Elsevier

Journal of Biomechanics

Volume 42, Issue 9, 19 June 2009, Pages 1163-1176
Journal of Biomechanics

Review
The role of interstitial fluid pressurization in articular cartilage lubrication

https://doi.org/10.1016/j.jbiomech.2009.04.040Get rights and content

Abstract

Over the last two decades, considerable progress has been reported in the field of cartilage mechanics that impacts our understanding of the role of interstitial fluid pressurization on cartilage lubrication. Theoretical and experimental studies have demonstrated that the interstitial fluid of cartilage pressurizes considerably under loading, potentially supporting most of the applied load under various transient or steady-state conditions. The fraction of the total load supported by fluid pressurization has been called the fluid load support. Experimental studies have demonstrated that the friction coefficient of cartilage correlates negatively with this variable, achieving remarkably low values when the fluid load support is greatest. A theoretical framework that embodies this relationship has been validated against experiments, predicting and explaining various outcomes, and demonstrating that a low friction coefficient can be maintained for prolonged loading durations under normal physiological function. This paper reviews salient aspects of this topic, as well as its implications for improving our understanding of boundary lubrication by molecular species in synovial fluid and the cartilage superficial zone. Effects of cartilage degeneration on its frictional response are also reviewed.

Introduction

Articular cartilage is the bearing material of diarthrodial joints. Its primary function is to support and redistribute joint contact forces, and to reduce friction and wear. This function is closely dependent on the structure of this connective soft tissue, as reviewed in this paper. Interest in cartilage lubrication can be traced back to the early part of the twentieth century (Jones, 1936; Macconaill, 1932) and a review of the earlier cartilage lubrication literature can be found in a recent textbook chapter (Ateshian and Mow, 2005) as well as other review articles (Katta et al., 2008; Sah, 2009; Unsworth, 1991; Wright and Dowson, 1976). The low friction and wear of articular layers has been attributed to mixed modes of lubrication which include fluid film lubrication by synovial fluid (Dowson et al., 1969; Macconaill, 1932), boundary lubrication by a variety of candidate molecules in synovial fluid and cartilage (Charnley, 1960; Hills, 1989; Jay et al., 2001; McCutchen, 1966; Radin et al., 1970; Schmidt et al., 2007; Swann and Radin, 1972; Walker et al., 1968), and lubrication by pressurization of the interstitial fluid of cartilage (Forster and Fisher, 1996; Krishnan et al., 2004b; Lewis and McCutchen, 1959; McCutchen, 1962).

The science of lubrication, or tribology, is rooted in mechanics and surface chemistry. Several of the modes of lubrication hypothesized to prevail in articular joints can be modeled mathematically and the predictions of these models may be compared to experiments in a process that can support or reject specific hypotheses. This paper reviews recent findings related to the role of interstitial fluid pressurization in cartilage lubrication, summarizing major new insights, gained from theoretical predictions and experimental validations, that support this mode of lubrication.

A standard mode of lubrication familiar to engineers is fluid film lubrication, where a lubricant forms a thin layer that separates the bearing surfaces (Hamrock, 1994). The fluid in this layer is pressurized and is able to support the load transmitted across the bearing surfaces, avoiding direct contact between them, thereby minimizing friction and wear. The pressurization of this fluid occurs either as a result of the relative velocity of the bearing surfaces (hydrodynamic and squeeze film lubrication) or as a result of pumping of the lubricant into the space between the surfaces (hydrostatic lubrication). The film thickness is typically on the order of a micron or less. For example, this mode of lubrication prevails in automotive applications, such as the bearings supporting the crankshaft of a piston engine, or at the interface between cam and follower.

Fluid film lubrication had long been considered a likely mode of lubrication for articular cartilage because the viscous synovial fluid found in diarthrodial joints appeared to be well suited as a fluid film lubricant (Dowson et al., 1969; Macconaill, 1932). In principle, the validity of this lubrication mechanism may be tested either directly, by measuring the presence and thickness of the lubricant film, or indirectly, by analyzing the frictional response over a range of load magnitudes, sliding velocities, and lubricant viscosities, and comparing the outcome to theoretical predictions. In the case of articular cartilage, it has not been possible to measure the film thickness directly, because standard methods employ highly polished transparent bearing surfaces, relying on Newton fringes to detect the distance between them; cartilage is too opaque and insufficiently smooth to allow this type of measurement.

