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American Journal of Obstetrics and Gynecology (2005) 193, 7–15

www.ajog.org

EDITORS’ CHOICE

Discrepancies between classic anatomy and modern


gynecologic surgery on pelvic connective tissue
structure: Harmonization of those concepts by
collaborative cadaver dissection
Yoshihiko Yabuki, MD, DMSc,a,* Hiromasa Sasaki, MD, DMSc,b
Noboru Hatakeyama, MD, DMSc,c Gen Murakami, MD, DMScd

Department of Obstetrics and Gynecology, Hokuriku Central Hospital, Oyabe, Japana; Department of Obstetrics
and Gynecology, Ishikawa Prefectural Central Hospital, Kanazawa, Japanb; Department of Anesthesiology,
Toyama Medical and Pharmaceutical University, Toyama, Japanc; and Department of Anatomy, Sapporo
Medical University School of Medicine, Sapporo, Japand

Received for publication September 14, 2004; revised January 27, 2005; accepted February 22, 2005

KEY WORDS Objective: The purpose of this study was to solve a disagreement regarding the anatomy of the
Mackenrodt and pelvic connective tissue in 19th and 20th century, and to establish new surgical anatomy.
cardinal ligaments Study design: The study involved the dissection 26 female cadavers. The ligamentous structure of
Pelvic connective the pelvis was examined by developing the paravesical and pararectal spaces, using our standard
tissue procedure of radical hysterectomy.
Paravesical and Results: The lateral ligamentous structure of the pelvis was a plate complex, which consisted of
pararectal spaces the vesicohypogastric fascia, the transverse cervical ligament, and lateral ligament of the rectum.
Pelvic autonomic The 3-dimensional relationship of this complex and the pelvic organs was sagittaly perpendicular.
nerves The pelvic connective tissue was classified into 2 systems, musculofascial and mesentery-like
Radical hysterectomy structures.
Conclusion: The authors examined the discrepancies in 19th century anatomy for the pelvic
connective tissue that is widely accepted in today’s medical field, therewith proposing a new
surgical anatomy for this structure.
Ó 2005 Mosby, Inc. All rights reserved.

The condensation in the base of the broad ligament


was first depicted by Savage.1 Later, it was described as
the cardinal ligament by Kocks,2 and as the ligamentum
transversale colli by Mackenrodt.3 The lateral parame-
trium and paracolpium, known as the Mackenrodt
* Reprint requests: Yoshihiko Yabuki, MD, DMSc, Department of
Obstetrics and Gynecology, Hokuriku Central Hospital, 123 Nodera,
ligament,3,4 has been described as an anatomic structure
Oyabe, Toyama 932-8503, Japan. in which the transverse cervical ligament connects the
E-mail: hirosasa@coral.plala.or.jp short fibrous bundle in an L-like fashion at the level of

0002-9378/$ - see front matter Ó 2005 Mosby, Inc. All rights reserved.
doi:10.1016/j.ajog.2005.02.108
8 Yabuki et al

