Download Topography of the pelvic autonomic nervous system and its potential

Clinical Anatomy 16:119 –130 (2003)
ORIGINAL COMMUNICATION
Topography of the Pelvic Autonomic Nervous System
and Its Potential Impact on Surgical Intervention
in the Pelvis
B. BAADER*
AND
M. HERRMANN
Department of Anatomy and Cellular Neurobiology, University of Ulm, Ulm, Germany
Bladder, bowel, and sexual dysfunction caused by iatrogenic lesions of the inferior hypogastric plexus (IHP) are well known and commonly tolerated in pelvic surgery. Because the
pelvic autonomic nerves are difficult to define and dissect in surgery, and their importance
often ignored, we conducted a gross anatomic study of 90 adult and four fetal hemipelves.
Using various non-surgical approaches, the anatomic relations and pathways of the IHP were
dissected. The IHP extended from the sacrum to the genital organs at the level of the lower
sacral vertebrae. It originated from three different sources: the hypogastric nerve, the sacral
splanchnic nerves from the sacral sympathetic trunk (mostly the S2 ganglion), and the pelvic
splanchnic nerves, which branched primarily from the third and fourth sacral ventral rami.
These fibers converge to form a uniform nerve plate medial to the vascular layer and deep to
the peritoneum. The posterior portion of the IHP supplied the rectum and the anterior portion
of the urogenital organs; nerve fibers traveled directly from the IHP to the anterolateral wall
of the rectum and to the inferolateral and posterolateral aspects of the urogenital organs. The
autonomic supply from the IHP was supplemented by nerves accompanying the ureter and the
arteries. An understanding of the location of the autonomic pelvic network, including
important landmarks, should help prevent iatrogenic injury through the adoption of surgical
techniques that reduce or prevent postoperative autonomic dysfunction. Clin. Anat. 16:
119 –130, 2003. © 2003 Wiley-Liss, Inc.
Key words: pelvic plexus; hysterectomy; rectal surgery; prostatectomy; incontinence
INTRODUCTION
Nerve-sparing techniques are common in surgery;
for example, during an axillary lymph node dissection,
the thoracodorsal and long thoracic nerves are meticulously protected, except when they are directly involved by the extension of the cancer. Similarly, surgeons take great care to avoid injury to the recurrent
laryngeal nerves during thyroid surgery. Although
nerve protection is an indisputable objective in surgery, iatrogenic injury of the inferior hypogastric
plexus (IHP) is usually accepted as the norm. After
rectal resection for carcinoma, the incidence of urinary
dysfunction is between 7% and 70% and sexual dysfunction between 40% and 100% (Hojo et al., 1991). Ninety
percent of patients undergoing radical prostatectomy
were found to be impotent (Walsh and Mostwin, 1984).
These statistics clearly demonstrate the necessity for
autonomic nerve preservation in pelvic surgery.
©
2003 Wiley-Liss, Inc.
The preservation of the pelvic autonomic nervous
system is hampered by the fact that its nerves are not
distinctly seen in the surgical field because of their
tiny structure and the depth and narrowness of the
pelvis. In addition, confusing anatomical and surgical
nomenclature in this region encourages neglect of
nerve-sparing techniques. For instance, although originally named a peritoneal “plica,” current nomenclature uses the term “ligamentum,” which misleadingly
suggests the presence of only connective tissue ne*Correspondence to: Dr. Brigitte Baader, Department of Gynecology and Obstetrics, Frankenwaldklinik Kronach, Friesenerstrasse
41, D-96317 Kronach, Germany.
E-mail: [email protected]
Received 9 October 2001; Revised 16 August 2002
Published online in Wiley InterScience (www.interscience.wiley.
com). DOI 10.1002/ca.10105
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Baader and Herrmann
glecting nervous tissue: the ligamentum latum uteri,
the broad ligament of the uterus, contains an abundance of autonomic nerves.
Pelvic nerve-sparing techniques applied in adults
are based in large part on microscopic investigations of
fetuses, wherein relatively thick nerves are surrounded by little connective tissue (Fritsch, 1989). A
gross anatomic investigation of the IHP in adults
should demonstrate to better advantage the macroscopic topography of the autonomic pelvic network
and provide the necessary background for successful
dissection and protection of these nerves in adult
patients. Unfortunately, detailed descriptions of the
pelvic autonomic nerves reported earlier (Frankenhäuser, 1867) seem to have fallen into disuse. The
present topographic study provides further details
concerning the relationships between pelvic autonomic nerves and surgically important structures.
