus to allow for a calibration of the cardia. At the end of each procedure the abdomen was desufflated and the 5 trocar incisions were closed with 2 absorbable stitches each.

Postoperative investigations
Following each operation esophageal manometry was immediately performed in each animal. Oral feeding was started on postoperative day 1 and i.v. fluids were discontinued. All animals were kept under observation in our animal house for the period of 1 week with daily visits. Subsequently the animals returned to a farm until 2 months following each operation, when a follow-up endoscopy and manometry were performed in the Experimental Laboratory under general anesthesia according to the abovementioned protocol and the animals were subsequently sacrificed. For each investigated group the median, minimum, and maximum values of the four measured manometric parameters were calculated. A statistical comparison between the values of the individual pigs and between groups was performed according to their nature using the Wilcoxon Rank Sum Test for paired and unpaired values.

Antireflux procedures
All antireflux operations were performed laparoscopically. Four types of operations were performed on seven animals each: (1) anterior 180 hemifundoplication [14], (2) posterior 180 hemifundoplication according to Toupet [35], (3) 360 fundoplication according to Nissen-DeMeester [6], and (4) 360 fundoplication according to Nissen-Rossetti [27].

Results According to the study protocol, 28 mini-pigs were investigated successfully: following endoscopy and esophageal manometry the antireflux procedure was performed, imme-

1185 Table 1. Manometric characteristics of the LES in the mini-pig (serving as normal preoperative values) Manometric characteristics LES LES LES LES total length, cm intraabdominal length, cm resting pressure, mmHg pressure vector volume, mmHg2cm Median 3 1 5 506 Range 25 03 116 1292,212

diately followed by a control manometry and 2 months postoperatively by a control endoscopy and esophageal manometry. Preoperative investigations There were no pathologic findings in any of the animals on endoscopic inspection. The preoperative diet successfully led to an emptied upper GI tract, allowing for comparable conditions in all animals. The median values of the four parameters gathered from each preoperative esophageal manometry serving as normal values for the investigated animals are listed in Table 1. Operative data The operative time for all procedures ranged between 35 and 90 min. In six of the 28 animals we encountered intraoperative problems: In two animals of the anterior hemifundoplication group, one animal of the Nissen-DeMeester group, and two animals of the Nissen-Rossetti group, bleeding from the spleen occurred, which in each case could be treated by electrocoagulation. In one animal of the posterior hemifundoplication group a left-sided pneumothorax was detected intraoperatively. It was treated by insertion of a chest drain which could be extracted on extubation. The postoperative course in all animals was uneventful with no complications. Postoperative investigations The follow-up endoscopies 2 months after each operation did not show pathologic findings in any of the 28 investigated animals. There were no signs of a loosening of the wrap in any case. The manometric characteristics of LES competence were gathered for each animal immediately postoperatively and 2 months after the operation. Figure 1 delineates the course of the median values of these parameters. The graphs show that following all four antireflux procedures we found higher median values for the sphincter characteristics immediately postoperatively as compared to the 2-month values, probably due to postoperative tissue edema. When comparing the preoperative values of the LES characteristics with the values obtained 2 months postoperatively in each individual animal, we found the differences listed in Table 2. A better impression can be obtained regarding the relative change of the four manometric LES characteristics, i.e., the percentage increase of the postoperative values individually related to the preoperative values. The median val-

ues of this kind of representation of the obtained measurements are depicted in Fig. 2. Significant differences between the four operative groups with regard to the relative change of LES characteristics could only be found for LES intraabdominal length between both 360 fundoplications and the anterior 180 hemifundoplication (p < 0.03) and for LES pressure vector volume between both 360 and both 180 procedures (p < 0.01). These results can be summarized as follows: There is an immediate rise in all LES function characteristics; 2 months after the operation this edema effect has waned and the true mechanical effect of the fundoplication is measured. LES total length increases after all four procedures; however, it is statistically significant only after the NissenRossetti fundoplication. LES intraabdominal length is unaltered by the two hemifundoplications and doubled by both 360 procedures. LES resting pressure is significantly increased by all four operations. LES pressure vector volume is also significantly increased after all four fundoplications with increasing degrees proportional to the size of the wrap.

Discussion This experimental study focused on an optimal standardized comparison of different antireflux procedures to learn about the precise mechanical consequences that a surgeon can cause when applying these procedures. The rationale for our investigation is the frequently reported, troublesome side effects of antireflux operations such as dysphagia and gas bloat, as well as the (current discussion on the) usefulness of a tailored approach. Several factors contributed to the choice of the mini-pig as animal model. The ideal of an erect moving animal model is currently not available for ethical and economic reasons. The mini-pig offers a high degree of anatomical and physiologic congruence with the human conditions [26]. For these reasons it has already been used as an established model for physiologic investigations of the LES [19]. Further reasons for choosing this animal model, especially with regard to standardization, were availability, technical feasibility, and relativity of the planned procedures with regard to the subjective impairment of the individual animal. Due to the aforementioned anatomic and physiologic congruence to the human condition it was possible to perform the planned procedures (endoscopy, perfusion manometry, laparoscopic antireflux procedures) according to the same protocols and using the same instruments as are standard in the treatment of patients. A possible reservation regarding the use of an animal model was that operative procedures designed to treat pathologic conditions would be applied on healthy subjects presenting physiologic conditions. However, a sufficient comparison of different operative techniques is only possible with the prerequisite of constant starting conditions, which, in the case of this animal model are guaranteed by the physiologic structures of the esophagogastric junction. Four different antireflux procedures were chosen from the large spectrum of available operations. Their choice is explained by the fact that these four represent the clinically most established operations; hence, they can be performed with an appropriate amount of standardization. On the other

1186

Fig. 1. Course of manometric LES characteristics.

Fig. 2. A Relative change of manometric LES characteristics (pre-op. vs 2 months postop.). B Relative change of manometric LES characteristics (pre-op. vs 2 months postop.). Table 2. Comparison of pre- and postoperative values of the manometric LES characteristicsa Fundoplication Anterior 180 Posterior 180 Nissen-DeMeester Nissen-Rossetti
a

LES total length n.s. n.s. n.s. p < 0.04

LES intraabdominal length n.s. n.s. p < 0.04 n.s.

LES resting pressure p p p p < < < < 0.02 0.001 0.02 0.02

LES pressure vector volume p p p p < < < < 0.02 0.001 0.02 0.02

n.s. no statistical significant difference, p < significance value

hand, these operations should have a different mechanical action at the esophagogastric junction: two procedures involving the formation of a 360 wrap each having a different wrap length and two procedures with a 180 wrap, each presenting a different positioning and anchoring of the wrap at the esophagogastric junction. The 360 fundoplication according to Nissen-Rossetti was chosen since it represents the standard procedure worldwide. The second 360 procedure is the DeMeester modification of the Nissen procedure.

This modification had been established in order to reduce the ratio of postoperative problems such as dysphagia, gas bloat, and dumping syndrome. This modified version is currently routinely applied in several centers very successfully [4, 5, 12, 14]. The anterior 180 fundoplication and the posterior 180 fundoplication according to Toupet were chosen as hemifundoplications. Both procedures lead to a partial augmentation of the LES region requiring only a little mobilization of the fundus. The Toupet technique rep-

1187

resents a rather comprehensive procedure with positioning and fixation of the fundic wrap behind the esophagus on the right crus and on the right and left border of the esophagus. The manometric results of the experimental antireflux procedures show a rather uniform trend if comparing the immediate postoperative motility studies with the studies after 2 months: The median values of the four LES parameters were uniformly higher right after the operation than after 2 months. This finding can be explained by the tissue edema secondary to the operative trauma at the esophagogastric junction which had resolved after 2 months. Both partial fundoplications lead to rather similar mechanical changes at the LES: The LES total length increases slightly more with the posterior hemifundoplication according to the extent of dissection if compared with the anterior hemifundoplication. Neither procedure leads to a change in the intraabdominal LES length. The LES resting pressure increases slightly more following the posterior if compared to the anterior version, most probably because of a slight kinking phenomenon secondary to the posterior localization of the wrap and a concomitant ventralization of the esophagus. Following both 360 fundoplications a different situation is encountered, as expected: While the Nissen-Rossetti technique leads to a distinct prolongation of the LES total length (60%), the modified DeMeester technique with a short floppy wrap leads to a rather small increase of LES total length (25%) comparable to that following the anterior 180 hemifundoplication. However, both 360 wraps lead to a secure intraabdominal position of the LES region with a doubling of the intraabdominal LES length in both groups. Looking at the LES resting pressure increases we again find differences in both techniques: The Nissen-Rossetti technique leads to a doubling of the resting pressure, while the modified technique with the loose and floppy wrap leads to a pressure increase (75%) corresponding to that of the posterior hemifundoplication. The change of the manometrically determined LES characteristics can be thought of as the mechanical effect being exerted by an antireflux procedure. This mechanical effect can be measured best by means of the LES pressure vector volume. It is equivalent to the quantitative measure for the resistance put up by a sphincter against a passing particle. The comparison of the median values of the LES pressure vector volume demonstrates the different potencies of the antireflux procedures: The higher the degree of wrap formation, i.e., the more complex the anchoring mechanism at the esophagogastric junction, the more distinct is its mechanical effect. The weakest augmentation is achieved by the anterior hemifundoplication. A stronger reconstruction can be performed with the posterior hemifundoplication due to the complex fixation of the fundic wrap behind the esophagus, which also leads to an increase in LES total length. The Nissen-DeMeester procedure with the 360 wrap leads to a further increased mechanical reconstruction which finally reaches maximum values with the NissenRossetti technique because of the rather complex long and tight wrap formation. The historic development of antireflux surgery is characterized by a multitude of different techniques, which individually have been propagated by surgical schools. Consequently the experience in antireflux surgery was restricted

at different centers usually to one school operation. With developing knowledge on the pathophysiologic background of GERD, surgeons are gradually becoming aware of the fact that the choice of operation should no longer follow only the school opinion but rather be based on wellassessed and widely accepted data as well as on the individual functional defect causing GERD [9, 14]. In the current literature 21 studies report on manometric investigations before and after antireflux operations: From eight retrospective studies we find five reporting on the Nissen fundoplication [10, 18, 24, 25, 36], one on the Collis operation [28], one on the Belsey operation [21], and finally one on a comparison of the Nissen and Belsey techniques [32]. Five prospective studies investigate the Nissen, Hill, and Watson procedures [13, 11, 38]. Finally there are eight prospective randomized studies that compare the Nissen procedure with a second (2 Angelchik [17, 33], 3 Toupet [22, 23, 34], 1 Lind [37]) or with two further operative techniques (1 Belsey and Hill [8], 1 Toupet and LortatJacob [16]). The results of these comparative studies do not allow for a general recommendation on the individual procedures. Three studies report on advantages in applying the Nissen fundoplication [16, 17, 33], two studies rather favor the Toupet technique [22, 34], and three studies see no differences in the compared techniques [8, 23, 37]. A general recommendation on the best antireflux procedure seems therefore not possible, since the spectrum of possible causal factors and their combinations cannot be corrected by one standard operative procedure. There also remains a controversial discussion in the future on whether to use a partial or full wrap. In order to evaluate the applicability of the tailored operative concept it is necessary to obtain precise data on the preoperative status and on the mechanical effect being exerted by a distinct antireflux procedure. From the surgical technical point of view and from recent reports [14, 20, 23, 38] it appears that the mechanical effect at the esophagogastric junction can be well tailored according to the chosen operative procedure. However, a final judgment on whether a specific antireflux procedure is superior to another can only be answered by long-term patient follow-up. We conclude from our results that standardized antireflux operations with different degrees of fundic wrap formation can lead to a proportional mechanical effect at the LES according to the size of this wrap. Choosing a distinct type of fundoplication with a determined mechanical effect will allow for a tailored augmentation of the LES. Thus, it will be possible to offer GERD patients with an indication for an operative therapy the option of an antireflux procedure tailored according to the individual functional defect. References
1. Ackermann C, Margreth L, Muller C, Harder F (1988) Das Langzeitresultat nach Fundoplication. Schweiz Med Wochenschr 118: 774 2. Bell RCW, Hanna P, Powers B, Sabel J, Hruza D (1996) Clinical and manometric results of laparoscopic partial (Toupet) and complete (Rossetti-Nissen) fundoplication. Surg Endosc 10: 724 3. Csendes A, Braghetto I, Korn O, Corte s C (1989) Late subjective and objective evaluations of antireflux surgery in patients with reflux esophagitis: analysis of 215 patients. Surgery 105: 374 4. Cuschieri A (1993) Laparoscopic antireflux surgery and hiatal hernia repair. World J Surg 17: 40

