Advertisement

Frontiers of Mechanical Engineering

, Volume 12, Issue 2, pp 234–252 | Cite as

Characterization of the surface and interfacial properties of the lamina splendens

  • Joe T. Rexwinkle
  • Heather K. Hunt
  • Ferris M. Pfeiffer
Review Article
  • 109 Downloads

Abstract

Joint disease affects approximately 52.5 million patients in the United States alone, costing 80.8 billion USD in direct healthcare costs. The development of treatment programs for joint disease and trauma requires accurate assessment of articular cartilage degradation. The articular cartilage is the interfacial tissue between articulating surfaces, such as bones, and acts as low-friction interfaces. Damage to the lamina splendens, which is the articular cartilage’s topmost layer, is an early indicator of joint degradation caused by injury or disease. By gaining comprehensive knowledge on the lamina splendens, particularly its structure and interfacial properties, researchers could enhance the accuracy of human and animal biomechanical models, as well as develop appropriate biomimetic materials for replacing damaged articular cartilage, thereby leading to rational treatment programs for joint disease and injury. Previous studies that utilize light, electron, and force microscopy techniques have found that the lamina splendens is composed of collagen fibers oriented parallel to the cartilage surface and encased in a proteoglycan matrix. Such orientation maximizes wear resistance and proteoglycan retention while promoting the passage of nutrients and synovial fluid. Although the structure of the lamina splendens has been explored in the literature, the low-friction interface of this tissue remains only partially characterized. Various functional models are currently available for the interface, such as pure boundary lubrication, thin films exuded under pressure, and sheets of trapped proteins. Recent studies suggest that each of these lubrication models has certain advantages over one another. Further research is needed to fully model the interface of this tissue. In this review, we summarize the methods for characterizing the lamina splendens and the results of each method. This paper aims to serve as a resource for existing studies to date and a roadmap of the investigations needed to gain further insight into the lamina splendens and the progression of joint disease.

Keywords

cartilage lamina splendens characterization biomechanics orthopaedic review 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

We thank Khanh Van Nguyen for creating all unreferenced images in the paper and Jill Jouret and Paul J. D. Whiteside for their assistance in editing the paper prior to submission. The authors report no conflict of interest.