the ischial spine. Incidentally, the transverse cervical cervical cancer.13-16 As carried out in current radical
ligament was referred to by Mackenrodt as a stout hysterectomy, the following 6 spaces were developed16:
bundle of fibers emanating from the iliac fossa and the paravesical space, paravaginal space, caudal and
inserting into the sidewall of the cervix. Further, the cranial chambers of the pararectal space,6,7 vesicouter-
short fibrous bundle (superior fascia of the levator ani ine space, and rectouterine space. We investigated the
muscle) has also been described as a kind of inferior 6 connective tissue bands16 that appeared between
continuation of the transverse cervical ligament that the spaces, namely, the superficial and deep layers of the
arises from the tendinous arc of the levator ani muscle vesicouterine ligament,9 transverse cervical ligament of
and attaches to the side of the connective tissue sheath Mackenrodt, mesoureter, and the sacrouterine/rectou-
surrounding the vagina. terine ligaments. These maneuvers were followed by
Surgery for cervical cancer during the 20th century simultaneous observation of the fasciae, blood vessels,
was characterized by an extensive dissection of the and nerves, which were dissected while preserving the
connective tissue bundle, or the so-called cardinal liga- anatomic relationship between the fascial structure and
ment, which appeared following development of the the pelvic viscera.
paravesical and pararectal spaces. Latzko-Schiffmann5
incised the short fibrous bundle to develop the caudal Terminology
chamber of the pararectal space,6,7 and dissected the
ligamentous structure that emerged between the caudal In this article, we defined anatomy as practical anatomy
and cranial chambers of the pararectal space.6,7 In or surgical morphology the same as that referred to by
addition, Okabayashi performed a more extensive dis- surgeons such as Mackenrodt, Peham and Amreich; for
section of the vesicouterine ligament by dividing it into example, a term ligament does not denote skeletal liga-
superficial and deep layers following excavation of the ment. The parametrium (Virchow, 1864), cardinal liga-
paravaginal space.8,9 Their operative techniques, which ment (Kocks2), transverse cervical ligament (Mackenrodt3),
became mainstream during the 20th century, obviously retinaculum uteri (Martin17), or the web (Meigs18) is the
contained a component that departed from the concept bundle that connects the pelvic brim and uterine cervix,
of 19th century anatomy. However, during this time, and we generically defined this bundle as the lateral
there was no discussion of any new anatomic concept uterine ligament. The neurovascular stalk (Pern-
that accommodated these new operative techniques.10-12 kopf19,20), hypogastric sheath (Uhlenhuth21), or pelvic
In addition, a large discrepancy is apparent between connective tissue ground bundle (Peham and Amreich6,7)
systemic anatomy and clinical anatomy. In Nomina is the bundle that connects the lateral border of the pelvic
Anatomica, only the pelvic connective tissue bundle organs to the pelvic brim, and we generically defined this
covered with the peritoneum is given any terminology, bundle as the lateral ligament of the pelvis. The short
eg, Ligamentum terues uterii (Processus vaginalis peri- fibrous bundle of Mackenrodt (kurzere Faserbundel3)
tonei), Lig latum uteri, Lig suspensorium ovarii, and Plica denotes the superior fascia of the levator ani muscle or a
rectouterina. There is, however, no terminology what- part of the superior fascia of the pelvic diaphragm. The
soever for spaces and the connective tissue bundles cranial and caudal chambers of the pararectal space6,7 are
exposed by surgical maneuvers. Consequently, surgeons 2 chambers Peham and Amreich divided. The deep layer
have developed different concepts and nomenclature of of the vesicouterine ligament8,9: Okabayashi divided this
their own. A precise understanding of surgical morphol- ligament into superficial and deep layers that roughly
ogy is required in order to solve this problem. correspond to the sagittal bladder septum (Pfeiler,6 pillar)
In this paper, we attempted to establish a new pelvic and ascending bladder septum of Peham and Amreich.6,7
connective tissue anatomy by cadaver dissection in view The paravaginal space9,16 is a space that was created on
of our practical surgical theory.13-16 the lateral aspect of the uterine cervix by Okabayashi to
separate the deep layer of the vesicouterine ligament. The
Material and methods vesicohypogastric fascia or lamina ligamenti umbilica-
lis6,7 is a bundle that connects the lateral umbilical
Study subjects ligament and lateral border of the bladder, or the para-
cysticum. A pseudonym for this is the vesicoumbilical
Topographic dissection of the pelvic connective tissue stalk (Pernkopf).19,20 The lateral ligament of the rectum is
was carried out on 17 fixed Japanese female cadavers, referred to as the bundle that connects the pelvic side wall
and 9 fresh Japanese female cadavers aged 76 to 90 years. and the lateral aspect of the rectum, or the lateral
Procedure paraproctum.22,23 We defined the double-layered fascia
of the pelvic lateral ligament as the anterior fascia and the
The following intrapelvic dissection of tissue was based posterior fascia, respectively. The terminology used by
on previous knowledge from the surgical morphology of Peham and Amreich was referred to from the English
93 patients who had undergone radical hysterectomy for translation by L. K. Ferguson.7
Yabuki et al 9

Figure 1 Vesicohypogastric fascia and Mackenrodt ligament.


