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(Artigo) (Anatomia) Denonvilliers' Fascia Revisited
(Artigo) (Anatomia) Denonvilliers' Fascia Revisited
DOI 10.1007/s00276-014-1336-0
Original Article
Abstract Although several studies have reported that only at 7 weeks, whereas, at later stages, the peritoneal
the peritoneum does not contribute to the formation of a cavity did not extend inferiorly to the level of the pros-
fascia between the urogenital organs and rectum, Denon- tatic colliculus or the corresponding structure in females.
villiers’ fascia (DF), a fascia between the mesorectum and The cul-de-sac had completely disappeared in front of
prostate (or vagina) in adults, is believed to be a remnant the rectum at 8 weeks and homogeneous and loose mes-
of the peritoneum. Remnants of the peritoneum, however, enchymal tissue was present in front of the rectum at the
were reportedly difficult to detect in other fusion fasciae level of the colliculus at 12–16 weeks. We found no evi-
of the abdominopelvic region in mid-term fetuses. To dence that linearly arranged mesenchymal cells developed
examine morphological changes of the pelvic cul-de-sac into a definite fascia. Therefore, the development of the
of the peritoneum, we examined 18 male and 6 female DF in later stages of fetal development may result from
embryos and fetuses. A typical cul-de-sac was observed the mechanical stress on the increased volumes of the
mesorectum, seminal vesicle, prostate and vagina and/
or enlarged rectum. Therefore, we considered the DF as
J. H. Kim a tension-induced structure rather than a fusion fascia.
Department of Anatomy, Chonbuk National University Medical Fasciae around the viscera seemed to be classified into (1)
School, Jeonju, Korea a fusion fascia, (2) a migration fascia and (3) a tension-
Y. Kinugasa
induced fascia although the second and third types are
Division of Colorectal Cancer, Sizuoka Cancer Institute, Susono likely to be overlapped.
City, Sizuoka, Japan
Keywords Denonvilliers’ fascia · Peritoneum ·
S. E. Hwang
Cul-de-sac · Rectum · Prostate · Vagina
Department of Surgery, Daejeon Sun Hospital, Daejeon, Korea
G. Murakami
Division of Internal Medicine, Iwamizawa Kojin-kai Hospital, Introduction
Iwamizawa, Japan
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the distal parts of the pelvic plexus extend freely from the another concept of fasciae, the “migration fascia” [8] to
paracolpium to the mesorectum. many fascial structures of the human body based on fetal
The actual DF is regarded as the “anterior layer of the histology [5, 12, 13, 15, 21–23]. The term “migration fas-
DF”, whereas the “posterior layer of the DF” corresponds cia” is used due to the upward migration of the fetal kid-
to the fascia propria of the rectum [30, 32]. Several recent ney, but it essentially indicates mechanical stress- or ten-
anatomic studies have also used the term “anterior layer” sion-inducing fascial formation. This study was designed
for the actual DF [36, 37]. To date, however, no embryologi- to re-examine morphological changes in the pelvic cul-
cal studies have reported that the fascia propria of the rec- de-sac of the peritoneum in human embryos and fetuses at
tum is derived from the pelvic cul-de-sac of the peritoneum 7–16 weeks of gestation.
(i.e., an inferior protrusion of the peritoneal cavity in front of
the embryonic rectum). For simplicity, we use the term DF
to describe a definite membranous structure in front of the Materials and methods
mesorectum in both genders. Loose fatty tissue of the meso-
rectum between the fascia propria and DF contains abundant The study was performed in accordance with the provi-
blood vessels and nerves that supply the rectum. Several sions of the Declaration of Helsinki 1995 (as revised
hypotheses have been formulated to determine the embryo- in Edinburgh 2000). Eighteen paraffin-embedded male
logical origin of the DF. In one hypothesis, peritoneal fusion embryos and fetuses at an estimated gestational age (GA)
occurs, giving rise to the DF [3, 30]. In a second hypothesis, of 7–16 weeks [crown rump length (CRL) 20.5–115 mm]
fusion occurs but does not give rise to the DF because no were examined, including four embryos of GA 7 weeks
remnant of the peritoneum remains in fetuses [34]. In a third (CRL 20.5–23 mm), five fetuses of GA 9–10 weeks (CRL
hypothesis, fusion does not occur and the DF does not origi- 36–56 mm) and nine fetuses of GA 12–16 weeks (CRL 80–
nate from the pelvic cul-de-sac of the peritoneum [29]. 130 mm). For comparison, six female embryos and fetuses
A detailed morphometric analysis of the topographical were examined, two of GA 8 weeks (CRL 36 and 39 mm)
relationship between the cul-de-sac and other landmark and four of GA 12–14 weeks (CRL 62–95 mm). All fetuses
structures in the pelvis clearly demonstrated that the peri- and embryos were part of the large collection kept at the
toneal cul-de-sac disappears during the fetal stage, with embryology Institute of the Universidad Complutense,
smooth muscles derived from the longitudinal muscle layer Madrid, being the products of urgent abortions, miscar-
of the rectum later appearing behind the rectum [29]. This riages or ectopic pregnancies managed at the Department
finding suggested that the presence of aberrant smooth of Obstetrics of the University. Approval for the study was
muscles may erroneously suggest the presence of a fascia- granted by the ethics committee of the university.
