Skip to main content

Articular Cartilage Friction, Strain, and Viability Under Physiological to Pathological Benchtop Sliding Conditions

Abstract

In vivo, articular cartilage is exceptionally resistant to wear, damage, and dysfunction. However, replicating cartilage’s phenomenal in vivo tribomechanics (i.e., high fluid load support, low frictions and strains) and mechanobiology on the benchtop has been difficult, because classical testing approaches tend to minimize hydrodynamic contributors to tissue function. Our convergent stationary contact area (cSCA) configuration retains the ability for hydrodynamically-mediated processes to contribute to interstitial hydration recovery and tribomechanical function via ‘tribological rehydration’. Using the cSCA, we investigated how in situ chondrocyte survival is impacted by the presence of tribological rehydration during the reciprocal sliding of a glass counterface against a compressively loaded equine cSCA cartilage explant. When tribological rehydration was compromised during testing, by slow-speed sliding, ‘pathophysiological’ tribomechanical environments and high surface cell death were observed. When tribological rehydration was preserved, by high-speed sliding, ‘semi-physiological’ sliding environments and suppressed cell death were realized. Inclusion of synovial fluid during testing fostered ‘truly physiological’ sliding outcomes consistent with the in vivo environment but had limited influence on cell death compared to high-speed sliding in PBS. Subsequently, path analysis identified friction as a primary driver of cell death, with strain an indirect driver, supporting the contention that articulation mediated rehydration can benefit both the biomechanical properties and biological homeostasis of cartilage.

This is a preview of subscription content, access via your institution.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8

Abbreviations

FLS:

Fluid load support

ECM:

Extracellular matrix

MMP:

Matrix metalloproteinase

OA:

Osteoarthritis

SCA:

Stationary contact area

MCA:

Migrating contact area

cSCA:

Convergent stationary contact area

PBS:

Phosphate-buffered saline

CCM:

Chondrogenic culture media

SF:

Synovial fluid

:

Diameter

ε :

Strain

ε SoS :

Start-of-sliding strain

ε EoS :

End-of-sliding strain

ε Rec :

Recovered strain

ε TA :

Time-averaged strain

δ :

Compression (μm)

k δ,Stat :

Static compression rate (min−1)

k δ,Slid :

Sliding compression rate (min−1)

μ :

Friction coefficient

μ SoS :

Start-of-sliding friction coefficient

μ EoS :

End-of-sliding friction coefficient

μ TA :

Time-averaged friction coefficient

t Semi :

Time slid above semi-physiological friction threshold (min)

t Patho :

Time slid above pathophysiological friction threshold (min)

τ μ,Slid :

Characteristic friction recovery time constant (min)

r :

Pearson’s correlation coefficient

References

  1. Ateshian, G. A. The role of interstitial fluid pressurization in articular cartilage lubrication. J. Biomech. 42:1163–1176, 2009.

    Article  Google Scholar 

  2. Basalo, I. M., et al. Effects of enzymatic degradation on the frictional response of articular cartilage in stress relaxation. J. Biomech. 38:1343–1349, 2005.

    Article  Google Scholar 

  3. Baumgarten, M., R. D. Bloebaum, S. D. K. Ross, P. Campbell, and A. Sarmiento. Normal human synovial fluid: osmolality and exercise-induced changes. J. Bone Jt. Surg. Ser. A 67:1336–1339, 1985.

    Article  Google Scholar 

  4. Bonnevie, E. D., V. J. Baro, L. Wang, and D. L. Burris. In situ studies of cartilage microtribology: roles of speed and contact area. Tribol. Lett. 41:83–95, 2011.

    Article  Google Scholar 

  5. Bonnevie, E. D., D. Galesso, C. Secchieri, I. Cohen, and L. J. Bonassar. Elastoviscous transitions of articular cartilage reveal a mechanism of synergy between lubricin and hyaluronic acid. PLoS ONE 10:1–15, 2015.

    Article  Google Scholar 

  6. Bonnevie, E. D., et al. Microscale frictional strains determine chondrocyte fate in loaded cartilage. J. Biomech. 74:72–78, 2018.

