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Surg Radiol Anat

DOI 10.1007/s00276-014-1336-0

Original Article

Denonvilliers’ fascia revisited


Ji Hyun Kim · Yusuke Kinugasa · Si Eun Hwang ·
Gen Murakami · Jose Francisco Rodríguez‑Vázquez ·
Baik Hwan Cho 

Received: 16 January 2014 / Accepted: 20 June 2014


© Springer-Verlag France 2014

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

J. F. Rodríguez‑Vázquez  Denonvilliers’ fascia (DF), originally termed “aponévrose


Institute of Embryology, Complutense Universidad, Madrid, prostatopéritonéale”, was first described in 1838 [2, 6].
Spain This structure is nearly always present between the pros-
tate or vagina and the fatty tissue around the rectum, i.e.,
B. H. Cho 
Department of Surgery, Chonbuk National University Medical the mesorectum [14, 17, 18, 36]. DF is also sometimes
School, Jeonju, Korea referred to as the rectovesical septum, prostatorectal fascia,
rectogenital fascia, or rectovaginal septum [26, 27, 33]. In
B. H. Cho (*) 
contrast to the male DF, the histological architecture of the
Biomedical Research Institute, Chonbuk National University
Hospital, Deokjin‑gu, Jeonju, Korea rectovaginal septum has been described in detail [25, 37].
e-mail: chobh@jbnu.ac.kr DF in elderly women is often fragmented and unclear; thus,

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Surg Radiol Anat

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).

of the cul-de-sac (Fig. 2e). Although the amount of mate-


rial was limited, we observed no histologic evidence sug- Discussion
gesting that peritoneal fusion occurred at the edge of the
cul-de-sac. This study has shown that, after the disappearance of the
In the other specimens, of GA later than 7 weeks, the cul-de-sac of the peritoneum in front of the rectum at and
peritoneal cavity was not seen in the level behind the pro- around GA 8 weeks, the space between the rectum and
static colliculus (Figs. 1b, c, 3, 4). Moreover, covering by prostate (or vagina) was filled with homogeneous loose
the lowermost part of the peritoneal cavity was limited to tissue [29, 34]. We observed many morphologic character-
the anterior aspect of the rectum; it did not extend to the istics similar to a peritoneal cyst [30] or a remnant of the
lateral aspect (Figs. 3a, 4a). Thus, the typical U-shaped peritoneum, including intermingling among the developing
cul-de-sac was most likely to disappear at GA 8 weeks. nerve plexus, the thin veins and the artifactual space with
At GA 9–10 weeks, the future prostate faced the bottom or without artifactual banding of collagen fibers. However,
of the peritoneal cavity and, even at the level of the future we found no evidence that linearly arranged mesenchymal
prostatic colliculus under the bottom of the peritoneum, cells developed into a definite fascia, although we did not
the prostate and rectum were connected tightly (Fig. 3c). examine late-stage fetuses. Likewise, we found no evidence
This connection was invaded by the developing pelvic of peritoneal fusion at the edge or end of the cul-de-sac.
autonomic plexus. At GA 12–16 weeks, homogeneous Rather, the sac seemed to move or regress upward. There-
and loose mesenchymal tissue was present in front of the fore, our results support the third hypothesis, that fusion
rectum at the level of the colliculus. Although this tissue does not occur and the DF does not originate from the pel-
contained no fascial structures (Figs. 4, 5), we observed an vic cul-de-sac of the peritoneum [29]. A definite DF was
artifactual space with/without artifactual banding of col- shown to be present behind the seminal vesicles in a fetus
lagen fibers (Fig. 4c) and short but linear arrangements of of CRL 191 mm (GA 24 weeks) [7]. Since the fascia pro-
mesenchymal cells possibly due to a type of knife mark pria of the rectum is also established at a late stage [1],
(Fig. 4d). The artifactual space was similar to a cyst, except fetal development of the DF may occur in late-stage fetuses
for the absence of lining cells. Because the urethra and rec- in combination with formation of the fascia propria of the
tum were not straight along the supero-inferior axis, frontal rectum (Fig. 7).
sections also demonstrated mesenchymal tissue between Mechanical stress may be eliminated as a cause of fascia
the colliculus or prostate and the rectum (Fig. 5). Frontal during DF development, although the DF has been reported
sections elongated the space for the DF (Fig. 5b–d) and to be formed by condensation of mesenchymal tissue after
emphasized the homogeneous structure. The longitudinal absorption of the cul-de-sac [34]. The concept of “migra-
smooth muscles of the rectum extended upward and later- tion fascia” postulates that the upward migration of the fetal
ally toward the mesenchymal tissue (Fig. 5a). kidney results in mechanical stress or tension around it,
A junction between the urethra (urogenital sinus) and with the stress inducing linear condensation of mesenchy-
the descending vagina formed a colliculus-like structure mal tissues producing collagen fibers for the future renal
(Fig. 6). Thus, the morphology in females was very similar fascia [8]. In the musculoskeletal system, site-dependent
to that in males, including the prostatic colliculus. We pre- configurations of collagen fibers are dependent on the direc-
viously described this colliculus-like structure in females tion and strength of mechanical stress [11, 19]. In human
[20]. Similar to the developing prostate, the inferior end of fetal development, mechanical stress originates from early
the vagina faced the cul-de-sac at GA 7 weeks (Fig. 6a). developed striated muscles to provide fascial structures,
The mesenchymal tissue between the vagina and rectum as typified in the prevertebral lamina of the deep cervical

