Journal of Biomechanics 48 (2015) 1407–1411

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Effects of degeneration on the compressive and tensile properties of human meniscus Kristine M. Fischenich a, Jackson Lewis a, Kirk A. Kindsfater b, Travis S. Bailey a,c, Tammy L. Haut Donahue a,d,n a

School of Biomedical Engineering, Colorado State University, Fort Collins, CO, USA Orthopedic Center of the Rockies, Fort Collins, CO, USA c Department of Chemical and Biological Engineering, Colorado State University, Fort Collins, CO USA d Department of Mechanical Engineering, Colorado State University, Fort Collins, CO, USA b

art ic l e i nf o

a b s t r a c t

Article history: Accepted 17 February 2015

Healthy menisci function within the joint to prevent the underlying articular cartilage from excessive loads. Understanding how mechanical properties of menisci change with degeneration can drive future therapeutic studies to prevent this degeneration. Thus, the goal of this study was to characterize both compressive and tensile moduli of human menisci with varying degrees of gross damage due to osteoarthritis (OA). Twenty four paired menisci were collected from total knee joint replacement patients and the menisci were graded on a scale from 0–4 according to level of gross meniscal degeneration with 0¼normal and 4¼ full tissue maceration. Each meniscus was then sectioned into anterior and posterior regions and subjected to indentation relaxation tests. Samples were sliced into 1 mm thick strips, made into dumbbells using a custom punch, and pulled to failure. Significant decreases in instantaneous compressive modulus were seen in the lateral posterior region between grades 0 and 1 (36% decrease) and in the medial anterior regions between grades 1 and 2 (67% decrease) and 1 and 3 (72% decrease). Changes in equilibrium modulus where seen in the lateral anterior region between grades 1 and 2 (35% decrease), lateral posterior region between grades 0–2 (41% decrease), and medial anterior regions between grades 1 and 2 (59% decrease), 1 and 3 (67% decrease), 2 and 4 (54% decrease), and 3 and 4 (42% decrease). No significant changes were observed in tensile modulus across all regions and degenerative grades. The results of this study demonstrate the compressive moduli are affected even in early stages of gross degeneration, and continue to decrease with increased deterioration. However, osteoarthritic menisci retain a tensile modulus similar to that of previously reported healthy menisci. This study highlights progressive changes in meniscal mechanical compressive integrity as level of gross tissue degradation increases, and thus, early interventions should focus on restoring or preserving compressive integrity. & 2015 Elsevier Ltd. All rights reserved.

Keywords: Knee Meniscus Osteoarthritis Compressive modulus Equilibrium modulus

1. Introduction Menisci function within the knee joint to provide stability (Clark and Ogden, 1983) and protect the underlying articular cartilage (Mow et al., 1992). Damage to meniscal tissue can lead to the development of OA (Hunter et al., 2011). In fact, McGonagle et al., has suggested that many tissues, including menisci, likely contribute to the etiology of OA (McGonagle et al., 2010). Damage to menisci can be initiated from classical wear and tear with age, or from traumatic injury (Greis et al., 2002; Lohmander et al., 2007; Zhang and Jordan, 2010). Regardless, the mostly avascular meniscal tissue has limited natural healing ability (Bursac et al., 2009) and thus, treatment modalities to

n Correspondence to: Department of Mechanical Engineering, Colorado State University, 1374 Campus Delivery, Fort Collins, CO 80523, USA. E-mail address: [email protected] (T.L. Haut Donahue).

http://dx.doi.org/10.1016/j.jbiomech.2015.02.042 0021-9290/& 2015 Elsevier Ltd. All rights reserved.

prevent degenerative changes in meniscal tissue could be developed to slow or prevent development of OA. The mechanical properties of menisci are complex, including both tension/compression nonlinearities as well as time dependent behavior. A number of studies have investigated the mechanical properties of healthy human menisci. These previous investigations include testing in both confined (Joshi et al., 1995; Martin Seitz et al., 2013) and unconfined environments (Chia and Hull, 2008; Leslie et al., 2000; Moyer et al., 2013, 2012; Sandmann et al., 2009; Sweigart et al., 2004). Additionally, studies have investigated the mechanical properties of the tissue under tensile loading (Lechner et al., 2000; Tissakht and Ahmed, 1995). However, the majority of these studies only characterized the healthy medial meniscus. Indentation tests investigating both instantaneous and equilibrium compressive moduli, as well as tensile modulus from pull to failure tests have not been performed in a comprehensive study to date of both the lateral and medial menisci with varying amounts of gross tissue damage due to osteoarthritis.

