Gynecologic Oncology 107 (2007) S106 S112

www.elsevier.com/locate/ygyno

Do we need a new classification for radical hysterectomy? Insights in

surgical anatomy and local tumor spread from human embryology
Michael Hckel
University of Leipzig, Department of Obstetrics and Gynecology, Philipp-Rosenthal-Str. 55, 04103 Leipzig, Germany
Received 6 July 2007
Available online 28 August 2007

Abstract
Objective. Current surgical treatment of cervical carcinoma is based on the assumption of undirected intra- and transcervical local tumor
propagation and is executed by tailored excision of the paracervical tissues. We have recently demonstrated that cervical carcinoma spreads for
extended phases during its malignant progression within the permissive compartment of the Mllerian morphogenetic unit (Lancet Oncol
2005;6:75156) and proposed Mllerian compartment resection as the new principle for surgical treatment of cervical cancer. Do we need a new
classification of radical hysterectomy?
Methods. The therapeutic index of the surgical treatment of cervical carcinoma FIGO stages IB1IIB by extirpation of the Mllerian compartment
through total mesometrial resection (TMMR) without adjuvant radiation is evaluated by an ongoing controlled prospective trial at the University of
Leipzig.
Results. From 7/1998 to 12/2006, 163 patients with cervical carcinoma, FIGO stages IB1 (n = 94), IB2 (n = 21), IIA (n = 14) and IIB (n = 34) have
been treated with TMMR and nerve-sparing therapeutic lymph node dissection. Twenty-five patients received (neo)adjuvant chemotherapy. No
patient underwent adjuvant radiotherapy although 95 patients (58%) would have needed this additional modality in case of conventional radical
hysterectomy because of their high-risk histopathological tumor features. At a median follow-up time of 45 months (3104 months), recurrence-free
and disease-specific overall survival is 93% and 96%. Maximum treatment-related morbidity according to the Franco-Italian score has been grade 2 in
12 patients (8%).
Conclusions. The developmental view of local tumor spread and surgical anatomy holds a great promise for improving the therapeutic index of
surgical cervical cancer therapy and challenges both the classification of radical hysterectomy based on tailored paracervical resection and the
indication for adjuvant radiation.
2007 Elsevier Inc. All rights reserved.
Keywords: Cervical cancer; Radical hysterectomy; Human embryology; Pelvic anatomy; Adjuvant radiation

Introduction
Conventional concepts of local tumor spread follow the
model of undirected perifocal tumor growth. Tumor propagation
per continuitatem is considered to be a random process with
migrating tumor cells or cell clusters favoring paths of low
mechanical resistance such as vascular or perineural spaces. The
translation of that view into clinical practice has led to radical
organ resection and wide tumor excision as surgical treatment
for local tumor control. Radical organ resection removes the
macroscopically complete tumor-bearing organ together with
Fax: +49 341 9723419.
E-mail address: michael.hoeckel@medizin.uni-leipzig.de.
0090-8258/$ - see front matter 2007 Elsevier Inc. All rights reserved.
doi:10.1016/j.ygyno.2007.07.049

adjacent tissue tailored to the clinical tumor extent. Wide

excision describes the resection of a tumor surrounded by a
mantle of uninvolved tissue of defined thickness within an
organ. Both types of local operations are combined with more or
less extended lymph node dissections for regional tumor control
depending on the type and stage of the malignancy.
For carcinoma of the uterine cervix, local tumor spread with
undirected intra- and transcervical growth is assumed [1] and
standard surgical treatment of early macroscopic disease is time
honored radical hysterectomy [24]. The staged resection of the
paracervical tissues as main feature of conventional radical
hysterectomy is based on an uterocentric and ligament-focused
view of the surgical anatomy. Although the clinical results
obtained with this surgical treatment are favorable for small node

