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HISTORY
The anatomic and surgical history of the diaphragm is shown in Table 8-1.
Table 8-1. Anatomic and Surgical History of the Diaphragm
Homer (9th
Cent. B.C.)

Probably knew about the diaphragm as an anatomic entity because of his precise descriptions of Trojan War battle wounds

Empedocles
of
Agrigentum
(500-430
B.C.)

One of the first to study the physiology of respiration

Hippocrates
(460-359
B.C.)

"Wherefore, I say, that it is the brain which interprets the understanding. But the diaphragm has obtained its name [
;{
= mind}]
from accident and usage, and not from reality or nature, for I know no power which it possesses, either as to sense or understanding, except
that when the man is affected with unexpected joy or sorrow, it throbs and produces palpitations, owing to its thinness, and as having no belly
to receive anything good or bad that may present themselves to it, but it is thrown into commotion by both these, from its natural weakness."

Plato (427327 B.C.)

The diaphragm is not involved with respiratory movements, but separates parts of the soul

Aristotle
(384-322
B.C.)

The diaphragm, "separating the better upper part from the lower part which only helps the upper," does not play any role in respiration; "war
wounds in the region of the diaphragm provoke laughter because of the heat which arises from the injury"

Praxagoras
of Cos (fl.
335 B.C.)

Believed that the purpose of respiration was not to cool the innate heat, but rather to provide nourishment for the psychic pneuma (animal
spirits, or aerial principle)

Erasistratus
(3rd Cent.
B.C.)

The diaphragm is the main muscle of respiration

Galen (129200 A.D.)

Studied the diaphragm through the chest and the abdomen. Described diaphragmatic actions and how the rib cage is moved by the diaphragm
in spinal cord sections; the diaphragm can move upward with an isovolume maneuver during the period of expansion of the rib cage.

Oribasius
(4th Cent.)

Studied the interaction between the abdominal and rib cage muscles in maintaining the position of the diaphragm

Par
Riverius
(early 17th
Cent.)

1610 Described diaphragmatic hernias


First description of congenital diaphragmatic hernia

Morgagni

1761 Earliest clear description of hiatal hernia. First case of parasternal hernia through the foramina of Morgagni (spaces of Larrey).

Petit

1774 First description of eventration of the diaphragm

Percy

1812 A "sardonic smile" is a very sensitive indication of diaphragmatic injuries

Bright

1836 Described a massive hiatal hernia

Bochdalek

1848 Hernia through the pleuroperitoneal canal. (The name "foramen of Bochdalek" antedates the understanding of the development of the
pleuroperitoneal canals; perhaps the term "Bochdalek hernia" is inaccurate.)

Marsh

1867 First clinical case of eventration

Aue

1902 First successful repair of diaphragmatic hernia (report published in 1920)

Grenier de
Cardenal &
Bourderou

1903 Earliest reported case of defect of the central tendon

Broman

1905 Presented a schematic diagram of the adult diaphragm, indicating areas derived from various embryonic components

Morison

1923 First repair of eventration

kerlund

1926 One of the first to classify hernias of the esophageal hiatus; may have been first to use term "hiatus hernia"

Bremer

1943 Studied the diaphragm and its hernias

Allison

1951 Studied the anatomy of repair of hiatal hernia

Sweet

1952 Described anatomic characteristics and repair of hiatal hernia and congenital short esophagus

Wells

1954 Studied the development of the human diaphragm and the pleural sacs

Adzick et al. 1985 Used prenatal ultrasonography to diagnose congenital diaphragmatic hernia in 88 of 94 infants
Krzyzaniak
& Gray

1986 First report of accessory septum transversum

Connors et
al

1990 Used ECMO (extracorporeal membrane oxygenation) preoperatively and postoperatively in repair of congenital diaphragmatic hernia

Harrison et

1990 Treated six carefully selected fetuses with severe congenital diaphragmatic hernia, using open fetal surgery (all died)

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al
History table compiled by David A. McClusky III and John E. Skandalakis.
References
Derenne JP, Debru A, Grassino, Whitelaw WA. The earliest history of diaphragm physiology. Eur Respir J 1994;7:2234-2240.
Derenne JP, Debru A, Grassino, Whitelaw WA. History of diaphragm physiology: the achievements of Galen. Eur Respir J 1995;8:154-160.
Longrigg J. Medicine and the Lyceum. In: van der Eijk PJ, Horstmanshoff HFJ, Schrijvers PH (eds). Ancient Medicine in its Socio-Cultural Context. Amsterdam: Rodopi,
1995, pp. 331-343.
Proctor DF (ed). A History of Breathing Physiology. New York: Dekker, 1995.
Skandalakis JE, Gray SW. Embryology for Surgeons (2nd ed). Baltimore: Williams & Wilkins, 1994.

EMBRYOGENESIS

Normal Development
The mammalian diaphragm is a composite organ formed from four embryonic sources (Fig. 8-1A):
Transverse septum
Mediastinum (dorsal mesentery)

Pleuroperitoneal membranes
Muscles of the body wall

Fig. 8-1.

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Comparison of embryonic and adult diaphragms. A. Embryonic components of diaphragm. B. Adult diaphragm. Sites of closed pleuroperitoneal canals occupy a
relatively small area in adult diaphragm. E, Esophagus; IVC, Inferior vena cava; A, Aorta. (Modified from Skandalakis LJ, Colborn GL, Skandalakis JE. Surgical
anatomy of the diaphragm. In: Nyhus LM, Baker RJ, Fischer JE. Mastery of Surgery, 3rd Ed. Boston: Little, Brown, 1997; with permission.)

With the data currently available, it is not possible to delineate the exact boundaries of the four embryonic components of the adult diaphragm.

Transverse Septum
During the third embryonic week, the growing head fold of the embryo transfers a wall of mesoderm to a position cranial to the open midgut and caudal to
the heart (Fig. 8-2). This mesoderm forms the ventral component of the future diaphragm, its largest part.
Fig. 8-2.

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Formation of transverse septum. A. Third week. Heart and pericardium form anterior to head of embryo. B. Fourth week. Rapid growth of head rotates heart and
mesoderm, which will become transverse septum. Arrows indicate direction of growth of transverse septum. (Modified from Skandalakis LJ, Colborn GL, Skandalakis
JE. Surgical anatomy of the diaphragm. In: Nyhus LM, Baker RJ, Fischer JE. Mastery of Surgery, 3rd Ed. Boston: Little, Brown, 1997; with permission.)

The cranial surface of the septum also contributes to the connective tissue of the pericardium. The caudal surface provides the connective tissue of the
capsule and stroma of the liver.
The transverse septum is responsible for the genesis of the tendinous part of the diaphragm (central tendon).

Mediastinum (Dorsal Mesentery)


The mediastinum is the thick dorsal mesentery of the foregut, containing the future esophagus and the inferior vena cava (Fig. 8-1A). It is bilateral, and
continuous anteriorly with the transverse septum and posteriorly with the axial mesoderm. By posterior and caudal extension, it splits to form the
diaphragmatic crura.

Pleuroperitoneal Membranes
At about the eighth embryonic week, the pleuroperitoneal membranes close the right and left communication between the pleural and peritoneal cavities.
Originally, the membranes form a large part of the developing diaphragm (Fig. 8-1A), but relative growth of other elements reduces their contribution to a
small area (Fig. 8-1B). Perhaps the pleuroperitoneal membranes form the lateral parts of the diaphragm.
The pleuropericardial fold may be embryologically related to the pleuroperitoneal membranes. The pleuropericardial fold is a single fold between the
transverse septum and the xiphoid process.

Muscles of the Body Wall


By caudal excavation of the thoracic wall, myotomes of the seventh to twelfth segments contribute the lateral component of the diaphragm and form the
costodiaphragmatic recesses. This process produces the final domed shape of the diaphragm.
Phrenic nerve fibers are present in the diaphragm by the seventh week. Muscle fibers can be found a week later. Before birth there is a preponderance of
white, fast-twitch, low oxidative fibers. An increase in red, slow-twitch, high oxidative fibers takes place after birth until, by the eighth postnatal month,
about 55 percent of the fibers are of the red, slow-twitch type. These fibers are less easily fatigued than are white fibers.
It is not certain whether all muscle fibers originate from the thoracic wall and migrate centrally or originate in the transverse septum and migrate
peripherally. But because the diaphragm's muscle fibers are innervated by C-2, 3, 4 (phrenic nerve) and the thoracic nerve's contribution to diaphragmatic
innervation is confined to sensory fibers to the peripheral portion, it is more likely that the muscle fibers originate from the transverse septum.

Descent of the Diaphragm


In the third week, the transverse septum most likely lies at approximately the level of the third cervical vertebra. By the eighth week, the developing
diaphragm descends to its final position at the level of the first lumbar vertebra. Descent is probably due to very rapid growth of the vertebral column
(dorsal part of the embryo) (Fig. 8-3). The phrenic nerve, which originates from the third to fifth cervical levels, is carried caudad with the descending
diaphragm (Fig. 8-4).
Fig. 8-3.

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Descent of diaphragm. Numbers on right indicate vertebral levels. Numbers on left indicate embryonic length from 2 mm to 24 mm. Orientation of transverse
septum at given embryonic length shown on left. Arrows indicate stages of very rapid growth and descent of septum. O, Occipital region; C, Cervical; T, Thoracic; L,
Lumbar; Co, Celom. (Modified from Mall FP. Coelom and diaphragm. In: Keibel F, Mall FP, eds. Manual of Human Embryology. Philadelphia: JB Lippincott, 1910; with
permission.)

Fig. 8-4.

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Descent of diaphragm during development. Phrenic nerve arises from third to fifth cervical segments and follows diaphragm down to its final position. (Modified
from Skandalakis LJ, Colborn GL, Skandalakis JE. Surgical anatomy of the diaphragm. In: Nyhus LM, Baker RJ, Fischer JE. Mastery of Surgery, 3rd Ed. Boston: Little,
Brown, 1997; with permission.)

Congenital Anomalies
The enigmatic origin of congenital diaphragmatic defects can be summed up in two questions: Are embryologic entities that form the diaphragm present
without fusing? Or are these entities missing, so that diaphragmatic formation is impossible? This section will discuss congenital anomalies of the diaphragm
and their possible causes.

Diaphragmatic Agenesis
Diaphragmatic agenesis may be due to failure of formation of the diaphragmatic components, or their failure to join properly. Unilateral agenesis is rare;
bilateral agenesis is very rare. Pelizzo et al.2 reported 15 cases of diaphragmatic agenesis which were treated by muscle flap transposition.

Accessory and Duplicate Diaphragms


In rare instances, the hemithorax is divided into two spaces by an accessory sheet that can be fibrous, muscular, or both. Typically, the membrane
originates in the pericardial reflection. Its attachment ranges from the seventh rib to the apex of the pleura. Hypoplastic lung tissue is usually present in the
lower cavity. A hiatus in the membrane permits the passage of pulmonary vessels and bronchi. Anomalous pulmonary venous drainage into the inferior vena
cava is frequently associated.
An accessory diaphragm is usually located on the right, a condition equally distributed between the sexes. The first report of this anomaly was given by
Haeberlin in 1945.3 Becmeur and colleagues4 reviewed 31 cases of accessory diaphragm reported through 1995. Bruce et al.5 and Doi et al.6 both reported
cases of accessory diaphragm associated with pulmonary problems.
Differing from accessory diaphragm is an apparent duplication of the transverse septum, the ventral component of the diaphragm, reported by Krzyzaniak
and Gray.7 Both this defect and accessory diaphragm are amenable to surgical correction if no other severe defects are present.

