Cartilage boundary lubrication of ovine synovial fluid following anterior cruciate ligament transection: a longitudinal study.

OBJECTIVE To assess ovine synovial fluid (oSF) from different post-injury time points for (1) proteoglycan-4 (PRG4) and hyaluronan (HA) concentration, (2) HA molecular weight (MW) distribution, (3) cartilage boundary lubrication function, and (4) lubricant composition-function relationships. The association between cartilage boundary lubrication and gross cartilage changes after injury was also examined. METHODS oSF was collected 2, 4, 10, and 20 weeks post anterior cruciate ligament (ACL) transection in five skeletally mature sheep. PRG4 and HA concentrations were measured using sandwich enzyme-linked immunosorbent assay, and HA MW distribution by agarose gel electrophoresis. Cartilage boundary lubrication of oSF was assessed using a cartilage-cartilage friction test. Gross damage to articular cartilage was also quantified at 20 weeks using modified Drez scoring protocol. RESULTS Early (2-4 weeks) after ACL injury, PRG4 concentrations were significantly higher (P = 0.045, P = 0.037), and HA concentrations were substantially lower (P = 0.005, P = 0.005) compared to 20 weeks. The HA MW distribution also shifted towards lower ranges in the early post-injury stage. The kinetic friction coefficients were significantly higher 2-4 weeks post injury (P = 0.008 and P = 0.049) compared to 20 weeks. Poor cartilage boundary lubricating ability early after injury was associated with cartilage damage at 20 weeks. CONCLUSION Altered composition and diminished boundary lubrication of oSF early after ACL transection may pre-dispose the articular cartilage to degenerative changes and initiate osteoarthritis (OA). These observations also provide potential motivation for biotherapeutic interventions at earlier time points post injury.

[1]  B. R. Black,et al.  Cartilage Injury After Acute, Isolated Anterior Cruciate Ligament Tear , 2012, The American journal of sports medicine.

[2]  Braden C Fleming,et al.  Effects of Supplemental Intra-articular Lubricin and Hyaluronic Acid on the Progression of Posttraumatic Arthritis in the Anterior Cruciate Ligament–Deficient Rat Knee , 2011, The American journal of sports medicine.

[3]  A. R. Jones,et al.  Bioregulation of lubricin expression by growth factors and cytokines. , 2007, European cells & materials.

[4]  A. Pitsillides,et al.  Joint immobilization reduces synovial fluid hyaluronan concentration and is accompanied by changes in the synovial intimal cell populations. , 1999, Rheumatology.

[5]  J. Buckwalter,et al.  Hyaluronans in the treatment of osteoarthritis of the knee: evidence for disease-modifying activity. , 2005, Osteoarthritis and cartilage.

[6]  G. Jay,et al.  Coefficients of friction, lubricin, and cartilage damage in the anterior cruciate ligament‐deficient guinea pig knee , 2008, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[7]  Robert L Sah,et al.  Boundary lubrication of articular cartilage: role of synovial fluid constituents. , 2007, Arthritis and rheumatism.

[8]  E. Balazs,et al.  Hyaluronic acid in synovial fluid. I. Molecular parameters of hyaluronic acid in normal and arthritis human fluids. , 1967, Arthritis and rheumatism.

[9]  Miho Suzuki,et al.  High molecular weight hyaluronic acid relieved joint pain and prevented the progression of cartilage degeneration in a rabbit osteoarthritis model after onset of arthritis , 2010, Modern rheumatology.

[10]  Koichi Masuda,et al.  A systems biology approach to synovial joint lubrication in health, injury, and disease , 2012, Wiley interdisciplinary reviews. Systems biology and medicine.

[11]  T. Schmidt,et al.  Disulfide-bonded multimers of proteoglycan 4 PRG4 are present in normal synovial fluids. , 2009, Biochimica et biophysica acta.

[12]  Y. Iwamoto,et al.  Mechanical effects of the intraarticular administration of high molecular weight hyaluronic acid plus phospholipid on synovial joint lubrication and prevention of articular cartilage degeneration in experimental osteoarthritis. , 2003, Arthritis and rheumatism.

[13]  G. Firestein,et al.  The biophysical mechanisms of altered hyaluronan concentration in synovial fluid after anterior cruciate ligament transection. , 2012, Arthritis and rheumatism.

[14]  Spss,et al.  Discovering Statistics (4th Edition ed. , 2013 .

[15]  E. Tanaka,et al.  Superficial zone protein affects boundary lubrication on the surface of mandibular condylar cartilage , 2011, Cell and Tissue Research.

[16]  Margaret M. Smith,et al.  Proteoglycan 4 downregulation in a sheep meniscectomy model of early osteoarthritis , 2006, Arthritis research & therapy.

[17]  Braden C. Fleming,et al.  Treatment of Anterior Cruciate Ligament Injuries, Part I , 2005, The American journal of sports medicine.

[18]  A. Engström‐Làurent,et al.  Concentration and molecular weight of sodium hyaluronate in synovial fluid from patients with rheumatoid arthritis and other arthropathies. , 1985, Annals of the rheumatic diseases.

[19]  Andrew A. Marino,et al.  Pathophysiology of Osteoarthritis: Evidence against the Viscoelastic Theory , 2009, Pathobiology.

[20]  G. Jay,et al.  Lubricating ability of aspirated synovial fluid from emergency department patients with knee joint synovitis. , 2004, The Journal of rheumatology.