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Knowledge of degenerative changes in mechanical properties may provide rational for targeted treatment options for patients who have experienced meniscal degeneration and thus may prevent end-stage OA resulting in a total knee replacement. In this study, human menisci were recovered and mechanically tested from total knee arthroplasty (TKA) patients. It was hypothesized that the mechanical properties of the meniscal tissue will decrease as gross meniscal degeneration increases.

Fig. 1. Representation of slicing process for tensile testing.

2. Methods 2.1. Sample Harvesting Twenty four human menisci (paired lateral and medial) were obtained from TKA patients. All patients provided written consent to allow excised meniscal tissue from the surgery to be used for mechanical analysis. This study was approved by the institutional review board at Colorado State University. Patients (male n¼11, female n¼ 13) had a mean age of 57.874.6 years and a mean BMI of 31.975.5 kg/m2. Samples were collected following surgery and photographed for later assessment. All samples were wrapped in phosphate buffered saline (PBS) solution soaked gauze and frozen until mechanically tested. Meniscal mechanical properties have been shown to be regionally dependent (Chia and Hull, 2008; Fithian et al., 1990; Killian et al., 2010; Sweigart et al., 2004); therefore each meniscus was sectioned into anterior and posterior regions for testing. The general shape of human menisci has been previously documented (Haut et al., 2000), and therefore tissue loss based on an abnormal shape can be determined. Four blinded graders independently assigned each meniscal region a gross morphological grade from 0–4, similar to a previous study (Pauli et al., 2011) and the average grade, rounded to the nearest whole number, was used. A degenerative grade of 0¼ normal; 1¼ fraying at inner borders, tibial or femoral surface fibrillation; 2¼ partial substance tears, fraying, tibial or femoral side fibrillations; 3¼ near full substance tears, minor loss of tissue; 4¼full substance tears, major loss of tissue. 2.2. Indentation relaxation testing Specimens were kept hydrated with a 0.9% phosphate buffered saline solution before and during indentation relaxation tests (Fischenich et al., 2014), which were run on a servo hydraulic test system (Bionic Model 370.02 MTS Corp, Eden Prairie, MN). The water bath containing the sample was attached to a multi-degree of freedom camera mount, and an x–y plate allowing for the indentation surface to be oriented normal to the indenter and centered on the specimen respectively. A spherical tip with a diameter of 1.59 mm was used as an indenter, and loads were recorded using an 8.9 N load cell (Futek LSB200, Irvine, California). Due to the time dependent nature of the knee menisci in compression, both the equilibrium and instantaneous moduli were computed. All samples were preloaded to 20 mN, and preliminary tests determined a relaxation time of 1200 s resulted in equilibrium conditions. Specimens were indented 0.4 mm, which was determined based on the average thickness of indentation locations, or approximately 12% strain, which has been determined to be the average physiological strain in the axial direction (Tissakht and Ahmed, 1995). Hertzian contact (Eq. 1) was applied and used to determine the instantaneous and equilibrium moduli. The contact equation assumed contact between an elastic half space and a sphere where F is the force, R is the radius of the indenter, d is the indentation depth, E1 and υ1 are the elastic modulus and Poisson's ratio of the tissue, and E2 and υ2 are the elastic modulus and Poisson's ratio of the indenter. The elastic modulus and Poisson's ratio of the indenter tip were 210 GPa and 0.3, respectively. Based on a previous study (Sweigart et al., 2004) Poisson's ratio of the menisci was assumed to be 0.001 for all regions. E1 ¼ 

ð1  υ1 Þ2    2  ð1 Eυ2 2 Þ

3F 4R1=2 d3=2

Fig. 2. Dimensional measurements of custom punch showing specimen thickness to be 1 mm.

