NERVESPARING SURGERY IN CERVICAL

CARCINOMA
Shingo Fujii, MD
51
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 Figure 2. Locations of surgical damages to the pelvic nerves dur-
and the rectum in the paracervix area have a possibility ing Okabayashi‘s radical hysterectomy and Wertheim’s radical
to be damaged during radical hysterectomy. hysterectomy.

Anatomy of the Pelvic Nerve and Nerve-Sparing

Surgery (2). Locations of nerve damages during radical
(1). Nerve supply to the uterus, rectum and urinary hysterectomy (4) (Figure 2)
bladder (4) (Figure 1) During radical hysterectomy, surgical procedures to the
The uterus, vagina, urinary bladder and rectum are uterosacral ligament and the rectovaginal ligament can
innervated by a motor and sensory autonomic nerve scarify the hypogastric nerve. Surgery to the deep uterine
supply (sympathetic and parasympathetic origin). vein in the cardinal ligament can scarify the pelvic
The sympathetic fibers coming from T10-L2 form the splanchnic nerve. All surgical steps shown in the Figure 2
inferior hypogastric nerve. The parasympathetic fibers can scarify the pelvic nerves during Okabayashi’s radical
coming from S2, 3 and 4 at the pelvic wall form the pelvic hysterectomy (2). In contrast, Wertheim’s method usually
splanchnic nerve. These fibers merge and construct does not divide the deep uterine vein in the cardinal
the inferior hypogastric plexus that has branches to the ligament, it is difficult to injure the pelvic splanchnic
uterus, the rectum and the urinary bladder. 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
Figure 1. Nerve supply to the uterus, rectum and urinary bladder to preserve nerve functions during radical hysterectomy.
and cross-shaped inferior hypogastric plexus. In 1961, Kobayashi described the technique that result
455
 456 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 nerve- Figure 3. Principle of nerve-sparing radical hysterectomy is the
division of only the uterine branch from the inferior hypogastric
sparing radical hysterectomy could not clearly show a plexus. The cross-shaped inferior hypogastric plexus changes
surgical anatomy of the inferior hypogastric plexus with into the T-shaped inferior hypogastric plexus by the division of
bladder branch and uterine branch. Publications using only the uterine branch.
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 T-shaped inferior hypogastric plexus is the goal of this
isolation of the pelvic splanchnic nerve and the bladder surgery, with the outcome of the satisfactory urinary
branch from the inferior hypogastric plexus. The reason function for patients (4, 10).
is that Wertheim or Piver type III surgeries usually (6). Indication of nerve-sparing radical hysterectomy
neither reveal nor isolate the deep uterine vein beneath The nerve-sparing radical hysterectomy separates and
where the pelvic splanchnic nerve is residing. Moreover, preserves medially one tissue’s layer (containing pelvic
although these surgeries divide the anterior leaf of nerve plane) more than the classical radical hysterectomy
the vesicouterine ligament, the concept of separation (4) (Figure 4). Nerve-sparing radical hysterectomy is
and division of the posterior leaf of the vesicouterine recommended for patients with FIGO Ib stage disease.
ligament, beneath where the bladder branch is residing, However, during the nerve-sparing radical hysterectomy
is lacking. In contrast, Japanese doctors usually perform for patients with FIGO Ib2 stage, if invasion is strongly
Okabayashi’s radical hysterectomy. Okabayashi’s radical suggested in the area of the inferior hypogastric plexus,
hysterectomy separates and divides the posterior leaf of the surgery should abandon the preservation of the nerve.
