On the anatomy and histology of the pubovisceral muscle enthesis in women.
ABSTRACT The origin of the pubovisceral muscle (PVM) from the pubic bone is known to be at elevated risk for injury during difficult vaginal births. We examined the anatomy and histology of its enthesial origin to classify its type and see if it differs from appendicular entheses.
Parasagittal sections of the pubic bone, PVM enthesis, myotendinous junction, and muscle proper were harvested from five female cadavers (51-98 years). Histological sections were prepared with hematoxylin and eosin, Masson's trichrome, and Verhoeff-Van Gieson stains. The type of enthesis was identified according to a published enthesial classification scheme. Quantitative imaging analysis was performed in sampling bands 2 mm apart along the enthesis to determine its cross-sectional area and composition.
The PVM enthesis can be classified as a fibrous enthesis. The PVM muscle fibers terminated in collagenous fibers that insert tangentially onto the periosteum of the pubic bone for the most part. Sharpey's fibers were not observed. In a longitudinal cross-section, the area of the connective tissue and muscle becomes equal approximately 8 mm from the pubic bone.
The PVM originates bilaterally from the pubic bone via fibrous entheses whose collagen fibers arise tangentially from the periosteum of the pubic bone.
- SourceAvailable from: Ghazaleh Rostaminia[Show abstract] [Hide abstract]
ABSTRACT: OBJECTIVE: To determine the muscles comprising the minimal levator hiatus. DESIGN: Cross-sectional study. SETTING: The University of Oklahoma Health Sciences Center, USA. POPULATION: Eight female fresh frozen pelves and 80 nulliparouswomen. METHODS: Three-dimensional endovaginal ultrasound was performed in eight fresh frozen female pelves. The structures of the levator hiatus were tagged with needles and the cadavers were dissected to identify the tagged structures. A group of 80 nullipara underwent 3D endovaginal ultrasound, and the minimal levator hiatus area, puborectalis area, and anorectal angle were assessed, and normal values were obtained. MAIN OUTCOME MEASURES: Anatomic borders of minimal levator hiatus and normality in pelvic floor measurements. RESULTS: The pubococcygeus forms the inner lateral border and anterior attachment of the minimal levator hiatus to the pubic bone. The puboanalis fibres are immediately lateral to pubococcygeus attachments. There are variable contributions of the puborectalis fibres lateral to the puboanalis attachment. The posterior border of the minimal levator hiatus is formed by the levator plate. Eighty community-dwelling nulliparous women underwent 3D endovaginal ultrasound. The median age was 47 years (range 22-70 years). The mean of minimal levator hiatus and puborectalis hiatus areas were 13.4 cm(2) (±1.89 cm(2) SD) and 14.8 cm(2) (±2.16 cm(2) SD). The mean anorectal and levator plate descent angles were 156° (±10.04° SD) and 15.9° (±8.28° SD). CONCLUSION: Anterior and lateral borders of the minimal levator hiatus are formed mostly by pubococcygeus. The puborectalis, pubococcygeus, and iliococcygeus form the bulk of the levator plate.BJOG An International Journal of Obstetrics & Gynaecology 11/2012; · 3.76 Impact Factor
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ABSTRACT: Childbirth causes overstretching of the Levator ani muscle (LAM) predisposing to avulsion. LAM has not been evaluated early postpartum using Endovaginal Ultrasound (EVUS).The aim was to evaluate the relationship between haematomas and LAM avulsion using EVUS and palpation early and late postpartum. Nullipara were studied prospectively at 36 weeks gestation, within four days and three months postpartum. Palpation and high frequency 3D EVUS (BK-Medical 9-16MHz, 360°probe) were performed. Two independent investigators reviewed the scans. No antenatal LAM avulsions were found (n=269). 114/199 (57.3%) seen early postpartum agreed to examination. 