Theoretical predictions have depended on the level of modeling detail ascribed to the cartilage and synovial fluid lubricant. A review of the related literature is beyond the scope of this article but may be found elsewhere (Ateshian and Mow, 2005). Briefly, it appears that there are no studies in the literature that demonstrate direct agreement between theoretical predictions from fluid film lubrication and experimental measurements of friction. On the contrary, a recent detailed study has shown that experimental cartilage friction measurements do not support this mode of lubrication, based on the concept of Stribeck curves which predict a specific relationship between the friction coefficient and the non-dimensional Hersey number over a range of lubrication regimes (Gleghorn and Bonassar, 2008). This recent finding complements some of the earlier arguments presented in the literature against this mode of lubrication (Charnley, 1960; McCutchen, 1962).

A likely explanation for this observation has been provided from theory, when accounting for the porous nature of articular cartilage. In a series of increasingly sophisticated theoretical analyses, Hlavacek has shown that a fluid film gets depleted within a fraction of a second when porous deformable bearing surfaces are brought into contact (Hlavacek, 1993a, Hlavacek, 1993b, Hlavacek, 1995, Hlavacek, 1999, Hlavacek, 2000, Hlavacek, 2001; Hlavacek and Novak, 1995), because the pressurized fluid can filtrate into the porous cartilage layers. Thus, unlike traditional fluid film lubrication between impermeable bearing surfaces, where the escape path for the pressurized fluid film depends on the characteristic dimension of the apparent contact area, lubrication between cartilage surfaces provides a very short escape path for the lubricant.

Starting in the late 1950s, McCutchen and co-workers proposed an explanation for the mechanism of lubrication in articular cartilage which is related to the concept of hydrostatic lubrication (Lewis and McCutchen, 1959; McCutchen, 1959, McCutchen, 1962, McCutchen, 1983). McCutchen demonstrated experimentally that the friction coefficient of cartilage against glass rises over time under a constant applied load (McCutchen, 1962); when the load is temporarily removed for 1 s, then reapplied, the friction coefficient does not return to its lowest initial value, dropping only slightly before rising again under the applied load. These observations guided him in the formulation of his proposed lubrication mechanism.

According to this mechanism, pressing two articular layers together pressurizes the cartilage pore (interstitial) fluid, and this pressurized fluid supports most of the applied load, leaving only a small fraction to be supported by the solid matrix. The implication of this load sharing mechanism is that frictional forces would be significant only over the portion of the load transferred across the solid matrices of the opposing articular layers; thus, as long as the interstitial fluid pressure remains elevated, supporting most of the load, the friction should remain low. As the fluid pressure subsides over time and load sharing shifts progressively more to the opposing solid matrices, the friction should rise accordingly, as indeed observed in his experiments. On this basis, this proposed mechanism was described as that of a self-pressurized hydrostatic bearing.

To further explain the low values of the friction coefficient observed upon initial load application, McCutchen proposed that the pressurized fluid in the cartilage pores flows out into the space between the contacting surfaces, forming “…a thick film of lubricant, where ‘weeping’ through the porous wall supplies enough liquid to maintain the film” (McCutchen, 1959).

This self-pressurized hydrostatic and weeping lubrication mechanism offered an attractive alternative to the classical modes of hydrodynamic or elastohydrodynamic lubrication because it proposed a straightforward explanation for the time-dependent rise of the cartilage friction coefficient observed in experiments. Furthermore, by showing that the friction coefficient of cartilage against glass did not return to its initial low value when cartilage was unloaded for 1 s, McCutchen discounted the mechanism of squeeze-film lubrication on the basis that unloading the cartilage and separating it temporarily from the opposing glass surface should have allowed sufficient time for a squeeze film to be replenished.

Nevertheless, his proposed mechanism generated controversy with proponents of fluid film lubrication, most notably the renowned tribologist Duncan Dowson and his co-workers (Dowson, 1973; Dowson et al., 1969; Walker et al., 1969), who argued that his hypothesized weeping mechanism violated the axiom of conservation of linear momentum. In fact several investigators proposed that, contrary to McCutchen's weeping hypothesis, the synovial fluid trapped between the cartilage surfaces would undergo ultrafiltration whereby its water solvent and small molecular weight solutes would flow into the porous cartilage, leaving behind a hyaluronic acid gel that might act as a boundary lubricant (Longfield et al., 1969; Maroudas, 1967; Walker et al., 1968, Walker et al., 1970). This alternative mechanism was called ‘boosted lubrication’ (Longfield et al., 1969; Walker et al., 1968).

When this controversy arose in the 1960s, theoretical and computational modeling tools were insufficiently developed to address the feasibility of weeping flow or boosted lubrication between two bearing surfaces, where at least one of the bearing surfaces is porous and deformable. As the application of porous media theories to articular cartilage became more widespread, and with the formulation of more elaborate frameworks for modeling cartilage and synovial fluid, theoretical and computational predictions have mostly supported the hypothesis that the fluid between the bearing surfaces will flow into the cartilage, particularly in the central region of the contact (Hlavacek, 1993b, Hlavacek, 1995, Hlavacek, 1999, Hlavacek, 2000; Hlavacek and Novak, 1995; Hou et al., 1989; Soltz et al., 2003), though one computational study has been supportive of the weeping mechanism (Macirowski et al., 1994).