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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
Detailed histological studies using specimens from older
1. Arakawa T, Hayashi S, Kinugasa Y, Murakami G, Fujimiya M
individuals are necessary to understand DF morphology by
(2010) Development of the external anal sphincter with special
routine magnetic resonance imaging. reference to inter gender difference: observations of mid-term
fetuses (15–30 weeks of gestation). Okajimas Folia Anat Jpn
Acknowledgments  We are grateful to the families for agreeing 87:49–58. doi:10.2535/ofaj.87.49
to the fetuses and embryos donations for research and education on 2. Charran O, Muhleman M, Shoja MM, Tubbs RS, Loukas M
human anatomy without any economical benefit. This study was (2013) Charles-Pierre Denonvilliers (1808–1872): renowned

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anatomist, plastic surgeons, and influential member of French of the female urethra and descending vagina: a histological
society. Clin Anat 26:788–792. doi:10.1002/ca.22092 study of the early human fetal urethra. Ann Anat 193:500–508.
3. Cuneo B, Veau V (1989) De la signification morphologique des doi:10.1016/j.aanat.2011.03.010
aponeuroses périvésicales. J Anat 35:235–245 21. Matsubara A, Murakami G, Niikura H et al (2009) Develop-
4. Cho BH, Kimura W, Song CH, Fujimiya M, Murakami G ment of the human retroperitoneal fasciae. Cells Tissues Organs
(2009) An investigation of the embryologic development of 190:286–296. doi:10.1159/000209231
the fascia used as the basis for pancreaticoduodenal mobiliza- 22. Miyake N, Hayashi S, Cho BH et al (2010) Fetal anatomy of the
tion. J Hepatobiliary Pancreat Surg 16:824–831. doi:10.1007/ human carotid sheath and structures in and around it. Anat Rec
s00534-009-0126-2 293:438–445. doi:10.1002/ar.21089
5. Cho KH, Lee HS, Katori Y et al (2013) Deep fat of the face revis- 23. Miyake N, Takeuchi T, Cho BH et al (2011) Fetal anatomy of the
ited. Clin Anat 26:347–356. doi:10.1002/ca.22206 lower cervical and upper thoracic fasciae with special reference
6. Dietrich H (1997) Giovanni Domenico Santorini (1681–1737) to the prevertebral fascial structures including the suprapleural
Charles-Pierre Denonvilliers (1808–1872). First description of membrane. Clin Anat 24:607–618. doi:10.1002/ca.21125
urosurgically relevant structures in the small pelvis. Eur Urol 24. Myers RP, Cheville JC, Pawlina W (2010) Making anatomic