the vesicouterine ligament. Therefore, the publications Indication of nerve-sparing radical hysterectomy is not
from Japan had been showing both inferior hypogastric recommended to the patients with FIGO IIb stage disease,
nerve and pelvic splanchnic nerve, and more information because the location of the inferior hypogastric plexus is
on the inferior hypogastric plexus (9). In 2007, Fujii et usually very close to the invasive foci of IIb lesion. In this
al. (10) published a clear surgical anatomy of the cross- case, some doctors recommend the nerve-sparing radical
shaped inferior hypogastric plexus (Figure 1) and showed
hysterectomy to the side that is not invaded by cervical
how to divide only the uterine branch from the plexus. If
cancer (7). However, it is very important to confirm
only the uterine branch is divided, the urinary bladder
the extension of the cancer lesion very carefully. In case
function is perfect after the surgery. This publication
of younger aged patients with invasive lesion in the
stimulated many doctors and nerve-sparing radical
cardinal ligament of either side, total extirpation of the
hysterectomy became popular.
(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 cross-
shaped inferior hypogastric plexus into the T-shaped one Figure 4. Cutting line of the Okabayashi’s radical hysterectomy
composed of hypogastric nerve, the pelvic splanchnic and that of nerve-sparing radical hysterectomy are illustrated as
nerve and the bladder branch. The preservation of a cross section view on the level of cervix.
 Nerve-Sparing Surgery in Cervical Carcinoma 457

cardinal ligament with internal iliac blood vessel system the pararectal spaces is the cardinal ligament (Figure
(super-radical hysterectomy (11)), (lateral extended 5A). The cardinal ligament usually contains vascular
parametrectomy (LEP) (12) ) is a radical approach for structures and nerve structure that are running laterally
the patient. However, if the other side is intact, unilateral between the internal iliac blood vessels of the pelvic
nerve-sparing radical hysterectomy is a surgical choice. side wall and the uterine/upper-vaginal side wall. In
Preservation of T-shaped nerve plane in either side of the cardinal ligament, from the ventral to the dorsal-
the rectum results in satisfactory urinary function for the side, the uterine artery, the superficial uterine vein, the
patient. deep uterine vein and the pelvic splanchnic nerve are
It is necessary to perform a randomized study appreciated (Figure 5A shows the cardinal ligament
comparing the effectiveness, complications, and after the division of the uterine artery). The uterine
oncologic outcomes of classical radical hysterectomy with artery originated from the internal iliac artery and runs
nerve-sparing radical hysterectomy. However, in order to into the side wall of the uterus is easily isolated, doubly
perform a randomized study, the uniform surgical steps clamped and ligated. The uterine artery between the two
are required for reproducible results and to compare the ligatures is divided (Figure 5A). Then, in the connective
data between the studies (4) 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
Operative Procedure by Pean forceps. Then the superficial uterine vein is
The anatomy of the inferior hypogastric plexus divided between the two clamps. Each clamp is replaced
encompassing the hypogastric nerve, the pelvic by ligature. In the remaining cardinal ligament, the deep
splanchnic nerve and the bladder branch/the uterine uterine vein is always appreciated.
branch from this plexus is complicated and is not easy to
appreciate during the surgery of radical hysterectomy. In 2: Isolation and Separation of The Deep Uterine
order to detect the structure of the inferior hypogastric Vein From The Pelvic Splanchnic Nerve
plexus, it is essential to have the knowledge of the Careful separation of the connective tissue and lymph
anatomy of the cardinal ligament (deep uterine vein) to nodes in the cardinal ligament between the side wall of
preserve the pelvic splanchnic nerve (5, 10). Moreover, the uterus and the internal iliac blood vessels can reveal a
the anatomy of the vesicouterine ligament, particularly vein running from the uterine side wall to the internal iliac
the posterior leaf of the vesicouterine ligament (13) is vein. If we can confirm this anatomy, a vein is the deep
very important. As well as it is necessary to have surgical uterine vein. The connective tissue and adipose tissue
skill to separate carefully these tissues in order to reveal surrounding the deep uterine vein should be cleaned as
the structure of the inferior hypogastric plexus. The much as possible. Particularly, the dorsal side of the deep
surgical steps for nerve-sparing radical hysterectomy uterine vein is very important for the isolation of the deep
after the pelvic lymphadenectomy are described in this uterine vein from the pelvic splanchnic nerve (Figure 5B).