[21]  Yamini Achari,et al.  Early joint tissue changes are highly correlated with a set of inflammatory and degradative synovial biomarkers after ACL autograft and its sham surgery in an ovine model , 2011, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[22]  G. Jay,et al.  Prevention of cartilage degeneration and gait asymmetry by lubricin tribosupplementation in the rat following anterior cruciate ligament transection. , 2012, Arthritis and rheumatism.

[23]  G. Jay,et al.  Association of articular cartilage degradation and loss of boundary-lubricating ability of synovial fluid following injury and inflammatory arthritis. , 2005, Arthritis and rheumatism.

[24]  T. Kubo,et al.  Long-term effects of hyaluronan on experimental osteoarthritis in the rabbit knee. , 1998, Osteoarthritis and cartilage.

[25]  J. Boucher,et al.  Intra-articular injections with high molecular weight sodium hyaluronate as a therapy for canine arthritis , 2003, Veterinary Record.

[26]  Albert C. Chen,et al.  Proteoglycan 4 (PRG4) synthesis and immunolocalization in bovine meniscus , 2005, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[27]  Andy P. Field,et al.  Discovering Statistics Using Ibm Spss Statistics , 2017 .

[28]  M. Cowman,et al.  The effect of molecular weight on hyaluronan's cartilage boundary lubricating ability--alone and in combination with proteoglycan 4. , 2011, Osteoarthritis and cartilage.

[29]  E. Coudeyre,et al.  Animal evidence for hyaluronic acid efficacy in knee trauma injuries. Review of animal-model studies. , 2013, Physical therapy in sport : official journal of the Association of Chartered Physiotherapists in Sports Medicine.

[30]  C. Chichester,et al.  Review: Collagen markers in early arthritic diseases. , 2006, Clinica chimica acta; international journal of clinical chemistry.

[31]  K. Brandt,et al.  Effect of intraarticular hyaluronan injection on vertical ground reaction force and progression of osteoarthritis after anterior cruciate ligament transection. , 2005, The Journal of rheumatology.

[32]  G. E. Nugent-Derfus,et al.  Differential regulation of proteoglycan 4 metabolism in cartilage by IL-1α, IGF-I, and TGF-β1 , 2008 .

[33]  N. M. Aneloski,et al.  Dynamic shear stimulation of bovine cartilage biosynthesis of proteoglycan 4. , 2006, Arthritis and rheumatism.

[34]  Khaled Elsaid,et al.  Association between friction and wear in diarthrodial joints lacking lubricin , 2007, Arthritis and rheumatism.

[35]  B. Pierscionek,et al.  The kinetics of hyaluronan in normal and acutely inflamed synovial joints: observations with experimental arthritis in sheep. , 1993, Seminars in arthritis and rheumatism.

[36]  T. Schmidt,et al.  Diminished cartilage-lubricating ability of human osteoarthritic synovial fluid deficient in proteoglycan 4: Restoration through proteoglycan 4 supplementation. , 2012, Arthritis and rheumatism.

[37]  R. Sah,et al.  Effects of equine joint injury on boundary lubrication of articular cartilage by synovial fluid: role of hyaluronan. , 2012, Arthritis and rheumatism.

[38]  L. Moreland.  Intra-articular hyaluronan (hyaluronic acid) and hylans for the treatment of osteoarthritis: mechanisms of action , 2003, Arthritis research & therapy.

[39]  Jason P. Gleghorn,et al.  Prevention of cartilage degeneration in a rat model of osteoarthritis by intraarticular treatment with recombinant lubricin. , 2009, Arthritis and rheumatism.

[40]  G. Jay,et al.  The impact of anterior cruciate ligament injury on lubricin metabolism and the effect of inhibiting tumor necrosis factor alpha on chondroprotection in an animal model. , 2009, Arthritis and rheumatism.

[41]  K. Komvopoulos,et al.  Increased friction coefficient and superficial zone protein expression in patients with advanced osteoarthritis. , 2010, Arthritis and rheumatism.

[42]  K. Komvopoulos,et al.  Regulation of the friction coefficient of articular cartilage by TGF‐β1 and IL‐1β , 2009, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[43]  R. Sah,et al.  Effect of synovial fluid on boundary lubrication of articular cartilage. , 2007, Osteoarthritis and cartilage.

[44]  W. Bugbee,et al.  Effect of tibial plateau fracture on lubrication function and composition of synovial fluid. , 2012, The Journal of bone and joint surgery. American volume.

[45]  Braden C Fleming,et al.  Prevention of cartilage degeneration and restoration of chondroprotection by lubricin tribosupplementation in the rat following anterior cruciate ligament transection. , 2010, Arthritis and rheumatism.

[46]  Zhongmin Jin,et al.  Biotribology of articular cartilage--a review of the recent advances. , 2008, Medical engineering & physics.

[47]  G. Jay,et al.  Decreased lubricin concentrations and markers of joint inflammation in the synovial fluid of patients with anterior cruciate ligament injury. , 2008, Arthritis and rheumatism.

[48]  S. Kuriyama,et al.  Hyaluronan, cartilage destruction and hydrarthrosis in traumatic arthritis. , 1994, Osteoarthritis and cartilage.

[49]  C. Frank,et al.  Characterization of proteoglycan 4 and hyaluronan composition and lubrication function of ovine synovial fluid following knee surgery , 2013, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.