32:124–127 terminology of the prostate and contiguous structures clinically
7. Fritsch H, Kühnel W (1992) Development and distribution of adi- useful: historical review and suggestions for revision in the 21st
pose tissue in the human pelvis. Early Hum Dev 28:79–88 century. Clin Anat 23:18–29. doi:10.1002/ca.20895
8. Hayes M (1950) Abdominopelvic fasciae. Am J Anat 87:119–161 25. Nagata I, Murakami G, Furuya K, Koyama M, Ohtuka A (2007)
9. Hirata E, Fujiwara H, Hayashi S et al (2011) Intergender differ- Rectovaginal septum is often thin and interrupted in Japanese
ence in histological architecture of the fascia pelvis parietalis: a elderly women: a histologic study and a recommended surgery to
cadaveric study. Clin Anat 24:469–477. doi:10.1002/ca.21042 repair the weak dorsal vaginal wall. Int Urogynecol J 18:863–868
10. Jeong YJ, Cho BH, Kinugasa Y, Song CH et al (2009) Fetal topo- 26. Raychaudhuri B, Cahill D (2008) Pelvic fascia in urology. Ann R
histology of the mesocolon transversum with special reference to Coll Surg Engl 90:633–637. doi:10.1308/003588408X321611
the fusion with other mesenteries and fasciae. Clin Anat 22:716– 27. Richardson AC (1993) The rectovaginal septum revisited: its rela-
729. doi:10.1002/ca.20846 tionship to rectocele and its importance in rectocele repair. Clin
11. Kjaer M, Langberg H, Heinemeier K et al (2009) From mechani- Obstet Gynecol 36:976–983
cal loading to collagen synthesis, structural changes and func- 28. Secin FP, Karanikolas N, Gopalan A et al (2007) The anterior
tion in human tendon. Scand J Med Sci Sprts 19:500–510. layer of Denonvilliers’ fascia: a common misconception in the
doi:10.1111/j.1600-0838.2009.00986.x laparoscopic prostatectomy literature. J Urol 177:521–525
12. Katori Y, Kwase T, Cho KH et al (2012) Prestyloid compartment 29. Silver OHS (1956) The role of the peritoneum in the formation of
of the parapharyngeal space: a histological study using late-stage the septum recto-vesicale. J Anat 90:538–547
human fetuses. Surg Radiol Anat 34:909–920. doi:10.1007/ 30. Tobin CE, Benjamin JA (1945) Anatomical and surgical restudy
s00276-012-0975-2 of Denonvilliers’s fascia. Surg Gynecol Obstet 80:373–388
13. Katori Y, Kawase T, Cho KH et al (2013) Suprahyoid neck fascial 31. van der Putte SCJ (2005) The development of the perineum in the
configuration, especially in the posterior compartment of the par- human. A comprehensive histological study with a special refer-
apharyngeal space: a histological study using late-stage human ence to the role of the stromal components. Adv Anat Embryol
fetuses. Clin Anat 26:204–212. doi:10.1002/ca.22088 Cell Biol 177:1–131
14. Kinugasa Y, Murakami G, Uchimoto K et al (2006) Operating 32. van Ophoven A, Roth S (1997) The anatomy and embryological
behind Denonvilliers’ fascia for reliable preservation of urogeni- origins of the fascia of Denonvilliers: a medico-histrical debate. J
tal autonomic nerves in total mesorectal excision: a histologic Urol 157:3–9
study using cadaveric specimens, including a surgical experiment 33. Walsh PC (2002) Anatomic radical retropubic prostatectomy.

using fresh cadaveric models. Dis Colon Rectum 49:1024–1032 Cambell’s urology, vol 4, 8th edn. Elsevier Saunders, Amster-
15. Kinugasa Y, Niikura H, Murakami G et al (2008) Development of dam, pp 3107–3130
the human hypogastric nerve sheath with special reference to the 34. Wesson MB (1922) The development and surgical importance
topo histology between the nerve sheath and other prevertebral of the rectourethralis muscle and Denonvilliers’ fascia. J Urol
fascial structures. Clin Anat 21:558–567. doi:10.1002/ca.20654 8:339–359
16. Kinugasa Y, Arakawa T, Abe H et al (2013) Female longitudinal 35. Yang JD, Ishikawa K, Hwang HP et al (2013) Retropancreatic
anal muscles extend into the subcutaneous tissue along the vagi- fascia is absent along the pancreas facing the superior mesenteric
nal vestibule: a histological study using human fetuses. Yonsei artery: a histological study using elderly donated cadavers. Surg
Med J 54:778–784. doi:10.3349/ymj.2013.54.3.778 Radiol Anat 35:403–410. doi:10.1007/s00276-012-1051-7
17. Lin M, Chen W, Huang L, Ni J, Yin L (2010) The anatomy of lat- 36. Zhang C, Ding ZH, Li GX et al (2010) Perirectal fascia and
eral ligament of the rectum and its role in total mesorectal exci- space: annular distribution pattern around the mesorectum. Dis
sion. World J Surg 34:594–598. doi:10.1007/s00268-009-0371-1 Colon Rectum 53:1315–1322. doi:10.1007/DCR.0b013e31
18. Lindsey I, Warren BF, Mortensen NJ (2005) Denonvilliers’ fascia 81e74525
lies anterior to the fascia propria and rectal dissection plane in 37. Zhai LD, Liu J, Li YS, Yuan W, He L (2009) Denonvilliers’ fascia
total mesorectal excision. Dis Colon Rectum 48:37–42 in women and its relationship with the fascia propria of the rec-
19. Mackey AL, Heinemeier KM, Koskinen SOA, Kjaer M (2008) tum examined by successive slices of celloidin-embedded pelvic
Dynamic adaptation of tendon and muscle connective tis- viscera. Dis Colon Rectum 52:1564–1571. doi:10.1007/DCR.0b0
sue to mechanical loading. Connect Tiss Res 49:165–168. 13e3181a8f75c
doi:10.1080/03008200802151672
20. Masumoto H, Rodríguez-Vázquez JF, Verdugo-López S,

Murakami G, Matsubara A (2011) Fetal topographical anatomy

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