Congenital and Acquired Diaphragmatic Hernias


During the first two months of fetal life, there is no pressure on the developing diaphragm from above or below. Above, the lungs are not inflated. Below,
the growth of the gut is taking place extra-abdominally into the umbilical cord. The first mechanical pressure on the diaphragm comes during the tenth week
when the intestines return from the umbilical cord to the abdomen. By that time, all the diaphragmatic components are normally in place and have sufficient
strength to contain the abdominal viscera. This may not be the case if the normal developmental timetable is disturbed.
A number of areas of the diaphragm may give way under pressure from the abdominal viscera. Most diaphragmatic hernias start in these small areas of
weakness and enlarge with age.
Kluth et al.8 reported abnormal development of the diaphragmatic anlage. They noted the production of congenital diaphragmatic hernia (CDH) in embryos
at the age of 13 to 14 days. They stated that a defect at the dorsal part of the diaphragm will permit an early hepatic entrance, but intrathoracic
positioning of the gut will be seen in very late stages (approximately on the 21st or 22nd day). Kluth and colleagues disagreed with the theory that the
pleuroperitoneal canals fail to close at the end of the embryonic period.
Beaudoin et al.9 examined the relationship between the position of the liver and the path of the ductus venosus and umbilical vein. Their aim was to aid in
evaluating the prognosis of a left CDH at prenatal ultrasound examination. Twenty dead fetuses (12 with a left CDH and 8 without) underwent radiographic
assessment, anatomic dissection and cross-sectional study. These authors found that as more of the liver was in the thorax, the angle between the ductus
venosus and the sagittal plane was greater and the angle between the ductus venosus and umbilical vein was less. Since these angles can be easily
measured by prenatal ultrasound, a prognosis can be determined before birth.
Weber et al.10 reported significant improvement in survival rates in cases of CDH with preoperative extracorporeal membrane oxygenation (ECMO). They
advised that immediate repair of CDH without the availability of ECMO support should be abandoned.
A very rare case of diaphragmatic hernia in identical twins was reported by Harris et al.11 This case illustrates the possibility that diaphragmatic hernia can
be an inheritable defect.

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The Fetal Treatment Center at the University of California-San Francisco has performed intrauterine repair of congenital hernias.12-15 Though Nyhus
expressed some concern about the procedure, he nevertheless felt it offers "truly amazing therapeutic vistas."16 Skandalakis and Gray17 call this a triumph
of surgery over congenital anomalies.

Read an Editorial Comment


Specific hernias are described below and summarized in Table 8-2.
Table 8-2. Characteristics of Diaphragmatic Hernias
Hernia

Anatomy

Sac and Herniated Organs

Remarks

Hernia through the


foramen of Morgagni
(retrosternal hernia,
parasternal hernia,
anterior diaphragmatic
hernia)

Congenital potential hernia through muscular hiatus on either


side of the xiphoid process

Sac present at first. May rupture


later, leaving no trace.

Rare in infants and children

Usually on the right; bilateral hernias are known. Actual


herniation usually the result of postnatal trauma.

Contents
Infants: liver
Adults: omentum
In both infants and adults may be
followed by colon and stomach later

Hernia through the


foramen of Bochdalek
(posterolateral hernia
of the diaphragm)

Congenital hernia through the lumbocostal trigone

Sac present in 10-15%

Heart and mediastinum shifted to


contralateral side

May expand to include almost whole hemidiaphragm. More


common on left.

Contents: small intestine usual;


Ipsilateral lung collapsed but
stomach, colon, and spleen frequent. usually not hypoplastic
Pancreas and liver rare. Liver only in
right-sided hernia.
Secondary malrotation is common
Craniorachischisis, tracheoesophageal fistula, and heart
defects are common

Traumatic hernia

Peritoneopericardial
hernia (defect of the
central tendon, defect

Acquired hernia

No sac

Tear, usually from esophageal hiatus across dome to left costal


attachment of diaphragm

Herniated organs: none at first;


spleen, splenic flexure of colon,
stomach, left lobe of liver later

Congenital hernia through central tendon and pericardium

Sac rarely present

Has been seen in newborns and


adults

Contents: stomach, colon

Perhaps traumatic in adults

of the transverse
septum)
Eventration of the
diaphragm

Rare
Congenital hernia

"Sac" is formed by the attenuated


diaphragm organs under elevated

Heart and mediastinum shifted to


contralateral side

Diaphragm is thin with sparsely distributed, but normal, muscle


fibers

Contents: normal abdominal dome of Ipsilateral lung collapsed, but


hemidiaphragm
normal. Malrotation and inversion
of abdominal viscera are common

Either or both sides may be affected


Phrenic nerve appears normal
Acquired: paralysis of normal muscle resulting from phrenic
nerve injury
Hiatal hernia

Sliding hiatal hernia

No sac

Congenital potential hernia. The enlarged esophageal hiatus of Sac lies anterior and lateral to the
the diaphragm permits the cardia of the stomach to enter the
herniated stomach
mediastinum above the diaphragm. The phrenoesophageal
ligament is attenuated and stretched. The gastroesophageal
junction may be freely movable or fixed in the thorax.
Contents: cardiac stomach

As above, without malrotation and


inversion
A large hiatus (admitting three
fingers) may be a predisposing
factor; actual herniation usually
occurs in late adult life
Has been seen in newborn infants

Fixed hiatal hernia


Paraesophageal hernia Congenital potential hernia. The cardia is in the normal position. Sac lies anterior to the esophagus
The fundus has herniated through the hiatus, into the thorax.
and posterior to the pericardium

An esophageal hiatus larger than


normal may be the predisposing
factor

Contents: fundus of stomach; body of Actual herniation occurs in late


stomach, transverse colon, omentum, adult life
and spleen may enter the sac later
Combined sliding and
Congenital potential hernia. The G-E junction, cardia and much
paraesophageal hernia of the greater curvature of stomach have herniated into the
thorax.

Sac lies anterior to esophagus and


posterior to pericardium in right
posteroinferior mediastinum. Sac may
contain fundus and body of stomach,
omentum, transverse colon, spleen.

A hiatus already enlarged by a


hiatus hernia. Progresses to
complete thoracic stomach with
volvulus.

Short esophagus

No sac

This lesion is rare. It appears to be


the result of failure of the
embryonic esophagus to elongate
sufficiently to bring the
gastroesophageal junction into the
abdomen.

Congenital hernia

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The cardia of the stomach is fixed in the mediastinum

Source: Modified from Skandalakis LJ, Colborn GL, Skandalakis JE. Surgical anatomy of the diaphragm. In: Nyhus LM, Baker RJ, Fischer JE, eds. Mastery of Surgery, 3rd
Ed. Boston: Little, Brown, 1997; with permission.

Sliding hiatal hernia is described briefly under congenital anomalies. Fixed hiatal hernia is mentioned with congenital short esophagus. Various hiatal hernias
(including combined sliding and paraesophageal hernias) are presented in the "Surgical Anatomy" section.
PARASTERNAL (MORGAGNI) DEFECTS
A small gap in the musculature on either side of the xiphoid process (foramina of Morgagni) exists between attachments of the diaphragm to the xiphoid
process and to the seventh costal cartilage. According to Van Trigt,18 herniations at these sites represent only about 3% of surgically treated hernias of
the diaphragm. The gaps are filled with fat, and the superior epigastric arteries and veins pass through them (Figs. 8-5 and 8-6).
Fig. 8-5.

Diaphragm from below, showing foramen of Bochdalek and foramen of Morgagni. Both are weak areas of potential herniation. Arrows indicate direction of
enlargement after herniation has begun. (Modified from Skandalakis LJ, Colborn GL, Skandalakis JE. Surgical anatomy of the diaphragm. In: Nyhus LM, Baker RJ,
Fischer JE. Mastery of Surgery, 3rd Ed. Boston: Little, Brown, 1997; with permission.)

Fig. 8-6.

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Diaphragm viewed from below. Area in contact with pericardium is indicated. Pericardial fibrous tissue is continuous with that of the diaphragm. E, Esophagus; IVC,
Inferior vena cava; A, Aorta. (Modified from Skandalakis JE, Gray SW (Eds). Embryology for Surgeons, 2nd Ed. Baltimore: Williams & Wilkins, 1994; with permission.)

Omental herniation through the foramen of Morgagni was reported by Gossios et al.,19 Schmid et al.,20 and Kuster et al.21 Kuster and colleagues repaired
the hernia of a 67-year-old patient by a laparoscopic procedure. Lima et al.22 performed successful laparoscopic correction in a child without the use of a
prosthesis. Newman et al.23 also reported laparoscopic repair of Morgagni hernias. They attested to the usefulness of diagnostic laparoscopy.
Lin and Maginot 24 reported an unusual case of a woman 2 days postpartum with bowel incarceration and obstruction within her Morgagni hernia.
POSTEROLATERAL (BOCHDALEK) DEFECTS
This defect begins at the vertebrocostal trigone, above and lateral to the left lateral arcuate ligament (Fig. 8-5). At the time when the intestines return to
the abdomen, this trigone is membranous, with few muscle fibers. Even at maturity it is variable in size and degree of muscular development. The spreading
of the muscle fibers permits a defect (the foramen of Bochdalek) to form and spread upward and forward on the dome of the diaphragm to include the site
of the embryonic pleuroperitoneal canal.
The defect may be as small as 1 cm in diameter, or it may involve almost the entire hemidiaphragm. Small intestine, stomach, colon, or spleen may be
present in the thorax at birth. During operation, usually no hernial sac is found. The defect is much more common on the left. The lung on the affected side
is usually hypoplastic (Fig. 8-7).
Fig. 8-7.

Herniation of intestines through foramen of Bochdalek compressing left lung. Mediastinum is shifted to right also reducing volume of right lung. (Modified from
Skandalakis LJ, Colborn GL, Skandalakis JE. Surgical anatomy of the diaphragm. In: Nyhus LM, Baker RJ, Fischer JE. Mastery of Surgery, 3rd Ed. Boston: Little,
Brown, 1997; with permission.)

The incidence of the hernia of Bochdalek is 1 in 2,500 live births.25 It is unilateral in 97% of cases, of which 75 to 90% occur on the left side; this is due,
apparently, to the earlier closure of the right pleuroperitoneal opening.