Photograph showing development of the left paravesical space
followed by lifting of the uterus with forceps and upward
retraction of the lateral umbilical ligament by the use of a
thread. The vesicohypogastric fascia originating from the
lateral umbilical ligament and the transverse cervical ligament
forms a continuity. There is a hollow (arrowhead 1) between
the transverse cervical ligament and the short fibrous bundle,
leading to the caudal chamber of the pararectal space. In the
supine position, the vesicohypogastric fascia and the transverse
cervical ligament lie vertical to the bladder and uterine cervix,
and the short fibrous bundle is situated horizontally. The area
around the genital hiatus (arrowhead 2) is the true pelvic floor.
U, Uterus; B, bladder; II, internal iliac artery; Ur, ureter; LU,
lateral umbilical artery/ligament; VH, vesicohypogastric fas-
cia; CL, transverse cervical ligament; SB, short fibrous bundle;
TL, tendinous arc of levator ani muscle; TP, tendinous arc of
pelvic fascia; PS, pubic symphysis; SP, sacral promontory; BS, Figure 2 Lateral ligament of the pelvis and cranial chamber
paravesical space. of the pararectal space. This photograph shows a view of
Figure 1 from the cranial aspect, which presents the lateral
ligament of the pelvis with its anterior fascia and vessels
preserved, and only its posterior fascia excised. Also shown is
the exposed cranial chamber of the pararectal space. The
Results paravesical space is seen here filled with paper clay, showing
the border between the paravesical space and the caudal
Mackenrodt ligament and cardinal ligament chamber of the pararectal space (arrowhead). The excised
The Mackenrodt ligament was first observed following lateral ligament of the pelvis forms a plate from the lateral
umbilical ligament to the fascia of the piriformis muscle, which
the development of the paravesical and pararectal spaces
is a complex consisting of the vesicohypogastric fascia, trans-
(Figures 1 and 2). The transverse cervical ligament3,4 verse cervical ligament, and lateral ligament of the rectum. The
was shown to be a mesentery-like structure covered on visceral terminus of this complex crosses the pelvic autonomic
its anterior and posterior aspects with visceral endo- nerves. The direction of the inserted forceps indicates Oka-
pelvic fascia that was an extension of the perivascular bayashi’s space. A large opening via Latzko’s space is ‘the so-
sheath of the internal and external iliac artery/vein. In called pararectal space.’ The deep uterine vein and pelvic
contrast to the transverse cervical ligament, the short splanchnic nerve (S3) are shown here being suspended by a
fibrous bundle3,4 proved to be a part of the superior black thread. An asterisk indicates the paper clay filling of the
fascia of the pelvic diaphragm, or the superior fascia of paravesical space. II, Internal iliac artery; CPG, common
the levator ani muscle, which was stretched between the trunk of internal pudendal and inferior gluteal artery; LU,
tendinous arc of the levator ani muscle and the tendi- lateral umbilical ligament; SV, superior vesical artery; UA,
uterine artery; DV, deep uterine vein; MV, middle vesical
nous arc of the pelvic fascia (white line). In other words,
vessels; MR, middle rectal vessels; SN, pelvic splanchnic nerve;
the short fibrous bundle united, via the tendinous arc of HN, hypogastric nerve; NP, pelvic nerve plexus; Ur, ureter; D,
the pelvic fascia, or indirectly, with the rectovaginal pouch of Douglas; U, uterus; VF, vesicohypogastric fascia;
ligament (deszendierende Rektumpfeiler,6 descending SU, sacrouterine ligament.
rectal septum or pillar), lateral aspect of the vagina,
and pubovesical ligament (Figures 1 and 3).
10 Yabuki et al

Figure 3 Paravesical space and cranial chamber of the Figure 4 Okabayashi’s space for entry into the cranial
pararectal space. Shown here is the right side of the pelvic chamber of the pararectal space: findings of the right pelvic
cavity, which has been divided by the lateral ligament of the cavity. Photograph shows the visceral endopelvic fascia that
pelvis, which indicates the so-called surgical pelvic floor. In the lines the broad ligament being separated from the serosa of the
paravesical space (right photograph), the short fibrous bundle broad ligament, together with the ureter and hypogastric
is separated from the tendinous arc of the levator ani muscle nerves. A further separation in a dorsal direction results in
with a part of the muscle exposed (large arrowhead). On the reaching the cranial chamber of the pararectal space (Figure 6)
cranial aspect there is the cranial chamber of the pararectal (large arrowhead). The membranous tissue in the photograph
space opened via Latzko’s space. The pelvic splanchnic nerves shows the mesoureter formed by a union of the visceral
(S3-4) and the hypogastric nerve then form a pelvic nerve endopelvic fascia of the broad ligament, and the hypogastric
plexus, which, after crossing the lateral ligament of the pelvis, sheath separated from the internal iliac vessels. The ureter and
radiates to the vesical branch facing the paravesical space hypogastric nerves descend within it (small arrowhead). M,
(small arrowhead). SB, Short fibrous bundle; LM, levator ani Mesoureter; Ur, ureter; HN, hypogastric nerves; IF, infundib-
muscle; ML, Mackenrodt ligament; Ur, ureter; SN, pelvic ulopelvic ligament; BL, posterior leaf of broad ligament; OS,
splanchnic nerve; NP, pelvic nerve plexus; HN, hypogastric Okabayashi’s space; U, uterus; R, rectum; LS, Latzko’s space;
nerve; U, uterus; B, bladder; R, rectum; A, aorta. BS, paravesical space; EI, external iliac artery; II, internal iliac
artery.