References

  1. 1.
    Centers for Disease Control and Prevention. Osteoarthritis, 2014, http://www.cdc.gov/arthritis/basics/osteoarthritis.htmGoogle Scholar
  2. 2.
    Centers for Disease Control and Prevention. Arthritis: Cost Statistics. 2015, http://www.cdc.gov/arthritis/data_statistics/cost.htmGoogle Scholar
  3. 3.
    Centers for Disease Control and Prevention. Arthritis: National Statistics. 2016, http://www.cdc.gov/arthritis/data_statistics/national-statistics.htmlGoogle Scholar
  4. 4.
    Desrochers J, Amrein M A, Matyas J R. Structural and functional changes of the articular surface in a post-traumatic model of early osteoarthritis measured by atomic force microscopy. Journal of Biomechanics, 2010, 43(16): 3091–3098CrossRefGoogle Scholar
  5. 5.
    Weiss C, Mirow S. An ultrastructural study of osteoarthritic changes in the articular cartilage of human knees. The Journal of Bone and Joint Surgery. American Volume, 1972, 54(5): 954–972CrossRefGoogle Scholar
  6. 6.
    Hollander A P, Dickinson S C, Kafienah W. Stem cells and cartilage development: Complexities of a simple tissue. Stem Cells, 2010, 28(11): 1992–1996CrossRefGoogle Scholar
  7. 7.
    Jay G D, Torres J R, Rhee D K, et al. Association between friction and wear in diarthrodial joints lacking lubricin. Arthritis & Rheumatism, 2007, 56(11): 3662–3669CrossRefGoogle Scholar
  8. 8.
    Wu J P, Kirk T B, Zheng M H. Assessment of three-dimensional architecture of collagen fibers in the superficial zone of bovine articular cartilage. Journal of Musculoskeletal Research, 2004, 08(04): 167–179CrossRefGoogle Scholar
  9. 9.
    Thambyah A, Broom N. On how degeneration influences loadbearing in the cartilage-bone system: A microstructural and micromechanical study. Osteoarthritis and Cartilage, 2007, 15(12): 1410–1423CrossRefGoogle Scholar
  10. 10.
    MacConaill M A. The movements of bones and joints. Journal of Bone and Joint Surgery, 1951, 33-B: 251–257Google Scholar
  11. 11.
    Aspden R M, Hukins D W L. The lamina splendens of articular cartilage is an artefact of phase contrast microscopy. Proceedings of the Royal Society of London. Series B, Biological Sciences, 1979, 206(1162): 109–113CrossRefGoogle Scholar
  12. 12.
    Clark J M. The organisation of collagen fibrils in the superficial zones of articular cartilage. Journal of Anatomy, 1990, 171: 117–130Google Scholar
  13. 13.
    Weiss C, Rosenberg L, Helfet A J. An ultrastructural study of normal young adult human articular cartilage. Journal of Bone and Joint Surgery. American Volume, 1968, 50(4): 663–674CrossRefGoogle Scholar
  14. 14.
    Cohen N P, Foster R J, Mow V C. Composition and dynamics of articular cartilage: Structure, function, and maintaining healthy state. Journal of Orthopaedic & Sports Physical Therapy, 1998, 28(4): 203–215CrossRefGoogle Scholar
  15. 15.
    Wu J P, Kirk T B, Zheng M H. Study of the collagen structure in the superficial zone and physiological state of articular cartilage using a 3D confocal imaging technique. Journal of Orthopaedic Surgery and Research, 2008, 3(29): 1–11Google Scholar
  16. 16.
    Teshima R, Otsuka T, Takasu N, et al. Structure of the most superficial layer of articular cartilage. The Journal of Bone and Joint Surgery. British Volume, 1995, 77(3): 460–464CrossRefGoogle Scholar
  17. 17.
    Jeffery A K, Blunn G W, Archer C W, et al. Three-dimensional collagen architecture in bovine articular cartilage. Journal of Bone and Joint Surgery. British Volume, 1991, 73(5): 795–801CrossRefGoogle Scholar
  18. 18.
    Clarke I C. Articular cartilage: A review and scanning electron microscope study. Journal of Bone and Joint Surgery. British Volume, 1971, 53(4): 732–750CrossRefGoogle Scholar
  19. 19.
    Teshima R, Ono M, Yamashita Y, et al. Immunohistochemical collagen analysis of the most superficial layer in adult articular cartilage. Journal of Orthopaedic Science, 2004, 9(3): 270–273CrossRefGoogle Scholar
  20. 20.
    Fujioka R, Aoyama T, Takakuwa T. The layered structure of the articular surface. Osteoarthritis and Cartilage, 2013, 21(8): 1092–1098CrossRefGoogle Scholar
  21. 21.
    Coles J M, Zhang L, Blum J J, et al. Loss of cartilage structure, stiffness, and frictional properties in mice lacking PRG4. Arthritis and Rheumatism, 2010, 62(6): 1666–1674CrossRefGoogle Scholar
  22. 22.
    Jurvelin J S, Müller D J, Wong M, et al. Surface and subsurface morphology of bovine humeral articular cartilage as assessed by atomic force and transmission electron microscopy. Journal of Structural Biology, 1996, 117(1): 45–54CrossRefGoogle Scholar
