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REVIEW

CURRENT
OPINION Female pelvic floor biomechanics: bridging the gap
Deanna C. Easley a, Steven D. Abramowitch a, and Pamela A. Moalli b

Purpose of review
The pelvic floor is a complex assembly of connective tissues and striated muscles that simultaneously
counteracts gravitational forces, inertial forces, and intra-abdominal pressures while maintaining the
position of the pelvic organs. In 30% of women, injury or failure of the pelvic floor results in pelvic organ
prolapse. Surgical treatments have high recurrence rates, due, in part, to a limited understanding of
physiologic loading conditions. It is critical to apply biomechanics to help elucidate how altered loading
conditions of the pelvis contribute to the development of pelvic organ prolapse and to define surgeries to
restore normal support.
Recent findings
Evidence suggests the ewe is a potential animal model for studying vaginal properties and that uterosacral
and cardinal ligaments experience significant creep, which may be affecting surgical outcomes. A new
method of measuring ligament displacements in vivo was developed, and finite element models that simulate
urethral support, pelvic floor dynamics, and the impact of episiotomies on the pelvic floor were studied.
Summary
The current review highlights some contributions over the past year, including mechanical testing and the
creation of models, which are used to understand pelvic floor changes with loading and the impact of
surgical procedures, to illustrate how biomechanics is being utilized.
Keywords
ex-vivo mechanics, finite element analysis, pelvic floor biomechanics

INTRODUCTION interventions. With the ultimate goal of effectively


The pelvic floor consists of a complex and highly preventing and treating POP, defining the loading
interdependent network of connective tissues and conditions of the pelvis over the female lifespan is
&&

muscles designed to counteract gravitational forces, paramount [9 ].


inertial forces, and intra-abdominal pressures while In the last decade, progress has been made regard-
&&
providing support to the pelvic organs [1 ,2]. When ing the mechanical characterization of the vagina,
this network is compromised, pelvic floor disorders bladder, urethra, rectum, cervix, uterus, connective
&&

(PFDs) can occur including pelvic organ prolapse tissues, and musculature of the pelvic floor [10 ].
(POP). However, some of the greatest remaining challenges
Approximately 30% of all women experience stem from the ethical issues surrounding procure-
some degree of POP during their lifetime. Vaginal ment of human tissues, in significant quantities, that
parity incurs the greatest risk; however, age, span the average 35-year time gap between maternal
maternal birth injury, chronic straining, and obesity birth injury and the onset of symptoms for
& &&
& &
are also risk factors [3 ,4 ]. Roughly 12.6% of women POP [11 ,12 ]. Thus, researchers have begun to
will seek surgical treatment for their symptoms, and
of those who elect a native tissue repair, an esti-
a
mated 40% will experience a reoccurrence within 2 Department of Bioengineering and bDepartment of Obstetrics, Gyne-
cology, and Reproductive Sciences, School of Medicine, University of
years [5,6]. Although synthetic meshes have been
Pittsburgh, Pittsburgh, Pennsylvania, USA
widely adopted to improve surgical outcomes over
Correspondence to Pamela A. Moalli, MD, PhD, Associate Professor,
native tissue repairs, meshes have also been associ- Division of Urogynecology and Reconstructive Pelvic Surgery, Director of
ated with higher than expected recurrence rates Fellowship in Urogynecology and Female Pelvic Medicine, University of
[7,8]. As the pelvic floor comprises the primary load Pittsburgh, Pittsburgh, Pennsylvania, USA. Tel: +1 412 641 6052;
bearing structure of the pelvic organs, it has become fax: +1 412 641 5290; e-mail: pmoalli@mail.magee.edu
increasingly clear that mechanics contributes to Curr Opin Urol 2017, 27:262–267
the onset of prolapse and the failure of surgical DOI:10.1097/MOU.0000000000000380

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Female pelvic floor biomechanics Easley et al.

&&
as a change in mechanics [12 ]. Alternatively, non-
KEY POINTS human primates are more likely to demonstrate
 Additional animal models should be considered differences in mechanical properties between the
with care. nulliparous and parous groups, similar to humans,
&&
but are expensive and are a limited resource [12 ].
 Despite the challenges, more robust mechanical tests Thus, investigators study other animal models with
(i.e., creep and biaxial tests) should be considered to
the hope of finding a model that incurs birth injury
help further elucidate the mechanical properties of the &&

pelvic floor. and is less expensive to maintain. Knight et al. [12 ]


