Journal of Biomechanics 110 (2020) 109970

Contents lists available at ScienceDirect

Journal of Biomechanics
journal homepage: www.elsevier.com/locate/jbiomech
www.JBiomech.com

Effect of cracks on the local deformations of articular cartilage

Amin Komeili a, Saad Luqman b, Salvatore Federico b,a, Walter Herzog a,b,⇑
a
Human Performance Laboratory, Faculty of Kinesiology, The University of Calgary, Canada
b
Department of Mechanical and Manufacturing Engineering, The University of Calgary, Canada

a r t i c l e i n f o a b s t r a c t

Article history: Despite significant evidence regarding the increased risk of cartilage degeneration due to traumatic inju-
Accepted 21 July 2020 ries to joints, there is still a lack of understanding of the mechanisms underlying osteoarthritis develop-
ment following a joint injury. Injuries in knee cartilage are often characterized by lesions or tears. In
addition to acute traumatic joint injuries, microscale damages, which may form because of wear, are
Keywords: thought to be a contributing factor in the development of osteoarthritis.
Crack While the overall function of a joint may not be affected by the presence of microcracks, we hypothe-
Articular cartilage
sized that strain magnification in the vicinity of microcracks might be significant. We tested this hypoth-
Compression test
Local deformations
esis by creating partial cuts in articular cartilages and measuring the strain within 20 mm from the edge of
these cuts. Measurements were made in the superficial and middle zones of articular cartilage extract
samples. We found that local strain in the vicinity of cuts is magnified by a factor of 1.2–1.6 compared
to strains in intact regions for nominal compressions exceeding 5%. For nominal compressions of less than
5%, no strain magnification was detected in the vicinity of the cracks. We concluded that articular carti-
lage cracks magnify local strains by damaging the structural integrity and decreasing the fluid pressure in
the matrix.
Ó 2020 Elsevier Ltd. All rights reserved.

1. Introduction
Damage in cartilage may occur as a result of acute injuries or
degenerative diseases. Cartilage tears and fractures are common
in sports injuries and traffic accidents, and are examples of the for-
mer, while collagen defibrillation and microscale surface lesions
caused by osteoarthritis (OA) are examples of the latter. Increasing
sedentary lifestyles, aging, and obesity contribute to an exponen-
tial rate of increase of OA, and the growing participation in high-
risk recreational and competitive sports might be the cause for
the increasing rate of cartilage injuries in active and athletic popu-
lations (Arendt and Dick, 1995; Chow et al., 2004; Jones et al.,
2001; Martínez-González et al., 1999; Mithöfer et al., 2005). Acute
injuries of joints are associated with an increased risk of develop-
ing OA (Davis et al., 1989; Gelber et al., 2000; von Porat et al.,
2004).
In previous studies, the effects of load magnitude, load fre-
quency, hydration, and viscoelasticity on damage propagation in
cartilage have been investigated (Chin-Purcell and Lewis, 1996;
Espino et al., 2014; Fick and Espino, 2012, 2011; Fulcher et al.,
⇑ Corresponding author at: Human Performance Laboratory, Faculty of Kinesiol-
ogy, The University of Calgary, Canada.
E-mail address: wherzog@ucalgary.ca (W. Herzog).
2009; Lewis and Johnson, 2001; Murray et al., 2001; H Sadeghi
et al., 2015; Hamid Sadeghi et al., 2015; Stok and Oloyede, 2003,
2007; Verteramo and Seedhom, 2007). Studies aimed at the quali-
tative analysis of crack propagation in cartilage applied compres-
sive loads characterized by strain rates and peak stresses in the
range of 0.007–0.7 s
1 , and 7–14 MPa, respectively, (Chen et al.,
2001; McCormack and Mansour, 1997; Morel et al., 2006; Morel
and Quinn, 2004). Slower compressions would induce cell death
without crack propagation (Quinn et al., 2001). For crack property
characterization, such as fracture toughness, for which strict con-
trol of the crack length and force is required, tensile loads were
applied on cartilage samples with geometry constraints (Chin-
Purcell and Lewis, 1996; Oloyede et al., 1992; Rivlin and Thomas,
1953; Silyn-Roberts and Broom, 1990; Stok and Oloyede, 2007,
2003). Cartilage damage has been reported to result in increased
water content (Kurz et al., 2001; Torzilli et al., 1999), increased
hydraulic permeability (Thibault et al., 2002), loss of glycosamino-
glycan (DiMicco et al., 2004; Kurz et al., 2001; Patwari et al., 2003),
loss of collagen (Thibault et al., 2002), decreased chondrocytes via-
bility (Alexander et al., 2013; Backus et al., 2011; Craig, 2003;
Lewis et al., 2003; Torzilli et al., 1999), changes in gene expression
(Irie et al., 2003; Lohmander et al., 2003, 1994), and decreased
load-bearing capacity of joints (Morel et al., 2006; Owen and
Wayne, 2006; Thambyah and Broom, 2007).