27/114 (24%) had well delineated, hypoechoic areas consistent with haematomas (100% agreement); 26 following vaginal delivery, one following emergency caesarean section. In total, 38 haematomas were found (11 bilateral, 16 unilateral). Haematomas away from the LAM attachment zone to the pubic bone (n=22) resolved. Haematomas at the attachment zone (n=16) manifested as pubococcygeus avulsions three months postpartum. In addition to these 16 avulsions, we found another 20 three months postpartum. 13/20 were not scanned early postpartum and in 7 no haematoma but avulsion was seen early postpartum. Overall, LAM avulsion was found in 23/191 (12.0%) women (13 bilateral, 10 unilateral) three months postpartum. Haematomas were significantly associated with episiotomy, instrumental delivery and increased hiatus measurements. Palpation was unreliable early postpartum as only 7 avulsions were diagnosed. Haematomas at the site of LAM attachment to the pubic bone always result in avulsion diagnosed three months postpartum. However, one third of avulsions are not preceded by a haematoma.Ultrasound in Obstetrics and Gynecology 07/2013; · 3.56 Impact Factor
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ABSTRACT: AimsThe levator ani muscle (LA) injury associated with vaginal birth occurs in a characteristic site of injury on the inner surface of the pubic bone to the pubovisceral portion of the levator ani muscle's origin. This study investigated the gross and microscopic anatomy of the pubic origin of the LA in this region.Methods Pubic origin of the levator ani muscle was examined in situ then harvested from nine female cadavers (35–98 years). A combination of targeted feature sampling and sequential sampling was used where each specimen was cut sequentially in approximately 5 mm thick slices apart in the area of known LA injury. Histological sections were stained with Masson's trichrome.ResultsThe pubovisceral origin is transparent and thin as it attaches tangentially to the pubic periosteum, with its morphology changing from medial to lateral regions. Medially, fibers of the thick muscle belly coalesce toward multiple narrow points of bony attachment for individual fascicles. In the central portion there is an aponeurosis and the distance between muscle and periosteum is wider (∼3 mm) than in the medial region. Laterally, the LA fibers attach to the levator arch where the transition from pubovisceral muscle to the iliococcygeal muscle occurs.Conclusions The morphology of the levator ani origin varies from the medial to lateral margin. The medial origin is a rather direct attachment of the muscle, while lateral origin is made through the levator arch. Neurourol. Urodynam. © 2014 Wiley Periodicals, Inc.Neurourology and Urodynamics 08/2014; · 2.67 Impact Factor
Neurourology and Urodynamics 30:1366–1370 (2011)
On the Anatomy and Histology of the Pubovisceral Muscle
Enthesis in Women
Jinyong Kim,1* Rajeev Ramanah,2John O.L. DeLancey,3and James A. Ashton-Miller1
1Biomechanics Research Laboratory, Department of Mechanical Engineering, University of Michigan, Ann Arbor, Michigan
2Department of Obstetrics and Gynecology, University of Besancon Medical Centre, Besancon, France
3Department of Obstetrics and Gynecology, University of Michigan, Ann Arbor, Michigan
Aims: The origin of the pubovisceral muscle (PVM) from the pubic bone is known to be at elevated risk for injury during
enthesial classification scheme. Quantitative imaging analysis was performed in sampling bands 2 mm apart along the
enthesis to determine its cross-sectional area and composition. Results: The PVM enthesis can be classified as a fibrous
enthesis. The PVM muscle fibers terminated in collagenous fibers that insert tangentially onto the periosteum of the pubic
muscle becomes equal approximately 8 mm from the pubic bone. Conclusion: The PVM originates bilaterally from the
pubic bone via fibrous entheses whose collagen fibers arise tangentially from the periosteum of the pubic bone. Neurourol.
Urodynam. 30:1366–1370, 2011.
? 2011 Wiley-Liss, Inc.