  23. 23.
    Mansour J M. Biomechanics of Cartilage. In: Hughes C, ed. Kinesiology: The Mechanics and Pathomechanics of Human Movement. 2nd ed. Baltimore: Lippincott Williams & Wilkins, 2009, 66–79Google Scholar
  24. 24.
    Dunham J, Shackleton D R, Billingham ME J, et al. A reappraisal of the structure of normal canine articular cartilage. Journal of Anatomy, 1988, 157: 89–99Google Scholar
  25. 25.
    Davies D V, Barnett C H, Cochrane W, et al. Electron microscopy of articular cartilage in the young adult rabbit. Annals of the Rheumatic Diseases, 1962, 21(1): 11–22CrossRefGoogle Scholar
  26. 26.
    Jay G D, Torres J R, Warman M L, et al. The role of lubricin in the mechanical behavior of synovial fluid. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104 (15): 6194–6199CrossRefGoogle Scholar
  27. 27.
    Balazs E A, Bloom G A, Swann D A. Fine structure and glycosaminoglycan content of the surface layer of articular cartilage. Federation Proceedings, 1966, 25(6): 1813–1816Google Scholar
  28. 28.
    Walker P S, Sikorski J, Dowson D, et al. Behaviour of synovial fluid on surfaces of articular cartilage. A scanning electron microscope study. Annals of the Rheumatic Diseases, 1969, 28(1): 1–14CrossRefGoogle Scholar
  29. 29.
  30. 30.
    Silva C, Horkayne-Szakaly I, Lin D C, et al. Osmotic swelling behavior of bovine cartilage. Proceedings of the 238th ACS National Meeting. American Chemical Society. Polymer Preprints, 2009, 50(2): 553–554Google Scholar
  31. 31.
    von der Mark K, Park J, Bauer S, et al. Nanoscale engineering of biomimetic surfaces: Cues from the extracellular matrix. Cell and Tissue Research, 2010, 339(1): 131–153CrossRefGoogle Scholar
  32. 32.
    Krishnan R, Park S, Eckstein F, et al. Inhomogeneous cartilage properties enhance superficial interstitial fluid support and frictional properties, but do not provide a homogeneous state of stress. Journal of Biomechanical Engineering, 2003, 125(5): 569–577CrossRefGoogle Scholar
  33. 33.
    Basalo I M, Raj D, Krishnan R, et al. Effects of enzymatic degradation on the frictional response of articular cartilage in stress relaxation. Journal of Biomechanics, 2005, 38(6): 1343–1349CrossRefGoogle Scholar
  34. 34.
    O’Hara B P, Urban J P G, Maroudas A. Influence of cyclic loading on the nutrition of articular cartilage. Annals of the Rheumatic Diseases, 1990, 49(7): 536–539CrossRefGoogle Scholar
  35. 35.
    Das S, Banquy X, Zappone B, et al. Synergistic interactions between grafted hyaluronic acid and lubricin provide enhanced wear protection and lubrication. Biomacromolecules, 2013, 14(5): 1669–1677CrossRefGoogle Scholar
  36. 36.
    Elsaid K A, Chichester C O, Jay G D. Lubricin purified from bovine synovial fluid and from articular cartilage exhibit similar binding affinities to cartilage matrix proteins. In: Proceedings of 53rd Annual Meeting of the Orthopaedic Research Society. Poster Abstract, 2007Google Scholar
  37. 37.
    Chang D P, Abu-Lail N I, Coles J M, et al. Friction force microscopy of lubricin and hyaluronic acid between hydrophobic and hydrophilic surfaces. Soft Matter, 2009, 5(18): 3438–3445CrossRefGoogle Scholar
  38. 38.
    Chang D P, Abu-Lail N I, Guilak F, et al. Conformational mechanics, adsorption, and normal force interactions of lubricin and hyaluronic acid on model surfaces. Langmuir, 2008, 24(4): 1183–1193CrossRefGoogle Scholar
  39. 39.
    Bonnevie E D, Galesso D, Secchieri C, et al. Elastoviscous transitions of articular cartilage reveal a mechanism of synergy between lubricin and hyaluronic acid. PLoS ONE, 2015, 10(11): e043415CrossRefGoogle Scholar
  40. 40.
    Sypeck D. Damage evolution in titanium matrix composites. Dissertation for the Doctoral Degree. Charlottesville: University of Virginia, 1996Google Scholar
  41. 41.
    Ministry of Defence, England. Royal armament research and development establishment. In: Watson-Adams B R, Dibb J J, Wronski A S, eds. Mechanical Properties of Fiber-Reinforced Composites Tested Under Superposed Hydrostatic Pressures. VA: National Technical Information Services, 1975Google Scholar
  42. 42.
    Caligaris M, Ateshian G A. Effects of sustained interstitial fluid pressurization under migrating contact area, and boundary lubrication by synovial fluid, on cartilage friction. Osteoarthritis and Cartilage, 2008, 16(10): 1220–1227CrossRefGoogle Scholar
