Elsevier

Clinical Biomechanics

Volume 79, October 2020, 104880
Clinical Biomechanics

Review
The tribology of cartilage: Mechanisms, experimental techniques, and relevance to translational tissue engineering

https://doi.org/10.1016/j.clinbiomech.2019.10.016Get rights and content

Highlights

  • Loss of lubrication may harm morphology, biochemical, and mechanical properties of cartilage.

  • Regulatory guidelines should include standardized tribology testing of neocartilage implants.

  • Native tissue controls in tribology studies would better show translatability of neocartilages.

  • Comprehension of synovial joints neccesitates an increase in tribological characterization.

  • A standardized tribology testing assay would facilitate interlaboratory comparisons.

Abstract

Diarthrodial joints, found at the ends of long bones, function to dissipate load and allow for effortless articulation. Essential to these functions are cartilages, soft hydrated tissues such as hyaline articular cartilage and the knee meniscus, as well as lubricating synovial fluid. Maintaining adequate lubrication protects cartilages from wear, but a decrease in this function leads to tissue degeneration and pathologies such as osteoarthritis. To study cartilage physiology, articular cartilage researchers have employed tribology, the study of lubrication and wear between two opposing surfaces, to characterize both native and engineered tissues. The biochemical components of synovial fluid allow it to function as an effective lubricant that exhibits shear-thinning behavior. Although tribological properties are recognized to be essential to native tissue function and a critical characteristic for translational tissue engineering, tribology is vastly understudied when compared to other mechanical properties such as compressive moduli. Further, tribometer configurations and testing modalities vary greatly across laboratories. This review aims to define commonly examined tribological characteristics and discuss the structure-function relationships of biochemical constituents known to contribute to tribological properties in native tissue, address the variations in experimental set-ups by suggesting a move toward standard testing practices, and describe how tissue-engineered cartilages may be augmented to improve their tribological properties.

Introduction

Diarthrodial joints, such as the knee, contain hyaline articular cartilage, fibrocartilage, and intra-articular space filled with synovial fluid. Hyaline articular cartilage is a highly hydrated, anisotropic tissue composed primarily of collagen II, proteoglycans, and chondrocytes that covers the ends of long bones and acts as a load-bearing, lubricated surface during joint articulation (Athanasiou et al., 2017). Fibrocartilage structures, such as the meniscus in the knee, confine motion, dissipate loads, and contribute to essentially frictionless articulation of diarthrodial joints as well. Synovial fluid is confined to the joint space by the articular capsule and contains macromolecular components, such as superficial zone protein (SZP) and hyaluronan, which are essential to joint lubrication (Jay and Waller, 2014; Noyori et al., 1998). This review will focus on the articular surfaces of hyaline articular cartilage and the knee meniscus, as well as synovial fluid, since they are the components responsible for maintaining low-friction motion and lubrication, or tribological functions, in diarthrodial joints.

Tribology is the study of the interactions between two surfaces moving relative to one another. While it traditionally refers to the study of non-biological materials, tribological principles have been extended to understand the loading environment of diarthrodial joints. The quantitative properties when studying the tribology of diarthrodial joints are surface roughness, Ra, and coefficient of friction, μ. This review will utilize both of these properties for evaluation of tribological properties of the native and engineered tissues described in subsequent sections. A crucial characteristic of native hyaline articular cartilage is its ability to exhibit minimal friction at joint-gliding speeds between 0 and 0.03 m/s when subjected to loads that are five times bodyweight (Bergmann et al., 1993; Morrell et al., 2005). The replication of tribological properties is crucial to the translation of tissue-engineered articular cartilages, yet they remain under-characterized in tissue-engineered constructs. For instance, a PubMed search for “articular cartilage lubrication” yielded 422 results, but a search for “articular cartilage mechanical properties” produced 1789 references. Building on some of the tissue-engineering strategies described in this review to improve the tribological properties of engineered constructs could decrease this discrepancy.

It is predicted that by the year 2050 osteoarthritis, an articular cartilage degeneration disease, will affect at least 130 million people world-wide (Maiese, 2016). Articular cartilage degeneration causes pain and inflammation of the joint, loss in mechanical function, as well as loss in tribological function. As health care technologies expand and life expectancy in the United States consequently increases, incidences of articular cartilage degeneration will also increase, necessitating viable treatment options such as implantable tissue-engineered articular cartilage constructs with adequate mechanical and tribological properties.