M. Hckel / Gynecologic Oncology 107 (2007) S106S112

and vascular space negative tumors, the necessity of adding

adjuvant (chemo)radiation in patients with histopathological
high-risk features (which may exceed 50% in current series)
and the high moderate and severe treatment-related morbidity reported for standard surgical treatment are unsatisfactory
[5].
I propose that local tumor spread is not completely random
but may be confined for an extended phase in malignant progression to a permissive compartment which can be morphologically deduced from the embryologic development of the
organ from which the neoplasm arises. Although tumor
propagation is usually undirected within that compartment the
neoplasm respects the compartment borders for extended phases
in malignant progression. Only late in the disease process
adjacent compartments of different embryological origin are
invaded and even in these late stages a hierarchy of embryological kinship is maintained.
The logic from this developmental view is compartment
resection as new principle of surgical radicality for local tumor
control. Depending on the tumor features surgical radicality
may be reduced to sub- or intracompartment resection or has to
be extended to supra- and multicompartment resection.
Compartment resection should result in a high local tumor
control rate without additional radiation. As tissues of different
embryologic origin may be left in situ despite their close
proximity to a malignant tumor, treatment-related morbidity
should be significantly less than that of conventional radical
organ resection.
We have deduced the Mllerian morphogenetic unit in the
adult female from the study of uterovaginal development and
demonstrated that its distal part represents the permissive compartment for the local spread of cervical carcinoma. We have
shown that complete resection of the distal Mllerian morphogenetic unit by total mesometrial resection (TMMR) leads to
excellent pelvic tumor control without adjuvant radiation and
minimizes treatment-related morbidity in patients with carcinoma of the uterine cervix FIGO stages IBIIB [6]. Herein we
update the results of an ongoing prospective controlled trial at
the University of Leipzig. Moreover, we provide arguments to
favor the developmental view and compartment resection over
the uterocentric/ligament-focused perspective and classified
paracervical resection.
Methods
The resection of developmentally defined tissue compartments as principle
of surgical radicality is evaluated at the Department of Ob/Gyn in a prospective
controlled trial in patients with histologically proven carcinoma of the uterine
cervix, FIGO stages IBIIB, treated with total mesometrial resection (TMMR)
abandoning adjuvant radiation irrespective of the definitive histopathological
risk factors. Patients admitted for treatment are consecutively enrolled into the
study unless they meet the following exclusion criteria:
Patient related:

comorbidity that would pose a high risk on extended surgical treatment;

morbid obesity with a body mass index N35;
age 80 years;
second malignancy;
preference for primary (chemo)radiotherapy which is offered to all patients
as treatment alternative.

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Tumor related:
evidence for tumor involvement of the vesicouterine/-vaginal space from
clinical and/or MRI evaluation;
neuroendocrine tumor histology;
distant metastases except in the periaortic lymph nodes.
The tumors are initially staged strictly according to the FIGO criteria [5]. In
addition, all patients undergo pelvic MRI and the scans are presented during the
clinical examination under anesthesia. Patients with locally advanced tumors
(FIGO stages IB2, IIA N4 cm and IIB) and those with suspected lymph node
metastases are screened for distant metastases with CT abdomen, thorax, bone
scan or PET/CT.
TMMR is supplemented by nerve-sparing therapeutic pelvic lymph node
dissection [7]. In case of pelvic lymph node metastases detected by
intraoperative frozen section investigation, nerve-sparing staged periaortic
lymph node dissection is added. Bilateral ovariectomy is recommended in case
of adenocarcinoma [8] and with proven lymph node metastases. The step-bystep surgical techniques of TMMR and nerve-sparing pelvic and periaortic
lymph node dissection have been described earlier [6,7].
Patients with tumors of 5 cm clinical size receive neoadjuvant
chemotherapy (56 weekly courses cisplatinum 40 mg/m2). All patients are
informed about the concept and details of the surgical procedure. They have to
give informed consent before initiation of the treatment.
The TMMR specimens and the resected lymph node-bearing tissues are
prepared for histopathological investigation according to the protocol of the
Cancer Committee of the College of American Pathologists [9]. Resection status
is examined in paraffin tissue blocks covering the resection margins of the
vaginal cuff and the vascular as well as suspensory mesometrial tissue. The
anterior (bladder) and posterior (rectal) resection margins of the cervical stroma
are evaluated from tissue blocks containing the tumor and the adjacent surgical
margin of the cervix which have been inked.
From 2006 on patients with two and more pelvic lymph node metastases and
all patients with periaortic lymph node metastases have been offered adjuvant
chemotherapy with up to 6 courses cisplatinum 75 mg/m2 at 3 weeks intervals.
All patients treated with TMMR are enrolled in a follow-up program of 3 months
intervals for the first 2 years postoperatively and 6 months intervals thereafter.
All complications (intra- and postoperative) and sequelae of the treatment are
specified and graded according to the Franco-Italian glossary [10]. Diseasespecific overall and relapse-free survival is analyzed with the KaplanMeier
method using SPSS software (version 14.0). The study has been approved by the
Ethics Committee of the Medical Faculty of the University of Leipzig.

