You are on page 1of 17

Journal of the Mechanical Behavior of Biomedical Materials 74 (2017) 411–427

Contents lists available at ScienceDirect

Journal of the Mechanical Behavior of


Biomedical Materials
journal homepage: www.elsevier.com/locate/jmbbm

Mechanical properties of the abdominal wall and biomaterials utilized for MARK
hernia repair

Corey R. Deekena, Spencer P. Lakeb,
a
Covalent Bio, LLC, St. Louis, MO, USA
b
Department of Mechanical Engineering & Materials Science, Washington University in St. Louis, MO, USA

A R T I C L E I N F O A B S T R A C T

Keywords: Abdominal wall hernias are one of the most common and long-standing surgical applications for biomaterials
Abdominal wall engineering. Yet, despite over 50 years of standard use of hernia repair materials, revision surgery is still
Anisotropy required in nearly one third of patients due to hernia recurrence. To date, hernia mesh designs have focused on
Biomaterials maximizing tensile strength to prevent structural failure of the implant. However, most recurrences occur at the
Hernia repair
biomaterial-tissue interface. There is a fundamental gap in understanding the degree to which a mechanical
Mechanics
mismatch between hernia repair materials and host tissue contributes to failure at this interface. This review
Mesh
summarizes the current literature related to the anatomy and mechanics of both human and animal abdominal
wall tissues, as well as the mechanical properties of many commonly-utilized hernia repair materials. The studies
reviewed here reported greater compliance of the linea alba, larger strains for the intact abdominal wall, and
greater stiffness for the rectus sheath and umbilical fascia when the tissues were loaded in the longitudinal
direction compared to transverse. Additionally, greater stresses were observed in the linea alba when loaded in
the transverse direction compared to longitudinal. Given these trends, a few recommendations can be made
regarding orientation of mesh. The most compliant axis of the biomaterial should be oriented in the cranio-
caudal (longitudinal) direction, and the strongest axis of the biomaterial should be oriented in the medial-lateral
(transverse) direction. The human abdominal wall is also anisotropic, with anisotropy ratios as high as 8–9
reported for the human linea alba. Current biomaterial designs exhibit anisotropy ratios in the range of 1–3, and
it is unclear whether an ideal ratio exists for optimal match between mesh and tissue. This is likely dependent on
implantation location as the linea alba, rectus sheath, and other tissues of the abdominal wall exhibit different
characteristics. Given the number of unknowns yet to be addressed by studies of the human abdominal wall, it is
unlikely that any single biomaterial design currently encompasses all of the ideal features identified. More data
on the mechanical properties of the abdominal wall will be needed to establish a full set of guidelines for ideal
mesh mechanics including strength, compliance, anisotropy, nonlinearity and hysteresis.

1. Introduction revision surgery in nearly one in three patients, at a substantial cost to


the patient in the form of pain, disability, time off work, and procedural
Hernias are a debilitating and common condition, affecting over 1 costs (Poulose et al., 2012; Burger et al., 2004).
million Americans each year (Poulose et al., 2012). Surgical repair of Thus far, hernia mesh designs have focused primarily on maximiz-
ventral hernias comes at a tremendous cost of over $3.2 billion/year ing tensile strength to prevent structural failure of the implant.
and comprises more than 350,000 surgeries annually in the United However, the vast majority of hernia recurrences occur at the im-
States alone making this one of the most common procedures in all of plant-tissue interface rather than from mechanical failure of the mesh
general surgery (Poulose et al., 2012; Rutkow, 2003). The introduction material. Factors affecting integration at the interface such as insuffi-
of mesh materials to reinforce hernia repairs has improved surgical cient mesh-defect overlap (Langer et al., 2001; Cobb et al., 2009; Zuvela
outcomes. However, pain, infection, and recurrence are still common et al., 2014; Petro et al., 2015), failure to close the anterior myofascial
(Burger et al., 2004; Klosterhalfen et al., 2002; Klosterhalfen and layer (Langer et al., 2001; Cobb et al., 2009; Zuvela et al., 2014; Petro
Klinge, 2013; Cavallo et al., 2015). Hernia recurrence alone leads to et al., 2015), migration/damage from fixation devices (Petro et al.,


Correspondence to: Mechanical Engineering & Materials Science, Biomedical Engineering and Orthopaedic Surgery, Washington University in St. Louis, Campus Box 1185, USA, One
Brookings Drive, St. Louis, MO 63130, USA.
E-mail addresses: deekenc@covalentbiollc.com (C.R. Deeken), lake.s@seas.wustl.edu (S.P. Lake).

http://dx.doi.org/10.1016/j.jmbbm.2017.05.008
Received 24 February 2017; Received in revised form 26 April 2017; Accepted 4 May 2017
Available online 06 May 2017
1751-6161/ © 2017 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/BY/4.0/).
C.R. Deeken, S.P. Lake Journal of the Mechanical Behavior of Biomedical Materials 74 (2017) 411–427

2015; Lerdsirisopon et al., 2011), contracture of the wound mental difficulties in quantifying the mechanics of the composite
(Klosterhalfen et al., 2002; Klinge et al., 1998), poor tissue ingrowth structure, individual layers, and their connections/interactions, and
(Klosterhalfen et al., 2002; Klosterhalfen and Klinge, 2013; Cavallo (3) the complex in vivo loading environment of the abdomen where the
et al., 2015), or sustained inflammatory response (Klosterhalfen et al., abdominal wall regularly supports multiaxial physiologic loads during
2002; Klosterhalfen and Klinge, 2013; Cavallo et al., 2015; Klinge et al., normal function.
1999) have all been reported to contribute to the high incidence of Furthermore, specific layers often exhibit unique and complex
hernia recurrence. Surprisingly, the degree to which mechanical compositional and structural properties, which further challenge efforts
mismatch between biomaterial and host tissue contributes to failure to characterize these tissues and fully describe their properties. For
has not been evaluated, even though the primary purpose for utilizing example, the linea alba, a midline band of connective tissue that
biomaterials in hernia repair is mechanical support and integration separates the two parallel portions of the rectus abdominis muscle, has
with the native tissue. As a first step towards properly matching the been described as a highly structured, three-dimensional meshwork
mechanics of these structures, the full mechanical properties of composed predominantly of type I collagen. In addition to exhibiting
abdominal tissues and biomaterials used in hernia repair need to be location-specific width and thickness (increasing/decreasing in the
quantitatively described and compared. This review paper will address cranio-caudal direction, respectively), the linea alba has several zones
this topic, summarizing the current literature related to the anatomy throughout its thickness that exhibit distinct structural properties (Axer
and mechanics of both human and animal abdominal wall tissues, as et al., 2001). Specifically, from ventral to dorsal, the linea alba exhibits
well as the mechanical properties of many commonly-utilized hernia sequential layers of intermingling oblique fibers, predominantly trans-
repair materials. verse fibers, and variable small irregular fibers (Grabel et al., 2005). In
addition to this intricate collagenous organization, elastic fibers have
also been shown to form an interdigitating layer perpendicular to
2. Human abdominal wall collagen bundles in human and porcine linea alba, and are hypothe-
sized to contribute to the mechanical properties of this tissue (e.g.,
2.1. Anatomy and structure of the human abdominal wall elastic recoil) (Levillain et al., 2016). Similar to the linea alba, other
tissues of the abdominal wall also exhibit variable and unique structural
The human abdominal wall is a complex composite structure organization profiles, which likely correlate directly with mechanical
composed of various layers which vary depending on specific anato- properties and function, but which complicate mechanical analysis of
mical location (e.g., medial/lateral, above/below the arcuate line). The individual or composite abdominal tissues. The first sections of this
central abdominal wall is composed, from superficial to deep, of the paper will summarize experimental studies to date that have measured
following layers: skin, subcutaneous fat, anterior rectus sheath, rectus mechanical properties of specific tissue layers or whole abdominal
abdominis muscle or linea alba (depending on location), posterior walls, of humans and animals, and provide an overview of theoretical
rectus sheath (if above the arcuate line), preperitoneal fat, and and computational models that have been developed to further
peritoneum ((Kalaba et al., 2016); Fig. 1). In locations lateral to the represent and understand fundamental concepts relative to abdominal
central line, the rectus abdominis is replaced by a muscle layer wall mechanics.
composed of the external oblique, internal oblique, and transversalis
abdominis muscles. Several collagenous connective tissues (e.g., fascias, 2.2. Mechanical properties of the human abdominal wall
sheaths, linea alba) integrate the various layers into a functioning
composite structure. 2.2.1. Mechanical evaluation of individual components of the human
Some of the primary roles of the abdominal wall are mechanical in abdomen
nature: provide a mechanical barrier to protect internal organs, support Several studies have investigated the mechanical properties of
the intra-abdominal pressures (IAPs) that develop within the abdominal specific isolated layers of the abdominal wall structure (Table 1). We
cavity, and provide/facilitate motion and mobility of the torso. Hernias note that studies in the literature have used a wide range of different
represent a breakdown or disruption in the continuity of the abdominal measures and parameters to report mechanical properties of abdominal
wall, which (among other complicating issues) impair the mechanical tissues, which can make interpretation and direct comparison challen-
function of this composite tissue. To fully address such clinical issues, it ging. A few of the more common terms merit definition: stiffness is the
is first necessary to understand how the healthy intact abdominal wall slope of the force-elongation curve, modulus is the slope of the stress-
performs its mechanical function. Namely, what are the mechanical strain curve, compliance is the inverse of modulus (or amount of strain
properties of each of the different layers of the abdominal wall and how per given stress), deformation is the change in length or shape, and
do they function together to provide necessary mechanical support and strain is the deformation normalized by original geometry (i.e., length
strength? Answers to such questions are challenging due to (1) the or area).
heterogeneous anatomical configuration of the abdominal wall, where Uniaxial tensile tests of the linea alba in longitudinal (cranio-
specific layers of the composite tissue vary by location, (2) experi- caudal) and transverse (medial-lateral) directions showed anisotropic
properties; higher compliance in the longitudinal direction correlated
well with reported descriptions of microstructural collagen fiber
alignment (Grabel et al., 2005). Transverse stresses in the linea alba
have been reported to be 2–3 times larger than longitudinal stresses
(Levillain et al., 2016; Hollinsky and Sandberg, 2007; Forstemann et al.,
2011), while a study using biaxial tensile testing reported a much larger
anisotropy ratio of 8–9 (Cooney et al., 2016). One study found that
mechanics of the linea alba were significantly stronger (~30%) than
scar tissue (Hollinsky and Sandberg, 2007), which provides some
insight into heightened susceptibility to incisional hernia development
following surgical access through the linea alba (Muysoms et al., 2015).
A recent study reported non-linear viscoelastic anisotropic properties of
human linea alba and showed non-uniform realignment of collagen
Fig. 1. Schematic showing the various layers of the human abdominal wall (reprinted fibers in different layers under load, demonstrating the complex nature
with permission from Kalaba et al. (2016)). of this connective tissue (Levillain et al., 2016).

412
Table 1
Mechanical test data of human abdominal tissues (MOD = elastic modulus; UTS = ultimate tensile strength; IR = infrared; abd = abdominal).

Number of Mean Age Male Test Method Transverse Longitudinal Oblique Parallel to Perpendicular to Anisotropy Refs.
Donors (range) (Female) fibers fibers
C.R. Deeken, S.P. Lake

Individual Linea alba 60 Uniaxial ~70 kPa MOD ~8 kPa MOD ~8.2 (Forstemann et al.,
Layers Biaxial via simple ~80 kPa MOD ~32 kPa MOD ~2.5 2011)
model
31 (63–95) 16 (15) Uniaxial 0.6 cm/N 1.2 cm/N compliance 2.0 (Grabel et al.,
compliance 2005)
66 77 (17–94) 30 (36) Uniaxial ~9.2 MPa UTS ~4.3 MPa UTS ~2.1 (Hollinsky and
Sandberg, 2007)
3 86 Uniaxial 1.15 MPa stress at 0.5 MPa stress at ~2.3 (Levillain et al.,
stretch = 1.4 stretch = 1.4 2016)
13 > 60 6 (7) Uniaxial 72 MPa MOD 8 MPa MOD 9.0 (Cooney et al.,
Biaxial 335 MPa MOD 23 MPa MOD 14.5 2016)
Anterior rectus 3 78 (74–85) 1 (2) Uniaxial 5.6 MPa (slow) (Ben Abdelounis
sheath 14 MPa (fast) et al., 2013)
66 77 (17–94) 30 (36) Uniaxial ~8.3 MPa UTS 3.4 MPa UTS ~2.4 (Hollinsky and
Sandberg, 2007)
12 46 (18–65) 0 (12) Uniaxial 12.8 MPa UTS 3.4 MPa UTS 3.8 (Martins et al.,
30.3 MPa 10.1 MPa MOD 2012)
MOD
30 83 (62–95) 14 (16) Uniaxial & burst 4.9 MPa UTS (supra- (Rath et al., 1997)
strength arcuate); 7.5 MPa
UTS (infra-arcuate)
Posteror rectus 30 83 (62–95) 14 (16) Uniaxial & burst 6.1 MPa UTS (supra- (Rath et al., 1997)
sheath strength umbilical); 6.5 MPa
UTS (infra-umbilical)