  43. 43.
    Chan S M T, Neu C P, Duraine G, et al. Tribological altruism: A sacrificial layer mechanism of synovial joint lubrication in articular cartilage. Journal of Biomechanics, 2012, 45(14): 2426–2431CrossRefGoogle Scholar
  44. 44.
    Jay G D. Lubricin and Surfacing of Articular Joints. Current Opinion in Orthopaedics, 2004, 15(5): 355–359CrossRefGoogle Scholar
  45. 45.
    Guilak F, Ratcliffe A, Mow V C. Chondrocyte deformation and local tissue strain in articular cartilage: A confocal microscopy study. Journal of Orthopaedic Research, 1995, 13(3): 410–421CrossRefGoogle Scholar
  46. 46.
    Sung K B, Richards-Kortum R, Follen M, et al. Fiber optic confocal reflectance microscopy: A new real-time technique to view nuclear morphology in cervical squamous epithelium in vivo. Optics Express, 2003, 11(24): 3171–3181CrossRefGoogle Scholar
  47. 47.
    Yeh A T, Hammer-Wilson M J, Van Sickle D C, et al. Nonlinear optical microscopy of articular cartilage. Osteoarthritis and Cartilage, 2005, 13(4): 345–352CrossRefGoogle Scholar
  48. 48.
    Hanson K M, Bardeen C J. Application of nonlinear optical microscopy for imaging skin. Photochemistry and Photobiology, 2009, 85(1): 33–44CrossRefGoogle Scholar
  49. 49.
    Kumar P, Oka M, Toguchida J, et al. Role of uppermost superficial surface layer of articular cartilage in the lubrication mechanism of joints. Journal of Anatomy, 2001, 199(3): 241–250CrossRefGoogle Scholar
  50. 50.
    Kobayashi S, Yonekubo S, Kurogouchi Y. Cryoscanning electron microscopy of loaded articular cartilage with special reference to the surface amorphous layer. Journal of Anatomy, 1996, 188(Pt2): 311–322Google Scholar
  51. 51.
    Crockett R, Roos S, Rossbach P, et al. Imaging of the surface of human and bovine articular cartilage with ESEM and AFM. Tribology Letters, 2005, 19(4): 311–317CrossRefGoogle Scholar
  52. 52.
    Chan S M T, Neu C P, Duraine G, et al. Atomic force microscope investigation of the boundary-lubricant layer in articular cartilage. Osteoarthritis and Cartilage, 2010, 18(7): 956–963CrossRefGoogle Scholar
  53. 53.
    Han L, Frank E H, Greene J J, et al. Time-dependent nanomechanics of cartilage. Biophysical Journal, 2011, 100(7): 1846–1854CrossRefGoogle Scholar
  54. 54.
    Desrochers J, Amrein M W, Matyas J R. Viscoelasticity of the articular cartilage surface in early osteoarthritis. Osteoarthritis and Cartilage, 2012, 20(5): 413–421CrossRefGoogle Scholar
  55. 55.
    Park S, Costa K D, Ateshian G A. Microscale frictional response of bovine articular cartilage from atomic force microscopy. Journal of Biomechanics, 2004, 37(11): 1679–1687CrossRefGoogle Scholar
  56. 56.
    Moa-Anderson B J, Costa K D, Hung C T, et al. Bovine articular cartilage surface topography and roughness in fresh versus frozen tissue samples using atomic force microscopy. In: Proceedings of Summer Bioengineering Conference. New Orleans, 2003Google Scholar
  57. 57.
    Chan S M T, Neu C P, Komvopoulos K, et al. Dependence of nanoscale friction and adhesion properties of articular cartilage on contact load. Journal of Biomechanics, 2011, 44(7): 1340–1345CrossRefGoogle Scholar
  58. 58.
    Bae WC, Temple MM, Amiel D, et al. Indentation testing of human cartilage: Sensitivity to articular surface degeneration. Arthritis and Rheumatism, 2003, 48(12): 3382–3394CrossRefGoogle Scholar
  59. 59.
    Caligaris M, Canal C E, Ahmad C S, et al. Investigation of the frictional response of osteoarthritic human tibiofemoral joints and the potential beneficial tribological effect of healthy synovial fluid. Osteoarthritis and Cartilage, 2009, 17(10): 1327–1332CrossRefGoogle Scholar
  60. 60.
    Schmidt T A, Gastelum N S, Nguyen Q T, et al. Boundary lubrication of articular cartilage: Role of synovial fluid constituents. Arthritis and Rheumatism, 2007, 56(3): 882–891CrossRefGoogle Scholar
  61. 61.
    Krishnan R, Caligaris M, Mauck R L, et al. Removal of the superficial zone of bovine articular cartilage does not increase its frictional coefficient. Osteoarthritis and Cartilage, 2004, 12(12): 947–955CrossRefGoogle Scholar
  62. 62.
    Chan S M T, Neu C P, Komvopoulos K, et al. The role of lubricant entrapment at biological interfaces: Reduction of friction and adhesion in articular cartilage. Journal of Biomechanics, 2011, 44 (11): 2015–2020CrossRefGoogle Scholar
  63. 63.