MATERIALS AND METHODS
To investigate the anatomic location of the IHP, 67
cadavers, including 65 adults and two fetuses, were
studied. A total of 94 hemipelves were dissected in
the 67 cadavers: 45 male (20 right, 25 left) and 49
female (25 right, 24 left). The adult cadavers ranged in
age from 38 to 98 years; the two fetuses, a male and
female, were aged 24 and 23 weeks, respectively. The
cadavers were preserved with a formalin-based fluid
by infusion into the femoral artery. The dissections
were documented by photography and hand drawings.
A non-surgical laterocaudodorsal approach provided
for optimal dissection of the IHP in its native visceral
topography. After dissecting abdominal retroperitoneal nerves and vascular structures to the pelvic brim,
the hip bones were carefully removed, piece by piece,
while preserving the muscles of the pelvic floor and
the supportive connective tissue associated with the
subperitoneal pelvic organs. After careful dissection of
the nerves and vessels of the ischio-anal fossa, the
pelvic diaphragm was exposed and dissected off the
pelvic viscera without damaging nervous structures.
To expose the sacral ventral rami to define the
origins of the pelvic splanchnic nerves, the dorsal wall
and part of the lateral wall of the sacral canal were
removed. The ventral rami of the spinal nerves were
dissected and pelvic splanchnic branches traced to the
IHP. Then, the terminal end of the dural sac and its
associated spinal nerves were lifted away from the
sacrum, and the anterior bony plate of the sacrum and
coccyx were removed. This resulted in an exposed
visceral bloc containing intact nervous connections to
the spinal cord, and allowed for a detailed dissection
of the autonomic innervation of the viscera.
Our analysis of the autonomic innervation of the
pelvic viscera of the 94 hemipelves focused on the
following parameters: the origins of the contributing
nerves, the location of the autonomic network, including its relationship to arteries and the pudendal nerve,
and its branches to the pelvic organs. The results were
either combined or divided into gender-specific
groups.
RESULTS
Sources of the Inferior Hypogastric Plexus
Contributions to an IHP arose from three different
sources: from the superior hypogastric plexus via the
hypogastric nerve, from the sympathetic trunk via
sacral splanchnic nerves, and from ventral rami of
sacral spinal nerves via pelvic splanchnic nerves.
In all 67 cadavers investigated, we observed sympathetic innervation from the superior hypogastric
plexus projecting to the two IHPs via the bilateral
fiber bundles of the hypogastric nerves; there were no
differences between male and female cadavers (Figs.
1B and 3). In addition, we were able to observe that
the IHP received sympathetic input from the sacral
splanchnic nerves. The dissection in Figure 1A shows
a sacral splanchnic nerve originating from S2 sympathetic ganglion and contributing to the IHP. In 19
hemipelves, sacral splanchnic nerves could be identified arising from the sacral sympathetic ganglia: in
58% of these (11/19) the sacral splanchnic nerves originated primarily from the S2 sympathetic ganglion; in
15% (3/19) from the S4 ganglion; in 11% (2/19) from
the S1 ganglion; in 11% (2/19) from the S3 ganglion;
and in 5% of the hemipelves (1/19) from the sacral
splanchnic nerves originated primarily from the S5
sympathetic ganglion. In all female cadavers, sacral
splanchnic nerves derived from either S1 (14%, 1/7) or
S2 (86%, 6/7) sympathetic ganglia, whereas in males
all sacral sympathetic ganglia were involved.
In contrast to the contributions of the sympathetic
ganglia to the IHP, the parasympathetic contributions
derived from sacral ventral rami of more inferior levels. In 85 hemipelves, pelvic splanchnic nerves could
be identified: in 52 % of these hemipelves (44/85), the
pelvic splanchnic nerves originated primarily from the
ventral ramus of S3 (Fig. 1A,B); in 32% (27/85) from
ventral ramus S4; in 12% (11/85) from S2; and in 4% of
hemipelves (3/85) the pelvic splanchnic nerves arose
primarily from ventral ramus S5. Whereas male cadavers were in congruence with these observations, the
female IHP differed slightly, receiving its pelvic
splanchnic nerves mainly from either ventral ramus S3
(60%, 21/35) or S4 (37%, 13/35).