chapter. After isolation, the deep uterine vein is doubly clamped by
Pean’s forceps. The deep uterine vein is divided between
1: Treatment of The Cardinal Ligament the two clamps. Each clamp is replaced by ligature (Figure
After the pelvic lymphadenectomy, the paravesical 6A). In the dorsal part of the deep uterine vein, a white
space and pararectal space are well developed. The thick yellow bundle is running parallel to the deep uterine vein.
connective tissue bundle between the paravesical and 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 isola-
tion and division of the uterine artery and superficial uterine vein, in the cardinal ligament the deep uterine vein running from the side-
wall of the uterus to the internal iliac vein is appreciated.
 458 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 (1) Anatomy of The Vesicouterine Ligament (Figure 7A,B
Nerve (Figure 6B) and Figure 8A,B)
Since the ureter is running in the vesicouterine ligament,
In the rectal side-wall of the pararectal space, 2 to 3 cm it is essential to separate the connective tissue of the
dorsal portion from the ureter, a white bundle of the vesicouterine ligament during radical hysterectomy.
hypogastric nerve running parallel with the rectum is At first, the ventral part of the ureter should be
appreciated. This bundle should be searched on the same unroofed. However, the detailed vascular anatomy of
connective tissue plane of the ureter. The hypogastric the vesicouterine ligament was unclear for more than
nerve is scraped and separated from the rectal side-wall 100 years. Always there existed unexpected bleeding
that is usually difficult to control because the ureter is
(Figure 6B). A vessel tape is applied for a marker of the
running very close to these bleeding points. Without
isolated hypogastric nerve. Hypogastric nerve should be confirmation of the figure of the ureter, tissue clamping
separated as close as possible to the uterine-side of the is also dangerous and a surgeon usually tries to avoid
pelvic splanchnic nerve (Figure 6B). making damage to the ureter. Therefore, hemostasis
often becomes insufficient. This results in a considerable
4: Separation of The Connective Tissue Between amount of blood loss. Therefore, the detailed anatomy
the Rectum and The Vagina of blood vessel in the vesicouterine ligament is essential
for the doctors who would like to perform radical
5: Division of The Uterosacral Ligament hysterectomy. The Figure 7A is a transparent view of the
ureter and blood vessels in the vesicouterine ligament
6: Separation of the cut end of the deep uterine drawn by Shingo Fujii (Figure 7A).
vein from the pelvic splanchnic nerve (2) Anatomy of The Anterior Leaf of The Vesicouterine
Ligament
7: Separation of the urinary bladder and the Figure 7B is illustrating the blood vessels residing in
vesicouterine ligament 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 459

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 (4) Division of Blood Vessels in The Posterior Leaf of The
uterine vein, 3) ureter branch of the uterine artery, 4) Vesicouterine Ligament
superior vesical vein that drains into the superficial Division of the middle vesical vein (Figure 9A).and
uterine vein, and 5) cervicovesical vessels (13). Separation the inferior vesical vein (Figure 9B) reveal the inferior
and division of the vessels in the anterior leaf of the hypogastric plexus. Wertheim’s method separates
vesicouterine ligament reveals the ventral-surface of the the anterior leaf of the vesicouterine ligament, but
ureter (Figure 8A, B). not intentionally separates the posterior leaf of the
vesicouterine ligament. In contrast, Okabayashi’s method
(3) Anatomy of The Posterior Leaf of The Vesicouterine identifies the deep uterine vein and pelvic splanchnic
Ligament
nerve in the cardinal ligament (5, 10) and intentionally
The Figures 8A and B are illustrating the surface of the
separates the posterior leaf of the vesicouterine
posterior leaf of the vesicouterine ligament on where ligament (10, 13) that results in the identification of the
the ureter is rolled laterally. The posterior leaf of the inferior hypogastric plexus beneath the posterior leaf
vesicouterine ligament is the tissue residing dorsal-side of the vesicouterine ligament. Therefore, if we would
of the ureter with connection between the posterior wall like to perform nerve-sparing radical hysterectomy,
of the bladder and the lateral cervix/cranial vagina. The Okabayashi’s method is easier to identify the inferior
detailed anatomy of each blood vessel in the vesicouterine hypogastric plexus during the surgery.