ð1Þ

2.3. Tension testing Following indentation, specimens were sliced into 1 mm thick strips using a custom drop cutter. The first slice was taken from the periphery and slices were continued until a slice fell below the necessary dimensions (Fig. 1). A custom punch (Fig. 2) was then used to create dumbbell shaped samples with the long axis aligned parallel to the circumferential direction fibers. Graphite powder was used to create a random speckle pattern on the narrow section of the sample which was analyzed to determine strain (Fig. 3). Polishing paper (grade 100) was attached to the ends of the specimen using ethyl cyanoacrylate to ensure a nonslip grip surface. Specimens were placed into thin film grips (Imada FC-20) and attached to a 44.5 N load cell (Futek LSB303, Irvine, California) and pulled to failure (Bionic Model 370.02 MTS Corp, Eden Prairie, MN). All samples were preloaded to 50 mN

Fig. 3. Image of meniscal tensile test sample showing the random graphite powder speckling.

K.M. Fischenich et al. / Journal of Biomechanics 48 (2015) 1407–1411 to ensure grip alignment and deformed at 0.1 mm/sec, corresponding to the physiological loading rate of meniscal tissue (Jones et al., 1996). Images were taken throughout each test using a video camera (Point Grey Flea3 FW-14S3M-C, Richmond, BC, Canada) with a 25 mm f/1.4 2/3″ fixed focal machine vision lens (Fujinon HF25HA-1B). The acquisition of load cell and video data was synchronized with an internal trigger and images were collected at a rate of 15 frames per second. Samples that failed outside the uniform center portion of the dumbbell were discarded.

2.4. Data analysis Data was processed using MATLAB (Mathworks, Natick, MA) custom written analysis programs. Instantaneous compressive modulus values were assessed at the peak compressive force while equilibrium compressive modulus was assessed at relaxation, or 1200 s. Stress versus strain curves were generated from the tensile data. Using the acquired images and a MATLAB based digital image correlation code (E.M.C. Jones, University of Illinois) the speckle pattern on the tissue was tracked and used to calculate strain within the uniform central region of the tissue. Ultimate strength was determined at the peak force and the tensile modulus was determined from the 25% to the 75% linear portion of the stress strain curve. Since the distance from the outer periphery of the meniscus has been shown to have no effect on circumferential tensile modulus (Lechner et al., 2000), multiple tensile samples within the same region and specimen were averaged.

2.5. Statistics An interclass correlation coefficient (ICC) was performed to determine agreement between the four blinded graders on assessing gross degeneration. Grader agreement was acceptable with ICC values averaging 0.64. The degenerative grade was averaged amongst the four blinded graders and rounded to the nearest whole number. Factorial analysis of variance (ANOVA) with Tukey's post hoc tests (α ¼0.1) were conducted with Minitab statistical software (Minitab15, State College, PA) to assess differences in mechanical properties between degenerative grades within a given hemijoint and region. Factors included hemijoint (medial or lateral), region (anterior or posterior), and grade (0–4). The dependent variables assessed included compressive equilibrium modulus, compressive instantaneous modulus, and tensile modulus. Alpha of 0.1 was chosen to reduce probability of Type II errors and increase power. Hence, significance was taken to be po0.1 for all metrics.

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Table 1 Summary of meniscal samples and morphological degeneration grade. Not all samples were able to be tested in tension due to the degree of damage present. Degeneration grade Lateral Anterior

0 1 2 3 4 Posterior 0 1 2 3 4 Medial Anterior

0 1 2 3 4 Posterior 0 1 2 3 4

Number of samples for indentation testing

Number of samples for tension testing

1 13 8 1 0 8 12 3 1 0

1 10 7 0 0 8 12 2 0 0

1 3 11 6 2 0 6 5 5 3

1 4 7 5 0 0 8 4 2 1

3. Results The majority of lateral menisci received an average grade between 0–2 while the medial meniscus tended to be more deteriorated with a greater number of samples having an average grade of 1–3 (Table 1). The lateral anterior and posterior regions had no samples with an average grade of 4. The medial posterior region had no samples with an average grade of 0. Lateral anterior, lateral posterior, and medial anterior regions showed decreasing instantaneous and equilibrium moduli with increasing degeneration (Figs. 4 and 5). The medial posterior region had no apparent trend in mechanical properties with degeneration. In the lateral posterior region there was an average decrease in instantaneous compressive modulus between samples with grades 0 and 1 of 36% (p¼ 0.07). The medial anterior region showed the greatest change in instantaneous compressive modulus between grades with an average 67% decrease between grade 1 and grade 2 and 73% between grade 1 and 3 (p¼0.02 and p¼0.06 respectively). Changes to the equilibrium compressive modulus were more pronounced with significant decreases between grades of 1–2 in the lateral anterior region (p¼ 0.08), 0–2 in the lateral posterior region (p¼0.09), and 1–2, 1–3, 2–4, and 3–4 in the medial anterior region (p¼0.01, p¼0.04, p¼0.06, and p¼0.02 respectively). Similar to the instantaneous compressive modulus data, the medial anterior region was the most affected by meniscal degeneration, with an average decrease of 56% as degenerative score increased. No significant differences were found between degenerative groups for the tensile modulus (Fig. 6). Average tensile modulus for the lateral anterior region was 128.8762.5 MPa and the lateral posterior was 119.4775.6 MPa. The medial meniscus had a slightly lower average tensile modulus of 112.5756.6 MPa in the anterior region and