413
66 77 (17–94) 30 (36) Uniaxial ~5.3 MPa UTS ~2.0 MPa UTS ~2.6 (Hollinsky and
Sandberg, 2007)
Umbilical fascia 14 66.5 9 (5) Uniaxial ~9.3 MPa ~2.9 MPa MOD 3.2 (Kirilova et al.,
(46–87) MOD 2011)
Transversalis 14 66.5 9 (5) Uniaxial ~8.9 MPa ~3.0 MPa MOD 3.0 (Kirilova et al.,
fascia (46–87) MOD 2011)
20 hernia 4 19 (1) Uniaxial ~1.5 MPa UTS; ~0.7 MPa UTS; 2.0 (Kureshi et al.,
control ~3.0 MPa MOD ~1.5 MPa MOD 2008)
Rectus 12 45 (17–73) 7 (5) Uniaxial 0.52 MPa (Cardoso, 2012)
abdominis MOD
Transversus 12 45 (17–73) 7 (5) Uniaxial 1.03 MPa (Cardoso, 2012)
abdominis MOD
External oblique 12 45 (17–73) 7 (5) Uniaxial 1.00 MPa (Cardoso, 2012)
MOD
Internal oblique 12 45 (17–73) 7 (5) Uniaxial 0.65 MPa (Cardoso, 2012)
MOD

Composite Ex vivo abd wall 14 68 (48–86) 7 (5) Octagonal tensile ~16% strain ~27% strain ~12% strain (Junge et al.,
Layers test rig 2001)
7 82 (66–97) 3 (4) Linea alba forces ~40–50 N/cm (Konerding et al.,
tension at 200 mbar 2011)
6 76 (66–84) 4 (2) Internal vs external 2.6% int strain at 3.7% int strain at ~5.5% strain 1.4 (Podwojewski
strains 50 mm Hg; 5.0% ext 50 mm Hg; 6.6% ext at 50 mm Hg 1.3 et al., 2014)
strain at 50 mm Hg strain at 50 mm Hg
8 (77–98) 4 (4) 3D imaging/ ~0% strain at 3 kPa ~2.5% strain at (Tran et al., 2014)
elastography pressure 3 kPa pressure
In vivo 41 mesh 58 (37–77) 36 (5) 3D stereography 3.1 cm height; (Muller et al.,
68.6 cm max radius 1998)
21 control 38 (25–52) 12 (9) 5.5 cm height;
41 cm max radius
Journal of the Mechanical Behavior of Biomedical Materials 74 (2017) 411–427

(continued on next page)


C.R. Deeken, S.P. Lake Journal of the Mechanical Behavior of Biomedical Materials 74 (2017) 411–427

(Tran et al., 2016)


Early evaluation of the anterior and posterior rectus sheath used

(Smietanski et al.,
2006a, 2006b)
dynamometer and burst strength testing to quantify the failure proper-
(Welty et al.,

(Song et al.,
ties of this thin tissue, which surprisingly did not correlate with age, sex
2001) or body build (Rath et al., 1997). Subsequent testing has shown non-

2012)
Refs.

linear and anisotropic mechanical properties (stiffer in longitudinal


direction), greater stability for anterior than posterior rectus sheath,
and a rate-dependent response with greater elasticity at faster rates of
Anisotropy

cyclic loading (Hollinsky and Sandberg, 2007; Martins et al., 2012; Ben
Abdelounis et al., 2013). Consistently, the influence of aging, obesity,
and parity on the mechanics of the rectus sheath again could not be
demonstrated (Martins et al., 2012), however such lack of statistical
Perpendicular to

correlation may be influenced by limited sample numbers. Another thin


connective tissue of the human abdomen is the umbilical fascia, an
internal layer that attaches laterally to the deep layers of the rectus
fibers

sheath and helps protect against umbilical hernias (Oh et al., 2008;
Fathi et al., 2012). Studies of mechanics of the umbilical fascia reported
a non-linear viscoelastic response, similar to the rectus sheath (Kirilova
Parallel to

et al., 2011; Kirilova, 2012). Orthogonal tensile tests of fascia from


different anatomical locations showed relatively homogeneous me-
fibers

chanics (in contrast to the rectus sheath) but significant anisotropy,


where longitudinal samples showed larger mechanical parameters (e.g.,
~3X stiffer), longer relaxation times, and greater dependence on strain
elongation

than transverse samples (Kirilova et al., 2011, 2009; Kirilova, 2012).


Oblique

The transversalis fascia was also evaluated mechanically in uniaxial


20%

tension and was shown to exhibit anisotropy ratios of 2–3, depending


on whether test sample orientation was based on anatomical or collagen
~7 kPa shear MOD

fiber alignment axes (Kirilova et al., 2011; Kureshi et al., 2008).


19.4% elongation

~0.7–0.8 N/mm
resting stiffness
22.5 kPa MOD

Regarding the musculature of the abdominal wall, very few studies


Longitudinal

have examined the mechanics of isolated muscle layers from the human
abdomen. This may be due to experimental challenges, foremost of
which is the inability to evaluate active muscle properties of cadaveric
human muscle tissues; thus, experiments on human tissue have relied
~20 kPa shear MOD

solely on passive characterization. One set of experiments evaluated the


2.5–4.4 cm height

resting stiffness

rectus abdominis, transversus abdominis, external oblique and internal


42.5 kPa MOD

~0.5–1 N/mm
Transverse

oblique muscles using uniaxial and biaxial testing (Cardoso, 2012). A


elongation
5.2–9.4%

few of the interesting results within this large dataset were that (1) the
evaluated muscles were more compliant than abdominal fascia, (2) the
transversus abdominis sustained the largest stress, while the rectus
abdominis supported the lowest stress, and (3) muscles from male
3D stereography

Non-invasive IR

donors exhibited stiffer passive properties than tissues from female


Test Method

3D imaging/
elastography

donors. The dataset wasn’t sufficiently powered to detect significant


3D imaging
imaging

correlations between mechanics and age, sex, or body mass index


(BMI).

2.2.2. Mechanical evaluation of the intact human abdominal wall


(Female)

158 (77)

Since the layers of the abdominal wall do not function in isolation in


Male

9 (9)

6 (2)

8 (3)

the physiological environment, but rather as part of an integrated


composite structure, various studies have examined the mechanical
Mean Age

behavior of the intact abdominal wall (Table 1). Such studies typically
(23–35)

(40–62)
(range)

fall into one of two types of approaches: ex vivo testing of cadaveric


48.5

abdomens or non-invasive evaluation of the abdominal motion of living


56

subjects. We now summarize previous work using these two ap-


Number of

235 mesh

proaches.
Donors

A number of different experimental techniques have been devised to


18

11

evaluate the mechanics of the intact human abdominal wall. Junge


8

et al. (2001) developed a sophisticated multidirectional test configura-


tion with eight actuators arranged in a circular pattern; using this setup,
displacements in different directions were measured at various levels of
applied force. At a reference load of 16 N, the largest strains were found
in the cranio-caudal (~27% average), followed by medial-lateral
Table 1 (continued)

(~16%), and then oblique directions (~12%), with female abdomens


exhibiting increased compliance compared to males. Another experi-
mental approach utilized balloon-insufflation of the abdomen and
sutured gauges in the linea alba to measure forces in the abdominal
wall as a function of IAP (Konerding et al., 2011). This study reported a
nearly-linear increase in force vs. pressure, with a maximum of

414
C.R. Deeken, S.P. Lake Journal of the Mechanical Behavior of Biomedical Materials 74 (2017) 411–427

~40–50 N/cm at 200 mbar IAP. Consistent with other studies, trans- yielded valuable information describing the mechanical properties of
verse tensile forces in linea alba did not correlate with donor demo- human abdominal tissues. However, even with extensive and sophisti-
graphics (e.g., weight, height, BMI). A recent study simultaneously cated experimental analyses, not all aspects of biomechanical para-
evaluated strains on the internal and external surfaces of excised human meters within a given system can be realized solely with experimental
abdominal walls subjected to varying amounts of air pressure for three investigations. In addition, acquisition of human cadaveric tissue can be
different states: intact, incised (i.e., simulated hernia), and repaired challenging and expensive. Thus, some research efforts have focused on
(Podwojewski et al., 2014). Strains on the external surface were developing models to further elucidate structure-function properties of
homogeneous while strain maps on the internal surface appeared to the human abdomen and enable predictions of biomechanical behavior
relate to heterogeneities of the underlying anatomy. Interestingly, under other loading scenarios.
external surface strains were 2X larger than internal surface strains, To overcome difficulties in acquiring and handling human cadaveric
suggesting that predictions of internal strains deduced from measure- tissues, a few studies have developed synthetic model systems to
ments acquired of the external abdominal wall may not be reliable. explore tissue-level relationships (e.g., microstructural organization
Finally, one study utilized an ex vivo experimental setup to test full- and mechanical function) and evaluate surgical procedures (e.g.,
thickness abdominal walls at different pressures after a series of suturing techniques) that are relevant for abdominal tissues and hernia
sequential dissections to determine the relative degree to which specific repair. One such study created rubber-cotton composite materials by
tissues contribute mechanically (Tran et al., 2014). Consistent with adding cotton fibers to a latex rubber-oil composite (van Os et al.,
studies of individual wall layers, this study reported larger strains in the 2006). After evaluating a variety of different formulations, the authors
longitudinal direction compared to transverse (particularly for poster- designed a composite material with a specific mixture of latex rubber,
ior rectus sheath and linea alba), and results also demonstrated the oil (cis-cis linoleic acid) and eight layers of cotton thread in an ordered
relative mechanical importance of the anterior rectus sheath within the stacking sequence that yielded mechanical properties highly similar to
composite abdominal wall. the human linea alba. Another study created an in vitro model system
Several studies over the past twenty years have devised approaches with synthetic mesh and elastomeric matrix to represent an explanted
to measure motion/deformation of the abdominal wall in human mesh-tissue composite (Rohrnbauer and Mazza, 2013). Mechanical test
subjects using non-invasive means. The first published technique used results from uniaxial tensile tests and biaxial ball inflation tests showed
a three-dimensional (3D) stereography technique wherein a light grid that the composite material was different from dry mesh or elastomer
was projected on subjects’ abdomens and images captured at different alone, and was able to closely approximate the response of explanted
stages of respiration were analyzed to extract measurements of mesh-tissue composites from animal tests. While these studies rely on
abdominal wall motion based on how the light grid deformed between several simplifications and approximations, they offer potentially
paired images (Klinge et al., 1998). This technique showed reduced effective tools to characterize the properties of abdominal tissue and/
abdominal wall mobility/compliance for patients with a mesh-aided or meshes in physiologically relevant environments.
hernia repair compared to healthy controls, but no difference in the The majority of modeling studies of the human abdominal wall have
state of the abdominal wall at rest between these two groups (Muller sought to develop theoretical or computational approaches based on
et al., 1998). The 3D stereography technique was also used to measure experimental data that are capable of yielding novel insights and/or
the relative motion of abdominal walls of patients after surgical repair enabling predictive simulations. One model used segmented magnetic
with one of three different meshes of varying weights (Welty et al., resonance imaging (MRI) slices of a patient's torso and a large set of
2001). In this study, all meshes increased abdominal wall stiffness experimental tests of the linear alba to develop a 3D-contour model of
relative to control; since stiffness increased with increasing mesh the abdominal wall (Forstemann et al., 2011). In addition to computing
weight, the authors suggested that reducing the amount of mesh average biaxial radii of curvature (transverse = 201 mm; longitudingal
material used in hernia repair would be beneficial. Taking a different = 470 mm), this study also computed a relationship between IAP and
approach, Song et al. (2006a, 2006b) developed a non-invasive infrared plane states of stress and found, among other results, that stresses were
(IR) camera imaging system to measure in vivo elasticity of the 2X greater in the transverse compared to longitudinal direction.
abdominal wall during laparoscopic surgery. For this technique, a Another study utilized a hyperelastic, fiber-reinforced, almost-incom-
three-camera IR system tracked the 3D position of twelve markers pressible constitutive model to compute abdominal wall displacements
attached to the patient's abdominal wall at different IAPs. Results for IAPs corresponding to specific activities (standing, standing cough,
showed that the initial cylindrical shape of the abdomen became more jump) (Pachera et al., 2016). This model represented a significant
dome-like during insufflation, with most shape change occurring in the advancement as it included nonlinear anisotropy of abdominal tissues
sagittal plane (demonstrating an anisotropic response). Overall average and considered the mechanical state at large strains, both of which are
expansion was ~15–20% at 12 mm Hg IAP, with male patients often neglected in soft tissue modeling. Both of these studies were
exhibiting a slightly stiffer response. A similar approach used a two- formulated for the intact (non-herniated) abdominal wall, yet modeling
camera system to track a grid of markers on the external surface of the approaches also offer a useful tool for considering mechanical function
abdominal wall of healthy subjects to determine elongations during following injury and surgical repair.
three different torso motions: rotations to both sides, leaning to both A signficant amount of work on computational modeling of hernia-
sides, and leaning forwards/backwards (Smietanski et al., 2012). repaired abdominal walls has been completed by Hernandez-Gascon,
Although reported measurements in this study include some very large Calvo and colleagues. Using finite element (FE) models of the abdomen
(perhaps unrealistic) elongations, overall results suggest that strong with one of three synthetic meshes, this group found that surgical repair
mesh fixation should be used in hernia repair to accommodate large does not restore normal physiological conditions in the abdominal wall
abdominal wall deformations. A recent study utilized a four-camera (Hernandez-Gascon et al., 2011). Results of a follow-up study indicated
system to track abdominal surface markers combined with shear wave that post-repair mechancial function depends on the orientation of the
ultrasound elastography during four typical physiological activities implanted mesh, and that anisotropic meshes need to be positioned
(Tran et al., 2016). While this technique offers exciting potential, the with the most compliant axis of the mesh positioned along the cranio-
large coefficients of variation and lack of repeatability in this study caudal (i.e., longitudinal) direction (Hernandez-Gascon et al., 2013). A
suggest that further refinement of this technique is warranted. subsequent iteration of this model utilized a large deformation aniso-
tropic hyperelastic formulation and was the first model to define
2.3. Mechanical modeling of the human abdomen realistic geometry of the entire human abdomen (obtained from full
torso MRI) including different anatomical structures to simulate passive
The experimental studies outlined in the previous section have mechanical behavior under different physiological loads (Hernandez-

415
C.R. Deeken, S.P. Lake

Table 2
Mechanical testing data for animal abdominal tissues (MOD = elastic modulus; UTS = ultimate tensile strength; int = internal; ext = external; obl = oblique; trans = transversus; abd = abdominal or abdominis).