In this review, the components, such as SZP and hyaluronan, and mechanisms, such as shear-thinning of synovial fluid, known to contribute to the tribological properties of articular cartilages will be described. The pathologies that compromise articular cartilage tribological function will also be discussed. Specifically, this review will delve into how surface roughness, coefficient of friction, and lubrication regimes affect and are affected by the state of biochemical components known to regulate tribological function. Tribological properties will be compared quantitatively by looking at the spread of the coefficient of friction obtained across laboratories using a variety of tribometer modalities. Although there is a consensus toward testing articular cartilages under boundary lubrication regimes, variations exist from laboratory to laboratory in terms of tribometer configurations, testing substrates, and lubricants. A recommendation will be made toward reconciling and standardizing tribological measurements for articular cartilages. Therapeutic targeting of tribological properties will be presented and discussed, including the current state of recapitulating tribological properties in tissue-engineered articular cartilages for translation. Finally, the areas of articular cartilage tribology that remain understudied will be presented.

Section snippets

Commonly examined tribological characteristics in cartilage

The two quantitative tribological characteristics measured in both native and engineered articular cartilage are surface roughness and coefficient of friction. In this section, surface roughness and coefficient of friction are defined, and the values of native articular cartilage are presented. Finally, the coefficient of friction and surface roughness of synthetic materials are juxtaposed to native cartilage tribological properties for added context and perspective.

Tribological structure-function relationships in diarthrodial joints

In this section, the cartilage components that are essential for tribological function are identified. The capacity of lubricin and hyaluronan to modify the tribological characteristics of a diarthrodial joint is described. The importance of the interaction between lubricin and hyaluronan in the synovial fluid is also described and further discussed in the context of different lubrication modes. Lubrication modes, including boundary, mixed, elastohydrodynamic, and hydrodynamic, are defined, and

Methods for quantifying tribological properties

In this section, methods for quantifying tribological properties are listed and discussed. The most commonly used tribometer configurations, pin-on-disc, pin-on-plate, and rolling-ball-on-disc, for articular cartilage are described and compared. The use of atomic force microscopy to quantify surface roughness is also included. Because different testing configurations can lead to disparities in coefficient of friction and surface roughness values, suggestions for standardized practices are also

Toward engineering native tribological properties

Because adequate lubrication is vital for diarthrodial joint health and function, various strategies to engineer biomimetic tribological properties for both native tissue and engineered constructs have been explored. Approaches include the development of biolubricants to alter both fluid-film and boundary lubrication, low-friction scaffolds, as well as bioactive factors and mechanical stimulation regimens that promote endogenous lubrication mechanisms.

Perspectives

When articular cartilages are described, load-bearing capacity and nearly frictionless surfaces are presented as key characteristics. However, in many studies of tissue-engineered cartilages, mechanical properties are investigated while tribological properties are rarely explored. To augment the translatability of tissue-engineered cartilages, both mechanical and tribological functions should be considered as release criteria for cartilage implants. Because the FDA has guidelines for mechanical

Author contributions

Jarrett M. Link*: Conceptualization, Visualization, Writing – Original draft preparation, Writing – Reviewing and editing. Evelia Y. Salinas*: Conceptualization, Visualization, Writing – Original draft preparation, Writing – Reviewing and editing. Jerry C. Hu: Conceptualization, Writing – Reviewing and editing, Supervision. Kyriacos A. Athanasiou: Conceptualization, Writing – Reviewing and editing, Supervision. (*These authors contributed equally to this work).

Funding

This work was funded by NIH Grant No. 5R01AR067821-05 and NIH Grant No. 5R01AR071457-03. Jarrett M. Link was also in part funded by a National Science Foundation Graduate Research Fellowship (Grant No. DGE-1321846). Evelia Y. Salinas was also in part funded by the NIH Diversity Fellowship (Grant No. 3R01AR067821).

Declaration of competing interest

None.

References (79)

  • S. Grad et al.

    Sliding motion modulates stiffness and friction coefficient at the surface of tissue engineered cartilage

    Osteoarthr. Cartil.

    (2012)
  • S. Grenier et al.

    An in vitro model for the pathological degradation of articular cartilage in osteoarthritis

    J. Biomech.

    (2014)
  • K. Hyun et al.

