boundary cartilage lubrication: review of current concepts; grenzflächenknorpelschmierung – eine...

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88 1 3Boundary cartilage lubrication: review of current concepts

Received: 6 March 2013 / Accepted: 21 August 2013 / Published online: 1 October 2013© Springer-Verlag Wien 2013

Boundary cartilage lubrication: review of current concepts

Matej Daniel

Wien Med Wochenschr (2014) 164:88–94DOI 10.1007/s10354-013-0240-2

M. Daniel ()Division of biomechanics, Department of mechanics, biomechanics and mechatronics, Faculty of Mechanical Engineering,Czech Technical University in Prague, Technicka 4,16607 Prague 6, Czech Republice-mail: [email protected]

Summary Effective lubrication of synovial joints is important to prevent cartilage degeneration and to keep the joints healthy. This paper sets out the basics of engi-neering lubrication with respect to the composition and properties of synovial fluid constituents. Two basic types of boundary lubrication are discussed: the presence of highly hydrophilic proteoglycans that provide a water liq-uid film, and the existence of multilamellar phospholipids lubricating layers at the surface ofarticular cartilage. Based on current knowledge, we may conclude that no single mechanism of boundary lubrication exists, and that effec-tive boundary lubrication of synovial joints is maintained by the synergic effect of all synovial fluid constituents.

Keywords Hyaluronic acid · Lubricin · Phospholipids · Oligolamellar

Grenzflächenknorpelschmierung – Eine Übersicht der bestehenden Konzepte

Zusammenfassung Die effektive Schmierung der syn-ovialen Gelenke ist wichtig, um der Degeneration des Knorpelgewebes vorzubeugen und die Gelenke gesund zu erhalten. Die vorliegende Arbeit beschreibt die Grund-lagen des Schmierungsaufbaus, was die Zusammenset-zung und Eigenschaften der Synoviabestandteile betrifft. Zwei grundlegende Arten der Grenzflächenschmierung werden besprochen: das Vorkommen stark hydrophiler Proteoglykane, die einen wasserflüssigen Film bilden,

und die Existenz multilamellarer Phospholipide, die auf der Oberfläche des artikulären Knorpels als Schmier-schichten dienen. Nach heutigem Wissensstand dürfen wir schließen, dass es sich bei der Grenzflächenschmie-rung nicht um einen isolierten Mechanismus handelt. Vielmehr wird die effektive Grenzflächenschmierung der synovialen Gelenke durch den synergischen Effekt aller Bestandteile der Synovialflüssigkeit aufrechterhalten.

Schlüsselwörter Hyaluronsäure · Lubricin · Phospholi-pide · Oligolamellar

Introduction

The most frequent disease of synovial joints is osteoarth-ritis. Osteoarthritis is a multifactorial disorder of synovial joints, which is characterized by escalated degeneration and loss of articular cartilage [1]. Treatment of osteoarth-ritis is a critical unmet need in medicine for regeneration of damaged articular cartilage in elderly [2, 3].

Articulating ends of diarthroidal joints are covered by hyaline cartilage serving as a low friction, wear resis-tant surface for load support, load transfer and motion between the bones of diarthroidal joint. Under normal circumstances, the tissue bathed in synovial fluid (SF) is able to withstand millions of cycles of loading [4] each year after at stresses that may reach 18 MPa [5, 6].

It is believed that excessive friction accelerates carti-lage wear after failure of cartilage lubrication. Damage of cartilage is a key factor in the onset of osteoarthrosis. Experimental results show that removal of the cartilage surface layer in intact sheep joint greatly accelerated osteoarthritic damage to the articular cartilage [7]. Main-taining low friction coefficient includes maintaining effi-cient lubrication. The principles of cartilage lubrication have been studied for many decades, but the exact lubri-cation mechanism remains unclear.

891 3 Boundary cartilage lubrication: review of current concepts

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The aim of this paper is to explain basic mechanisms of cartilage lubrication mediated by SF components.

Engineering view on articular cartilage lubrication

The coefficient of friction (ratio of frictional force to com-pressive force) of cartilage gliding on cartilage has been reported as low as 0.002 [8]. The mechanisms through which the synovial joint achieves these properties involve combination of biomechanical and biomolecular factors. For example, joint congruity and cartilage deformation serve to distribute loads over a large contact area, thereby minimizing contact stresses [9]. The high water content and low hydraulic permeability of the cartilage extracel-lular matrix provide a unique mechanism of supporting loads whereby fluid pressurization within the tissue can bear nearly 90 % of the load and thus minimize stresses on the solid extracellular matrix [10].

