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NERVESPARING SURGERY IN CERVICAL
CARCINOMA
51
Shingo Fujii, MD
Kentaro Sekiyama, MD
Introduction
Radical hysterectomy was introduced in 1911 by
Wertheim (1), and now there are many different types
of radical hysterectomy in all over the world (2, 3).
Interestingly, almost all types of radical hysterectomy
were often associated with severe bladder dysfunction
and colorectal motility disorders that deteriorated the
patient’s quality of life. The cause exists in the surgical
processes of radical hysterectomy for the removal of the
longer vaginal cuff. The nerves to the urinary bladder
and the rectum in the paracervix area have a possibility
to be damaged during radical hysterectomy.
Anatomy of the Pelvic Nerve and Nerve-Sparing
Surgery
(1). Nerve supply to the uterus, rectum and urinary
bladder (4) (Figure 1)
The uterus, vagina, urinary bladder and rectum are
innervated by a motor and sensory autonomic nerve
supply (sympathetic and parasympathetic origin).
The sympathetic fibers coming from T10-L2 form the
inferior hypogastric nerve. The parasympathetic fibers
coming from S2, 3 and 4 at the pelvic wall form the pelvic
splanchnic nerve. These fibers merge and construct
the inferior hypogastric plexus that has branches to the
uterus, the rectum and the urinary bladder.
Figure 1. Nerve supply to the uterus, rectum and urinary bladder
and cross-shaped inferior hypogastric plexus.
Figure 2. Locations of surgical damages to the pelvic nerves during Okabayashi‘s radical hysterectomy and Wertheim’s radical
hysterectomy.
(2). Locations of nerve damages during radical
hysterectomy (4) (Figure 2)
During radical hysterectomy, surgical procedures to the
uterosacral ligament and the rectovaginal ligament can
scarify the hypogastric nerve. Surgery to the deep uterine
vein in the cardinal ligament can scarify the pelvic
splanchnic nerve. All surgical steps shown in the Figure 2
can scarify the pelvic nerves during Okabayashi’s radical
hysterectomy (2). In contrast, Wertheim’s method usually
does not divide the deep uterine vein in the cardinal
ligament, it is difficult to injure the pelvic splanchnic
nerve. However, Wertheim’s method (1) tries to remove
the uterosacral ligament as much as possible, and can
scarify the hypogastric nerve during the division of
the uterosacral ligament. Instead to divide the cardinal
ligament, by the division of the parametrial tissues and
rectovaginal ligament, Wertheim’s method can scarify
the inferior hypogastric plexus itself. Moreover, by the
division of the paracervical tissues that contains vaginal
blood vessels (paracolpium) and the posterior leaf of the
vesicouterine ligament, Wertheim’s method can scarify
the bladder branch from the inferior hypogastric plexus.
(3). Efforts on nerve-sparing radical hysterectomy
Kobayashi modified Okabayashi’s method in an attempt
to preserve nerve functions during radical hysterectomy.
In 1961, Kobayashi described the technique that result
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Nerve-Sparing Surgery in Cervical Carcinoma
in improved postoperative bladder function preserving
the pelvic splanchnic nerve by the separation of the
vascular part (containing the deep uterine vein) from
the lower hard bundle (containing the pelvic splanchnic
nerve) during the division of the cardinal ligament (5).
In 1983, Fujiwara (6) at Kitano Hospital described the
importance of the preservation of the bladder branch as
well as the hypogastric nerve with the pelvic splanchnic
nerve by the division of only uterine branch from the
inferior hypogastric plexus. Since then, many surgeons
have adopted the nerve-sparing radical hysterectomy
(7). Nevertheless, almost all published papers on nervesparing radical hysterectomy could not clearly show a
surgical anatomy of the inferior hypogastric plexus with
bladder branch and uterine branch. Publications using
Wertheim or Piver type III (8) surgery show mainly the
process of isolation of the inferior hypogastric nerve;
however, they usually lack a clear description of the
isolation of the pelvic splanchnic nerve and the bladder
branch from the inferior hypogastric plexus. The reason
is that Wertheim or Piver type III surgeries usually
neither reveal nor isolate the deep uterine vein beneath
where the pelvic splanchnic nerve is residing. Moreover,
although these surgeries divide the anterior leaf of
the vesicouterine ligament, the concept of separation
and division of the posterior leaf of the vesicouterine
ligament, beneath where the bladder branch is residing,
is lacking. In contrast, Japanese doctors usually perform
Okabayashi’s radical hysterectomy. Okabayashi’s radical
hysterectomy separates and divides the posterior leaf of
the vesicouterine ligament. Therefore, the publications
from Japan had been showing both inferior hypogastric
nerve and pelvic splanchnic nerve, and more information
on the inferior hypogastric plexus (9). In 2007, Fujii et
al. (10) published a clear surgical anatomy of the crossshaped inferior hypogastric plexus (Figure 1) and showed
how to divide only the uterine branch from the plexus. If
only the uterine branch is divided, the urinary bladder
function is perfect after the surgery. This publication
stimulated many doctors and nerve-sparing radical
hysterectomy became popular.