Results and discussion

Mllerian compartment
The Mllerian compartment is a morphogenetic unit in the
female derived from the paramesonephric ducts and the
periductal mesenchyme of the uterovaginal anlage.
Assuming topographical robustness during tissue differentiation the Mllerian compartment can be deduced from the tissue
complex of the uterovaginal anlage in the 8- to 9-week-old
female embryo, followed morphologically through the later
stages of fetal development and identified in the adult. The
proximal part of the Mllerian compartment is located mainly
intraperitoneally and the distal part mainly subperitoneally. The
proximal subcompartment consists of the Fallopian tubes,
mesosalpinx, uterine corpus and peritoneal mesometrium
(broad ligament). As these structures are completely covered
with peritoneum they are easily to be identified. The distal
subcompartment contains the uterine cervix, vagina, paracervical and paravaginal tissues. Its three-dimensional structure is

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M. Hckel / Gynecologic Oncology 107 (2007) S106S112

of dense fibrous tissue. In the axial plane its section is

horseshoe-like extending over the anterior mesorectum, in the
sagittal plane it follows the pelvic curvature. The more proximal
parts of the suspensory mesometrium are dorsally covered by
peritoneum and correspond to the rectouterine (uterosacral)
ligaments. Laterally attached to the suspensory mesometrium
runs the inferior hypogastric plexus on both sides.
The topographic anatomy of the Mllerian compartment as a
morphogenetic unit is schematically depicted in Fig. 1. In situ,
the Mllerian compartment can be clearly identified in axial
sections of the human female pelvis such as the Visible Woman
Project (National Library of Medicine, NIH, Bethesda ML,
USA) and with high resolution pelvic MRI. Due to its bordering
lamellae the subperitoneal parts of the Mllerian compartment
can be completely separated from the attached non-Mllerian
tissues. Major vascular connections that need to be ligated or
sealed exist only between the vascular mesometrium and the
mesobladder.
MRI imaging of locally advanced cervical carcinomas and
the histopathological and clinical results with total mesometrial
resection [6] are consistent with the theory of local tumor spread
within the permissive compartment of the morphogenetic unit
defined by embryological development.
Total mesometrial resection
Fig. 1. Schematic demonstration of the Mllerian compartment. For clarification
of the complex spatial extension of the morphogenetic unit derived from the
uterovaginal anlage, it has been depleted from the peritoneum and subperitoneally separated from the attached non-Mllerian tissues (mesorectum,
autonomic nerve plexus, mesobladder). Moreover, the Mllerian compartment
highlighted with green coloring has been transected mid-sagittally omitting its
right half. See text for further details.

With TMMR compartment resection, a new principle of

radicality, is applied for surgical therapy to achieve local tumor
control. This operation removes the complete Mllerian
compartment except parts of the vagina. With respect to the
vagina the resection is intracompartmental and therefore a
resection margin of 1.52 cm microscopically tumor-free tissue

complex and its topography is further complicated due to its

attachment to compartments of different embryological origin
such as the genitourinary, rectal and pelvic parietal compartments. In order to differentiate the paracervical/paravaginal
tissues belonging to the Mllerian compartment from the nonMllerian ones I suggest to apply the term mesometrium in a
broader sense to designate not only the peritoneal fold between
the uterus and the lateral pelvic wall but also the Mllerian part
of the paracervix and paracolpos. This subperitoneal mesometrium (mesocervix, mesocolpos) is made up on both sides of a
dorsolaterally directed soft tissue sheet containing the uterine
and vaginal arteries and veins, lymphatic vessels, small amounts
of fatty tissue and occasionally small lymph nodes. This vascular mesometrium is covered both ventrally and dorsally by a
continuous bordering lamella. Anterolaterally to the vascular
mesometrium abuts the bilateral mesobladder containing the
superior and inferior vesical arteries and veins and autonomic
bladder nerves. Both the vascular mesometrium and the
mesobladder are attached to each other and exhibit numerous
vascular connections, particularly venous ones.
The second mesometrial tissue components are the dorsally
directed fixation structures of the uterovaginal tract. This suspensory mesometrium can be described as a double curved sheet