1188 5. Dallemagne B, Weerts JM, Jehaes C, Markiewicz S (1996) Causes of failures of laparoscopic antireflux operations. Surg Endosc 10: 305 6. DeMeester TR, Bonavina L, Albertucci M (1986) Nissen fundoplication for gastroesophageal reflux disease. Evaluation of primary repair in 100 consecutive patients. Ann Surg 204: 19 7. DeMeester TR (1987) Definition, detection and pathophysiology of gastroesophageal reflux disease. In: DeMeester TR, Matthews HR (eds) International trends in general thoracic surgery. Benign Esophageal Disease. CV Mosby, St Louis, p 99 8. DeMeester TR, Fuchs KH (1988) Comparison of operations for uncomplicated reflux disease. In: Jamieson GG (ed) Surgery of the oesophagus. Churchill Livingstone, Edinburgh, p 299 9. DeMeester TR, Stein HJ, Fuchs KH (1991) Diagnostic studies in the evaluation of the esophagus: physiologic diagnostic studies. In: Orringer MB (ed) Shackelfords surgery of the alimentary tract. 3rd ed. WB Saunders, Philadelphia, p 94 10. Ellis FH Jr (1985) Nissen fundoplication: a clinical and manometric assessment of results. In: DeMeester TR, Skinner DB (eds) Esophageal disorders: pathophysiology and therapy. Raven Press, New York, p 197 11. European Study Group of Antireflux Surgery (ESGARS) Current status and trends in laparoscopic antireflux surgery. Endoscopy (in press) 12. Feussner H, Siewert JR (1992) Hat die Antirefluxchirurgie noch eine Indikation?aus chirurgischer Sicht. Chir Gastroenterol 8: 184 13. Freys SM, Heuer-Jo hnk U (1991) In: Fuchs KH, Hamelmann H (eds) Gastrointestinale Funktionsdiagnostik in der Chirurgie. Praktischer sophagusmanometrie. Blackwell, Berlin, p 255 Kurs: Stationa re O 14. Fuchs KH, Heimbucher J, Freys SM, Thiede A (1994) Management of gastro-esophageal reflux disease 1995. Tailored concept of anti-reflux operations. Dis Esoph 7: 250 15. Fuchs KH, Freys SM, Heimbucher J, Fein M, Thiede A (1995) Pathophysiologic spectrum in patients with gastroesophageal reflux disease in a surgical GI-function laboratory. Dis Esoph 8: 211 16. Hay JM, Zeitoun G, Segol Ph, Pottier D (1990) Surgical treatment for gastroesophageal reflux: which procedure is the best? In: Little AG, Ferguson MK, Skinner DB (eds) Diseases of the esophagus, vol II: benign diseases. Futura, Mount Kisco, NY, p 189 17. Hill ADK, Walsh TN, Borger CM, Byrne PJ, Hennessy TPJ (1994) Randomized controlled trial comparing Nissen fundoplication and the Angelchick prosthesis. Br J Surg 81: 72 18. Johansson J, Johnsson F, Joelsson B, Flore n CH, Walther B (1993) Outcome 5 years after 360 fundoplication for gastro-oesophageal reflux disease. Br J Surg 80: 46 19. Johnsson F, Joelsson B (1985) Mechanical and physiologic properties of the distal esophageal sphincter: a study in the piglet. In: DeMeester TR, DB Skinner (eds) Esophageal disorders: pathophysiology and therapy. Raven Press, New York, p 35 20. Kauer WK, Peters JH, DeMeester TR, Heimbucher J, Ireland AP, Bremner CG (1995) A tailored approach to antireflux surgery. J Thorac Cardiovasc Surg 110: 141146 21. Lerut T, Coosemans W, Christiaens R, Gruwez JA (1990) The Belsey Mark IV antireflux procedure: indications and long-term results. In: Little AG, Ferguson MK, Skinner DB (eds) Diseases of the esophagus, vol II: benign diseases. Futura, Mount Kisco, NY, p 181 22. Lundell L, Abrahamsson H, Magnus R, Sandberg N, Olbe LC (1991) Lower esophageal sphincter characteristics and esophageal acid exposure following partial or 360 fundoplication: results of a prospective, randomized, clinical study. World J Surg 15: 115 23. Lundell L, Abrahamsson H, Ruth M, Rydberg L, Lo nroth H, Olbe L (1996) Long term results of a prospective randomized comparison of total fundic wrap (Nissen-Rossetti) or semifundoplication (Toupet) for gastro-oesophageal reflux. Br J Surg 83: 830 24. Luostarinen M, Isolauri J, Laitinen J, Koskinen M, Keyrilainen O, Markkula H, Lahtinen E, Uusitalo A (1993) Fate of Nissen fundoplication after 20 years. A clinical, endoscopical, and functional analysis. Gut 34: 1015 25. Martinez de Haro L, Parilla Paricio P, Ortiz Escandell MA, Morales Cuenca G, Videla Troncoso D, Cifuentes Tebar J, Garax Pelegrin V (1992) Antireflux mechanism of Nissen fundoplication. Scand J Gastroenterol 27: 417 26. Nickel R, Schummer A, Seiterle E (1987) Lehrbuch der Anatomie der Haustiere. Paul Parey Verlag, Band III, p 147 ff 27. Nissen R (1956) Eine einfache Operation zur Beeinflussung der Refluxoesophagitis. Schweiz Med Wochenschr 86: 590 28. Orringer MB (1985) The combined Collis-gastroplasty-Nissen fundoplication for gastroesophageal reflux. In: DeMeester TR, Skinner DB (eds) Esophageal disorders: pathophysiology and therapy. Raven Press, New York, p 203 29. Richter JE (1994) Pathophysiological basis of therapy for gastroesophageal reflux disease. Dis Esoph 7: 223 30. Stein HJ, DeMeester TR, Naspetti R (1991) Three-dimensional imaging of the lower esophageal sphincter in gastroesophageal reflux disease. Ann Surg 214: 374 31. Stein HJ, Barlow AP, DeMeester TR, Hinder RA (1992) Complications of gastroesophageal reflux disease: role of the lower esophageal sphincter, esophageal acid/alkaline exposure, and duodenogastric reflux. Ann Surg 216: 35 32. Stipa S, Fegiz G, Iascone C, Paolini A, Moraldi A, deMarchi C, Addario Cieco P (1989) Belsey and Nissen operations for gastroesophageal reflux. Ann Surg 210: 583 33. Stuart RC, Dawson K, Keeling P, Byrne PJ, Hennessy TPJ (1989) A prospective randomized trial of Angelchik prosthesis versus Nissen fundoplication. Br J Surg 76: 86 34. Thor KBA, Silander T (1989) A long-term randomized prospective trial of the Nissen procedure versus a modified Toupet technique. Ann Surg 210: 719 35. Toupet A (1963) Technique doesophago-gastroplastie avec phrenogastropexie appliquee dans la cure radicale des hernies hiatales et comme complement de loperation dHeller dans les cardiospasmes. Mem Acad Chir 89: 394 36. Vassilakis JS, Xynos E, Kasapidis P, Chrysos E, Mantides A, Nicolopoulos, N (1993) The effect of floppy Nissen fundoplication on esophageal and gastric motility in gastroesophageal reflux. Surg Gynecol Obstet 177: 608 37. Walker SJ, Holt S, Sanderson CJ, Stoddard CJ (1992) Comparison of Nissen total and Lind partial transabdominal fundoplication in the treatment of gastro-oesophageal reflux. Br J Surg 79: 410 38. Watson A, Jenkinson LR, Ball CS, Barlow AP, Norris TL (1991) A more physiological alternative to total fundoplication for the surgical correction of resistent gastro-oesophageal reflux. Br J Surg 78: 1088 39. Zaninotto G, DeMeester TR, Schwizer W, Johansson KE, Cheng SC (1988) The lower esophageal sphincter in health and disease. Am J Surg 155: 104

Surg Endosc (1997) 11: 11711178

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

The dramatic reality of biliary tract injury during laparoscopic cholecystectomy

An anonymous multicenter Belgian survey of 65 patients
J.-F. Gigot, J. Etienne, R. Aerts, E. Wibin, B. Dallemagne, F. Deweer, D. Fortunati, M. Legrand, L. Vereecken, J.-M. Doumont, P. Van Reepinghen, C. Beguin
The Belgian Group for Endoscopic Surgery (B.G.E.S.), rue Saint Georges, Feluy, Belgium Received: 21 February 1997/Accepted: 10 March 1997

Abstract Background: Most reports concerning the outcome of patients with biliary tract injury during laparoscopic cholecystectomy come from tertiary referral centers, and results could be very different in the everyday practice of community surgeons. Objective: The objective is to define the presentation, mechanisms, results of treatment, and long-term outcome of biliary tract injuries during laparoscopic cholecystectomy in the setting of a community surgeons practice. Methods: An anonymous retrospective multicenter survey of 9,959 patients who underwent laparoscopic cholecystectomy was conducted by the Belgian Group for Endoscopic Surgery, composed mainly of community general surgeons. Results: Sixty-five patients with bile duct injury were reported on; the incidence was 0.5%, varying from 0.35 to 1.3% according to the experience of the surgeon. Thirtyfour percent of ductal injuries occurred with experienced surgeons, often in association with local predisposing risk factors. Injury occurred in 87% of cases during dissection of the Calot triangle, with severe injury occurring in 46% of patients. Intraoperative cholangiography was performed in 34% of patients and was associated with a significantly improved operative detection rate of injury (68% vs 32%, p 0.007). Operative detection of injury occurred in 45% of patients; diffuse bile ascitis was encountered postoperatively in 29%. The overall mortality was 9%, the postoperative biliary complication rate 31%, and the reintervention rate 14%. During a median follow-up of 49 months (range, 378 months), 20 of the 61 surviving patients (33%) had recurrent biliary strictures. Multivariate analysis demonstrated that the age of the patient (odds ratio: 0.893) and the

presence of biliary peritonitis (odds ratio: 0.061) were independent predictive factors for mortality and that the age of the patient (odds ratio: 1.049) and the occurrence of postoperative biliary complications (odds ratio: 0.161) after the initial biliary repair were independent predictive factors for late biliary stricture. Conclusions: Biliary tract injury is associated with significant mortality and complications in the practice of Belgian community surgeons. Intraoperative detection of ductal injury by the routine use and a correct interpretation of intraoperative cholangiography improved outcome. The impact of the primary biliary repair on long-term outcome is an argument to refer these patients to specialized multidisciplinary experts. The results highlight the importance of surgical experience, proper selection of patients for laparoscopic cholecystectomy, and conversion to laparotomy in difficult cases. Key words: Biliary tract injury Laparoscopic cholecystectomy

Correspondence to: J.-F. Gigot, Department of Digestive Surgery, SaintLuc University Hospital, Hippocrate Avenue, 10, 1200 Brussels, Belgium

Despite worldwide acceptance of laparoscopic cholecystectomy (LC) as the gold standard in the treatment of cholelithiasis [2, 22, 23] biliary tract injury (BTI) remains the most serious complication encountered with this procedure. Compared with open cholecystectomy, an increased rate of BTI during LC has been reported [6, 12, 15, 21, 28, 30]. Moreover, the incidence of BTI in various multicenter European surveys reaches 0.21% [7, 9, 11, 14, 15, 31, 32, 34, 3739]. Most reports concerning the outcome of patients with BTI have come from tertiary referral centers [1, 5, 10, 20, 27, 29, 40] and these results could be very different from those obtained in more general surgical practice [19, 26, 32]. The expertise in these highly specialized centers and

1172

the selection of patients there could represent a bias in reporting the results of treatment. Thus, the most severely ill patients might have died before referral, and successfully treated patients might not have been referred to these centers. To determine the short-term and long-term outcomes of patients with BTI in routine surgical practice, we undertook an anonymous multicenter survey within a Belgian multicenter surgical association. The Belgian Group for Endoscopic Surgery (BGES), which includes mainly community surgeons.

Table 1. Surgeons experience in laparoscopic cholecystectomy for the 50 patients with a primary biliary tract injury Experience (no. of cases) <10 1050 50100 >100 No. of patients 8 14 11 17 (%) (16) (28) (22) (34)

(44)

Materials and methods

Ninety-eight Belgian surgeonsmembers of the BGESreceived the proposal that they review retrospectively and anonymously their experience with LC, focusing on patients presenting with BTI. Seventy-five surgeons (77%) agreed to participate in the study (67 community surgeons and eight academic surgeons). Thirty-two of the surgeons included some patients with BTI in the survey. BTI was defined as an injury of any part of the major extrahepatic biliary tract, excluding biliary leakage from the cystic duct or the gallbladder fossa with an intact extrahepatic biliary system. Anonymity of patients for each participating surgeon was guaranteed by the first author, as the scientific coordinator of the group. An extensive questionnaire was sent to the surgeons concerning their overall biliary laparoscopic experience; the number of patients with BTI; their biliary laparoscopic experience at the time of the BTI; the clinical data for the patients; the intraoperative findings, including mechanism, site, and type of BTI; the postoperative course of the patients; the need for reintervention; the number and type of biliary repairs; and the long-term follow-up (focusing on biliary-related mortality and late biliary stricture). Patients files, cholangiographies, and any videotapes of the intervention were reviewed. A primary BTI was defined as an injury caused and repaired by the surgeon performing the initial LC. The incidence of primary BTI during LC was estimated for the entire group of surgeons, and for each individual surgeon. Inclusion of patients referred for secondary biliary repair allowed for some surgeons to correct their real incidence of bile duct injury. The French technique of LC described by Dubois [13] and Perissat [25] was used in all patients. Electrocautery was the method of choice for dissection of the triangle of Calot and cholecystectomy. Statistical analysis included use of the Fisher exact test for categorical variables and the Wilcoxon test for continuous variables. Multivariate analysis was performed by logistic regression, using the SAS software. For death and late biliary strictures, the model gives a value of 1 in case of presence and of 0 otherwise. A p value of <0.05 was considered significant. Data are expressed as mean and median values, with ranges.

Fig. 1. Distribution of bile tract injury (BTI) according to the laparoscopic experience of the surgeon (number of laparoscopic cholecystectomies) (LC) at the time of BTI.

patients) (range, 04%) when the surgeon had less than 50 cases of experience and 0.35% (29 BTI in 8,242 patients) (range, 02.5%) when the surgeon had more than 50 cases of experience (p < 0.0001). The distribution of primary BTI repairs according to the laparoscopic experience of the surgeon at the time of BTI is illustrated in Fig. 1. Thirty-two surgeons were responsible for 50 primary BTIs: 20 surgeons (62%) were responsible for one injury and 12 (38%) for multiple injuries (two BTIs for seven surgeons, three for four surgeons, and four for one surgeon). Preoperative clinical presentation Forty-two patients (65%) presented before LC with clinically uncomplicated gallstones (with biliary colic in 38 patients and nonspecific symptoms in 4). Acute cholecystitis was observed in 14 patients, of whom eight underwent emergency operation and six were operated on after 68 weeks of medical treatment. Chronic cholecystitis was present in five patients, and four patients presented clinical or biochemical signs of choledocholithiasis. Preoperative biliary workup included ultrasonography in all patients, intravenous cholangiography in 32 (49%), and endoscopic retrograde cholangiopancreatography in 13 (20%). Preoperative endoscopic sphincterotomy was performed in six patients (9%) for common bile duct stone extraction. The presence of an aberrant right posterior hepatic duct was identified in one patient by preoperative endoscopic retrograde cholangiopancreatography. Intraoperative features Laparoscopic exploration revealed that the gallbladder was normal in 34 patients (52%). Acute cholecystitis was

Results From February 1990 to October 1993, 9,959 LCs were included in this study. Sixty-five patients with BTI were reported, with primary BTI repair in 50 cases. A secondary (referred) repair of the BTI was performed in 15 patients, mainly in university hospitals (11 patients). There were 46 female and 19 male patients. The mean age was 55 years (median, 57; range, 1980 years), but 14 patients were less than 40 years old (22%) and six less than 30 (9%). The extent of surgical experience with LC for the 50 patients with primary repair of BTI is given in Table 1.

Incidence The overall incidence of primary BTI in this group of surgeons was 0.5% (50 primary BTI in a total experience of 9,959 LC), with a range varying for each surgeon from 0 to 4%. The incidence of BTI was 1.3% (21 BTI in 1,600

1173 Table 2. Details of 51 local risk factors for biliary tract injury present during laparoscopic cholecystectomy in 40 patients (62%) Risk factors Acute inflammation in the triangle of Calot Scleroatrophic cholecystitis with a short cystic duct Huge impacted gallstone in the gallbladder neck Biliary anomaly (aberrant right posterior hepatic duct) Instrumental endobiliary maneuver during transcystic laparoscopic common bile duct exploration Mirizzi syndrome: gangrenous cholecystitis Gallbladder cancer No. of patients 19 14 8 5 3 1 1

present in 14 patients (including two cases of gangrenous cholecystitis) and scleroatrophic gallbladder in 17. A total of 51 local predisposing risk factors for BTI were observed during the surgical dissection in 40 patients (62%) (Table 2). The average experience of the surgeon when local predisposing risk factors were absent was 65 LCs, compared with 150 LCs, when risk factors were present (p < 0.01). In the group of patients with primary BTI repair, excluding ductal injury during laparoscopic common bile duct exploration, BTI occurred in the absence of local predisposing risk factors in 55% (12 of 22 patients) when the surgeon had less than 50 cases of experience, whereas BTI occurred with the presence of these risk factors in 76% (19 of 25 patients) when the surgeon had more than 50 cases of experience (p 0.03). The mechanism of the BTI at LC was identified in 63 patients (97%) (Table 3). The injury occurred during dissection of Calots triangle in 55 patients (87%), during the phase of cholecystectomy in five (8%), and during instrumental transcystic maneuvers for common bile duct exploration in three (5%). Details on the mechanism of bile duct injury are listed in Table 3. Failure to distinguish between the cystic duct and the common bile duct was the most common cause of injury; this was followed by instrumental injury and abuse of electrocautery, these two mechanisms usually being associated and related to the hook dissector. The type and site of the bile duct injury were determined in all patients. Partial injury occurred in 31 patients, complete transsection in 20, wide resection of the extrahepatic bile duct in six, local bile duct coagulation in four, and extensive thermal bile duct necrosis in four. Thus, severe injurycomplete transection, extensive resection, or thermal necrosiswas present in 30 patients (46%). The biliary injury was located at the level of the choledochus in 34 patients, at the common hepatic duct in 24, at the right hepatic duct in three, at an aberrant right posterior hepatic duct in three, and at the bifurcation of the hepatic duct in one patient. According to the Bismuth classification [4], type I bile duct injury occurred in 33 patients, type II in 18, type III in six, type IV in two, and type V in six. Intraoperative cholangiography (IOC) was performed in only 22 patients (34%); it resulted in the prompt detection of BTI in 15 patients (68%). In the remaining seven patients, IOC failed to detect the BTI because of misinterpretation by the surgeon. In five of these patients, the lack of opacifica-

tion of the proximal bile duct system was erroneously considered as normal or related to preferential transpapillary passage of contrast material due to preoperative endoscopic sphincterotomy. In two of these patients, IOC was normal at the time of initial LC, but these patients presented with postoperative biliary peritonitis related to thermal injury. When IOC was not performed (43 patients), BTI was detected intraoperatively in 14 patients (33%)by the occurrence of bile in the operative field in seven patients, by further surgical dissection in six patients, and during conversion to laparotomy because of hemorrhage in one patient. The detection rate of BTI was 68% when IOC was performed compared with 32% when IOC was not used (p 0.007). If, when IOC was performed, it had been correctly interpreted, this tool would have detected ductal injury in 20 of 22 patients (91%). The mean surgical experience when BTI was detected during surgery was 183 LCs, compared with 63 LCs when BTI was not detected (p < 0.002). There was no relation between the type and severity of BTI and the performance of IOC.