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Bilateral congenital posterolateral diaphragmatic hernia is extremely rare and difficult to diagnose. Zamir et al.26 reported a case of a female newborn with
this defect which was not diagnosed correctly until the left hemidiaphragm had been repaired. These authors cited eight other cases. In these reports, only
two patients survived and in only one was the preoperative diagnosis correct.
Ildstad et al.27 reported the case of a newborn with right-sided Bochdalek hernia, involving high apical insertion of the right hemidiaphragm at the level of
the second rib. Another report details two cases with high right diaphragmatic insertion.28
Ehren et al.29 stated that despite successful early repair of congenital diaphragmatic hernia through the foramen of Bochdalek, mortality is still high.
Perhaps this is due to pulmonary hypoplasia.
TRAUMATIC HERNIA
Herniation through muscular gaps is almost always the result of postnatal trauma. It occurs most often on the right. The herniated organs are usually the
omentum, colon, and, eventually, stomach. A sac may be present, or it may have ruptured and disappeared. There may be a predisposition to herniation in
persons with large foramina or in those with more fat between muscle fibers, but this has not been demonstrated.
Diaphragmatic rupture and rib fracture from paroxysmal coughing was reported by George et al.30 Intrathoracic pressure swings or opposing muscle forces
may have been the cause.
PERITONEOPERICARDIAL HERNIA
This rare hernia is embryologically inexplicable. It has been found in newborn infants and in adults. A hernial sac, or a trace of one, has been found in a few
instances.31-33 Because the defect is in the central tendon and the overlying pericardium, it originates in the part of the diaphragm formed by the
transverse septum.
Liver herniation into the pericardium through the central tendon has been reported.34-36 Investigators have found that symptoms of diaphragmatic hernia
may not appear until visceral incarceration occurs years after a causal injury.
EVENTRATION OF THE DIAPHRAGM
Congenital eventration (Fig. 8-8) describes the abnormal elevation of one leaf of the diaphragm. The entire leaf bulges upward, in contrast to the localized
defect of a foramen of Bochdalek hernia. The left side is affected more often than the right, and males are affected more often than females. The phrenic
nerve appears normal, but the leaf eventration may consist of a fascial layer with few or no muscle fibers between the pleura and peritoneum. The failure is
of muscularization rather than fusion of embryonic components. Intestinal malrotation is often associated. The lung is usually partially collapsed but not
hypoplastic. The mediastinum is shifted to the contralateral side, further reducing ventilation.
Fig. 8-8.

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Eventration of (left) diaphragm. Herniated abdominal organs remain beneath attenuated but intact leaf of diaphragm. Both lungs are compressed and mediastinum
is shifted to right. Compare with Fig. 8-7. (Modified from Skandalakis LJ, Colborn GL, Skandalakis JE. Surgical anatomy of the diaphragm. In: Nyhus LM, Baker RJ,
Fischer JE. Mastery of Surgery, 3rd Ed. Boston: Little, Brown, 1997; with permission.)

By contrast, acquired eventration is the result of phrenic nerve injury with normal musculature. The acquired lesion may be temporary. The congenital lesion
is permanent unless repaired.
An unusual case of eventration, combined with a hiatal hernia, was observed by Kaplan et al.37 They emphasized the importance of a transthoracic surgical
approach to correct the hernia. This avoids compromising the singular, intact phrenic nerve.
Eventration may be unilateral or bilateral38 and may rupture in later life. Such a case in a 51-year-old man was presented by Mitchell et al.39 Oh et al.40
described a case of bilateral congenital diaphragmatic eventration in a child that was complicated by perforated gastric volvulus. Eventration and acute
gastric volvulus in nine pediatric patients was reported by McIntyre et al.41 seven had eventration of the diaphragm. Sigmoid volvulus associated with
eventration of the diaphragm was reported by Tsunoda et al.42
Ascent of the stomach into the thorax through the esophageal hiatus of the diaphragm is a common and poorly understood lesion. It has been found in
stillborn infants, but its congenital origin is not well established.
SLIDING HIATAL HERNIA
The two requirements for a sliding hiatal hernia appear to be an enlarged hiatus and a weakened phrenoesophageal ligament. Because both conditions are
exacerbated by a hernia, the opening is further dilated and the ligament further stretched. When actual herniation occurs, there is an empty hernial sac on
the left side of the stomach. On the right, the small bare area of the stomach has no peritoneal covering (Fig. 8-9A).
Fig. 8-9.

Hiatal hernias. A, Sliding hiatal hernia seen from left. Gastroesophageal junction in thorax. B, Paraesophageal hernia seen from left. Gastroesophageal junction in
its normal location; fundus has herniated into thorax through hiatus anterior to esophagus. (Modified from Skandalakis LJ, Colborn GL, Skandalakis JE. Surgical
anatomy of the diaphragm. In: Nyhus LM, Baker RJ, Fischer JE. Mastery of Surgery, 3rd Ed. Boston: Little, Brown, 1997; with permission.)

PARAESOPHAGEAL HIATAL HERNIA

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If the gastroesophageal junction remains in its normal position, the fundus of the stomach may herniate through an enlarged hiatus anterior to the
esophagus. This may produce a paraesophageal hiatal hernia (Fig. 8-9B). There is a peritoneal sac anterior to the esophagus containing stomach and, in
extreme instances, transverse colon and omentum. Obstruction of the distal esophagus or the stomach is the usual result.
CONGENITAL SHORT ESOPHAGUS
Congenital short esophagus may simulate hiatal hernia. It is present in children, although it may be asymptomatic. The phrenoesophageal ligament is normal;
there is no hernial sac; and the left gastric artery is not displaced upward. The condition is often familial. It is more common in males. It is sometimes
associated with pyloric stenosis, malrotation, and Marfan's syndrome. We believe that although it is rare, short esophagus is a true congenital malformation.
Congenital short esophagus has long been the subject of debate. We illustrate three possible configurations:
Grossly normal esophagus
Irreducible, partially supradiaphragmatic true stomach
Irreducible, partially supradiaphragmatic true stomach existing from birth

In the grossly normal esophagus, the lower portion of the esophagus is lined by gastric mucosa (Barrett's esophagus).43 This condition may also be
described as heterotopic gastric mucosa. Far from being a benign anomaly as some authors believed,44 it may be a precursor of adenocarcinoma.45,46 This
metaplasia is often associated with gastroesophageal reflux.47,48
In the irreducible, partially supradiaphragmatic true stomach, the stomach has herniated into the thorax through an enlarged diaphragmatic esophageal
hiatus and become fixed. This is a true fixed hiatal hernia. Occasionally, the fixed hernia is not congenital but acquired, with tissue adhesions.
A finding of irreducible, partially supradiaphragmatic true stomach existing from birth is necessary for true "congenital short esophagus" (Fig. 8-10). It is
very rare.
Fig. 8-10.

Congenital short esophagus. (Modified from Gray SW, Skandalakis LJ, Skandalakis JE. Classification of hernias through the esophageal hiatus. In: Jamieson GG, ed.
Surgery of the Oesophagus. Edinburgh: Churchill Livingstone, 1988; with permission.)

Nyhus49 stated that short esophagus is not congenital. Rather, the shortening is caused by secondary factors in an esophagus of normal length. He
believed that infants with chalasia develop peptic esophagitis, followed by shortening of the esophagus.
Barrett 50 believed that congenital short esophagus could be recognized by the absence of a hernial sac. Branches of the left gastric artery do not pass
upward through the hiatus. Only a small percentage of hiatal hernias belongs to this group.17
Gozzetti et al.51 stated that acquired short esophagus is the result of gastroesophageal reflux of gastric and biliopancreatic fluids.

Other Anomalies Associated with Diaphragmatic Defects


It is known that diaphragmatic anomalies may be associated with other congenital anomalies such as Cantrell's pentalogy, tracheal agenesis, genetic
syndromes with omphalocele, gastroschisis, intestinal atresia and stenosis, and obstructive uropathy.

SURGICAL ANATOMY

Pediatric Diaphragm
Devlieger et al.52 reported the following observations based on anatomic and ultrasonographic studies of the diaphragm in newborn infants.

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The diaphragm inserts only on the anterior costodiaphragmatic rib cage border.
From anterolateral to posterior, the diaphragmatic insertion has an increasingly greater distance from the rib cage.
The dorsal diaphragm ends its free course at the 11th rib and continues caudally, ending between the 12th rib and the crista iliaca.

In the adult, the downward angulation of the ribs from posterior to anterior results in the so-called "pump-handle movement" of the ribs to increase the
anterior-posterior dimensions of the thoracic cavity. The same adult downward angulation of the ribs from medial to lateral results in a "bucket-handle
movement" of the lateral aspects of the ribs, to increase the transverse internal volume of the thorax. Because of the horizontal orientation of the ribs in
the newborn, rib excursion plays little part in respiratory mechanics. The infant relies almost wholly upon diaphragmatic breathing, with the most significant
changes in thoracic volume occurring in the vertical plane.
Devlieger and colleagues52 concluded that the diaphragm in the newborn acts as a bellows, moving mainly in the posterior part. In the adult, the diaphragm
acts like a piston (Fig. 8-11). They stated, therefore, that the diaphragm of the newborn, which has a flat curve because of its large angle of insertion on
the rib cage and small area of apposition, has only one physiological destiny: "to suck in the rib cage rather than air." It is this rib cage action that reduces
the area of apposition, and results in an increase in chest volume.
Fig. 8-11.

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Developmental changes of rib cage and anterior and lateral diaphragmatic insertion from birth (top) to adulthood (bottom). Stippled surface represents anterior
projection of diaphragm.

Adult Diaphragm
Origins and Insertions of the Diaphragmatic Musculature
The diaphragm is composed of a central tendinous area from which muscle fibers radiate in all directions toward their peripheral attachments (Fig. 8-12).
Fig. 8-12.

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Attachments of muscles of diaphragm seen from below. (Modified from Skandalakis LJ, Colborn GL, Skandalakis JE. Surgical anatomy of the diaphragm. In: Nyhus
LM, Baker RJ, Fischer JE. Mastery of Surgery, 3rd Ed. Boston: Little, Brown, 1997; with permission.)

STERNAL PORTION (ANTERIOR)


Paired slips of muscle originate from the xiphoid process and the aponeurosis of the transversus abdominis muscle. Small triangular spaces (foramina of
Morgagni) separate those slips from the costal fibers and from each other (Figs. 8-5 and 8-12).
Kleinman and Raptopoulos53 reported that anteriorly the diaphragm is attached to the lower six ribs and the sternum, from the anterior axillary line to the
xiphoid process. They stated that understanding this anatomy is helpful in assessing anterior paradiaphragmatic collections of air.
COSTAL PORTION (ANTEROLATERAL)
Muscle fibers arise from the cartilages of the seventh and eighth ribs, the cartilage and bony portions of the ninth rib, and the distal bony portions of the
tenth to twelfth ribs. Anteriorly, these origins are related to those of the transversus abdominis. On the twelfth rib, they are related to the attachment of
the thoracolumbar fascia.
LUMBAR PORTION (POSTERIOR)
Posteriorly, the diaphragmatic muscle arises from the crura and the medial and lateral arcuate ligaments (lumbocostal arches).
CRURA
The crura arise from the anterior surface of the first to fourth lumbar vertebrae on the right, the first two or three lumbar vertebrae on the left, and from
the intervertebral disks and the anterior longitudinal ligament. The crural fibers pass superiorly and anteriorly, forming the muscular arms that surround the
openings for the aorta and the esophagus. They then insert on the central tendon.
At their origins from the vertebrae, the crura are tendinous, becoming increasingly muscular as they ascend into the diaphragm proper (Fig. 8-13). Studies
of cadavers by Gray et al.44 found the crura to be tendinous in 90 percent of cadavers, posteriorly and medially, from their vertebral origins to the level of
the tenth thoracic vertebra. Sutures to approximate the crura should always be placed through the tendinous portions.
Fig. 8-13.

