Gynecologic Oncology 122 (2011) 264–268

Contents lists available at ScienceDirect

Gynecologic Oncology
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / y g y n o

New classification system of radical hysterectomy: Emphasis on a

three-dimensional anatomic template for parametrial resection☆
D. Cibula a,⁎, N.R. Abu-Rustum b, P. Benedetti-Panici c, C. Köhler d, F. Raspagliesi e,
D. Querleu f, g, C.P. Morrow h
a
Gynecologic Oncology Centre, Department of Obstetrics and Gynaecology, General University Hospital, First Medical School, Charles University, Prague, Czech Republic
b
Department of Surgery, Gynecology Service, Minimally Invasive Surgery, Memorial Sloan-Kettering Cancer Center, New York, NY, USA
c
Department of Obstetrics and Gynecology, University "Sapienza", Rome, Italy
d
Department of Gynecology, Campus Mitte, Charité University Medicine, Berlin, Germany
e
Gynecologic Oncology Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy
f
Department of Gynecologic Oncology, Comprehensive Cancer Center, Institut Claudius Regaud, University of Toulouse, France
g
McGill University, Montreal, Canada
h
Keck School of Medicine, University of Southern California, Los Angeles, CA, USA

a r t i c l e i n f o a b s t r a c t

Article history: Objective. The international acceptance of a universal classification system for radical hysterectomy is one of
Received 26 March 2011 the important challenges in gynecologic oncology. The recently published classification system by Querleu
Accepted 19 April 2011 and Morrow is a relevant proposal that has been well received by the professional community. However, it
Available online 17 May 2011 does not include a description of parametrial resection in three dimensions, which mostly determines post-
operative morbidity.
Keywords:
Methods. The intention of this follow-up paper was to further develop the classification system based on the
Radical hysterectomy
Classification
four proposed types of radical hysterectomy (A–D) into a three-dimensional model using standard
Nerve sparing anatomical landmarks for definition of resection margins in longitudinal and transverse dimensions and
demonstrate it on pictures.
Results. Resection margins were defined in longitudinal and transverse dimensions for each suggested type
of radical hysterectomy on all three parts of the parametria. Besides precise description using stable
anatomical landmarks, all resection lines have been shown on intra-operative photographs.
Conclusion. Four types of radical hysteretomy can be precisely defined on a three-dimensional anatomical
template, including nerve sparing procedure. Our paper should contribute to better standardization
(including nomenclature) of the radical hysterectomy, enhancing harmonization of clinical practice in
gynecological oncology.
© 2011 Elsevier Inc. All rights reserved.

Introduction
The proposed radical hysterectomy classification system of Querleu
and Morrow (Q–M classification) [1] has been quoted many times since
its publication in 2008. Its fast acceptance by the professional
community indicates that the principles of the classification system
are properly chosen and the descriptions of the various types of the
procedure correspond to surgical execution. The key strong points of the
Q–M classification include the following: a) it recognizes the extent of
☆ There were no funds received for this work from any of the following organizations:
National Institutes of Health (NIH); Wellcome Trust; Howard Hughes Medical Institute
(HHMI); and other(s).
⁎ Corresponding author at: Gynecological Oncology Centre, Department of Obstetrics
and Gynecology, First Faculty of Medicine and General University Hospital, Charles
University in Prague, Apolinarska 18, Prague 2, Czech Republic. Fax: +420 224967451.
E-mail address: david.cibula@iol.cz (D. Cibula).
parametrial resection as the key and sole parameter for differentiation
between types of radical hysterectomy; b) besides classification, it also
unifies terminology; c) it uses anatomical landmarks to classify
parametrial resection; and d) it includes a nerve-sparing modification
of radical hysterectomy.
The Q–M classification system, however, does not include a
description of parametrial resection in three dimensions, which is a
significant topic that requires further clarification, particularly in the
most frequent types of the procedure, i.e., types C1 and C2. Clear
identification of the resection line in the longitudinal (vertical/deep)
plane is the determining factor for late morbidity and long-term quality
of life [2–5]; this is due to the different requirements for ureteral
dissection and, most importantly, damage to the autonomic pelvic
nerves [6]. The lack of standardization of the longitudinal deep resection
limits of the parametria in radical hysterectomy is a universal problem
that has been mainly unexplored in most educational manuscripts
describing parametrectomy.