A classical paper of Wright and Downson [11], descri-bes two basic types of lubrication: that in which articu-lating surfaces are separated by a fluid film, and that in which the load is supported by surface-to-surface contact. The former is denoted as the fluid film lubrication while the latter is being denoted as the boundary lubrication.

Fluid film lubrication might be related to joint motion which draws in film of fluid between the opposing carti-lage surfaces. This type of lubrication is well described in engineering practice as hydrodynamic lubrication [12]. As contact surfaces of cartilage are not rigid, deforma-tion of cartilage enhances the fluid film formation during motion, the process being described as elastohydrody-namic lubrication [13]. Another type of fluid film lubri-cation may occur when cartilage surfaces are pressed

to each other in normal direction giving rise to squeeze film lubrication [14]. In recent years, the mechanism of articular cartilage lubrication has been shown to depend significantly on the pressurization of cartilage intersti-tial water, which supports most of the joint contact load and helps to shift it away from the collagen-proteoglycan matrix, thereby producing a low friction coefficient. This mechanism is denoted as biphasic lubrication [15] or weeping lubrication if the interstitial fluid is exuded to the surface. As the articular cartilage is porous, the high pressure in the SF also causes the SF to flow into the tis-sue, leaving a concentrated gel of macromolecules on the cartilage surface, so-called boosted lubrication [16].

The fluid film lubrication is active provided opposing surfaces of articular cartilage slide with respect to each other. In long-term static loading position, all fluid for-ming the film flow out from between the load-bearing articular surfaces [17]. This suggests that boundary lubri-cation, where the articular surfaces come into direct con-tact, occurs as well.

Difference between the modes of lubrication can be observed in Stribeck curve used in mechanical engi-neering. In the classic Stribeck curve, the measured friction coefficient μ is a function of the Hersey number,

/v Nη , where η is the dynamic viscosity of the lubricant solution, v the sliding velocity, and N is the normal load [18]. The classic Stribeck curve has two import-ant regimes: hydrodynamic lubrication at high speeds where the details of the boundary lubricant are not criti-cally important and boundary lubrication at low speed, which is very sensitive to the molecular properties of the lubricant [19] (Fig. 1). Stribeck curve obtained for cartilage friction coefficient experimentally is consis-tent with the classic Stribeck curve, except that even at

Fig. 1 Stribeck curve; a clas-sic Stribeck curve, b Stribeck curve for cartilage. (Adapted from Daniel [50])


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very low speeds and solution viscosity, i.e., at very low Hersey numbers, where the boundary lubrication is expected, the curve does not show a “boundary-mode region” in which friction coefficient is invariant as the Hersey number changes [20]. This observation shows an effective lubrication at low speed probably by existence of permanent fluid like film at the cartilage surface.

Boundary lubrication

The boundary lubrication is conditioned by the proper-ties of the cartilage uppermost layer. The surface layer of cartilage is usually referred as lamina splendens. Recent studies identified additional acellular and nonfibrous, i.e., amorphous surface layer over the lamina splendens [21] denoted as the surface amorphous layer (SAL). Ato-mic force microscopy and environmental scanning elec-tron microscopy showed a clear distinction between the amorphous layer and the collageneous bulk of the lamina splendens [22]. The thickness of gel-like SAL was estima-ted to be 20 ± 10 μm [22]. It is believed that low coeffi-cient of friction in the boundary lubrication of articular cartilage is conditioned by surface layer of specialized molecules in SF adhered to the cartilage surface like hya-luronic acid, lubricin, or surface-active phospholipids.

Hyaluronic acid

Earlier models considered hyaluronic acid as the pre-dominant boundary lubricant [14]. Hyaluronic acid is a polymer of disaccharides, themselves composed of D-glucuronic acid and D-N-acetylglucosamine (Fig. 2a). Concentration of hyaluronan in normal SF is around 3,000 μg/ml [23, 24]. The hyaluronic acid forms long chains that considerably influence the viscosity of SF. For example, 1 % solution of hyaluronic acid with molecular weight 3–4 × 106 g/mol has 500,000 times higher viscosity at low shear rate than water [24]. According to Stribeck curve (Fig. 1), high viscosity enhance hydrodynamic lubrication. However, the role of hyaluronic acid itself in cartilage boundary lubrication has been questioned as it possesses a negligible loadbearing capacity [25] and degradation of the viscous hyaluronic acid by the use of hyaluronidase does not have a detrimental effect on the lubricating ability of the SF [26].