Crura consist of both tendinous and muscular tissue; only tendinous portion holds sutures. In 9 out of 10 persons, medial edge of crura is tendinous. (Modified
from Gray SW, Rowe JS Jr, Skandalakis JE. Surgical anatomy of the gastroesophageal junction. Am Surg 45(9):575-587, 1979; with permission.)

The pattern of the crural arms at the esophageal hiatus is variable. In 50 percent or more of the population, both right and left arms arise from the right
crus (Fig. 8-14 A-1, A-2, A-3). In another third or more, the left arm arises from the right crus and the right arm arises from both crura (Fig. 8-14 B-1, B-2,
B-3). The remaining individuals present a variety of uncommon patterns. Hiatal hernia is not associated with any specific hiatal pattern.

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Fig. 8-14.

Most common patterns of diaphragmatic crura. A-1 and B-1 seen from below. A-2, A-3 and B-2, B-3 seen from above. E, Esophagus; A, Aorta. (Modified from
Skandalakis LJ, Colborn GL, Skandalakis JE. Surgical anatomy of the diaphragm. In: Nyhus LM, Baker RJ, Fischer JE. Mastery of Surgery, 3rd Ed. Boston: Little,
Brown, 1997; with permission) (Data from Pataro VA, et al. Anatomic aspects of the esophageal hiatus: distribution of the crura in its formation. J Int Coll Surg
35:154, 1961.)

Delattre et al.54 considered the diaphragmatic crura a true extrinsic sphincter. However, we need more physiological studies to understand the actions of
the crura and their surgical applications.
ARCUATE LIGAMENTS
The lateral arcuate ligaments (lumbocostal arches) form the thickened aponeurotic tissue covering the cranial extremities of the quadratus lumborum
muscles. These tendinous bands attach to the twelfth ribs laterally and to the transverse processes of the first lumbar vertebra medially.
The medial arcuate ligaments (medial arches) compose the similarly-thickened fascia of the psoas muscles. They attach laterally to the transverse
processes of the first lumbar vertebra and medially to the body of the first or second lumbar vertebra. The medial arcuate ligaments are separated from
each other by the crura and the median arcuate ligament (to be described later).
The muscle fibers of the posterior portion of the diaphragm arise from these two pairs of arcuate ligaments on either side (Fig. 8-12). However, dissections
of 15 cadavers by Deviri et al.55 showed both arcuate ligaments attached to the transverse process of L-2 in 10 cases and to the transverse process of L3 in 5 cases.

Central Tendon
All the musculature described to this point inserts on the fibrous central tendon of the diaphragm. The thickened portion anterior to the esophageal hiatus
and to the left of the caval aperture is sometimes called the cruciform (transverse) ligament. Fibers on the superior surface of the central tendon blend
with those of the fibrous pericardium. Patches of muscle are often present among the fibers of the central tendon.

Openings of the Diaphragm


HIATUS OF THE INFERIOR VENA CAVA
The hiatus of the inferior vena cava lies in the right dome of the central tendon about one inch (2.5 cm) to the right of the midline and at the level of the
eighth thoracic vertebra. The margins of the hiatus are fixed to the vena cava, which is accompanied by branches of the right phrenic nerve (see Fig. 8-6).
The collagen fiber bundles forming the right margin of the caval hiatus cross inferiorly to the bundles forming the medial and posterior margins. Together,
they form a fibrous limb that can be traced to the edge of the central tendon.

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they form a fibrous limb that can be traced to the edge of the central tendon.
The tendinous fibers forming the medial margin of the hiatus are attached to the muscle fibers of the right crus. This arrangement is often omitted in
textbook illustrations of the caval hiatus. Whether this arrangement of fibers constricts or enlarges the caval hiatus during inspiration has been a source of
controversy for many years. Although no anatomic parallel can be drawn between other species and human beings, constriction of the vena cava during
inspiration is known to occur in diving mammals such as the seal. In these animals, a muscular sphincter takes the place of the fibrous bundles found in the
human diaphragm.
ESOPHAGEAL HIATUS
The elliptical esophageal hiatus is in the muscular portion of the diaphragm an inch or less (2.0-2.5 cm) to the left of the midline at the level of the tenth
thoracic vertebra (Figs. 8-15 and 8-16). The anterior and lateral margins of the hiatus are formed by the muscular arms of the diaphragmatic crura. The
posterior margin is formed by the median arcuate ligament (see Fig. 8-12).
Fig. 8-15.

Apertures of diaphragm seen from below with traversing structures. E, Esophagus; IVC, Inferior vena cava; A, Aorta. (Modified from Skandalakis LJ, Colborn GL,
Skandalakis JE. Surgical anatomy of the diaphragm. In: Nyhus LM, Baker RJ, Fischer JE. Mastery of Surgery, 3rd Ed. Boston: Little, Brown, 1997; with permission.)

Fig. 8-16.

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Diaphragmatic openings for inferior vena cava (IVC), esophagus, and aorta seen from left. (Modified from Skandalakis LJ, Colborn GL, Skandalakis JE. Surgical
anatomy of the diaphragm. In: Nyhus LM, Baker RJ, Fischer JE. Mastery of Surgery, 3rd Ed. Boston: Little, Brown, 1997; with permission.)

The anterior and posterior vagal trunks and the esophageal arteries and veins from the left gastric vessels pass through the hiatus with the esophagus.
This is a region in which the portal circulation (left gastric vein) communicates with the systemic circulation (esophageal branches of the azygos veins).
After studying 50 human diaphragms, Botros et al.56 reported these five variations in the formation of the esophageal hiatus.
In 62%, the hiatus was formed by both crura. The right crus constituted most of the border. The left crus shared only in the formation of the posterior border.
In 10%, the hiatus was formed equally by the medial parts of both crura.
In 10%, the hiatus was formed by the right crus only.
In 2%, the left crus exclusively formed the hiatus.
In 16%, both crura were located posteriorly. The hiatus was separated from the median arcuate ligament by a V-shaped band.
NOTE: The esophageal hiatus is of great surgical importance and is considered in more detail later in this chapter.

Hiatal Hernia
Hiatal hernia can be defined as the protrusion of a portion of the stomach or other organ into the thoracic mediastinum through the esophageal hiatus of
the diaphragm. A hernial sac is present.
kerlund57 was one of the first to classify hernias in this area. He may have been the first to use the term "hiatus hernia." [We are using the term "hiatal
hernia."] He recognized three types of hiatal hernias: sliding, paraesophageal, and congenital short esophagus. Today, we recognize two additional types:
combined sliding and paraesophageal, and fixed. Following is a description of each type of hiatal hernia.
The anatomy of the normal esophageal hiatus is shown in Fig. 8-17A.
Fig. 8-17.

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Esophageal hiatus (sagittal section). A. Normal anatomy. B. Sliding hiatal hernia, C. Paraesophageal hiatal hernia. D. Combined sliding and paraesophageal hernia.
E. Congenital short esophagus. (Modified from Gray SW, Skandalakis LJ, Skandalakis JE. Classification of hernias through the esophageal hiatus. In: Jamieson GG,
ed. Surgery of the Oesophagus. Edinburgh: Churchill Livingstone, 1988; with permission.)

Sliding Hiatal Hernia (Fig. 8-17B). In sliding hiatal hernia, the esophagus moves freely through the hiatus. At different times, the gastroesophageal junction
may be in the thorax or in the normal position. It is usually found in the normal position at autopsy. Sliding hernias make up 90% of all hiatal hernias. Even
though these hernias do slide back and forth through the hiatus, they are called sliding hernias principally because the stomach makes up part of the wall of
the hernia sac. Thus, they are analogous to sliding inguinal hernias, which typically involve partially retroperitoneal structures.
A sliding hiatal hernia can become secondarily fixed in the thorax by adhesion. In such cases, the esophagus appears to be too short to reach the
diaphragm because of contraction of the longitudinal muscle coat. This type is uncommon.
Bozzuto58 reported a sliding incarcerated hiatal hernia with the whole stomach in the thorax. The patient exhibited symptoms of intermittent obstruction
when the stomach was above the diaphragm.
Paraesophageal Hiatal Hernia (Fig. 8-17C). In paraesophageal hiatal hernia, the gastroesophageal junction remains in its normal location. The gastric fundus
and greater curvature bulge through the hiatus anterior to the esophagus. Volvulus of the herniated stomach is a major complication.
Combined Sliding and Paraesophageal Hernia (Fig. 8-17D). Combined sliding and paraesophageal hernias have been described by Peters and DeMeester59
and several other surgeons. The gastroesophageal junction is displaced upward as in a sliding hernia. The fundus and greater curvature are herniated as in
a paraesophageal hernia.
Peters and DeMeester59 believe most paraesophageal hernias are of the combined type. Further evidence for this view has been provided by Walther et
al.,60 who found that more than half of their patients with paraesophageal hernias had abnormal gastroesophageal reflux.
Rahr et al.61 reported a case of intrathoracic perforation of gastric ulcer in a massive hiatal hernia.

Congenital Short Esophagus


(Fig. 8-17E). Congenital short esophagus has been discussed previously in this chapter in the section "Embryogenesis (Congenital Anomalies)."
AORTIC OPENING AND MEDIAN ARCUATE LIGAMENT

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The oblique course of the aorta takes it behind the diaphragm rather than through it (Fig. 8-16). The thoracic duct and (usually) the azygos vein
accompany the aorta through the "opening." At the level of the twelfth thoracic vertebra, the anterior border of the opening is bridged by the median
arcuate ligament. Laterally, the diaphragmatic crura form the margins of the opening. The median arcuate ligament can appear entirely muscular or as a
tendinous band of variable thickness.
The esophageal hiatus is separated from the aortic hiatus by fusion of the arms of the left and right crura. If the tendinous portions of the crura are fused,
the median arcuate ligament is present as a fibrous arch passing over the aorta, connecting the right and left crura. If the fusion is muscular only, the
ligament is ill-defined or absent.
The median arcuate ligament passes in front of the aorta at the level of the first lumbar vertebra, just above the origin of the celiac trunk (Fig. 8-12). The
celiac ganglia lie just below and lateral to the celiac trunk. The ligament and the origin of the celiac artery become slightly lower with increasing age.
In 16% of patients, a low median arcuate ligament covers the celiac artery and may compress it. At angiography, such compression may simulate
atherosclerotic plaques. Adequate collateral circulation exists, since such patients usually do not have symptoms.
The median arcuate ligament has been implicated in abdominal angina in cases wherein substantial, tense, fibromuscular tissue at the hiatus exerted a
constrictive effect upon the celiac trunk or the aorta.62
If there is no true ligament, and the muscular arms of the crura are thinned by posterior extension of the esophageal hiatus, the aortic and esophageal
openings may become practically confluent, although there is always some connective tissue between them.
In about half of the cadavers with hiatal hernia examined by Gray et al.,44 the ligament was sufficiently well-developed to use in surgical repair of the
esophageal hiatus. In the remainder, there was enough preaortic fascia lateral to the celiac trunk to perform a posterior fixation of the gastroesophageal
junction. The celiac ganglion, just below the arcuate ligament, must be avoided.
Wagner et al.63 presented a rare case of a patient with herniation of the transverse colon through the aortic hiatus. This patient had previously had a
laparoscopic Nissen procedure.
OTHER OPENINGS IN THE DIAPHRAGM
Anteriorly, the superior epigastric vessels pass through the parasternal spaces (foramina of Morgagni). In the dome of the diaphragm, the phrenic nerves
pierce the upper surface to become distributed over the lower surface between the muscle and the peritoneum.
The azygos vein may pass behind the diaphragm with the aorta (to the right of the right crus), or it may pierce the right crus. Also passing through the
crura are the greater, lesser, and least thoracic splanchnic nerves (see Fig. 8-15).