Mode of postoperative clinical presentation Twenty-nine patients (45%) had their bile duct injury detected during surgery (group I), mainly by IOC (15 patients, 52%). Eight patients (12%) presented with postoperative external biliary fistula (group II). Three patients (5%) had a localized peritoneal bile collection and 19 patients (29%) a diffuse bile ascitis (group III). Six patients (9%) presented with a postoperative biliary stricture (group IV)in the early postoperative period in three patients (after a mean of 3 days; range, 15 days) and later in three other patients (after a mean of 4 months; range, 35 months).

Treatment and postoperative results Six patients died, for an overall mortality of 9%. Four patients died during the initial hospital stay, and two patients had late biliary-related deaths due to severe cholangitis and recurrent biliary stenosis. Immediate and late postoperative outcome are reported in Table 4. In group I, all 29 patients were converted to laparotomy and treated by primary biliary suture without biliary drainage in three patients, primary biliary suture with a T-tube in 22, and hepaticojejunostomy in four. When a T-tube was inserted, the mean duration of biliary drainage was 47 days (range, 10120 days). Two of these patients underwent successful primary biliary suture laparoscopically. One patient (3.5%) died from biliary peritonitis and multiple organ failure after primary biliary suture without T-tube drainage; the postoperative course was complicated by bile ascitis from suture breakdown and necrosis. Postoperative biliary complications occurred in seven patients (24%), including biochemical pancreatitis (one patient), repeated cholangitis (one), external biliary fistula (four) (associated with residual common bile duct stone and hemobilia in one patient each), and postoperative bile ascitis (one). Reintervention was nec-

1174 Table 3. Mechanism of biliary tract injury during laparoscopic cholecystectomy in 63 patients in whom the mechanism was identified (97%) Mechanism of injury During dissection of the triangle of Calot Anatomic confusion between common bile duct and cystic duct: During cholangiography During surgical dissection and the cystic artery: Instrumental injury Coagulation Cystic duct avulsion Common bile duct tenting During urgent hemostasis Lateral clipping Adhesiolysis in front of common bile duct During the phase of cholecystectomy Gallbladder neck adherent to common bile duct Biliary anomaly Coagulation During laparoscopic common bile duct exploration Transcystic balloon dilatation Instrumental Dormia basket injury No. of patients

4 22 1 13 8 2 2 1 1 1 3 1 1 2 1

Table 4. Postoperative and long-term outcome in patients with biliary tract injury Long-term outcome Postoperative outcome, no. of patients (%) Mode of presentation, no. of patients Operative detection, 29 Biliary fistula, 8 Biliary peritonitis, 22 Biliary stricture, 6 Entire series, 65 Mortality 1 (3.5) 0 3 (14) 0 4 (6) Biliary complications 7 (24) 2 11 (50) 0 20 (31) Reintervention 4 (14) 0 5 (23) 0 9 (14) Follow-up, median (months) 46 46 53 58 49 Late mortality, no. of patients (%) 1 (3.5) 0 1 (4.5) 0 2 (3) Late stricture, no. of patients (%) 8 (29) 3 (37) 9 (47) 0 20 (33)

essary in four patients (14%), including repositioning of the T-tube (one patient), endoscopic sphincterotomy for common bile duct stone extraction with endoscopic stenting (one), external biliary diversion (one), and repeat hepaticojejunostomy with arterial ligation for a hepatic artery aneurysm (one). In group II, conservative medical treatment was initially instituted in all eight patients, leading to resolution of the external biliary fistula in two patients, at 21 and 30 days. Biliary fistula persisted in the remaining six patients. After a mean interval of 3 months (range, 0.27 months), all eight patients underwent biliary repair, with hepaticojejunostomy in five patients and biliary suture with T-tube in one. The two remaining patients underwent negative reexploration, with choledochotomy and T-tube insertion, without detection of a type V BTI retrospectively. Biliary leak persisted postoperatively in these two patients but resolved spontaneously with subsequent dilatation of the posterior bile duct system at 50 and 70 months postoperatively, but without evidence of clinical biliary complaints. A third patient presented with a partial residual biliary stricture after two previous attempts at surgical repair. There was no hospital mortality in this group. In group III, with 22 patients, two patients with a localized collection of bile were treated by combining percutaneous peritoneal drainage and endoscopic sphincterotomy in one patient and endoscopic stenting in the other. The

postoperative course in these two patients was uncomplicated, and they remained free of symptoms 50 and 56 months later. Twenty patients with diffuse bile ascitis underwent biliary repair by laparotomy after a mean of 11 days (median, 8; range, 141 days). Treatment approaches included biliary suture without drainage in one patient, biliary suture with T-tube in six, surgical biliary stenting in one, hepaticojejunostomy in six, and total external biliary diversion in six. Three patients (14%) died from septic biliary complications. Eleven patients (50%) had biliary postoperative complications, including external biliary fistula in nine, cholangitis in one, and bile peritonitis in two. Five patients (23%) underwent reintervention, either with total external biliary diversion, in four patients (with two postoperative deaths), or with reexplorative laparotomy for hemorrhage, in one. Hospital deaths occurred in two of five patients (40%) who required reintervention and one of 17 patients (6%) who did not require reintervention. The difference is not statistically significant. In group IV with six patients, five patients underwent surgery at 1, 2, 5, 120, and 150 days postoperatively. Biliary repair consisted of primary suture with T-tube in one patient and hepaticojejunostomy in four. The remaining patient was treated at 3 months postoperatively by endoscopic stenting, with a successful result 77 months later. No hospital mortality, postoperative biliary complication, or reintervention was encountered in this group of patients.

1175 Table 5. Univariate analysis of predictive risk factors for mortality and late biliary stricture Variable Mortality Mean patients age (range) Biliary peritonitis (%) Late biliary stricture Mean patients age (range) Bismuth type III injury Postoperative biliary complications Outcome Death 68 (5480) 5/21 (24%) Stricture 48 (1974) 5/5 (100%) 12/20 (60%) Surviving 53 (1977) 1/44 (2%) No stricture 58 (2980) 16/60 (27%) 9/45 (20%) p value 0.02 0.01 0.02 0.02 0.003

Table 6. Multivariate analysis of predictive risk factors for mortality and late biliary stricture Variable Mortality Age Biliary peritonitis Late biliary stricture Age Postop. biliary complications p value 0.035 0.021 0.021 0.004 Coefficient (standard error) 0.0535 1.2089 0.0207 0.6314 Odds ratio 0.893 0.061 1.049 0.161 95% confidence interval 0.80420.9919 0.00570.6514 1.00741.0925 0.04680.5559

Long-term results The mean follow-up for the 61 surviving patients was 48 months (median, 49; range, 378 months). Four patients were dead at the time of follow-up, from a nonbiliary cause. Twenty patients (33%) presented with a late biliary stricture during the follow-up period. Sixteen patients had jaundice or cholangitis related to biliary stricture after a mean interval of 11 months (median, 5; range, 248 months) and were reoperated on with construction of a hepaticojejunostomy. Two of these patients died from septic biliary complications (one patient in group I and one in group III). Two other patients presented with partial biliary stricture 3 and 51 months postoperatively without any clinical symptoms. Finally, the two patients with an undetected Bismuth type V injury had bile duct dilatation and atrophy of the posterior liver segments at 50 months and 70 months postoperatively without any biliary complaints. The incidence of late biliary stricture was 29% (eight of the 28 surviving patients, including two with partial stenosis) in group I, 37% (three of the eight surviving patients, including the two patients with untreated Bismuth type V injury) in group II, 47% (nine of the 19 surviving patients) in group III, and 0% in group IV (Table 4). Univariate statistical analysis demonstrated that the age of the patient and biliary peritonitis were significant predictive factors for mortality and that the age of the patient, Bismuth type III injury, and occurrence of postoperative biliary complications after initial biliary repair were predictive factors for late biliary stricture in patients suffering from bile duct injury (Table 5). Multivariate statistical analysis (Table 6) determined that the age of the patient (odds ratio: 0.893) and the occurrence of biliary peritonitis (odds ratio: 0.061) were independent predictive factors for mortality (c value 0.857) and that the age of the patient (odds ratio: 1.049) and the occurrence of postoperative biliary complications (odds ratio: 0.161) were independent predictive factors for late biliary stricture in these patients (c value 0.778).

Discussion The incidence of BTI in this multicenter series (0.5%) is similar to that reported in other European national surveys (Table 7) [7, 9, 11, 14, 15, 31, 32, 34, 3739] and that found in a previous multicenter survey in Belgium [37]. The anonymous inclusion of patients, the small size of the country, and the participation of academic hospitals to which biliary repairs are usually referred are all factors that tend to ensure that the reported incidence is an objective one. However, the incidence could still be underestimated, because at the time of the survey the BGES represented only about 80% of all laparoscopic surgeons in Belgium and the surgeons participation rate was only 77%. This incidence nonetheless does reflect the daily practice of Belgian community surgeons rather than that of experts in this field. The causes of BTI during LC are multifactorial: inherent risk factors of the laparoscopic approach, lack of adequate surgeons experience with LC, presence of local anatomic risk factors, use of inappropriate surgical technique during dissection of the triangle of Calot, lack of liberal conversion to laparotomy in difficult cases, and absence of completed and correctly interpreted intraoperative cholangiography. Compared with open cholecystectomy, several factors inherent in the laparoscopic approach could be implicated in the occurrence of BTI: limitation to two-dimensional vision, loss of manual palpation of the porta hepatis, use of tangential and inferior approach to the common bile duct (in comparison with the vertical approach obtained with a right subcostal incision) giving suboptimal visualization of the common hepatic duct, poor visualization of the operative field and thus difficulty in the control of bleeding when it occurs, surgeons dependence on the material and on the camera-holding assistant, blind manipulation of instruments, use (or abuse) of electrocautery, and surgeons inexperience with this new technology [26, 33]. As previously reported [10, 12, 24, 35, 36], the role of the surgeons learning curve was again highlighted here, since the incidence of BTI reaches 1.3% for surgeons with

1176 Table 7. Incidence of biliary tract injury during laparoscopic cholecystectomy in various multicenter European surveys Country Belgium France France Holland France Austria Holland Switzerland Italy Spain Norway Reference 37 34 11 14 7 39 15 31 9 38 32 Year of publication 1992 1992 1992 1993 1993 1993 1994 1994 1994 1994 1995 No. of operations 3,244 3,606 6,512 6,076 3,673 7,351 2,932 3,722 6,865 2,342 2,612 Incidence of injury (%) 0.50 0.78 0.44 0.86 0.60 0.50 1.1 0.60 0.26 0.28 0.61

less than 50 cases of experience. In 55% of these cases, the procedure was even described as an easy cholecystectomy, without any predisposing local risk factors for BTI. However, adequate surgical training alone does not protect the patient against the occurrence of BTI. It is indeed surprising to note that one-third of the patients in this survey were operated on by surgeons with more than 100 cases of experience and that in most of the cases in which experienced surgeons were responsible for BTI, there were local predisposing risk factors for ductal injury, such as acute inflammation or chronic scarring in Calots triangle. Thus, this series demonstrated that even for experienced surgeons proper selection of biliary diseases for the laparoscopic approach remains a key factor in avoiding BTI. Ready conversion to laparotomy in such difficult cases involving inflammatory changes, aberrant anatomy, or excessive bleeding is not to be considered a failure but rather good surgical judgment, to ensure the patients safety. All types of ductal injury mechanisms previously reported were encountered in this survey, but misidentification between the common bile duct and the cystic duct, defined as the classic injury [5, 10, 29, 33], was the most common. Combined instrumental and thermal injury with the hook dissector was the second-most-common mechanism. Thermal injury due to electrocautery is specific to the LC technique, and therefore great caution should be used during dissection of the triangle of Calot [5, 10, 20, 29]. The quality of the surgical dissection is obviously of the most importance in preventing BTI. We advocated strict adherence to the principles of surgical dissection described by French [13, 25] and American experts [1, 5, 8, 10, 16, 17, 20, 27, 29, 33, 40]. These guidelines for safe LC with the French technique included (1) adequate exposure and visualization of the operative field, (2) opening of Calots triangle by lateral and inferior traction on the gallbladder neck, (3) blunt dissection of Calots triangle avoiding overuse of electrocautery, (4) starting the dissection at and clear identification of the cystic ductgallbladder junction, freeing both ventral and dorsal aspects of the Calots triangle and of the upper part of the gallbladder neck, (5) avoiding excessive traction on the gallbladder infundibulum to prevent tenting of CBD, (6) avoiding blind use of clip or cautery to control bleeding, (7) routine performance of IOC after complete dissection of all structures in Calots triangle and before any division, and finally and mostly important, (8)

liberal conversion to open cholecystectomy (OC) when the anatomy remains unclear during the surgical dissection. Intraoperative detection of ductal injury appears to have contributed to success in the final outcome of patients in this series. Hospital mortality, postoperative biliary complications, and reintervention rate were all reduced in the group of patients with intraoperative detection and repair, especially when compared with patients with biliary peritonitis. Inexperience of the surgeons and the omission of IOC were clearly implicated in the nondetection of BTI in this survey. Use of IOC was associated with a statistically significantimprovement in detection of ductal injury. However, a wrong interpretation of the IOC occurred in 23% of patients. The presence of contrast material extravasation, lack of opacification of the proximal bile duct system, and incomplete opacification of the right posterior intrahepatic bile ducts should raise suspicion of BTI [33, 41]. When the anatomy is unclear during surgical dissection, cholangiography must also be performed to give the surgeon an anatomic road map [3, 33]. IOC also has the advantage of alerting the surgeon to the problem of tenting of the common bile duct during clip placement [8], which is also one of the mechanisms of BTI encountered in this series. It has been reported that the use of IOC should decrease the severity of ductal injury [26, 40, 41] but this was not confirmed in all cases in our study. However, in four patients misidentification between the common bile duct and the cystic duct during IOC led to the detection of a lateral ductal injury and prevented further transsection or wide excision. These patients successfully underwent simple repair with T-tube insertion and suture. A normal IOC can also be associated with undetected BTI (1) if the injury occurs later during cholecystectomy, after the performance of cholangiography, or (2) if there is thermal injury due to electrocautery, leading to postoperative localized biliary necrosis or late stricture, as described in this series. Finally, a correctly interpreted IOC increases the chance of detecting BTI [8, 12, 30, 40, 41], and its routine use should be advised especially during the learning experience of the surgeons. The timing and precise means of performing IOC are of the most importance. Cholangiography should be performed early in the procedure, after complete blunt dissection of the Calot triangle and the upper part of the gallbladder neck anteriorly and posteriorlywith clear identification and adequate clipping of arterial and ductal cystic structures, be-