0090-8258/$ – see front matter © 2011 Elsevier Inc. All rights reserved.
doi:10.1016/j.ygyno.2011.04.029
 D. Cibula et al. / Gynecologic Oncology 122 (2011) 264–268 265

The article does not include any discussion on the role of different
types of radical hysterectomy in the management of cervical or
endometrial cancer. It should be emphasized that the oncological
outcome or morbidity can be evaluated and data compared between
the institutions only if one classification system is accepted and each
type of the procedure is precisely standardized.
The aim of this paper is to extend the proposed classification
system by defining parametrial resection margins in both transversal
and longitudinal (parametrial deep) dimensions, especially for types
C1 and C2 radical hysterectomy, using stable anatomical landmarks.
We describe the required ureteral dissection and resection margins on
the three parametrial parts and pictorially demonstrate each type of
the procedure.

Terminology

We re-introduce in this paper the term “parametrium”, which is

broadly accepted and provides a single term applicable to all three
anatomical parts: the ventral parametrium (including vesico-uterine
and vesico-vaginal ligaments), the lateral parametrium (paracervix),
and the dorsal parametrium (including recto-uterine and recto-vaginal
ligaments) (Fig. 1).
In line with the Q–M paper, the terms “ventral”, “lateral”, and
“dorsal” are used to describe spatial orientation. The term "mesoureter"
describes the lateral laminar part of the dorsal parametria, which is
stretched dorsally and caudally from the ureter and contains the inferior
hypogastric plexus [7].
Two parts of the ventral parametria are recognized in a sagittal
plane—cranial (above the ureter) and caudal (below the ureter),
divided by the course of the ureter. Due to the tangential route of the
ureter through the ventral parametria, a bigger portion of the medial
leaf of the ventral parametria is exposed and removed in types B or C1
radical hysterectomies.
Two different spaces are described dorsally—the sacro-uterine
space (medial pararectal space) between the rectum and the dorsal
parametrium, and the pararectal fossa (pararectal space) between the
dorsal parametrium and iliac vessels (Fig. 1).
The deep uterine vein (vaginal vein) is an important landmark in
the lateral parametrium (Fig. 2). It is being found during caudal
parametrial dissection located about 1–2 cm below the uterine artery
and vein.
Fig. 2. Perioperative picture of resection lines on the lateral parametrium. A—
paravesical space; B—deep uterine vein (vaginal vein); C—internal iliac vein; D—
uterine vein; E—uterine artery; F—pararectal fossa C1, C2—resection lines on the lateral
parametrium for types C1 and C2 radical hysterectomy.
Types of radical hysterectomy
Type A
This type corresponds to the extrafascial hysterectomy, which
guarantees full removal of the pericervical tissue up to the attachment
of the vaginal fornices.
Ureteral dissection—the ureter does not need to be unroofed.
Parametria—this type does not allow for the resection of the ventral
or lateral parametria, it does not include resection of the dorsal
parametria. The hypogastric plexus, therefore, remains fully preserved.
Type B
This type corresponds to the modified radical hysterectomy.
Identification of autonomic nerves is not required, and the hypogas-
tric plexus remains fully preserved.
Ureteral dissection—the ureter is unroofed and dissected from the
cervix (Fig. 3).