Topography of Pelvic Autonomic Nervous System
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Fig. 1. Nerve fibers to the IHP in the female. A: Lateral view of
pelvic viscera of a female fetus at gestational age 24 weeks, left side.
B: Female adult, right side. In (A) the sympathetic trunk (1) is giving
off a sacral splanchnic nerve (2) from the S2 ganglion to the IHP (4).
In addition, a pelvic splanchnic nerve (3) is shown arising from ventral
ramus S3. The hemostat is holding the sciatic nerve; (B) shows the
sacral plexus reflected posteriorly (4) giving rise to the pudendal nerve
(5) and pelvic splanchnic nerves (3). Both connect to the IHP (2).
Furthermore, the most inferior parts of the IHP contribute to a neurovascular bundle (1). The hemostat shown in the right upper corner
holds the superior hypogastric plexus (SHP). Orientation icons: sup,
superior; inf, inferior; ant, anterior; post, posterior.
Pudendal Nerve and Its Relationship to the IHP
tions, the pudendal nerve is located inferior to the
pelvic diaphragm in the ischio-anal fossa and the IHP
is found superior to the pelvic diaphragm. In our
examinations, this seemingly distinct difference be-
It is generally accepted that the pudendal nerve has
purely somatic function and that the IHP only regulates autonomic function. Consistent with their func-
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Fig. 2. Comparisons of origins of sacral parasympathetic contributions to the IHP and sacral contributions to the pudendal nerve in
male (A) and female (B) pelvic cavities. Values were given as percent
incidences for each sacral ventral ramus that provides a contribution to
pelvic splanchnic and pudendal nerves in the male (A) and female (B)
pelves (male: nparasympathetic,right ⫽ 31, nparasympathetic,left ⫽ 19; npudendal
nerve,right ⫽ 8, npudendal nerve,left ⫽ 7; female: nparasympathetic,right ⫽ 22,
nparasympathetic,left ⫽ 13; npudendal nerve,right ⫽ 15, npudendal nerve,left ⫽ 7).
tween the topography and function of the pudendal
nerve and IHP was put into question.
In 37 hemipelves, sacral contributions to the pudendal nerve could be identified: in 40% of these
hemipelves (15/37), the pudendal nerve derived
mostly from ventral ramus S3; in 35% (13/37) from
ventral ramus S4; and in 19% (7/37) from ventral
ramus S2. Ventral rami L5 (3%, 1/37) and S1 (3%,
1/37) were less involved in providing the major contribution to the pudendal nerve. A comparison of the
parasympathetic and the pudendal nerve origins in
both males and females showed no differences. In
both genders the pudendal and pelvic splanchnic
nerves received fibers from S2–S4 in similar percentages (Fig. 2); for each gender somatic and autonomic
nerves derived from the same sacral ventral ramus to
similar degrees. In 49% of hemipelves (18/37), the
pudendal nerve and pelvic splanchnic nerves’ major
contribution to the IHP derived from the same ventral
ramus. The typical anatomy of these nerves observed
in laterocaudodorsal dissections are shown in Figures
1B and 5A.
Location of the IHP Within the True Pelvis
In addition to elucidating where contributing
nerves to the IHP originate, it is important to investigate the exact position of the IHP. The location of
the plexus was investigated in three different planes:
coronal, horizontal, and sagittal. Irrespective of gender, in the horizontal plane the IHP was localized at
about the level of sacral vertebrae S4 and S5.
In the coronal plane, the IHP of males was located
within and deep to the peritoneal fold between urinary bladder and rectum as well as pararectally. In
surgery, it is important to know the percentage of
cases in which the nerve fibers of the IHP can be
found at a distinct position; therefore, the values given
below are related to the number of instances where
the IHP occurred in distinct locations, taking into
account that the fibers of the IHP of one single
hemipelvis can be located in two or more positions.
Thus, a total of 55 locations were identified in 45 male
hemipelves. In 73% of these cases (40/55), the IHP
was found in the fold between urinary bladder and
rectum (Fig. 3); in 27% of cases (15/55), the IHP was
localized pararectally.