Species Number of Age or Sex Test method Transverse Longitudinal Parallel to fibers Perpendicular to Aniotropy Ref.
animals Weight fibers

Individual Linea alba Pig 20 26–28 weeks mixed Uniaxial 61 MPa MOD 7 MPa MOD 8.7 (Cooney et al., 2015)
Layers Biaxial 240 MPa MOD 30 MPa MOD 8
Pig 4 4 months Uniaxial 2.1 MPa stress at 0.85 MPa stress at ~2.5 (Levillain et al.,
stretch = 1.4 stretch = 1.4 2016)
Anterior rectus Pig 20 26–28 weeks mixed Uniaxial ~80 MPa MOD ~8 MPa MOD ~10 (Lyons et al., 2014)
sheath Biaxial ~130 MPa MOD ~25 MPa MOD ~5.2
Rat 18 450–510 g male Uniaxial 49 N/cm MOD 2.2 N/cm MOD ~22 (Anurov et al., 2012)
Posterior rectus Rat 18 450–510 g male Uniaxial 18.5 N/cm MOD 2.0 N/cm MOD ~9.3 (Anurov et al., 2012)
sheath
Rectus abdominis Rabbit 7 2150 g male Uniaxial ~6.5 MPa MOD (Hernandez et al.,
2011)
Transversus Dog 11 15–23 kg Uniaxial/ ~10 MPa MOD ~75 MPa MOD ~0.1 (Hwang et al., 1985)

416
abdominis Biaxial
External oblique Rabbit 7 2150 g male Uniaxial ~13.3 MPa MOD ~2 MPa MOD ~6.6 (Hernandez et al.,
2011)
Internal oblique Rat 7 250–300 g male Uniaxial 0.41 N/mm stiffness (DuBay et al., 2007)
0.17 MPa max stress
Dog 11 15–23 kg Uniaxial/ ~15 MPa MOD ~35 MPa MOD ~0.4 (Hwang et al., 1985)
Biaxial

Composite Ex vivo whole abd Pig 6 4–5 months female int vs ext 5.3% int principal strain (Podwojewski et al.,
Layers wall strains 13.7% ext principal strain 2013)
Ext Obl; Int Obl; Rabbit 7 2150 g male Uniaxial ~4.7 MPa MOD ~1.4 MPa MOD ~3.4 (Hernandez et al.,
Trans Abd 2011)
Ext Obl; Int Obl ~5.7 MPa MOD ~1.35 MPa MOD ~4.2
Int Obl; Trans Abd ~1.1 MPa MOD ~0.7 MPa MOD ~1.6
In vivo intact abd Rabbit 4 2–2.3 kg Tracked 3.0–22.4% strain 1.3–8.7% strain at (Simon-Allue et al.,
wall surface at 12 mm Hg 12 mm Hg 2015)
markers
Journal of the Mechanical Behavior of Biomedical Materials 74 (2017) 411–427
C.R. Deeken, S.P. Lake Journal of the Mechanical Behavior of Biomedical Materials 74 (2017) 411–427

Gascon et al., 2013). When used to evaluate the mechanical response to 3. Animal abdominal walls
different activities (e.g., Valsalva maneuver, standing cough, jumping),
this model demonstrated that the stiffest tissues, particularly the linea 3.1. Mechanical properties of animal abdominal walls
alba, are the most important structures that contribute to mechanical
stability of the abdominal wall. Most recently, this FE model was used Animal models offer a variety of advantages for evaluating the
to examine the immediate post-repair response using hernia meshes of mechanical environment and function of the abdominal wall. For
different sizes (Simon-Allue et al., 2016a). When evaluating IAP example, animal studies provide: (1) the ability to conduct studies that
magnitudes corresponding to a jumping motion, the meshes showed are not possible in humans, (2) greater control over experimental
varying wall displacements, thereby demonstrating that the mechanical design (e.g., age, time-points, injury state), (3) greater consistency
match of mesh to tissue is an important consideration that influences across different animals than is possible within human cohorts, and (4)
post-operative deformation. Lastly, this group compared two simple lower costs. Although several inherent limitations reduce the degree to
theoretical models, namely a beam model and a membrane model, each which animal results can be translated directly to human care (e.g.,
with a different balance of precision and computational expense different mechanical loading between bipeds and quadrupeds), the
(Hernandez-Gascon et al., 2014). Consistent with the more complex advantages of such approaches have led several investigators to use
FE formulations, these models showed that the distribution of stresses is animal models to examine fundamental concepts in abdominal wall
modified when a surgical mesh is placed in a healthy abdominal wall mechanics. A summary of these studies is provided in the subsequent
and that surgical repair does not restore normal physiological condi- sections and in Table 2.
tions. In the future, extending these models to include simulations of
tissue remodeling may yield insights into the long-term behavior of the 3.1.1. Mechanical evaluation of individual components of animal abdomens
abdominal wall following mesh implantation. A number of animal species have been utilized to quantify the
One other group developed mathematical models of post-hernia mechanical properties of individual layers of the abdominal wall. A
repair abdominal tissues with mesh implants (Lubowiecka, 2013a, study that examined the rectus sheath of Wistar rats found similar
2013b). These studies used a membrane-based model to consider the results to human tissue, namely that anterior rectus sheath was much
connection points between implanted mesh and host tissue and to stronger than posterior sheath and that both sheaths exhibited larger
examine the effect of mesh placement and orientation on mechanical moduli in transverse loading compared to longitudinal (Anurov et al.,
response. These studies showed that optimal mesh orientation is highly 2012). Another study utilized Sprague-Dawley rats to investigate the
dependent on hernia location and demonstrated that validated model effect of hernia on a specific muscle response (DuBay et al., 2007). In
simulations can estimate the repair persistance of meshes placed in this study, internal oblique muscles from herniated abdominal walls
varying orientations. showed changes similar to those seen in mechanically-unloaded
muscles, specifically pathologic fibrosis, disuse atrophy, and muscle
fiber changes, which led to decreased compliance of the abdominal
2.4. Limitations of previous studies of human abdominal wall mechanics wall.
In a rabbit model, the transversus abdominis and rectus abdominis
The studies summarized in the previous sections have yielded were isolated and tested using uniaxial longitudinal and transverse
significant insight regarding the mechanical properties and function tensile tests; results were compared to tests of composite samples of
of individual layers of the human abdomen as well as the intact multiple muscle layers (Hernandez et al., 2011). Mechanical anisotropy
abdominal wall. However, results of these studies should be considered was greater for separated muscles than any composite tissue testing and
in the context of a number of limitations and approximations. For collagen was found to be responsible for passive mechanical strength of
experimental ex vivo studies, limiting issues include: (1) the use of different layers. Among abdominal muscles in the rabbit, the external
previously frozen human specimens without considering the effects of oblique was stiffer in the transverse direction than longitudinal, while
freezing on the measured mechanical response, (2) issues of dehydra- the internal oblique was stiffer in longitudinal than transverse; con-
tion and rigor mortis in sample preparation, (3) the evaluation of sidered together, these contrasting results help explain the more
cadaver tissues from aged donors, which may not approximate the isotropic response for composite samples. More recently, a study
mechanical response of younger tissues, (4) variable test conditions evaluated the active properties of individual muscles and multi-layered
(e.g., fixturing technique, loading rate, strain/stress/tension levels muscle composites from the rabbit abdomen (Grasa et al., 2016). Using
evaluated) making comparisons across studies difficult, and (5) the experimental analysis and computational simulations, this study eval-
inherent issue that ex vivo post-mortem testing may not adequately uated how directions of muscle and collagen fibers in each layer
replicate the in vivo physiologic loading environment. For the in vivo contribute to active muscle contraction force. Importantly, this appears
experiments, several of the issues inherent in ex vivo testing are not to be the first study to evaluate active muscle properties in considering
applicable, however such studies are impacted by other limitations. abdominal wall mechanics; more work in this area is desperately
Primary among these concerns is that these studies often measure needed. As such measurements are difficult in human tissues, animal
abdominal wall motion on the external skin surface, which may not studies provide a useful tool for future investigations.
approximate deformations occuring at the level of hernia-related tissue Several studies have evaluated tissues from porcine abdomens. In
disruption or location of implanted mesh during hernia repair uniaxial and biaxial tensile testing of the linea alba, the transverse
(Podwojewski et al., 2014). Other potential issues for non-invasive in direction was shown to be ~8x stiffer than the longitudinal direction,
vivo studies are the limited validation of experimental techniques and such that deformation occured predominantly in the longitudinal
variability across different subjects, making it difficult to draw broad direction (Cooney et al., 2015). Compared to their previous data of
conclusions from study results. Finally, mathematical and computa- human linea alba tested using similar protocols (Cooney et al., 2016),
tional modeling studies are often limited by flawed assumptions (e.g., this group found no significant differences for uniaxial data and
isotropic properties of tissues, uniform thickness of wall or layers, linear transverse biaxial loading, and only slight differences in biaxial long-
mechanical properties) and the lack of experimental data to properly itudinal response between porcine and human tissues. Other studies
motivate mathematical representations of physical phenomena (e.g., have also reported anisotropic behavior of the porcine linea alba, but
interactions between layers of the abdominal wall). Many areas of not to the same degree; an analysis of a small number of animals
opportunity remain to further elucidate the mechanical properties and showed a ratio of ~2.5 for transverse-longitudinal stress (Levillain
behavior of the human abdominal wall. et al., 2016). Another study compared the properties of porcine and
human linea alba tested in uniaxial tension and reported non-linear

417
C.R. Deeken, S.P. Lake Journal of the Mechanical Behavior of Biomedical Materials 74 (2017) 411–427

Table 3
Permanent synthetic biomaterials for hernia repair applications.

Bare Barriers & Coatings Reinforced

3D Max (Bard/Davol Inc.)a Permanent Resorbable Fibers


3D Max Light (Bard/Davol Inc.)a SERAMESH PA (Serag Wiessner)
Bard Mesh (Bard/Davol Inc.) Permanent Barrier, Non-Composite ULTRAPRO Hernia System (Ethicon Inc.)a
Bard Soft Mesh (Bard/Davol Inc.) CRURASOFT Patch (Bard/Davol Inc.) ULTRAPRO Mesh (Ethicon Inc.)
DynaMesh-CICAT (FEG Textiltechnik mbH) DUALMESH Biomaterial (W.L. Gore & Assoc. Inc.) ULTRAPRO Plug (Ethicon Inc.)a
DynaMesh-ENDOLAP (FEG Textiltechnik mbH) DUALMESH PLUS Biomaterial (W.L. Gore & Assoc. Inc.) VYPRO Mesh (Ethicon Inc.)
DynaMesh-IPOM (FEG Textiltechnik mbH) DULEX Mesh (Bard/Davol Inc.) VYPRO II Mesh (Ethicon Inc.)
DynaMesh-Lichtenstein (FEG Textiltechnik mbH) MYCROMESH Biomaterial (W.L. Gore & Assoc. Inc.)
DynaMesh-PP Light (FEG Textiltechnik mbH) MYCROMESH PLUS Biomaterial (W.L. Gore & Assoc. Inc.)
DynaMesh-PP Standard (FEG Textiltechnik mbH) Reconix Reconstruction Patch (Bard/Davol Inc)
EASY PLUG PATCH SYSTEM (Apside/BG Medical)a
Freedom Octomesh (Insightra Medical) Permanent Barrier, Composite
INFINIT Mesh (W.L. Gore & Assoc. Inc.) Composix (Bard/Davol Inc.)
Kugel Patch/Modified Kugel Patch (Bard/Davol Inc.) Composix E (Bard/Davol Inc.)
Marlex (Bard/Davol Inc.) Composix E/X (Bard/Davol Inc.)
MERSILENE Mesh (Ethicon Inc.) Composix Kugel Patch (Bard/Davol Inc.)
MK Hernia Patch (Bard/Davol Inc.) Composix L/P (Bard/Davol Inc.)
MotifMesh (Proxy Biomedical) CK Parastomal Hernia Patch (Bard/Davol Inc.)
Omyra Mesh (B Braun) SURGIMESH XB (Apside/BG Medical)
Optilene Mesh (B Braun) VENTRALEX Hernia Patch (Bard/Davol Inc.)
Optilene Mesh Elastic (B Braun) VENTRIO Hernia Patch (Bard/Davol Inc.)
Optilene Mesh LP (B Braun)
Optilene Mesh Plug (B Braun) Permanent Coating
Parietene (Covidien) TIMESH Extralight (Biomet Biologics/GfE Med. GmbH)
Parietex Anatomic Mesh (Covidien) TIMESH Light (Biomet Biologics/GfE Med. GmbH)
Parietex Flat Sheet 2D Weave (TEC) Mesh (Covidien) TIMESH Strong (Biomet Biologics/GfE Med. GmbH)
Parietex Flat Sheet 3D Weave (TET) Mesh (Covidien)
Parietex Folding Mesh (Covidien) Resorbable
Parietex Easegrip Mesh (Covidien)
Parietex Lightweight Monofilament Polyester Mesh (Covidien) Resorbable Barrier, Composite
Parietex ProGrip Self-Fixating Mesh (Covidien) Adhesix (Cousin Biotech)
Parietex Plug and Patch System (Covidien)a C-QUR Mesh (Atrium Medical Corp.)
PerFix Light Plug (Bard/Davol Inc.)a C-Qur Mosaic Mesh (Atrium Medical Corp.)
PerFix Plug (Bard/Davol Inc.)a C-QUR TacShield (Atrium Medical Corp.)
Polysoft Hernia Patch (Bard/Davol Inc.) C-QUR V-Patch (Atrium Medical Corp.)
Premilene Mesh (B Braun) GORE® SYNECOR Biomaterial (W.L. Gore)
Premilene Mesh Plug (B Braun) Parietex Composite (PCO) Mesh (Covidien)
PROLENE 3D Patch (Ethicon Inc.)a Parietex Composite Hiatal (PCO 2H) Mesh (Covidien)
PROLENE Mesh (Ethicon Inc.) Parietex Composite Open Skirt (PCO OS) Mesh (Covidien)
PROLENE Polypropylene Hernia System (Ethicon Inc.)a Parietex Composite Parastomal (PCO) Mesh (Covidien)
PROLENE Soft Mesh (Ethicon Inc.) Parietex Composite Ventral Patch (Covidien)
ProFlor (Insightra Medical)a PHYSIOMESH (Ethicon Inc.)
ProLite Mesh (Atrium Medical Corp.) PROCEED Surgical Mesh (Ethicon Inc.)
ProLite Ultra Mesh (Atrium Medical Corp.) PROCEED Ventral Patch (PVP) (Ethicon Inc.)
ProLoop Mesh (Atrium Medical Corp.)a Sepramesh (Bard/Davol Inc.)
Rebound HRD (MMDI) Sepramesh IP COMPOSITE (Bard/Davol Inc.)
Rebound HRD V (MMDI) Symbotex (Covidien)
SURGIMESH WN (Apside/BG Medical) VENTRALEX ST Hernia Patch (Bard/Davol Inc.)
Surgipro Polypropylene Monofilament (Covidien) VENTRALIGHT ST Mesh (Bard/Davol Inc.)
Surgipro Multifilament Polypropylene (Covidien) VENTRIO ST Hernia Patch (Bard/Davol Inc.)
Surgipro Polypropylene Open Weave (Covidien)
Versatex (Covidien) Resorbable Coating
VISILEX Mesh (Bard/Davol Inc.) C-QUR FX Mesh (Atrium Medical Corp.)
VITAMESHTM (Atrium Medical Corp.) C-QUR Lite Mesh (Atrium Medical Corp.)
VITAMESHTM BLUE (Atrium Medical Corp.) C-QUR CENTRIFX (Atrium Medical Corp.)a