https://doi.org/10.1016/j.jbiomech.2020.109970
0021-9290/Ó 2020 Elsevier Ltd. All rights reserved.
2 A. Komeili et al. / Journal of Biomechanics 110 (2020) 109970
Microscale damages on the articular surface of cartilage, in the
form of microcracks, are also thought to contribute to the develop-
ment of OA (Madry et al., 2012). However, little attention has been
devoted to discovering the mechanisms underlying the propaga-
tion of microcracks. Methods to measure microscale (i.e., 10–
100 mm) deformations of cartilage in regions near the loaded site
have only been developed recently (Alexander et al., 2013;
Bartell et al., 2015). Indirect evidence, such as high cell death
(Bartell et al., 2015), and results of numerical models (Komeili
et al., 2019) suggest that excessive deformation occurs in the vicin-
ity of cracks, sometimes referred to as the damage zone (Hull,
1970). However, the state of deformation within the few microm-
eters of a microcrack has never been measured experimentally.
This leaves an important, unexplored gap in understanding the
microscale mechanobiology of cartilage in the early stages of OA
when microcracks start to form at the cartilage surface. Knowledge
of the real-time, local deformations of cartilage in the damage zone
may prove crucial information in the effort to develop ideal scaf-
folds with functional properties that promote tissue regeneration
and provide proper resistance to mechanical loading.
Therefore, the objective of this work was to investigate the
changes in local strain distribution of cartilage in the vicinity of
microcracks. Combined with external loading data, this informa-
tion may be beneficial in informing the design of scaffold struc-
tures and validating numerical models.
2. Material and Methods
2.1. Sample preparation
Cylindrical osteochondral plugs were harvested from skeletally
immature pig knee joints (n = 5, with an average age of ~6 months
and an average weight of ~ 100 kg). Samples (n = 10, mean ± 1SD
cartilage thickness = 1,543 ± 504 mm) were fixed in a custom-
designed compression testing device (Komeili et al., 2018a). The
thickness of cartilage was measured at 3 different locations from
the microscopy images, and the mean value was used to calculate
the applied strain. During mechanical testing, samples were fully
immersed in phosphate-buffered saline (PBS) solution to prevent
dehydration (Fig. 1). The thickness of the samples was measured
at three locations using light microscopy, and the average value
was used as a reference for calculating the nominal applied strain.
2.2. Crack simulation
To simulate cartilage cracks, vertical cuts were made in the
superficial zone (SZ) and the middle zone (MZ) of the cartilage
explants prior to mechanical tests (Fig. 2-a). Cuts were made using
a custom-made blade with a thickness and height of 0.08 mm and
0.7 mm, respectively. The blade was fixed in a custom-designed
compression testing device (Komeili et al., 2018a) and actuated
Fig. 1. Schematic representation of the compression system (Komeili et al., 2018a). The 6-mm-diameter semi-cylindrical sample (7) was fixed in the sample holder (9) with
its flat face in front of a multi-photon microscope. The compressive axial load was applied using a piezo-actuator (2). The compression plate (6) had the same size and shape
as the cartilage explant.
by a piezoelectric motor to a pre-determined depth at a speed of
200 mm/s. Cuts of 4–7% and 15–16% of the total cartilage thickness
were made in SZ and MZ, respectively, which translated into cuts
of 50 – 87.5 lm, and 187.5 – 200 lm, respectively.
2.3. Microscopy
The deformation field in cartilage can be characterized by the
local axial strains in the direction of the cartilage thickness and
in a plane perpendicular to the cartilage thickness. In this study,
the local strains were measured using rectangular fiducial markers
of dimension 15x15 mm that were photo-bleached into the extra-
cellular matrix (ECM). Photo-bleaching was done using a 105
mW laser (InSight DeepSee-OL, Spectra-Physics, CA, USA)
(Komeili et al., 2018a). Two markers were photo-bleached within
a distance of 20 mm from the cut edges (damage zone), and these
are labelled L-D and R-D in Fig. 2-a. At the same depth, two addi-
tional markers were photo-bleached at least 70 mm from the cut
(intact area), and these are labelled L-I and R-I in Fig. 2-a.
Upon mechanical loading, the cartilage was continuously
imaged using a multi-photon excitation microscope (FVMPE-RS,
Olympus, Tokyo, Japan; field of view 509  300 lm2; pixel size:
0.314 mm  0.314 mm; pixel dwell time: 2 ms; imaging rate: 1.5
frame/second). Details of the microscopy technique can be found
in (Komeili et al., 2018a).
2.4. Loading protocol
A tare load of 0.02 N was applied for 5 min to ensure that there
was initial contact between the compression plate and the carti-
lage surface. For the samples with an SZ cut, a linear ramp com-
pression was applied at a rate of 0.2% per second until a 10%
nominal applied strain was reached (Fig. 3). For the samples with
MZ cuts, the corresponding parameters were 0.3% per second and
15%, respectively. The linear ramp compression was followed by
a stress relaxation phase for 10 min. The compression plate was
an impermeable half-cylinder steel plate with a diameter of
6 mm, simulating an unconfined compression configuration.
2.5. Strain measurements
The 2D images obtained during cartilage loading were analyzed
using the open-source software (ImageJ, NIH, USA). The locations
of the 4 corners for each square marker were manually digitized
from the 2D images at defined time points. We evaluated the strain
of each marker following standard continuum mechanical argu-
ments (Fig. 4).
The configuration map, /, relates points X in the reference (un-
deformed) configuration, fBg; to points x in the current (deformed)
configuration, /ðBÞ. The deformation gradient F (with components
F iK ¼ /i;K ¼ @/=@X K ) maps the material vector M (representing the
 A. Komeili et al. / Journal of Biomechanics 110 (2020) 109970 3