1177

fore any definitive division is undertaken [10, 16, 17]. This type of dissection offers the best chance of preventing BTI. With this approach, inadvertent clipping of an aberrant or accessory right posterior bile duct will be immediately detectable by IOC, preventing a definitive injury and allowing clip removal and repeat cholangiographic examination. This occurred in one patient in this survey, who was therefore not included in the study as a true case of BTI. The role of IOC remains controversial regarding its ability to prevent BTI [5, 18, 40]. Indeed, in our opinion, the major advantage of IOC is not in preventing injury to the extrahepatic portion of the biliary tract but in detecting such ductal injury and therefore reducing early postoperative and late complications [41]. Multivariate statistical analysis demonstrated that the occurrence of biliary peritonitis was predictive for mortality, as was the patients age. On the other hand, it is important to stress that the quality of preoperative biliary workup in this series had only a minor role in preventing intraoperative BTI. Indeed, 20% of the patients in this series underwent preoperative endoscopic retrograde cholangiopancreatography, and in one of these patients a biliary anomaly was detected preoperatively, but subsequent injury during a difficult surgical dissection was not avoided. Finally, the most striking features in this series were the high mortality (9%) and morbidity and the late recurrent stricture rate (33%). These disastrous results, which had been observed as well in a previous Dutch survey [15], are clearly a result of nonoptimal primary treatment. The problems are related to the technical difficulties of restoring biliary continuity in patients with normal-sized bile ducts and to difficult local conditions caused by biliary peritonitis, especially when biliary repair is performed by nonexpert surgeons. The inclusion of patients anonymously in this series made the reporting of such results possible, and we believe they are representative of daily surgical practice. Late complications could still be underestimated, as 1015 years of follow-up are mandatory before definitive conclusions can be drawn. However, to the best of our knowledge, the follow-up achieved in this series is one of the longest reported in the literature on biliary repair after LC. The importance of an optimal initial primary repair in the patient with BTI is highlighted in this series by the significant relation, shown by the multivariate statistical analysis, between the occurrence of postoperative biliary complications after the initial repair and the occurrence of late biliary stricture. For optimal care, such difficult patients should thus be treated in specialized referral centers, where expert multidisciplinary teams are available [30, 33, 40].
Acknowledgments. The following members of B.G.E.S. are acknowledged for their substantial contribution to the present study: Raymond Aerts, M.D., (Leuven), Thierry Ballet, M.D., (Brussels), Claude Bertrand, M.D., (Haine-St-Paul), Dany Burnon, M.D., (Brussels), Bernard Dallemagne, M.D., (Lie ` ge), Robert de Keuleneer, M.D., (Auvelais), Johan de Mol, M.D., (Kortrijk), Frans Deweer, M.D., (Bonheiden), Claude Desaive, M.D., (Lie ` ge), Marc Domb, M.D. (Brussels), Jean-Marie Doumont, M.D., (Malmedy), Marie-Lou Druart, M.D., (Brussels), Jose Etienne, M.D. (Namur), Didier Fortunati, M.D., (Lobbes), Michel Gelin, M.D., (Brussels), Jean-Franc ois Gigot, M.D., (Brussels), Yves Hoebecke, M.D., (Haine-St-Paul), Marc Huyghe (Antwerpen), Paul-Jacques Kestens, M.D., (Brussels), Andre Lantin, M.D., (Brussels), Marc Legrand, M.D., (Lie ` ge), Baudouin Mansvelt, M.D., (Haine-St-Paul), Michel Meessen, M.D., (Auvelais), Beno t Navez, M.D., (Gilly), Freddy Penninckx, M.D., (Leuven), Jean Saey, M.D., (Mons), Baki Topal, M.D. (Leuven), Jean Vandestadt,

M.D. (Brussels), Patrick van Reepinghen, M.D., (Namur), Etienne van Vyve, M.D., (Brussels), Ludo Vereecken, M.D., (Gent), Paul Vincent, M.D., (Frameries), Ernest Wibin, M.D., (Ottignies), and Jean-Pierre Yvergneaux, M.D., (Gent). The authors acknowledge Dr. W. Heidel for editorial assistance and Mrs. N. Thiebaut for secretarial assistance.

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1178 scopic cholecystectomy, appendectomy, and hernia repair. Consensus statementsSeptember 1994. The Educational Committee of the European Association for Endoscopic Surgery. Surg Endosc 9: 550563 NIH Consensus conference (1993) Gallstones and laparoscopic cholecystectomy. JAMA 269: 10181024 Orlando R, Russell JC, Lynch J, Mattie A (1993) Laparoscopic cholecystectomy: a statewide experience. Arch Surg 128: 494499 Perissat J, Collet DR, Belliard R (1989) Laparoscopic treatment, intracorporeal lithotripsy followed by cholecystostomy or cholecystectomya personal technique. Endoscopy 21 (Suppl 1): 373374 Rantis PC, Greenlee HB, Pickleman J, Prinz RA (1993) Laparoscopic cholecystectomy bile duct injuries: more than meets the eye. Am Surg 59: 533540 Ress AM, Sarr MG, Nagorney DM, Farnell MB, Dohohue JH, McIlrath DC (1993) Spectrum and management of major complications of laparoscopic cholecystectomy. Am J Surg 165: 655662 Roslyn JJ, Binns GS, Hughes EFX, Saunders-Kirkwood K, Zinner MJ, Cates JA (1993) Open cholecystectomy. A contemporary analysis of 42,474 patients. Ann Surg 218: 129137 Rossi RL, Schirmer WJ, Braasch JW, Sanders LB, Munson JL (1992) Laparoscopic bile duct injuries: risk factors, recognition and repair. Arch Surg 127: 596602 Russell JC, Walsh SJ, Mattie AS, Lynch JT (1996) Bile duct injuries, 19891993. A statewide experience. Arch Surg 131: 382388 Schlumpf R, Klotz HP, Wehrli H, Herzog U (1994) A nations experience in laparoscopic cholecystectomy. Prospective multicenter analysis of 3722 cases. Solheim K, Buanes T (1995) Bile duct injury in laparoscopic cholecystectomy. Int Surg 80: 361364 Soper NJ, Flye MW, Brunt LM, Stockmann PT, Sigard GA, Picus D, Edmundowicz SA, Aliperti G (1993) Diagnosis and management of biliary complications of laparoscopic cholecystectomy. Am J Surg 165: 663669 Suc B, Fontes Dislaire I, Fourtanier G, Escat J (1992) 3606 cholecystectomies sous coelioscopie: registre de la Socie te Franc aise de Chirurgie Digestive. Ann Chir 46: 219226 The Southern Surgeons Club (1991) A prospective analysis of 1518 laparoscopic cholecystectomies. New Engl J Med 324: 16, 10731078 The Southern Surgeons Club, Moore MJ, Bennett CL (1995) The learning curve for laparoscopic cholecystectomy. Am J Surg 170: 55 59 Vereecken L (for the Belgian Group for Endoscopic Surgery) (1992) Laparoscopic cholecystectomy: the Belgian registry. Br J Surg 79 (Suppl): S73 (abstract) Vincent-Hamelin E, Pallares AC, Felipe JAR, Rosello EL, Caperochipi JA, Cantero JLB, Gomis RD, Corvinos FF, Sanchez SP, Lesquereux JP, Puig OP (1994) National survey on laparoscopic cholecystectomy in Spain. Results of a multiinstitutional study conducted by the Committee for Endoscopic Surgery (Associacio n Espan ola de Cirujanos). Surg Endosc 8: 770776 Wayand WU, Gitter T, Woisetschla ger R (1993) Laparoscopic cholecystectomy: the Austrian experience. J R Coll Surg Edinb 38: 152253 Woods MS, Traverso LW, Korzareck RA, Tsao J, Rossi RL, Gough D, Donohue JH (1994) Characteristics of biliary tract complications during laparoscopic cholecystectomy: a multi-institutional study. Am J Surg 167: 2734 Woods MS, Traverso LW, Kozarek RA, Donohue JH, Fletcher DR, Hunter JG, Oddsdottir M, Rossi RL, Tsao J, Windsor J (1995) Biliary tract complications of laparoscopic cholecystectomy are detected more frequently with routine intraoperative cholangiography. Surg Endosc 9: 10761080

34.

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Surg Endosc (1997) 11: 11671170

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

VATS-guided epicardial pacemaker implantation

Hand-sutured fixation of atrioventricular leads in an experimental setting
M. Furrer,1 J. Fuhrer,2 H. J. Altermatt,3 H.-B. Ris,1 D. Mettler,4 U. Althaus,1 T. Carrel1
1 2

Department of Thoracic and Cardiovascular Surgery, Inselspital, University of Berne, CH-3010 Bern, Switzerland Division of Cardiology, Inselspital, University of Berne, CH-3010 Bern, Switzerland 3 Institute of Pathology, Inselspital, University of Berne, CH-3010 Bern, Switzerland 4 Surgical Research Unit, Inselspital, University of Berne, CH-3010 Bern, Switzerland Received: 14 October 1996/Accepted: 14 April 1997

Abstract Background: In neonates and infants epicardial stimulation may be preferred to endocardial stimulation because of growth-associated lead problems and the risk of vascular complications associated with transvenous electrodes. This study analyzes the feasibility of atrioventricular implantation of a new epicardial lead using the video-assisted thoracic surgical (VATS) technique in an animal model. Methods: Bipolar steroid-eluting epicardial leads were implanted in seven young white pigs. In five animals bipolar atrial and ventricular pacing leads (n 10) were inserted and fixed by the VATS technique, while two animals served as controls and underwent implantation through anterolateral thoracotomy. Surgical feasibility, pacing, and sensing thresholds of the leads as well as hemodynamic parameters during pacing were studied. Histological changes beneath the electrodes were evaluated 1 week after the implantation. Results: All animals survived the pacemaker lead implantation. One animal which underwent thoracotomy died because of irreversible ventricular fibrillation induced by rapid ventricular pacing. One animal in the VATS group exhibited intraoperative herniation of the heart through the pericardial window. All animals with left-sided VATS implantations demonstrated good individual pacing and sensing threshold values. The mean cardiac output was 1.6 times higher during AAI-mode pacing as compared to VVI-mode pacing at a heart rate of 140/min. One animal died postoperatively due to respiratory failure. No displacements of the pacemaker leads were observed in the survivors. Conclusion: While VATS-guided implantation of epicardial, atrial, and ventricular leads is feasible, technical improvements of the system are mandatory for safe clinical application. Key words: VATS Hand suture Pacemaker implantation
Correspondence to: M. Furrer

Transvenous implantation of permanent atrial or ventricular pacing leads is the method of choice in adults: It is a welltolerated procedure that is generally performed with local anesthesia under fluoroscopic control [7]. In neonates and infants, however, epicardial stimulation may be preferable because of growth-associated lead problems and the risk of vascular complications with transvenous electrodes [6, 8, 13, 15]. Left-sided cardiac pacing might be advantageous for optimizing hemodynamics, especially when intraatrial conduction disturbances prevent physiological electrical stimulation [3, 9, 11]. Unfortunately an endocavitary approach to the left side of the heart for pacing is not presently feasible, but it remains an interesting theoretical option. For patients requiring epicardial placement of atrial or ventricular pacing leads, thoracoscopy presents an interesting alternative to more extensive surgical approaches (e.g., midline superior laparotomy with a subxiphoid approach to the ventricles, left anterolateral thoracotomy or sternotomy). Thus, a thoracoscopic technique has already been advocated for the implantation of monopolar epi-/myocardial screw-in or fish-hook-type electrodes [4, 10] as well as for the placement of epicardial patches of implantable cardioverterdefibrillator systems [1, 2, 5, 12, 14]. This study analyzes the feasibility of hand suturing atrioventricular implants of a new steroid-eluting epicardial lead to the left and right heart cavities using the VATS (video-assisted thoracic surgery) technique in an animal model. Hemodynamic parameters during ventricular pacing (VVI-mode) and atrial stimulation (AAI-mode) were recorded. Histological changes of the epicardium and myocardium beneath these new electrodes were evaluated 1 week after implantation. Methods Animals/types of interventions
This study was performed on young white pigs weighing between 20 and 25 kg. A complete pacemaker system was inserted in seven animals. Two

1168 suture was passed through the two holes of the pacemaker lead outside of the thoracic cavity and a second stitch was placed in the heart more caudally. The first ventricular pacemaker lead was then introduced through the minithoracotomy incision and fixed by tightening the suture using the extracorporal technique. The second lead of the bipolar system was fixed in an analogous fashion, respecting a minimal distance of 2 cm from the first lead. Bipolar atrial leads were fixed using a similar technique (Fig. 1). For the endoscopic sutures applied to the beating heart we used an endoscopic needle holder introduced through the lateral trocar sleeve and a conventional forceps introduced through the minithoracotomy wound to control the needle after it passed the ventricular and atrial myocardium. Subcutaneous placement of the leads was performed using a separate abdominal incision of approximately 3 cm. A Charriere 18 G chest tube was introduced and the minithoracotomy and the abdominal incisions were closed in two layers: The trocar incisions were closed using skin sutures only. Before extubation and removal of the chest tube complete expansion of the lung was confirmed by chest X-ray. All operations were performed by the same surgeon (M.F.).

Fig. 1. Bipolar atrioventricular pacing leads (Medtronic CapSure Epi 10366, Minneapolis, Inc.).

control animals underwent anterolateral thoracotomy for lead placement. In five animals bipolar atrial and ventricular pacing leads were implantated using the VATS technique (thoracoscopic fixation of 20 leads). The rightsided VATS approach was abandoned after one case because anatomic considerations created technical difficulties for this technique.

Postoperative assessment
The following endpoints were assessed: 1. Primary endpoint: Successful lead placing Intraoperative mortality and morbidity 2. Secondary endpoints: Operating time (including pacemaker assessment) Assessment of pacing and sensing thresholds Hemodynamic parameters relative to the stimulation mode Stimulation was performed in the AAI and VVI modes at a rate of 140 beats/min. Three measurements of cardiac output were performed before and during atrial or ventricular stimulation. The following parameters were assessed intraoperatively: R- and Pwave reading (baseline/peak; mV), the slew rates (V/s), resistance (; 2.5 V/0.5 ms output) and the stimulation threshold (V; width: 0.5 ms). After extubation the animals were observed for 7 days to assess their general condition and eating behavior. Before sacrificing the animals, complete assessment of the pacemaker system was repeated under general anesthesia. The implantation sites of the pacemaker leads were examined macroscopically and histologically.

Pacemaker system
Steroid-eluting epicardial leads (Medtronic CapSure Epi10366, Minneapolis, Inc., Fig. 1) were implanted. The pacing system analyzer was PSA 5311 B, Medtronic, Inc., Minneapolis. In the animals which underwent thoracotomy (No. 1 and 2) monopolar hook electrodes were used as atrial leads (4951 M, Medtronic, Minneapolis, Inc.).

Perioperative management and anesthesia

Perioperative care of the animals was performed according to the guidelines of the Committee on Animal Care of the University of Berne. The operation was performed in the lateral decubitus position. Perioperative antibiotic prophylaxis consisted of 1 g amoxycillin. The animals were premedicated with ketamine hydrochloride 10 mg/kg and standard endotracheal intubation was performed. A Fogarty catheter was introduced through the endotracheal tube and positioned in the left or right main bronchus, under direct vision using a flexible bronchoscope (Olympus BF type P10), which allowed selective blockage of one lung. Inhalation anesthesia consisted of O2 and NO2-halothane. Perioperative monitoring was performed with on-line invasive measurements of arterial blood pressure obtained by cannulation of the common carotid artery. Cardiac output was assessed by thermodilution using a Swan-Ganz catheter introduced through the internal jugular vein.