    Greene G W, Banquy X, Lee D W, et al. Adaptive mechanically controlled lubrication mechanism found in articular joints. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(13): 5255–5259CrossRefGoogle Scholar
  64. 64.
    Schmidt T A, Sah R L. Effect of synovial fluid on boundary lubrication of articular cartilage. Osteoarthritis and Cartilage, 2007, 15(1): 35–47CrossRefGoogle Scholar
  65. 65.
    Basalo I M, Chen F H, Hung C T, et al. Frictional response of bovine articular cartilage under creep loading following proteoglycan digestion with chondroitinase ABC. Journal of Biomechanical Engineering, 2006, 128(1): 131–134Google Scholar
  66. 66.
    John Innes Center. What is light microscopy? https://www.jic.ac.uk/microscopy/intro_LM.html
  67. 67.
    Shackleton D R, Nahir A M, Billingham M E J, et al. The lamina splendens of articular cartilage: Fact or artifact. Clinical Science, 1984, 66(6): 22CrossRefGoogle Scholar
  68. 68.
    University of Utah. Electron Microscopy Tutorial. http://advancedmicroscopy.utah.edu/education/electron-micro/index.html
  69. 69.
    University of Iowa. Transmission Electron Microscopy. https://cmrf.research.uiowa.edu/transmission-electron-microscopy
  70. 70.
    University of Iowa. Scanning Electron Microscopy. https://cmrf.research.uiowa.edu/scanning-electron-microscopy
  71. 71.
    Sargent J A. Low temperature scanning electron microscopy: Advantages and applications. Scanning Microscopy, 1988, 2(2): 835–849Google Scholar
  72. 72.
    Donald A M. The use of environmental scanning electron microscopy for imaging wet and insulating materials. Nature Materials, 2003, 2(8): 511–516CrossRefGoogle Scholar
  73. 73.
    Meyer E. Atomic force microscopy. Progress in Surface Science, 1992, 41(1): 3–49CrossRefGoogle Scholar
  74. 74.
    Chan S M T, Neu C P, Komvopoulos K, et al. Dependence of nanoscale friction and adhesion properties of articular cartilage on contact load. Journal of Biomechanics, 2011, 44(7): 1340–1345CrossRefGoogle Scholar
  75. 75.
    Mitchell N, Laurin C, Shepard N. The effect of osmium tetroxide and nitrogen mustard on normal articular cartilage. Journal of Bone and Joint Surgery. British Volume, 1973, 55(4): 814–821CrossRefGoogle Scholar
  76. 76.
    Hollander A P, Pidoux I, Reiner A, et al. Damage to Type II collagen in aging and osteoarthritis starts at the articular surface, originates around chondrocytes, and extends into the cartilage with progressive degeneration. Journal of Clinical Investigation, 1995, 96(6): 2859–2869CrossRefGoogle Scholar
  77. 77.
    Sun Y, Chen M Y, Zhao C, et al. The effect of hyaluronidase, phospholipase, lipid solvent and trypsin on the lubrication of canine flexor digitorum profundus tendon. Journal of Orthopaedic Research, 2008, 26(9): 1225–1229CrossRefGoogle Scholar
  78. 78.
    Muir H. Molecular approach to the understanding of osteoarthrosis. Annals of the Rheumatic Diseases, 1977, 36(3): 199–208CrossRefGoogle Scholar
  79. 79.
    Banquy X, Lee D W, Das S, et al. Shear-induced aggregation of mammalian synovial fluid components under boundary lubrication conditions. Advanced Functional Materials, 2014, 24(21): 3152–3161CrossRefGoogle Scholar
  80. 80.
    Israelchvili J, Min Y, Akbulut M, et al. Recent advances in the surface forces apparatus (SFA) technique. Reports on Progress in Physics, 2010, 73(3): 036601CrossRefGoogle Scholar
  81. 81.
    Andresen Eguiluz R C, Cook S G, Brown C N, et al. Fibronectin mediates enhanced wear protection of lubricin during shear. Biomacromolecules, 2015, 16(9): 2884–2894CrossRefGoogle Scholar
  82. 82.
    Hou J S, Holmes M H, Lai W M, et al. Boundary conditions at the cartilage-synovial fluid interface for joint lubrication and theoretical verifications. Journal of Biomechanical Engineering, 1989, 111(1): 78–87CrossRefGoogle Scholar
  83. 83.
    Teeple E, Elsaid K A, Jay G D, et al. Effects of supplemental intraarticular lubricin and hyaluronic acid on the progression of posttraumatic arthritis in the anterior cruciate ligament-deficient rat knee. American Journal of Sports Medicine, 2011, 39(1): 164–172CrossRefGoogle Scholar

Copyright information

© Higher Education Press and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Joe T. Rexwinkle
    • 1
  • Heather K. Hunt
    • 2
  • Ferris M. Pfeiffer
    • 2
    • 3
  1. 1.Mechanical EngineeringUniversity of MissouriColumbiaUSA
  2. 2.BioengineeringUniversity of MissouriColumbiaUSA
  3. 3.Orthopaedic SurgeryUniversity of MissouriColumbiaUSA

Personalised recommendations