1 Introduction
Articular cartilage is the biological bearing material responsible for load support and lubrication of mammalian joints. The most important functions of articular cartilage, which include lubrication [
1‐
4]), pressurization of interstitial fluid [
1,
5‐
7], mechanical stiffness [
5,
8‐
11], load support [
1,
5‐
7,
12], and stress shielding [
12‐
14], are fundamentally related to the hydration state of the tissue. Although cartilage water content is usually described as a fixed material property on the order of 80%, it is well documented that water content (tissue thickness) is lost during loading [
4,
8,
15‐
19].
McCutchen first measured the fluid exudation process using controlled explant experiments more than 50 years ago and showed that the loss of sample thickness via fluid exudation led to proportionally increased friction over time [
1]. Biphasic modeling, pioneered by Mow and colleagues [
20,
21], has shown that the load-induced exudation response of cartilage is fundamentally the same as that of other porous materials like rocks, soils, sponges, and hydrogels; loading necessarily pressurizes the incompressible interstitial fluid, which subsequently flows toward low pressure outside the porous media according to Darcy’s Law.
While the exudation response of cartilage to static loading is well studied, the rehydration process is less clear. One well-known mechanism for fluid recovery is based on the density of the fixed charges within the tissue. These fixed charges set up an osmotic stress that creates a driving force for rehydration when the cartilage is unloaded [
19,
21‐
23]. In vivo studies of the human knee have shown that recovery rates due to joint unloading are on the order of a few percent per hour [
19,
24] and that the strains accumulated each day are reversed each night [
23]. During the active part of the day, when joints are frequently loaded, tissue strains due to load-induced fluid exudation are large and accumulate quickly (e.g., ~ 50% strain in 90 min) [
15,
19,
24]. However, strains in the human knee at the end of the day remain below ~ 5% [
23], suggesting additional modes of fluid recovery. Eckholm and Inglemark found that mammalian joints recovered thickness during articulation [
17,
25‐
27]; this observation implies a motion-induced recovery mode. In situ measurements by Linn on dog ankles again demonstrated this articulation-induced recovery effect; the recovery from static unloading was slower than that from loaded articulation and many times slower than that from unloaded articulation [
28]. Linn concluded that articulation periodically exposed the dehydrated zones to the bath, which enabled rapid free swelling and net fluid recovery even during loaded articulation. Until recently, activity-induced fluid recovery and retention has been attributed entirely to the migratory nature of our joints [
4,
7,
12,
13].
A few years ago, however, we used in situ strain and solute transport measurements to demonstrate that cartilage can actively recover interstitial hydration during sliding within a constantly loaded stationary contact area that precludes any possible contribution from contact migration [
29‐
31]; we called the phenomenon ‘tribological rehydration’ to reflect the fact that recovery was induced by sliding. While existing theories fail to explain the tribological rehydration phenomenon, our results are consistent with hydrodynamic origins. Furthermore, a hydrodynamic interpretation appears physically plausible given the large body of theoretical research indicating that significant hydrodynamic pressures do develop within joints and significantly affect their tribological behaviors [
32‐
35].
Although the observation of tribological rehydration has provided new and important insights into how joints recover and retain interstitial fluid, nutrients, and mechanical functions, it remains uncertain if tribological rehydration is primarily sliding-induced. Recent observations from Bonnevie et al. [
36], for example, pave the grounds for an alternate hypothesis. They showed that cartilage produces a significant ‘wedge’ at the trailing edge of contact; the squeeze-film effect from the closing of this wedge during sliding reversals can be expected to produce a rehydration effect that depends on the frequency of reversal and, thus, sliding speed in fixed track-length experiments. Since all of our previous studies involved reciprocation, it is impossible to distinguish between the contributions from sliding and the reversals. Our first objective in this paper was to isolate the contribution of sliding alone by eliminating reciprocal wedging with unidirectional sliding. Our second objective was to determine how hydrodynamic factors, namely, speed, load, lubricant composition, and contact geometry, contribute to the tribological rehydration of cartilage.
4 Discussion
This study isolated how sliding contributes to tribological rehydration by eliminating potential contribution from reciprocal wedging. During unidirectional sliding, we observed the same qualitative relationship between rehydration and sliding speed that we observed in our previous reciprocal sliding studies [
29‐
31,
39]; thus, we can reasonably conclude that the tribological rehydration effects observed therein were primarily caused by sliding and less so (if at all) by effects from reciprocation.
Our results were generally consistent with the hydrodynamic hypothesis presented previously [
29,
39]. Rehydration effects increased with sliding speed (Fig.
2) and sample diameter (Fig.
5), each of which is consistent with a hydrodynamic cause. While viscosity was not controlled or measured, it was increased by the HA solution (Fig.
4), which enhanced tribological rehydration. Furthermore, tribological rehydration was diminished at increased loads (Fig.
3), which is consistent with our hypothesis that tribological rehydration reflects a competition between external hydrodynamic pressure (increases with speed) and interstitial pressure [
39] (increases with load). As expected, we observed less competitive rehydration at increased loads when controlling for other conditions.