Results All animals survived the pacemaker lead implantation. One control animal operated on through a left thoracotomy died because of irreversible ventricular fibrillation, probably induced by rapid ventricular pacing. One animal in the VATS group operated on through the right side exhibited intraoperative herniation of the heart through the pericardium with subsequent cardiac arrest: Successful resuscitation was performed with restoration of sinus rhythm. Because of prolonged low cardiac output following the cardiac resuscitation this animal was sacrificed at the end of the operation. Postmortem examination demonstrated that the Swan-Ganz catheter had been fixed tightly intraatrially by one suture of the right atrial leads. In two animals additional sutures were necessary to close small lesions of the very thin atrial wall caused by the fixation sutures of the pacemaker leads. The correct placement of the leads to the surface of the beating heart and tightening the sutures was time consuming and this maneuver had to be repeated in one-third of the implanted leads. The operating time (including the assessment of pacing and sensing thresholds and hemodynamic measurements) ranged from 105 to 120 min for the two control animals. In the left-side VATS group operating time

Surgical technique
VATS technique was performed with three lateral incisions of 710 mm and an anterior minithoracotomy in the fourth intercostal space (maximal length of 4 cm without rib spreading). A 10-mm rigid trocar sleeve (Autosuture Company Division, United States Surgical Corporation, Norwalk, CT) was inserted in the sixth intercostal space posteriorly for the introduction of an endoscopic needle holder and two 7-mm flexible trocar sleeves (Richard Wolf, GmbH, Knittlingen/Germany) were introduced in the eighth intercostal space. One was placed laterally for introduction of a 0 7-mm telescope and a more anterior trocar was for endoscopic clamps and forceps. The endoscopic picture was transmitted to two television screens situated on either side of the animal. Two control animals underwent anterolateral thoracotomies which included division of the intercostal muscles and spreading the ribs up to 7 cm. Pericardial fenestration (3 3 cm) was performed anterior to the phrenic nerve at the atrioventricular junction. A first stitch of 5-0 polypropylene suture was placed in the ventricle avoiding epicardial vessels. This

1169 Table 1. Technique, operating time, intra- and postoperative complications Animal No. 1 2 3 4 5 6 Technique Conv. Conv. VATS VATS VATS VATS Side Right Left Left Left Left Right Operation time (min) 120 105 195 180 170 235 Intraop. complications No Yes No No No Yes Remarks Ventricular fibrillation after ventr. stimulation

Intraop. herniation of the heart through the pericardium, inadverted fixation of Swan-Ganz catheter

VATS

Left

170

No

decreased during the study period from 195 to 170 (mean 179) min (Table 1). The main parameters of pacemaker assessment are summarized in Table 2. The systemic mean arterial pressure (MAP) and the pulmonary artery pressure (PAP) remained stable after pacing at a rate of 140 (mean prepacing heart rate 101 11). The cardiac output (CO) did not significantly differ before and during AAI pacing (2.9 1.0 vs 3.0 1.1 l/min.). However, VVI pacing induced a significant decrease in cardiac output as compared with AAI pacing2.0 0.9 vs 3.1 1.4 l/min (p < 0.05, paired t-test)in four animals operated on using the VATS technique on the left side (Table 3). Animal No. 3 suffered from severe postoperative respiratory failure caused by bronchial obstruction and died after extubation. Postmortem examination of another animal (No. 5) revealed a severe left side bronchopneumonia with significant pleuritic and pericarditic changes. Optimal pacemaker function was maintained in the surviving animals with uneventful postoperative recoveries. No displacement of the pacing leads occurred and histology of the myocardium beneath the leads showed a mild inflammatory infiltrate. Animal No. 5 had a severe postoperative infection involving the entire thoracic cavity and the granulocytic infiltration beneath the leads might have been responsible for the pacemaker dysfunction observed 1 week postoperatively. Discussion The epicardial pacemaker system represents the most promising option in newborns, small infants, and children because of growth-associated lead problems inherent to the endocardial pacemaker system [3, 6, 8, 9, 11, 13, 15]. This study examines the feasibility of thoracoscopic implantation of a new epicardial pacing lead system, avoiding more extensive surgical approaches like anterior thoracotomy, subxiphoid laparotomy, or sternotomy. In the past, several attempts have been made to minimize surgical trauma, (e.g., to insert epicardial patches for implantable cardioverter defibrillators (ICD) [1, 2, 5, 12, 14] or to place monopolar sutureless screw-in or hook leads by the pericardioscopic or the left thoracoscopic route [4, 10]). However, the feasibility of adequate placement using hand-sutured epicardial fixation of this new generation of bipolar steroid-eluting leads by the VATS technique has not yet been evaluated. Endoscopic placement of 5.0 sutures in the beating heart is technically demanding and not only

Table 2a. Assessment of atrial leads (P wave, slew rate, resistance, and stimulation threshold): mean value of all animals, individual values for the left-side VATS implantation group (animal No. 3, 4, 5, and 7) P wave (mV) Mean Animal No. 3 4 5 7
a

Slew rate (V/s) 0.89 1.56 2.04 0.31 0.90

Impedance (W) 582 382 424 1,021 625

Threshold (V)a 1.3 0.7 1.1 0.6 0.8

3.5 6.6 4.6 2.0 1.8

Width: 0.5 ms.

Table 2b. Assessment of ventricular leads (R wave, slew rate, resistance, and stimulation threshold): mean value of all animals, individual values for the left-side VATS implantation group (animal No. 3, 4, 5, and 7) R wave (mV) Mean Animal No. 3 4 5 7
a

Slew rate (V/s) 2.46 3.20 1.48 2.57 4.00

Impedance (W) 935 1,022 714 714 1,190

Threshold (V)a 0.7 0.6 0.6 0.7 1.0

13.9 22.2 9.0 22.0 10.2

Width: 0.5 ms.

corresponds to the actual surgical technique used in open heart surgery but may also have some impact on the evolution of videoscopic assisted coronary artery bypass surgery. Despite the successful implantation of 10 bipolar pacing leads (endoscopic fixation of a total of 20 leads) in all five animals operated on using the VATS technique, endoscopic cardiac suturing was judged to be difficult. Suturing of the atrial wall is a delicate procedure in this animal model. Small lesions of the atrial wall following fixation of the leads can induce substantial bleeding; this occurred in two animals but was managed by additional endoscopic sutures. The two-dimensional view and the limited freedom of guiding the instruments (limitations of endoscopic surgical techniques) were responsible for the difficulties encountered in placing sutures with precision and in correctly positioning the four leads on the beating heart. Nevertheless, the operation time decreased continuously in the left-side VATS group from 195 to 170 min. It was significantly shorter in the control animals which underwent conventional thoracotomies (105120 min).

1170 Table 3. Hemodynamic parameters before and after pacinga Animal No. 1 No. 2 No. 4 No. 5 No. 6* No. 7
a

HR before stimulation 102 98 106 91 120 90

MAP 70 75 73 67 49 70

PAP 17/12 20/10 35/18 34/10 21/17 30/21

CO 2.9 0.2 3.0 0.1 3.7 0.3 4.1 0.2 1.2 0.0 2.5 0.1

HR after stimulation 139(AAI140) 139(AAI140) 136(AAI140) 136(VVI140) 139(AAI140) 139(VVI140) 139(AAI140) 139(VVI140) 140(AAI140) 139(VVI140)

PAP 21/18 19/10 37/19 34/17 37/16 31/15 23/17 24/16 34/26 29/20

CO 3.1 0.1 2.7 0.1 3.8 0.1 2.6 0.1 4.6 0.2 2.8 0.1 1.5 0.0 0.9 0.1 2.5 0.1 1.6 0.1

Cardiac output (CO) was compared after AAI and VVI stimulation in animals No. 47. In animal No. 3 correct positioning of Swan-Ganz-catheter was not possible and hemodynamic parameters could therefore not be assessed. In animal No. 6 (*) hemodynamic parameters were measured after prolonged cardiac arrest and successful resuscitation (low output). HR heart rate, MAP mean arterial pressure (mmHg), PAP pulmonary artery pressure (mmHg), CO cardiac output (ml/min).

According to the results of the intraoperative pacemaker assessment it was not necessary to change the position of the leads to improve the pacing or sensing threshold. All leads of the left-sided VATS group revealed good pacing and sensing threshold values. The cardiac output was approximately 1.6 times higher during AAI-mode as compared to VVI-mode pacing at a heart rate of 140 beats/min. This corresponds to the wellknown beneficial effect of AV-sequential dual-chamber pacing systems on hemodynamics. The narrow right thoracic cavity in these small animals barely allowed placement of the pacing leads to the right atrium and right ventricle. The right-sided VATS implantation technique was therefore abandoned because of these anatomic difficulties, as well as the risk of heart herniation through a large pericardial window and the risk of fixation of central endovenous catheters during placement of the sutures in the right atrial wall. The limited survival rate of animals after successful pacemaker implantations by the VATS technique was related to postoperative respiratory problems, most probably due to the single lung ventilation. One animal had a severe postoperative infection. In none of the survivors did displacement of the pacemaker leads occur. Close contact between the pacemaker leads to the myocardium was documented by histology. Conclusions This study demonstrates that video-assisted implantation of epicardial atrial and ventricular pacemaker leads is feasible. However, there are many technical difficulties which still need to be overcome with additional experience and technical improvement of the system. The VATS technique has the potential to minimize the surgical trauma associated with open implantation of atrioventricular pacemaker systems in children, especially if the left ventricle needs to be stimulated.

References
1. Bielefeld MR, Yano OJ, Cabreriza SE, Treat MR, Kirby TJ, Spotnitz HM (1993) Thoracoscopic placement of implantable cardioverterdefibrillator patch leads in sheep. Circulation 88/5 II: 447451 2. Brodman RF, Furman S, Fell SC, Foxx MJ, Frame RA, Fisher JD, Kim SG, Roth JA, Ferrick KJ (1994) ICD implantation via thoracoscopy, mailslot thoracotomy, and subxiphoid incision. Ann Thorac Surg 57(2): 475476 3. Burke RP, Wernovsky G, van der Velde M, Hansen D, Castaneda AR (1995) Video-assisted thoracoscopic surgery for congenital heart disease. J Thorac Cardiovasc Surg 109(3): 499508 4. Cuschieri A (1994) Technique of thoracoscopic insertion of epicardial pacemaker. In: Cuschieri A, Buess G, Pe rissat J (eds) Operative manual of endoscopic surgery 2. Springer-Verlag, Berlin, pp 121129 5. Ely SW, Kron IL (1993) Thoracoscopic implantation of the implantable cardioverter defibrillator. Chest 103(1): 271272 6. Esperer H-D, Singer H, Riede FT, Blum U, Mahmoud FO, Weniger J (1993) Permanent epicardial and transvenous single- and dualchamber cardiac pacing in children. Thorac Cardiovasc Surg 41: 21 27 7. Furman S, Hayes DL, Holmar DR (1993) A practice of cardiac pacing. Futura, Mount Kisco, pp 261308 8. Gilette PC, Zeigler VL, Winslow AT, Kratz JM (1992) Cardiac pacing in neonates, infants, and preschool children. PACE Pacing Clin Electrophysiol 15: 20462049 9. Hesslein PS, Williams WG, Finaly CD (1987) Dual chamber pacing in children: transvenous versus epicardial leads. PACE Pacing Clin Electrophysiol 10: 441449 10. Kolesov EV, Lukashev SN, Gaiduk AI (1993) Pericardioscopic implantation of electrodes for myocardial electrocardiostimulation. Endosc Surg Allied Technol 1: 275276 11. Kratz JM, Gilette PC, Crawford FA, Sade RM, Zeigler VL (1992) Atrioventricular pacing in congenital heart disease. Ann Thorac Surg 54: 485489 12. Mack MJ, Acuff TE, Ryan WH (1993) Implantable cardioverter defibrillator: the role of thoracoscopy. Ann Thorac Surg 56(3): 739740 13. Molina JE, Dunnigan AC, Crosson JE (1995) Implantation of transvenous pacemakers in infants and small children. Ann Thorac Surg 59: 659694 14. Obadia JF, Lehot JJ, Thevenet F, Kirkorian G, Touboul P, Chassignolle JF (1994) New approach for implantation of automatic defibrillators using videothoracoscopy. Ann Cardiol Angeiol (Paris) 43(7): 384388 15. Walsh CA, Mc Alister HF, Andrews CA, Steeg CN, Eisenberg R, Furman S (1988) Pacemaker implantation in children: a 21-year experience. PACE Pacing Clin Electrophysiol 11: 19401944

Surg Endosc (1997) 11: 11591162

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Selection of locally advanced gastric carcinoma by preoperative staging laparoscopy

D. M. DUgo,1 R. Persiani,1 F. Caracciolo,2 P. Ronconi,1 C. Coco,1 A. Picciocchi1
1 2

Department of General Surgery, A. Gemelli Hospital, Catholic University of Rome, Largo Gemelli, 8, 00168Rome, Italy Department of General Surgery, G. Moscati Hospital, Via Otranto, 2, 83100Avellino, Italy

Received: 3 April 1997/Accepted: 19 May 1997

Abstract Background: The present study is a prospective evaluation of immediate preoperative laparoscopy compared to ultrasound/computed tomography (US/CT) staging for gastric cancer in a series of 100 patients observed at two major Italian hospitals from April 1995 through September 1996. Methods: After a complete preoperative work-up all c-M0 patients underwent laparoscopy immediately prior to an eventual surgical exploration. pTNM was considered as the gold standard for the evaluation of the results. Results: Laparoscopy detected 21 unsuspected M+ cases out of 100. As regards locally advanced tumors, laparoscopy showed a sensibility of 69.7% for T3 and 89.6% for T4, significantly higher than US/CT staging (23.2% and 48.3%, respectively; p < 0.02). In this series laparoscopic staging altered clinical staging in 58% of cases. Conclusions: This procedure plays two crucial roles in the preoperative evaluation of advanced gastric cancer: It makes it possible to avoid unnecessary surgical exploration in M+ cases and, to date, it represents the most reliable and economic tool for the selection of locally advanced tumors in the light of neoadjuvant treatment. Key words: Laparoscopy Gastric cancer staging Neoadjuvant chemotherapy

ventional preoperative workup based on ultrasonography (US) and computed tomography (CT) [6, 14, 17], which implies a high percentage of unhelpful exploratory laparotomies. The value of preoperative video-laparoscopy in the prevention of unnecessary surgical exploration has been evidenced by previous reports [1, 3, 5, 7, 11, 17], but to date an even more crucial task has been given to preoperative laparoscopy. In fact, after 30 years of adjuvant treatment trials, it has been ascertained that patients who present with locally advanced but resectable disease (T3-4, N-any) have a low chance of cure after a complete surgical resection followed by an adjuvant chemotherapeutic regimen. Consequently an increasing number of institutions throughout the world are now recommending a neoadjuvant treatment protocol for locally advanced gastric cancers, provided that these are properly staged [16]. In this light laparoscopy has been increasingly employed for screening high risk patients with resectable advanced disease [6, 12, 16] even if no published study until 1996 had prospectively evaluated the actual diagnostic efficacy of preoperative videolaparoscopy compared to a conventional staging based upon US and CT scan. Materials and methods
In April 1995 we started a prospective study on the clinical value of immediately preoperative video-laparoscopy for gastric cancer. In September 1996 the protocol was closed after the enrollment of 100 eligible patients from two major hospitals (A. Gemelli Medical Center, Rome, Italy; G. Moscati Hospital, Avellino, Italy). We proceeded to immediate preoperative laparoscopy in every patient with proven adenocarcinoma of the stomach after a complete diagnostic workup (upper G.I. X-ray, endoscopy, liver US, and abdominal CT); extra information obtained from endoscopic ultrasound imaging (EUS) in a selected group of patients was not considered for the present study. Patients with clear-cut unresectable tumors (e.g. evidence of liver metastasis by US or CT scanning, neoplastic ascites, pelvic dissemination of tumor, extraabdominal lymphoadenopathy) were excluded from this protocol. Patients with tumors of the gastric cardia were also excluded. All patients underwent laparoscopic staging under general anesthesia immediately before an eventual surgical exploration. With the patient supine on the operating table a 12-mm Hasson trocar is inserted in the peritoneal cavity at the umbilicus and a 30 angled laparo-

Although declining in incidence, gastric cancer remains a common malignant tumor in Italy and a major cause of cancer death since most patients (as in the rest of the western world) have locally advanced or metastatic disease on presentation. These cases are often understaged by a con-

Presented at the annual meeting of the Society of American Gastrointestinal Endoscopic Surgeons (SAGES), San Diego, California, USA, 1922 March 1997 Correspondence to: D. M. DUgo