Biological Tissue-Derived Barrier


ZenaproTM (Cook Medical)

a
Available in preformed shapes.

viscoelastic anisotropic responses for both tissues, with ~1.5x stiffer were less compliant than the isolated muscles in the direction of the
response for the porcine linea alba compared to human (Levillain et al., muscle fibers, but more compliant in the direction perpendicular to the
2016). The porcine anterior rectus sheath was also examined using fibers. Interestingly, the anisotropy of composite samples was less
uniaxial/biaxial tests aligned parallel and perpendicular to the collagen pronounced than individual muscle samples, likely because the fiber
fiber direction; results showed a highly anisotropic response with the directions in these two muscles are not coincident and balance each
fiber direction exhibiting higher stiffness and failure stress than the other. While perhaps obvious, this observation demonstrates the
cross-fiber direction (Lyons et al., 2014). importance of not only evaluating mechanical properties of individual
A single study has examined canine adbominal tissues as an animal layers within the abdominal wall, but to also consider the functional
model. In this study, the mechanics of the transversus abdominis and behavior of the composite structure when all layers are combined in the
internal oblique muscles were evaluated individually and also together anatomical environment.
as a composite structure (Hwang et al., 1985). The composite samples

418
C.R. Deeken, S.P. Lake Journal of the Mechanical Behavior of Biomedical Materials 74 (2017) 411–427

Table 4 2016; Cooney et al., 2015)) have also shown greater transverse stiffness
Resorbable synthetic biomaterials for hernia repair applications. compared to the longitudinal direction, so other factors specific to the
test setup or the rabbit model itself may be responsible.
Bare Barriers & Coatings

BIO-A Tissue Reinforcement (W.L. Gore & Resorbable Barrier, Composite


Assoc. Inc.) 3.2. Mechanical modeling of animal abdomens
BIO-A Hernia Plug (W.L. Gore & Assoc. Inc.) PhasixTM ST Mesh (Bard/Davol Inc.)
DEXON Mesh (Covidien) Although not as common as the work that has been done for human
Safil Mesh (B Braun)
Seri Scaffold (Sofregen Medical)
tissues, some theoretical and computational models have been devel-
TIGR Matrix Surgical Mesh (Insightra oped to provide deeper analyses and enable predictive responses of
Medical) animal abdomens. Simon-Allue et al. (2015) expanded upon their
VICRYL Knitted/Woven Mesh (Ethicon Inc.) previously described technique to measure the elasticity of the rabbit
Phasix (Bard/Davol Inc.)
abdominal wall, then evaluated the ability of two distinct inverse
analysis procedures to predict region-specific mechanics (i.e., shear
modulus and non-linearity parameter) from the measured deformations
3.1.2. Mechanical evaluation of intact animal abdominal walls and known IAPs (Simon-Allue et al., 2016b). This study utilized a 3D FE
For similar reasons as outlined previously for human tissue, several model with an isotropic two-parameter constitutive model and demon-
studies have examined the mechanical behavior of the intact abdominal strated a stiffer region in the center of the abdominal wall correspond-
wall in animal models. Namely, the in vivo mechanical function of the ing to linea alba and fascia layers. While this study was for the intact
abdominal wall relies on the integration and cooperation of the various rabbit abdomen, a few other studies have developed mathematical
layers of the composite tissue structure rather than on actions of models of rabbit tissues following mesh implantation. Hernandez-
individual tissues. One group developed an experimental test method Gascon et al. (2011) formulated a FE model of repaired abdominal
to measure the deformation and strains on both the internal and wall tissue, which showed smaller displacements and higher stresses in
external surfaces of an excised porcine abdominal wall under pressure implanted abdominal wall compared to the intact wall. As the simula-
applied via air or a spherical indenter (Podwojewski et al., 2013). Using tion of repair with three representative meshes led to very different
this setup, speckle patterns were applied to the internal and external mechanics of abdominal wall compared to the intact case, the authors
abdominal surfaces and 3D strain fields were computed for both suggested that no mesh can reproduce the displacements of the healthy
surfaces of pressurized abdominal walls in intact, defect, and repaired abdominal wall. While this conclusion may be overly broad after
states. Similar to results obtained using this system for human tissue examination of only a small subset of possible meshes, it does highlight
(Podwojewski et al., 2014), external surface strains were ~2.5X greater the difficulty in properly matching properties of implanted synthetic
than internal strains and, importantly, the stiffness and strains of the meshes to the mechanics of the complex, composite abdominal wall.
repaired walls were not different from the intact state. Another group Another study by this group utilized the rabbit animal model to
developed a non-invasive analysis technique to measure the in vivo examine the mechanics of defect repair using three different meshes,
deformation of the surface of the abdominal wall of anesthetized rabbits evaluated at three different post-operative time points (Hernandez-
at different IAPs (Simon-Allue et al., 2015). This procedure was utilized Gascon et al., 2012). This study found that the ingrowth of collagen into
to evaluate healthy and hernia-repaired rabbits (using SurgiproTM, a implanted meshes seemed to somewhat unify the mechanics of mesh-
high-density non-absorbable polypropylene mesh), which showed that tissue explants, thereby indicating that detailed characterization of pre-
max displacements were ~30% lower for repaired abdomens. Interest- implantation synthetic meshes without considering changes that occur
ingly, in this study the longitudinal direction appeared to be stiffer than following repair is likely not sufficient to optimize mesh-tissue mechan-
transverse, which disagrees with much of the literature. The authors ical match.
suggest that this may be partially due to biped vs. quadruped animals, An extensive study using a porcine animal model evaluated various
however even studies in other quadrupeds (e.g., pigs (Levillain et al., combinations of synthetic meshes of varying properties attached via
one of several different types of connectors (i.e., fixation methods)

Table 5
Biological tissue-derived biomaterials for hernia repair applications.

Bare Barriers & Coatings Reinforced

AlloDerm Tissue Matrix (LifeCell Corp.) Antibacterial Coating Permanent Fibers


AlloMax Surgical Graft (Bard/Davol Inc.) XenMatrixTM AB Surgical Graft (Bard/Davol Inc.) OviTex Reinforced BioScaffold with Permanent Polymer (TELA Bio)
CollaMend Implant (Bard/Davol Inc.)
CollaMend FM Implant (Bard/Davol Inc.) Permanent Fibers + Barrier
DermaMatrix Acellular Dermis (Synthes Inc.) OviTex 1S Reinforced BioScaffold with Permanent Polymer (TELA Bio)
FlexHD Acellular Dermis (MTF/Ethicon Inc.) OviTex 2S Reinforced BioScaffold with Permanent Polymer (TELA Bio)
Fortiva (RTI Biologics)
MatriStem (ACell, Inc.) Resorbable Fibers
Medeor Matrix (Kensey Nash Corp.) OviTex Reinforced BioScaffold with Resorbable Polymer (TELA Bio)
Meso BioMatrix Scaffold (Kensey Nash Corp.)
Miromesh Biologic Matrix (Miromatrix Medical Inc.) Resorbable Fibers + Barrier
Peri-Guard Repair Patch (Synovis) OviTex 1S Reinforced BioScaffold with Resorbable Polymer (TELA Bio)
Permacol Surgical Implant (Covidien) OviTex 2S Reinforced BioScaffold with Resorbable Polymer (TELA Bio)
Strattice Reconstructive Tissue Matrix (LifeCell Corp.)
Supple Peri-Guard Repair Patch (Synovis)
SurgiMend Collagen Matrix (TEI Biosciences Inc.)
Surgisis/Biodesign Hernia Grafts (Cook Medical)
Surgisis FM/Biodesign Hernia Grafts (Cook Medical)
Veritas® Collagen Matrix (Insightra)
XCM Biologic Tissue Matrix (Ethicon)
XenMatrixTM Surgical Graft (Bard/Davol Inc.)

419
C.R. Deeken, S.P. Lake Journal of the Mechanical Behavior of Biomedical Materials 74 (2017) 411–427

Fig. 2. Classification system for biomaterials utilized for hernia repair applications.

(Tomaszewska et al., 2013). Evaluation included a total of 57 different comprised of either a permanent synthetic material (e.g. polypropylene,
configurations, corresponding to over 200 total individual experiments, polytetrafluoroethylene, polyester) (Deeken et al., 2011b, 2011c), a
to repair two sizes of surgically-created hernia defects (5 or 8 cm). biological tissue-derived material (e.g. dermis, pericardium, rumen, or
Some predictable results were confirmed (e.g., larger diameter hernias small intestine submucosa derived from human, porcine, bovine, or
correspond to larger forces, stiffer implants led to larger tearing forces ovine sources) (Deeken et al., 2012; Ferzoco, 2016b), or a resorbable
on the connectors), and other unique insights into the relative strength synthetic material (e.g. poly-4-hydroxybutyrate, polyglycolic acid,
of fixation methods were provided (e.g., trans-abdominal sutures carry trimethylene carbonate) (Deeken and Matthews, 2013b; Martin et al.,
highest load). This study also introduced a simple FE model of 2013; Hjort et al., 2012). These structural meshes are also often paired
implanted mesh, yielding results that compared favorably to experi- with anti-adhesion barriers/coatings (Deeken et al., 2012), antibacter-
mental data. ial coatings (Cohen et al., 2016; Majumder et al., 2016), or reinforcing
fibers (Sahoo et al., 2014; Ferzoco, 2016a).
3.3. Limitations of previous studies of animal abdominal wall mechanics As shown in Tables 3–5, some important nuances exist in the
classification of the biomaterials available today. Composite barrier
As noted previously for studies of human tissues, there are a number meshes are comprised of two discrete layers, the structural mesh and
of limitations which should be considered when interpreting results and the anti-adhesion barrier. The two layers are sewn or vacuum pressed
conclusions from the studies that have utilized animal model systems together. Non-composite barrier meshes are comprised of a single layer
and tissues to examine abdominal wall mechanics. Applicable limita- of material that exhibits anti-adhesion characteristics on one side and
tions that were described previously include (1) inconsistencies in how tissue ingrowth features on the other side. Anti-adhesion coatings, on
tissues are preserved/treated (e.g., live tissue vs. fresh post-mortem vs. the other hand, merely surround the individual mesh fibers but do not
frozen/thawed, relative state of hydration, effect of rigor mortis), (2) form a barrier layer that bridges across the interstices between fibers.
variable test conditions and protocols across different studies (e.g., To date, antibacterial coatings have only been applied to porcine
loading rate, type of mechanical test, such as uniaxial vs. biaxial vs. ball dermis, forming a layer on the surface of the underlying biological
burst, specifics of test setup), and (3) flawed assumptions in mathema- tissue-derived scaffold (Cohen et al., 2016; Majumder et al., 2016).
tical modeling formulations (e.g., isotropic tissue properties, homo- Additional fibers are also often added to reinforce basic structural
geneous structure/mechanics, uniform thickness of wall or layers). A meshes (Sahoo et al., 2014; Ferzoco, 2016). The function of these fibers
few additional issues specific to animal models should also be con- is to provide a gradual transfer of load back to the native tissue as the
sidered, namely (4) relevance of each particular animal species to repair site heals and regenerates native tissue. This is accomplished
humans (e.g., biped vs. quadruped loading patterns, variations in when permanent synthetic fibers are used to reinforce biological tissue-
anatomical structures and interactions), and (5) relevance of compar- derived materials or when resorbable fibers are used to reinforce
isons across different animal species and different muscle types (e.g., permanent synthetic meshes. One component is gradually resorbed,
relative consistency of results across rat, rabbit, pig or dog tissues), while the other component remains intact.
making it difficult to ascertain whether each species is unique or if data In addition to knowledge of material composition, understanding
can be compared and/or combined across different species. the mechanical characteristics of these devices is also critical to
selecting the biomaterial design and orientation that is optimal for
4. Biomaterials for hernia repair the mechanical environment of a patient's specific hernia. A variety of
techniques have been utilized to assess the mechanics of hernia repair
4.1. Classification system materials, including biomechanical testing, animal models, and com-
puter simulations.
The environment of the biomaterial-tissue interface is dictated by
both the biomaterial chosen and the host tissue. Patient-to-patient 4.2. Biomechanical characterization
variability in muscle mass, fat mass, sex and age, as well as hernia
defect size and location create a wide range of environments into which Several biomechanical testing techniques have been described for
a hernia mesh may be placed. Though the host environment is a fixed characterizing hernia repair materials, including suture retention
factor, the particular biomaterial selected for repair is not. Currently, (Deeken et al., 2011b, 2011c, 2012; Todros et al., 2017), tear resistance
nearly 150 biomaterial designs exist for hernia repair applications (Deeken et al., 2011b, 2011c, 2012; Todros et al., 2017), uniaxial
(Tables 3–5). tension (Deeken et al., 2011b, 2011c, 2012; Todros et al., 2017;
Historically, several classification systems have been proposed to Hollinsky et al., 2008; Saberski et al., 2011), ball burst (Deeken et al.,
organize biomaterial designs into practical categories with similar 2011b, 2011c, 2012; Todros et al., 2017), and biaxial testing (Todros
features (Amid, 1997; Earle and Mark, 2008). However, many of these et al., 2017; Deeken et al., 2014; Cordero et al., 2016). In suture
systems are now outdated with the development of more sophisticated retention testing, a stainless steel wire is passed through the material at
devices in recent years. An updated classification system is presented a fixed distance to the edge to simulate a suture. Tension is applied to
here in Fig. 2. This system groups meshes in a hierarchical fashion, the material, and suture retention strength is recorded as the maximum
beginning with the structural “mesh” component, which is typically load sustained prior to failure at the suture point (Deeken et al., 2011b,