Lubricin

Another component of SF considered as boundary lubri-cant is a glycoprotein fraction of SF named lubricin [27] also known as superficial zone protein (SZP) or PRG4. Lubri-cin concentration in the SF is 250 μg/ml and its molecular weight is 2.3–3 × 105 g/mol [28]. Lubricin appears like an elongated and flexible molecule. High molecular weight is attributed to heavy glycolisation of the central part of the molecule similar to mucins in structure. The dense glycoli-

sation of mucin region gives it considerable water-holding capacity with negative total charge. The end domains con-tain of lubiricin are globular with positive total charge and are similar to somatomedin-B and homeopexin known to be involved in cell contacts (Fig. 2b).

It was shown, that effective boundary lubrication can be achieved when brushes of charged polymers (poly-electrolytes) are attached to sliding surfaces [29]. These polymers are charged in water and are surrounded by a sheath of water molecules bound to the charged and polar groups. The structure of lubricin might be conside-red as biological polyelectrolyte that function as molecu-lar brushes [28]. The peripheral parts of the molecule are attached to the negatively charged cartilage matrix while the mucin region with water sheats is looped toward the surface (Fig. 3a). Highly hydrophilic mucin region at the cartilage surface contribute to water binding to the car-tilage surface thereby providing low friction liquid film.

Fig. 2 Constituents of synovial fluid; a hyaluronic acid, b lu-bricin, c surface-active phosholipid


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Surface-active phospholipids

According to the theory of molecular brushes, the surface of the cartilage should be hydrophilic. However, when a droplet of saline is placed on the fresh articular surface, it beads up, displaying a contact angle of 100° ± 5° [30]. It indicates highly hydrophobic surface comparable to Tef-lon (contact angle 108°) [21]. Rinsing the articular surface with a lipid solvent or incubation with a lipase renders the surface hydrophilic and increases the coefficient of friction [31].

Based on the fact that phospholipids have been iden-tified in appreciable quantities in SF and cartilage SAL, Hills [32] hypothesized that a lamellar phospholipid adsorbed to the articular surface contributes to joint lubrication. Phosphatidylcholines have a zwitterionic headgroup, as they have a negative charge on the phos-phate group and a positive charge on the amine (Fig. 2c). Mobile cations with positive charge, e.g., Ca2+, can inter-act with the negatively charged phosphate ions to render the molecules effectively cationic (Fig. 3). Like others cationic surfactants [33], they will then be strongly adsor-bed to a negatively charged matrix composed of hyalu-ronic acid and/or glycoproteins [34]. Interspersion of these mobile cations between phosphate groups will pull the adsorbed phosphatidylcholine molecules into a very cohesive plane. Strong adsorption and strong cohesion are the essential properties needed for a surfactant to pro-vide excellent boundary lubrication [21], while exposing the non-polar part outwards making the surface quite

hydrophobic as observed in experiments [30]. Hydro-phobic surfaces are very attractive for direct bonding by adsorption of another monolayer of surfactants. Based on these observations, Hills 1989, proposed a lamellar theory of lubrication described as “shearing between surface lamellae of phospholipid layers just as occurs in graphite when writing with a pencil” (Fig. 3) [35]. Experiments proved that the multilayered phospholipid surfaces result in a lower friction coefficient than single bilayer covered surfaces [36]. It is assumed that friction occurs in between the bilayers and this of lubrication is denoted as oligolamellar lubrication [37].

Discussion—identification of boundary lubricant

In general, two main theories describing surface lubri-cation have been proposed. The first theory assumes presence of highly hydrophilic proteoglycans or glyco-proteins that contribute to water binding to the cartilage surface thereby providing low friction liquid film [38]. The second theory postulates the existence of phospho-lipids lubricating layers on the surface of articular carti-lage [39].

Immunohistochemical methods [40], infrared spec-troscopy [41], and atomic force microscopy (AFM) [42] revealed that the surface layer of the cartilage consists of phosphatidylcholine colocalized with hyaluronic acid. SAL also contained protein and sulfated glycosaminog-lycan [41]. Crockett, 2009 [43] concluded that two dis-

Fig. 3 Theories of boundary lubrication. a lubricin-media-ted lubrication that contribu-tes to water binding to the cartilage surface [29], b oligolamellar phospholipids lubricating layer on the surfa-ce of articular cartilage [51]


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tinct layers in SAL observed in AFM and histochemical analysis are the layer of phospholipids and the layer of hyaluronate while the uppermost hydrophobic layer that forms on removal of the cartilage from SF was made up mostly of phospholipids [43].

