Hostname: page-component-8448b6f56d-gtxcr Total loading time: 0 Render date: 2024-04-16T17:03:49.393Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of intra-articular hyaluronic acid on ex vivo responses by third carpal bone cartilage from horses with experimentally induced synovitis

Published online by Cambridge University Press:  09 March 2007

Jan L Palmer ,
Joseph Mansour ,
Charles J Malemud  and
Alicia L Bertone
Jan L Palmer
Affiliation:
Department of Veterinary Clinical Sciences, Orthopaedic Research Laboratory, The Ohio State University, Columbus, OH, USA
Joseph Mansour
Affiliation:
Department of Mechanical and Aerospace Engineering, Case Western Reserve University, Cleveland, OH, USA
Charles J Malemud*
Affiliation:
Department of Medicine and Department of Anatomy, Case Western Reserve University, Cleveland, OH, USA Department of Medicine/Division of Rheumatic Diseases, University Hospitals of Cleveland, Foley Building Room 207, 2061 Cornell Road, Cleveland, OH 44106–5076, USA
Alicia L Bertone
Affiliation:
Department of Veterinary Clinical Sciences, Orthopaedic Research Laboratory, The Ohio State University, Columbus, OH, USA
*
*cjm4@cwru.edu
Get access

Abstract

We studied the extent to which intra-articular hyaluronic acid (HA) administered to horses with experimentally induced synovitis in the third middle carpal joint altered cartilage proteoglycans (PGs) and the biomechanical properties of the third carpal bone. Intra-articular HA (Hylartin-V®) was administered to the middle carpal joints of healthy horses before and after the induction of synovitis by Escherichia coli lipopolysaccharide (LPS). Two groups of horses received intra-articular HA only, with evaluation 2 and 6 weeks later (group 2 and group 4). Two other groups (group 1 and group 3) received LPS followed by intra-articular HA and evaluation 2 and 6 weeks later. Ex vivo third carpal bone cartilage PG synthesis was measured by 35SO4 incorporation and third carpal bone cartilage PG content was determined by an assay for glucuronic acid. Biomechanical properties were measured by indentation testing. At the 2-week evaluation, HA did not ablate the quantitative reduction in PG synthesis and PG content in animals with experimental synovitis. However, by 6 weeks, there was a significant rebound effect in that PG synthesis and PG content were elevated in horses with experimental synovitis that had received intra-articular HA, compared with horses that had received HA only for that period of time. There were also alterations in the gel filtration profiles of newly synthesized PGs on Sepharose CL-2B among the groups. However, there were no de novo PG species associated with any of the treatments. Furthermore, we found that the biomechanical properties of third carpal bone cartilage were not altered in any of the groups. These studies showed that intra-articular HA administered to horses with experimentally induced synovitis did not provide short-term (i.e. 2-week) benefit to third carpal bone cartilage PG synthesis. However, a long-term benefit of intra-articular HA may occur after the acute effects of synovitis on PG synthesis and PG content subside.

Keywords

hyaluronic acidequine bone cartilagesynovitis
Type
Research Article
Information
Equine and Comparative Exercise Physiology , Volume 1 , Issue 2 , May 2004 , pp. 119 - 129
Copyright
Copyright © Cambridge University Press 2004