like structure in fetuses. Smooth muscles in fetuses actu- The donated fetuses were fixed in 10 % v/v formalin
ally originate from the longitudinal muscle layer of the rec- solution for more than 3 months. After division into the
tum as well as from the bladder, and migrate and disperse head and neck, thorax, abdomen and pelvis, and the four
around these structures to form smooth muscle tissues extremities, the abdominopelvic specimens from the eight
embedded in the pelvic floor [1, 9, 16]. The histology of larger fetuses (GA 12–15 weeks) were decalcified by incu-
the actual peritoneal fusion behind the duodenum has been bation at room temperature for 3–5 days in Plank-Rychlo
compared with the artifactual fusion at the edge of the pel- solution (AlCl2/6H2O, 7.0 w/v %; HCl 3.6; HCOOH 4.6).
vic cul-de-sac [29]. After routine procedures for paraffin-embedded histology,
The retroduodenal or retropancreatic fascia (i.e., the 7-µm-thick horizontal sections of the entire abdomen and
fascia of Treitz) has been famous for a fusion fascia of the pelvis were prepared serially from the nine earlier speci-
peritoneum rather than the DF. The retroduodenal fascia mens, with sections of similar thickness prepared at 50 µm
provides a classical plane in abdominal surgery during ret- intervals from the nine later specimens. The sectional planes
ropancreatic mobilization of the pancreatic head and duo- were horizontal (two specimens of GA 7 weeks; three of
denum (i.e., the Kocher maneuver). After rotation of the GA 9 weeks; and five of GA 12–15 weeks), frontal (two
midgut mesentery, however, a remnant of the secondary of GA 10 weeks; two of GA 13 weeks) or sagittal (two of
fusion of the peritoneum becomes unclear at the mid-term GA 7 weeks; two of GA 15–16 weeks). The sections were
fetuses [4, 35]. Likewise, following secondary attachment stained with hematoxylin and eosin (HE) or azan stain.
of the mesocolon transversum to the pancreas and duode-
num, the fused peritoneal layer is changed into irregularly
arrayed fibrous tissues [10]. Therefore, it may be difficult Results
to determine whether or not the so called fusion fascia cor-
responds to a true remnant of the fused peritoneum. In con- In earlier-stage specimens, the urogenital sinus did not dif-
trast to the concept of fusion fascia, our group has applied ferentiate into the bladder and urethra. Likewise, Műllerian
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Fig. 1 Sagittal sections showing the bottom of the peritoneal cavity. cavity in the superior side of the developing prostate. No fascia is evi-
a (7 weeks) displays the cul-de-sac of the peritoneum (stars) reach- dent behind the rectum (R). Scale bars in each panel, 1 mm. CO coc-
ing a level inferior to the future prostate (PR). The future urethra cyx, EAS external anal sphincter, PB pubis, R rectum, S sacrum, VAS
(UR) and bladder are not differentiated from the urogenital sinus, vas deferens
b (14 weeks) and c (16 weeks) exhibit the bottom of the peritoneal
and Wolffian ducts did not differentiate into the vas def- The pelvic cul-de-sac of the peritoneum extended
erens, prostate, seminal vesicles and vagina. The prostatic below the level of the future prostatic colliculus, reaching
colliculus and the corresponding structure in females are the level of the second or third sacral vertebra at 7 weeks
derived from complexes of the Műllerian and Wolffian (Fig. 1). This lowermost part of the peritoneal cavity sur-
ducts [31]. However, for easy comparison between stages rounded the anterior half of the rectum. Behind the rec-
or with adult morphology, we used terms of adult anatomy: tum, a mesentery-like structure attached to the presacral
the bladder and/or urethra for the urogenital sinus; and the loose mesenchymal tissue (Fig. 2). The cul-de-sac was a
vas deferens, prostate and vagina for the Műllerian and U-shaped cavity sandwiching the rectum. The developing
Wolffian ducts. pelvic nerve plexus was thicker than the cul-de-sac and
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extended along the anteroposterior axis of the pelvis near the primitive levator ani muscle. Because the nerve plexus
the rectum and urogenital sinus. The lower end of the cul- was penetrated by and intermingled with abundant veins,
de-sac was located in the superior side of the inferior end of spongy tissues were located on the immediately lateral side
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◂ Fig. 2 Horizontal sections of a 7-week embryo. a The most superior initially contained a connecting band running along the
section in this figure, displays the future vas deferens (VAS) merging anteroposterior axis (Fig. 6b, c), but, as the size of the fetus
either the future urethra (UR) or urogenital sinus. Intervals between
a–b, b–c and c–d are 0.1 mm. The cul-de-sac of the peritoneum increased, the mesenchymal tissue became more homoge-
(stars) surrounding the anterior half of the rectum (R) provides a neous (Fig. 6d).