Fig. 2. Images of a cartilage sample in unloaded and loaded conditions. A pair of squares were laser burned on the left (right) side of the cartilage cut; the squares close to the
cut and in the intact area were labelled L-D(R-D) and L-I(R-I), respectively. (a) a superficial cut (f = 0.05) before starting the compression and (b) with a 10% nominal applied
strain. (c) A cut in the middle zone (f = 0.15) in the unloaded condition, and (d) with a 15% nominal applied strain.

segment joining X to a ‘‘very close” material point P) into a spatial 1 T

E¼ ðF F
IÞ ð4Þ
vector m (representing the segment joining the current positions 2
x ¼ /ðXÞ and p ¼ /ðP Þ in the current configuration), given by and obtain
m ¼ FM: ð1Þ jjmjj2
jjMjj2 ¼ 2M:½EM  ð5Þ
The squared norm (or magnitude) of the deformed vector m is In two dimensions, and in Cartesian X-Y coordinates (see Fig. 4),
given by the component expression of Equation (5) reads
jjmjj2 ¼ m:m ¼ ðFM Þ:ðFM Þ ¼ M:½ðF T FÞM ð2Þ
jjmjj2
jjMjj2 ¼ 2EXX M 2X þ 4EXY M X M Y þ 2EYY M2Y ð6Þ
Comparing the squared norm of m with the squared norm of the
where we used the symmetry of E, i.e., EYX ¼ EXY .
undeformed vector m, we obtain
Having the X-Y coordinates for 4 corners of the fiducial markers,
jjmjj2
jjMjj2 ¼ m:m
M:M ¼ M:½ðF T FÞM
M:ðIM Þ 6 vectors M ðaÞ were reconstructed in the reference (undeformed)
configuration and the corresponding 6 vectors mðaÞ were recon-
¼ M:½ðF T F
IÞM ð3Þ
structed in the current (deformed) configuration. This resulted in
where we used the identity tensor I in the substitution a system of 6 equations in the form (6) in the 3 unknown Green-
M:M ¼ M:IM. Now, we recall the definition of the Green- Lagrange strain components EXX , EXY and EYY , an overdetermined
Lagrange strain, i.e., system of equations that was solved using the least square method.
4 A. Komeili et al. / Journal of Biomechanics 110 (2020) 109970

Fig. 3. The primary vertical axis (black curves): The force response of intact and cut cartilage samples, respectively. The microscale cut did not affect the load response of the
cartilage. Secondary axis: a 10% ramp compression protocol that was used for studying cartilage samples with SZ cuts. A similar force relaxation behaviour to the one shown
here for SZ cut samples was also observed for samples with MZ cuts, even though these latter samples were loaded to a 15% nominal strain.

Fig. 4. Representation of the deformation. The distance between points X and Pand points x and p is ‘‘large” for ease of graphical representation.

3. Results
3.1. Axial strains - superficial zone (f = 0.05)
Axial strains in regions close to the cut edges (damage zone),
marked with D, and in intact regions, marked with I, are shown
in Fig. 5. Compressive axial strains increased with increasing nom-
inal applied strain and during stress relaxation in the SZ and the
MZ (Fig. 5 and Fig. 6).
Axial strains were significantly larger in the damage zone com-
pared to the intact area when the applied nominal strain was
greater than 5% (Fig. 5 and Fig. 6). For example, for a 10% dynamic
nominal strain, the compressive strain in the damage zone was 23%
greater than the strain measured in the intact area. Similar results
were obtained during stress relaxation, where the average axial
strains in the damage zone and the intact area were 0.71 and
0.60, respectively (Fig. 5).
3.2. Axial strains - middle zone (f = 0.15)
The axial strains in the MZ were calculated for three levels of
nominal compression, 5%, 10%, and 15% (Fig. 6). Similarly, to the

Fig. 5. The axial strain in the damage zone (D) and intact area (I) located in the SZ. Markers L-D and L-R were located on the left side while markers R-D and R-I were located
on the right side of the cut.
 A. Komeili et al. / Journal of Biomechanics 110 (2020) 109970 5

Fig. 6. Compressive axial strains in the middle zone during the loading and the relaxation phase in the intact (I) and damage (D) regions. R: right side of the cut, L: left side of
the cut.

SZ results, 10% was the minimum nominal strain for which statis-
tically significant differences were measured between the axial
strains of the intact region and the damage zone in the MZ. The
compressive axial strains were consistently greater in the damage
zone with respect to the intact area. During stress relaxation, the
average axial strains were 0.50 and 0.38 in the damage zone and
intact area, respectively. The largest difference in axial strains
occurred for an applied nominal dynamic strain of 10%, where
strains were greater by a factor of 1.6 in the damage zone com-
pared to those measured in the intact area.
3.3. Axial strains - validation
2018b). Fig. 8 shows a comparison of cartilage axial strains at
f = 0.15 in the intact region of the current study and three other
studies (Gao et al., 2013; Grillo et al., 2015; Komeili et al.,
2018b). The axial strains measured in the current study were smal-
ler than those reported earlier (Komeili et al., 2018b) at corre-
sponding nominal strains of 10% and 15%. However, the results
of the paired t-test showed that the difference was not significant
at the level of p less than 0.05.The reported local strains by Gao
et al. (Gao et al., 2013) and Grillo et al. (Grillo et al., 2015) at
12.5% applied nominal strain were in the range of what we
obtained at 10% and 15% nominal strains.