420
C.R. Deeken, S.P. Lake Journal of the Mechanical Behavior of Biomedical Materials 74 (2017) 411–427

Table 6
Physical characteristics of biomaterials utilized for hernia repair applications.

Diameter of Area of Pores Diameter of Thickness Density Refs.


Pores (mm) (mm2) Fibers (µm) (mm) (g/m2)

PERMANENT SYNTHETIC
Bare
Bard Mesh 0.44–0.58 185.7 0.73–0.76 102.4–105 (Deeken et al., 2011c; Martin et al., 2013)
Bard Soft Mesh 2.5 44 (Kalaba et al., 2016; Schug-Pass et al., 2010)
Dyna-Mesh 4.16 36 (Cordero et al., 2016)
INFINIT 4 116.2 0.16 65.6–70 (Deeken et al., 2011c; Cordero et al., 2016)
Marlex 0.46 0.63 95 (Kalaba et al., 2016; Hollinsky et al., 2008; Klinge
et al., 2002; Cobb et al., 2005)
MERSILENE Mesh 1.0 33–40 (Kalaba et al., 2016; Brown and Finch, 2010; Conze
et al., 2005)
Optilene Mesh 1.0 7.64 36–48 (Kalaba et al., 2016; Cordero et al., 2016; Schug-
Pass et al., 2010; Pascual et al., 2008)
Parietene 1.0–1.6 0.53 77–78 (Kalaba et al., 2016; Hollinsky et al., 2008;
Langenbach and Sauerland, 2013)
Parietene Light 1.5–1.7 0.36 36–38 (Kalaba et al., 2016; Hollinsky et al., 2008; Schug-
Pass et al., 2010; Hollinsky et al., 2009)
Parietex Flat Sheet 2D 2.0 1.75 338.8 0.52–0.53 100–119.2 (Deeken et al., 2011c; Hollinsky et al., 2008)
Mesh (TEC)
Parietex (TECR) 2.0 0.53 120 (Hollinsky et al., 2008)
PROLENE Mesh 0.8–1.6 0.39 130.4 0.51–0.53 79.5–108 (Kalaba et al., 2016; Deeken et al., 2011c; Hollinsky
0.8–1.6 et al., 2008; Cobb et al., 2005; Brown and Finch,
2010; Langenbach et al., 2008)
ProLite Mesh 0.8 0.33 151.2 0.47 85–90 (Kalaba et al., 2016; Deeken et al., 2011c; Cobb
et al., 2005; Orenstein et al., 2012)
ProLite Ultra Mesh 0.34 99.0 0.39 50.1 (Deeken et al., 2011c)
Serapren 0.08–0.1 116 (Kalaba et al., 2016; Langenbach et al., 2008)
Surgipro 0.8 0.26 0.57 84–110 (Kalaba et al., 2016; Hollinsky et al., 2008; Cordero
et al., 2016; Cobb et al., 2005)
Trelex 0.35–0.6 95 (Kalaba et al., 2016; Brown and Finch, 2010;
Orenstein et al., 2012)
Permanent Barrier, Non-Composite
DUALMESH Biomaterial 0.003/0.022 n/a n/a 1.18 320–420 (Kalaba et al., 2016; Deeken et al., 2011b; Doctor,
2006; Voskerician et al., 2010)
MYCROMESH 0.025/0.3 (Kalaba et al., 2016; Voskerician et al., 2006)
Permanent Barrier, Composite
Composix E/X 0.43 183.70 0.89 255.80 (Deeken et al., 2011b)
Composix L/P 6.07 163.20 0.69 187.40 (Deeken et al., 2011b)
Permanent Coating
TIMESH Extralight 1.24 0.21 16 (Hollinsky et al., 2008)
TIMESH Light 1.24 0.29 33 (Hollinsky et al., 2008)
Resorbable Barrier, Composite
C-QUR Mesh 0.33 151.2 0.56 321.0 (Deeken et al., 2011b)
Parietex Composite (PCO) 3.68 160.20 0.76 155.90 (Deeken et al., 2011b)
PROCEED 5.46 96.85 0.57 189.50 (Deeken et al., 2011b)
Sepramesh IP Composite 0.40 155.70 0.82 240.60 (Deeken et al., 2011b)
Resorbable Coating
C-QUR Lite Mesh (≤6 in. 0.34 99.00 0.28 69.19 (Deeken et al., 2011c)
size mesh)
C-QUR Lite Mesh (> 6 in. 0.33 151.20 0.46 128.70 (Deeken et al., 2011c)
size mesh)
Reinforced - Resorbable Fibers
ULTRAPRO 2.28 3.45–4.10 102.5 0.44–0.5 28–58 (Deeken et al., 2011c; Hollinsky et al., 2008;
Cordero et al., 2016)
VYPRO 3.0 0.34 26 (Hollinsky et al., 2008)
VYPRO II 2.6 0.39 40 (Hollinsky et al., 2008)

RESORBABLE SYNTHETIC
Bare
BIO-A Tissue 33.8 1.57 (Ebersole et al., 2012)
Reinforcement
TIGR Matrix Surgical 1 ~13 ~0.5 (Cordero et al., 2016; Ebersole et al., 2012)
Mesh
VICRYL 13.1 0.07 (Ebersole et al., 2012)
PHASIX Mesh 0.26 0.51 182 (Martin et al., 2013)

BIOLOGICAL TISSUE-DERIVED
Bare
AlloDerm Tissue Matrix n/a n/a n/a 2.02 n/a (Deeken et al., 2012)
AlloMax Surgical Graft n/a n/a n/a 1.29 n/a (Deeken et al., 2012)
CollaMend Implant n/a n/a n/a 1.22 n/a (Deeken et al., 2012)
CollaMend FM Implant n/a n/a n/a 1.34 n/a (Deeken et al., 2012)
FlexHD Acellular Dermis n/a n/a n/a 1.15 n/a (Deeken et al., 2012)
Peri-Guard Repair Patch n/a n/a n/a 0.47 n/a (Deeken et al., 2012)
Permacol Surgical n/a n/a n/a 0.91 n/a (Deeken et al., 2012)
(continued on next page)

421
C.R. Deeken, S.P. Lake Journal of the Mechanical Behavior of Biomedical Materials 74 (2017) 411–427

Table 6 (continued)

Diameter of Area of Pores Diameter of Thickness Density Refs.


Pores (mm) (mm2) Fibers (µm) (mm) (g/m2)

Implant
Strattice Reconstructive n/a n/a n/a 1.76 n/a (Deeken et al., 2012)
Tissue Matrix
SurgiMend Collagen n/a n/a n/a 0.84 n/a (Deeken et al., 2012)
Matrix
Surgisis/Biodesign Hernia n/a n/a n/a 1.37 n/a (Deeken et al., 2012)
Grafts
Veritas Collagen Matrix n/a n/a n/a 0.80 n/a (Deeken et al., 2012)
XenMatrix Surgical Graft n/a n/a n/a 1.95 n/a (Deeken et al., 2012)

2011c, 2012; Todros et al., 2017). To assess tear resistance, a small tear on tensile stress within the abdominal wall when the abdomen was
of a defined length is initiated in the material. Tension is applied to assumed to behave as a thin-walled pressure vessel (Deeken et al.,
either side of the tear, and the tear resistance value is recorded as the 2011b, 2011c). In the most extreme scenario, with the highest
maximum load sustained prior to propagation of the tear (Deeken et al., intraabdominal pressure and greatest abdominal circumference, the
2011b, 2011c, 2012; Todros et al., 2017). In ball burst testing, a resulting tensile stress was 47.8 N/cm, leading to the recommendation
stainless steel ball is applied to the material in compression, simulating that biomaterials possess a tensile strength of at least 50 N/cm when
intraabdominal pressure on the material (Deeken et al., 2011b, 2011c, used in hernia repair applications (Deeken et al., 2011b, 2011c). When
2012; Todros et al., 2017). A variety of values can be calculated from human abdominal wall tissues were subjected to tensile testing, Junge
the data generated during ball burst testing, including ultimate tensile et al. (2001) reported a strain of 10–30%, leading to the recommenda-
strength and strain, but this method does not assess anisotropy and tion that hernia repair materials should possess similar strain values in
other important characteristics of hernia repair materials. In uniaxial order to approximate the mechanics of the human abdominal wall.
tensile testing, a strip of material is subjected to tension in a single
direction (Deeken et al., 2011b, 2011c, 2012; Todros et al., 2017;
Hollinsky et al., 2008; Saberski et al., 2011), while in biaxial tensile 4.3. Preclinical implantation studies
testing, the material is subjected to tension in two orthogonal directions
(Todros et al., 2017; Deeken et al., 2014; Cordero et al., 2016). Both In the field of hernia repair, a number of animal models have been
methods assess the strength and stiffness of the material and character- developed utilizing rats (Anurov et al., 2012; DuBay et al., 2005),
istics such as anisotropy, but biaxial testing more realistically simulates rabbits (Hernandez-Gascon et al., 2012; Konerding et al., 2012; Peeters
the mechanics of the human abdomen. A recent study revealed et al., 2013), monkeys (Ferzoco, 2016a, 2016b; Xu et al., 2008), sheep
dramatic variation in anisotropy, non-linearity, and hysteresis when (Hjort et al., 2012), dogs (Greca et al., 2001), and pigs (Cavallo et al.,
several commonly-utilized hernia repair materials were assessed via 2015; Deeken and Matthews, 2013a, 2012, 2013b; Deeken et al.,
planar biaxial testing, underscoring the importance of understanding 2011a; Jenkins et al., 2011; Melman et al., 2011; Scott et al., 2016).
the characteristics of these materials prior to implantation (Deeken Many of these models are very similar, involving surgical creation of
et al., 2014; Cordero et al., 2016). hernia defects with subsequent mesh repair and evaluation of mechan-
Several groups have utilized biomechanical techniques to charac- ical and histological characteristics after a period of implantation. In
terize biomaterials for hernia repair applications (Deeken et al., 2011b, many of these models, the hernia defects are repaired immediately
2011c, 2012; Todros et al., 2017; Hollinsky et al., 2008; Saberski et al., while the wound is still in an acute healing phase (Anurov et al., 2012;
2011; Cordero et al., 2016), and the results are summarized in Tables Hernandez-Gascon et al., 2012; Ferzoco, 2016a, 2016b; Deeken and
6–7. Differences in experimental procedures (e.g., specific test setup, Matthews, 2013a, 2013b; Hjort et al., 2012; Konerding et al., 2012;
testing rate, orientation, specimen dimensions) and methods of data Peeters et al., 2013; Xu et al., 2008; Greca et al., 2001; Scott et al.,
analysis have led to inconsistencies in values reported by different 2016). In other models, the meshes are implanted after a 4–5 week
groups. Many of the materials shown in Tables 6–7 demonstrate “maturation” period, allowing the wound to reach a chronic state prior
characteristics that meet the guidelines suggested for failure properties to mesh implantation (Cavallo et al., 2015; DuBay et al., 2005; Deeken
of materials utilized for hernia repair applications (Deeken et al., et al., 2011a; Jenkins et al., 2011; Melman et al., 2011). Thus, chronic
2011b, 2011c, 2012). However, there are currently no established models more closely recreate the wound environment encountered in
guidelines for more nuanced aspects of mechanical properties such as the clinical setting. Hernia repair technique is another variable; meshes
anisotropy, nonlinearity, and hysteresis, leading to an incomplete may be implanted in the onlay (Hjort et al., 2012), inlay (Hernandez-
description of mechanical characteristics. Gascon et al., 2012; Ferzoco, 2016a, 2016b; Deeken and Matthews,
In a series of previous publications, we recommended that hernia 2013b; Xu et al., 2008; Greca et al., 2001), sublay (Cavallo et al., 2015;
repair materials exhibit suture retention strength and tear resistance Anurov et al., 2012; Deeken et al., 2011a; Jenkins et al., 2011; Melman
values greater than 20 N, ball burst strength greater than 50 N/cm, and et al., 2011; Scott et al., 2016), or underlay (DuBay et al., 2005;
strain in the range of 10–30% (Deeken et al., 2011b, 2011c, 2012). Konerding et al., 2012; Peeters et al., 2013; Deeken and Matthews,
These suggested failure properties were based on previous animal 2012; Jenkins et al., 2011; Scott et al., 2016) position. The fascia is
studies or theoretical calculations. For example, Melman et al. (2010) closed, and the mesh is placed on the anterior fascia when implanted in
conducted a study in which polypropylene sutures (size 0) were utilized the onlay position. For inlay repairs, the mesh is placed within the
to attach hernia meshes to porcine abdominal wall tissue, and the entire defect and is sutured to the edges of the defect, leading to what is
construct was then subjected to lap shear testing. The maximum load commonly referred to as a “bridged” repair without closure of the
sustained prior to failure was approximately 20 N per fixation point, fascia. In a sublay repair, the mesh is placed in a retrorectus or
with three sutures utilized in each construct. Failure occurred in the preperitoneal position, and the underlay repair refers to intraperitoneal
porcine abdominal wall tissue while the mesh and suture material mesh implantation. In rats, rabbits, dogs, and monkeys, relatively small
remained intact. In another study, intraabdominal pressure and meshes are typically utilized due to the small size of these animals
abdominal circumference values were varied to demonstrate the impact compared to humans. The porcine abdomen is much larger, comparable
in size to the human abdomen. Thus, clinically relevant hernia defect