There was found to be a hollow buried in abundant within which ran the middle rectal artery/vein piercing
adipose tissue at the junction of the short fibrous bundle, the pelvic nerve plexus, which proved to be the lateral
and the anterior fascia of the transverse cervical ligament ligament of the rectum.22,23 As for the transverse cervi-
communicating to the caudal, or anterior, chamber of the cal ligament, it was continuous with the vesicohypogas-
pararectal space (Figure 1, arrowhead 1). These findings tric fascia, which did not correspond with the accepted
negated the existence of any structural continuity of the opinion of it being the condensation in the base of the
transverse cervical ligament and the short fibrous bundle. broad ligament (Figure 1).
The lateral ligament of the pelvis was observed as 1 In summary, the lateral ligament of the pelvis was
continuous plate from the lateral umbilical ligament to a complex in which the lateral paracysticum, or the
the surface of the sacrum (Figures 2 and 3). This plate was vesicohypogastric fascia,5,6 lateral parametrium, or the
then dissected in the area between the space created by a transverse cervical ligament3 and lateral paraproctium
combination of the paravesical space and the caudal or the lateral ligament of the rectum22,23 lay side by side
chamber of the pararectal space, and the cranial chamber in a ventro-dorsal direction. From these findings, it was
of the pararectal space. Further, the caudal chamber of reasonable to conjecture that the superior part of the
the pararectal space was exposed by incision of the short transverse cervical ligament was composed of the uterine
fibrous bundle, and its cranial chamber by separation of artery, and the inferior part was composed of the deep
the posterior fascia of the lateral ligament of the pelvis uterine vein or the middle vesical artery/vein. Further,
(Figures 2 and 3). The exposed vessels within the plate, in this complex proved to be in either a frontal or perpen-
descending order, were from the ventral to the dorsal dicular relationship, and not parallel to the sagittal
aspect, the lateral umbilical artery/ligament, superior plane of each pelvic organ (Figures 2 and 3).
vesical artery, uterine artery, deep uterine vein, middle
vesical vessels, and middle rectal vessels (Figure 2). Two pelvic floors
A septum was developed between the cranial and
caudal chambers of the pararectal space. This septum Traditional anatomic understanding of the pelvic
was a continuation of the transverse cervical ligament, floor3,23,24 is conceived as that of the pubic part of the
Yabuki et al 11