However, these disparate hypotheses and predictions on the direction of fluid flow have somewhat obscured the other relevant aspect of McCutchen's proposed lubrication mechanism, namely the role of interstitial fluid load support in the lubrication of cartilage, and its regulation of the temporal response of the friction coefficient. Starting from the late 1970s, porous media models of cartilage were formulated which could be used to predict interstitial fluid pressurization from theory. These models were significantly refined over the following decades, and starting in the 1990s, experimental measurements of interstitial fluid pressure were shown to agree with these theoretical frameworks. Investigators focused again on the potential tribological role of this interstitial fluid load support, irrespective of the direction of fluid flow at the articular surface, armed with these validated theoretical and experimental tools. Prior to reviewing the salient findings on this topic, we start by summarizing the cartilage structure and composition, and salient aspects of cartilage mechanics.

Section snippets

Cartilage structure and composition

Articular cartilage is a soft connective tissue consisting primarily of water (68–85% by weight), a fibrillar matrix of type II collagen (10–20%), large aggregating proteoglycans (aggrecans, 5–10%), and chondrocytes (Mow and Ratcliffe, 1997). The articular layer exhibits compositional heterogeneity from the surface to the subchondral bone; it is typically divided into three regions commonly called the superficial, middle and deep zones (SZ, MZ and DZ, respectively) (Maroudas, 1979; Mow and

Cartilage mechanics

Based on experimental studies of articular cartilage mechanics, it is well recognized that this tissue exhibits a range of complex characteristics and behaviors. Cartilage exhibits flow-dependent viscoelasticity, which represents the energy dissipation mechanism resulting from the frictional interactions between the interstitial fluid and the solid matrix (Mow et al., 1980; Zarek and Edward, 1963). It exhibits flow-independent viscoelasticity, which represents energy dissipation mechanisms

Theoretical predictions

In addition to the Donnan osmotic pressure arising from physicochemical effects, the interstitial fluid of cartilage will pressurize as a result of mechanical loading of the tissue. Even in the absence of direct experimental evidence, this pressurization was hypothesized to occur because of the hydrated nature of the tissue and the ability of its interstitial fluid to flow through the pores (McCutchen, 1962; Zarek and Edward, 1963). The ability to predict the pressurization and flow of this

Temporal variation in the friction coefficient

McCutchen's early study (McCutchen, 1962) provided direct evidence of the temporal increase of the friction coefficient under constant loading. More extensive experimental results were subsequently reported in a doctoral dissertation by Malcom (1976), who measured the frictional response of cartilage against cartilage, using bovine shoulder joints. Malcolm investigated a variety of testing conditions, including variations in the magnitude and temporal profile of the applied load, the sliding

Facilitating the investigation of boundary lubrication

Understanding the role of interstitial fluid pressurization on the frictional response of articular cartilage considerably facilitates the investigation of boundary lubrication mechanisms imparted by molecular constituents of synovial fluid (Hills, 1989; Jay, 1992; Schmidt et al., 2007; Swann et al., 1984) and the superficial zone of articular cartilage (Basalo et al., 2007, Basalo et al., 2006; Flannery et al., 1999; Jay et al., 2001; Krishnan et al., 2004a). Indeed, to ascertain the role of

Conclusion

For many decades the literature on cartilage biotribology was unable to conclusively identify the modes of lubrication prevailing in articular cartilage. For some investigators, the attractiveness of fluid-film lubrication was difficult to overcome, particularly in light of the fact that alternative theories such as weeping, boosted and boundary lubrication, did not appear to provide stronger experimental support. However, with advances in theoretical modeling of the porous-permeable nature of

Conflict of interest statement

The author does not have any financial conflicts of interest with regard to this review article and the materials contained herein.

Acknowledgments

The author's studies related to cartilage mechanics and lubrication were supported by the National Institute of Arthritis, Musculoskeletal and Skin Diseases of the US National Institutes of Health (AR43628, AR46532). The author would like to acknowledge the contributions to these studies of former and current students, Dr. Huiqun (Laura) Wang, Dr. Michael A. Soltz, Dr. Ramaswamy Krishnan, Dr. Monika Kopacz, Dr. Seonghun Park, Dr. Ines M. Basalo, Dr. Nadeen O. Chahine, Mr. Michael Carter, Mr.

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