422
Table 7
Mechanical properties of biomaterials utilized for hernia repair applications (L = longitudinal, T = transverse testing orientation).

Suture Retention Tear Resistance (N) Uniaxial Tensile Ball Burst Planar Biaxial Tensile
(N) Strength (MPa)
C.R. Deeken, S.P. Lake

L T L T L T Tensile Strain (%) Stiffness (N/cm) Stiffness (N/cm) Anisotropy Refs.


Strength Index
(N/cm)

PERMANENT SYNTHETIC MESHES


Bare
Bard Mesh 50.78 66.8 46.84 38.36 11.64 0.16 157.7 10.76 75.69 37.53 2.03 (Deeken et al., 2011c,
2014)
Bard Soft Mesh 124.53 52.89 2.36 (Deeken et al., 2014)
Dyna-Mesh 190.1 100.1 1.84 (Cordero et al., 2016)
INFINIT 26.71 32.36 14.29 16.35 13.6 7.36 9.25 n/a 168.40–479.1 119.83–139.7 1.42–3.37 (Deeken et al., 2011c,
2014; Cordero et al.,
2016)
Optilene Mesh 191.1 100.1 1.82 (Cordero et al., 2016)
Parietex Flat Sheet 2D Mesh 51.4 58.38 32.66 28.6 6.63 15.51 112.90 3.49 (Deeken et al., 2011c)
(TEC)
PROLENE Mesh 61.2 70.49 33.66 39.33 0.76 16.06 156.60 5.27 180.04 143.42 1.26 (Deeken et al., 2011c,
2014)
ProLite Mesh 48.75 57.71 33.35 33.10 11.64 0.16 138.00 9.61 106.19 82.97 1.29 (Deeken et al., 2011c,
2014)
ProLite Ultra Mesh 36.07 23.89 19.27 17.84 11.40 4.90 50.72 16.35 92.24 76.36 1.21 (Deeken et al., 2011c,
2014)
Surgipro 148.7 128.5 1.18 (Cordero et al., 2016)
Permanent Barrier, Non-Composite

423
DUALMESH Biomaterial 65.18 72.95 30.47 41.28 7.52 5.52 97.76 10.24 137.59 125.97 1.08 (Deeken et al., 2011b,
2014)
Permanent Barrier, Composite
Composix E/X 70.47 60.28 30.14 48.75 1.44 10.74 237.8 9.62 (Deeken et al., 2011b)
Composix L/P 34.04 48.58 32.76 16.96 6.10 1.48 76.77 11.06 (Deeken et al., 2011b)
Resorbable Barrier, Composite
C-QUR Mesh 41.78 62.75 25.79 30.79 1.73 4.74 144.30 9.07 177.00 177.78 1.00 (Deeken et al., 2011b,
2014)
Parietex Composite (PCO) 28.15 36.32 19.74 16.21 2.56 1.03 38.87 6.46 178.13 119.34 1.50 (Deeken et al., 2011b,
2014)
PHSIOMESH 168.91 151.62 1.12 (Deeken et al., 2014)
PROCEED 34.06 41.62 19.84 20.19 4.44 4.78 52.60 7.25 129.72 128.34 1.01 (Deeken et al., 2011b,
2014)
Sepramesh IP Composite 99.22 85.89 51.07 54.18 4.38 2.64 200.7 3.68 (Deeken et al., 2011b)
Ventralight ST 123.57 50.82 2.43 (Deeken et al., 2014)
Resorbable Coating
C-QUR Lite Mesh (≤6 in) 22.86 33.83 19.36 18.35 1.11 2.56 50.53 13.22 (Deeken et al., 2011c)
C-QUR Lite Mesh (> 6 in) 61.83 40.00 35.04 42.77 13.75 3.52 170.00 11.32 (Deeken et al., 2011c)
Biological Tissue-Derived Barrier
OviTex 1S ~60 (Ferzoco, 2016a)
OviTex 2S ~75 (Ferzoco, 2016a)
Resorbable Fibers
ULTRAPRO 15.08 16. 10.47 5.07 13.52 0.08 35.50 16.23 98.63–171.2 53.01–79.6 1.87–2.17 (Deeken et al., 2011c,
2014; Cordero et al.,
2016)

RESORBABLE SYNTHETIC
Bare
BIO-A Tissue Reinforcement ~45 16.6 ~4.5 74.9 7.3 (Ebersole et al., 2012)
TIGR Matrix Surgical Mesh ~45 59.0 ~30 33.3 ~7 0.2 86.5 < 10 409.2 272.4 1.47 (Cordero et al., 2016;
Journal of the Mechanical Behavior of Biomedical Materials 74 (2017) 411–427

(continued on next page)


Table 7 (continued)

Suture Retention Tear Resistance (N) Uniaxial Tensile Ball Burst Planar Biaxial Tensile
(N) Strength (MPa)

L T L T L T Tensile Strain (%) Stiffness (N/cm) Stiffness (N/cm) Anisotropy Refs.


C.R. Deeken, S.P. Lake

Strength Index
(N/cm)

Ebersole et al., 2012)


VICRYL 39.4 ~25 145.2 ~70 5.8 (Ebersole et al., 2012)
PHASIX Mesh 59.2 49.1 30.3 29.5 140.7 15.4 (Deeken and Matthews,
2013b)

BIOLOGICAL TISSUE-DERIVED
Bare
AlloDerm Tissue Matrix 127.2 84.73 20.32 1028.00 17.02 (Deeken et al., 2012)
AlloMax Surgical Graft 29.09 16.86 14.36 290.80 26.22 (Deeken et al., 2012)
CollaMend Implant 47.90 17.13 11.48 110.3 5.85 (Deeken et al., 2012)
CollaMend FM Implant 37.53 13.21 10.65 86.18 13.58 (Deeken et al., 2012)
FlexHD Acellular Dermis 55.34 31.05 14.36 929.50 21.20 (Deeken et al., 2012)
Peri-Guard Repair Patch 30.54 14.34 21.51 99.05 20.05 (Deeken et al., 2012)
Permacol Surgical Implant 23.75 10.1 8.22 66.23 13.1 (Deeken et al., 2012)
Strattice Reconstructive 63.76 27.54 9.92 270.5 9.59 (Deeken et al., 2012)
Tissue Matrix
SurgiMend Collagen Matrix 87.85 27.86 28.54 432.4 6.41 (Deeken et al., 2012)
Surgisis/Biodesign Hernia 50.29 32.13 2.53 200.2 13.57 (Deeken et al., 2012)
Grafts
Veritas Collagen Matrix 23.92 15.06 9.38 128.6 25.6 (Deeken et al., 2012)
XenMatrix Surgical Graft 99.74 24.5 11.95 377.0 11.59 (Deeken et al., 2012)
Reinforced

424
Permanent OviTex Reinforced ~42 (Ferzoco, 2016a)
Fibers BioScaffold with Permanent
Polymer
Resorbable OviTex Reinforced ~42 (Ferzoco, 2016a)
Fibers BioScaffold with Resorbable
Polymer
Journal of the Mechanical Behavior of Biomedical Materials 74 (2017) 411–427
C.R. Deeken, S.P. Lake Journal of the Mechanical Behavior of Biomedical Materials 74 (2017) 411–427