Figure 5 Paravaginal space and cranial chamber of the Figure 6 Separation of the caudal reflection of the lateral
pararectal space: findings of the right pelvic cavity. The ligament of the pelvis: right pelvic cavity seen from the pubic
paravaginal space formed between the uterine cervix and aspect. Entrance into the paravaginal space and caudal cham-
ureter and its continuing caudal chambers of the pararectal ber of the pararectal space (Figure 4) is made by inserting
space are developed. An asterisk indicates the peripheral scissors between the uterine cervix and ureter. The tip of the
branch of the pelvic nerve plexus. The cranial space is the scissors pierces the tendinous arc of the pelvic fascia, protrud-
cranial chamber of the pararectal space, developed by entering ing into the paravesical space. The superior aspect of the
Okabayashi’s space. The fascia of the transverse cervical caudal reflection is the deep layer of the vesicouterine ligament,
ligament has already been reflected in a cranio-caudal direc- and the inferior aspect being the bundle that covers the
tion, with the photograph showing the parametrium lacking paracolpium. In addition, with excavation of the paravesical
visceral fascia. OS-Cr, Okabayashi’s space and cranial cham- and pararectal spaces, we can conjecture that there is a change
ber of the pararectal space; VS-Ca, paravaginal space and in direction of the lateral ligament of the pelvis from
caudal chamber of the pararectal space; PM, parametrium; Ur, ventrocranial-to-dorsocaudal to lateral-to-medial during ob-
ureter; U, uterus; B, bladder; AV, superficial layer of the servation of the hypogastric and pelvic visceral nerves. CaR,
vesicouterine ligament; UA, uterine artery; LS, Latzko’s space; Caudal reflection of the lateral ligament of the pelvis; UA,
SP, sacral promontory; AN, pelvic autonomic nerve. uterine artery; DV, deep uterine vein; U, uterus; Ur, ureter;
HN, hypogastric nerves; SN, pelvic splanchnic nerve; SB, short
fibrous bundle; R, rectum; B, bladder.
pelvic diaphragm or the pubococcygeus through which
the vagina pierces the genital hiatus (Figure 1). But the
pelvic floor5-9,11,12 in contemporary pelvic surgery is
following separation of the posterior fascia of the
found to be the iliac part of the pelvic diaphragm
transverse cervical ligament and the internal iliac vessel
or the iliococcygeus and the fascia of the piriformis
sheath from the main body.6,7 This space for the
muscle to which the lateral ligament of the pelvis attaches
development of the origin of the cardinal ligament was
(Figure 3).
so named Latzko’s space (Figures 2 and 3).16
Surgically developed cavities and the There were also 2 routes by which to develop the
connective tissue bundle caudal chamber of the pararectal space. One was the
route invented by Latzko, through which we entered via
Within the pelvic cavity there exist the paravesical and the paravesical space (Figures 1 and 3).6,7,16 The other
pararectal spaces as physiologic or potential spaces. The was the route by which we entered the space following
paravesical space takes part in micturition and forms the separation of the uterine cervix and the ureter (Figures
parturient canal, and the pararectal space aides in 5–7).8,9,16 This space was named Okabayashi’s para-
performance of defecation. We developed these 2 spaces vaginal space.16
in our radical hysterectomy, and severed the connective As a result, the connective tissue bundle that emerged
tissue bundle that emerged between these spaces. between the paravesical space and Latzko’s space was
There were found to be 2 routes to enable excavation found to be a fasciovascular complex that lacked pos-
of the cranial chamber of the pararectal space. One terior fascia, as shown in Figure 2, and we called it the
route was constructed by separation of the visceral cardinal ligament. The connective tissue bundle that
pelvic fascia that lines the broad ligament from the emerges between Okabayashi’s and Latzko’s spaces is
serous membrane (Figures 2, 4, and 5).8,9 We named this the so-called mesoureter (or Ureterblatt or ureteral
space Okabayashi’s space, created for the development leaf25) (Figures 4 and 7). This mesoureter is the one in
of the visceral attachment of the cardinal ligament which 2 visceral pelvic fasciae are fused, and between
(Figure 4).16 The other route was by entering a space which the ureter, hypogastric nerve, and ureteral branch
12 Yabuki et al