Figure 3. Principle of nerve-sparing radical hysterectomy is the
division of only the uterine branch from the inferior hypogastric
plexus. The cross-shaped inferior hypogastric plexus changes
into the T-shaped inferior hypogastric plexus by the division of
only the uterine branch.
T-shaped inferior hypogastric plexus is the goal of this
surgery, with the outcome of the satisfactory urinary
function for patients (4, 10).
(6). Indication of nerve-sparing radical hysterectomy
The nerve-sparing radical hysterectomy separates and
preserves medially one tissue’s layer (containing pelvic
nerve plane) more than the classical radical hysterectomy
(4) (Figure 4). Nerve-sparing radical hysterectomy is
recommended for patients with FIGO Ib stage disease.
However, during the nerve-sparing radical hysterectomy
for patients with FIGO Ib2 stage, if invasion is strongly
suggested in the area of the inferior hypogastric plexus,
the surgery should abandon the preservation of the nerve.
Indication of nerve-sparing radical hysterectomy is not
recommended to the patients with FIGO IIb stage disease,
because the location of the inferior hypogastric plexus is
usually very close to the invasive foci of IIb lesion. In this
case, some doctors recommend the nerve-sparing radical
hysterectomy to the side that is not invaded by cervical
cancer (7). However, it is very important to confirm
the extension of the cancer lesion very carefully. In case
of younger aged patients with invasive lesion in the
cardinal ligament of either side, total extirpation of the
(4). Principle of nerve-sparing radical hysterectomy
(Figure 3)
The principle of nerve-sparing radical hysterectomy is
very simple. Identify the inferior hypogastric nerve, and
confirm the cross-shaped inferior hypogastric plexus, the
branches to the uterus (uterine branch) and the urinary
bladder (bladder branch). Only the uterine branch is
isolated and should be divided (4).
(5). A destination of anatomy for nerve-sparing
radical hysterectomy (Figure 3)
The division of the uterine branch changes the crossshaped inferior hypogastric plexus into the T-shaped one
composed of hypogastric nerve, the pelvic splanchnic
nerve and the bladder branch. The preservation of
Figure 4. Cutting line of the Okabayashi’s radical hysterectomy
and that of nerve-sparing radical hysterectomy are illustrated as
a cross section view on the level of cervix.
Nerve-Sparing Surgery in Cervical Carcinoma
cardinal ligament with internal iliac blood vessel system
(super-radical hysterectomy (11)), (lateral extended
parametrectomy (LEP) (12) ) is a radical approach for
the patient. However, if the other side is intact, unilateral
nerve-sparing radical hysterectomy is a surgical choice.
Preservation of T-shaped nerve plane in either side of
the rectum results in satisfactory urinary function for the
patient.
It is necessary to perform a randomized study
comparing the effectiveness, complications, and
oncologic outcomes of classical radical hysterectomy with
nerve-sparing radical hysterectomy. However, in order to
perform a randomized study, the uniform surgical steps
are required for reproducible results and to compare the
data between the studies (4)
Operative Procedure
The anatomy of the inferior hypogastric plexus
encompassing the hypogastric nerve, the pelvic
splanchnic nerve and the bladder branch/the uterine
branch from this plexus is complicated and is not easy to
appreciate during the surgery of radical hysterectomy. In
order to detect the structure of the inferior hypogastric
plexus, it is essential to have the knowledge of the
anatomy of the cardinal ligament (deep uterine vein) to
preserve the pelvic splanchnic nerve (5, 10). Moreover,
the anatomy of the vesicouterine ligament, particularly
the posterior leaf of the vesicouterine ligament (13) is
very important. As well as it is necessary to have surgical
skill to separate carefully these tissues in order to reveal
the structure of the inferior hypogastric plexus. The
surgical steps for nerve-sparing radical hysterectomy
after the pelvic lymphadenectomy are described in this
chapter.