In Fig. 7-a and 7-c, we compare the axial strains in the damage
zone located on the left and right side of the cut, i.e., marker L-D vs.
R-D. No difference was observed between the axial strains in the
damage zone at the left and right sides of the cut through the
entire compression phase. Similarly, no difference was observed
between the axial strains in the intact areas: locations L-I and R-I
(Fig. 7-b and -d).
Previously, we studied the continuous strain variations
throughout the depth of intact cartilage samples (Komeili et al.,
3.4. Shear strains
In-plane XY shear strains as a function of location and applied
nominal strains are shown in Fig. 9. Positive and negative XY shear
strains were always less than 5%, and the strain variations were
relatively large, specifically in the damage zone. In the middle
zone, the XY shear strains were approximately zero in the intact
area, while they were non-zero in the damage zone of the cartilage
samples (Fig. 9-b).

Fig. 7. Comparison of axial strain distributions within the damage zone (a, c), and the intact area (b, d).
6 A. Komeili et al. / Journal of Biomechanics 110 (2020) 109970

Fig. 8. Comparison of local axial strains in the intact area in the present study with the strain distributions measured by [*]: Komeili et al. (Komeili et al., 2018b), [**]: Gao
et al. (Gao et al., 2013), and [***] Grillo et al. (Grillo et al., 2015). Markers represent the average values. Bars show 1 standard deviation.

Fig. 9. XY shear strain in the damage zone and the intact area during the dynamic testing and for the stress relaxation (S.R.) states.

4. Discussion permeability, respectively. In the present study, with d ¼ 1:5mm,

The fundamental basis of the analysis in this work is the ability
to characterize the real-time local deformations around partial-
depth cracks in articular cartilage to complement previous mea-
surements that have been made for static, steady-state loading
conditions. Therefore, a ramp compression was selected that
allowed for imaging the deformations and interpreting the results.
To verify that the applied strain rate induced a dynamic condition,