In females, nerve fibers of the IHP were identified
in four locations; a total of 60 locations were observed
in 49 female hemipelves. In 57% of these cases (34/
60), the IHP was observed in the uterosacral ligament;
in 30% of cases (18/60), it was found parametrially; in
only 2% (1/60) and 11% of cases (7/60) was the IHP
found pararectally and in the fold between the urinary
bladder and the uterus, respectively.
Within the sagittal plane it is important to determine the order in which neurovascular structures are
oriented between the levator ani and pelvic organs. In
all 42 cases in which the orientations in the sagittal
plane could be defined, the IHP was positioned immediately lateral to the pelvic organs. With respect to
the position of arteries, veins, and nerves, three groups
could be distinguished: in one group the veins were
most lateral, followed by the arteries and the nerves
(VAN, vein-artery-nerve group); the second group was
composed of arteries lying lateral to the veins, which
again were lateral to the nerves (AVN, artery-veinnerve group, Fig. 4); and in the last group, arteries and
veins were intermingled and an exact layering could
not be observed, but again the nerves were positioned
most medially, giving a VN (vessel-nerve) group. The
VAN order was found in 62% of IHPs (26/42) in which
a clear arrangement could be determined; the VN
arrangement was present in 31% of cases (13/42); and
only a few hemipelves (7%, 3/42) showed an AVNordered neurovascular structure. The AVN order was
only found in male cadavers (Fig. 4).
Structure of the Inferior Hypogastric Plexus and
Its Pattern of Innervation
Compared to the variable topographic relationships
of arteries and veins to the IHP, the plexus itself
consistently appeared as a homogeneous nerve plate
with no obvious layers (Fig. 3). Irrespective of gender,
autonomic fibers emerged from the anterior part of the
IHP and innervated the urogenital tract and the inferior part of the rectum (Figs. 5A and 6A). The superior
part of the rectum received fibers from the posterior
part of the IHP.
Topography of Pelvic Autonomic Nervous System
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Fig. 3. Position of the IHP within the pelvic cavity. Lateral view
of an adult male pelvis, right side. The IHP (3) is located between the
rectum (6) and the bladder (7) along a line between the bladder and
coccyx (8). 1, 2, and 4 represent contributions to the IHP: pelvic
splanchnic nerves (1, 2); right hypogastric nerve (4). The levator ani is
labeled 5. Orientation icons: sup, superior; inf, inferior; ant, anterior;
post, posterior.
As shown in Figure 6A, the anterior part of the IHP
was positioned in 62% of male hemipelves (28/45) in
the region where the ureter, seminal gland, prostate
gland, and neck of the urinary bladder converged. In
about half of the female hemipelves (24/49), the bulk
of the plexus was restricted to a region between the
ureter, uterine artery, cervix, and urinary bladder.
From the anterior part of the IHP, several groups of
fibers coursed to the pelvic organs. According to their
location, they were designated superior, central, and
inferior branches. In females, superior branches,
which mostly commingled with the ureter, were responsible for the innervation of the urinary bladder.
Inferior fibers of the anterior part of the IHP innervated the inferior part of the rectum and formed the
neurovascular bundle to the erectile tissue. The central branches of the anterior part of the plexus, in
general, followed the course of the uterine artery to
the uterine cervix (Fig. 5A).
The topographical division of the female IHP was
found to be similar in males; the only difference between genders was that the central portion of the
anterior part of the plexus innervated the prostate and
seminal gland in males.
The vertical organization of the IHP followed the
tilt of the pelvic viscera: the urinary bladder was located superior and the rectum inferior to the sexual
organs. Thus, the upper part of the IHP innervated
more ventral pelvic organs and the lower portions
supplied dorsal organs. The pelvic organs, however,
were also innervated by fibers that penetrated the
IHP as they traveled on the ureter and arteries.
Vessels
As described above, the IHP was positioned medial
to the blood vessels in all cadavers. Therefore, to
reach the pelvic organs, some of the arteries have to
penetrate the IHP. In 33% of hemipelves (31/94), the
inferior vesical artery, in 23% (22/94) the middle rectal
artery, and in 6% of hemipelves (6/94) the superior
vesical artery penetrated the IHP (Fig. 4). In 45% of
female hemipelves (22/49), the uterine artery penetrated the IHP close to where it crossed the ureter
(Fig. 5B).