Fig. 4. Instantaneous compressive modulus mean with standard deviation. Statistical comparisons were made only between grades within a specific hemijoint and region and only between groups with n4 1 (n ¼1 regions are presented, in a diagonal pattern, but were not included in statistics), *denotes significant difference p o 0.1.

95.9755.6 MPa in the posterior region. Regardless of degenerative grade or region the average strain at failure was 18.275.2%.

4. Discussion The purpose of this study was to do a comprehensive analysis of both the compressive and tensile moduli of human medial and lateral menisci at various stages of gross tissue degradation. Although some degenerative scores within a region could not be compared due to small sample size within that particular group, it is evident there is some negative association between level of meniscal degradation and compressive modulus; supporting the hypothesis of the study.

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Fig. 5. Equilibrium compressive modulus mean with standard deviation. Statistical comparisons were made only between grades within a specific hemijoint and regions and only between groups with n41 (n¼ 1 regions are presented, in a diagonal pattern, but were not included in statistics), *denotes significant difference po 0.1.

Fig. 6. Tensile elastic modulus mean with standard deviation. Statistical comparisons were made only between grades within a specific hemijoint and regions and only between groups with n41 (n¼ 1 regions are presented, in a diagonal pattern, but were not included in statistics), *denotes significant difference p o0.1.

However, there appeared to be no change in tensile modulus with increasing levels of meniscal gross damage due to OA. This data suggests that the compressive modulus is the first and perhaps only change with progressive degeneration, and should be the focus of future therapies. Given the changes in compressive modulus seen in this study, and the association between glycosaminoglycans (GAG) and compressive integrity (Sanchez-Adams et al., 2011), future pharmacological therapies should be targeted at preventing GAG loss. Such therapies have been proposed to similarly treat glycosaminoglycan loss in articular cartilage. Parathyroid hormone (Sampson et al., 2011), Interleukin-1 receptor antagonist (Lotz and Kraus, 2010), matrix-metalloproteinase