2
the minimum strain rate s
1 m ¼ HA :j:d condition of Mow et al.
(Mow et al., 1980) was used, where sm ; d; HA , and j are the
characteristic time, sample thickness, modulus of elasticity, and
HA ¼ 0:5MPa, and j ¼ 0:001mm4 ðN:sÞ
1 (Komeili et al., 2019), the
applied strain rate of 0.2% s
1 was larger than the minimum strain
rate of 0.022% s
1 that ensures a poroelastic behavior, including
significant fluid pressurization. Our experimental setup allows for
studying the changes in the local and overall mechanical response
of intact and damaged cartilage with superficial cuts.
The local cartilage matrix deformations were measured within a
20 mm distance from the cut edges in the SZ and MZ under static
and dynamic loading conditions. For cartilage samples with super-
ficial cuts, the ultimate compression was limited to 10% because of
the large strain magnification in the SZ, which distorted the
 A. Komeili et al. / Journal of Biomechanics 110 (2020) 109970
markers so much that it was hard to obtain reliable results. The
reduced strain magnification in the MZ compared to the SZ allowed
for compression of the samples up to 15% nominal strain and
confidently locating the corners of the fiducial squares.
Local strains in articular cartilage have typically been measured
using the local displacements of the nuclei of chondrocytes
(Schinagl et al., 1996), but the resulting strains represent the aver-
age of strain variations between the two target nuclei. The spatial
resolution of local strains achieved in this manner may not be ade-
quate to identify the true differences of local tissue deformations
obtained at different locations of cartilage samples, and subtle dif-
ferences in strains, as observed here for the intact and damaged
cartilage, may not be discernible with confidence. In this study,
the deformations were measured directly from the deformation
of the cartilage ECM, thereby reducing uncertainty in the strain
measurements and improving the spatial resolution.
Although the horizontal distance between two reference mark-
ers was smaller than 200 lm, it is possible that the difference in
strains in the intact and damaged zones (Fig. 5 and Fig. 6) was
caused by the non-homogeneity in the properties of the cartilage
samples. However, the non-significant difference between axial
strains at site L-D vs. site R-D and site L-I vs. site R-I (Fig. 7) sug-
gests that the axial strain distribution between two sites at the
same depth within the image frame is uniform. Hence, the strain
variation between intact and damaged zones is likely caused by
the cut, rather than variations in the material properties. The good
agreement between the strains in the intact area measured in this
study with previously reported experimental measurements (Gao
et al., 2013; Komeili et al., 2018b, 2018a; Zhang et al., 2012), which
employed different techniques for local strain measurements, sug-
gests that our results are valid (see Fig. 8). As expected, the axial
strains tended to increase as the nominal compressive strains
increased. The local strain measurements suggest that the cut
(damage) had no visible effect (within the resolution of our sys-
tem) on the axial compressive strains for compressions smaller
than 5% (Fig. 5 and Fig. 6). However, for nominal compressive
strains of 10% and higher, the damaged regions of the cartilage
had greater compressive strains compared to the intact regions,
in both the SZ and MZ, indicative of a softer ECM near the cut
edges. The most likely cause for the greater strain close to the
cut is the disrupted structural integrity of the matrix.
We did not measure fluid pressure in our experiments.
However, local fluid pressure changes around the cut edges could
be inferred from the differences between strains in the dynamic
and the static states. The average dynamic compressive strain in
the SZ for a nominal compression of 10% was 0.52 close to the
cut edge and 0.40 in the intact region, for a 31% difference between
the two locations (Fig. 7-a and b). The corresponding static strain
values after 10 min of stress relaxation were 0.72 and 0.60, for a
20% difference between sites. The only variable parameter between
the dynamic and the static state was the absence of fluid pressure
in the static state. In the stress relaxation phase, the applied com-
pression was held constant, and the compressive force decreased
primarily because of a reduction in fluid pressure. We speculate
that, in the presence of the cut, which may act like a free-flow sur-
face, fluid pressure decreases, which in turn lowers the local tissue
stiffness, and consequently, increases the local deformation in
regions close to the cut. The same observations as for SZ samples
were also made for MZ samples: i.e., differences between strains
in the damage and intact regions were 38% and 35% for the
dynamic and static tests, respectively. The increased strains in
the damaged compared to the intact regions may be the primary
reason for the great cell death observed in areas of damaged carti-
lage tissues (Backus et al., 2011). As a result, the proteoglycan
synthesis would be inhibited around the cartilage crack and may
constitute a biological mechanism for damage propagation in
7
cartilage. The results of the present study might be most directly
applicable to the evaluation of appropriate properties for engi-
neered cartilage constructs. Such constructs may be used to ‘‘seal”
macro cracks between native tissue and osteochondral implants