1160 Table 1. M-staging: sensitivity of lap-stage in 100 patientsa M0 c-stage lap-stage

a

Table 2. N-staging: laparoscopy vs US/CT Sensitivity 100% US/CT Laparoscopy p NSa

a

M+ 21

Agreement with the gold standard 51% 58%

K (Cohen test) 0.321 0.416

100 79

C-stage: US/CT staging; lap-stage: laparoscopic staging

NS: Not statistically significant

scope is passed through it. A second 5-mm port is then inserted under direct vision, lateral to the rectus muscle in the left subcostal region. Unless peritoneal dissemination or neoplastic ascites are evident, a third 1012mm trocar is inserted in the right abdominal quadrant over the umbilical line to provide an alternative angle of view and possibly direct access to the lesser sac [2]; 100300 ml of saline is then instilled in the subphrenic area and in the pelvis and then aspirated for delayed cytologic examination. Laparoscopic staging is conducted following an inverted TNM mode, evaluating the M factor first, followed by the N and the T factors. The parietal and serosal surfaces of the peritoneum are inspected initially for malignant implants. In female patients the ovaries must be visualized in a Trendelenburg position in order to exclude Krukenberg metastases. The visible surfaces of omentum, diaphragm, and liver are then inspected. A palpating probe passed through the second 5-mm port to the left of the midline permits manipulation of the left liver lobe and the small bowel. Tilting the table facilitates the approach to the area of the stomach that is covered by the left liver lobe. Before determining the extent of tumor infiltration on the gastric wall, the perigastric nodes are inspected along the greater and the lesser curvature, on the gastrohepatic ligament, and at the hepatic hilum. Most of the anterior wall of the stomach can be inspected without further manipulation. Therefore, we did not initially employ a third port. During the study, however, it became evident that a supplementary instrument is needed for a more accurate evaluation of posterior infiltration of the tumor. Occasionally the laparoscope may be inserted through the third 12-mm port in order to penetrate the lesser sac through the foramen of Winslow. More often, when the tumor originates from the posterior wall or a posterior fixity is suspected, one of the probes may be carefully inserted behind the stomach through an avascular area of the greater omentum. The posterior tumor mass may then be lifted to test its mobility. No laparoscopic ultrasound technique (LUS) was employed in the course of the present study. Conventional clinical staging (c-stage) and preoperative laparoscopic staging (lap-stage) were registered separately on a database. Macroscopic exploration, cytology, and pathologic examination of biopsies and surgically resected specimens were considered as the gold standard for pTNM staging. The pTNM classification was used to compare the results obtained from conventional preoperative US and CT staging with the laparoscopic findings. The agreement of the two diagnostic procedures (c-stage vs lap-stage) with the gold standard was statistically verified by the Cohen test, and their sensitivity was measured.

aroscopy failed to show a statistically significant difference from conventional staging. It must be stressed that the use of LUS with lymph node biopsies was not considered in our study protocol, as it is our current practice to perform a D2 lymphadenectomy in all resectable cases. The N-stage is certainly an important determinant of tumor curability, but in clinical practice the decision on surgical resectability is mainly guided by assessment of the T-stage. As regards the evaluation of the T factor alone, laparoscopy correctly evaluated 56 out of 72 locally advanced T3 and T4 cases with a specific sensitivity of 69.7% and 89.6%, respectively (Table 3). In this subset of extraserosal tumors, a case-by-case analysis showed that false results were due to subtle alterations in the gastric serosa over the tumor, which pathology showed had not been infiltrated, or due to undetected posterior extension of the tumor to the transverse mesocolon or to the body of the pancreas. Laparoscopy shows an overall TNM staging accuracy of 72%, compared to 38% for US/CT. Differences are more marked as regards locally advanced tumors: If stages IIIa, IIIb, and IV are considered separately, the predictive value of laparoscopic staging is 87.5% (Table 4). Out of the total 100 patients, lap-stage altered c-stage in 58% of the cases. No perioperative complications were associated with the laparoscopic procedure. Discussion In Europe and in the United States curative resections are performed in less than 60% of all gastric cancers [4, 18]. It has also been stated [1, 6, 14, 15] that more than 25% of newly diagnosed gastric cancer patients will be found (at subsequent laparotomy) to have been understaged, with severe ethical, economic, and quality-of-life implications. Perioperative complications occur in 1223% of unresectable patients, with a reported mortality ranging up to 21.1%; patients who do not undergo a surgical exploration have a longer mean survival than those who have laparotomy or bypass [7, 18]. Even before the introduction of endocameras, in a series of 360 gastric cancer patients who underwent laparoscopy, Possik and others [9, 13] reported a sensitivity of 83% in the detection of peritoneal metastases and 87% in the detection of liver metastases. Kriplani and Kaipur [11] performed preoperative staging video-laparoscopy in a series of 40 patients who were considered resectable after US and CT workup. In their series laparoscopy showed the presence of unsuspected M+ disease in 11.5% and unresectable T4 cancer in 27.5% of patients. In a study performed at the University of Munich, Germany [5, 15], 23% of 111 patients

Results As regards the M factor, laparoscopy detected 21 M+ cases out of the total 100 cases, all of which had been clinically staged as M0 by preoperative US and CT. Compared to the gold standard, there were no false positives and no false negatives in this subset, if the macroscopic appearance of the tumor is considered. A theoretical exception can be represented by two out of the 79 patients declared M0 after laparoscopic staging, whose peritoneal lavage appeared to be microscopically contaminated by tumor cells (Table 1). However, the presence of free-floating cancer cells in the peritoneal cavity is not in itself a contraindication to surgical resection; thus our data confirm that laparoscopy can be considered the most specific method for detecting a macroscopic peritoneal dissemination of tumor or unsuspected subcapsular liver metastases, ruling out unresectable cancers from an unnecessary open exploration. As regards N-staging sensitivity (Table 2), standard lap-

1161 Table 3. T-staging: sensitivity of laparoscopy vs US/CT Cases verified by pathology Overall T3 T4 100 43 29 US/CT 40% 23.2% 48.3% Laparoscopy 81% 69.7% 89.6% p <0.02 <0.02 <0.02

Table 4. TNM staging: sensitivity of laparoscopy vs US/CT Cases verified by pathology Overall Stage III Stage IV 100 36 31 US/CT 38% 19.4% 25.8% Laparoscopy 72% 58.3% 90.3% p <0.02 <0.02 <0.02 Fig. 1. Treatment algorithm for gastric cancer.

staged by laparoscopy were found to have a previously undetected carcinomatosis. In a recently published prospective evaluation of 103 gastric cancers, mainly located in the upper third of the stomach, Stell [17] stresses that both US and CT have severe limitations in staging these tumors; in his study laparoscopy clearly showed a better accuracy in the detection of peritoneal and hepatic metastases. As regards the detection of M+ disease, the data obtained from our prospective study [7] confirm the superiority of preoperative laparoscopy compared to conventional staging. Its routine utilization makes it possible to avoid an unnecessary noncurative operation for many patients, since M+ disease should not be resected in the absence of obstruction or bleeding. However, this is not the only good reason for extending the use of laparoscopy in the staging of gastric carcinoma. To date, after conclusive reports from extensive clinical trials [4, 18], postoperative chemotherapy has not shown evident results in high risk tumors; such risk is directly related to cancer penetration beyond the gastric serosa (T3 and T4) [10]. There are sound theoretical bases for the selection of these locally advanced cases for a neoadjuvant treatment regimen; nevertheless, no published study to date has prospectively and statistically demonstrated the actual efficacy of laparoscopic-based patient selection compared to conventional staging techniques. In this particular context our prospective study has demonstrated a highly significant difference between laparoscopy and US/CT staging as regards locally advanced tumors (69.7% vs 23.2% for T3; 89.6% vs 48.3% for T4). We think that neoadjuvant regimens for technically resectable gastric cancers are to be administered only in the context of research studies; since there is no definite proof of their efficacy [1], patients with a good outcome with surgery alone must be spared the substantial toxicities of these treatments. We now believe that there is enough evidence to consider laparoscopy the most accurate and economic tool for detecting serosal invasion of a gastric tumor: Preoperative laparoscopic staging is therefore appropriate to select locally advanced cancers for primary neoadjuvant chemotherapy in the hope of locally controlling improvement and possibly increasing the percentage of delayed curative resections with tumor downstaging [8, 19, 20]. Based upon our results, the current algorithm for operable gastric cancer at our institution (Fig. 1) attributes pre-

operative laparoscopy a central role. Moreover, the application of second look laparoscopy in selected cases offers the unique possibility of verifying the possible sites of residual disease after preoperative treatment.

Conclusions Immediately preoperative staging laparoscopy is a safe, simple, and relatively cheap procedure at most medical institutions. As regards locally advanced gastric cancer, our data support the belief that to date laparoscopy plays two fundamental roles: On one hand, it undoubtedly represents the most specific method for detecting previously unsuspected M+ disease, thus sparing unresectable cases from unnecessary surgical exploration. On the other hand, following the increasing application of neoadjuvant treatment protocols for stage IIIaIIIb tumors, we have seen that laparoscopy permits the most reliable and accurate selection of T3 and T4 cases, avoiding an unhelpful delay of surgery in nonadvanced cases. Accurate staging by preoperative videolaparoscopy allows for a more homogeneous evaluation of the treatment results in the context of research studies; finally, the application of second-look laparoscopy in selected cases may offer a chance to verify a possible tumor downstaging and to detect the sites of residual disease after neoadjuvant chemotherapy.

References
1. Ajani JA, Mansfield PF, Ota DM (1995) Potentially resectable gastric carcinoma: current approaches to staging and preoperative therapy. World J Surg 19: 216220 2. Asencio Arana F (1994) Laparoscopic access to the lesser sac in gastric cancer staging. Surg Laparosc Endosc 4(6): 438440 3. Brady PG, Peebles M, Goldshmid S (1991) Role of laparoscopy in the evaluation of patients with suspected hepatic or peritoneal malignancy. Gastrointest Endosc 37(1): 2730 4. Brennan MF, Karpeh MS (1996) Surgery for gastric cancer: the American view. Semin Oncol 23(3): 352359 5. Colin-Jones DJ, Rosch T, Dittler HG (1993) Staging of gastric cancer by endoscopy. Endoscopy 25: 3048

1162 6. Conlon KC, Karpeh MS (1996) Laparoscopy and laparoscopic ultrasound in the staging of gastric cancer. Semin Oncol 23(3): 347351 7. DUgo DM, Coppola R, Persiani R, Ronconi P, Caracciolo F, Picciocchi A (1996) Immediately preoperative laparoscopic staging for gastric cancer. Surg Endosc 10: 996999 8. Fink U, Stein HJ, Schuhmacher, Wilke HJ (1995) Neoadjuvant chemotherapy for gastric cancer: an update. World J Surg 19: 509516 9. Gross E, Bancewicz J, Ingram G (1984) Assessment of gastric cancer by laparoscopy. Br Med J 288: 1577 10. Kelsen DP (1996) Adjuvant and neoadjuvant therapy for gastric cancer. Semin Oncol 23(3): 379389 11. Kriplani AK, Kaipur BLM (1991) Laparoscopy for preoperative staging and assessment of operability in gastric carcinoma. Gastrointest Endosc 37(4): 441443 12. Lightdale CJ (1992) Laparoscopy for cancer staging. Endocopy 24: 682686 13. Possik RA, Franco EL, Pires DR, Wohnrath DR, Ferreira EB (1986) Sensitivity, specificity and predictive value of laparoscopy for the staging of gastric cancer and for the detection of liver metastases. Cancer 58: 16 14. Rohde H, Gebbensleben B, Bauer P (1989) Has there been any improvement in the staging of gastric cancer? Findings from the German Gastric Cancer TNM Study Group. Cancer 64: 2452481 15. Sendler A, Dittler HJ, Feussner H (1995) Preoperative staging of gastric cancer as precondition for multimodal treatment. World J Surg 19(4): 501508 16. Siewert JR, Maruyama K (1995) Whats new in gastric cancer? (Editorial) World J Surg 19: 483 17. Stell DA, Carter CR, Stewart I, Anderson JR (1996) Prospective comparison of laparoscopy, ultrasonography and computed tomography in the staging of gastric cancer. Br J Surg 83: 12601262 18. Wanebo HJ, Kennedy BJ, Chmiel J, Steele GJ, Winchester D, Osteen R (1993) Cancer of the stomach. A patient care study by the American College of Surgeons. Ann Surg 218(5): 583592 19. Wils J (1996) The treatment of advanced gastric cancer. Semin Oncol 23(3): 397406 20. Yonemura Y, Sawa T, Kinashita K, Matsuki N, Fushida S, Tanaka S, Omijama S, Takashima T, Kimura H, Kamata T, Fujimura T, Sugijama K, Shima K, Miyazaki I (1993) Neoadjuvant chemotherapy for high-grade advanced gastric cancer. World J Surg 17: 256252

Surg Endosc (1997) 11: 12181220

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Hand-assisted laparoscopic vertical banded gastroplasty

Initial report
D. I. Watson, P. A. Game
The Royal Adelaide Centre for Endoscopic Surgery, Department of Surgery, Level 6, Royal Adelaide Hospital, Adelaide, South Australia, 5000, Australia Received: 4 March 1997/Accepted: 25 March 1997

Abstract. Laparoscopic approaches to surgery for morbid obesity offer to reduce the morbidity associated with conventional weight reduction surgery. This paper describes a hand-assisted laparoscopic technique for vertical banded gastroplasty, a method which shortens and simplifies the laparoscopic approach to this established open surgical procedure. Key words: Morbid obesity Vertical banded gastroplasty Hand-assisted technique

Because nonsurgical methods of weight control usually fail to achieve desired weight reduction targets, and morbid obesity is a significant health problem associated with poor self-esteem and an increased risk of premature death [13], patients continue to present to interested surgeons for gastric restriction procedures. A variety of operative techniques have been developed and evaluated, and studies now demonstrate good long-term outcomes following both gastric bypass and vertical banded gastroplasty [5, 8]. Following the recently demonstrated advantages of reduced hospital stay, reduced wound-related morbidity and shortened convalescence following other laparoscopic procedures [10, 15], interest has been generated in laparoscopic variants of gastric restriction procedures for morbid obesity. Due to the simplicity of the placement procedure, the laparoscopic placement of an adjustable gastric band has generated most interest [1, 3, 9]. However, the equivalent open surgical procedure was not widely used before the advent of laparoscopic placement, and long-term results following laparoscopic placement are not yet available. An incidence of gastric obstruction requiring surgical revision has been reported following this laparoscopic procedure [12, 14]. In comparison, vertical banded gastroplasty performed
Correspondence to: D. I. Watson

through an upper midline abdominal incision has been used widely for the operative treatment of morbid obesity, and has a well-established role [8]. Lonroth et al. [6] have recently described a laparoscopic technique for vertical banded gastroplasty. Our own early experience with a similar technique applied after initial laboratory development (unpublished data) found this to be a technically demanding procedure, particularly with the current limitations of laparoscopic instrumentation which can make establishing an initial gastric window with a circular stapling instrument difficult. However, with the recent development of equipment which enables surgeons to introduce their own hand into the insufflated peritoneal cavity during laparoscopic surgery [2], we have developed a modified technique for laparoscopic vertical banded gastroplasty, which simplifies the performance of this procedure.

Methods Surgical technique

Following the induction of general anesthesia, the patient is placed in the reverse Trendelenburg position with both legs extended in stirrups and with the hips minimally flexed. The surgeon stands between the patients legs and an assistant on the patients left. Initial insufflation achieved through a Veress needle inserted immediately below the left costal margin in the midclavicular line is followed by the insertion of three laparoscopic ports (Fig. 1). A 12-mm port (A) is inserted immediately above the umbilicus, providing access for either the laparoscope or a dissecting instrument. A second 12-mm port (B) is placed in the left midclavicular line just above the level of the umbilicus, providing alternative access for the laparoscope or for dissecting and suturing instruments. The third port (C) is a 5-mm port which is placed laterally in the left flank just below the level of the umbilicus. A 5-mm incision is made in the epigastrium, for the passage of a large Nathanson liver retractor (Cook Medical Technology, Eight Mile Plains, Queensland, Australia) which is then attached to a self-retaining retraction system. This provides excellent exposure of the operative field and eliminates the need for an extra assistant. A 7-cm-long transverse incision is made, approximately 35 cm above the level of the umbilicus, and centered over the right midclavicular line.