1: Treatment of The Cardinal Ligament
After the pelvic lymphadenectomy, the paravesical
space and pararectal space are well developed. The thick
connective tissue bundle between the paravesical and
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the pararectal spaces is the cardinal ligament (Figure
5A). The cardinal ligament usually contains vascular
structures and nerve structure that are running laterally
between the internal iliac blood vessels of the pelvic
side wall and the uterine/upper-vaginal side wall. In
the cardinal ligament, from the ventral to the dorsalside, the uterine artery, the superficial uterine vein, the
deep uterine vein and the pelvic splanchnic nerve are
appreciated (Figure 5A shows the cardinal ligament
after the division of the uterine artery). The uterine
artery originated from the internal iliac artery and runs
into the side wall of the uterus is easily isolated, doubly
clamped and ligated. The uterine artery between the two
ligatures is divided (Figure 5A). Then, in the connective
tissue of the cardinal ligament the superficial uterine vein
running parallel to the uterine artery is appreciated. The
superficial uterine vein is isolated and doubly clamped
by Pean forceps. Then the superficial uterine vein is
divided between the two clamps. Each clamp is replaced
by ligature. In the remaining cardinal ligament, the deep
uterine vein is always appreciated.
2: Isolation and Separation of The Deep Uterine
Vein From The Pelvic Splanchnic Nerve
Careful separation of the connective tissue and lymph
nodes in the cardinal ligament between the side wall of
the uterus and the internal iliac blood vessels can reveal a
vein running from the uterine side wall to the internal iliac
vein. If we can confirm this anatomy, a vein is the deep
uterine vein. The connective tissue and adipose tissue
surrounding the deep uterine vein should be cleaned as
much as possible. Particularly, the dorsal side of the deep
uterine vein is very important for the isolation of the deep
uterine vein from the pelvic splanchnic nerve (Figure 5B).
After isolation, the deep uterine vein is doubly clamped by
Pean’s forceps. The deep uterine vein is divided between
the two clamps. Each clamp is replaced by ligature (Figure
6A). In the dorsal part of the deep uterine vein, a white
yellow bundle is running parallel to the deep uterine vein.
This is the pelvic splanchnic nerve (Figure 6B).
Figure 5. (A). Cardinal ligament between the paravesical space and paravesical space after division of the uterine artery (B). After isolation and division of the uterine artery and superficial uterine vein, in the cardinal ligament the deep uterine vein running from the sidewall of the uterus to the internal iliac vein is appreciated.
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Nerve-Sparing Surgery in Cervical Carcinoma
Figure 6. (A). Isolation and division of the deep uterine vein reveals the pelvic splanchnic nerve (B). Along the rectal side wall of the
pararectal space, the hypogastric nerve is appreciated, isolated, and a vessel tape is applied for a marker.
3: Isolation and Separation of The Hypogastric
Nerve (Figure 6B)
In the rectal side-wall of the pararectal space, 2 to 3 cm
dorsal portion from the ureter, a white bundle of the
hypogastric nerve running parallel with the rectum is
appreciated. This bundle should be searched on the same
connective tissue plane of the ureter. The hypogastric
nerve is scraped and separated from the rectal side-wall
(Figure 6B). A vessel tape is applied for a marker of the
isolated hypogastric nerve. Hypogastric nerve should be
separated as close as possible to the uterine-side of the
pelvic splanchnic nerve (Figure 6B).
4: Separation of The Connective Tissue Between
the Rectum and The Vagina
5: Division of The Uterosacral Ligament
6: Separation of the cut end of the deep uterine
vein from the pelvic splanchnic nerve
7: Separation of the urinary bladder and the
vesicouterine ligament
(1) Anatomy of The Vesicouterine Ligament (Figure 7A,B
and Figure 8A,B)
Since the ureter is running in the vesicouterine ligament,
it is essential to separate the connective tissue of the
vesicouterine ligament during radical hysterectomy.