Fig. 1. Perioperative picture of the ventral, lateral and dorsal parametrium. A—ventral
parametrium; B—paravesical space; C—lateral parametrium; D—ureter; E—pararectal Fig. 3. Perioperative picture of horizontal resection lines on the ventral parametrium. A—
fossa (lateral pararectal space); F—dorsal parametrium; G—sacro-uterine space (medial paravesical space; B—umbilical ligament; C—ureter; B, C1, C2—resection lines on the
pararectal space); H—rectum; I—cervix. ventral parametrium for types B, C1 and C2 radical hysterectomy.
266 D. Cibula et al. / Gynecologic Oncology 122 (2011) 264–268

Ventral parametria—as the ureter is only unroofed in its course

through the parametria, it allows only for the resection of a small
initial part of the medial leaf of the ventral parametria (Figs. 3, 4).
Lateral parametria—as the ureter is unroofed, dissected from the
cervix, and displaced laterally, but not dissected from the lateral or
ventral parametria, the resection margin is at a medial aspect of the
ureteral bed, thus allowing for the horizontal resection of about 1–
1.5 cm of the lateral parametria (Figs. 3,4). The ureteral artery,
branching from the uterine artery at its crossing of the ureter, can
serve as a helpful landmark, and is usually easily identified and can be
spared. Longitudinal (deep parametrial or vertical) resection limit is
formed by a tangential plane of the vaginal cuff resection.
Dorsal parametria—type B aims for horizontal resection of 1–2 cm
dorsally from the cervix (Fig. 5). The resection line corresponds to the
amount of removed lateral parametria. Longitudinally, the removal
margin is at the level of the vaginal cuff resection, but it must not be
deeper below the course of the ureter due to the branches of the
hypogastric plexus.

Fig. 5. Perioperative picture of resection lines on the dorsal parametrium. A—ureter; B—

Type C
The Q–M classification system distinguishes between a type C1
procedure, which corresponds to the nerve-sparing modification, and
the type C2, which aims for a complete parametrial resection. There
are significantly distinct resection margins between the two types,
particularly in the longitudinal (deep parametrial or vertical)
dimension, which are determined by the course of the main branches
of the inferior hypogastric plexus in the C1 type.
Type C1 requires separation of two parts of the dorsal parametria:
the medial part, which entails recto-uterine and recto-vaginal
ligaments, and the lateral laminar structure, also called mesoureter,
which contains the hypogastric plexus. Furthermore, type C1 requires
only a partial dissection of the ureter from the ventral parametria,
which is usually asymmetric towards more extensive resection of the
medial leaf of the cranial (above the ureter) part of the ventral
parametria (Figs. 3,4). In the C2 type, the ureter is completely
dissected from the ventral parametria up to the urinary bladder wall
(Figs. 3,4). Defining the resection limits on the longitudinal (deep
parametrial or vertical) plane is crucial for distinguishing between
types C1 and C2.
Ureteral dissection—in the C1 type, the ureter is unroofed, dissected
from the cervix and from the lateral parametria, but only partially
mesoureter; C—space between the recto-uterine ligament and mesoureter (hypogastric
plexus); D—branches of the hypogastric plexus (white strips); E—recto-uterine
ligament; F—cervix B, C1, C2—resection lines on the dorsal parametrium for types B,
C1 and C2 radical hysterectomy.
from the ventral parametria (1–2 cm). The C2 type requires complete
dissection of the ureter from the ventral parametria up to the bladder
wall.
Lateral parametria
Transverse (horizontal) resection margins
• C1–C2—the lateral border is identical for both types, formed by the
medial aspect of the internal iliac vein and artery (Fig. 2).
Longitudinal (deep parametrial or vertical) resection margins
• C1—vaginal vein (deep uterine vein)—the deep parametrial resection
margin is formed by the vaginal vein, thus the caudal part of the lateral
parametria containing the splanchnic nerves is preserved (Fig. 2).
• C2—pelvic floor (sacral bone)—the resection line continues alongside
the medial aspect of the internal iliac vessels and pudendal vessels
caudally up to the pelvic floor (Fig. 2). The pararectal and paravesical
spaces are completely unified sacrificing the splanchnic nerves in the
caudal part. Such deep resection allows for greater mobility of the
lateral parametria, facilitating its complete removal.