(Obradovic et al., 2001). The findings of this study suggest that,
on average, a 20% increase in local strains should be expected
within a distance of 20 lm from the crack edges compared to
intact regions of the cartilage.
The overall compressive tissue force response did not change
after the introduction of the cut (Fig. 3), suggesting that the carti-
lage mechanics is not affected by superficial cuts for small applied
loads. This might be a reason, in addition to the lack of sensory
nerves in cartilage, for OA to go unnoticed in its early stages. How-
ever, local tissue deformations around the cut increased signifi-
cantly, which may affect the mechanotransduction of cells in the
damaged areas and initiate cartilage degradation. In advanced
OA, cartilage microcracks increase in number and then may affect
the overall tissue mechanics. At this stage, joint contact pressure
distributions may become non-uniform, resulting in stress concen-
trations that may cause pain in the underlying bone.
During compression, our square-shaped markers deformed into
rectangles, suggesting near-zero shear strains in the middle zone of
the intact tissue (Fig. 9-b). This result was expected, as the loading
conditions were uniaxial, unconfined compression. The shear
strains in the intact regions of the SZ were small (Fig. 9-a) and
within the error of our detection limits. The mean shear strains
in the damage zone were also small and within the limits of our
detection ability (Fig. 9-a).
Our system was designed to simulate a single vertical cut in the
SZ and MZ of cartilage (Fig. 2) to simiulate cracks on the articular
surface of cartilage. However, clinically observed microcracks are
oriented randomly (Wong et al., 2008; Yu et al., 2016). A more real-
istic experimental model thus should include randomly oriented
cuts. Identifying the exact location of the tip of a cut for strain mea-
surements was challenging, and the effect of cuts on tissue defor-
mation could not always be captured successfully. Therefore, strain
deformations at the exact tip of a cut, and their effect on the cut
propagation could not be fully captured here and awaits proper
investigation. Another limitation of this study was its relatively
low applied strain rate, which was due to the limited image acqui-
sition time. Although the strain rate was high enough to attain
dynamic conditions, it did not exceed the restraining capacity of
the collagen network. Therefore, our experimental protocol is not
suggested for the study of crack propagation or quantifying the
fracture mechanics parameters.
5. Conclusion
The experimental technique developed for this study allowed
measurements of strain deformations close to a simulated crack
in articular cartilage. It was shown that the effects of a microcrack
on whole tissue mechanics are not detectable, but changes to local
strains are substantial. These substantial strain magnifications may
be the reason for crack propagation, and once of sufficient size,
cracks will also affect the tissue mechanics. This study may con-
tribute to a more accurate characterization of the mechanobiology
of cartilage in response to mechanical trauma or the progression
from mild to severe OA when the crack size and crack number
increase as the disease progresses.
Acknowledgments
This work was supported by The Canada Research Chair Pro-
gramme for Molecular and Cellular Biomechanics [grant number
950-230603, 2015], The Canadian Institutes of Health Research
8 A. Komeili et al. / Journal of Biomechanics 110 (2020) 109970
(CIHR) Foundation scheme grant [grant number MOP-111205,
2015], The Killam Foundation, and Alberta Innovates Health Solu-
tions [award number 201610102, 2016]. The authors have no com-
peting interests to declare. This work was carried out in accordance
with the University of Calgary guidelines with ethical approval
AC18-0082.
References
Alexander, P.G., Song, Y., Taboas, J.M., Chen, F.H., Melvin, G.M., Manner, P.A., Tuan, R.
S., 2013. Development of a Spring-Loaded Impact Device to Deliver Injurious
Mechanical Impacts to the Articular Cartilage Surface. Cartilage 4, 52–62.
https://doi.org/10.1177/1947603512455195.
Arendt, E., Dick, R., 1995. Knee Injury Patterns Among Men and Women in
Collegiate Basketball and Soccer. Am. J. Sports Med. 23, 694–701. https://doi.
org/10.1177/036354659502300611.
Backus, J.D., Furman, B.D., Swimmer, T., Kent, C.L., McNulty, A.L., DeFrate, L.E.,
Guilak, F., Olson, S.A., 2011. Cartilage viability and catabolism in the intact
porcine knee following transarticular impact loading with and without articular
fracture. J. Orthop. Res. 29, 501–510. https://doi.org/10.1002/jor.21270.
Bartell, L.R., Fortier, L.A., Bonassar, L.J., Cohen, I., 2015. Measuring microscale strain
fields in articular cartilage during rapid impact reveals thresholds for
chondrocyte death and a protective role for the superficial layer. J. Biomech.
48. https://doi.org/10.1016/j.jbiomech.2015.05.035.
Chen, C.T., Burton-Wurster, N., Borden, C., Hueffer, K., Bloom, S.E., Lust, G., 2001.
Chondrocyte necrosis and apoptosis in impact damaged articular cartilage. J.
Orthop. Res. 19, 703–711. https://doi.org/10.1016/S0736-0266(00)00066-8.
Chin-Purcell, M.V., Lewis, J.L., 1996. Fracture of articular cartilage. J. Biomech. Eng.
118, 545–556. https://doi.org/10.1115/1.2796042.
Chow, J.C.Y., Hantes, M.E., Houle, J.B., Zalavras, C.G., 2004. Arthroscopic autogenous
osteochondral transplantation for treating knee cartilage defects: A 2- to 5-year