Esophageal Hiatus and Abdominal Esophagus


Anatomically, the last 0.5-4.0 cm of the esophagus lies below the diaphragm, forming the abdominal esophagus.
DeMeester and colleagues64 reported that with decrease in the length of the abdominal esophagus, the pressure necessary for competence of the
sphincter rises exponentially. According to Winans,65 normal lower esophageal sphincter pressure values vary from 14.5 to 34 mm Hg.
Kraemer et al.,66 discussing the Hill procedure for gastroesophageal reflux, stated that suture tension should be adjusted to provide an intraluminal pressure
of 35 to 45 mm Hg. They indicated that pressure exceeding 50 mm Hg causes dysphagia, while pressure less than 25 mm Hg may allow reflux.
If the lower esophageal sphincter pressure falls below 5 mm Hg, reflux will be present in 90% of patients, regardless of the length of the abdominal
esophagus. Similarly, reflux occurs in 90% of patients if the length of the abdominal esophagus is less than 1 cm.67 Thus, sphincteric incompetence is the
result of a low sphincter pressure, a short abdominal esophagus, or both.
Maher and Rogers68 observed that if the abdominal esophagus were the only factor governing reflux, all patients with hiatal hernia would have esophagitis.
This is not the case. They stated that the hernial sac, carried up into the mediastinum, can transmit intraabdominal pressure to the distal esophagus, and
thus support the sphincter. That the abdominal esophagus plays a role in the prevention of reflux seems clear. Precisely what that role is remains to be
determined.
For further information on the esophagus and points of clinical and surgical relevance, please consult the chapter on the esophagus.

Phrenoesophageal Ligament (Membrane)


A strong, flexible, airtight seal is necessary at the esophageal hiatus of the diaphragm. The seal is provided by the pleura above and the peritoneum below.
Strength and flexibility are provided by the phrenoesophageal ligament.
The major components of the phrenoesophageal ligament are collagenous and elastic fibers which arise as a continuation of the endoabdominal
(transversalis) fascia beneath the diaphragm. One leaf of this fascia passes upward through the hiatus forming a truncated cone. This inserts into the
adventitia and intermuscular connective tissue of the esophagus 1 or 2 cm above the diaphragm. A second leaf of the fascia turns downward and inserts
into the adventitia of the abdominal esophagus and the stomach. A weaker and less constant component (found in approximately 25% of cases, according
to Bombeck et al.69) may arise from the endothoracic fascia, passing upward to join the fibers of the endoabdominal fascia. The relations of these
components of the phrenoesophageal ligament are shown in Fig. 8-18.
Fig. 8-18.

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Structures at gastroesophageal junction and diaphragmatic hiatus. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General
Surgery. New York: Mc Graw-Hill, 1983; with permission.)

The upper leaf of the phrenoesophageal ligament inserts into the esophagus an average of 3.35 cm above the squamocolumnar epithelial junction. In 227
patients with esophagitis, the insertion was only about 0.5 cm above the epithelial junction.69
The development of the phrenoesophageal membrane has been studied by Botros et al.70 They agreed with Carey and Hollinshead71 that loose connective
tissue with collagenous and elastic fibers arises from both surfaces of the diaphragm, and attaches to the esophagus. A layer of striated crural muscle is
found between these fascial components in the 10-week-old fetus. With age, the muscle fibers undergo gradual regression and replacement with collagen
fibers. Muscle fibers in the adult phrenoesophageal membrane should be considered vestigial.
Botros and colleagues70 found that the superior component of the membrane, from the superior diaphragmatic fascia, appears first. It forms about twothirds of the total thickness at 16 weeks of embryonic age. By 20 weeks, the superior and inferior diaphragmatic fasciae contribute equally to the
membrane. The first result in postnatal life is the fusion of the inner, compact layers from the upper and lower surfaces of the diaphragmatic fascia. When
they reach the esophagus, they fan out to end in the esophageal adventitia. We agree with the conclusion of Botros and associates that further
development of the membrane occurs after birth.

Descriptions of the phrenoesophageal ligament vary because the tissue changes with age. In the fetus, the esophagus and diaphragm are tightly joined at
the hiatus by connective tissue. With the onset of respiratory movements and swallowing in postnatal life, the two structures become less firmly attached,
and the space between them fills with loose connective tissue and fat.
The development of the phrenoesophageal ligament can be summarized as follows, as investigated by Androulakis et al:72
In newborn infants, the phrenoesophageal ligament is present.
In adults, the ligament is attenuated, and subperitoneal fat accumulates at the hiatus.

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For all practical purposes, the ligament does not exist in adults with hiatal hernias.

Gastroesophageal Junction
Shackelford73 observed that the gastroesophageal junction (Fig. 8-19) is a complex of structures which may be defined differently by the anatomist, the
surgeon, the radiologist, and the endoscopist. Figure 8-20 shows the gastroesophageal junction from several points of view:
Gross Anatomist: "the termination of the tube (the esophagus), and the beginning of a pouch (the stomach)" 74
Microscopic Anatomist: the squamocolumnar junction
Surgeon: just below the diaphragm at the upper border of the reflection of the peritoneum from the stomach on to the distal esophagus
Radiologist: an imaginary line from the angle of His to the middle of the junctional mucosa at the lesser curvature. Longitudinal mucosal folds of esophagus change
to transverse folds of stomach.
Endoscopist: the junction of the pale pink esophageal mucosa with the bright red gastric mucosa (Z line)

Fig. 8-19.

The gastroesophageal junction. E, Endoscopic gastroesophageal junction; R, Anatomic gastroesophageal junction. (Modified from Gray SW, Skandalakis LJ,
Skandalakis JE. Classification of hernias through the esophageal hiatus. In: Jamieson GG, ed. Surgery of the Oesophagus. Edinburgh: Churchill Livingstone, 1988;
with permission.)

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Fig. 8-20.

Gastroesophageal junction. Point of view of: 1) Anatomist, 2) Surgeon, 3) Radiologist, and 4) Endoscopist. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr.
Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)

The external gastroesophageal junction can be described as the point at which the esophageal tube becomes the gastric pouch. A portion of the tube
ranging from 0.5 to 4.0 cm lies in the abdomen. The external junction lies at the level of the eleventh or twelfth thoracic vertebra.
Internally, the junction is marked by an irregular boundary between stratified squamous esophageal epithelium and columnar gastric epithelium. This
boundary may lie as far as 1 cm above the external junction. A biopsy specimen of esophageal mucosa should be taken at least 2 cm above the external
junction.
The columnar epithelium below the internal junction contains mucus-secreting glands (the cardiac glands of the histologists). These lack the chief and
parietal cells that characterize the true gastric glands of the body of the stomach. The term junctional epithelium was proposed by Hayward for this
area.75
The external and internal gastroesophageal junctions do not coincide. In addition, the loose submucosal connective tissue permits considerable movement
between the mucosa and the muscularis externa, changing the relation between them as the stomach fills with food.
For additional details about the gastroesophageal junction, see the chapter on the esophagus.

Lower Esophageal Sphincter


For more information about the lower esophageal sphincter, see the chapter on the esophagus.

Diagnosis of Hiatal Hernia


Since precise definition of the gastroesophageal junction is practically impossible in living patients whether or not they have sliding hiatal hernia, it is
difficult to relate specific symptoms to specific anatomic structures and their functions. Only the squamocolumnar Z line can be located precisely by direct
vision.76 Even this line is highly mobile with respect to the other tissues.

Radiology
Anatomic entities not always demonstrated radiographically are the:
Squamocolumnar epithelial junction (Z line)
Lower esophageal sphincter (LES)
Gastric sling (rare exceptions)

Anatomic entities usually demonstrable by radiography are the:

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Angle of His
Phrenic ampulla, that part of the distal esophagus that balloons slightly at the intrathoracic portion. It is probably the part of the esophagus encompassed by the
phrenoesophageal ligament. Peristaltic waves cease at the proximal ampullary region.
"Submerged segment," the abdominal esophagus
Cardia, showing flaccidity or nonconcentric contractions due to the oblique gastric sling

Concentric contractions, which are observed in the ampulla and submerged segment of the distal esophagus under fluoroscopy, are usually demonstrable by
radiography.
As mentioned previously, the gastroesophageal junction of the radiologist is the imaginary line of the gastric sling from the angle of His to the lesser
curvature. If the physician can identify a supradiaphragmatic gastric pouch, contracting nonconcentrically, the diagnosis is hiatal hernia.
Paraesophageal hernias are readily recognized on plain X-ray by observing the relative position of the diaphragm. The stomach is partly above the level of
the diaphragm and the gastroesophageal junction is at or below the diaphragm.

Endoscopy
The normal cardiac opening appears as a contracted rosette of pale esophageal mucosa, descending during inspiration and ascending during expiration. In
hiatal hernia, the cardiac opening does not descend during inspiration. Instead, it opens widely, displaying pink gastric mucosa in longitudinal folds (Fig. 821A,B).
Fig. 8-21.

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Endoscopy. A, Normal. H-shaped appearance of collapsed distal esophagus. B, Normal. Squamocolumnar junction (Z line). C, Sliding hiatal hernia. Relation of Z line
to diaphragm. (Modified from Gray SW, Skandalakis LJ, Skandalakis JE. Classification of hernias through the esophageal hiatus. In: Jamieson GG, ed. Surgery of the
Oesophagus. Edinburgh: Churchill Livingstone, 1988; with permission.)

Normally, with the epithelial junction (Z line) under direct vision, when the patient is asked to sniff two or three times, the esophageal orifice contracts or is
obliterated, probably by contraction of the diaphragm. If there is a hiatal hernia, endoscopy will reveal the Z line above the level of luminal obliteration when
the patient sniffs (Fig. 8-21C). The endoscopist can quantify the hiatal hernia by measuring the distance between the Z line and the area of contracted
lumen during the sniff.
The epithelial junction (Z line) can be readily visualized endoscopically, and is thus the most precisely defined of the elements of the gastroesophageal
junction. These observations apply to sliding hiatal hernias. Endoscopy in patients with paraesophageal hiatal hernias is usually not informative.