investigated the uniaxial mechanical properties,
 More accurate mechanical data and geometric models collagen content, and collagen structure of the
can be combined to create mathematical finite element nulliparous and parous Dorset ewe and found that
models that can further help predict and understand
the ewe could serve as a possible animal model
pelvic floor disorders.
alternative.
Similar to humans and nonhuman primates,
parity incurs dramatic decreases in both the tangent
implement cross-disciplinary techniques to help modulus (a measure of material stiffness) and tensile
bridge the gap. Urogynecology is shifting toward strength of the vagina in the ewe. The vagina of
computational methods, in which the results of the nulliparous ewe becomes more compliant with
mechanical, biochemical, and histological tests are parity [i.e., decreased tangent modulus: 27.0  11.5–
used as inputs to complex mathematical models. The 12.8  6.6 MPa (P < 0.025)]. This suggests that
future of this field is in recognizing that a diverse set understanding the mechanisms by which delivery
of factors contribute to the function and dysfunction negatively impacts vaginal mechanics may be ascer-
of the pelvic floor and that the application of bio- tained through the ewe. Moreover, the parity status
mechanics can help establish more specific research of nonhuman primates tends to be considerably
questions and identify paths that can lead to provable higher than the ewe, raising questions for further
findings versus conjectures based on anecdotes. investigation, such as determining the mechanical
The current review highlights developments impact of single versus multiple births, with the
over the past year, ranging from ex-vivo mechanical hypothesis that an increase in parity will decrease
testing to complex finite element models, illustrat- mechanical properties [14].
ing how the field has progressed at bridging knowl- Although mechanical outcomes are comparable
edge between the known and unknown. between the nonhuman primate and the ewe, there
are significant anatomical differences. The vagina is
an intra-abdominal organ in the ewe (as opposed
EXPERIMENTAL MECHANICS to retroperitoneal in humans and nonhuman
Although no animal is a perfect model for humans, primates), meaning that the in-vivo conditions
nonhuman primates, rodents, and swine are fre- are likely drastically different from nonhuman
quently used to study pelvic floor biomechanics primates and humans. Although further investi-
[13]. Their use depends on the research question gation is necessary to determine if the ewe is a
of interest. Previous work established a basic mech- reliable animal model for pelvic floor biomechanics,
anical understanding of the vagina, pelvic muscles, the strength in this initial outcome is that the same
and supportive connective tissues using animal mechanical testing protocols from the same labora-
models, and this work has progressed with a few tory were used for the animal models, allowing for a
recent developments that will be reviewed. reliable cross-species comparison.

VAGINAL PROPERTIES UTEROSACRAL LIGAMENT COMPLEX


Parity is acknowledged as a leading risk factor in the Of the connective tissues that provide support to the
development of POP, and the rodent and nonhu- vagina, the uterosacral ligament (USL) complex,
man primate are two animal models that are used to which supports the upper vagina (apex) and cervix,
&& &
study the mechanical impact of parity. Although has been most studied [10 ,15,16 ]. Restoration
rodents are relatively inexpensive and homogenous of apical support to the vagina is, indeed, key in
within breeds, they have small pup sizes and are less achieving successful anatomical outcomes in the
likely to spontaneously incur birth injuries during long term, and approximately 50% of what is
delivery. This presents challenges in observing observed as anterior prolapse is due to loss of sup-
differences between nulliparous and parous groups port at the apex [17–19]. In addition, addressing
with respect to maternal injuries that may manifest apical support at the time of hysterectomy for POP