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Fig. 4. Sagittal arrangement of the IHP and vessels in the pelvis.
Shown is an adult male pelvis in a lateral view from the right side. The
arrangement represents an AVN (artery-vein-nerve) layering showing
the inferior vesical artery (3) most lateral followed by the pelvic veins
(2) and the IHP (5). The middle rectal artery (4) deriving from the
internal iliac artery (1) leaves the arterial layer to penetrate the IHP and
to course toward the inferior part of the rectum. Orientation icons: sup,
superior; inf, inferior; ant, anterior; post, posterior.
Rectum
The urinary bladder was observed to be innervated
by the IHP in 79% of hemipelves (74/94). In general,
all fibers coursed from a lateral, inferior, and posterior
direction (Fig. 6A) such that fibers of the IHP were
found lateral to the neck of the bladder and along the
inferior vesical artery and ureter. The anterior surface
of the urinary bladder was free of innervating fibers in
all of the dissections in which they were observed.
In half of the hemipelves investigated (47/94), the
rectum was observed to be innervated by the IHP.
The posterior part of the IHP innervated the superior
part of the rectum; the inferior part of the rectum was
innervated by inferior branches of the anterior part of
the IHP. In addition, fibers accompanying the middle
rectal artery after its penetration of the IHP provided
innervation to the rectum. Of surgical importance is
the finding that the rectum was always innervated on
its lateral aspect, but never on its posterior aspect.
Urinary System
In 77% of hemipelves (72/94), a close association of
autonomic fibers to the ureter could be shown. Irrespective of gender, only a few autonomic fibers
coursed alongside the proximal part of the ureter
within the abdomen and into the pelvis. During their
course to the urinary bladder, the ureter and these
autonomic fibers descended in parallel, and, just before the ureter entered the urinary bladder (near the
seminal gland in males and near the isthmus of the
uterus in females), the fibers of the IHP joined the
ureter (Figs. 5A and 6A).
Gender-Specific Organs
An autonomic supply of the uterus was found in
73% of female hemipelves (36/49). Most of the fibers
left the central portion of the anterior part of the IHP
at about the isthmus of the uterus and innervated the
uterus from a lateral direction (Fig. 5A,B). An additional supply could be shown from fibers running
along the uterine artery as well as from fibers leaving
the ureter as it crossed the uterine artery. The upper
third of the lateral wall of the vagina was supplied by
uterine branches of the IHP in 24% of cases (12/49);
this might indicate a high degree of variability in the
autonomic innervation of the vagina.
Similar to the urinary bladder, the prostate was
supplied by autonomic fibers from a lateral, inferior,
Topography of Pelvic Autonomic Nervous System
Fig. 5. Innervation of pelvic viscera by the IHP in fetal (A) and
adult (B) females. A: Lateral view of the fetal visceral bloc from the
right showing the ureter (1), IHP (2), cervix uteri (3), neck of the
bladder (4), pudendal nerve (5), pelvic splanchnic nerve (6), and right
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hypogastric nerve (7). B: Lateral view of the adult pelvic viscera from
the left showing the uterine artery (1), internal iliac artery (2), IHP (3),
uterus (4), and uterine tube (5). Orientation icons: sup, superior; inf,
inferior; ant, anterior; post, posterior.
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Fig. 6. Innervation of pelvic viscera by the IHP in fetal (A) and
adult (B) males. A: Lateral view of the fetal visceral bloc, right side.
IHP (1), bladder (2), ureter (3), prostate (4), neurovascular bundle (5).
B: Lateroposterior view of adult male pelvic viscera, left side. Poste-
riorly reflected ureter (1) and ductus deferens (2), seminal gland (3),
IHP (4), and urinary bladder (5). The IHP was reflected anteriorly by
the hemostat. Orientation icons: sup, superior; inf, inferior; ant, anterior; post, posterior.
and posterior direction (Fig. 6A), and its anterior surface was also free of innervating fibers. The innervation to the prostate was observed in 73% of male
hemipelves (33/45). In about half of male hemipelves
(23/45), the seminal gland was found to be innervated
by the IHP; innervation was from all sides, but favored a lateral direction. Figure 6B illustrates the close
relationship between the seminal gland and the IHP.