follow-up study. Arthrosc. - J. Arthrosc. Relat. Surg. 20, 681–690. https://doi.org/
10.1016/j.arthro.2004.06.005.
Craig, S.T.T., 2003. Effects of in vivo joint loading on articular cartilage chondrocyte
viability. University of Calgary.
Davis, M.A., Ettinger, W.H., Neuhaus, J.M., Cho, S.A., Hauck, W.W., 1989. The
association of knee injury and obesity with unilateral and bilateral
osteoarthritis of the knee. Am. J. Epidemiol. 130, 278–288. https://doi.org/
10.1093/oxfordjournals.aje.a115334.
DiMicco, M.A., Patwari, P., Siparsky, P.N., Kumar, S., Pratta, M.A., Lark, M.W., Kim, Y.-
J., Grodzinsky, A.J., 2004. Mechanisms and kinetics of glycosaminoglycan
release following in vitro cartilage injury. Arthritis Rheum. 50, 840–848.
https://doi.org/10.1002/art.20101.
Espino, D.M., Shepherd, D.E.T., Hukins, D.W.L., 2014. Viscoelastic properties of
bovine knee joint articular cartilage: dependency on thickness and loading
frequency. BMC Musculoskelet. Disord. 15, 205. https://doi.org/10.1186/1471-
2474-15-205.
Fick, J.M., Espino, D.M., 2012. Articular cartilage surface failure: An investigation of
the rupture rate and morphology in relation to tissue health and hydration.
Proc. Inst. Mech. Eng. Part H J. Eng. Med. 226, 389–396. https://doi.org/10.1177/
0954411912439824.
Fick, J.M., Espino, D.M., 2011. Articular cartilage surface rupture during
compression: Investigating the effects of tissue hydration in relation to
matrix health. J. Mech. Behav. Biomed. Mater. 4, 1311–1317. https://doi.org/
10.1016/j.jmbbm.2011.04.018.
Fulcher, G.R., Hukins, D.W.L., Shepherd, D.E.T., 2009. Viscoelastic properties
of bovine articular cartilage attached to subchondral bone at high
frequencies. BMC Musculoskelet. Disord. 10, 61. https://doi.org/10.1186/1471-
2474-10-61.
Gao, L.L., Zhang, C.Q., Yang, Y.B., Shi, J.P., Jia, Y.W., 2013. Depth-dependent strain
fields of articular cartilage under rolling load by the optimized digital image
correlation technique. Mater. Sci. Eng. C 33, 2317–2322. https://doi.org/
10.1016/j.msec.2013.01.054.
Gelber, A.C., Hochberg, M.C., Mead, L.A., Wang, N.Y., Wigley, F.M., Klag, M.J., 2000.
Joint injury in young adults and risk for subsequent knee and hip osteoarthritis.
Ann. Intern. Med. 133. https://doi.org/10.7326/0003-4819-133-5-200009050-
00007.
Grillo, A., Guaily, A., Giverso, C., Federico, S., 2015. Non-linear model for
compression tests on articular cartilage. J. Biomech. Eng. 137. https://doi.org/
10.1115/1.4030310.
Hull, D., 1970. Effect of crazes on the propagation of cracks in polystyrene. J. Mater.
Sci. 5, 357–363.
Irie, K., Uchiyama, E., Iwaso, H., 2003. Intraarticular inflammatory cytokines in acute
anterior cruciate ligament injured knee. Knee 10, 93–96.
Jones, S.J., Lyons, R.A., Sibert, J., Evans, R., Palmer, S.R., 2001. Changes in sports
injuries to children between 1983 and 1998: comparison of case series. J. Public
Health Med. 23, 268–271.
Komeili, A., Abusara, Z., Federico, S., Herzog, W., 2018a. A Compression System for
Studying Depth Dependent Mechanical Properties of Articular Cartilage Under
Dynamic Loading Conditions. Med. Eng. Phys. 60, 103–108. https://doi.org/
10.1016/j.medengphy.2018.07.004.
Komeili, A., Abusara, Z., Federico, S., Herzog, W., 2018b. Effect of Strain Rate on
Transient Local Strain Variations in Articular Cartilage. JMBBM.
Komeili, A., Chau, W., Herzog, W., 2019. Effects of macro-cracks on the load bearing
capacity of articular cartilage. Biomech. Model. Mechanobiol. 18, 1371–1381.
https://doi.org/10.1007/s10237-019-01149-x.
Kurz, B., Jin, M., Patwari, P., Cheng, D.M., Lark, M.W., Grodzinsky, A.J., 2001.
Biosynthetic response and mechanical properties of articular cartilage after
injurious compression. J. Orthop. Res. 19, 1140–1146. https://doi.org/10.1016/
S0736-0266(01)00033-X.
Lewis, J.L., Deloria, L.B., Oyen-Tiesma, M., Thompson, R.C., Ericson, M., Oegema, T.R.,
2003. Cell death after cartilage impact occurs around matrix cracks. J. Orthop.
Res. 21, 881–887. https://doi.org/10.1016/S0736-0266(03)00039-1.
Lewis, J.L., Johnson, S.L., 2001. Collagen architecture and failure processes in bovine
patellar cartilage. J. Anat. 199, 483–492.
Lohmander, L.S., Atley, L.M., Pietka, T.A., Eyre, D.R., 2003. The release of crosslinked
peptides from type II collagen into human synovial fluid is increased soon after
joint injury and in osteoarthritis. Arthritis Rheum. 48, 3130–3139. https://doi.
org/10.1002/art.11326.
Lohmander, L.S., Roos, H., Dahlberg, L., Hoerrner, L.A., Lark, M.W., 1994. Temporal
patterns of stromelysin-1, tissue inhibitor, and proteoglycan fragments in
human knee joint fluid after injury to the cruciate ligament or meniscus. J.
Orthop. Res. 12, 21–28. https://doi.org/10.1002/jor.1100120104.
Madry, H., Luyten, F.P., Facchini, A., 2012. Biological aspects of early osteoarthritis.
Knee Surgery, Sport. Traumatol. Arthrosc. https://doi.org/10.1007/s00167-011-
1705-8
Martínez-González, M.Á., Martínez, J.A., Hu, F.B., Gibney, M.J., Kearney, J., 1999.
Physical inactivity, sedentary lifestyle and obesity in the European Union. Int. J.
Obes. 23, 1192–1201. https://doi.org/10.1038/sj.ijo.0801049.
McCormack, T., Mansour, J.M., 1997. Reduction in tensile strength of cartilage
precedes surface damage under repeated compressive loading in vitro. J.
Biomech. 31, 55–61. https://doi.org/10.1016/S0021-9290(97)00103-6.
Mithöfer, K., Peterson, L., Mandelbaum, B.R., Minas, T., 2005. Articular Cartilage
Repair in Soccer Players with Autologous Chondrocyte Transplantation. Am. J.
Sports Med. 33, 1639–1646. https://doi.org/10.1177/0363546505275647.