Diaphragmatic-Pleural-Mediastinal Relations
The fibrous tissue of the central tendon is continuous with the fibrous pericardium over much of the anterosuperior surface of the diaphragm (see Fig. 8-6).
The right mediastinum (Fig. 8-22) contains the:
Pericardium
Inferior vena cava
Right phrenic nerve and pericardiophrenic vessels
Right pulmonary ligament
Esophagus with the right vagal trunk
Thoracic duct
Azygos vein, azygos arch
Vertebral bodies
Greater and lesser right thoracic splanchnic nerves
Right sympathetic trunk
Right posterior intercostal arteries

Fig. 8-22.

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Structures of inferior portion of right mediastinum. (Modified from Skandalakis LJ, Colborn GL, Skandalakis JE. Surgical anatomy of the diaphragm. In: Nyhus LM,
Baker RJ, Fischer JE. Mastery of Surgery, 3rd Ed. Boston: Little, Brown, 1997; with permission.)

The left mediastinum (Fig. 8-23) contains the:


Pericardium
Left phrenic nerve and pericardiophrenic vessels
Esophagus
Left vagal trunk
Descending aorta
Vertebral bodies
Hemiazygos vein, accessory hemiazygos vein, highest intercostal vein
Greater and lesser left thoracic splanchnic nerves
Left sympathetic trunk

Fig. 8-23.

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Structures of inferior portion of left mediastinum. (Modified from Skandalakis LJ, Colborn GL, Skandalakis JE. Surgical anatomy of the diaphragm. In: Nyhus LM,
Baker RJ, Fischer JE. Mastery of Surgery, 3rd Ed. Boston: Little, Brown, 1997; with permission.)

The triangle (of Truesdale) formed by the pericardium, aorta, and diaphragm contains the left pulmonary ligament and the distal esophagus. In sliding hiatal
hernia, the stomach is in this triangle.
The remainder of the superior surface of the diaphragm is covered with parietal pleura. The approximation of the right and left pleurae between the
esophagus and the aorta forms the so-called mesoesophagus.
The right pleura is in contact with the lower third of the esophagus almost as far down as the esophageal hiatus (Fig. 8-24). This proximity creates the risk
of accidental entrance into the pleural cavity during abdominal operations on the esophageal hiatus. Even so, because surgeons work on the right side of
the operating table, they are more likely to produce a pneumothorax or hemopneumothorax on the left.
Fig. 8-24.

Cross section through the thorax at the level of T10. Relation of pleura to distal esophagus. IVC, Inferior vena cava. (Modified from Gray SW, Rowe JS Jr,
Skandalakis JE. Surgical anatomy of the gastroesophageal junction. Am Surg 45(9):575-587, 1979; with permission.)

The diaphragmatic pleura is part of the parietal pleura and covers all parts of the diaphragm except that part of the central tendon that is in contact with
the pericardium. It is heavily fixed to the diaphragm through the phrenopleural fascia of the endothoracic fascia in such a way that separation from the
diaphragm is practically impossible. This is in contrast with the costal pleura, which can be stripped away along with the endothoracic fascia.
The costodiaphragmatic recess is located at the reflection of the parietal pleura from the ribs to the diaphragm. The phrenomediastinal recess is between
the mediastinum and the diaphragm.
The blood supply of the diaphragmatic pleura springs from the internal thoracic artery, thoracic aorta, and abdominal aorta or celiac artery. At the inferior
surface of the diaphragm, these arteries form internal and external branches, which anastomose with the vascular plexus of the costal pleura.
According to Testut and Jacob77 and Testut 78 (as reported by Bernaudin and Fleury79), the inferior phrenic veins drain into the inferior vena cava and into
the superior phrenic (pericardiophrenic) veins. However, different collateral circulation exists. The right inferior phrenic vein drains to the IVC. The left
inferior phrenic vein drains to the IVC and to the left suprarenal vein. The veins run parallel with the phrenic nerves and terminate in the right and left
internal thoracic veins.

Peritoneal Reflections of the Inferior Surface of the Diaphragm and


Gastroesophageal Junction
The primitive dorsal and ventral mesenteries of the abdomen form several ligaments related to the diaphragm and the gastroesophageal junction (Fig. 8-25).
These ligaments are the:
Falciform, coronary, and triangular
Hepatogastric (gastrohepatic)
Gastrosplenic (gastrolienal)

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Gastrophrenic

Fig. 8-25.

Peritoneal reflections of stomach, gastroesophageal junction, and bare area of diaphragm. IVC, Inferior vena cava. (Modified from Skandalakis JE, Gray SW, Rowe
JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)

Falciform, Coronary, and Triangular Ligaments


The falciform ligament (a remnant of the primitive ventral mesentery) (Fig. 8-25) arises from the anterior abdominal wall and extends to the anterior
surfaces of the liver and the diaphragm. Its free edge encircles the round ligament of the liver, the obliterated left umbilical vein.
The leaves of the falciform ligament separate over the liver to form the anterior and posterior layers of the coronary ligament. Enclosing the bare area on
the right, these leaves unite laterally to form the right triangular ligament. On the left, the leaves are in apposition to each other, forming the left triangular
ligament.
One approach to the gastroesophageal junction is to section the left triangular ligament and left portion of the posterior layer of the coronary ligament. In
operating, one must be careful when mobilizing the liver, especially the left lobe, not to injure the left hepatic vein or the inferior vena cava.

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operating, one must be careful when mobilizing the liver, especially the left lobe, not to injure the left hepatic vein or the inferior vena cava.

Hepatogastric (Gastrohepatic) Ligament


The abdominal esophagus lies between the two layers of the hepatogastric ligament (Fig. 8-26), which is the superior part of the lesser omentum, deriving
from the primitive ventral mesentery. The inferior portion is the hepatoduodenal ligament (Fig. 8-26). The hepatogastric ligament extends from the porta
hepatis to the lesser curvature of the stomach and the abdominal esophagus. The ligament contains the left gastric artery and vein, hepatic division of the
left vagus nerve, and lymph nodes. It may also contain both vagal trunks, branches of the right gastric artery and vein, and left hepatic artery if it arises
from the left gastric artery (26% of individuals).
Fig. 8-26.

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Hepatogastric, hepatoduodenal, gastrosplenic, and gastrophrenic ligaments. (From Ferner H, ed. Pernkopf Atlas of Topographical and Applied Human Anatomy.
Baltimore: Urban & Schwarzenberg, 1980; with permission.)

Gastrosplenic (Gastrolienal) Ligament


On the right, the hepatogastric ligament divides to enclose the stomach. The leaves of peritoneum rejoin on the left to form the gastrosplenic ligament (Fig.
8-26), which is part of the primitive dorsal mesentery. The hepatogastric ligament separates the lesser sac from the rest of the peritoneal cavity. At the
level of the abdominal esophagus, the hepatogastric ligament is formed by the anterior leaf. The posterior leaf does not reach the gastroesophageal
junction. Thus, a small bare area is left on the posterior wall of the stomach that lies over the left crus of the diaphragm and is easily separated from it by
the surgeon's finger.
The upper portion of the gastrosplenic ligament contains the short gastric vessels and the pancreaticosplenic lymph nodes. The lower portion contains the
left gastroepiploic vessels, lymph nodes, and the terminal branches of the splenic artery.

Gastrophrenic Ligament
The gastrophrenic ligament (the superior portion of the dorsal mesentery) (Fig. 8-26) arises from the greater curvature of the fundus and extends upward
to the diaphragm. The upper part is transparent, avascular, and continuous with the posterior layer of the coronary ligament on the left. The lower part is
continuous with the gastrosplenic ligament, and contains some short gastric vessels and lymph nodes.
The upper avascular area can be perforated by the surgeon's finger in order to insert a Penrose drain around the cardia. The surgeon can thus apply gentle
traction on the esophagus, a useful maneuver in vagotomy.

Vascular Supply
Arteries
The arterial supply to the superior surface of the diaphragm consists of two branches from the internal thoracic arteries (pericardiophrenic and
musculophrenic) and two branches from the thoracic aorta (superior phrenic). All these branches are small.
The major blood supply to the diaphragm is to the inferior surface. It comes from the inferior phrenic arteries (Fig. 8-27), which arise from the aorta or the
celiac axis just below the median arcuate ligament of the diaphragm. In a small percentage of individuals, the right inferior phrenic artery arises from the
right renal artery. The inferior phrenic arteries also supply branches to the suprarenal glands.
Fig. 8-27.

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Arterial supply of diaphragm from below. Inferior phrenic arteries can arise from celiac trunk or directly from aorta. E, Esophagus; IVC, Inferior vena cava. (Modified
from Skandalakis LJ, Colborn GL, Skandalakis JE. Surgical anatomy of the diaphragm. In: Nyhus LM, Baker RJ, Fischer JE. Mastery of Surgery, 3rd Ed. Boston: Little,
Brown, 1997; with permission.)

Comtois et al.80 studied the diaphragmatic circulation in 48 mongrel dogs, and reported the following:
Anastomoses between the phrenic arteries and internal thoracic arteries form an arterial circle around the medial leaflet of the tendinous diaphragm.
From the arterial circle described above, vascular branches travel toward the periphery of the diaphragm. These branches anastomose with branches of the
intercostal arteries, forming costophrenic arcades along the costal diaphragm.
Anastomoses of the intercostal arteries with one another within the muscular diaphragm form another arterial ring at the area of origin of the diaphragm from the
ribs.

LEFT INFERIOR PHRENIC ARTERY AND LEFT GASTRIC ARTERY


The abdominal esophagus and the proximal stomach are supplied by esophageal branches of the left gastric artery. These branches usually, but not always,
anastomose above the diaphragm with esophageal arteries from the aorta (Fig. 8-28A). In some persons, the lower esophagus also receives twigs from the
left inferior phrenic artery (Fig. 8-28B). In still others, branches of the inferior phrenic artery supply the lower esophagus with branches of the left gastric
artery confined to the cardia and fundus of the stomach (Fig. 8-28C). The margin of the hiatus is always supplied by a branch of the left inferior phrenic
artery.
Fig. 8-28.

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Variations in blood supply to distal esophagus and esophageal hiatus. A, Inferior phrenic artery supplies margin of hiatus. Esophageal branch of left gastric artery
supplies esophagus and anastomoses with thoracic esophageal arteries. This pattern is the most frequent one. B, Esophagus supplied by esophageal branches of
left gastric and inferior phrenic arteries without cranial anastomoses. C, Esophagus supplied entirely by a branch of the inferior phrenic artery, which anastomoses
with thoracic esophageal arteries. This pattern is rare. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New York:
McGraw-Hill, 1983; with permission.)

ABERRANT LEFT HEPATIC ARTERY


An aberrant left hepatic artery arising from the left gastric artery lies in the hepatogastric ligament in about 26% of persons. One must consider the
possibility of such an artery before dividing the ligament to reach the gastroesophageal junction.

Veins
On the superior surface of the diaphragm, small tributaries form the pericardiophrenic and musculophrenic veins. These veins run with the corresponding
arteries and empty into the internal thoracic veins. Posteriorly, there is some local drainage into the azygos and hemiazygos veins.
The studies of Comtois and colleagues80 found that the distribution of the veins in dogs is similar to that of the arteries and that the valves in the veins
may have a role in directing blood flow.
On the inferior surface, the right inferior phrenic vein runs with the artery, and empties into the inferior vena cava. The left inferior phrenic vein may enter
the inferior vena cava, but it usually has a posterior branch that descends posteriorly to enter the left suprarenal vein (Fig. 8-29).
Fig. 8-29.