and mesh sizes can be utilized in the porcine abdomen, and similar incompletely understood. Future studies should address a number of
intraabdominal pressures are encountered (Gudmundsson et al., 2002; topics, including: 1) additional tissue characterization studies involving
Cobb et al., 2005), making this the preferred preclinical model for greater numbers of fresh human tissue specimens, 2) evaluation of
device evaluation, especially for mechanical characterization. active muscle mechanics using animal studies and computer simula-
tions to determine how contractile forces contribute, along with passive
5. Conclusions properties of tissues and biomaterials, to the mechanical function of the
composite abdominal wall, 3) better computational models that more
Most of the datasets reviewed in this paper were not sufficiently closely approximate the human abdomen with appropriate assumptions
powered to detect significant correlations between tissue mechanics of regarding anisotropy, thickness, etc., and 4) external means of evaluat-
the human abdominal wall and patient demographics such as age, sex, ing mesh-tissue mechanics in living subjects, in both humans and
BMI, and parity. However, a few studies showed that abdominal wall animals.
tissue specimens procured from male subjects were stiffer or less
compliant than those procured from female subjects (Cardoso, 2012; Disclosures
Junge et al., 2001; Song et al., 2006a, 2006b). This trend was
demonstrated in mechanical evaluations of both cadaveric samples Dr. Deeken is an employee of, and Dr. Lake is a consultant for,
(Cardoso, 2012; Junge et al., 2001) and living subjects (Song et al., Covalent Bio, LLC (St. Louis, MO) which received funding for this work
2006a, 2006b). Thus, it is critical that future studies are undertaken from TELA Bio, Inc. (Malvern, PA).
with larger numbers of human abdominal wall specimens to determine
whether other factors are also influential and deserve consideration References
when selecting an appropriate biomaterial for hernia repair applica-
tions. Amid, P., 1997. Classification of biomaterials and their related complications in
The human abdominal wall is a complex composite structure abdominal wall hernia surgery. Hernia 1, 15–21.
Anurov, M.V., Titkova, S.M., Oettinger, A.P., 2012. Biomechanical compatibility of
composed of many layers which vary depending on specific anatomical surgical mesh and fascia being reinforced: dependence of experimental hernia defect
location. The studies reviewed here reported greater compliance of the repair results on anisotropic surgical mesh positioning. Hernia 16 (2), 199–210.
linea alba (Grabel et al., 2005), larger strains for the intact abdominal Axer, H., Keyserlingk, D.G., Prescher, A., 2001. Collagen fibers in linea alba and rectus
sheaths. I. General scheme and morphological aspects. J. Surg. Res. 96 (1), 127–134.
wall (Junge et al., 2001), and greater stiffness for the rectus sheath and Ben Abdelounis, H., Nicolle, S., Ottenio, M., Beillas, P., Mitton, D., 2013. Effect of two
umbilical fascia (Hollinsky and Sandberg, 2007; Martins et al., 2012; loading rates on the elasticity of the human anterior rectus sheath. J. Mech. Behav.
Ben Abdelounis et al., 2013; Kirilova et al., 2011, 2009; Kirilova, 2012) Biomed. Mater. 20, 1–5.
Brown, C.N., Finch, J.G., 2010. Which mesh for hernia repair? Ann. R Coll. Surg. Engl. 92
when the tissues were loaded in the longitudinal direction compared to (4), 272–278.
transverse. Additionally, 2–3x greater stresses were observed in the Burger, J.W., Luijendijk, R.W., Hop, W.C., Halm, J.A., Verdaasdonk, E.G., Jeekel, J.,
linea alba (Levillain et al., 2016; Hollinsky and Sandberg, 2007; 2004. Long-term follow-up of a randomized controlled trial of suture versus mesh
repair of incisional hernia. Ann. Surg. 240 (4), 578–583.
Forstemann et al., 2011) when loaded in the transverse direction
Cardoso M., 2012. Experimental Study of the Human Anterolateral Abdominal Wall:
compared to longitudinal. Given these trends, a few recommendations Biomechanical Properties of Fascia and Muscles (Master’s Thesis).
can be made regarding orientation of mesh. For instance, the most Cavallo, J.A., Greco, S.C., Liu, J., Frisella, M.M., Deeken, C.R., Matthews, B.D., 2015.
compliant axis of the biomaterial should be oriented in the cranio- Remodeling characteristics and biomechanical properties of a crosslinked versus a
non-crosslinked porcine dermis scaffolds in a porcine model of ventral hernia repair.
caudal, or “longitudinal”, direction (Hernandez-Gascon et al., 2013), Hernia 19 (2), 207–218.
and the strongest axis of the biomaterial should be oriented in the Cobb, W, Carbonell, A, Novitsky, Y, Matthews, B., 2009. Central Mesh Failure with
medial-lateral, or “transverse”, direction. It is also clear from the Lightweight Mesh: A Cautionary Note. EHS. 2009. Berlin, Germany.
Cobb, W.S., Kercher, K.W., Heniford, B.T., 2005. The argument for lightweight
literature that the human abdominal wall is anisotropic, with anistropy polypropylene mesh in hernia repair. SurgInnov 12 (1), 63–69.
ratios as high as 8–9 reported for the human linea alba (Cooney et al., Cobb, W.S., Burns, J.M., Kercher, K.W., Matthews, B.D., James, N.H., Todd, H.B., 2005.
2016). Current biomaterial designs exhibit anisotropy ratios in the Normal intraabdominal pressure in healthy adults. J. Surg. Res. 129 (2), 231–235.
Cohen, L., Imahiyerobo, T., Scott, J., Spector, J., 2016. Comparison of antibiotic-coated
range of 1–3 (Deeken et al., 2014), and it is unclear whether an ideal versus uncoated porcine dermal matrix. Plast. Reconstr. Surg. 138 (5), 844e–855ee.
ratio exists for optimal match between mesh and tissue. It is likely Conze, J., Kingsnorth, A.N., Flament, J.B., et al., 2005. Randomized clinical trial
dependent on implantation location, since the linea alba, rectus sheath, comparing lightweight composite mesh with polyester or polypropylene mesh for
incisional hernia repair. Br. J. Surg. 92 (12), 1488–1493.
and other tissues of the abdominal wall exhibit extremely different
Cooney, G.M., Moerman, K.M., Takaza, M., Winter, D.C., Simms, C.K., 2015. Uniaxial and
characteristics. Given the number of unknowns yet to be addressed by biaxial mechanical properties of porcine linea alba. J. Mech. Behav. Biomed. Mater.
current studies of the human abdominal wall, it is unlikely that any 41, 68–82.
Cooney, G.M., Lake, S.P., Thompson, D.M., Castile, R.M., Winter, D.C., Simms, C.K., 2016.
single biomaterial design currently encompasses all of the ideal features
Uniaxial and biaxial tensile stress-stretch response of human linea alba. J. Mech.
identified. In addition, nearly all studies to date that have evaluated Behav. Biomed. Mater. 63, 134–140.
mechanics of individual muscles or layered structures have soley Cordero, A., Hernandez-Gascon, B., Pascual, G., Bellon, J.M., Calvo, B., Pena, E., 2016.
considered passive muscle properties; future work must also address Biaxial mechanical evaluation of absorbable and nonabsorbable synthetic surgical
meshes used for hernia repair: physiological loads modify anisotropy response. Ann.
mechanical implications of active muscle contration on abdominal wall Biomed. Eng. 44 (7), 2181–2188.
function. Deeken, C.R., Matthews, B.D., 2012. Comparison of contracture, adhesion, tissue
Several other aspects of biomaterial design also deserve considera- ingrowth, and histologic response characteristics of permanent and absorbable
barrier meshes in a porcine model of laparoscopic ventral hernia repair. Hernia 16
tion, but fall outside the scope of the current review. These character- (1), 69–76.
istics include low risk of adhesions, resistance to bacterial colonization Deeken, C.R., Matthews, B.D., 2013. Ventralight ST and sorbaFix versus physiomesh and
and infection, and low cost to support a broad range of applications. securestrap in a porcine model. JSLS: J. Soc. Laparoendosc. Surg./Soc. Laparoendosc.
Surg. 17 (4), 549–559.
Although subjective and driven by surgeon preference and experience, Deeken, C.R., Matthews, B.D., 2013. Characterization of the mechanical strength,
hernia repair materials must also possess appropriate handling char- resorption properties, and histologic characteristics of a fully absorbable material
acteristics for ease of implantation and fixation to the abdominal wall. (poly-4-hydroxybutyrate-PHASIX mesh) in a porcine model of hernia repair. ISRN
Surg. 238067.
Perhaps most important, hernia repair materials must support an Deeken, C.R., Melman, L., Jenkins, E.D., Greco, S.C., Frisella, M.M., Matthews, B.D.,
appropriate host tissue response leading to integration within the 2011a. Histologic and biomechanical evaluation of crosslinked and non-crosslinked
native abdominal wall and regeneration of host tissue with character- biologic meshes in a porcine model of ventral incisional hernia repair. J. Am. Coll.
Surg. (212), 880–888.
istics similar to the intact abdominal wall prior to mesh implantation.
Deeken, C.R., Abdo, M.S., Frisella, M.M., Matthews, B.D., 2011. Physicomechanical
Although current studies have provided important insights into the evaluation of absorbable and nonabsorbable barrier composite meshes for
characteristics of the human abdominal wall, many aspects remain laparoscopic ventral hernia repair. Surg. Endosc. 25, 1541–1552.

425
C.R. Deeken, S.P. Lake Journal of the Mechanical Behavior of Biomedical Materials 74 (2017) 411–427

Deeken, C.R., Abdo, M.S., Frisella, M.M., Matthews, B.D., 2011c. Physicomechanical Mater. 1 (1), 2–17.
evaluation of polypropylene, polyester, and polytetrafluoroethylene meshes for Kirilova, M., 2012. Time-dependent properties of human umbilical fascia. Connect. Tissue
inguinal hernia repair. J. Am. Coll. Surg. 212 (1), 68–79. Res. 53 (1), 21–28.
Deeken, C.R., Faucher, K.M., Matthews, B.D., 2012. A review of the composition, Kirilova, M., Stoytchev, S., Pashkouleva, D., Tsenova, V., Hristoskova, R., 2009. Visco-
characteristics, and effectiveness of barrier mesh prostheses utilized for laparoscopic elastic mechanical properties of human abdominal fascia. J. Bodyw. Mov. Ther. 13
ventral hernia repair. Surg. Endosc. 26 (2), 566–575. (4), 336–337.
Deeken, C.R., Eliason, B.J., Pichert, M.D., Grant, S.A., Frisella, M.M., Matthews, B.D., Kirilova, M., Stoytchev, S., Pashkouleva, D., Kavardzhikov, V., 2011. Experimental study
2012. Differentiation of biologic scaffold materials through physiomechanical, of the mechanical properties of human abdominal fascia. Med. Eng. Phys. 33 (1), 1–6.
thermal, and enzymatic degradation techniques. Ann. Surg. 255, 595–604. Klinge, U., Muller, M., Brucker, C., Schumpelick, V., 1998. Application of three-
Deeken, C.R., Thompson Jr, D.M., Castile, R.M., Lake, S.P., 2014. Biaxial analysis of dimensional stereography to assess abdominal wall mobility. Hernia 2, 11–14.
synthetic scaffolds for hernia repair demonstrates variability in mechanical Klinge, U., Klosterhalfen, B., Muller, M., Ottinger, A.P., Schumpelick, V., 1998. Shrinking
anisotropy, non-linearity and hysteresis. J. Mech. Behav. Biomed. Mater. 38, 6–16. of polypropylene mesh in vivo: an experimental study in dogs. Eur. J. Surg. 164 (12),
Doctor, H.G., 2006 Sep. Evaluation of various prosthetic materials and newer meshes for 965–969.
hernia repairs. J Minim. Access Surg. 2 (3), 110–116. Klinge, U., Klosterhalfen, B., Muller, M., Schumpelick, V., 1999. Foreign body reaction to
DuBay, D.A., Wang, X., Adamson, B., Kuzon Jr, W.M., Dennis, R.G., Franz, M.G., 2005. meshes used for the repair of abdominal wall hernias. Eur. J. Surg. 165 (7), 665–673.
Progressive fascial wound failure impairs subsequent abdominal wall repairs: a new Klinge, U., Klosterhalfen, B., Birkenhauer, V., Junge, K., Conze, J., Schumpelick, V., 2002.
animal model of incisional hernia formation. Surgery 137 (4), 463–471. Impact of polymer pore size on the interface scar formation in a rat model. J. Surg.
DuBay, D.A., Choi, W., Urbanchek, M.G., et al., 2007. Incisional herniation induces Res. 103 (2), 208–214.
decreased abdominal wall compliance via oblique muscle atrophy and fibrosis. Ann. Klosterhalfen, B., Klinge, U., 2013. Retrieval study at 623 human mesh explants made of
Surg. 245 (1), 140–146. polypropylene – impact of mesh class and indication for mesh removal on tissue
Earle, D.B., Mark, L.A., 2008. Prosthetic material in inguinal hernia repair: how do I reaction. J. Biomed. Mater. Res. Part B Appl. Biomater. 101 (8), 1393–1399.
choose? Surg. Clin. North Am. 88 (1), 179–201. Klosterhalfen, B., Junge, K., Hermanns, B., Klinge, U., 2002 Aug. Influence of
Ebersole, G.C., Buettmann, E.G., MacEwan, M.R., et al., 2012. Development of novel implantation interval on the long-term biocompatibility of surgical mesh. Br. J. Surg.
electrospun absorbable polycaprolactone (PCL) scaffolds for hernia repair 89 (8), 1043–1048.
applications. Surg. Endosc. 26 (10), 2717–2728. Konerding, M.A., Bohn, M., Wolloscheck, T., et al., 2011. Maximum forces acting on the
Fathi, A.H., Soltanian, H., Saber, A.A., 2012. Surgical anatomy and morphologic abdominal wall: experimental validation of a theoretical modeling in a human
variations of umbilical structures. Am. Surg. 78 (5), 540–544. cadaver study. Med. Eng. Phys. 33 (6), 789–792.
Ferzoco, S., 2016a. Biomechanical evaluation of reinforced bioscaffolds: a new approach Konerding, M.A., Chantereau, P., Delventhal, V., Holste, J.L., Ackermann, M., 2012.
to hernia repair. Poster at Abdominal Wall Reconstruction Conference. Biomechanical and histological evaluation of abdominal wall compliance with
Ferzoco, S., 2016b. Novel reinforced bioscaffolds in non-human primate abdominal wall intraperitoneal onlay mesh implants in rabbits: a comparison of six different state-of-
repair model. Poster at Abdominal Wall Reconstruction Conference. the-art meshes. Med. Eng. Phys. 34 (7), 806–816.
Ferzoco, S., 2016c. Long-term results with various hernia repair materials in non-human Kureshi, A., Vaiude, P., Nazhat, S.N., Petrie, A., Brown, R.A., 2008. Matrix mechanical
primates. Poster at Abdominal Wall Reconstruction Conference. properties of transversalis fascia in inguinal herniation as a model for tissue
Forstemann, T., Trzewik, J., Holste, J., et al., 2011. Forces and deformations of the expansion. J. Biomech. 41 (16), 3462–3468.
abdominal wall – a mechanical and geometrical approach to the linea alba. J. Langenbach, M.R., Sauerland, S., 2013. Polypropylene versus polyester mesh for
Biomech. 44 (4), 600–606. laparoscopic inguinal hernia repair: short-term results of a comparative study. Surg.
Grabel, D., Prescher, A., Fitzek, S., Keyserlingk, D.G., Axer, H., 2005. Anisotropy of Sci. 4 (1), 29–34.
human linea alba: a biomechanical study. J. Surg. Res. 124 (1), 118–125. Langenbach, M.R., Schmidt, J., Ubrig, B., Zirngibl, H., 2008. Sixty-month follow-up after
Grasa, J., Sierra, M., Lauzeral, N., Munoz, M.J., Miana-Mena, F.J., Calvo, B., 2016. Active endoscopic inguinal hernia repair with three types of mesh: a prospective randomized
behavior of abdominal wall muscles: experimental results and numerical model trial. Surg. Endosc. 22 (8), 1790–1797.
formulation. J. Mech. Behav. Biomed. Mater. 61, 444–454. Langer, C., Neufang, T., Kley, C., Liersch, T., Becker, H., 2001. Central mesh recurrence
Greca, F.H., de Paula, J.B., Biondo-Simoes, M.L., et al., 2001. The influence of differing after incisional hernia repair with Marlex – are the meshes strong enough? Hernia 5
pore sizes on the biocompatibility of two polypropylene meshes in the repair of (3), 164–167.
abdominal defects. Experimental study in dogs. Hernia 5 (2), 59–64. Lerdsirisopon, S., Frisella, M.M., Matthews, B.D., Deeken, C.R., 2011. Biomechanical
Gudmundsson, F.F., Viste, A., Gislason, H., Svanes, K., 2002. Comparison of different evaluation of potential damage to hernia repair materials due to fixation with helical
methods for measuring intra-abdominal pressure. Intensive Care Med. 28 (4), titanium tacks. Surg. Endosc. 25 (12), 3890–3897.
509–514. Levillain, A., Orhant, M., Turquier, F., Hoc, T., 2016. Contribution of collagen and elastin
Hernandez, B., Pena, E., Pascual, G., et al., 2011. Mechanical and histological fibers to the mechanical behavior of an abdominal connective tissue. J. Mech. Behav.
characterization of the abdominal muscle. A previous step to modelling hernia Biomed. Mater. 61, 308–317.
surgery. J. Mech. Behav. Biomed. Mater. 4 (3), 392–404. Lubowiecka, I., 2013a. Mathematical modelling of implant in an operated hernia for
Hernandez-Gascon, B., Pena, E., Melero, H., et al., 2011. Mechanical behaviour of estimation of the repair persistence. Comput. Methods Biomech. Biomed. Eng., 1–9.
synthetic surgical meshes: finite element simulation of the herniated abdominal wall. http://dx.doi.org/10.1080/10255842.2013.807506.
Acta Biomater. 7 (11), 3905–3913. Lubowiecka, I., 2013b. Behaviour of orthotropic surgical implant in hernia repair due to
Hernandez-Gascon, B., Pena, E., Pascual, G., Rodriguez, M., Bellon, J.M., Calvo, B., 2012. the material orientation and abdomen surface deformation. Comput. Methods
Long-term anisotropic mechanical response of surgical meshes used to repair Biomech. Biomed. Eng., 1–11, http://dx.doi.org/10.1080/10255842.2013.789102.
abdominal wall defects. J. Mech. Behav. Biomed. Mater. 5 (1), 257–271. Lyons, M., Winter, D.C., Simms, C.K., 2014. Mechanical characterisation of porcine rectus
Hernandez-Gascon, B., Mena, A., Pena, E., Pascual, G., Bellon, J.M., Calvo, B., 2013. sheath under uniaxial and biaxial tension. J. Biomech. 47 (8), 1876–1884.
Understanding the passive mechanical behavior of the human abdominal wall. Ann. Majumder, A., Scott, J., Novitsky, Y., 2016. Evaluation of the antimicrobial efficacy of a
Biomed. Eng. 41 (2), 433–444. novel Rifampin/Minocycline-coated, non-crosslinked porcine acellular dermal matrix
Hernandez-Gascon, B., Pena, E., Grasa, J., Pascual, G., Bellon, J.M., Calvo, B., 2013. compared to uncoated scaffolds for soft tissue repair. Surg. Innov. 23 (5), 442–455.
Mechanical response of the herniated human abdomen to the placement of different Martin, D.P., Badhwar, A., Shah, D.V., et al., 2013. Characterization of poly-4-
prostheses. J. Biomech. Eng. 135 (5), 51004. hydroxybutyrate mesh for hernia repair applications. J. Surg. Res. 184 (2), 766–773.
Hernandez-Gascon, B., Espes, N., Pena, E., Pascual, G., Bellon, J.M., Calvo, B., 2014. Martins, P., Pena, E., Jorge, R.M., et al., 2012. Mechanical characterization and
Computational framework to model and design surgical meshes for hernia repair. constitutive modelling of the damage process in rectus sheath. J. Mech. Behav.
Comput. Methods Biomech. Biomed. Eng. 17 (10), 1071–1085. Biomed. Mater. 8, 111–122.
Hjort, H., Mathisen, T., Alves, A., Clermont, G., Boutrand, J.P., 2012. Three-year results Melman, L., ED, J., CR, D., et al., 2010. Evaluation of acute fixation strength for
from a preclinical implantation study of a long-term resorbable surgical mesh with mechanical tacking devices and fibrin sealant versus polypropylene suture for
time-dependent mechanical characteristics. Hernia 16, 191–197. laparoscopic ventral hernia repair. Surg. Innov. 17 (4), 285–290.
Hollinsky, C., Sandberg, S., 2007. Measurement of the tensile strength of the ventral Melman, L., Jenkins, E.D., Hamilton, N.A., et al., 2011. Histologic and biomechanical
abdominal wall in comparison with scar tissue. Clin. Biomech. 22 (1), 88–92. evaluation of a novel macroporous polytetrafluoroethylene knit mesh compared to
Hollinsky, C., Sandberg, S., Koch, T., Seidler, S., 2008. Biomechanical properties of lightweight and heavyweight polypropylene mesh in a porcine model of ventral
lightweight versus heavyweight meshes for laparoscopic inguinal hernia repair and incisional hernia repair. Hernia 15 (4), 423–431.
their impact on recurrence rates. Surg. Endosc. 22 (12), 2679–2685. Muller, M., Klinge, U., Conze, J., Schumpelick, V., 1998. Abdominal wall compliance after
Hollinsky, C., Kolbe, T., Walter, I., et al., 2009. Comparison of a new self-gripping mesh Marlex mesh implantation for incisional hernia repair. Hernia 2, 113–117.
with other fixation methods for laparoscopic hernia repair in a rat model. J. Am. Coll. Muysoms, F.E., Antoniou, S.A., Bury, K., et al., 2015. European hernia society guidelines
Surg. 208 (6), 1107–1114. on the closure of abdominal wall incisions. Hernia 19 (1), 1–24.
Hwang, W., Carvalho, J.C., Tarlovsky, I., Boriek, A.M., 1985. Passive mechanics of canine Oh, C.S., Won, H.S., Kwon, C.H., Chung, I.H., 2008. Morphologic variations of the
internal abdominal muscles. J. Appl. Physiol. 98 (5), 1829–1835. umbilical ring, umbilical ligaments and ligamentum teres hepatis. Yonsei Med. J. 49
Jenkins, E.D., Melman, L., Deeken, C.R., Greco, S.C., Frisella, M.M., Matthews, B.D., 2011. (6), 1004–1007.
Biomechanical and histologic evaluation of fenestrated and nonfenestrated biologic Orenstein, S.B., Saberski, E.R., Kreutzer, D.L., Novitsky, Y.W., 2012. Comparative analysis
mesh in a porcine model of ventral hernia repair. J. Am. Coll. Surg. 212 (3), 327–339. of histopathologic effects of synthetic meshes based on material, weight, and pore
Junge, K., Klinge, U., Prescher, A., Giboni, P., Niewiera, M., Schumpelick, V., 2001. size in mice. J. Surg. Res. 176 (2), 423–429.
Elasticity of the anterior abdominal wall and impact for reparation of incisional Pachera, P., Pavan, P.G., Todros, S., Cavinato, C., Fontanella, C.G., Natali, A.N., 2016. A
hernias using mesh implants. Hernia 5 (3), 113–118. numerical investigation of the healthy abdominal wall structures. J. Biomech. 49 (9),
Kalaba, S., Gerhard, E., Winder, J.S., Pauli, E.M., Haluck, R.S., Yang, J., 2016. Design 1818–1823.
strategies and applications of biomaterials and devices for Hernia repair. Bioact. Pascual, G., Rodriguez, M., Gomez-Gil, V., Garcia-Honduvilla, N., Bujan, J., Bellon, J.M.,