Figure 8 Fascial capsule of the uterus and uterine vessels: the


frontal section seen through the uterine cervix and the anterior
margin of the uterine body. A group of small arrowheads show
merging of the fascial capsule of the uterus covering the uterine
artery/vein (AB, VB) into the fascial capsule of the rectum via
the sacrouterine ligament (SU). Also observed are the middle
rectal vessels that pierce the pelvic nerve plexus passing within
the paraproctum (MR). The surrounding tissue that covers the
visceral fascia is probably the longitudinal section of the
supporting system. AB, Branches of uterine artery; VB,
branches of uterine vein; SU, sacrouterine ligament; MR,
middle rectal vessels; NP, pelvic nerve plexus; Ur, ureter; UB,
Figure 7 Schematic illustration of the pelvic connective uterine body; UC, uterine cervix; R, rectum.
tissue. The pelvic connective tissue is classified into a muscu-
lofascial bundle, or the suspensory system (X) and a fascio-
vascular bundle or the supporting system (Y). The supporting and connected the fascial capsules of the pelvic viscera in
system is further divided into a cranially reflected bundle (Y-1)
a chain-like fashion from the pubis to the sacrum/
and a caudally reflected bundle (Y-2). The ureter and pelvic
autonomic nerves pass within this suspensory system. U,
coccyx. It consisted of the pubovesical ligament, super-
Uterus; B, bladder; R, rectum; Ur, ureter; SN, pelvic splanch- ficial layer of the vesicouterine ligament, rectouterine
nic nerve; HN, hypogastric nerve; VN, vesical nerve branch; or sacrouterine ligament, and rectococcygeal ligament,
SB, short fibrous bundle; LS, Latzko’s space; BS, paravesical which suspended and anchored the pelvic organs to the
space; VF, vesicouterine space; RF, rectouterine space; X, pubis, sacrum/coccyx (Figure 8).
pubovesical ligament, superficial layer of the vesicouterine The supporting system was found to be a more specif-
ligament, rectouterine ligament, and rectococcygeal ligament; ically conceptualized entity of the lateral ligament of the
Y-1, mesoureter, etc; Y-2, deep layer of the vesicouterine pelvis. That is, the supporting system was a neurovascular
ligament, etc. fascial complex consisting of the vesicohypogastric fascia,
transverse cervical ligament, and lateral ligament of the
pelvis (Figures 1 and 2). This supporting system crossed in
of the internal iliac vessels pass (Figure 4). The connec- front, or on the lateral aspect, of the ureter and pelvic
tive tissue bundle that emerges between the paravesical nerve plexus and, consequently, divided into 3, namely,
space and Okabayashi’s paravaginal space is the deep the core, cranial reflection, and caudal reflection. The core
layer of the vesicouterine ligament advocated by Oka- was found to be a stalk consisting of blood vessels, lymph
bayashi (Figures 3, 6, and 7).8,9,20 This deep layer of the vessels, and nerves, and with no termed fascia. This
vesicouterine ligament was found to be a neurovascular areolar tissue pierced through the proper fascia and
bundle that connected the bladder and the lateral fanned out underneath it.
ligament of the pelvis.14,15 The cranial reflection was found to be the mesoureter,
or posterior fascia, of the supporting system reflected in
The structure of the pelvic connective tissue a cranial direction accompanied with a small part of the
areolar tissue. The caudal reflection was found to be a
The pelvic connective tissue was classified into 2, the neurovascular bundle that included the deep layer of the
suspensory system and the supporting system (Figure vesicouterine ligament, or the anterior fascia, of the
7).16 The suspensory system was found to be a group of supporting system that reflected in a caudal direction
true ligaments that had a musculofascial consistency, accompanied with a small part of the areolar tissue.
Yabuki et al 13

Table Dease pelvic connective tissue of Peham and Amreich


Horizontal ground bundle Frontal ground bundle
Mackenrodt ligament Bladder septum Ascending bladder septum Sagittal bladder septum
Vaginal-cervical septum Vaginal septum Cervical septum
Rectal septum Descending rectal septum Sagittal rectal septum