At first, the ventral part of the ureter should be
unroofed. However, the detailed vascular anatomy of
the vesicouterine ligament was unclear for more than
100 years. Always there existed unexpected bleeding
that is usually difficult to control because the ureter is
running very close to these bleeding points. Without
confirmation of the figure of the ureter, tissue clamping
is also dangerous and a surgeon usually tries to avoid
making damage to the ureter. Therefore, hemostasis
often becomes insufficient. This results in a considerable
amount of blood loss. Therefore, the detailed anatomy
of blood vessel in the vesicouterine ligament is essential
for the doctors who would like to perform radical
hysterectomy. The Figure 7A is a transparent view of the
ureter and blood vessels in the vesicouterine ligament
drawn by Shingo Fujii (Figure 7A).
(2) Anatomy of The Anterior Leaf of The Vesicouterine
Ligament
Figure 7B is illustrating the blood vessels residing in
the anterior leaf of the vesicouterine ligament that are
Figure 7. (A). A transparent view of the ureter and blood vessels in the vesicouterine ligament (B). Blood vessels in the anterior leaf of
the vesicouterine ligament.
Nerve-Sparing Surgery in Cervical Carcinoma
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Figure 8. (A). A transparent view of the posterior leaf of the vesicouterine ligament after the separation and division of the blood vessels
in the anterior leaf of the vesicouterine ligament (B). A view of the blood vessels in the posterior leaf of the vesicouterine ligament after
the displacement of the ureter.
separated or divided; 1) uterine artery, 2) superficial
uterine vein, 3) ureter branch of the uterine artery, 4)
superior vesical vein that drains into the superficial
uterine vein, and 5) cervicovesical vessels (13). Separation
and division of the vessels in the anterior leaf of the
vesicouterine ligament reveals the ventral-surface of the
ureter (Figure 8A, B).
(3) Anatomy of The Posterior Leaf of The Vesicouterine
Ligament
The Figures 8A and B are illustrating the surface of the
posterior leaf of the vesicouterine ligament on where
the ureter is rolled laterally. The posterior leaf of the
vesicouterine ligament is the tissue residing dorsal-side
of the ureter with connection between the posterior wall
of the bladder and the lateral cervix/cranial vagina. The
detailed anatomy of each blood vessel in the vesicouterine
ligament is described as the transparent view (Figure
8A). In the posterior leaf of the vesicouterine ligament,
we usually appreciate two major vesical veins that start
from the urinary bladder and drain into the deep uterine
vein (13) (Figure 8B). Division of these veins reveals the
inferior hypogastric plexus.
(4) Division of Blood Vessels in The Posterior Leaf of The
Vesicouterine Ligament
Division of the middle vesical vein (Figure 9A).and
the inferior vesical vein (Figure 9B) reveal the inferior
hypogastric plexus. Wertheim’s method separates
the anterior leaf of the vesicouterine ligament, but
not intentionally separates the posterior leaf of the
vesicouterine ligament. In contrast, Okabayashi’s method
identifies the deep uterine vein and pelvic splanchnic
nerve in the cardinal ligament (5, 10) and intentionally
separates the posterior leaf of the vesicouterine
ligament (10, 13) that results in the identification of the
inferior hypogastric plexus beneath the posterior leaf
of the vesicouterine ligament. Therefore, if we would
like to perform nerve-sparing radical hysterectomy,
Okabayashi’s method is easier to identify the inferior
hypogastric plexus during the surgery.
8: Identification of the Inferior Hypogastric
Plexus and Isolation of The Bladder Branch and
The Uterine Branch
After removal of the fatty tissues residing between the
dorsal portion of the urinary bladder and the rectal
Figure 9. (A). A view of the posterior leaf of the vesicouterine ligament (B). Separation and division of the middle vesical vein in the
posterior leaf of the vesicouterine ligament.
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Nerve-Sparing Surgery in Cervical Carcinoma
Figure 10. (A). Separation and division of the inferior vesical vein reveals the bladder branch from the cross-shaped inferior hypogastric
plexus. The nerves composing the inferior hypogastric plexus is residing in the same connective tissue of the pelvic nerve plane (B).