426
C.R. Deeken, S.P. Lake Journal of the Mechanical Behavior of Biomedical Materials 74 (2017) 411–427

2008. Early tissue incorporation and collagen deposition in lightweight Simon-Allue, R., Calvo, B., Oberai, A.A., Barbone, P.E., 2016. Towards the mechanical
polypropylene meshes: bioassay in an experimental model of ventral hernia. Surgery characterization of abdominal wall by inverse analysis. J. Mech. Behav. Biomed.
144 (3), 427–435. Mater. 66, 127–137.
Peeters, E., van Barneveld, K.W., Schreinemacher, M.H., et al., 2013. One-year outcome Smietanski, M., Bury, K., Tomaszewska, A., Lubowiecka, I., Szymczak, C., 2012.
of biological and synthetic bioabsorbable meshes for augmentation of large Biomechanics of the front abdominal wall as a potential factor leading to recurrence
abdominal wall defects in a rabbit model. J. Surg. Res. 180 (2), 274–283. with laparoscopic ventral hernia repair. Surg. Endosc. 26 (5), 1461–1467.
Petro, C.C., Nahabet, E.H., Criss, C.N., et al., 2015. Central failures of lightweight Song, C., Alijani, A., Frank, T., Hanna, G., Cuschieri, A., 2006. Elasticity of the living
monofilament polyester mesh causing hernia recurrence: a cautionary note. Hernia abdominal wall in laparoscopic surgery. J. Biomech. 39 (3), 587–591.
19 (1), 155–159. Song, C., Alijani, A., Frank, T., Hanna, G.B., Cuschieri, A., 2006. Mechanical properties of
Podwojewski, F., Ottenio, M., Beillas, P., Guerin, G., Turquier, F., Mitton, D., 2013. the human abdominal wall measured in vivo during insufflation for laparoscopic
Mechanical response of animal abdominal walls in vitro: evaluation of the influence surgery. Surg. Endosc. 20 (6), 987–990.
of a hernia defect and a repair with a mesh implanted intraperitoneally. J. Biomech. Todros, S., Pavan, P.G., Pachera, P., Natali, A.N., 2017. Synthetic surgical meshes used in
46 (3), 561–566. abdominal wall surgery: Part II-Biomechanical aspects. J. Biomed. Mater. Res. B
Podwojewski, F., Ottenio, M., Beillas, P., Guerin, G., Turquier, F., Mitton, D., 2014. Appl. Biomater. 105, 892–903.
Mechanical response of human abdominal walls ex vivo: effect of an incisional hernia Tomaszewska, A., Lubowiecka, I., Szymczak, C., et al., 2013. Physical and mathematical
and a mesh repair. J. Mech. Behav. Biomed. Mater. 38, 126–133. modelling of implant-fascia system in order to improve laparoscopic repair of ventral
Poulose, B.K., Shelton, J., Phillips, S., et al., 2012 Apr. Epidemiology and cost of ventral hernia. Clin. Biomech. 28 (7), 743–751.
hernia repair: making the case for hernia research. Hernia 16 (2), 179–183. Tran, D., Mitton, D., Voirin, D., Turquier, F., Beillas, P., 2014. Contribution of the skin,
Rath, A., Zhang, J., Chevrel, J., 1997. The sheath of the rectus abdominis muscle: an rectus abdominis and their sheaths to the structural response of the abdominal wall
anatomical and biomechanical study. Hernia 1, 139–142. ex vivo. J. Biomech. 47 (12), 3056–3063.
Rohrnbauer, B., Mazza, E., 2013. A non-biological model system to simulate the in vivo Tran, D., Podwojewski, F., Beillas, P., et al., 2016. Abdominal wall muscle elasticity and
mechanical behavior of prosthetic meshes. J. Mech. Behav. Biomed. Mater. 20, abdomen local stiffness on healthy volunteers during various physiological activities.
305–315. J. Mech. Behav. Biomed. Mater. 60, 451–459.
Rutkow, I.M., 2003 Oct. Demographic and socioeconomic aspects of hernia repair in the van Os, J.M., Lange, J.F., Goossens, R.H., et al., 2006. Artificial midline-fascia of the
United States in 2003. Surg. Clin. North Am. 83 (5), 1045–1051 (v–vi). human abdominal wall for testing suture strength. J. Mater. Sci. Mater. Med. 17 (8),
Saberski, E.R., Orenstein, S.B., Novitsky, Y.W., 2011. Anisotropic evaluation of synthetic 759–765.
surgical meshes. Hernia 15 (1), 47–52. Voskerician, G., Gingras, P.H., Anderson, J.M., 2006. Macroporous condensed poly
Sahoo, S., DeLozier, K.R., Dumm, R.A., Rosen, M.J., Derwin, K.A., 2014. Fiber-reinforced (tetrafluoroethylene). I. In vivo inflammatory response and healing characteristics. J.
dermis graft for ventral hernia repair. J. Mech. Behav. Biomed. Mater. 34, 320–329. Biomed. Mater. Res. A 76 (2), 234–242.
Schug-Pass, C., Lippert, H., Kockerling, F., 2010. Mesh fixation with fibrin glue (Tissucol/ Voskerician, G., Jin, J., White, M.F., Williams, C.P., Rosen, M.J., 2010. Effect of
Tisseel(R)) in hernia repair dependent on the mesh structure-is there an optimum biomaterial design criteria on the performance of surgical meshes for abdominal
fibrin-mesh combination?-Investigations on a biomechanical model. Langenbecks hernia repair: a pre-clinical evaluation in a chronic rat model. J. Mater. Sci. Mater.
Arch.Surg. 395, 569–574. Med. 21 (6), 1989–1995.
Scott, J.R., Deeken, C.R., Martindale, R.G., Rosen, M.J., 2016. Evaluation of a fully Welty, G., Klinge, U., Klosterhalfen, B., Kasperk, R., Schumpelick, V., 2001. Functional
absorbable poly-4-hydroxybutyrate/absorbable barrier composite mesh in a porcine impairment and complaints following incisional hernia repair with different
model of ventral hernia repair. Surg. Endosc. 30 (9), 3691–3701. polypropylene meshes. Hernia 5 (3), 142–147.
Simon-Allue, R., Montiel, J.M., Bellon, J.M., Calvo, B., 2015. Developing a new Xu, H., Wan, H., Sandor, M., et al., 2008. Host response to human acellular dermal matrix
methodology to characterize in vivo the passive mechanical behavior of abdominal transplantation in a primate model of abdominal wall repair. Tissue Eng. Part A 14
wall on an animal model. J. Mech. Behav. Biomed. Mater. 51, 40–49. (12), 2009–2019.
Simon-Allue, R., Hernandez-Gascon, B., Leoty, L., Bellon, J.M., Pena, E., Calvo, B., 2016. Zuvela, M., Galun, D., Djuric-Stefanovic, A., Palibrk, I., Petrovic, M., Milicevic, M., 2014.
Prostheses size dependency of the mechanical response of the herniated human Central rupture and bulging of low-weight polypropylene mesh following recurrent
abdomen. Hernia 20, 839–848. incisional sublay hernioplasty. Hernia 18 (1), 135–140.

427

You might also like