Analysis of factors influencing the qualitative characteristics of equine synovial fluid


Keywords:
horse osteoarthritis synovial fluid rheological properties
P TYRNENOPOULOU
N DIAKAKIS
E RIZOS
S CHAINTOUTIS
MN PATSIKAS
P PAPADOPOULOU
A AGGELI
ZS POLIZOPOULOU
L PAPAZOGLOU
Abstract

The objective of the present study was to investigate the viscoelastic properties in synovial fluid between normal horses and horses with naturally occurring OA and to detect factors affecting synovial fluid viscosity. In total, 105 horses were included in this study. Synovial fluid samples were obtained from 60 mature horses with mild to moderate osteoarthritis in the 2nd interphalangeal, the metacarpophalangeal or the intercarpal joint. Forty-five horses were used as controls. Full rheological sample characterization was performed in order to measure the elastic G’ and viscous G’’ moduli. For determining hyaluronic acid concentrations a commercially available ELISA kit was used. The results of the linear mixed effect (LME) model revealed statistically significant (p < 0.001) effect of HA concentration, on the mean values of logG’ and logG” measurements. The ANOVA findings of the final model revealed statistically significant effect of joint type (p < 0.001) on the mean values of viscoelastic measurements. Interpreting the coefficients of the covariates osteoarthritis (p < 0.001) and age (p = 0.013), a negative correlation was detected on the response logG’ and logG” measurements. Geldings seemed to present lower viscous properties compared to mares. To the authors’ knowledge this is the first multivariate study to quantitatively evaluate the several factors that affect the viscoelastic properties of equine synovial fluid. Horses with osteoarthritis seemed to present lower viscoelastic properties compared to the healthy subjects that are joint type dependant. Finally, considering the multifactorial nature of osteoarthritis, one should expect an emerging need of personalized disease-modifying treatments.