In 40% of hemipelves (18/45), the ductus deferens
was observed to be supplied by the IHP in its most
distal part (Fig. 6B); innervating fibers arose from
branches to the seminal gland. In the male fetus the
ductus deferens was not surrounded by any autonomic
nerves, suggesting that it obtains its innervation from
the IHP secondarily during maturation.
Neurovascular Bundle
Besides the innervation pattern of the pelvic organs
described above, the IHP is responsible for erectile
function. The nervous stimulus for erection is provided by the cavernous nerves, which produce an
increase in blood flow in the arteries that supply erectile tissue. The cavernous nerves derive from the most
inferior part of the IHP and pass through the urogenital diaphragm along vessels, giving the combined
structure the name “neurovascular bundle.” In males,
Topography of Pelvic Autonomic Nervous System
this neurovascular bundle was demonstrated in 40% of
hemipelves (18/45). It formed at the inferior border of
the prostate and penetrated the urogenital diaphragm
parallel to the urethra (Fig. 6A). The pathway of the
neurovascular bundle was found to be similar in females. It originated along the lateral surface of the
vagina and traveled within the vesicovaginal septum
and inferiorly through the urogenital diaphragm (Fig.
1B). The cavernous nerves in the female, however,
were demonstrated in only 25% of hemipelves (12/49).
DISCUSSION
Topographic Aspects of the Inferior Hypogastric
Plexus
This study describes in detail the topography of the
IHP that may be useful in improving nerve-sparing
surgical approaches in pelvic surgery. The observations of the sympathetic and parasympathetic sources
of the IHP described in previous reports were verified
in our study; however, we expanded upon these studies by presenting a systematic view of the sources and
distribution of fibers to and from the IHP. Also, previous reports described the sympathetic sources of the
IHP as deriving from sympathetic ganglia S1 to S5
(Davis, 1933; Curtis et al., 1942; Pearson and Sauter,
1970; Walsh and Donker, 1982) and parasympathetic
sources from S2 to S5 (Baljet and Drukker, 1981;
Walsh and Donker, 1982; Stelzner et al., 1989). We
demonstrated a more specific distribution in the participation of different ganglia and ventral rami. For
example, sacral splanchnic nerve branches from sacral
sympathetic ganglion S2 were the main sources of
sympathetic fibers to the IHP and sacral ventral rami
S3 and S4 were the primary sources of parasympathetic fibers to the IHP. Variations in results may be
due in large measure to the fact that the autonomic
nerve fibers are extremely tiny and difficult to dissect.
An interesting observation of this study was that we
demonstrated a similar source for the pudendal nerve
and parasympathetic fibers forming the pelvic
splanchnic nerves, suggesting that the somatic and
autonomic nervous systems may be interrelated. Such
a relationship was suggested earlier based on findings
that the sacral ventral rami from which the autonomic
and somatic fibers emerge have been identical (Clara,
1953; Alverdes, 1968) and that autonomic fibers were
found to be enclosed within the pudendal nerve
(Walsh and Donker, 1982; Colombel et al., 1999).
A major focus of this study, the description of the
topographic anatomy of the IHP within the pelvic
cavity, is of critical significance in pelvic surgery. Basic
aspects of the topography of the IHP along the hori-
127
zontal and coronal planes have been described previously in fetuses (Fritsch, 1989) and are consistent with
the present findings. Extending previous work about
the mediolateral organization of nervous and vascular
structures in the pelvic cavity, we described more
precisely the relationship of the nervous and vascular
layers and the variety of their arrangements. The
medial position of the IHP has significant implications
for surgical procedures, as described in more detail
below.
We observed that the IHP is a homogeneously
arranged ganglionic plate that is not divided into distinct layers and secondary structures on the macroscopic level. This is consistent with the findings of
Baljet and Drukker (1981) and Lee et al. (1973).
Although one can get the impression that trilaminar or
bilaminar sheets exist within the IHP, as postulated
by Ashley and Anson (1946), it is difficult to impose
any functional significance to these layers. In addition,
the frequently cited existence of multiple, widely
separated subplexuses is unlikely. Even if there are
distinct groups of neural crest cells responsible for the
innervation of different organs (Kuntz, 1952), there is
no data to suggest that they are distinguishable under
intraoperative conditions.