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1Radin, EL, Paul, IL, Swann, DA and Schottstaed, ES (1971). Lubrication of synovial membrane. Annals of the Rheumatic Diseases 30: 322–325.Google Scholar
2Simkin, PA (1992). Biology and function of synovium. In: Finerman, GAM and Noyes, FR (eds), Biology and Biomechanics of the Traumatized Synovial Joint. American Association of Orthopaedic Surgeons, Rosemont, IL, pp. 5–16.Google Scholar
3Prehm, P (1986). Mechanism, localization and inhibition of hyaluronate synthesis. In: Kuettner, KE, Schleyerbach, R and Hascall, VC (eds), Articular Cartilage Biochemistry Raven Press, New York, pp. 81–91.Google Scholar
4Wilkinson, LS, Pitsillides, AA, Worral, JG and Edwards, JC (1992). Light microscopic characterization of the fibro-blast-like synovial intimal cell (synoviocyte). Arthritis and Rheumatism 35: 1179–1184.CrossRefGoogle Scholar
5Caterson, B, Calabro, T, Donohue, PJ and Jahnke, MR (1986). Monoclonal antibodies against cartilage proteoglycan and link protein. In: Kuettner, KE, Schleyerbach, R and Hascall, VC (eds), Articular Cartilage Biochemistry Raven Press, New York, pp. 59–73.Google Scholar
6Hardingham, TE and Muir, H (1972). The specific interaction of hyaluronic acid with cartilage proteoglycan. Biochimica et Biophysica Acta 279: 398–400.Google Scholar
7Malemud, CJ, Goldberg, VM and Miller, LM (1987). Synthesis of a ‘free’ form of hyaluronic acid by articular chondrocytes in monolayer culture. Biochemistry International 14: 987–995.Google ScholarPubMed
8Chow, G, Knudson, CB, Homandberg, G and Knudson, W (1995). Increased CD44 expression in bovine articular chondrocytes by catabolic mediators. Journal of Biological Chemistry 270: 27734–27741.CrossRefGoogle Scholar
9Knudson, W, Aguiar, DJ, Hua, Q and Knudson, CB (1996). CD44 anchored hyaluronan-rich pericellular matrices: an ultrastructural and biochemical analysis. Experimental Cell Research 228: 216–228.CrossRefGoogle ScholarPubMed
10Knudson, W, Casey, B, Nishida, Y, Eger, W, Kuettner, KE and Knudson, CB (2000). Hyaluronan oligosaccharides perturb cartilage matrix homeostasis and induce chondrocyte chondrolysis. Arthritis and Rheumatism 43: 1165–1174.Google Scholar
11Balazs, EA and Denlinger, H (1993). Viscosupplementation: a new concept in the treatment of osteoarthritis. Journal of Rheumatology 20: (Suppl. 39) 3–9.Google Scholar
12Tulamo, RM, Houtti, J, Tupamaki, A and Salonen, M (1996). Hyaluronate and large molecular weight proteoglycans in synovial fluid from horses with various arthritides. American Journal of Veterinary Research 57: 932–937.Google Scholar
13Asheim, A and Lindblad, G (1976). Intra-articular treatment of arthritis in race-horses with sodium hyaluronate. Acta Veterinaria Scandinavica 17: 379–394.Google Scholar
14Gingerich, DA, Auer, JA and Fackelman, GE (1979). Force plate studies on the effect of exogenous hyaluronic acid on joint function in equine synovitis. Journal of Veterinary Pharmacology and Therapeutics 2: 291–298.CrossRefGoogle Scholar
15Rose, RJ (1979). The intra-articular use of sodium hyaluronate in the treatment of osteoarthritis in the horse. New Zealand Veterinary Journal 27: 5–8.Google Scholar
16Auer, JA, Fackelman, GE, Gingerich, DA and Fetter, AW (1980). Effect of hyaluronic acid in naturally and experimentally induced osteoarthritis. American Journal of Veterinary Research 41: 568–574.Google ScholarPubMed
17Phillips, MW (1989). Clinical trial comparison of intra-articular sodium hyaluronate products in the horse. Veterinary Review 9: 39–40.Google Scholar
18Caron, JP, Kaneene, JB and Miller, R (1996). Results of a survey of equine practitioners on the use and perceived efficacy of polysulfated glycosaminoglycans. Journal of the American Veterinary Association 209: 1564–1568.Google Scholar
19Hilbert, BJ, Rowley, G, Antonas, KN, McGill, CA, Reynoldson, JA and Hawkins, CD (1985). Changes in synovia after intra-articular injection of sodium hyaluronate into normal horse joints and after arthrotomy and experimental cartilage damage. Australian Veterinary Journal 62: 182–184.CrossRefGoogle ScholarPubMed
20Peloso, JG, Stick, JA, Caron, JP, Peloso, PM and Soutas-Little, RW (1993). Effects of hylan on amphotericin-induced carpal lameness in equids. American Journal of Veterinary Medicine 54: 1527–1534.Google ScholarPubMed
21Dahlberg, L, Lohmander, L and Ryd, L (1994). Intra-articular injections of hyaluronate in patients with cartilage abnormalities and knee pain. Arthritis and Rheumatism 37: 521–528.CrossRefGoogle ScholarPubMed