Key words: avulsion injury; elastic fiber; enthesis; levator ani; myotendinous junction; pelvic floor dysfunction; pub-
An enthesis is the specialized arrangement of connective tis-
sue that comprises the attachment of a muscle to bone while
permitting the muscle’s fibers to be organized in appropriate
based on the characteristics of the tissue at the bone–tendon
interface. A fibrous enthesis is composed with mainly dense
fibrous connective tissues and can be further divided into two
categories—periosteal and bony, depending on the place to
which the tendon attaches. On the other hand, a fibrocartilagi-
nous enthesis appears in the area which is subject to com-
pression and shows two more additional zones between
connective tissue and bone—uncalcified fibrocartilage and
calcified fibrocartilage. Entheses are often the sites of muscu-
loskeletal overuse injuries that include tennis elbow and
jumper’s knee.1Several different types of entheses have been
in Terminologia Anatomica) nearest its origin from the pubic
bone,6because it is subject to increased risk for injury during
difficult vaginal births.7,8This stretch-related injury, which
occurs during labor, is thought to be due to the PVM having to
the value that striated muscle can withstand without injury in
in causing pelvic organ prolapse, a common female pelvic floor
impairment that is a common cause of surgical treatment later
Several attributes of an enthesis can help protect against
injury at the junction of the three structures having differing
sue, and bone. First, dense embedded fibrous fasciae and/or the
periosteum can help dissipate stress concentrations and
mitigate against the risk of tensile failure or tearing.4Second,
the enthesis can be anchored to the bone via Sharpey’s fibers,
which perforate the superficial lamellae of the bone.2Thirdly,
abrupt increases in load by deforming under load.13Finally,
certain morphological features, such as a flaring near the bone,
could systematically reduce high tensile stresses and/or strains
However, to our knowledge the literature contains no descrip-
tions of the morphology or histology of the PVM enthesis.
The first goal of this paper, therefore, was to classify the PVM
second goal was to test the hypothesis that one or more of the
above stress-reduction mechanisms would be observed in the
MATERIALS AND METHODS
Five female cadavers were dissected to examine the detailed
morphology and histology of the origin of the PVM at the pubic
Conflicts of interest: Dr. DeLancey and Dr. Ashton-Miller are consultants for
from American Medical Systems and Kimberly-Clark. The other authors have no
disclosures to report.
Dirk De Ridder led the review process.
This study was presented at the 31st American Urogynecologic Society Annual
Scientific Meeting, Long Beach, California, USA, September 2010.
Grant sponsor: National Institutes of Health Office of Research on Women’s Health
(ORWH); Grant sponsor: Specialized Center of Research (SCOR) on Sex and Gender
Factors Affecting Women’s Health; Grant Numbers: P50 HD044406.
*Correspondence to: Jinyong Kim, M.S., E-mail: firstname.lastname@example.org
Received 6 August 2010; Accepted 18 October 2010
Published online 12 May 2011 in Wiley Online Library
? 2011 Wiley-Liss, Inc.
years old (mean 77 years). All the specimens appeared to be
parous from inspection of the perineal body and cervix when
present. None showed signs of pelvic floor muscle damage
omist with experience in evaluating the levator ani muscle
(JOLD). Characteristics such as the detailed morphological and
structural relationships around the PVM and its attachment
area, and the specific fiber orientation and connection of the
PVM enthesis were examined before the pubic bones and the
where PVM injury is known to occur7,14,15was determined by
visual inspection, using magnification when necessary.
Smaller samples were removed for histochemical processing
were fixed in 10% neutral buffered formalin, decalcified in 10%
was then applied followed by serial sectioning of samples less
ing to standard procedures for selected slides for analyzing
CA) and a Super COOLSCAN 5000 ED film scanner (Nikon,
Shinjuku, Tokyo, Japan) were used to convert the slides into
For the quantitative observation, custom designed software
written in Matlab (The MathWorks, Natick, MA) was developed
to allow the interactive selection of the quadrangular sampling
2 mm intervals, resulting in 6–7 sampled locations depending
upon the length of the enthesis in each sample. The location
where no muscle was present was defined as the origin of the
measurement. At each location, bands with 1 mm width were
placed perpendicular to the PVM line-of-action and used to
collect pixel image information in the sampling bands. Color-
based segmentation using the k-means clustering technique
was applied to the trichrome digital images of the specimens
to distinguish the muscle (stained in red) from the connective
tissue (stained in blue). Descriptive statistics were generated as
mean and SD.
with its encompassing structures. The striated PVM muscle
fibers mainly insert tangentially onto the periosteum of the
superior pubic rami and the posteroinferior margin of the body
linking the PVM to the pubic bone ranges from tens of
micrometers to a few millimeters (Fig. 3c). The PVM is bounded
and dorsal surfaces until each merges with the periosteum
5–10 mm apart. No flaring of the PVM enthesis was observed
Fig. 1. View looking down towards the left pelvic sidewall showing the
location of the PVM enthesis (PVMe, below bracket). SPRL, superior pelvic
ramus (left); PS, pubic symphysis.