Table 1
Histopathologic characterization of 163 TMMR, 163 extended pelvic and 45
periaortic lymph node specimens
Number of patients
Stage
pT1b1 + ypT1b1
pT1b2 + ypT1b2
pT2a
pT2b + ypT2b
pT3a
pN0 + ypN0
pN1 + ypN1
pM0(LYM) + ypM0(LYM)
pM1(LYM)
Resection state
R0/R1
Lymphvascular involvement
L0/L1/LX
V0/V1/VX
Histologic types
Squamous cell carcinoma
Adenocarcinoma
Adenosquamous carcinoma
Other
Invasion depth
1/3/2/3/3/3

101 + 6
15 + 5
6
20 + 9
1
116 + 15
27 + 5
23 + 15
7
162/1
61/98/4
146/14/3
125
28
9
1
47/41/74

M. Hckel / Gynecologic Oncology 107 (2007) S106S112

S109

Fig. 2. KaplanMeier curves of relapse-free survival (left panels) and disease-specific survival (right panels) of the whole patient cohort (A, B) and of subgroups stratified for
FIGO stages (C, D) and histopathologic risk factors (E, F). High-risk factors were pN1, pT2b stages and combinations of lymph vascular space involvement, cervical stroma
invasion and tumor size according to the GOG#92 trial in pT1b pN0 stages.

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M. Hckel / Gynecologic Oncology 107 (2007) S106S112

Table 2
Total number of complications according to the Franco-Italian glossary by organ
system and grade which occurred in 163 patients treated with TMMR

Gastrointestinal
Urinary
Vascular
Cutaneous
Peripheral nerves
Total

G1

G2

7
12
34
3
3
59

2
3
7
1
2
15

G3

G4

Total
9a
15b
41c
4d
5e
74

Subileus; b impaired bladder function, stress incontinence, bladder lesion;

lymphcyst, lymphedema, thrombosis or thromboembolism; dabdominal wound
infection; efemoral nerve symptoms.

is regarded obligatory. Otherwise, the presence of an intact

bordering lamella represents radical tumor resection. Contrary
to the traditional radical hysterectomy, the paracervical and
paravaginal resection of FIGO IB and IIA cases is not tailored
to the tumor extension, but generally the complete Mllerian
compartment is removed. Non-Mllerian tissues such as the
mesorectum, inferior hypogastric plexus and mesobladder
with the vesical vessels and autonomic nerves remain in situ
despite their (possible) proximity to the tumor.
For regional tumor control, TMMR is supplemented by
therapeutic pelvic lymph node dissection sparing the autonomic
nerves (hypogastric nerves, superior hypogastric plexus).
Staged nerve-sparing periaortic lymph node dissection is
performed in case of intraoperatively detected pelvic lymph
node metastases.
From 7/1998 until 12/2006, 163 consecutive patients
underwent TMMR without adjuvant radiation and were
followed prospectively. Median age of the patients was
41 years (2477 years), median body mass index 24 (1535).
FIGO stage distribution was IB1 in 94 patients, IB2 in 21
patients, IIA in 14 patients and IIB in 34 patients. Twenty
patients with tumors 5 cm received preoperative chemotherapy
and so far 5 patients with N2 pelvic and/or periaortic lymph
node metastases were treated with adjuvant chemotherapy.
The histopathological results are summarized in Table 1.
Median tumor size was 2.7 cm (0.710.0 cm). Mean count of
removed pelvic lymph nodes was 46 12. 11 7 periaortic
lymph nodes were resected as in most cases only the lower
lymph node basins were treated. Thirty-two patients (20%) had
pelvic lymph node metastases (median 2, range 118) and 7
patients (4%) exhibited periaortic lymph node metastases. All
except one TMMR specimens had microscopically tumor-free
resection margins (R0). The one patient with lymph vascular
space involvement of the dorsolateral resection margin also had
49 pelvic and periaortic lymph node metastases.
No patient has been lost for follow-up. Median observation
time for all patients was 45 months (range: 3104 months).
Four of the 163 patients had a local recurrence. Two patients
relapsed with simultaneous locoregional tumors and distant
metastases. In four patients only distant metastases were found
at the time of relapse. Five patients with recurrences died of
their disease, one patient died of intercurrent disease (alcoholinduced liver insufficiency). The KaplanMeier curves for
relapse-free and disease-specific survival are shown in Fig. 2.