    Article  Google Scholar 

  7. Brand, R. A. Joint contact stress: a reasonable surrogate for biological processes? Iowa Orthop. J. 25:82–94, 2005.

    Google Scholar 

  8. Buckwalter, J. A., D. D. Anderson, T. D. Brown, Y. Tochigi, and J. A. Martin. The roles of mechanical stresses in the pathogenesis of osteoarthritis. Cartilage 4:286–294, 2013.

    Article  Google Scholar 

  9. Burris, D. L., L. Ramsey, B. T. Graham, C. Price, and A. C. Moore. How sliding and hydrodynamics contribute to articular cartilage fluid and lubrication recovery. Tribol. Lett. 67:1–10, 2019.

    Article  Google Scholar 

  10. Bush, P. G., and A. C. Hall. The osmotic sensitivity of isolated and in situ bovine articular chondrocytes. J. Orthop. Res. 19:768–778, 2001.

    Article  Google Scholar 

  11. Caligaris, M., and G. A. Ateshian. Effects of sustained interstitial fluid pressurization under migrating contact area, and boundary lubrication by synovial fluid, on cartilage friction. Osteoarthr. Cartil. 16:1220–1227, 2008.

    Article  Google Scholar 

  12. Cameron, M. L., F. H. Fu, H. H. Paessler, M. Schneider, and C. H. Evans. Synovial fluid cytokine concentrations as possible prognostic indicators in the ACL-deficient knee. Knee Surg. Sport Traumatol. Arthrosc. 2:38–44, 1994.

    Article  Google Scholar 

  13. Chan, D. D., et al. In vivo articular cartilage deformation: noninvasive quantification of intratissue strain during joint contact in the human knee. Sci. Rep. 6:19220, 2016.

    Article  Google Scholar 

  14. Clarke, I. C., R. Contini, and R. M. Kenedi. Friction and wear studies of articular cartilage: a scanning electron microscopic study. Am. Soc. Mech. Eng. 97:358–366, 1975.

    Google Scholar 

  15. Durney, K. M., et al. Physiologic medium maintains the homeostasis of immature bovine articular cartilage explants in long-term culture. J. Biomed. Eng. 141:021004, 2019.

    Google Scholar 

  16. Durney, K. M., et al. Immature bovine cartilage wear by fatigue failure and delamination. J. Biomech. 107:109852, 2020.

    Article  Google Scholar 

  17. Eckstein, F., M. Tieschky, S. Faber, K. H. Englmeier, and M. Reiser. Functional analysis of articular cartilage deformation, recovery, and fluid flow following dynamic exercise in vivo. Anat. Embryol. 200:419–424, 1999.

    Article  Google Scholar 

  18. Ewers, B. J., D. Dvoracek-Driksna, M. W. Orth, and R. C. Haut. The extent of matrix damage and chondrocyte death in mechanically traumatized articular cartilage explants depends on rate of loading. J. Orthop. Res. 19:779–784, 2001.

    Article  Google Scholar 

  19. Farnham, M. S., R. E. Larson, D. L. Burris, and C. Price. Effects of mechanical injury on the tribological rehydration and lubrication of articular cartilage. J. Mech. Behav. Biomed. Mater. 101:551–556, 2020.

    Article  Google Scholar 

  20. Farnham, M. S., et al. Lubricant effects on articular cartilage sliding biomechanics under physiological fluid load support. Tribol. Lett. 69:56, 2021.

    Article  Google Scholar 

  21. Feeney, E., et al. Temporal changes in synovial fluid composition and elastoviscous lubrication in the equine carpal fracture model. J. Orthop. Res. 37:1071–1079, 2019.

    Article  Google Scholar 

  22. Forster, H., and J. Fisher. The influence of loading time and lubricant on the friction of articular cartilage. Proc. Inst. Mech. Eng. Part H J. Eng. Med. 210:109–118, 1996.

    Article  Google Scholar 

  23. Forster, H., and J. Fisher. The influence of continuous sliding and subsequent surface wear on the friction of articular cartilage. Proc. Inst. Mech. Eng. Part H J. Eng. Med. 213:329–345, 1999.