22Henderson, EB, Smith, EC, Pegley, F and Blake, DR (1994). Intra-articular injections of 750 kD hyaluronan in the treatment of osteoarthritis: a randomised single centre doubleblind placebo-controlled trial of 91 patients demonstrating lack of efficacy. Annals of the Rheumatic Diseases 53: 529–534.CrossRefGoogle ScholarPubMed
23Altman, RD and Moskowitz, RW (1998). Intra-articular sodium hyaluronate (Hyalgan) in the treatment of patients with osteoarthritis of the knee: a randomized clinical trial. Journal of Rheumatology 25: 2203–2212.Google Scholar
24Huskisson, EC and Donnelly, S (1999). Hyaluronic acid in the treatment of osteoarthritis of the knee. Rheumatology (Oxford) 38: 602–607.CrossRefGoogle ScholarPubMed
25Wright, KE, Maurer, SG and DiCesare, PE (2000). Viscosupplementation for osteoarthritis. American Journal of Orthopedics 29: 80–88.Google Scholar
26Larsen, NE, Lombard, KM, Parent, EG and Balazs, EA (1992). Effect of hylan on cartilage and chondrocyte cultures. Journal of Orthopaedic Research 10: 23–32.Google Scholar
27Morris, EA, Wilcon, S and Treadwell, BV (1992). Inhibition of interleukin-1-mediated proteoglycan degradation in bovine explants by addition of sodium hyaluronate. American Journal of Veterinary Research 53: 1977–1982.Google Scholar
28Shimazu, A, Ikko, A, Iwamoto, M, Koike, T, Yan, W, Okada, Y et al. (1993). Effects of hyaluronic acid on release of proteoglycan from the cell matrix in rabbit chondrocyte cultures in the presence or absence of cytokines. Arthritis and Rheumatism 36: 247–253.CrossRefGoogle ScholarPubMed
29Scheller, M, Zimmerman, B, Bernimoulin, JP and Scholtz, P (1995). Induction of metalloproteinase activity, cartilage matrix degradation and inhibition of endochondral mineralization in vitro by E coli lipopolysaccharide is mediated by interleukin-1 alpha. Cytokine 7: 331–337.Google Scholar
30Yamada, A, Uegaki, A, Nakamura, T and Ogawa, K (2000). ONO-4817, an orally active matrix metalloproteinase inhibitor, prevents lipopolysaccharide-induced proteoglycan release from joint cartilage in guinea pigs. Inflammation Research 49: 144–146.CrossRefGoogle ScholarPubMed
31Palmer, JL and Bertone, AL (1994). Experimentally-induced synovitis as a model for acute synovitis in the horse. Equine Veterinary Journal 26: 492–495.Google Scholar
32Abatangelo, G, Botti, P, Del Bue, M, Gei, G, Samson, JC, Cortivo, R et al. (1989). Intraarticular sodium hyaluronate injections in the Pond–Nuki experimental model of osteoarthritis in dogs. I. Biochemical results. Clinical Orthopaedics and Related Research 241: 278–285.Google Scholar
33Schiavinato, A, Lini, E, Guidolin, D, Pezzoli, G, Botti, P, Martelli, M et al. (1989). Intra-articular sodium hyaluronate injections in the Pond-Nuki expermental model of osteoarthritis in dogs. II Morphological findings. Clinical Orthopaedics and Related Research 241: 286–299.Google Scholar
34Wiig, ME, Amiel, D, van de Berg, J, Kitabayashi, L, Harwood, FL and Arfors, KE (1990). The early effect of high molecular weight hyaluronan (hyaluronic acid) on anterior cruciate ligament healing: an experimental study in rabbits. Journal of Orthopaedic Research 8: 425–434.CrossRefGoogle ScholarPubMed
35Armstrong, S, Read, R and Ghosh, P (1994). The effects of intra-articular hyaluronan on cartilage and subchondral bone changes in an ovine model of early osteoarthritis. Journal of Rheumatology 21: 680–688.Google Scholar
36Roneus, B, Lindblad, A, Lindholm, A and Jones, B (1993). Effects of intra-articular corticosteroid and sodium hyaluronate injections on synovial fluid production and synovial fluid contents of sodium hyaluronate and proteoglycans in normal equine joints. Journal of Veterinary Medicine 40: 10–16.CrossRefGoogle Scholar
37Palmer, JL, Bertone, AL, Malemud, CJ and Mansour, J (1996). Biochemical and biomechanical alterations in equine articular cartilage following experimentally-induced synovitis. Osteoarthritis and Cartilage 4: 127–137.CrossRefGoogle ScholarPubMed
38Kawcak, CE, Firsbie, DD, Trotter, GW, McIlwaith, CW, Gillete, SM, Powers, BE et al. (1997). Effects of intravenous administration of sodium hyaluronate on carpal joints after arthroscopic surgery and osteochondral fragmentation. American Journal of Veterinary Research 58: 1132–1140.Google Scholar