Between the uterine branch and the upper-vagina above the level of the hypogastric nerve and bladder branch, Pean’s forceps is insinuated in order to isolate only the uterine branch in the pelvic nerve plane.
side wall, if we trace the pelvic splanchnic nerve toward
the uterus, we can appreciate the cross-shaped inferior
hypogastric plexus formed by the pelvic splanchnic
nerve, the hypogastric nerve, the uterine branch and
the bladder branch from the inferior hypogastric plexus.
These nerves reside in the same connective tissue plane
that we call the pelvic nerve plane (4) (Figure 10A).
On the same level of the hypogastric nerve, the
bladder branch from the inferior hypogastric plexus can
be separated from the blood vessels of the paracolpium.
Then Pean’s forceps is insinuated from the v-shaped
depression created between the bladder branch and the
blood vessels of the paracolpium into the connective
tissue between the pelvic nerve plane and the cervix/
upper vagina at the level a little bit ventral side of the
hypogastric nerve and a little bit dorsal side of the cut
end of the deep uterine vein (Figure 10B).
9: Division of The Uterine Branch From the
Inferior Hypogastric Plexus (Figure 11A) and
Division of The Uterosacral Ligament (Figure
11B)
The uterine side of the pelvic nerve plane including the
uterine branch from the inferior hypogastric plexus is
clamped, divided, and ligated. When we cut the uterine
branch of the pelvic nerves, there is a feeling resembling a
stretched string breaking with a snap (Figure 11A). After
the division of the uterine branch, the hypogastric nerve,
the pelvic splanchnic nerve and the bladder branch of
the inferior hypogastric plexus forms the T-shaped nerve
plane. The remaining uterosacral ligament residing
between the uterus and the rectum is divided (Figure
11B). Then, the connective tissue between the lower
uterus/vagina and the rectum is appreciated. This is the
rectovaginal ligament (Figure 11B).
Figure 11. (A). Illustrating the figure of the division of the only uterine branch and the remaining uterosacral ligament. The cross-shaped
inferior hypogastric plexus turned into the T-shaped one. (B). Division of the remaining the uterosacral ligament reveals the rectovaginal
ligament.
Nerve-Sparing Surgery in Cervical Carcinoma
461
Figure 12. (A). Separation and division of the rectovaginal ligament to obtain vaginal length deemed appropriate by the level of cervical disease, excluding the T-shaped inferior hypogastric plexus (B). Blood vessels of the paracolpium are ligated at the designated level
Figure 13. (A). Division of the paracolpium (B). Division of the paracolpium creates the situation that the uterus is only connected with
the vagina. After the confirmation of the length of the vaginal cuff, the vagina is incised and the uterus is amputated from the vagina.
10: Division of The Rectovaginal Ligament and
Ligation of The Paracolpium
By pushing the rectum up, the rectovaginal ligament rises
to the surface between the T-shaped inferior hypogastric
plexus and the rectum. Only the rectovaginal ligament is
divided using bipolar scissors toward the upper vagina
excluding the T-shaped nerve plane. By the division of
the rectovaginal ligament close to the upper vagina, the
bladder branch from the inferior hypogastric plexus
forming T-shaped nerve plane is gradually separated
from the blood vessels of the paracolpium (Figure
12A). The separation and division of the rectovaginal
ligament is extended caudally to obtain vaginal length
deemed appropriate by the level of cervical disease. At
the designated level, the blood vessels of the paracolpium
are ligated (Figure 12B). Now, the T-shaped nerve plane
formed by the hypogastric nerve, the pelvic splanchnic
nerve and the bladder branch of the inferior hypogastric
nerve is completely preserved.
11: Extirpation of The Uterus
By the division of the paracolpium, the uterus is only
connected with the vagina. After the same procedure
on the opposite side, the length of the vaginal cuff is
confirmed. Then the uterus is amputated from the vagina
(Figure 13 A, B).
Conclusion
If the surgeon can perform separation of the posterior
leaf of the vesicouterine ligament, and could trace
the cross-shaped inferior hypogastric plexus, we can
successfully divide only the uterine branch from
the inferior hypogastric plexus. By these operative
procedures, the T-shaped inferior hypogastric plexus,
is able to be preserved and we can archive the urinary
functions of complete voiding, a sense of fullness and a
sense of micturition.
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