The 3-year relapse-free and disease-specific survival probabilities are 93% and 96% for the whole group; 98% and 100% for
the histopathological low-risk subgroup of 68 patients and 90%
and 95% for the 95 patients with histopathological high-risk
factors (pN1; pT2b; lymphvascular space involvement, cervical
stroma invasion and tumor size according to the GOG#92 trial
[11]) who did not receive adjuvant radiation.
By histopathological investigation macroscopic and microscopic extracervical continuous local tumor spread (pT2a, pT2b
and pT3a) was detected in 36 patients. In 59 additional cases
exhibiting pelvic and periaortic lymph node metastases or poor
prognostic combinations of tumor size, deep cervical stroma
invasion and lymph vascular space involvement, a high risk of
occult extracervical local tumor spread had to be assumed [12].
Since additional radiation has been used not at all, the high R0
resection rate and the low local failure rate strongly support the
hypothesis that macroscopic, microscopic and occult local tumor
spread is confined to the resected Mllerian compartment in
FIGO stages IBIIB cervical carcinomas.
The complications and sequelae of the TMMR treatment in
163 patients assessed according to the Franco-Italian glossary
[10] are compiled in Table 2. TMMR treatment did not lead to
severe (grades 3 and 4) complications/sequelae. The most
frequent sequelae were lymph edema of the legs or the mons
pubis region classified as mild (grade 1) in 16 patients (10%)
and moderate (grade 2) in 6 patients (4%). One hundred and
three patients (63%) had a completely uneventful posttreatment
course without sequelae other than infertility/menopause and a
laparotomy scar.
Resection margin status, pelvic control, relapse-free and
disease-specific survival and treatment-related morbidity
obtained by TMMR without adjuvant radiation are favorable

Table 3
Terminology of subperitoneal pericervicovaginal tissues
Uterocentric view

Ligamentfocused view

Developmental view

Anterior parametrium

Vesicouterine
ligament
Pubocervical
ligament
Anterior leaf
Vesicocervical
ligament
Posterior leaf
Vesicovaginal
ligament
Cardinal ligament
Transverse
cervical ligament

Mesobladder

Lateral parametrium,
paracervix, paracolpium

Posterior parametrium

Uterosacral
ligament
Rectouterine
ligament
Rectovaginal
ligament

Anterior mesobladder

Posterior mesobladder

Vascular mesometrium
Deep internal iliac
(paracervical) lymph nodes
Distal inferior hypogastric
plexus
Suspensory mesometrium
Proximal inferior
hypogastric plexus

Italics: Structures integral to the embryologically defined Mllerian compartment.