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Pelvic health

reduces recurrence and reoperation rates [20]. Char- organs and hence, surgical management employ
acterizing the mechanical properties of the USL and forces that are at least 40 times greater than the
its interdependency with other pelvic floor suppor- force required, possibly leading clinicians to per-
tive structures will enhance our understanding of form more aggressive procedures that are unwar-
normal support, effective treatments, and surgical ranted. The magnitude of the forces experienced
procedures. may not be as significant in contributing to failure
Previously, the mechanical properties of the USL as not providing any support to the appropriate
were studied in primates, cadavers, and swine [21– locations. Studies such as this demonstrate that
25]. It was found that the tensile properties of the MRI combined with mechanics can hold a wealth
USL/cardinal ligaments are variable in all species, of information and that this approach can be
depending on the location with respect to the applied to improve our understanding the pelvic
vagina, uterus, and cervix. In the swine, the USL/ floor.
cardinal ligament complex was stiffer in the primary Experiments such as those described in this
physiological loading direction (vagina to sacrum). section provide insight into how these tissues
It was also noted that the preferential orientation of behave from a mechanical standpoint and provide
fibers was congruent with this in-vivo loading direc- important first approximations that can serve as
tion. This is similar to work by Tan et al. [15], who inputs into computational models to formulate
this past year determined the microstructural and new questions and refine our notions of what is
mechanical properties of the USL/cardinal ligament plausible versus what is not.
complex in the swine. The USL/cardinal ligament
specimens experienced large deformations and sig-
nificant biaxial creep (continued increases in stretch COMPUTATIONAL MECHANICS: FINITE
when held at a constant force) in over a 2-h period. ELEMENT MODELING
The largest differences, although NS, were seen in Finite element analysis is a method that determines
the amount that the tissue deformed along the main approximate solutions to complex problems by
loading direction of the USL/cardinal ligament ver- breaking them into smaller interconnected pieces
sus perpendicular to the main direction in response (elements) for which the mathematics is tractable.
to small forces, with the latter direction demonstrat- Strengths include the ability to approximate
ing slightly more. solutions to problems that cannot be tested physi-
Overall, this study demonstrated that the cally due to budgetary, ethical, or practical con-
connective tissues supporting the vagina display straints. However, major weaknesses are that
significant viscoelastic behaviors, indicating that solutions are only as good as the assumptions and
the mechanical properties change on the basis of inputs used to develop the model. Thus, answers
how much time the tissue has experienced loading. that look reasonable and clinically plausible could
Understanding these, time-dependent mechanical be incorrect and subject to unconscious biases. Find-
properties are important in understanding the ings must be validated and verified before establish-
contribution of these tissues during events such ing them as truth. In the field of pelvic floor
as gestation, labor, and delivery, as well as identify- mechanics, our understanding of the inputs (e.g.,
ing reconstruction materials that display similar properties of tissues) and validity of the assumptions
behaviors [15]. (e.g., how tissues interact) are rudimentary, at best.
An in-vivo imaging approach is an alternative Thus, clinicians should interpret models with cau-
experimental approach to improve our understand- tion and question model assumptions. Nevertheless,
ing of the USL/cardinal ligament complex. Forces on the introduction of finite element modeling to Uro-
the USL/cardinal ligament complex can be approxi- gynecology has been monumental. Researchers are
mated by observing the displacement of the uterus able to recreate and test a number of scenarios
in dynamic stress MRI, in which it is allowed to related to POP, such as vaginal birth, maternal
displace physiologically. Recent work found that muscle and connective tissue injury with vaginal
&&
only 90 g of traction force is required to match birth, and the impact of repetitive strain [27 ]. Most
the uterine displacement visualized in MRI, models used to date, however, are patient-specific
suggesting that valsalva is not a significant physio- (based on a single patient), so the interpretation of
&&
logical movement [26 ]. The finding also indicates findings as they relate to broad populations of indi-
&&
that there may be additional factors to consider viduals should always be questioned [28 ].
other than the USL/cardinal ligament supports One of the most anatomically complete pelvic
when trying to understand the positioning of the models to date contains 44 different structures,
uterus. Furthermore, the tests that are performed based on a 21-year-old healthy patient. This model
clinically to define displacement of the pelvic was developed to determine the role of individual

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Female pelvic floor biomechanics Easley et al.