    Article  Google Scholar 

  24. Furmann, D., et al. The effect of synovial fluid composition, speed and load on frictional behaviour of articular cartilage. Materials 13:1334, 2020.

    Article  Google Scholar 

  25. Graham, B. T., A. C. Moore, D. L. Burris, and C. Price. Mapping the spatiotemporal evolution of solute transport in articular cartilage explants reveals how cartilage recovers fluid within the contact area during sliding. J. Biomech. 71:271–276, 2018.

    Article  Google Scholar 

  26. Graham, B. T., A. C. Moore, D. L. Burris, and C. Price. Detrimental effects of long sedentary bouts on the biomechanical response of cartilage to sliding. Connect. Tissue Res. 61:375–388, 2020.

    Article  Google Scholar 

  27. Henao-Murillo, L., K. Ito, and C. C. van Donkelaar. Collagen damage location in articular cartilage differs if damage is caused by excessive loading magnitude or rate. Ann. Biomed. Eng. 46:605–615, 2018.

    Article  Google Scholar 

  28. Hlaváček, M. A note on an asymptotic solution for the contact of two biphasic cartilage layers in a loaded synovial joint at rest. J. Biomech. 32:987–991, 1999.

    Article  Google Scholar 

  29. Horibata, S., S. Yarimitsu, and H. Fujie. Effect of synovial fluid pressurization on the biphasic lubrication property of articular cartilage. Biotribology 19:100098, 2019.

    Article  Google Scholar 

  30. Hwang, H. S., and H. A. Kim. Chondrocyte apoptosis in the pathogenesis of osteoarthritis. Int. J. Mol. Sci. 16:26035–26054, 2015.

    Article  Google Scholar 

  31. Ingelmark, B. E., and R. Ekholm. A study on variations in the thickness of articular cartialge in association with rest and periodical load; an experimental investigation on rabbits. Upsala Lakareforen. Forh. 53:61, 1948.

    Google Scholar 

  32. Jepsen, K. J., et al. Phenotypic integration of skeletal traits during growth buffers genetic variants affecting the slenderness of femora in inbred mouse strains. Mamm. Genome 20:21–33, 2009.

    Article  Google Scholar 

  33. Kaplan, J. T., C. P. Neu, H. Drissi, N. C. Emery, and D. M. Pierce. Cyclic loading of human articular cartilage: the transition from compaction to fatigue. J. Mech. Behav. Biomed. Mater. 65:734–742, 2017.

    Article  Google Scholar 

  34. Klein, J. Hydration lubrication. Friction 1:1–23, 2013.

    Article  Google Scholar 

  35. Krishnan, R., M. Kopacz, and G. A. Ateshian. Experimental verification of the role of interstitial fluid pressurization in cartilage lubrication. J. Orthop. Res. 22:565–570, 2004.

    Article  Google Scholar 

  36. Lad, N. K., et al. Effect of normal gait on in vivo tibiofemoral cartilage strains. J. Biomech. 49:2870–2876, 2017.

    Article  Google Scholar 

  37. Linn, F. C. Lubrication of animal joints. J. Bone Jt. Surg. 49:1079–1098, 1967.

    Article  Google Scholar 

  38. Mabuchi, K., Y. Tsukamoto, T. Obara, and T. Yamaguchi. The effect of additive hyaluronic acid on animal joints with experimentally reduced lubricating ability. J. Biomed. Mater. Res. 28:865–870, 1994.

    Article  Google Scholar 

  39. Mansour, J. M. Biomechanics of Cartilage. In: Kinesiology: The Mechanics and Pathomechanics of Human Movement, Third Edition. Philadelphia, PA: Lippincott Williams and Wilkins, 2017, pp. 77–92.

  40. Moore, A. C., and D. L. Burris. Tribological rehydration of cartilage and its potential role in preserving joint health. Osteoarthr. Cartil. 25:99–107, 2017.

    Article  Google Scholar 

  41. Moore, A. C., J. L. Schrader, J. J. Ulvila, and D. L. Burris. A review of methods to study hydration effects on cartilage friction. Tribol. Mater. Surf. Interfaces 11:202–214, 2017.