Ventral parametria

Transverse resection margins

• C1—partial dissection of the ureter from the ventral parametria allows

for resection of 1–2 cm of the ventral parametria (Figs. 3,4).
• C2—urinary bladder wall—complete dissection of the ureter from the
ventral parametria is required, which allows for complete removal of
the ventral parametria up to the urinary bladder wall; both medial and
lateral leafs of the ventral parametria are resected equally (Figs. 3,4).

Longitudinal resection margins

• C1—resection line is formed by bladder branches of the hypogastric

plexus localized below the course of the ureter [8,9] (Fig. 4).
Fig. 4. Perioperative picture of resection lines on the ventral parametrium. A—urinary
• C2—resection line is formed by the level of the paracolpium and vaginal
bladder; B—ureter; C—cervix B, C1, C2—resection lines on the ventral parametrium for resection. Both cranial and caudal (below the ureter) parts of the
types B, C2 and C2 radical hysterectomy. ventral parametria are removed (Fig. 4). Bladder branches of the
 D. Cibula et al. / Gynecologic Oncology 122 (2011) 264–268
hypogastric plexus are sacrificed; thus, their identification is not
required.
Dorsal parametria
Transverse resection margins
• C1–C2—the dorsal border is identical for both types, formed by the
recto-uterine ligament attachment to the rectum (Fig. 5).
Longitudinal resection margins
• C1—this type requires sagittal dissection of the hypogastric nerves
from recto-uterine and recto-vaginal ligaments (Figs. 5,6). Main
branches of the hypogastric plexus must be preserved on the lateral
part (mesoureter), while the caudal limit on the recto-uterine and
recto-vaginal ligaments is formed by the tangential plane of the
vaginal cuff resection.
• C2—this type aims at a complete resection of the dorsal parametria
deeply below the rectal attachment, thus branches of the hypogastric
plexus are sacrificed (Figs. 5,6).
Type D
This type differs from type C2 only in the lateral extent of the lateral
parametria resection. Ureteral dissection and resection of both dorsal
and ventral parametria is identical to the type C2. Laterally, however, it
requires ligation and removal of the internal iliac artery and vein,
together with their branches, including the gluteal, internal pudendal,
and obturator vessels.
Lateral parametria
Transverse resection margin
• ligation of the internal iliac artery and vein, their removal together
with their branches in the lateral parametria, allows for further lateral
extension of the resection. The lateral resection line is formed by the
lumbosacral nerve plexus, piriformis muscle, and obturator internal
muscle. This type of radical hysterectomy is rarely performed for
locally advanced tumors [10].
Fig. 6. Perioperative picture of resection lines on the mesoureter (left side). A—recto-
uterine ligament; B—space between the recto-uterine ligament and mesoureter
(hypogastric plexus); C—branches of the hypogastric plexus; D—mesoureter; E—ureter
C1, C2—resection lines for types C1 and C2 radical hysterectomy.
267
Discussion
Different terminology and classifications are currently being used
to describe the varieties of the radical hysterectomy. An absence of
uniformly accepted classification is a major limitation for sharing of
results, conducting credible multicenter surgical trials, and setting
standards for postgraduate education.
The detailed description and proper understanding of the different
types of radical hysterectomy is of utmost importance, as the extent of
parametria resection determines late morbidity, especially bladder
and rectal dysfunctions [2–4,11]. It is likely that both, damage to
autonomic nerves and distinct extent of tissue removal, contribute to
the morbidity [12].
The classification of radical hysterectomy should incorporate
certain principles. The key and sole parameter for differentiation
between types of radical hysterectomy is the extent of parametria
resection. The extent of resection should be precisely defined for all
three parts of the parametria (ventral, lateral and dorsal) in three
dimensions. The type of the procedure may be different on each side