39Caron, JP and Genovese, RL (2003). Principles and practices of joint disease treatment. In: Ross, MW and Dyson, SJ (eds), Diagnosis and Management of Lameness in the Horse, Saunders, Philadelphia, PA, pp. 746–764.CrossRefGoogle Scholar
40Stashak, TS (2002). Examination for lameness. In: Troy, D (Ed.), Adam's Lameness in Horses Vol. 3. Lippincott, Williams and Wilkins, Philadelphia, PA, p. 122.Google Scholar
41Palmer, JL, Bertone, AL, Malemud, CJ, Carter, BG, Papay, RS and Mansour, J (1995). Site-specific proteoglycan characteristics of third carpal bone articular cartilage in exercised and non-exercised horses. American Journal of Veterinary Research 56: 1570–1576.CrossRefGoogle Scholar
42Burba, DJ, Collier, MA, DeBault, LE and Walls, RC (1992). An arthroscopic biopsy procedure for obtaining osteochondral samples from the equine midcarpal joint. Journal of Investigative Surgery 5: 343–359.Google Scholar
43Palmer, JL, Bertone, AL, Malemud, CJ and Mansour, J (1998). Changes in third carpal bone articular cartilage after synovectomy in normal and inflamed joints. Veterinary Surgery 27: 321–330.CrossRefGoogle ScholarPubMed
44Bertone, AL (2003). Non-infectious arthritis. In: Ross, MW and Dyson, SJ (eds), Diagnosis and Management of Lameness in the Horse, Saunders, Philadelphia, PA, pp. 606–610.Google Scholar
45Bitter, T and Muir, HM (1962). A modified uronic acid carbazole reaction. Analytical Biochemistry 4: 330–334.CrossRefGoogle ScholarPubMed
46Smith, PK, Krohn, RI, Hermanson, GT, Mallia, AK, Gartner, PH, Provenzano, DJ et al. (1985). Measurement of protein using bicinochoninic acid. Analytical Biochemistry 150: 76–85.Google Scholar
47Mak, AF, Lai, WM and Mow, VC (1987). Biphasic indentation of articular cartilage – I. Theoretical analysis. Journal of Biomechanics 20: 703–714.Google Scholar
48Mow, VC, Gibbs, MC, Lai, WM, Zhu, WB and Athanasiou, KA (1989). Biphasic indentation of articular cartilage – II. A numerical algorithm and an experimental study. Journal of Biomechanics 22: 853–861.Google Scholar
49Athanansiou, KA, Rosenwasser, MP, Buckwalter, JA, Malinin, TI and Mow, VC (1991). Interspecies comparisons of in situ intrinsic mechanical properties of distal femoral cartilage. Journal of Orthopaedic Research 9: 330–340.CrossRefGoogle Scholar
50Palmer, JL, Bertone, AL and Litsky, AS (1994). Contact area and pressure distribution of the equine third carpal bone during loading. Equine Veterinary Journal 26: 197–202.CrossRefGoogle ScholarPubMed
51Palmer, JL, Bertone, AL, Mansour, J, Carter, BG and Malemud, CJ (1995). Biomechanical properties of third carpal bone articular cartilage in exercised and non-exercised horses. Journal of Orthopaedic Research 13: 854–860.Google Scholar
52Myers, SL (1995). Effect of synovial fluid hyaluronan on the clearance of albumin from the canine knee. Annals of the Rheumatic Diseases 54: 433–434.CrossRefGoogle ScholarPubMed
53Myers, SL, Brandt, KD and Eilam, O (1995). Even low-grade synovitis accelerates the clearance of protein from the canine knee: Implications for the measurement of synovial fluid ‘markers’ of osteoarthritis. Arthritis and Rheumatism 38: 1085–1091.CrossRefGoogle ScholarPubMed
54Aviad, AD, Arthur, RM, Brenick, VA, Ferguson, HO and Teigland, MB (1988). Synacid vs. hylartin V in equine joint disease. Journal of Equine Veterinary Science 8: 112–116.Google Scholar
55Antonas, KN, Fraser, JRE and Muirden, KD (1973). Distribution of biologically labelled radioactive hyaluronic acid injected into joints. Annals of the Rheumatic Diseases 32: 103–111.Google Scholar
56Todhunter, PG, Kincaid, S, Todhunter, RJ, Kammermann, JR, Johnstone, B, Baird, AN et al. (1996). Immunohistochemical analysis of an equine model of synovitis-induced arthritis. American Journal of Veterinary Research 57: 1080–1093.Google Scholar
57Malemud, CJ (1999). Fundamental pathways in osteoarthritis: an overview. Frontiers in Bioscience 4: d659–d661.Google Scholar
58Caterson, B and Hughes, C (1995). Anabolic and catabolic markers of proteoglycan metabolism. In: Kuettner, KE and Goldberg, VM (eds), Osteoarthritic Disorders, American Academy of Orthopaedic Surgeons, Rosemont, IL, pp. 315–327.Google Scholar
59Pritzker, KPH (1991). Post-traumatic cartilage hypertrophy: edema or repair? Journal of Rheumatology 18: 314–315.Google ScholarPubMed
60Kikuchi, T, Yamada, H and Shinmei, M (1996). Effect of high molecular weight hyaluronan on cartilage degeneration in a rabbit model of osteoarthritis. Osteoarthritis and Cartilage 4: 99–110.Google Scholar