1219 stomach and manipulated past the stapler along the lesser curve aspect to ensure that an adequate gastric lumen remains at the future exit point of the proximal gastric pouch. Once the stapler is fired, access is available for the passage of one of the blades of the 30-mm linear cutting stapler (Ethicon ELC-30, Johnson & Johnson) which is used to partition the stomach. With the bougie remaining in place to calibrate the proximal gastric pouch, the blades of the stapler are manipulated so that they lie parallel to the lesser curve. The gastric wall is retracted laterally to ensure that the volume of the created proximal pouch is not too large. This maneuver is facilitated by the surgeons hand. The stapler is progressively fired two or three times to reach the angle of His, fashioning a divided gastroplasty, whose proximal pouch will contain between 20 and 30 ml of liquid or solid material. The lesser omentum is next dissected from the lesser curve adjacent to the distal end of the staple line, creating a small window. This can usually be achieved using careful diathermy dissection. A grasper is then passed from left to right, behind the distal part of the gastric pouch, through the small window adjacent to the lesser curve. A 1-cm-wide, 6-cm-long piece of Marlex mesh is pulled through the lesser curve window and wrapped around the distal outlet of the gastric pouch, while the calibrating bougie remains in place. The Marlex band is sutured firmly around the bougie calibrated stoma with two or three 2/0 polypropylene sutures to restrict the outlet of the proximal pouch, completing the procedure. The bougie is removed and a nasogastric tube is passed into the upper stomach. This tube is used to inflate the proximal stomach with 0.9% sterile saline solution while the outlet is compressed between two fingers to check for possible leakage from the staple lines. The nasogastric tube is left in place overnight.

Postoperative care
A barium contrast X-ray is obtained on the 1st postoperative day to exclude a staple line leak and to verify the adequacy of the surgical anatomy. Oral fluids are commenced on the 1st postoperative day, soft food on 2nd, and discharge from hospital occurs on the 3rd. Fig. 1. Port placement for hand-assisted vertical banded gastroplasty. A 11 mm, B 11 mm, C 5 mm, D liver retractor, E Dexterity Pneumo Sleeve.

Initial experience
Two patients (one male and one female) have undergone hand-assisted laparoscopic vertical banded gastroplasty. Preoperative weights were 116 and 119 kg (body mass index 37 and 50). One of the procedures was combined with a laparoscopic cholecystectomy. Operating time was 100 min for each procedure. Both patients had an uncomplicated postoperative course, were discharged on the 3rd postoperative day, and resumed normal physical activity within 3 weeks of surgery. The first patient, a policeman, returned to work 1 week after surgery. Following short-term follow-up of 3 months one patient has lost 27 kg weight and is eating food of normal consistency including red meat. The other patient has lost 10 kg weight during the first 2 months following surgery and is eating soft food without difficulty.

This is deepened through all layers of the abdominal wall to allow the placement of a Dexterity Pneumo Sleeve (Pilling-Weck USA, Research Triangle Park, NC). This allows the repeated introduction of the surgeons left hand as well as a circular stapling instrument into the peritoneal cavity without the loss of pneumoperitoneum and laparoscopic exposure. The assistant manipulates the laparoscope and assists with a grasping instrument placed through the left flank port (C) while the surgeon uses his left hand for manipulation and dissection and manipulates laparoscopic instruments through either of the 12-mm ports. Surgery commences by using left-hand-finger dissection to open an avascular window in the lesser omentum below the hepatic branch of the vagus nerve, thereby rapidly accessing the lesser sac. The surgeons index and middle finger are passed behind the body and cardia of the stomach, toward the angle of His, digitally checking for retrogastric adhesions and lifting the upper part of the gastrosplenic mesentery forward to facilitate dissection of a window at the angle of His, above the uppermost short gastric vessel. This ensures that stapling instruments can be easily passed behind the upper stomach for later gastric partitioning. Next, a point adjacent to the lesser curvature of the stomach is identified 6 cm below the gastroesophageal junction and 2 cm lateral to the lesser curve and marked for the passage of the circular stapling instrument used to fashion a transgastric window. The head of a 20-mm circular stapler with its detachable sharp spike attached (Ethicon Endosurgery, Johnson & Johnson) is then introduced into the peritoneal cavity through the Dexterity Pneumo Sleeve, manipulated into the lesser sac, and pushed through the posterior and then anterior gastric walls at the previously marked site. Most of this manipulation is performed using the left hand, aided by laparoscopic dissecting and cutting instruments. Once the stapler head is in place it is held securely by the assistant using a laparoscopic grasping instrument, and the sharp spike is removed. The body of the stapler is next introduced, through the Dexterity Pneumo Sleeve, alongside the left hand, joined to the stapler head, and closed. Before firing, a 36 Fr bougie is passed into the

Discussion Since 1993 a number of centers have described laparoscopic techniques for surgery for morbid obesity, including descriptions of laparoscopic vertical banded gastroplasty [6], gastric bypass [7], and the laparoscopic placement of an adjustable gastric band [1, 3, 9]. Uncontrolled prospective follow-up of patients who have undergone each of these procedures has demonstrated reduced respiratory morbidity and more rapid recovery. However, each technique is associated with potential difficulties. The procedures of totally laparoscopic vertical banded gastroplasty and gastric bypass are technically demanding and may exceed the laparoscopic skills currently possessed by the average surgeon. Our own earlier experience with totally laparoscopic vertical banded gastroplasty (unpublished data) confirmed the technical dif-

1220

ficulties associated with manipulation of the circular stapler through the gastric wall to fashion the initial gastric window, as well as difficulties guaranteeing that the proximal gastric pouch was an appropriate size. Laparoscopic placement of an inflatable adjustable gastric band offers to reduce the complexity of the laparoscopic approaches and may be simplest laparoscopic procedure for general surgeons with variable laparoscopic skill levels to perform. For this reason, it has recently been taken up by many surgeons in Australia and Europe. However, unlike vertical banded gastroplasty, it fails to replicate a widely practiced open surgical technique, and it is associated with specific problems. An incidence of proximal pouch enlargement due to slippage of the band has been reported. This can lead to proximal gastric obstruction which requires surgical revision [12, 14]. Also reported is an incidence of infection of the implantable prosthesis, and even erosion of the prosthesis into the lumen of the stomach [4, 11]. The use of the Dexterity Pneumo Sleeve during laparoscopic vertical banded gastroplasty simplifies the laparoscopic performance of this established open surgical procedure. Similar advantages have been reported for the use of this device during laparoscopic colon resection [2]. In our experience, the use of the sleeve reduced the operating time required for laparoscopic vertical banded gastroplasty by approximately 1 h and greatly facilitated the establishment of the gastric window and the proximal gastric pouch. The use of the surgeons hand may make this laparoscopic option feasible for surgeons with less advanced laparoscopic skills. Significantly, the use of a muscle-splitting incision to provide access for the surgeons hand did not adversely impact on the length of hospital stay. The 3-day postoperative stay compares favorably with the 37 days reported following alternative laparoscopic techniques [2, 3, 6, 9]. In comparison with the placement of an adjustable laparoscopic gastric band, the consumable cost for this procedure in our institution is reduced considerably; US$1,900 vs US$900 including all staplers and the Dexterity Pneumo Sleeve. Hand-assisted laparoscopic vertical banded gastroplasty offers a viable alternative to other laparoscopic approaches for patients with morbid obesity.

Acknowledgment. The authors wish to acknowledge the assistance of Mr. Jonathan Meek, Ethicon Endosurgery, Australia, who provided valuable assistance during preliminary animal studies performed before commencing clinical applications of laparoscopic gastric partitioning techniques.

References
1. Belachew M, Legrand MJ, Defechereux TH, Burtheret MP, Jacquet N (1994) Laparoscopic adjustable silicone gastric banding in the treatment of morbid obesity. A preliminary report. Surg Endosc 8: 1354 1356 2. Benelman WA, Ringers J, Meijer DW, de Wit CWM, Bannenberg JJG (1996) Laparoscopic-assisted colectomy with the Dexterity Pneumo Sleeve. Dis Colon Rectum 39: S59S61 3. Cadiere GB, Bruyns J, Himpens J, Favretti F (1994) Laparoscopic gastroplasty for morbid obesity. Br J Surg 81: 1524 4. Chelala E, Cadiere GB, Favretti F, et al. (1996) Laparoscopic gastroplasty (LASGB). Obesity Surg 6: 316 (Abstract) 5. Hall JC, Watts J McK, OBrien PE, et al. (1990) Gastric surgery for morbid obesity. The Adelaide study. Ann Surg 211: 419427 6. Lonroth H, Dalenback J, Haglind E, et al. (1996) Vertical banded gastroplasty by laparoscopic technique in the treatment of morbid obesity. Surg Laparosc Endosc 102: 107 7. Lonroth H, Dalenback J, Haglind E, Lundell L (1996) Laparoscopic gastric bypass. Another option in bariatric surgery. Surg Endosc 10: 636638 8. Mason EE (1992) Gastric surgery for morbid obesity. Surg Clin North Am 72: 501513 9. Morino M, Toppino M, Garrone C, Morino F (1994) Laparoscopic adjustable silicone gastric banding for the treatment of morbid obesity. Br J Surg 81: 11681169 10. Schirmer BD, Edge SB, Dix J, Hyser MJ, Hanks JB, Jones RS (1991) Laparoscopic cholecystectomy. Treatment of choice for symptomatic cholelithiasis. Ann Surg 213: 665676 11. Susewind M, Klein S, Kunath U (1996) Problems in laparoscopic gastric banding. Obesity Surg 6: 320 (Abstract) 12. Toppino M, Morino M, Garrone C, Comba A (1996) Disappointing long-term results of laparoscopic adjustable silicone gastric banding. Surg Endosc 10: 572 (Abstract) 13. Van Itallie TB (1979) Obesity: adverse effects on health and longevity. Am J Clin Nutr 32: 27232733 14. Vertruyen M, Cadiere GB, Himpens J, Bruyns J (1996) Reoperation for total and irreversible food intolerance after laparoscopic adjustable silicone gastroplasty banding (LASGB). Surg Endosc 10: 570 (Abstract) 15. Watson DI, Jamieson GG, Baigrie RJ, Mathew G, Devitt PG, Game PA (1996) Laparoscopic surgery for gastro-oesophageal reflux: beyond the learning curve. Br J Surg 83: 12841287

Surg Endosc (1997) 11: 1226

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

Laparoscopic and conventional closure of perforated peptic ulcer

We read with interest the paper by Miserez and colleagues (Surg. Endosc. 1996; 10: 831836), in which the authors conclude from the results of their study that laparoscopic closure of perforated peptic ulcer is technically feasible. However, the safety of the method and the benefit for the patient would need proof by means of a randomized controlled trial. As we agree with the authors on the need for further research in the field we would like to make some remarks concerning the design of such future studies. While the precise monitoring of pain intensity and consumption of analgesics is appreciated in this study, a major concern is that a surgical standard of open closure was not met in the laparoscopic procedure. Open repair of perforated ulcer included local excision of the ulcer formation. In contrast to the open procedure, the authors neglected local ulcer excision in the laparoscopic operation. Compromises of surgical standards set in conventional open surgery may disparage minimal invasive surgery and therefore must not be accepted. In an experimental study in the rat we have recently reported that carbon dioxide pneumoperitoneum accentuates the extent and severity of peritonitis, assessed by histopathologic peritonitis severity score and microbiologic cultures of abdominal swabs and blood samples, when the interval between gastric ulcer perforation and pneumoperitoneum lasts 12 h or longer [1]. As more than 30% of patients suffering from peptic ulcer perforation are subject to surgical intervention with a delay of more than 24 h between perforation and surgery [2], this experimental finding may be of clinical importance. In the report by Miserez and associates the time lag between ulcer perforation and surgical intervention is only mentioned indirectly in the data summarized by the Mannheim Peritonitis Index. We would like to draw attention to the association between duration of peritonitis and adverse events in laparoscopic surgery for peritonitis-related conditions. Therefore, detailed information should be given on the time interval between perforation and surgical intervention in future studies. In the study by Miserez and colleagues, conversion to open surgery was necessary in some patients in which laparoscopic surgery was started but proved technically infeasible. The fact that these patients were redistributed to the conventional surgery group is troubling. In light of our experimental study, patients who have been under the influence of pneumoperitoneum should not be transferred to the conventional surgical group after conversion. This may distort the results. Furthermore, it is questionable whether a patient who underwent BII gastrectomy should be included in the group for conventional closure of perforated peptic ulcer. We are strongly convinced that further sound experimental and clinical studies, which focus on potential risks of laparoscopic management of peritonitis, are needed to define the impact laparoscopic surgery holds in the therapeutic concept of peritonitis-related conditions.

References
1. Bloechle C, Emmermeann A, Treu H, Achilles E, Mack D, Zornig C, Broelsch CE (1995) Effect of a pneumoperitoneum on the extent and severity of peritonitis induced by gastric ulcer perforation in the rat. Surg Endosc 9: 898901 2. Lanng C, Palnas Hansen C, Christensen A, Thagard CS, Lassen M, Klarke A, Tonnesen H, Ostgard SE (1988) Perforated gastric ulcer. Br J Surg 75: 758759

C. Bloechle A. Emmermann C. Zornig

Department of Surgery University of Hamburg Martinistr. 52 20251 Hamburg Germany

Surg Endosc (1997) 11: 11631166

Surgical Endoscopy
Springer-Verlag New York Inc. 1997

The effect of laparoscopy on the movement of tumor cells and metastasis to surgical wounds
G. Mathew, D. I. Watson, T. Ellis, N. De Young, A. M. Rofe, G. G. Jamieson
The Royal Adelaide Centre for Endoscopic Surgery, Department of Surgery, Royal Adelaide Hospital, Adelaide, South Australia, 5000, Australia Received: 17 March 1997/Accepted: 6 June 1997

Abstract Background: A variety of mechanisms have been proposed to explain tumor growth in port sites following laparoscopic cancer surgery. We devised two experimental models to determine whether carbon dioxide (CO2) insufflation during laparoscopic surgery influences the movement of tumor cells and leads to tumor implantation and growth in surgical wounds. Methods: Model 1: Viable adenocarcinoma cells were introduced into the upper abdomen of six syngeneic immunecompetent rats during laparoscopy with CO2 insufflation; the same procedure was followed for a further six rats during gasless laparoscopy. A length of plastic tubing introduced through the anterolateral aspect of the rats left lower abdominal wall was used to vent the insufflation gas through the abdomen of a recipient rat for 30 min. After 21 days, the peritoneal cavity and surgical wounds of the recipient rat were examined for implanted tumor. Model 2: A suspension of radiolabeled adenocarcinoma cells was introduced into the upper abdomen of five rats during laparoscopy with CO2 insufflation and an additional five rats during gasless laparoscopy. A length of plastic tubing introduced through the anterolateral aspect of the left lower abdominal flank was used to vent the insufflation gas through phosphate-buffered saline solution. After 30 min, the solution was counted for radioactivity. Results: Tumor growth occurred at the site of both the insufflation and venting ports in the second rat in five of the six rats from the group undergoing insufflation, but it was found in none of the gasless laparoscopy group (p 0.015). In the second model, significant transfer of tumor cells to the vented gas occurred only in the rats undergoing laparoscopy with insufflation (median, 2.71% versus 0% of the introduced labeled cells; p 0.008). Conclusions: Carbon dioxide insufflation results in tumor dissemination during laparoscopy, leading to port site metastasis. Gasless laparoscopy may prevent this problem. Key words: LaparoscopyInsufflationTumor WoundMetastasis