Fig. 2. a: Lateral view of a parasagittal section through a female cadaveric pelvis for orientation. The rectangular
box shows an area that includes the pubic bone and the origin of the pubovisceral muscle on which detailed
histological and quantitative analyses were performed. b: The pubovisceral muscle origin showing the sampling
bands (dashed quadrangles) at six different locations along the pubovisceral muscle, where color-based segmen-
tation was conducted (Masson’s trichrome stain, scale bar ¼ 2 mm). [Note: this specimen is from a different
cadaver from that shown in (a)] c: After the image filtered by color, the pre-defined sampling bands were quanti-
tatively analyzed to compute unit area and relative composition of the collagenous tissue (blue; top image) and
the muscle (red, bottom image). In this and the following images, PVM, pubovisceral muscle; OIM, obturator
internus muscle; PB, pubic bone; B, bladder; U, uterus; V, vagina.
Pubovisceral Muscle Origin Histology
Neurourology and Urodynamics DOI 10.1002/nau
to thearcus tendineusfascia pelvis, passinglateral to thetendi-
that of the PVM.
enthesis rather than a fibrocartilaginous enthesis, because nei-
ther the fibrocartilaginous zone nor the tidemark—a basophilic
line separating the fibrocartilage into the calcified zone and the
uncalcified zone—was present. The PVM attaches to the pubic
bone at an acute angle. While the superficial layer of the
penetration of the deeper collagen through the periosteum
directly to the pubic bone was not seen. The thickness of the
be different than elsewhere on the pubic bone. No Sharpey’s
the enthesial region.
Figure 4 demonstrates the change in composition of the
muscle fibers and the connective tissue in the PVM in the
sampling quadrangles. Moving from the muscle towards the
bone, the unit area occupied by the muscle fibers gradually
shows a lesser change than the muscle fiber does. It is notable
Fig. 4. Longitudinal distribution of the muscle and the connective tissue at
the sampling bands along the PVM from its origin. Values are mean (bars
indicate SD) areas within the 1-mm wide sampling bands taken normal to
the line-of-action of the PVM. The table shows the composition of the
muscle in each location. The unit area of the muscle matches that of the
connective tissue at a point approximately 8 mm (location 5) from the
pubic bone origin.
Fig. 3. Two examples of entheses. a: Right parasagittal section through the
PVM origin on the pubic bone 2–3 cm from the midline taken from the
superior pubic ramus area. The PVM emanates tangentially from the pubic
bone and the OIM lies caudally to the PVM and also originates from the PB
with its fiber direction being perpendicular to that of the PVM (Masson’s
trichrome stain, scale bars ¼ 2 mm). b: Another parasagittal section
through the PVM origin on the pubic bone 1–2 cm from the midline. Note
the varied morphology of the pubic bone due to different harvesting
locations as well as different cadaveric samples (Masson’s trichrome stain,
scale bars ¼ 2 mm). c: Higher magnification view of the PVM origin in (b)
showing the enthesis. The collagenous fibers from the PVM blend in with
the periosteum of the PB, and can sometimes be seen to insert on irregular-
ities on the surface of the PB. Notice the absence of Sharpey’s fibers pene-
trating into the bone, and the presence of the periosteum. The vertical dark
lines in the PB are artifacts due to tissue folding during the microtome sec-
tioning. Also note that the image is slightly rotated counterclockwise
(Masson’s trichrome stain, Scale bar ¼ 0.3 mm). d: Myo-tendinous junction
(arrow) of the PVM (green) and the collagenous tissue (red), (Verhoeff-Van
Gieson stain, scale bar ¼ 20 mm). SF, superior fascia of pelvic diaphragm;
PER, periosteum; COL, collagenous fibers; MUS, muscle fibers.
Kim et al.