Venous drainage of diaphragm from below. Left inferior phrenic vein may enter (A), the inferior vena cava; (B), the left suprarenal vein, or both. IVC, Inferior vena
cava. (Modified from Skandalakis LJ, Colborn GL, Skandalakis JE. Surgical anatomy of the diaphragm. In: Nyhus LM, Baker RJ, Fischer JE. Mastery of Surgery, 3rd Ed.
Boston: Little, Brown, 1997; with permission.)

LEFT INFERIOR PHRENIC VEIN


The left inferior phrenic vein may drain into the left suprarenal vein, the inferior vena cava, or both. The branch draining into the vena cava passes in front
of the esophagus closely enough to be injured.
LEFT GASTRIC (CORONARY) VEIN
The left gastric vein passes upward along the lesser curvature to a point 2 to 3 cm from the esophageal hiatus, where it receives one to three esophageal
tributaries. From this point, it turns downward and obliquely to the right to join the portal vein, or backward to enter the splenic vein.
In dissections of 22 cadavers, Skandalakis et al.81 found the left gastric vein entering the portal vein in 16 and entering the splenic vein in the remaining
six. It is important to remember that the severed distal tributaries of the left gastric vein bleed from anastomoses with esophageal and hemiazygos veins in
the thorax.

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the thorax.
OTHER VESSELS

The celiac trunk, the aorta, and the inferior vena cava are all close enough to the esophageal hiatus to be at risk during operations on the hiatus.

Lymphatics
All the diaphragmatic lymph nodes lie on the superior surface of the diaphragm. These nodes can be divided into anterior, middle, and posterior groups (Fig.
8-30). They receive drainage from the upper surface of the liver, the gastroesophageal junction, and the abdominal surface of the diaphragm.
Fig. 8-30.

Lymphatic drainage of diaphragm seen from above. Diaphragm receives lymph from liver below and sends it to ascending sternal, anterior, and posterior
mediastinal nodes. E, Esophagus; IVC, Inferior vena cava; A, Aorta. (Modified from Skandalakis LJ, Colborn GL, Skandalakis JE. Surgical anatomy of the diaphragm.
In: Nyhus LM, Baker RJ, Fischer JE. Mastery of Surgery, 3rd Ed. Boston: Little, Brown, 1997; with permission.)

Efferent lymph vessels from these nodes drain upward to parasternal and mediastinal nodes anteriorly and to posterior mediastinal and brachiocephalic
nodes posteriorly.
Both thoracic and abdominal serosal surfaces of the diaphragm are active in the removal of fluid and cells from the pleural and peritoneal cavities. Pores
between mesothelial cells from 4 to 12 mm in diameter open directly into the lymphatic vessels of the diaphragm. First seen in 1863 by von
Recklinghausen,82 their existence has been confirmed by electron microscopy.
In a computed tomographic study by Kullnig et al.83 of 132 patients with malignant lymphoma, 11.3% revealed involvement of lymph nodes of the
diaphragm.
Using CT in 125 patients, Libshitz and Holbert 84 observed diseased and healthy anterior diaphragmatic lymph nodes (ADLNs). In enlarged ADLNs,
malignancies were found in the following percentages:
Lymphoma

41%

Breast cancer

12%

Colon cancer

10%

Lung cancer

6%

Other malignancies 30%

They reported that right-sided lymph nodes were more common than left-sided lymph nodes. They concluded that good anatomic knowledge of both the
right and left cardiophrenic nodes will help the radiotherapist plan treatment for Hodgkin's disease and other malignancies.
The right and left triangular ligaments and the falciform ligament of the liver transmit superficial lymphatic vessels from the liver. The vessels enter the
precardiac, superior phrenic, and juxtaesophageal lymph nodes or pass to the celiac nodes.85
Table 8-3 lists the lymph nodes that are responsible for the drainage of pleural structures in human beings.
Table 8-3. Lymph Nodes Draining Pleural Structures in the Human
Groups of Lymph Nodes

Pleural Structures Drained

Sternal

Parietal pleura: anterior thoracic wall


Diaphragmatic pleura: anterior portion

Intercostal

Parietal pleura

Middle mediastinal

Diaphragmatic pleura: middle portion


Visceral pleura

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Anterior mediastinal

Visceral pleura

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Diaphragmatic pleura: anterior portion


Mediastinal pleura

Posterior mediastinal

Diaphragmatic pleura: posterior portion


Visceral pleura: lower lobes

Source: From JF Bernaudin, J Fleury. Anatomy of the blood and lymphatic circulation of the pleural serosa. In J Chretien, J Bignon, A Hirsch (eds.), The Pleura in Health
and Disease. New York: Marcel Dekker, 1985. Reproduced with permission.

THORACIC DUCT
The cisterna chyli (when present) lies on the bodies of the first and second lumbar vertebrae between the right crus of the diaphragm and the aorta.
Division of the thoracic duct or other large lymph vessels in this area can result in chylous ascites. Ligation of the thoracic duct produces no ill effects.

Innervation
The right phrenic nerve enters the diaphragm through the central tendon just lateral to the opening for the inferior vena cava. Occasionally, it passes
through that opening with the vena cava. The left phrenic nerve pierces the superior surface of the muscular portion of the diaphragm just lateral to the
left border of the heart.
Both nerves divide or trifurcate at or just above the diaphragm. These branches travel together into the musculature. Small sensory branches are given off
to the pleura and pericardium, and to the peritoneum over the central part of the diaphragm. The larger motor branches separate within the diaphragm into
three or four major nerve trunks. The four are as follows: sternal, anterolateral, posterolateral, and crural (Fig. 8-31). The posterolateral and crural nerve
trunks usually have a common trunk. These nerve trunks travel partly within the diaphragmatic musculature and partly on the inferior surface. They are
covered only by the peritoneum. The sternal branches of the two sides may anastomose behind the sternum.
Fig. 8-31.

Major branches of phrenic nerves from below. Each phrenic nerve divides just before entering diaphragm from above. E, Esophagus; IVC, Inferior vena cava; A,
Aorta. (Modified from Skandalakis LJ, Colborn GL, Skandalakis JE. Surgical anatomy of the diaphragm. In: Nyhus LM, Baker RJ, Fischer JE. Mastery of Surgery, 3rd Ed.
Boston: Little, Brown, 1997; with permission.)

The peripheral portions of the pleura and peritoneum have an independent sensory innervation that arises from the seventh to the twelfth intercostal
nerves.
In addition to the phrenic and intercostal nerves, fibers to the inferior surfaces of the right posterior portion of the diaphragm arise from the celiac ganglion,
often forming a phrenic ganglion before their distribution. A connection has been claimed between these fibers and a posterior branch of the right phrenic
nerve. One of the authors [GLC] has dissected this on a number of occasions.

Vagal Trunks
Among 100 cadavers dissected by Skandalakis et al.,86 the anterior and posterior vagal trunks passed through the hiatus with the esophagus in 88
individuals (Fig. 8-32). In three others, the esophageal plexus was present at the hiatus and the trunks lay entirely within the abdomen (Fig. 8-33). In
another nine, the trunks had divided above the hiatus and their major divisions passed through the hiatus.
Fig. 8-32.

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The terminology of vagal structures of the thorax and abdomen. In this example, two vagal trunks pass through the hiatus to the abdomen. 1 = hepatic division; 2
= anterior gastric division; 3 = celiac division; 4 = posterior gastric division. (Modified from Skandalakis JE, Rowe JS Jr, Gray SW, Androulakis JA. Identification of
vagal structures at the esophageal hiatus. Surgery 75:233-237, 1974; with permission.)

Fig. 8-33.

Where four or more vagal structures emerge through the hiatus, they may be: A, divisions that have separated just above the diaphragm; B, divisions and their
branches that arise above the diaphragm; or C, elements of the esophageal plexus that extend below the diaphragm. The vagal trunks are entirely within the
abdomen. 1 = hepatic division; 2 = anterior gastric division; 3 = celiac division; 4 = posterior gastric division. (Modified from Skandalakis JE, Rowe JS Jr, Gray SW,
Androulakis JA. Identification of vagal structures at the esophageal hiatus. Surgery 75:233-237, 1974; with permission.)

For further details on the vagal trunks, see the chapter on the stomach.

Celiac Ganglia
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The celiac ganglia are adherent to the celiac artery at its origin from the aorta, and closely related to the crura of the diaphragm bilaterally. Sutures to
approximate the crura must be placed above the ganglia and behind the celiac division of the posterior vagal trunk.

Subphrenic Spaces
A portion of the inferior surface of the diaphragm is attached directly to the liver without a serosal covering. This is known as the bare area of the
diaphragm (or liver). The margins of the bare area are peritoneal reflections that form the falciform, coronary, and triangular ligaments of the liver (see Fig.
8-25).
Outside the bare area, the serous (peritoneal) surfaces of the diaphragm and the liver are in apposition with a potential space between. This potential
space is divided by the falciform ligament into right and left subphrenic (suprahepatic) compartments (see Fig. 8-25). These spaces may become the sites
of peritoneal fluid collection and subphrenic abscesses.
The right and left compartments are defined as follows:
The right subphrenic space is bounded above by the inferior surface of the right leaf of the diaphragm. It is bounded below by the anterosuperior leaf of the
diaphragm, the anterosuperior surface of the right lobe of the liver, and the medial segment of the left lobe. It is bounded medially by the falciform ligament,
and posteriorly by the right anterior coronary and right triangular ligaments. Anteriorly and inferiorly, the space opens into the greater peritoneal cavity.
The left subphrenic space is bounded above by the inferior surface of the left leaf of the diaphragm. It is bounded below by the superior surface of the
lateral segment of the left lobe of the liver and the fundus of the stomach. Medially it is bounded by the falciform ligament; posteriorly, by the left anterior
coronary and left triangular ligaments. Anteriorly and laterally, the space communicates with the infrahepatic space and the greater peritoneal cavity. On
the left, the anterior and posterior leaves of the coronary ligament are in apposition.
In the absence of disease, there is no distinction between anterior and posterior portions of the right space. However, fluid may collect or an abscess may
form anteriorly between the liver and diaphragm just beneath the sternum (right anterior subphrenic abscess) (Fig. 8-34A), or an abscess may form at the
reflection of the anterior leaf of the coronary ligament between the liver and the diaphragm (right posterior subphrenic abscess) (Fig. 8-34B). Thus, the
single normal space can become compartmentalized by pseudomembranes into the anterior or posterior abscess sites seen by the clinician.
Fig. 8-34.

Right parasagittal sections. A, Fluid accumulation in anterior portion of right subphrenic space. B, Fluid accumulation in posterior portion of right subphrenic space.
Fluid-filled spaces are usually walled off by pseudomembranes. Diaphragm abnormally elevated over region of fluid accumulation. (Modified from Skandalakis JE,
Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)

On the left, the subphrenic space may be similarly compartmentalized by pseudomembranes between the liver and diaphragm or abdominal wall (Fig. 8-35).
If the collection of fluid is large, it can spread from the left subphrenic space into the communicating subhepatic space. There, the stomach and spleen as
well as the liver participate in walling off the infection. The diaphragm is usually elevated over the space occupied by the fluid collection.
Fig. 8-35.

