Immature bovine cartilage wear by fatigue failure and delamination

Abstract

This study investigated wear damage of immature bovine articular cartilage using reciprocal sliding of tibial cartilage strips against glass or cartilage. Experiments were conducted in physiological buffered saline (PBS) or mature bovine synovial fluid (SF). A total of 63 samples were tested, of which 47 exhibited wear damage due to delamination of the cartilage surface initiated in the middle zone, with no evidence of abrasive wear. There was no difference between the friction coefficient of damaged and undamaged samples, showing that delamination wear occurs even when friction remains low under a migrating contact area configuration. No difference was observed in the onset of damage or in the friction coefficient between samples tested in PBS or SF. The onset of damage occurred earlier when testing cartilage against glass versus cartilage against cartilage, supporting the hypothesis that delamination occurs due to fatigue failure of the collagen in the middle zone, since stiffer glass produces higher strains and tensile stresses under comparable loads. The findings of this study are novel because they establish that delamination of the articular surface, starting in the middle zone, may represent a primary mechanism of failure. Based on preliminary data, it is reasonable to hypothesize that delamination wear via subsurface fatigue failure is similarly the primary mechanism of human cartilage wear under normal loading conditions, albeit requiring far more cycles of loading than in immature bovine cartilage.

Introduction

Osteoarthritis (OA) affects millions of Americans: it is a progressive, complex, multi-tissue joint disease with degenerative changes in the articular cartilage and subchondral bone (Ashkavand et al., 2013), with a long asymptomatic early development and debilitating late stages. OA is viewed today as a disease of the joint as an organ, with inflammation, injury, and changes in bone, articular cartilage, and synovial fluid (SF) as potential driving forces. The degradation of the extracellular matrix (ECM) components of cartilage is key to the progression of the disease (Dijkgraaf et al., 1995, Loeser, 2013).

Regardless of the initiating factors of OA, cartilage stresses produced by sliding contact of the articular layers mediate the progression of tissue degeneration. The mechanisms by which stresses produce progressive tissue degeneration via mechanical pathways remain poorly understood. OA is often described as a natural process of wear and tear associated with aging, or an initiating traumatic event. The cartilage mechanics literature has mostly focused on examining the friction coefficient µ as a surrogate for understanding wear and tear in cartilage (Ateshian and Mow, 2005). The friction coefficient of articular cartilage is not constant (McCutchen, 1962). The lowest reported value of µ for cartilage against glass is typically µ ≈ 0.002 (Krishnan et al., 2004), which is exceptionally low. However, µ may rise over time, depending on loading conditions, to achieve values as high as µ ≈ 0.15 against glass (Krishnan et al., 2004), or even µ ≈ 0.5 against stainless steel (Forster and Fisher, 1996, Forster and Fisher, 1999). These values are expected to be detrimental to the integrity of cartilage, though they are not normally achieved under physiologic loading conditions (Ateshian, 2009).

When cartilage slides against cartilage, it produces a migrating contact area (MCA) configuration that sustains elevated interstitial fluid load support (Caligaris and Ateshian, 2008). As a result, the friction coefficient remains low for sustained durations; for bovine and human cartilage in saline, it is typically µ ≈ 0.025; for human cartilage in SF it is only slightly lower, µ ≈ 0.020 (Caligaris and Ateshian, 2008, Caligaris et al., 2009). Implicitly, a low value of µ has been assumed to produce low wear while an elevated value could lead to significant wear. Despite the prominence of this hypothesized mechanism, only a few cartilage wear studies have been performed under controlled conditions, most notably by investigating PRG4 knockout mice (Jay et al., 2007), since PRG4/lubricin has been shown to reduce the friction coefficient of cartilage in vitro (Schmidt et al., 2007) and prevent degeneration in vivo (Flannery et al., 2009). However, it has also been shown that advancing osteoarthritic degeneration does not increase the friction coefficient of human cartilage (Caligaris et al., 2009), suggesting that OA wear may progress without a concomitant increase in µ.

Wear is a generally complex phenomenon that may manifest itself in different ways. In the engineering tribology literature, a broad range of wear mechanisms are reported, many of which are mostly applicable to metals and other artificial surfaces (Moore, 1975). However, some of these mechanisms may also be candidates for wear of biological tissues. These mechanisms include abrasive wear, which removes particulates of matter from the bearing surfaces, third-body wear, where particulate matter causes further abrasion of the bearing surfaces, fatigue wear with delamination, where the load-bearing material fails below the surface due to fatigue and the failure propagates until a lamina shears off, and chemical wear, where breakdown of the bearing material is initiated by chemical reactions, such as proteolysis in biological tissues. Other phenomena such as adhesion or stick–slip friction have also been proposed as initiators of cartilage damage (Han and Eriten, 2018, Lee et al., 2013).

Biological tissues, such as articular cartilage and tendons have been reported to fail in fatigue under both tension and compression. In studying tensile fatigue of human articular cartilage, Weightman found that fatigue life is reduced with an increase in tensile stress and the tissue’s resistance to fatigue decreases with age (Weightman, 1976). In another study, Weightman et al. showed that fatigue failure of articular cartilage is a possibility in the span of an average lifetime (Weightman et al., 1978). Additionally, in a study of fatigue of human tendons, Schechtman and Bader found a highly significant relationship between stress and $\ln N$, where $N$ is the number of cycles to failure, suggesting that tendons fail in fatigue (Schechtman and Bader, 1997). Recent studies confirmed that fatigue is the failure mechanism of articular cartilage when under cyclic compression loading (Kaplan et al., 2017, Vazquez et al., 2019).

In our recent study on immature bovine cartilage (Oungoulian et al., 2015), wear tests were performed on cartilage plugs sliding against glass or various metals used in orthopaedic implants, producing delamination of the superficial zone with negligible abrasive wear. These results were consistent with the fact that delamination is a clinically recognized symptom of OA (Meachim, 1982, Pritzker et al., 2006). However, a potential limitation of that study was our adoption of a stationary contact area (SCA) testing configuration, which promoted loss of interstitial fluid pressurization over time. It could be argued that the elevated friction coefficient achieved under those conditions would not occur under more physiological loading conditions. Furthermore, with prolonged wear testing, complete delamination and removal of the top layer of these plugs was observed (Oungoulian et al., 2015), raising the possibility that the initiating failure resulted from edge effects between the flat counterface material and the circular edge of the plug surface.

Therefore, in this study, we performed experiments on immature bovine cartilage to test our primary hypothesis (H1) that delamination wear occurs even when the friction coefficient µ remains low under a migrating contact area configuration (MCA) (Caligaris and Ateshian, 2008, Caligaris et al., 2009, Northwood et al., 2007). We used large, rectangular cartilage strips harvested from the medial or lateral tibial plateau, loaded with a glass lens under low physiological contact stresses, such that the contact area remains well within the strip boundaries to avoid edge effects.

Based on prior literature findings regarding the role of SF boundary lubricants on the reduction of friction and wear (Flannery et al., 2009, Jay et al., 2007, Schmidt et al., 2007), we also tested the hypothesis (H2) that SF delays the onset of cartilage delamination when compared to physiological buffered saline (PBS).

Based on our previously reported model for the dependence of the frictional force on interstitial fluid load support and the solid-on-solid contact area fraction (Ateshian et al., 1998, Soltz et al., 2003), we tested the hypothesis (H3) that loading cartilage against cartilage delays the onset of delamination wear compared to testing glass on cartilage, since contacting porous cartilage layers exhibit a much smaller solid-on-solid contact area fraction than porous cartilage contacting impermeable glass.