inhibitors (DiMicco et al., 2004), and Interleukin-10 (Lotz and Kraus, 2010) are among the potential therapies that can be used to target either restoration of lost GAGs or prevention of glycosaminoglycan loss following a traumatic event. If used early in OA, these therapies may be able to save the compressive mechanical integrity of the menisci, enabling protection of the underlying articular cartilage from excessive loads and thereby halting or slowing the progression of OA. The changes to the compressive properties and the lack of changes to the tensile properties of the tissue might suggest that the collagen fibers are still intact and functioning, but other tissue components such as GAG might be compromised (Sanchez-Adams et al., 2011). GAG is crucial in controlling fluid flow which in turn, under normal compressive loading conditions, creates an internal pressure loading the collagen (Mow et al., 1992). If GAG content is reduced, fluid retention could be compromised (Makris et al., 2011) and load may not be transferred appropriately to the collagen in the in vivo setting. Bursac et al. reported similar findings with compressive properties being independent of collagen content but significantly affected by GAG content (Bursac et al., 2009). Therefore, while the current data suggests that the collagen network is intact, it is unclear if the connective tissue network and load transfer would be functioning in the in vivo situation and properly loading the collagen network. Future studies should investigate this transfer of compressive load to hoop stress in degenerative tissue. Results of the indentation testing of samples in the current study are within the range of previously reported values of human meniscus. Sweigart et al. performed indentation relaxation testing on healthy medial menisci and reported an aggregate modulus of 0.12 MPa (Sweigart et al., 2004). Other confined compression studies have reported equilibrium values 0.23 MPa for the medial meniscus. Values in this study, which fall between 0.04 and 0.3 MPa, were within what one might expect. Equilibrium values of the medial posterior region in this study are lower than those reported for aggregate modulus in the other regions, but match previously reported values (Sweigart et al., 2004) for healthy tissue. Instantaneous compressive modulus is rarely reported in the literature; thus making comparisons to the current study difficult. Moyer et al. reported both equilibrium and instantaneous results from an unconfined creep test, but utilized a nanoindentation test procedure and likely did not penetrate past the randomly aligned surface collagen mesh (Moyer et al., 2012). However, when comparing instantaneous modulus values to equilibrium values, Moyer et al., reported instantaneous values that were approximately three times equilibrium values, which is in agreement with the results from this study. The steady decline in compressive modulus was especially notable in the medial anterior region where significant decreases were seen between almost all degenerative levels. The lateral meniscus had a similar trend of decreasing modulus with increasing degenerative grade within a given region, but fewer significant differences were found which may be attributed to the limited range of samples at certain levels of damage. However, of the three possible comparisons, two were significantly different, suggesting that with increased samples sizes there would likely be more significant differences detected in the lateral hemijoint. Interestingly, the significant changes in the compressive mechanical properties that were seen to occur in the medial anterior and lateral regions did not occur in the medial posterior region regardless of how much degeneration was present. It has been shown in healthy tissue that the medial posterior region has a greater percent of GAGs (Bursac et al., 2009); thus perhaps the higher amount of GAGs in the tissue originally, may enable the medial posterior region to retain its compressive mechanical properties even with gross tissue damage. Surprisingly, the tensile elastic modulus did not seem to be affected by degree of degeneration. In fact, the tension test results almost identically match those for previous studies on healthy human menisci (Lechner et al., 2000; Tissakht and Ahmed, 1995).

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In the current study, the circumferential tensile modulus was seen to be slightly elevated in the anterior regions (121 7 61 MPa) with respect to the posterior regions (110 770 MPa) and the lateral meniscus (124771 MPa) had slightly higher tensile modulus values than the medial meniscus (105758 MPa), in agreement with previous studies. Thus, it would appear that even for these TKA patients, the circumferential tensile modulus does not decrease and remains comparable to healthy human menisci. One limitation of the current study is the small sample size for specific degenerative grade levels of a given region. It is clear from the summary of samples (Table 1) that degeneration was more severe in the medial meniscus compared to the lateral. Additionally the samples were typically not healthy (grade 0), since they were obtained from osteoarthritic joints, nor were they completely macerated (grade 4), as patients typically present with pain and undergo a TKA prior to this extreme level of meniscal degeneration. Tensile samples from a given sample region were also averaged, so any differences in zonal changes (inner or outer) were not accounted for. Previous work has shown for healthy menisci there are no significant differences in tensile modulus across this radial direction (Lechner et al., 2000); however it is not clear if this holds true for osteoarthritic tissue. Expanding the sample size would allow for more analysis, for example assessing the potential of other predictors such as sex and body mass. Future studies should consider a histological analysis of the menisci. This additional data would provide the biochemical composition of the osteoarthritic tissue and shed light on why there are significant changes to the compressive moduli but not the tensile moduli. Specifically assessing glycosaminoglycan and collagen content would be of interest. Work is currently being performed to assess the mechanical changes to the underlying articular cartilage both covered and uncovered by the meniscus and correlate those results to these findings. 5. Conclusions With increased gross meniscal degeneration, compressive modulus decreases in all regions except the medial posterior region. The equilibrium modulus is affected more severely than the instantaneous compressive modulus. Tensile modulus did not appear to be affected with increased meniscal degeneration. This study is of importance as it provides a more comprehensive evaluation of compressive and tensile properties of both the medial and lateral human menisci in tissue with varying degrees of gross damage due to OA. Conflict of interest The authors have no conflict of interest to disclose. Acknowledgments The authors would like to acknowledge Dr. Kirk Kindsfater and his surgical staff at Orthopedic Center of the Rockies for aiding with sample collection. References Bursac, P., Arnoczky, S., York, A., 2009. Dynamic compressive behavior of human meniscus correlates with its extra-cellular matrix composition. Biorheology 46, 227–237.

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Effects of degeneration on the compressive and tensile properties of human meniscus.

Healthy menisci function within the joint to prevent the underlying articular cartilage from excessive loads. Understanding how mechanical properties ...
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