of the cervix if tumor growth is asymmetrical. The excision or
removal of other organs or structures (urinary bladder, ureter,
rectum, and pelvic floor muscle) should not be included in the
classification system. Also, the size of the removed vaginal cuff is not
a decisive parameter for procedure classification. Although the
classification system is proposed for radical hysterectomy, it can
also apply to the radical trachelectomy and the radical parame-
trectomy (a procedure that usually follows inadequate simple
hysterectomy).
For the proper execution, teaching, and reproducibility of each
surgical procedure, it is crucial to identify stable anatomical landmarks.
It should be understood, however, that only a few such structures are
found in the pelvis, including the urinary bladder, rectum, ureter, larger
vessels, and nerves. The above landmarks are used in this paper to define
the majority of resection margins, thus allowing for the precise
standardization of a procedure´s execution.
In conclusion, the aim of this consensus paper has been to refine
the parametrial resection for the most common types of radical
hysterectomy (types B, C1, and C2), with emphasis on a three-
dimensional description of the resection limits. We believe that the Q–
M classification system is an excellent proposal to be applied in
clinical practice. Our extension of the proposal should contribute to
better standardization of the different types of the procedure,
enhancing reproducibility and harmonization for clinical practice in
gynecological oncology.
Conflict of interest statement
Authors Cibula D, Abu-Rustum NR, Benedetti-Panici P, Köhler C, Raspagliesi F, Querleu
D and Morrow P have no conflicts of interest.
References
[1] Querleu D, Morrow CP. Classification of radical hysterectomy. Lancet Oncol
2008;9:297–303.
[2] Landoni F, Maneo A, Cormio G, Perego P, Milani R, Caruso O, Mangioni C. Class II
versus class III radical hysterectomy in stage IB-IIA cervical cancer: a prospective
randomized study. Gynecol Oncol 2001;80:3–12.
[3] Cibula D, Velechovska P, Sláma J, Fischerova D, Pinkavova I, Pavlista D, et al. Late
morbidity following nerve-sparing radical hysterectomy. Gynecol Oncol
2010;116:506–11.
[4] Ditto A, Martinelli F, Hanozet F, Reato C, Solima E, Zanaboni F, et al. Class III NSRH:
oncological outcome in 170 cervical cancer patients. Gynecol Oncol 2010;119:
192–7.
[5] Possover M, Stober S, Plaul K, Schneider A. Identification and preservation of the
motoric innervation of the bladder in radical hysterectomy type III. Gynecol Oncol
2000;79:154–7.
[6] Ercoli A, Delmas V, Gadonneix P, Fanfani F, Villet R, Paparella P, Manusco S,
Scambia G. Classical and nerve-sparing radical hysterectomy: an evaluation of
the risk of injury to the autonomous pelvic nerves. Surg Radiol Anat 2003;25:
200–6.
268 D. Cibula et al. / Gynecologic Oncology 122 (2011) 264–268
[7] Trimbos JB, Maas CP, Deruiter MC, Peters AA, Kenter GG. A nerve-sparing radical
hysterectomy: guidelines and feasibility in Western patients. Int J Gynecol Cancer
2001;11:180–6.
[8] Kato T, Murakami G, Yabuki Y. Does the cardinal ligament of the uterus contain a nerve
that should be preserved in radical hysterectomy? Anat Sci Int 2002;77:161–8.
[9] Katahira A, Niikura H, Ito K, Takano T, Nagase S, Murakami G, Yaegashi N.
Vesicouterine ligament contains abundant autonomic nerve ganglion cells: the
distribution in histology concerning nerve-sparing radical hysterectomy. Int J
Gynecol Cancer 2008;18:193–8.
[10] Palfalvi L, Ungar L. Laterally extended parametrectomy (LEP), the technique for
radical pelvic side wall dissection: feasibility, technique and results. Int J Gynecol
Cancer 2003;13:914–7.
[11] Raspagliesi F, Ditto A, Fontanelli R, Zanaboni F, Solima E, Spatti G, et al. Type II
versus Type III nerve sparing radical hysterectomy: comparison of lower urinary
tract dysfunctions. Gynecol Oncol 2006;102:256–62.
[12] Cibula D, Sláma J, Velechovská P, Fischerova D, Zikán M, Pinkavová I, Hill M.
Factors affecting spontaneous voiding recovery after radical hysterectomy. Int J
Gynecol Cancer 2010;20:685–90.