Neurourology and Urodynamics DOI 10.1002/nau
that the areas of the connective tissue and the muscle become
from about 2% at the origin to approximately 60% at the last
Figure 5 shows the myotendinous junction stained with
Verhoeff-Van Gieson staining method, which renders elastic
The current study has shown that the PVM is attached to the
pubic bone by short collagenous fibers, the proximal ending of
the fibrocartilaginous zones and the tidemark. Quantitative
analysis demonstrates that the proportion of muscular tissue
becomes equal to that of the connective tissue at location 5
about 8 mm away from the osteotendinous junction. Neither
flaring of the enthesis at the muscle–bone interface nor
region. Therefore, the hypothesis that flaring and Sharpey’s
fibers form an important part of its structure was rejected.
Finally, elastic fibers appear to be distributed along the
findings of our research extends earlier studies on the PVM and
cal features of the levator hiatus including the PVM have been
demonstrated with the help of magnetic resonance as well as
three-dimensional ultrasound.6,8Thesestudies showthe lossof
muscle that occurs after vaginal birth; however, they lack the
connection to the bone. The present study is more concerned
with the nature of the normal muscle’s origin with a view to
The PVM enthesis arises tangentially from the periosteum of
in the manner of the insertion of the pronator teres on the mid-
structure and function,3,4the absence of the tidemark and the
fibrocartilaginous zones in the PVM enthesis might mean that
tensional loading rather than compressive loading is predom-
inantin thisarea.This makessenseconsidering thatthePVM is
There is growing knowledge concerning injury to the portion
of the levator ani muscle that is attached to the pubis. Avulsion
injury is associated with the development of pelvic organ pro-
nature of the levator ani damage itself may not be the only
distortion,’’ which may be defined as a characteristic abnormal
is associated with an increased occurrence of pelvic organ pro-
lapse compared to women who have muscle injury but no dis-
tortion.19Itis possible that the architectural distortion signifies
are responsible for pelvic organ support, become defective or
These elements are interconnected to each other by the perios-
teum of the pelvis, the arcus tendineus fascia pelvis, the arcus
structures is affected by abnormal external loading, the input
work can be transmitted to others.
sample size is modest and the samples were likely parous indi-
viduals who, although not having any distortion or injury to a
trained eye, might have some changes secondary to birth.
Therefore, the results of the present study might have affected
by this possible histological changes consequent upon vaginal
but young nulliparous cadavers are so rare in anatomical
donation programs as to prevent analysis of more than one or
individuals. Thirdly, more detailed histological descriptions are
lar enthesis.20Fourthly, considering the size of elastic fibers
being in the order of a few micrometers, observation through
images of these elastic fibers along the collagenous tissue.
injury during the second stage of labor occurs.8,21The details of
the exact injury mechanism have not yet been fully elucidated.
This research provides a detailed picture of the structural basis
for the attachment of the muscle to the bone and suggests
hypotheses helpful in predicting that failure location. It seems
before the cross-sectional area of the enthesis becomes big
Fig. 5. a: Elastic fibers (stained in black, arrowhead) are sparsely distributed
in a fibrillar form along the collagenous fibers (red; Verhoeff-Van Gieson
stain, scale bar ¼ 0.3 mm). b: Higher power view of the boxed region in
(a) showing the elastic fibers in more detail (Verhoeff-Van Gieson stain,
scale bar ¼ 50 mm).
Pubovisceral Muscle Origin Histology
Neurourology and Urodynamics DOI 10.1002/nau
stretch-related injuries than muscle, because they are highly
aligned in the enthesis. Now that the anatomical details of this
our growing understanding. For example, one can use the
ical models of the PVM enthesis and explore the effect of the
enthesis on this injury-prone region. This work may also be
extended and compared to the connective tissue attachment
of the levator ani muscle along the pelvic sidewall.
The pubovisceral portion of the levator ani muscle originates
tangentially from the pubic bone through fibrous entheses.
Collagenous fibers, which lie between the PVM and the pubic
bone and connect each other, mainly arise from theperiosteum
the connective tissue and muscular tissue becomes equal at
approximately 8 mm from the pubic bone.
We would like to thank the histology core facility at the
University of Michigan, School of Dentistry for the histological
services. Digital conversion of the slides was performed in the
Cell & Developmental Biology and the Virtual Microscopy
Facility, Department of Pathology at the University of
Michigan with the assistance of Shelley Almburg and Ronald
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Kim et al.
Neurourology and Urodynamics DOI 10.1002/nau