Recent reports of tumor metastasis to the access wounds used for the laparoscopic excision of tumors has raised concern about the suitability of laparoscopic techniques for the resection of abdominal and thoracic malignancies [4, 12]. Unfortunately, evidence from human studies that might support or refute these concerns remains anecdotal, and is based principally on case reports [9]. However, recent studies using small animal models have found an increased incidence of wound metastasis following laparoscopy in the presence of intraabdominal malignancy [6, 7]. In addition, studies using large animal models have shown that laparoscopy for malignancy can lead to the contamination of laparoscopic instruments and trocar shafts with tumor cells [1, 5, 10]. Different mechanisms have been postulated to explain this phenomenon [7, 9, 10]. Metastasis could be the result of direct contact between laparoscopic instruments or trocars and a tumor, resulting in wound contamination when the instruments are withdrawn during the laparoscopic procedure or the trocars are removed at the end of the operation [1, 10]. Alternatively, the tumor cells might be aerosolized by the insufflation gas, then transported by the gas to the laparoscopic wounds, instruments, and trocar shafts, thus resulting in wound contamination without direct physical contact with tumor-bearing tissue. We have previously reported a study of an immunecompetent syngeneic rat model that showed an increased incidence of wound metastasis following laparoscopy with CO2 insufflation [7]. The finding that this adverse effect can be minimized by use of gasless laparoscopic exposure techniques [8, 11] suggests that CO2 insufflation during laparoscopy promotes wound metastasis. To investigate this hypothesis, we developed two additional models. Materials and methods Preparation of viable adenocarcinoma suspension
The tumor cell line (DAMA) used for these studies was originally derived from a spontaneously occurring mammary adenocarcinoma native to the Dark Agouti (DA) rat strain [3]. Viable DAMA cells were prepared using the standard technique of homogenizing fresh tumors propagated in and resected from the female carrier rats. Subcutaneous tumors of 5 g were excised from the carriers and dissected from any surrounding tissue. The

Correspondence to: D. I. Watson

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Fig. 1. Port placement for experiment 1. Arrows indicate the direction of gas flow during CO2 insufflation. A primary insufflation port and minilaparoscope port, B 20-gauge cannula for the introduction of tumor suspension, C 14-gauge plastic tubing, D 18-gauge venting cannula. tumor was then diced and washed in phosphate-buffered saline (PBS) (sterile 10 mmol/L sodium phosphate buffer, pH 7.0, containing 0.15 mol/L sodium chloride). The tissue was homogenized in a motor-driven Potter Elvehjen homogenizer (radial clearance, 0.5 mm) (Wheaton Homogenizer, Millville, NJ, USA). The crude debris was removed by filtration through sterile gauze. The cell suspension was then centrifuged four times in 10 volumes of PBS at 400 g, each for 1 min. The viability of the suspension was assessed by trypan blue exclusion, and the cell number was determined using a Neubauer counting chamber (Improved Neubauer, Weber, UK; depth 0.1 mm, 1/400 m2). The final concentration was adjusted to give 1 108 viable cells in 1.0 ml of sterile PBS. This solution was then introduced into the epigastric region of the peritoneal cavity of all animals at the commencement of each experiment.

Fig. 2. Port placement for experiment 2. Arrows indicate the direction of gas flow during CO2 insufflation. A primary insufflation port and minilaparoscope port, B 20-gauge cannula for the introduction of tumor suspension, C 14-gauge plastic tubing, D PBS solution.

Model 1
Under general anesthesia, using a combination of halothane and nitrous oxide supplemented with oxygen via a close-fitting mask, 24 male syngeneic immune-competent DA rats underwent one of two different surgical procedures. The respiratory status of each animal was closely monitored, and the procedures were performed under sterile operating conditions. The model consisted of donor rats that underwent either a laparoscopic procedure facilitated by conventional CO2 pneumoperitoneum or a gasless laparoscopic procedure. A recipient rat was connected to the donor rat by a 14-gauge plastic tube inserted into the abdomen (Fig. 1). This cannula arrangement provided a conduit for carbon dioxide insufflation gas to be vented first from the donor rat through the peritoneal cavity of the recipient rat and subsequently to the atmosphere in the insufflation group, as well as a control group, using gasless laparoscopic exposure. Six pairs of rats underwent a laparoscopic procedure facilitated by conventional CO2 pneumoperitoneum. Pneumoperitoneum was initially established in both the donor and recipient rats using a Veress needle placed through a small stab incision in the right anterolateral abdominal wall of each rat. We slid a disposable mini-laparoscopy cannula (Imagyn Medical, Laguna Niguel, CA, U.S.A.) over the needle to provide access for a 2-mm mini-laparoscope (Imagyn Medical) attached to a conventional laparoscopic camera. Under laparoscopic vision, a second mini-laparoscopy cannula was introduced through the left lower quadrant of the anterior abdominal cavity of the donor rat only. This cannula was then removed, and the end of a piece of 14-gauge plastic tubing (7 cm in length) was introduced through the wound so that 5 mm lay within the peritoneal cavity. A pursestring suture was placed around the cannula to achieve a gas-tight seal. Under laparoscopic vision, an 18-gauge cannula was introduced through the anterolateral aspect of the left lower abdominal wall of the recipient rat. It was left open to allow subsequent venting of the insufflation gas. Once the insufflation tube was disconnected from the recipient, the mini-laparoscopy cannula used for initial laparoscopy was removed. Then the other end of the plastic tubing, which had been placed earlier in the donor rat, was introduced through the wound and secured with a pursestring suture. Insufflation was commenced through the mini-laparoscopy cannula remaining in the donor. The cannulae and tubes were checked during insufflation to ensure that gas leaked through the open cannula in the recipient rat only.

A 20-gauge intravenous cannula was then introduced through the abdominal wall in the epigastric region of the donor, and 1.0 ml of the DAMA cell suspension containing 1 108 cells was introduced slowly, before sealing of the cannula to prevent subsequent gas leakage. CO2 gas was insufflated at a flow rate of 0.2 L/min and a maximum pressure of 6 mm Hg for 30 min, achieving a constant circulation of carbon dioxide through the peritoneal cavities of the two animals. To prevent direct contamination of the cannulae with tumor cells or siphoning of fluid from the donor to the recipient, care was taken to ensure that the cannula tips in both rats did not come into contact with the abdominal contents or any intraabdominal fluid. The insufflation phase was terminated by disconnecting the plastic tubing from the recipient, before removal of the other 18-gauge cannula. All wounds were closed with 3/0 Prolene sutures. The donor rats were killed 6 days after surgery. An autopsy was performed to establish tumor growth within the peritoneal cavity of these rats and therefore confirm the viability of the tumor cell suspension. The recipient rats were housed in the laboratory for 21 days before being killed. At autopsy, the abdomen was opened and examined for tumor deposits. All of the surgical access wounds were examined for evidence of tumor implantation. Histological examination using hemotoxylin-and-eosin staining of formalin-fixed, wax-embedded tissue was used to confirm the macroscopic assessment. A further six pairs of rats underwent laparoscopic surgery using a protocol identical to the study using carbon dioxide insufflation, except that insufflation was omitted and a gasless technique was used [11]. A Veress needle without insufflation was used for the introduction of the first trocar in each rat. A working space in the abdominal cavity of each rat was maintained by suspending the anterior abdominal wall from a wire frame, using multiple 3/0 silk sutures passed through the abdominal wall skin and anchored to the frame. The experiment was concluded in a fashion similar to the insufflation study, with an autopsy of the donor rat at 6 days (to confirm the viability of the tumor cell suspension) and the recipient rat at 21 days.

Model 2
A suspension of 2 108 DAMA cells in 2.0 ml of sterile PBS was prepared using the methods described earlier. These cells were then radiolabeled with 51Crsodium chromate 1MBq, 0.6 g Cr ions (CRIM4, Radioisotypes, Australia). The cell suspension was incubated for 60 min with 51 Cr, and the cells were washed five times in sterile PBS. In all instances, >75% incorporation of the 51Cr into the tumor cells was obtained. A total of 10 DA rats were used for this phase of the study. Five of them underwent laparoscopy with carbon dioxide insufflation, and five had gasless laparoscopy. Laparoscopic exposure was achieved using methods identical to those in the first model. A Veress needle was introduced through a stab incision in the left anterolateral abdominal wall of each rat, and a mini-laparoscopy cannula was used to provide access for the minilaparoscope (Fig. 2). A second mini-laparoscope cannula was introduced

1165 Table 1. Recovery of radiolabelled cells in model 2 With insufflation (median; range) % Recovery of introduced cells Absolute no. of cells recovered 2.71% (0.4117.32) p 0.008 2.7 106 (4.1 105 to 1.8 107) Gasless laparoscopy (median; range) 0.00% (0.000.03) 0.0 (0.0 to 3 104)

Discussion Even though many surgeons still question the significance of metastases arising in trocar wounds following laparoscopic surgery for malignant disease, there is increasing evidence, both clinical and laboratory, to suggest a need for greater caution in the application of laparoscopy to malignant growths [2, 4, 69, 12]. It has been postulated that wound metastasis occurs following the direct contamination of laparoscopic instruments with tumor cells during the laparoscopic manipulation of malignant tumors, with resultant spread to abdominal wall wounds by direct transfer when trocars and instruments are withdrawn from the peritoneal cavity [1, 2, 5, 10]. In this instance, the development of barrier strategies to protect the wounds during laparoscopic surgery may be sufficient to overcome the problem. However, it is also possible that cells are moved around by the insufflation gas used for laparoscopy and transferred to wounds without any direct physical contact with contaminated instruments [6, 7]. If this is the case, then the phenomenon of port site metastasis may be a prognostic marker, indicating generalized tumor spread due to adverse effects of the laparoscopic environment. Previous experimental studies using small animal models in our department and elsewhere [6, 7] have shown an increased incidence of metastasis to trocar wounds following laparoscopy in the presence of intraabdominal malignancy. Further studies have demonstrated that the use of gasless laparoscopic techniques during laparoscopic manipulation of solid tumors and tumor cell suspensions results in a reduced incidence of wound metastasis and a pattern of tumor spread similar to that seen following conventional open laparotomy [2, 8, 11]. This work suggests that insufflation is a major contributing factor in the development of laparoscopic wound metastasis. Studies by Whelan et al. [13], however, have produced conflicting results. Their studies used a quantity of tumor cells that was 1000 times smaller than that used in the current studies, and insufflation was continued for only 10 min. Outcome differences may therefore reflect a doseresponse relationship. Our initial cell suspension studies [8] suggested that tumor implantation patterns are influenced by the number of viable cells introduced into the peritoneal cavity. It is possible that the duration of exposure to the laparoscopic environment may also be important. In the current studies, the presence of wound metastases in the recipient rat in most of the rats undergoing carbon dioxide insufflation, and none of the rats in the gasless laparoscopy group, provides additional evidence that insufflation is essential for the promotion of wound metastases. However, since it could be argued that the study outcomes were due to siphoning of fluid between the donor and recipient rats, we took care to prevent this from happening. Furthermore, if siphoning of fluid had occurred, metastases would be expected in the recipient rat in the gasless laparoscopy group, and they should have been more prominent around the inflow port wound in the recipient rats. However, tumor nodules of equal size occurred at both the inflow and outflow port wounds in the recipient rats undergoing insufflation. These results were reinforced by the second study, which investigated the movement of cells from the donor rat. We found significant numbers of cells in the

through the left lower quadrant anterior abdominal wall and then removed to allow a 7-cm length of 14-gauge plastic tubing to be introduced through the wound, 5 mm into the peritoneal cavity, in a fashion similar to the first experiment. A pursestring suture was done to maintain an airtight seal around the tubing. A 20-gauge intravenous cannula was then introduced through the abdominal wall in the epigastrium. The open end of the plastic tubing was placed in a container of 4 ml of PBS with its opening 5 mm below the fluids surface. Laparascopic CO2 insufflation was then commenced, and the vented gas was bubbled though the PBS solution. Gasless laparoscopic exposure was obtained in a fashion similar to our first experiment. The cannula and tubing positions were identical to those used in the insufflation group. At this point, 1 ml of the radiolabelled DAMA cells (1 108), premeasured for radioactivity, was introduced into the peritoneal cavity through the 20-gauge cannula in the epigastrium of each rat. The cannula was then sealed. To prevent siphoning of fluid through the venting tube, care was taken to ensure that the tubing within the peritoneal cavity did not come into direct contact with the abdominal contents or any intraabdominal fluid. Thirty minutes after the introduction of the radiolabelled DAMA cells, the rats were killed and the radioactivity of the PBS solution was determined using a gamma counter. It was expressed as a percentage of the total introduced radioactivity of the cell suspension at the commencement of the study. In addition, 4 ml of a control solution of uncontaminated PBS was scanned to document background radioactivity levels.

Statistics
Fishers exact test was used for the analysis of the data sets expressed by 2 2 contingency tables in experiment 1; the Mann-Whitney U test was used for analysis of the radioactivity levels in experiment 2. The protocol for these studies was approved by the Animal Ethics Committees of the Institute of Medical and Veterinary Science and the University of Adelaide, Adelaide, South Australia.

Results In the first experiment, extensive tumor growth was evident throughout the peritoneal cavity of all donor rats, irrespective of surgical technique, and at all wound sites. This finding confirmed the viability of the cell suspension in all instances. Nodular tumor metastases were found around the site of both the venting port and the inflow tubing site in five of six of the recipient rats in the group that underwent carbon dioxide insufflation. Tumor was not seen at any other sites within the abdominal cavity of the recipient rats. None of the recipient rats in the gasless laparoscopy group developed metastatic tumor, either around the venting cannula site (p 0.015, Fishers exact test), or elsewhere. The results from the second model are summarized in Table 1. The recovery of the cells introduced into the peritoneal cavity in the rats undergoing laparoscopy with insufflation was significantly greater than for the rats that had gasless laparoscopy (p 0.008).

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gas vented from the peritoneal cavity of rats undergoing insufflation, versus either no cells or very few when using gasless laparoscopy. A larger inoculum of tumor cells was introduced into the donor rats in these studies than that used in earlier studies [8] both to maximize the likelihood of metastases developing in the recipient rats and to optimize the likelihood of demonstrating differences in tumor implantation patterns between the insufflation and gasless laparoscopy groups. Similarly, because of the possible small tumor load in the recipient rats, a longer latency period of 21 days (previously, 7 days) was used to maximize the likelihood of tumor growth being clinically evident in the recipient rats. The current studies assess a laparoscopic environment that may be different from that thought to exist during clinical laparoscopic cancer surgery. The CO2 leak of 0.2 L/min in the rat model, when extrapolated to clinical surgery, represents a gas leak of 1015 L/min. Also, a large number of tumor cells were introduced into the peritoneal cavity, and no operative intervention was performed. Nevertheless, it should be remembered that during clinical laparoscopic surgery, high-volume gas leaks do occur during some procedures, and the inadvertent liberation of large numbers of tumor cells into the peritoneal cavity can occur. Although careful laparoscopic technique can help to avoid the liberation of tumor cells, this cannot be guaranteed preoperatively, and tumor cell spillage remains a real possibility. If this spillage is combined with CO2 insufflation and a significant gas leak, the necessary environment for clinically significant port site metastases may be created. These new studies employing two additional experimental models suggest that laparoscopy with carbon dioxide insufflation can transport tumor cells to laparoscopic access wounds and result in the development of metastases. It appears that this effect can be prevented by the use of gasless laparoscopy. The precise mechanism for the phenomenon, however, is not clear. Whether the differences are due to the mechanical effects of insufflation, or a metabolic effect specific to CO2 gas, or a combination of these two, requires further elucidation. Though our investigation confirms the need for caution when applying laparoscopic techniques to malignant growth in humans, further investigation of gasless laparoscopy in clinical studies is also needed.

Acknowledgment: This work was supported by grants from the University of Adelaide Faculty of Health Sciences and from the National Health and Medical Research Council of Australia. Dr. G. Mathew is the recipient of a grant from the Burnside War Memorial Hospital, Burnside, South Australia.

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