Morel, V., Berutto, C., Quinn, T.M., 2006. Effects of damage in the articular surface on
the cartilage response to injurious compression in vitro. J. Biomech. 39, 924–
930. https://doi.org/10.1016/j.jbiomech.2005.01.026.
Morel, V., Quinn, T.M., 2004. Cartilage injury by ramp compression near the gel
diffusion rate. J. Orthop. Res. 22, 145–151. https://doi.org/10.1016/S0736-0266
(03)00164-5.
Mow, V.C., Kuei, S.C., Lai, W.M., Armstrong, C.G., 1980. Biphasic creep and stress
relaxation of articular cartilage in compression? Theory and experiments. J.
Biomech. Eng. 102, 73–84.
Murray, R.C., Birch, H.L., Lakhani, K., Goodship, A.E., 2001. Biochemical composition
of equine carpal articular cartilage is influenced by short-term exercise in a site-
specific manner. Osteoarthr. Cartil. 9, 625–632. https://doi.org/10.1053/
joca.2001.0462.
Obradovic, B., Martin, I., Padera, R.F., Treppo, S., Freed, L.E., Vunjak-Novakovic, G.,
2001. Integration of engineered cartilage. J. Orthop. Res. 19, 1089–1097. https://
doi.org/10.1016/S0736-0266(01)00030-4.
Oloyede, A., Flachsmann, R., Broom, N.D., 1992. The Dramatic Influence of Loading
Velocity on the Compressive Response of Articular Cartilage. Connect. Tissue
Res. 27, 211–224. https://doi.org/10.3109/03008209209006997.
Owen, J.R., Wayne, J.S., 2006. Influence of a superficial tangential zone over
repairing cartilage defects: implications for tissue engineering. Biomech. Model.
Mechanobiol. 5, 102–110. https://doi.org/10.1007/s10237-006-0022-5.
Patwari, P., Cook, M.N., DiMicco, M.A., Blake, S.M., James, I.E., Kumar, S., Cole, A.A.,
Lark, M.W., Grodzinsky, A.J., 2003. Proteoglycan degradation after injurious
compression of bovine and human articular cartilage in vitro: interaction with
exogenous cytokines. Arthritis Rheum. 48, 1292–1301. https://doi.org/10.1002/
art.10892.
Quinn, T.M., Allen, R.G., Schalet, B.J., Perumbuli, P., Hunziker, E.B., 2001. Matrix and
cell injury due to sub-impact loading of adult bovine articular cartilage
explants: effects of strain rate and peak stress. J. Orthop. Res. 19, 242–249.
https://doi.org/10.1016/S0736-0266(00)00025-5.
Rivlin, R.S., Thomas, A.G., 1953. Rupture of rubber. I. Characteristic energy for
tearing. J. Polym. Sci. 10, 291–318. https://doi.org/10.1002/
pol.1953.120100303.
Sadeghi, H., Espino, D.M., Shepherd, D.E.T., 2015a. Variation in viscoelastic
properties of bovine articular cartilage below, up to and above healthy gait-
relevant loading frequencies. Proc. Inst. Mech. Eng. Part H J. Eng. Med. 229, 115–
123. https://doi.org/10.1177/0954411915570372.
Sadeghi, H., Shepherd, D.E.T., Espino, D.M., 2015b. Effect of the variation of loading
frequency on surface failure of bovine articular cartilage. Osteoarthr. Cartil. 23,
2252–2258. https://doi.org/10.1016/j.joca.2015.06.002.
Schinagl, R.M., Ting, M.K., Price, J.H., Sah, R.L., 1996. Video Microscopy to Quantitate
the Inhomogeneous Equilibrium Strain Within Articular Cartilage During
Confined Compression. Ann. Biomed. Eng. 24, 500–512.
Silyn-Roberts, H., Broom, N.D., 1990. Fracture behaviour of cartilage-on-bone in
response to repeated impact loading. Connect. Tissue Res. 24, 143–156. https://
doi.org/10.3109/03008209009152430.
Stok, K., Oloyede, A., 2007. Conceptual fracture parameters for articular cartilage.
Clin. Biomech. 22, 725–735. https://doi.org/10.1016/j.clinbiomech.2007.03.005.
Stok, K., Oloyede, A., 2003. A qualitative analysis of crack propagation in articular
cartilage at varying rates of tensile loading. Connect. Tissue Res. 44, 109–120.
Thambyah, A., Broom, N., 2007. On how degeneration influences load-bearing in the
cartilage–bone system: a microstructural and micromechanical study.
Osteoarthr. Cartil. 15, 1410–1423. https://doi.org/10.1016/j.joca.2007.05.006.
 A. Komeili et al. / Journal of Biomechanics 110 (2020) 109970
Thibault, M., Poole, A.R., Buschmann, M.D., 2002. Cyclic compression of cartilage/
bone explants in vitro leads to physical weakening, mechanical breakdown of
collagen and release of matrix fragments. J. Orthop. Res. 20, 1265–1273. https://
doi.org/10.1016/S0736-0266(02)00070-0.
Torzilli, P.A., Grigiene, R., Borrelli, J., Helfet, D.L., 1999. Effect of Impact Load on
Articular Cartilage: Cell Metabolism and Viability, and Matrix Water Content. J.
Biomech. Eng. 121, 433. https://doi.org/10.1115/1.2835070.
Verteramo, A., Seedhom, B.B., 2007. Effect of a single impact loading on the
structure and mechanical properties of articular cartilage. J. Biomech. 40, 3580–
3589. https://doi.org/10.1016/j.jbiomech.2007.06.002.
von Porat, A., Roos, E.M., Roos, H., 2004. High prevalence of osteoarthritis 14 years
after an anterior cruciate ligament tear in male soccer players. Ann Rheum Dis
63, 269–273. https://doi.org/10.1136/ard.2003.008136.
9
Wong, B.L., Bae, W.C., Chun, J., Gratz, K.R., Lotz, M., Sah, R.L., Sah, R.L., 2008.
Biomechanics of cartilage articulation: Effects of lubrication and degeneration
on shear deformation. Arthritis Rheum. 58, 2065–2074. https://doi.org/
10.1002/art.23548.
Yu, J., Zhang, M., Zhang, W., 2016. Biomechanical Prediction of Crack Angle Effect on
Local Tensile Stress of Articular Cartilage. J. Bone Reports Recomm. 02. https://
doi.org/10.4172/2469-6684.100030.
Zhang, C.Q., Gao, L.L., Dong, L.M., Liu, H.Y., 2012. Depth-dependent normal strain of
articular cartilage under sliding load by the optimized digital image correlation
technique. Mater. Sci. Eng. C 32, 2390–2395. https://doi.org/10.1016/j.
msec.2012.07.012.