mesentery-like structure (arrowheads in a) at the posterior side of d, In specimens of both genders of GA >10 weeks, the
the most inferior section in this figure, the cul-de-sac disappears and, smooth muscles of the bladder neck surface (i.e., the fetal
instead, nerves and veins occupy in the space alongside the rectum.
a–d were prepared at the same magnification (scale bar in a 1 mm). detrusor apron [9]) extended posterolaterally to connect
e (Scale bar 0.1 mm), a higher magnification view of the central part with a fascial structure (Fig. 3b). At GA 10 weeks, the pre-
of c, exhibits numerous veins intermingling with nerves near the peri- sacral fascia (Fig. 4a, b) as well as the fascia pelvis parieta-
toneum. The peritoneum is slightly thicker than endothelium of the lis (Fig. 4e) appeared. The latter fascia was much thicker
veins. IS ischium (developing bone), PN sacral roots of the pudendal
nerve, S sacrum along the obturator internus muscle (i.e., above the arcus
tendineus levator ani) than along the levator ani (Fig. 5c, d).
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Fig. 3 Horizontal sections of a 10-week fetus. a The most superior to connect with a fascial structure (arrows). In the inferior side of the
section in this figure, displays the ureter (UT) passing through walls bottom (c), the urethral wall (UR) is connected with the rectum (R)
of the bladder (B). Note the anteriorly restricted covering of the peri- by a dense mesenchymal tissue (arrowheads). In the more inferior
toneum (stars). Thus, a mesentery-like structure behind the rectum is levels (d), a homogeneous loose tissue is present between the ure-
not evident (cf, see Fig. 2a, b). Intervals between panels are 0.9 mm thra and rectum. All panels were prepared at the same magnification
(a–b), 0.6 mm (b–c) and 1.1 mm (c–d), respectively, b includes the (scale bar in a, 1 mm). LA levator ani, PB pubis, PR future prostate,
bottom of the peritoneal cavity (star). From the anterior aspect of the VAS vas deferens
neck of the bladder (B neck), smooth muscles extend posterolaterally
fascia and other cervical fasciae [22, 23]. Rapidly growing In short, early developed, relatively hard structures tend to
tissues or organs are another major source of mechanical accompany fascial structures. Fusion fasciae from the mes-
stress. These structures compress the surrounding mesen- entery of the colon around the kidney also seem to contrib-
chymal tissues into a linear orientation, providing a fascial ute to fascia formation (i.e., the lateroconal fascia [21]).
structure around them, as typified by the renal fasciae [21]. The ureteral sheath and the hypogastric fascia are likely
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Fig. 4 Horizontal sections of a 12-week fetus. a The most superior sec- ferent from nearby veins with endothelial lining (c). In the more inferior
tion in this figure, displays the ureter (UT) joining the bladder (B). The levels (d, e), it is difficult to find fascial structures between the prostatic
vas deferens (VAS) is located in the immediately anterior side of the peri- colliculus or urethra (UR) and the rectum (R). Multiple, short and linear
toneal cavity (stars). Intervals between panels are 1.2 mm (a–b), 0.1 mm arrangements of mesenchymal cells (arrows in d) appeared to be a kind
(b–c), 1.4 mm (c–d) and 1.5 mm (d–e), respectively. b includes the bot- of knife mark (artifact). There are primitive forms of the presacral fascia
tom of the peritoneal cavity. In the inferior side of the bottom, there is (arrows in a, b) as well as the fascia pelvis parietalis (arrows in e). Scale
an artifactual space due to histological procedure (asterisks) and it is dif- bars in each panel, 1 mm. PB pubis, PR future prostate, S sacrum
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Fig. 5 Frontal sections of a 14-week fetus. a, d corresponds to the elongated views due to frontal sections: it is filled with a homoge-
most posterior (anterior) side of the figure. Intervals between panels neous loose tissue. The fascia pelvis parietalis is much thicker along
are 2.5 mm (a–b), 1.2 mm (b–c) and 0.5 mm (c–d), respectively. a the obturator internus muscle (arrowheads in c, d) than that along
(Scale bar in a, 1 mm) includes outward extensions of longitudinal the levator ani muscle (arrows in c). B bladder, LA, levator ani mus-
smooth muscles (arrows) of the rectum (R). In b–d, a space between cle, IC, ischiocavernosus muscle, OI Obturator internus muscle, UA
the prostate (PR) or urethra (UR) and the rectum is emphasized by umbilical artery, UT ureter, VAS vas deferens
to be formed by mechanical stress between the ureter or of tensor-vascular-styloid and prestyloid fasciae [5, 12, 13].