Hill and Monds [44] studied the effect of destruction of particular SF component on the cartilage lubrication. Destroying hyaluronic acid with hyaluronidase, no sig-nificant change in frictional tests was found. Destroying surface-active phospholipids with phospholipase A2, there was a highly significant dose-dependent compro-mise of lubrication. Trypsin actually improved lubrica-tion of cartilage, surprisingly [44]. This result confirmed the hypothesis of surface-active phospholipids mediated boundary cartilage lubrication.

Contradictory results were obtained by Jay and Cha [45]. Lubrication properties were studied in in vitro sys-tem and bovine SF were tested in vitro in a bearing of latex oscillating against polished glass. Digestions of bovine SF by phospholipase C and A2 in the presence of protease inhibitors did not remove boundary lubricating ability compared to an undigested control. Digestion of bovine SF with trypsin removed all lubricating ability and raised friction [45].

Using a polystyrene spherical probe tip (r = 5 μm), Chan et al. [46] assessed microscale friction upon the removal of certain molecular components. Removal of hyaluronic acid or surface-active phospholipids resulted in no significant impact on coefficient of friction, sugge-sting that hyaluronic acid and phospholipids do not pro-vide boundary lubrication on the cartilage surface in the absence of other surface-interacting molecules. In con-trast, trypsin treatment to remove all proteoglycan consi-derably increased friction coefficient.

As proposed by Crockett et al. [41], the diverse results in the different studies are probably because of the unstable composition of articular cartilage after removal from the physiological environment and difference in extraction methods between the experiments. In some studies, the surface is collagenous, whereas, in others, a noncollagen amorphous layer has been defined as the surface [41].

Schmidt et al. [47] observed the effect of synergic activity of hyaluronic acid, lubricin, and phospholipids on friction decrease. The combination of all three SF constituents at physiologic concentrations achieves, but not fully, the boundary-lubricant ability of SF [47].

It was shown hyaluronan and phospholipids form together a gel-like substance [41]. Strong interactions between hyaluronan and phospholipids origins through hydrophobic interactions between the tails of the phos-pholipid and the hydrophobic faces of the sugar units in hyaluronan [48]. In addition, incubation of phospholi-pids with hyaluronan stabilizes phospholipid layer and increases the lamellar spacing of bilayers [37]. Hyaulu-ran might also protect surface-active phospholipids from digestion by phospholipase [49].

It was also suggested that the lubricin molecule might serve as water-soluble carrier for small surface-active phospholipids molecules that are otherwise very insolu-

ble in water [3]. Lubricin might also improve phospho-lipid anchoring to cartilage surface. Recent AFM and biotribological techniques suggest that SF is composed by a network of vesicles containing glycoproteic gel sepa-rated by lipid multilayers [36].

The characteristics of the articular surfaces, in addi-tion to those of the SF, must be taken into account to fully understand low boundary friction in human articular cartilage. It is probable, that low friction coefficient in boundary lubrication is caused not only by the presence of boundary lubricant molecules but also by the structure of underlying collagen fibers. Tangentially located colla-gen fibrils in the upper cartilage layer may redistribute loads evenly on the surface [52] and provide a framework for supramolecular boundary lubricants organization. The formation of boundary lubricant film also depend on the ability of SF to penetrate a superficial layer of carti-lage in boosted lubrication mode [53]. The whole compo-site structure of articular cartilage should be considered in long-term loading, where the intersticial fluid flow within the cartilage is considered.

Conclusions

Two basic types of cartilage boundary friction were postulated: lubricin molecular brushes retaining water at the surface and oligolamellar phospholipid lubrication. Based on the results of experimental measurements, we may hypothesize that no single boundary lubricant molecule exists and the effective boundary friction in cartilage is a combination of synergic action of all com-ponents of SF. To restore cartilage lubrication in diseased hip, it seems to be important to maintain equilibrium of all components of SF. Appropriate kinesiotherapy and nutrition has potential to bioregenerate the cartilage metabolism and improve the boundary lubrication.

Acknowledgments This study was supported by the Technology Agency of the Czech Republic, grant no. TA01010185.

Conflict of interestThe authors declare that there are no actual or potential conflicts of interest in relation to this article.

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