    Large amplitude oscillatory shear as a way to classify the complex fluids

    J. Non-Newtonian Fluid Mech.

    (2002)
  • G.D. Jay et al.

    The biology of lubricin: near frictionless joint motion

    Matrix Biol.

    (2014)
  • Y. Kanca et al.

    Tribological evaluation of biomedical polycarbonate urethanes against articular cartilage

    J. Mech. Behav. Biomed. Mater.

    (2018)
  • Y. Kanca et al.

    Tribological properties of PVA/PVP blend hydrogels against articular cartilage

    J. Mech. Behav. Biomed. Mater.

    (2018)
  • C.W. McCutchen

    The frictional properties of animal joints

    Wear

    (1962)
  • A.C. Moore et al.

    Tribological and material properties for cartilage of and throughout the bovine stifle: support for the altered joint kinematics hypothesis of osteoarthritis

    Osteoarthr. Cartil.

    (2015)
  • S.R. Oungoulian et al.

    Wear and damage of articular cartilage with friction against orthopaedic implant materials

    J. Biomech.

    (2015)
  • S. Park et al.

    Microscale frictional response of bovine articular cartilage from atomic force microscopy

    J. Biomech.

    (2004)
  • G. Peng et al.

    The distribution of superficial zone protein (SZP)/lubricin/PRG4 and boundary mode frictional properties of the bovine diarthrodial joint

    J. Biomech.

    (2015)
  • J.J. Rongen et al.

    Biomaterials in search of a meniscus substitute

    Biomaterials

    (2014)
  • D.L. Sedin et al.

    Influence of tip size on AFM roughness measurements

    Appl. Surf. Sci.

    (2001)
  • I. Šimkovic et al.

    Preparation of water-soluble/insoluble derivatives of hyaluronic acid by cross-linking with epichlorohydrin in aqueous NaOH/NH4OH solution

    Carbohydr. Polym.

    (2000)
  • D. Warnecke et al.

    Friction properties of a new silk fibroin scaffold for meniscal replacement

    Tribol. Int.

    (2017)
  • M. Woydt et al.

    The history of the Stribeck curve and ball bearing steels: the role of Adolf Martens

    Wear

    (2010)
  • L. Ambrosio et al.

    Rheological study on hyaluronic acid and its derivative solutions

    J. Macromol. Sci. A

    (1999)
  • J.M. Antonacci et al.

    Effects of equine joint injury on boundary lubrication of articular cartilage by synovial fluid: role of hyaluronan

    Arthritis Rheum.

    (2012)
  • K.A. Athanasiou et al.

    Articular Cartilage

    (2017)
  • C.J. Bell et al.

    Influence of hyaluronic acid on the time-dependent friction response of articular cartilage under different conditions

    Proc. Inst. Mech. Eng. H J. Eng. Med.

    (2006)
  • J.M. Coles et al.

    Loss of cartilage structure, stiffness, and frictional properties in mice lacking PRG4

    Arthritis Rheum.

    (2010)
  • W.D. Comper et al.

    Physiological function of connective tissue polysaccharides

    Physiol. Rev.

    (1978)
  • M.K. Cowman et al.

    The content and size of hyaluronan in biological fluids and tissues

    Front. Immunol.

    (2015)
  • C.R. Flannery et al.

    Prevention of cartilage degeneration in a rat model of osteoarthritis by intraarticular treatment with recombinant lubricin

    Arthritis Rheum.

    (2009)
  • S.A. Flowers et al.

    Lubricin binds cartilage proteins, cartilage oligomeric matrix protein, fibronectin and collagen II at the cartilage surface

    Sci. Rep.

    (2017)
  • N.K. Galley et al.

    Frictional properties of the meniscus improve after scaffold-augmented repair of partial meniscectomy: a pilot study

    Clin. Orthop. Relat. Res.

    (2011)
  • S. Ghosh et al.

    Status of surface modification techniques for artificial hip implants

    Sci. Technol. Adv. Mater.

    (2016)
  • J.P. Gleghorn et al.

    Alteration of articular cartilage frictional properties by transforming growth factor β, interleukin-1β, and oncostatin M

    Arthritis Rheum.

    (2009)
  • G.W. Greene et al.

    Adaptive mechanically controlled lubrication mechanism found in articular joints

    Proc. Natl. Acad. Sci.

    (2011)
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