The autonomic innervation of the female genital
tract, principally described by Frankenhäuser (1867),
is consistent with the present findings. The uterosacral ligament, however, which is generally considered
as containing only connective tissue, actually contains
nerve fibers that travel to the uterus. A new finding of
this study was the observation that the cavernous
nerves in the female derived from the most inferior
branches of the IHP and not from terminal branches
of the vaginal plexus as postulated earlier (Testut,
1911). In contrast to the female cavernous nerves, the
neurovascular bundles in males have been described
previously in detail because of their importance in
prostatic cancer surgery (Lue et al., 1984); this description is consistent with the present findings. Similarly, the innervation of the prostate is well known
(Lepor et al., 1985; Schlegel and Walsh, 1987) and
concordant with our study. In contrast to published
literature describing no clear pattern of innervation of
the seminal gland, it was found to be heavily surrounded by a network of IHP fibers in our study.
The innervation of the urinary bladder is controversial. It has been reported that the bladder receives
innervation from all sides (Ashley and Anson, 1946). It
has also been demonstrated that the bladder receives
only fibers traveling along with the ureter (Fritsch,
1989). Although there is little doubt that the ureter is
accompanied by autonomic fibers (Davis, 1933; Stelzner, 1977), our study demonstrates an autonomic
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nerve supply to the bladder via direct fibers from the
IHP from a lateral, inferior, and posterior direction as
well as from indirect fibers traveling along the ureter
and inferior vesical artery.
This dual supply of the urinary bladder is similar to
the innervation of the rectum. Whereas Long and
Bernstein (1959) reported contributions from the IHP
via fibers along the middle rectal artery, Fritsch (1989)
reported a direct innervation of the rectum by the IHP
from an anterolateral direction. Our observations support both of these pathways. A still-unanswered question remains: Are there autonomic fibers from the IHP
to the posterior aspect of the rectum? Whereas Pearson and Sauter (1970) and Taguchi et al. (1999) described such an innervation pattern, we could not
verify these findings.
Implications of the Topographic Anatomic
Knowledge of IHP on Surgical Interventions
From our knowledge of the detailed topography of
the IHP, we can now better predict regions of iatrogenic injury to the autonomic nervous system during
surgery within the pelvic cavity. In the following discussion, we describe endangered regions in a superiorto-inferior orientation, and then describe specific implications for urologists, surgeons, and gynecologists.
The promontory is the most superior region where
operative injuries may occur. Aortocaval lymph node
dissections, colorectal surgeries, and promontory fixations are surgical interventions that can injure the
superior hypogastric plexus. Proceeding caudally, the
retrorectal space (the mesorectum in surgical vernacular) is an important area of potential harm to sources
of the IHP. For example, during a mesorectal excision
for rectal cancer, the superior hypogastric plexus as
well as the more inferiorly located pelvic and sacral
splanchnic nerves can be injured. Pelvic lymph node
dissections around the internal iliac artery can damage
the IHP itself; therefore, knowledge of the topography of the vasculonervous layers can be extremely
helpful. Dissections along the middle rectal artery
bear potential risks not only to the nerves supplying
the rectum but also for the entire IHP because it is
formed by its contributing nerves around this artery.
The anterior part of the IHP is endangered during
surgical interventions near the distal end of the ureter,
the uterine or inferior vesical arteries, the seminal
gland, and Denonvilliers’ fascia. During ligations of
the bladder and rectal stalks, as well as during dissection of the uterosacral ligaments, attention should be
paid to dissecting immediately adjacent to the organs
to prevent injury to nerves. The deepest region of
predictable injury is the area where the neurovascular
bundle pierces the urogenital diaphragm.
It might be of general importance in pelvic surgery
to first dissect the superior hypogastric plexus, which
is relatively constant in its position, and then proceed
into the depth of the pelvis along the bilateral hypogastric nerves, and finally to the IHP.