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Left parasagittal sections. A, Fluid accumulation in anterior portion of left subphrenic space. B, Fluid accumulation in posterior portion of left subphrenic space.
Pseudomembranes limit space occupied by fluid accumulations. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery.
New York: McGraw-Hill, 1983; with permission.)

The surgical approach to fluid collections in the subphrenic spaces is chosen after localization and determination of size and degree of extension of the
abscess. Changes in the anatomy caused by the formation of pyogenic membranes and pressure of the abscess must be evaluated. Close cooperation
between the surgeon and radiologist is necessary.
There are typically no anatomic complications using the anterior approach from beneath the costal margin. The posterior approach (Fig. 8-36) requires an
incision at the level of the spinous process of the first lumbar vertebra to avoid entering the pleura. Spain et al.87 advocated twelfth rib resection.
Fig. 8-36.

Potential danger during posterior approach. Pleura can be accidently opened when 12th rib does not project beyond outer border of sacrospinalis.

HISTOLOGY
A histologic summary of the diaphragm is represented by the peritoneum below, diaphragmatic pleurae above, and musculoaponeurotic stroma in between.

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A histologic summary of the diaphragm is represented by the peritoneum below, diaphragmatic pleurae above, and musculoaponeurotic stroma in between.
These entities are discussed in other chapters.

PHYSIOLOGY
It is not within the scope of this chapter to present the physiology of the diaphragm, but the following information is pertinent.
Roentgenographic findings of Reddy et al.88 support the hypothesis that the cardiac mass is responsible for the caudad displacement of the related
hemidiaphragm. The same researchers dispute the classic teaching that it is the liver that lifts the corresponding hemidiaphragm.
The function of the diaphragm, which is composed of skeletal voluntary muscle, is as automatic as the function of the heart. Sharp89 and Macklem90 rightly
stated that the diaphragm is second in importance only to the heart in sustaining life.

We quote from Boczkowski et al.91:


From a general point of view, functional and biochemical characteristics of the diaphragm are similar to those of other skeletal muscles with a similar
fiber type composition. However, the diaphragm presents some specificities allowing a high supply of metabolic substrates. This could serve to
preserve contractile function in different physiological and physiopathological situations. Such specificities concern muscular vascularization, the
microvascular network and the content of mitochondria and myoglobin.

SURGERY OF THE DIAPHRAGM


Surgery of the diaphragm is the surgery of congenital anomalies and acquired problems, such as trauma, etc.
Zierold et al.92 developed a porcine model of penetrating diaphragmatic injury, and reported the following:

Ultrasonography may prove to be an important diagnostic adjunct in evaluating diaphragm injuries with and without herniation. Moreover, since the
"protected" diaphragm injuries in our model healed spontaneously, a role may exist for the nonoperative treatment of diaphragm injuries in clinical
practice.
The central tendon of the diaphragm is partially fused with the pericardium. Therefore, when repairing a peritoneopericardial defect, the hernial ring should be
closed to incorporate both anatomic entities as one.
An elevated paralyzed hemidiaphragm partially compresses the ipsilateral lower pulmonary lobe. Intraperitoneal pressure also is responsible for such lobar
compression.
Bedini et al.93 performed diaphragm reconstruction after extrapleural pneumonectomy with muscle flap instead of prosthetic material. They reported the following:
"The distal latissimus dorsi can be used for total reconstruction of one hemidiaphragm, ensuring a watertight separation between the pleural and peritoneal cavities
and avoiding paradoxical respiratory motion."
Placement of nonabsorbable sutures in the crura (including the attached pleura) is absolutely necessary to narrow the hiatus for repair of hiatal hernia. The
surgeon must be sure that the sutures are in the tendinous portions of the crura and not in the muscular part only. The type of closure, vertical or horizontal, is the
choice of the surgeon and depends on the local anatomic situation.
If the surgeon chooses to close the hiatus anterior to the esophagus, nonabsorbable sutures must partially incorporate the transverse ligament as well as the
right and left arms of the crura.
Remember to observe the topography of the median arcuate ligament in relation to the celiac axis. Remember also that this ligament is present in approximately
50 percent of cases.
The gastroesophageal junction is mobilized by dividing the phrenoesophageal membrane (ligament) when it is present.
In a study of 22 cadavers by Skandalakis et al.77 :
a curved Kocher clamp applied to the lesser curvature at the hepatogastric omentum always included the following:
Left gastric artery
Anterior and posterior nerves of the lesser curvature (nerves of Latarjet)

Hepatic division of the vagus nerve


Left aberrant hepatic artery (present in four cases)
Left gastric vein (present in all cases with portal vein drainage and three cases with splenic vein drainage)
a regular curved or straight Kocher clamp applied to the hepatogastric omentum at a 45 angle in the same cadaver always included the following:
All the structures listed above
Left gastric vein (regardless of its drainage)

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John G. Hunter (personal communication to John E. Skandalakis, February 2000) provided the following information about laparoscopic surgery of diaphragmatic
hernias: Hiatal hernias are perhaps the most common type of abdominal hernia, but are most frequently asymptomatic. When hiatal hernias become symptomatic
they may do so with symptoms of gastroesophageal reflux (such as heartburn) or with symptoms created by the herniated stomach. These include postprandial
chest pain, nausea, vomiting, and frank GI bleeding. Small asymptomatic hernias may be left alone, but large hernias need operative repair. Today the laparoscopic
repair is preferred by most patients.
The laparoscopic technique starts with the placement of five abdominal trocars, and elevation of the left lobe of the liver. This allows access to the hiatal hernia. The
entire stomach and esophagus is reduced into the abdomen and the diaphragmatic crura are circumferentially dissected. If the esophagus has been foreshortened
by a stricture or prolonged gastroesophageal reflux, an esophageal lengthening procedure such as a Collis gastroplasty is usually performed prior to hiatal hernia
repair. The hernia is repaired posterior to the esophagus, with interrupted heavy sutures. The use of prosthetic mesh to cover a hiatal hernia should not be
condoned. The hiatus should be closed to the diameter of the empty esophagus. Usually, it is advantageous to perform a loose floppy fundoplication after hiatal
hernia repair. Not only does the fundoplication prevent postoperative reflux, but it helps anchor the fundoplication within the abdomen.
The recurrence rate of hiatal hernia after a laparoscopic repair should be no more than five percent. The recurrent hernias can be fixed in a similar fashion to the
first operation but more attention should be paid toward the possibility of a shortened esophagus. Complications with the laparoscopic repair are few and are more
related to the size of the hernia and the age of the patient than anything else. Nevertheless, this revolutionary advance in the repair of hiatal hernia has conferred
a much improved quality of life for hundreds of thousands of individuals with symptomatic gastroesophageal reflux and large hiatal hernias.
Krhenbhl et al.94 advised laparoscopic paraesophageal hernia repair including reduction of the stomach, complete excision of the hernial sac, closure of the
hiatal defect, floppy Nissen fundoplication, and anterior gastropexy.
Perdikis et al.95 recommended management of paraesophageal hernia by laparoscopy.
Schauer et al.96 reported that the laparoscopic repair of paraesophageal hernia is the preferred approach.
There is controversy about the surgical approach to giant paraesophageal hernia. Geha et al.97 advise that the defect be repaired soon after recognition, with
evaluation of reflux before surgery. If an antireflux repair is required, fundoplication, reduction, excision of the sac, gastropexy, and crural closure should be
performed. Buenaventura et al.98 reported that laparoscopic repair of giant paraesophageal hernia may be associated with lower morbidity, shorter hospital stay,
faster recovery and excellent clinical results.
We quote from Watson et al.:99

Large hiatal hernias can be treated effectively laparoscopically. Dissecting the sac fully from the mediastinum before dissecting the esophagus helps
to safely mobilize the esophagus.
Swanstrom et al.100 reported that laparoscopic repair of paraesophageal hernia in combination with fundoplication is well tolerated. Horgan et al.101 reported
that laparoscopic repair of paraesophageal hernia, including antireflux procedure, improves symptoms, resolves anemia, and in nearly all patients prevents
incarcerations.
Carlson et al.102 advised the use of mesh prosthesis for the treatment of large hiatus hernia with intrathoracic stomach. In the same issue of the Journal of the
American College of Surgery, DeMeester103 stated that surgeons doing esophageal surgery occasionally will encounter a wide hiatus and that the advice of Carlson
et al. is "pertinent and priceless."
Schneider et al.104 stated that laparoscopic management of acute traumatic diaphragmatic rupture offers a favorable alternative to conventional surgery.
We quote from Cougard et al.105 :

The laparoscopic approach in lateral position provides good visibility of the diaphragmatic lesions, easy reduction of herniated organs, complete
thorax exploration and cleaning, and easy diaphragmatic repair. This technique is only feasible in patients with stable hemodynamic conditions and
does not provide a complete abdominal exploration.

ANATOMIC COMPLICATIONS OF DIAPHRAGMATIC SURGERY


The anatomic complications of surgery of the diaphragm can be divided (in a very unorthodox way) into two groups. The first group consists of
complications arising from the repair of specific congenital diaphragmatic hernias (Bochdalek, Morgagni, eventration, pericardial) (Fig. 8-37). The second
group consists of complications arising from the repair of hiatal and paraesophageal hernias. The complications of the second group are presented in the
chapter on the esophagus.
Fig. 8-37.

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Diaphragmatic hernias. A, Posterolateral hernia through foramen of Bochdalek. B, Anterior hernia through foramen of Morgagni. C, Hernia through esophageal
hiatus. D, Confluence of esophageal and aortic hiatus in absence of arcuate ligament. IVC, Inferior vena cava. (Modified from Skandalakis JE, Gray SW, Akin JT Jr.
Surgical anatomy of hernial rings. Surg Clin North Am 54:1227, 1974; with permission.)

The anatomic complications of the first group are the usual problems arising from abdominal or thoracic incisions used in the repair of defects.

Remember
Most anatomic complications associated with Bochdalek hernia repair occur in the liver and spleen during a second operation to correct recurrence. A transthoracic
approach through the sixth or seventh interspace is recommended by Salzberg and Ducey106 to avoid these complications.
Phrenic nerve injury should be avoided during plication of the diaphragm through the abdomen or the chest (Fig. 8-38).
Additional information pertaining to the diaphragm can be found in the chapters on the esophagus and stomach.

Fig. 8-38.

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Distribution of branches of phrenic nerve (from above). Location of incisions (broken lines) that will not seriously impair diaphragmatic function. A, Diaphragmatic
component of combined abdominothoracic incision extending into esophageal hiatus. B, Circumferential incision. C, D. Incisions extending from lateral (midaxillary)
and posterior costal areas into central tendon (from above). IVC, inferior vena cava. (Modified from Merendino KA. The intradiaphragmatic distribution of the phrenic
nerve. Surg Clin North Am 44:1217, 1964; with permission.)

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