ligament is described as the transparent view (Figure
8A). In the posterior leaf of the vesicouterine ligament, 8: Identification of the Inferior Hypogastric
we usually appreciate two major vesical veins that start Plexus and Isolation of The Bladder Branch and
from the urinary bladder and drain into the deep uterine The Uterine Branch
vein (13) (Figure 8B). Division of these veins reveals the After removal of the fatty tissues residing between the
inferior hypogastric plexus. 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.
 460 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 insinu-
ated in order to isolate only the uterine branch in the pelvic nerve plane.

side wall, if we trace the pelvic splanchnic nerve toward 9: Division of The Uterine Branch From the
the uterus, we can appreciate the cross-shaped inferior Inferior Hypogastric Plexus (Figure 11A) and
hypogastric plexus formed by the pelvic splanchnic Division of The Uterosacral Ligament (Figure
nerve, the hypogastric nerve, the uterine branch and 11B)
the bladder branch from the inferior hypogastric plexus. The uterine side of the pelvic nerve plane including the
These nerves reside in the same connective tissue plane uterine branch from the inferior hypogastric plexus is
that we call the pelvic nerve plane (4) (Figure 10A). clamped, divided, and ligated. When we cut the uterine
On the same level of the hypogastric nerve, the branch of the pelvic nerves, there is a feeling resembling a
bladder branch from the inferior hypogastric plexus can stretched string breaking with a snap (Figure 11A). After
be separated from the blood vessels of the paracolpium. the division of the uterine branch, the hypogastric nerve,
Then Pean’s forceps is insinuated from the v-shaped the pelvic splanchnic nerve and the bladder branch of
depression created between the bladder branch and the the inferior hypogastric plexus forms the T-shaped nerve
blood vessels of the paracolpium into the connective plane. The remaining uterosacral ligament residing
tissue between the pelvic nerve plane and the cervix/ between the uterus and the rectum is divided (Figure
upper vagina at the level a little bit ventral side of the 11B). Then, the connective tissue between the lower
hypogastric nerve and a little bit dorsal side of the cut uterus/vagina and the rectum is appreciated. This is the
end of the deep uterine vein (Figure 10B). 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 cervi-
cal 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 on the opposite side, the length of the vaginal cuff is
Ligation of The Paracolpium confirmed. Then the uterus is amputated from the vagina
By pushing the rectum up, the rectovaginal ligament rises (Figure 13 A, B).
to the surface between the T-shaped inferior hypogastric
plexus and the rectum. Only the rectovaginal ligament is Conclusion
divided using bipolar scissors toward the upper vagina
If the surgeon can perform separation of the posterior
excluding the T-shaped nerve plane. By the division of
leaf of the vesicouterine ligament, and could trace
the rectovaginal ligament close to the upper vagina, the
the cross-shaped inferior hypogastric plexus, we can
bladder branch from the inferior hypogastric plexus
successfully divide only the uterine branch from
forming T-shaped nerve plane is gradually separated
the inferior hypogastric plexus. By these operative
from the blood vessels of the paracolpium (Figure
12A). The separation and division of the rectovaginal procedures, the T-shaped inferior hypogastric plexus,
ligament is extended caudally to obtain vaginal length is able to be preserved and we can archive the urinary
deemed appropriate by the level of cervical disease. At functions of complete voiding, a sense of fullness and a
the designated level, the blood vessels of the paracolpium sense of micturition.
are ligated (Figure 12B). Now, the T-shaped nerve plane
formed by the hypogastric nerve, the pelvic splanchnic References
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