hypogastric nerve and other prevertebral tissues [15]. In Overall, migration of a structure covered by the fascia is
the fetal head, rapidly developing fatty tissue masses seem not usually required in fetuses. Therefore, with an excep-
to play a major role in fascia formation, with the regressed tion (i.e., fasciae around the kidney), the term “migration
Reichert’s cartilage especially contributing to the formation fascia” seems unsuitable; “tension-induced fascia” may be
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Fig. 6 Horizontal sections of four female fetuses. All panels dis- connecting between the vagina and rectum (R) in panels B and C
play a level including the inferior end of the vagina (scale bar in each (arrows), while the space is filled with a homogeneous loose tissue in
panel, 1 mm). At the level, the cul-de-sac is seen in a (8 weeks), but d. Scale bar in each panel, 1 mm. LA levator ani muscle, OI obturator
not in b (12 weeks), c (13 weeks) and d (14 weeks). In a and b, a internus muscle, PB pubis, UA umbilical artery, UT ureter, VAS vas
colliculus-like structure is evident at the merging between the ure- deferens
thra (UR) and vagina (VAG). A mesenchymal condensation is seen
better. Fasciae around the viscera seemed to be classified DF. Gender differences in the fibrous architecture of the
into (1) a fusion fascia, (2) a migration fascia and (3) a ten- endopelvic fascia (fascia pelvis parietalis or fascia diaphrag-
sion-induced fascia although the second and third types are matis pelvis superior) have been observed [9]. Likewise,
likely to be overlapped. Tension-induced fasciae are charac- in the DF, the composition as well as the direction of fib-
terized by inter-individual differences because morphology ers is likely to show gender differences. Moreover, because
is dependent on slight differences in topographical anatomy. DF morphology seems to depend on mechanical stress, we
In the rectovaginal septum, i.e., the female DF, elastic hypothesized that individual variations in DF architecture,
fibers are regularly arrayed, with transverse and horizontal such as fragmentary fibrous tissue, multilaminar thin fas-
directed fibers suggesting tensions caused by sexual behav- ciae or solid monolayer fasciae, are likely to occur in the
ior and vaginal delivery [25]. No information is yet availa- pelvic floor of elderly individuals due to benign prostatic
ble, however, on composite fibers and their direction in male hyperplasia and vaginal delivery (Fig. 7). Actually, we had
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Fig. 7 Hypothetical processes
of fetal development and
postnatal changes of Denonvil-
liers’ fascia. At 7 weeks, the
cul-de-sac (stars) of the perito-
neal cavity (PC) is between the
rectum (R) and the urethra (UR)
and vas deferens (VAS). At and
around 15 weeks, the cul-de-sac
disappears and a homogene-
ous mesenchymal tissue fills
a space (asterisks) in front
of the rectum. The presacral
fascia is formed at this stage. In
later stages, mechanical stress
makes Denonvilliers’ fascia
as well as the fascia propria
of the rectum (dotted lines). A
tube-like loose connective tissue
space (i.e., the mesorectum;
asterisks) appears around the
fascia propria: it is delineated
anteriorly by Denonvilliers’
fascia and posteriorly by the
presacral fascia. In the postnatal
life, depending on direction and
strength of mechanical stress
from the surrounding structures,
the fetal Denonvilliers’ fascia is
changed into (1) a solid mon-
olayer, (2) multilayer structure
or, (3) a fragmentary, unclear
fibrous tissue. This scheme can
be adapted to Denonvilliers’
fascia in females when the vas
and prostate are replaced by the
vagina. The adult variations are
based on our unpublished data.
B bladder, PR prostate
a histological data of the DF in 30 adult males: (1) the DF supported by a grant (0620220-1) from the National R&D Program
usually took a multilayer configuration, but (2) it was often for Cancer Control, Ministry of Health & Welfare, Republic of Korea.
fragmented into short pieces, i.e., unclear, or composed of a
Conflict of interest The authors declare that they have no conflict
very thick leaf and the other thin leaves, i.e., a pseudo mon- of interest.
olayer, depending on the sites (data, submitted now). An
extension of the DF to the anterior side of the seminal vesi-
cles [28] seems also to be one of the individual variations. References
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