Article Details
  • Section
  • Research Articles
Downloads
Download data is not yet available.
References
Auer JA, Fackelman GE, Gingerich DA (1980) Effect of hyaluronic acid in naturally occurring and experimentally induced osteoarthritis. Am J Vet Res;41:568.
Back W, Schamhardt HC, Barneveld A (1996) Are kinematics of the walk related to the locomotion of a warmblood horse at the trot? Vet Q.;18:79-84. doi:10.1080/01652176.1996.9694699.
Band PA, Heeter J, Wisniewski HG, Liublinska V, Pattanayak CW, Karia RJ, Stabler T, Balazs EA, Kraus VB (2015)Hyaluronan molecular weight distribution is associated with the risk of knee osteoarthritis progression. Osteoarthr Cartil ;23(1):70-76. doi:10.1016/j.joca.2014.09.017.
Bingöl AÖ, Lohmann D, Püschel K, Kulicke WM (2010) Characterization and comparison of shear and extensional flow of sodium hyaluronate and human synovial fluid. Biorheology.;47(3-4):205-224. doi:10.3233/BIR-2010-0572.
Blagojevic M, Jinks C, Jeffery A, Jordan 1KP (2010) Risk factors for onset of osteoarthritis of the knee in older adults: a systematic review and meta-analysis. Osteoarthr Cartil;18(1):24-33.
Bonnevie ED, Galesso D, Secchieri C, Cohen I, Bonassar LJ (2015) Elastoviscous transitions of articular cartilage reveal a mechanism of synergy between lubricin and hyaluronic acid. PLoS One ;10(11):1-15. doi:10.1371/journal.pone.0143415.
Borzacchiello A, Mayol L, Schiavinato A, Ambrosio L (2010) Effect of hyaluronic acid amide derivative on equine synovial fluid viscoelasticity. J Biomed Mater Res - Part A.;92(3):1162-1170. doi:10.1002/jbm.a.32455.
Budsberg SC, Lenz ME, Thonar EJ-MA (2006) Serum and synovial fluid concentrations of keratan sulfate and hyaluronan in dogs with induced stifle joint osteoarthritis following cranial cruciate ligament transection. Am J Vet Res ;67(3):429-432. doi:10.2460/ajvr.67.3.429.
Clayton HM, Sha DH, Mullineaux DR (2011). Three-dimensional torques and power of horse forelimb joints at trot. arXiv Prepr arXiv11083980.
Courties A, Gualillo O, Berenbaum F, Sellam J (2015) Metabolic stress-induced joint inflammation and osteoarthritis. Osteoarthr Cartil; 23(11):1955-1965. doi:10.1016/j.joca.2015.05.016.
Ferris DJ, Frisbie DD, Mcilwraith CW, Kawcak CE (2011) Current joint therapy usage in equine practice: A survey of veterinarians 2009. Equine Vet J 43(5):530-535. doi:10.1111/j.2042-3306.2010.00324.x
Giap SGE(2010) The Hidden Property of Arrhenius-type Relationship: Viscosity as a Function of Temperature. J Phys Sci;21(1):29-39.
Goudoulas TB, Kastrinakis EG, Nychas SG, Papazoglou LG, Kazakos GM, Kosmas P V(2010) Rheological study of synovial fluid obtained from dogs: Healthy, pathological, and post-surgery, after spontaneous rupture of cranial cruciate ligament. Ann Biomed Eng.;38(1):57-65.doi:10.1007/s10439-009-9832-9.
Hanna FS, Teichtahl AJ, Wluka AE, Wang Y, Urquhart DM, English DR, Giles GG, Cicuttini FM (2009)Women have increased rates of cartilage loss and progression of cartilage defects at the knee than men: a gender study of adults without clinical knee osteoarthritis. Menopause; 16(4):666-670.
Henderson EB, Grootveld M, Farrell A, Smith EC, Thompson PW, Blake DR (1991) A pathological role for damaged hyaluronan in synovitis. Ann Rheum Dis;50(3):196.
Kuroki K, Cook JL, Kreeger JM (2002) Mechanisms of action and potential uses of hyaluronan in dogs with osteoarthritis. J Am Vet Med Assoc;221(7):944-950.
Kuznetsova A, Brockhoff PB, Christensen RHB (2015) lmerTest: tests in linear mixed effects models. R package version 2.0-20. Vienna R Found Stat Comput.
Madkhali A, Grecov D, Kwok E (2018) Rheological and Structural Characterization of Synovial Fluid from Patients with Osteoarthritis. C Proc.;35.
Morrison FA (2001) Understanding Rheology. Topics in Chemical Engineering.
Moyer W, Schumacher J, Schumacher J (2007) Guide to Equine Joint Injection and Regional Anesthesia. Veterinary Learning Systems.
Neu CP, Komvopoulos K, Reddi AH (2008) The interface of functional biotribology and regenerative medicine in synovial joints. Tissue Eng Part B Rev;14(3):235-247.
O’Connor MI (2007) Sex differences in osteoarthritis of the hip and knee. JAAOS-Journal Am Acad Orthop Surg;15:S22-S25.
Ogston BYAG, Stanier JE (1953) THE PHYSIOLOGICAL FUNCTION OF HYALURONIC ACID IN SYNOVIAL FLUID ; VISCOUS , ELASTIC AND LUBRICANT PROPERTIES From the Department of Biochemistry , University of Oxford & Bauer, J Physiol, 119 (2-3) pp.244-252.
Pitsillides AA, Skerry TM, Edwards JC (1999) Joint immobilization reduces synovial fluid hyaluronan concentration and is accompanied by changes in the synovial intimal cell populations. Rheumatology (Oxford);38(11):1108-1112. doi:10.1093/rheumatology/38.11.1108.
Plickert HD, Bondzio A, Einspanier R, Tichy A, Brunnberg L (2013) Hyaluronic acid concentrations in synovial fluid of dogs with different stages of osteoarthritis. Res Vet Sci ;94(3):728-734. doi:10.1016/j.rvsc.2012.11.007.
Ross MW, Dyson SJ (2010) Diagnosis and Management of Lameness in the Horse-E-Book. Elsevier Health Sciences.
Schmidt TA, Gastelum NS, Nguyen QT, Schumacher BL, Sah RL (2007) Boundary lubrication of articular cartilage: role of synovial fluid constituents. Arthritis Rheum ;56(3):882-891.
Squires GR, Okouneff S, Ionescu M, Poole AR (2003) The pathobiology of focal lesion development in aging human articular cartilage and molecular matrix changes characteristic of osteoarthritis. Arthritis Rheum;48(5):1261-1270. doi:10.1002/art.10976.
Team RC (2013) R: A language and environment for statistical computing.
Temple-Wong MM, Ren S, Quach P, Hansen BC, Chen AC, Hasegawa A, D’Lima DD, Koziol J, Masuda K, Lotz MK, Sah RL (2016) Hyaluronan concentration and size distribution in human knee synovial fluid: Variations with age and cartilage degeneration. Arthritis Res Ther;18(1):1-8. doi:10.1186/s13075-016-0922-4.
Trotter GW, McIlwraith CW (1996) Clinical features and diagnosis of equine joint disease. Jt Dis horse:120-145.
Venable RO, Stoker AM, Cook CR, Cockrell MK, Cook JL (2008) Examination of synovial fluid hyaluronan quantity and quality in stifle joints of dogs with osteoarthritis. Am J Vet Res ;69(12):1569-1573.doi:10.2460/ajvr.69.12.1569.
Vitanzo PC, Sennett BJ (2006) Hyaluronans: is clinical effectiveness dependent on molecular weight? Am J Orthop (Belle Mead NJ) ;35(9):421—428. http://europepmc.org/abstract/MED/17036778.
Yu F, Zhang F, Luan T, Zhang Z, Zhang H (2014) Rheological studies of hyaluronan solutions based on the scaling law and constitutive models. Polym (United Kingdom);55(1):295-301. doi:10.1016/j.polymer.2013.11.047.
Most read articles by the same author(s)