M. Hckel / Gynecologic Oncology 107 (2007) S106S112

compared to historical controls. Microscopic and macroscopic

intralesional resections with standard radical hysterectomy are
reported in N10% of the cases [13]. According to the recent
FIGO Annual Report, 3-year relapse-free and overall survival
for a patient cohort matched by FIGO stages are 87% and 88%
with a local failure rate of 6% [14]. Using the same instruments
for the prospective evaluation of morbidity caused by cervical
cancer treatment [10] TMMR has been associated with 8%
grade 2 and no grade 3 complications so far as compared to 28%
grades 2 and 3 complications in the standard surgical treatment
[13]. Systematic prospective evaluation of the long-term
urethrovesical, vulvovaginal and anorectal functions could not
detect major disturbances in patients after therapy with TMMR
[7].
Certainly, confirmation of the results by other groups is the
next necessary step. A prospective controlled multicenter trial
comparing the treatment of patients with carcinoma of the
uterine cervix FIGO stages IBIIA by TMMR, therapeutic
lymph node dissection (neo)adjuvant chemotherapy without
adjuvant radiation with those receiving standard radical
hysterectomy adjuvant (chemo)radiation has been set up by
the Working Group Gynecologic Oncology (AGO) of the
Germany Society of Obstetrics and Gynecology (Uterus trial
#12).
Classification of radical hysterectomy
The widely accepted current surgical treatment concept of
cervical carcinoma FIGO stages IBIIA is tailored radical
hysterectomy and adjuvant (chemo)radiation in case of histopathological high-risk features. Tumor-adapted tailoring
relates to the amount of paracervical and vaginal resection. In
order to standardize this variable part of radical hysterectomy
classification schemes have been proposed by several authors
[1517]. The five classes of extended hysterectomy by Piver
et al. [15] gained the greatest popularity, particularly the classes
II and III. Recently (February 2007), expert consensus for a
revised classification was aspired at the International Symposium on Radical Hysterectomy in Kyoto, Japan. The Kyoto
consensus applies strict anatomical definitions according to the
Terminologia Anatomica [18] and considers new developments
such as sparing of autonomic nerves, fertility preservation,
lateral extension, laparoscopic and robotic techniques. However, all proposals for classifying radical hysterectomy including
the Kyoto consensus adhere to the traditional concepts of local
tumor spread and hold an uterocentric and ligament-focused
view of the subperitoneal anatomy in the female pelvis.
The uterocentric perspective is misleading as it does not
distinguish tissues integral to the uterovaginal tract from those
which are only attached or connected to it, such as the paracervical lymph nodes (which belong to the parietal pelvic compartments) and the mesobladder with the vesical vessels and the
bladder branches of the distal inferior hypogastric plexus. The
ligament-focused view is also misleading as prominent structures such as the cardinal ligament and the posterior leaf of the
vesicouterine ligament do not exhibit any suspensory functions
at all. Moreover, the sagittal pelvic curvature is usually not

S111

considered, pretending a transverse location of the dorsally

directed uterovaginal attachments in the deep pelvis.
The developmental view of local tumor spread and surgical
anatomy avoids these shortcomings as it indicates the origin and
function of the pericervicovaginal tissues (Table 3). A
classification of paracervical and paravaginal tissue resection
for the surgical treatment of FIGO stage IBIIA cervical carcinomas is obsolete with TMMR as the therapeutic goal is the
resection of the complete morphogenetic unit, i.e., the Mllerian
compartment in order to dispense with adjuvant radiation. Only
the vaginal resection is variable depending on the caudal tumor
extension and the occasional presence of VAIN III.
The new principle of radicality in surgical oncology in terms
of compartment resection is versatile as it can be reduced to suband intracompartmental resection on one hand and extended to
supra- and multicompartmental resection on the other hand.
With respect to the treatment of cervical cancer intracompartmental resection with preservation of fertility may be performed
in small, node and vascular space negative tumors. For
supracompartmental resection, TMMR is extended by including
the common root of the urogenital mesentery and eventually the
whole internal iliac vessel system that allows surgical pelvic
control of advanced tumors with (confluent) lymph node
metastases. Pelvic multimesovisceral resection and the laterally
extended endopelvic resection (LEER) are further surgical
extensions applying the same principle [19].
In conclusion, the developmental view on adult topographic
anatomy and on local tumor spread as well as its consequence in
terms of compartment resection for local tumor control offer a
new perspective in surgical oncology which may challenge the
traditional treatment standard of various tumor entities. The
logic of the approach and the excellent results from its application in the treatment of cervical cancer in one institution justify
to consider participation in a prospective multi-institutional trial
for the evaluation of TMMR without classifying paracervical
resection and without adjuvant radiation for cervical cancer
FIGO stages IBIIA irrespective of histopathological risk
factors.
Conflict of interest statement
I declare that I have no conflict of interest.

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