These tissues enveloped the suspensory system, thereby Mackenrodt ligament into the horizontal and frontal
pulling and anchoring the pelvic organs en masse. ground bundles, whereas our concept has nothing akin
to the horizontal ground bundle. In addition, our
Pelvic autonomic nerves structure is stacked from the top to bottom, while their
The pelvic nerve plexus positioned itself a little dorsal or septa lay parallel to each other.
deeper to the deep uterine vein, with the middle rectal However, our concept has many common denomi-
vessels piercing almost its center (Figures 3 and 8). The nators with other theories. The sketches drawn by
hypogastric nerve, pelvic splanchnic nerves, pelvic nerve Rieffenstuhl25,29 and us are, in appearance, very similar.
plexus, and vesical nerve branch created a potential Our caudal reflection corresponded conceptually with
plane along the reflected parts of the supporting system, Okabayashi’s deep layer of the vesicouterine ligament,
which, in turn, crossed the potential plane formed by the together with the ascending bladder septum of Peham
vessels of the stem (Figures 2 and 3). As for the passage and Amreich,6,7 and the inferior hypogastric wing of
of the vesical nerve, please refer to Yabuki et al.14 Uhlenhuth.21 Further, the cranial reflection was found
to resemble both the mesoureter25 and sagittal rectal
septum.6,7 In addition, the neurovascular stalk of
Comment Pernkopf substantiated our concept of the supporting
system. We can state confidently that our results clar-
Gray’s anatomy defines Mackenrodt ligament as ‘‘the ified the relationship between the pathway of both the
fascia over the ventral and dorsal walls of the vagina and pelvic autonomic nerves and ureter and the ligaments,
cervix come together at the lateral border of these organs, and enabled the preservation of the vesical nerve branch
and the resulting sheet extends across the pelvic floor as a by selective dissection of the vesicouterine ligament.14-16
deeper continuation of the broad ligament.’’24 Peham and In many past studies the existence of the cardinal
Amreich,6 having analyzed the relationship between the ligament has come into question.26-28 Our answer to this
adjacent organs and connective tissue bands, classified the question is that this is caused by the lack of visceral
Mackenrodt ligament into bladder, vaginal-cervical, and terminal fascia. Further, we easily lose sight, during
rectal septa (Table). These 2 concepts show that the surgical maneuver, of the posterior fascia of the cardinal
vesicohypogastric fascia, transverse cervical ligament, ligament, which is an extension of the internal iliac
and lateral ligament of the rectum are independent vessel’s sheath, as shown in Latzko’s space.
bundles that are parallel to the longitudinal axis of each In recent years an increase in research and reports on
corresponding organ, and do not cross each other. How- surgery concerning nerve-sparing radical hysterectomy
ever, this theory cannot explain contemporary surgical has been evident.30-33 Our surgical technique,32 and that
dissection of the cardinal ligament, in which the bottom of of others,30,31,33 aim to preserve the parasympathetic
the Mackenrodt ligament is separated from the coccygeus nerve by dividing the cardinal ligament into vascular and
and piriformis fasciae. neural portions. However, their articles are saturated with
In order to answer this question we proposed that the classic clinical anatomy. It is anatomically contradictory
vesicohypogastric fascia, transverse cervical ligament, to divide the continuation consisting of the transverse
and lateral ligament of the rectum form 1 plate. How- cervical ligament of Mackenrodt and the paracolpium
ever, this proposition alone was insufficient to fully into vascular and neural portions, which cannot explain
explain contemporary radical hysterectomy. Accord- the exact pathway of the parasympathetic nerves. We do
ingly, we meticulously carried out and investigated not deny the existence of the accessory nerve of McCrea,34
Okabayashi and Latzko’s surgery, and conceived a but it is likely that most of the parasympathetic nerves
structure of a plate that becomes divided into 3 at its may be distributed to the bladder via the pelvic nerve
periphery. Our hypothesis is not a duplicate of Peham plexus. Particularly, effort on our part has been made to
and Amreich’s, but rather reference to the hypogastric establish a surgical procedure to preserve the pelvic nerve
wing of Uhlenhuth,21 and the neurovascular stalk of plexus and its vesical branch.13-16
Pernkopf.19,20 The difference between Peham/Amreich/ If the authors were to describe the Mackenrodt liga-
Reiffenstuhl’s (who belonged to the Amreich school)25,29 ment and the present-day cardinal ligament in one
and our concepts is that they classified the 3 septa of the phrase, we would say that: the lateral parametrium, or
14 Yabuki et al

Mackenrodt ligament, of the 19th century is a conception and Pharmaceutical University, and Dr Yoshiaki
observed from the paravesical space (Figure 1), whereas Nojoh, Professor and Chair of the Department of
the lateral parametrium of the 20th century, or the Anatomy, Fukui Medical University School of Medi-
present-day cardinal ligament, is a conception primarily cine for providing us with the opportunity to dissect
observed from ‘the so-called pararectal space (Figure 2).’ cadavers. The authors also wish to acknowledge Dr
In other words, the former is a continuation consisting of Shimpachiro Ogiwara, Professor of Physical Therapy,
the transverse cervical ligament and the short fibrous University of Kanazawa, and Mrs Sandra M. Ogiwara
bundle, and the latter a complex consisting of the in preparing this manuscript.
transverse cervical ligament and the lateral ligament of
the rectum. To be precise, both of these have to be
distinguished, and even Peham and Amreich in their References
surgical textbook apply to the former structure in regards
to anatomy and the latter for surgery.6 The description of 1. Savage H. The surgery, surgical pathology and surgical anatomy
of the female pelvic organs. London: J Churchill & Sons; 1870.
the cardinal ligament (of Mackenrodt) by Reiffenstuhl29 2. Kocks J. Die normale und pathologische lage und gestalt des
and Gray’s anatomy24 add to this confusion. uterus sowie deren mechanik. Bonn: Max Cohen & Sohn; 1886.
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