    Article  Google Scholar 

  42. Neu, C. P., A. H. Reddi, K. Komvopoulos, T. M. Schmid, and P. E. Di Cesare. Increased friction coefficient and superficial zone protein expression in patients with advanced osteoarthritis. Arthr. Rheum. 62:2680–2687, 2010.

    Article  Google Scholar 

  43. Prince, D. E., and J. K. Greisberg. Nitric oxide-associated chondrocyte apoptosis in trauma patients after high-energy lower extremity intra-articular fractures. J. Orthop. Traumatol. 16:335–341, 2015.

    Article  Google Scholar 

  44. Robinson, D. L., et al. Mechanical properties of normal and osteoarthritic human articular cartilage. J. Mech. Behav. Biomed. Mater. 61:96–109, 2016.

    Article  Google Scholar 

  45. Rosseel, Y. L. An R Package for Structural Equation Modeling. J. Stat. Softw. 48, 2012.

  46. Sanchez-Adams, J., H. A. Leddy, A. L. McNulty, C. J. O’Conor, and F. Guilak. The mechanobiology of articular cartilage: bearing the burden of osteoarthritis. Curr. Rheumatol. Rep. 16:451, 2014.

    Article  Google Scholar 

  47. Schneider, C. A., W. S. Rasband, and K. W. Eliceiri. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9:671–675, 2012.

    Article  Google Scholar 

  48. Simič, R., M. Yetkin, K. Zhang, and N. D. Spencer. Importance of hydration and surface structure for friction of acrylamide hydrogels. Tribol. Lett. 68:1–12, 2020.

    Article  Google Scholar 

  49. Streiner, D. L. Finding our way: an introduction to path analysis. Can. J. Psychiatry 50:115–122, 2005.

    Article  Google Scholar 

  50. Takahashi, K. Z., T. M. Kepple, and S. J. Stanhope. A unified deformable (UD) segment model for quantifying total power of anatomical and prosthetic below-knee structures during stance in gait. J. Biomech. 45:2662–2667, 2012.

    Article  Google Scholar 

  51. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Au, 2013. http://www.R-project.org/.

  52. Trevino, R. L., C. A. Pacione, A. M. Malfait, S. Chubinskaya, and M. A. Wimmer. Development of a cartilage shear-damage model to investigate the impact of surface injury on chondrocytes and extracellular matrix wear. Cartilage 8:444–455, 2017.

    Article  Google Scholar 

  53. Vazquez, K. J., J. T. Andreae, and C. R. Henak. Cartilage-on-cartilage cyclic loading induces mechanical and structural damage. J. Mech. Behav. Biomed. Mater. 98:262–267, 2019.

    Article  Google Scholar 

  54. Waller, K. A., et al. Role of lubricin and boundary lubrication in the prevention of chondrocyte apoptosis. Proc. Natl. Acad. Sci. USA 110:5852–5857, 2013.

    Article  Google Scholar 

  55. Warnecke, D., et al. Articular cartilage and meniscus reveal higher friction in swing phase than in stance phase under dynamic gait conditions. Sci. Rep. 9:5785, 2019.

    Article  Google Scholar 

Download references

Acknowledgments

This material was supported by the National Science Foundation (NSF) Biomaterials and Mechanobiology program [1635536] and the NSF Graduate Research Fellowship Program [1247394]. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the NSF.

Conflict of interest

The authors declare no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christopher Price.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Associate Editor James L. McGrath oversaw the review of this article.

Supplementary Information

Below is the link to the electronic supplementary material.

Electronic supplementary material 1 (DOCX 21103 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Farnham, M.S., Ortved, K.F., Burris, D.L. et al. Articular Cartilage Friction, Strain, and Viability Under Physiological to Pathological Benchtop Sliding Conditions. Cel. Mol. Bioeng. 14, 349–363 (2021). https://doi.org/10.1007/s12195-021-00671-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12195-021-00671-2

Keywords

  • Tribological rehydration
  • Fluid load support
  • Osteoarthritis
  • Cartilage tribology
  • Convergent stationary contact area
  • Path analysis