&&
structures on urethral support [27 ]. Uniformly Finite element modeling can also be applied to
distributed pressures were applied to the model to understand circumstances surrounding delivery and
simulate a maximal strain maneuver. As a first step birth injury, one of the primary risk factors for the
toward validating the model, gross behaviors were eventual development of POP. The episiotomy, an
compared with dynamic MRI images of a strain incision into the perineal body to facilitate delivery,
maneuver. It was found that the vaginal wall, pubor- was previously one of the most common surgical
ectalis muscle, and pubococcygeus muscle were piv- procedures performed in the United States. How-
otal in providing urethral support. When these ever, the benefits versus maternal risks have come
factors were simulated as weakened, they produced into question. Now, clinicians only perform episiot-
large urethral excursion angles of 20.1, 19.4, and omies when complications necessitate an expedited
18.8 degrees, respectively. Simulations weakening delivery. As damage to pelvic floor muscles is a
the levator muscles led to angles of more than leading risk factor in the later development of PFDs,
30 degrees. In contrast, weakening the illiococcy- it is crucial that we understand how the episiotomy
geus, piriformis, coccygeus, and obturator internus procedure impacts the pelvic floor during normal
produced angles that were less than 17 degrees. In delivery [30]. To address this problem, a finite
addition, this study identified patterns of pelvic element model of the medial lateral episiotomy
floor deformation, through changing combinations was simulated during passage of a fetal head
&&
of weakened muscles, that could be further explored [31 ]. The investigators then quantified damage
in future studies. within the model for both normal and episiot-
The same model was used to study the dynamics omy-assisted deliveries. They found that both con-
&&
of the pelvic floor during athletic activities [29 ]. A ditions resulted in an increase in quantified damage
jump landing was simulated on the basis of exper- in the pubovisceral muscle; however, the episiot-
imental accelerometer data collected from individ- omy appeared to reduce the extent of the damage.
uals. First, the model demonstrated two distinct Although this study provides valuable information
types of pelvic floor deformations that occur during showing that an episiotomy can be protective to
a jump. The first deformation can be described as a surrounding tissues, the degree to which it is protec-
‘leaning forward compression’, in which the bladder tive still needs to be further investigated as this model
is pressed against the pubic bone and stretched in becomes more refined. Overall, the damage caused by
the anteroposterior direction. Following this move- performing the episiotomy needs to be balanced with
ment, the bladder ‘bounces back’. The data demon- its potential to protect the pubovisceral muscle from
strates that this activity differs significantly from a damage to minimize future risk for POP.
maximal strain maneuver, suggesting that it may It is well known that the outcome of surgical
not be the best method to detect Stress Urinary procedures to repair POP are in part due to the
Incontinence (SUI) clinically in female athletes. unique parameters of each patient, in addition to
Instead, the model suggests that pelvic floor defor- surgical practices, including but not limited to the
mation, and not urethral hypermobility, is more approach and type of materials used for repair.
&&
important in predicting SUI. Jeanditgautier et al. [32 ] investigated how the size
In a separate study, finite element modeling was of a simulated mesh impacted mobility of pelvic
used to simulate varying degrees of bladder fullness organs in an abdominal sacrocolpopexy procedure.
(from 0 to 100%) to determine effects on the Consistent with mechanical principles, it was found
anterior vaginal wall. Mechanical strain (a measure that larger meshes decreased the mobility of the
of how much the tissue deformed) was reported as pelvic organs. Indeed, increasing the amount of
four times as high at 100% bladder fill when com- mesh in contact with the vagina increased support
pared with 10% bladder fill. Thus, a bladder fill of at and decreased pelvic organ descent. In addition, it
least 60% is recommended to assess anterior vaginal was observed that the suture attachments to the
prolapse. When vaginal stiffening increases, stress vaginal apex were a site of high-stress concen-
(force per unit area of tissue) was distributed more trations as the total force of the mesh was transferred
regionally throughout the anterior vaginal wall; to the vagina over the small area in which the suture
however, the peak stress value (1.98  0.05 MPa) was placed. This stress can be more evenly distrib-
changed minimally. These simulations suggest that uted by placing more sutures, which is also consist-
measuring pressures in a clinical setting may not ent with basic mechanical principles. In this
provide an adequate indication of deterioration of simulation, the number of sutures had little effect
the anterior vaginal wall. This demonstrates that on the mobility of the pelvic organs, suggesting
there may be a role for diagnostic and compu- more is likely better. It should be noted, however,
tational models to be used in conjunction with that this study does not factor in the biological
&&
clinical measurements to improve clinical care [9 ]. response to suture or increased mesh burden. Thus,

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Pelvic health

7. Nygaard I, Brubaker L, Zyczynski HM, et al. Long-term outcomes following


this study provides strong support for a research abdominal sacrocolpopexy for pelvic organ prolapse. JAMA 2013; 309:
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CONCLUSION 9. Chanda A, Unnikrishnan V, Richter HE, Lockhart ME. A biofidelic computa-
&& tional model of the female pelvic system to understand effect of bladder fill and
Although there are still many questions that need to progressive vaginal tissue stiffening due to prolapse on anterior vaginal wall.
Int J Numer Method Biomed Eng 2016; 1–16.
be addressed, significant progress has been achieved This article uses finite element modeling to simulate varying levels of bladder fill and
over the past year with respect to pelvic floor bio- anterior vaginal prolapse in an effort to understand the mechanical impact on the
anterior vaginal wall.
mechanics. Some of the challenges and hurdles 10. Baah-Dwomoh A, McGuire J, Tan T, De Vita R. Mechanical properties of
associated with this field of research are being && female reproductive organs and supporting connective tissues: a review of the
current state of knowledge. Appl Mech Rev 2016; 68:60801.
approached with innovative solutions that explore This review article provides an in-depth review of all literature that characterize the
new animal models, apply mechanical tests that have mechanical properties of pelvic organs, muscles, and connective tissues.
11. Alperin M, Kaddis T, Pichika R, et al. Pregnancy-induced adaptations in
been successful in other fields, and quantify medical & intramuscular extracellular matrix of rat pelvic floor muscles. Am J Obstet
diagnostic images in ways that lay the groundwork Gynecol 2016; 215:210.e1–210.e7.
This article utilizes a rat model to investigate how pregnancy impacts the intra-
for clinically relevant care. Furthermore, the field is muscular extracellular matrix with respect to its mechanical and biochemical
creating models that are helping to reveal mechan- properties.
12. Knight KM, Moalli PA, Nolfi A, et al. Impact of parity on ewe vaginal mechanical
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Knight et al. investigate the uniaxial mechanical properties, collagen content, and
surgical treatments and prevention measures. collagen structure of the nulliparous and parous Dorset ewe.
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Conflicts of interest between mouse, rat, and human pelvic ligaments to determine if mouse and rat are
There are no conflicts of interest. appropriate animal models.
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Female pelvic floor biomechanics Easley et al.

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