Awareness of the structure of the IHP might significantly improve outcomes in all fields of pelvic
surgery. After prostatectomies, only 10% of patients
are still potent; cystoprostatectomy leads to impotence
in all patients (Walsh and Mostwin, 1984). These poor
outcomes prompted urologists to develop plexus-preserving methods. Walsh and Donker (1982) described
a nerve-sparing technique that prevents injury to the
IHP by: 1) transecting the membranous part of the
urethra very close to its muscular wall during apical
dissection of the prostate, and 2) ligating the lateral
vascular and nerve supply to the prostate (known as
the lateral pedicle in surgical vernacular) close to the
organ during lateral mobilization. Based on more detailed neuroanatomic studies, Lepor et al. (1985) suggested an anterior incision of the lateral pelvic fascia to
preserve the IHP and recommended using the prostatovesical vessels as landmarks for identifying the
neurovascular bundle. Schlegel and Walsh (1987) described the seminal gland as the most important landmark to avoid injury to the IHP when dissecting the
posterior pedicle. Based on these methods, the percentage of potent patients after prostatectomy has
been reported at 69%, without compromising removal
of tumor (Walsh et al., 1987).
Surgeons have also been prompted to develop a
nerve-sparing technique for rectal surgery because of
an incidence of sexual and urinary dysfunction in
40 –100% and 7–70% of patients, respectively; the
technique is called PANP (pelvic autonomic nerve
preservation). Hojo et al. (1991) and Sugihara et al.
(1996) describe four to five degrees of preserving autonomic pelvic tissue, depending on the preoperative
staging: Degree 1 entails complete preservation of the
superior and inferior hypogastric plexuses, whereas
Degrees 4 and 5 only preserve the nerves from the
ventral ramus of S4 to the urinary bladder. The best
results have been obtained with Degree 1 surgeries,
yielding no urinary dysfunction; however, 70% of patients still have sexual dysfunction. To improve outcome, the general conclusion of this and other work is
that for mesorectal dissections it is important to stay
medially and to dissect the superior hypogastric
plexus with its hypogastric nerves (Long and Bernstein, 1959; Weinstein and Roberts, 1977; Hida et al.,
1999). Furthermore, rectal dissection close to the rectal fascia (Muntean, 1999), identification of the middle
Topography of Pelvic Autonomic Nervous System
rectal artery as a landmark for the IHP (Long and
Bernstein, 1959), preservation of Denonvilliers’ fascia
within the prerectal space, and protection of the rectourethral fascia (described as the rectourethral muscle by Stelzner et al., 1989) for sparing the neurovascular bundle during the perineal approach (Stelzner et
al., 1989) are all techniques that help to preserve the
IHP and its sources and branches.
In the 1960s, the supravaginal hysterectomy was
preferentially used to preserve the autonomic supply of the pelvic viscera and the integrity of the
pelvic floor in benign gynecologic diseases; however, because of the risk of developing a carcinoma
of the cervical stump, gynecologists abandoned this
procedure. Semm (1991, 1993) rediscovered the supracervical method using the intrafascial hysterectomy. This technique leaves a highly vascularized
fascial collar and its contained nerves untouched,
and enucleates the intrafascial cervical tissue,
thereby eliminating a potential malignancy. Urinary
and sexual dysfunctions could thus be prevented,
and the vagina and pelvic floor remain intact, which
seems to be of significant importance for female vita
sexualis (Semm, 1991, 1993; Lüttges et al., 1994;
Mettler et al., 1995). More serious problems in gynecology are oncologic interventions that fail to
consider nerve-sparing techniques. Höckel et al.
(1998), however, described a fascinating technique
for cervical carcinoma. Their nerve-sparing, extended
radical hysterectomy uses liposuction to remove all
parametrial lymphoid tissue and subperitoneal adipose tissue without affecting the pelvic splanchnic
nerves and the IHP. Additionally, they incised the
vesico-uterine and recto-uterine pouches in the midline to ligate the uterine artery immediately after it
branches from the internal iliac artery, to expose the
IHP and its branches, and to dissect the recto-uterine
and recto-vaginal ligaments in the anterolateral mesorectal planes.
In conclusion, preserving the autonomic nervous
system in the true pelvis has already been realized by
the aforementioned surgical techniques and is currently a focus in several surgical fields. The techniques used, however, still need to be improved. This
will require establishing a standard in surgery based
on the topographic anatomy of the IHP, including its
contributing nerves and branches. The present work
demonstrates that the autonomic nerves of the pelvis
can be dissected in detail at the macroscopical level;
this should help the surgeon visualize anatomic relationships in the pelvis for further improving their
nerve-sparing techniques.
129
ACKNOWLEDGMENTS
The authors gratefully acknowledge the excellent
technical assistance of Mrs. S. Doll and Mr. E. Voigt.
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