The observation that load diminished tribological rehydration highlights an important limitation of this and previous studies on the topic. The maximum load we can apply with our current instruments is ~ 5 N; this load typically produces a contact stress of ~ 0.2 MPa, which is below the physiological contact stresses observed in most joints under most conditions (0.5–5 MPa) [
50‐
52]. Based on the findings of this study, we can assume that tribological rehydration rates become less competitive with exudation rates at physiological contact pressures (although the same can be said for migration and osmotic pressure). However, it is also worth pointing out that previous predictions that fluid films form in the joint also imply that hydrodynamic pressures are competitive with contact pressures in vivo [
35,
53,
54]. The degree to which tribological rehydration contributes to fluid recovery at physiological pressures remains an open question but we are currently developing a high force instrument with in situ contact area and pressure measurements to provide the answer.
The observed effect of lubricant composition is non-obvious based on a hydrodynamic interpretation of tribological rehydration. Although HA shear thins [
55], there is no doubt that it increased the viscosity of the PBS lubricant solution under all conditions. We expected competing effects from increased hydrodynamic pressure and increased resistance to interstitial recovery. Our observation that HA reduced the transition speed from 17 to 10 mm/s suggests that HA enhanced hydrodynamic pressurization more than it impeded flow into the porous articular surface. This observation is consistent with the ‘ultra-filtration’ hypothesis from Walker et al. [
53], which suggests that that water preferentially flows into the articular surface, leaving the larger molecules to aggregate at the leading edge of contact [
56]. While their ‘boosted lubrication’ theory was intended to explain the otherwise unlikely formation of hydrodynamic fluid films, our results suggest that the underlying ultra-filtration process, which is independent of fluid film formation, plays important roles in the recovery and long-term retention of interstitial hydration, thickness, mechanical function, and lubrication.
These results generally support a causal role of hydrodynamics in tribological rehydration, but they also reveal one significant departure from theoretical expectations. The smallest sample diameter in this study is typical of the stationary contact area (SCA) cartilage testing configuration, which is often used explicitly to defeat interstitial pressure for the purpose of isolating other effects (e.g., boundary, mixed-mode, and fluid film [
4,
42,
45]). Thus, we expected the smallest sample diameter to eliminate tribological rehydration entirely by compromising the convergence zone and disrupting the dependent hydrodynamic environment. Although trimming the sample to mimic typical SCA conditions significantly impaired tribological rehydration, it failed to prevent it entirely. Although subtle evidence of this fact is found in the cartilage tribology literature, observations of similar friction reductions with increased speeds (> 10 mm/s) have been interpreted as a transition to more traditional mixed-mode lubrication [
4,
42,
45]; Gleghorn and Bonassar, for example, describe this transition as ‘a shift of load support from asperity contact to a fluid film’ [
42]. Our compression measurements suggest that the friction reductions we observed in the SCA are attributable to increased interstitial hydration, pressure, and lubrication with sliding, which appears to have been unanticipated as a possibility prior to our original observation of tribological rehydration [
29]. Our observation of rehydration in the SCA suggests that the friction reductions Gleghorn and Bonassar observed may also have been due to the transfer of load to interstitial pressure rather than hydrodynamic pressure in a partial fluid film. It also indicates that tribological rehydration and interstitial pressure are far more difficult to defeat experimentally, especially at speeds greater than 10 mm/s, than even we appreciated prior to this study. The finding has important implications for how future and previous studies interpret equilibrium in the SCA. Specifically, it is unsafe to assume the absence of interstitial pressure during sliding at equilibrium without the benefit of in situ compression or interstitial pressure measurements. The inability of existing theory to foresee these important functional effects highlights the need for significant improvements in our ability to model the response of cartilage to sliding whether in the joint or under controlled experimental conditions.
Finally, we feel obliged to comment on why tribological rehydration is not more sensitive to sample curvature and diameter. One possibility we have considered is that the unique mechanics of this fibrous tissue (e.g., high tensile stiffness, low shear stiffness [
57]) helps create a micro-wedge at the leading edge of contact with little connection to the observable geometry of the macro-wedge [
31]. This idea has emerged in our minds based primarily on three observations. First, cursory modeling results, which are currently unpublished, have suggested to us that the slopes necessary to support hydrodynamic pressure-induced tribological rehydration must be far shallower than the steep slopes we have observed in the macro-wedge [
30,
31]. Secondly, we find that significant deformations are necessary before we begin detecting tribological rehydration, even at high sliding speeds [
29]. Finally, Bonnevie et al. actually documented their observation of a microscale wedge in response to shear during reciprocal sliding in the SCA [
58]. Thus, the effect of sample diameter may be more directly linked to features that drive the formation of the micro-wedge (e.g., the collagen network, its alignment, and its destruction near the sample perimeter) than those of the macro-wedge. We offer this speculative hypothesis as a starting point for future investigations, modeling efforts, and discussions.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and
institutional affiliations.