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BMC veterinary research2021; 17(1); 189; doi: 10.1186/s12917-021-02873-2

Investigation of synovial fluid lubricants and inflammatory cytokines in the horse: a comparison of recombinant equine interleukin 1 beta-induced synovitis and joint lavage models.

Abstract: Lameness is a debilitating condition in equine athletes that leads to more performance limitation and loss of use than any other medical condition. There are a limited number of non-terminal experimental models that can be used to study early inflammatory and synovial fluid biophysical changes that occur in the equine joint. Here, we compare the well-established carpal IL-1β-induced synovitis model to a tarsal intra-articular lavage model, focusing on serial changes in synovial fluid inflammatory cytokines/chemokines and the synovial fluid lubricating molecules lubricin/proteoglycan 4 and hyaluronic acid. The objectives of this study were to evaluate clinical signs; synovial membrane and synovial fluid inflammation; and synovial fluid lubricants and biophysical properties in response to carpal IL-1β synovitis and tarsal intra-articular lavage. Results: Hyaluronic acid (HA) concentrations, especially high molecular weight HA, and synovial fluid viscosity decreased after both synovitis and lavage interventions. Synovial fluid lubricin concentrations increased 17-20-fold for both synovitis and lavage models, with similar changes in both affected and contralateral joints, suggesting that repeated arthrocentesis alone resulted in elevated synovial fluid lubricin concentrations. Synovitis resulted in a more severe inflammatory response based on clinical signs (temperature, heart rate, respiratory rate, lameness and joint effusion) and clinicopathological and biochemical parameters (white blood cell count, total protein, prostaglandin E, sulfated glycosaminoglycans, tumor necrosis factor-α and CC chemokine ligands - 2, - 3, - 5 and - 11) as compared to lavage. Conclusions: Synovial fluid lubricin increased in response to IL-1β synovitis and joint lavage but also as a result of repeated arthrocentesis. Frequent repeated arthrocentesis is associated with inflammatory changes, including increased sulfated glycosaminoglycan concentrations and decreased hyaluronic acid concentrations. Synovitis results in more significant inflammatory changes than joint lavage. Our data suggests that synovial fluid lubricin, TNF-α, CCL2, CCL3, CCL5, CCL11 and sGAG may be useful biomarkers for synovitis and post-lavage joint inflammation. Caution should be exercised when performing repeated arthrocentesis clinically or in experimental studies due to the inflammatory response and loss of HA and synovial fluid viscosity.
Publication Date: 2021-05-12 PubMed ID: 33980227PubMed Central: PMC8117281DOI: 10.1186/s12917-021-02873-2Google Scholar: Lookup
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  • Comparative Study
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The study examined the changes in horse joint lubricants and inflammatory compounds during inflammation, comparing two experimental models: the carpal IL-1β-induced synovitis model and the tarsal intra-articular lavage model. The researchers found that both methods significantly affected the concentration of lubricating molecules and caused an inflammatory response, but the synovitis model resulted in a more severe response.

Study Overview

  • This research study was conducted on equine athletes to understand the early inflammatory changes in horse joints and the impact on the synovial fluid and its lubricating properties.
  • The researchers compared two models – the carpal IL-1β-induced synovitis model and the tarsal intra-articular lavage model, to draw parallels, if any, between their responses.

Objectives and Outcomes

  • The primary objectives were to evaluate the clinical symptoms, inflammation in the synovial membrane and fluid, and changes in the lubricating properties of the synovial fluid in the equine subjects.
  • The study found that both models experienced a decrease in high molecular weight hyaluronic acid (HA) and synovial fluid viscosity.
  • However, the concentrations of synovial fluid lubricin, a critical lubricating molecule, increased 17-20-fold across both models.
  • More severe inflammatory response and clinical signs such as temperature, heart rate, respiratory rate, and lameness were observed in the synovitis model compared to the lavage model.

Significance of the Study

  • The findings suggest that both IL-1β synovitis and joint lavage have a significant impact on the lubricating properties of the synovial fluid, leading to an inflammatory response. However, the severity was more pronounced with synovitis.
  • The increase in lubricin levels following frequent arthrocentesis, a clinical procedure where the joint cavity is punctured to aspirate fluid, suggests that it may cause inflammatory changes.
  • Identified biomarkers such as TNF-α, CCL- (2, 3, 5, and 11), and sGAG could potentially be used in diagnosing joint inflammation following synovitis or post-lavage.
  • The study advises caution when performing repeated arthrocentesis as it seems to result in inflammatory responses and loss of HA and synovial fluid viscosity.

Cite This Article

APA
Watkins A, Fasanello D, Stefanovski D, Schurer S, Caracappa K, D'Agostino A, Costello E, Freer H, Rollins A, Read C, Su J, Colville M, Paszek M, Wagner B, Reesink H. (2021). Investigation of synovial fluid lubricants and inflammatory cytokines in the horse: a comparison of recombinant equine interleukin 1 beta-induced synovitis and joint lavage models. BMC Vet Res, 17(1), 189. https://doi.org/10.1186/s12917-021-02873-2

Publication

ISSN: 1746-6148
NlmUniqueID: 101249759
Country: England
Language: English
Volume: 17
Issue: 1
Pages: 189
PII: 189

Researcher Affiliations

Watkins, Amanda
  • Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY, USA.
Fasanello, Diana
  • Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY, USA.
Stefanovski, Darko
  • Department of Biostatistics, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA, USA.
Schurer, Sydney
  • Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY, USA.
Caracappa, Katherine
  • Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY, USA.
D'Agostino, Albert
  • Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY, USA.
Costello, Emily
  • Robert Frederick Smith School of Chemical and Biomolecular Engineering, Cornell University, Ithaca, NY, USA.
Freer, Heather
  • Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY, USA.
Rollins, Alicia
  • Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY, USA.
Read, Claire
  • Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY, USA.
Su, Jin
  • Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY, USA.
Colville, Marshall
  • Robert Frederick Smith School of Chemical and Biomolecular Engineering, Cornell University, Ithaca, NY, USA.
Paszek, Matthew
  • Robert Frederick Smith School of Chemical and Biomolecular Engineering, Cornell University, Ithaca, NY, USA.
Wagner, Bettina
  • Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY, USA.
Reesink, Heidi
  • Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY, USA. hlr42@cornell.edu.

MeSH Terms

  • Animals
  • Arthrocentesis / adverse effects
  • Arthrocentesis / veterinary
  • Cytokines / metabolism
  • Female
  • Glycoproteins / metabolism
  • Horse Diseases
  • Horses
  • Hyaluronic Acid / metabolism
  • Inflammation
  • Injections, Intra-Articular / veterinary
  • Interleukin-1beta / administration & dosage
  • Interleukin-1beta / adverse effects
  • Male
  • Synovial Fluid / metabolism
  • Synovitis / chemically induced
  • Synovitis / metabolism
  • Synovitis / pathology
  • Therapeutic Irrigation / veterinary

Conflict of Interest Statement

The authors declare that they have no competing interests.

References

This article includes 78 references
  1. Goodrich LR, Nixon AJ. Medical treatment of osteoarthritis in the horse - a review.. Vet J 2006 Jan;171(1):51-69.
    doi: 10.1016/j.tvjl.2004.07.008pubmed: 16427582google scholar: lookup
  2. Rossdale PD, Hopes R, Digby NJ, offord K. Epidemiological study of wastage among racehorses 1982 and 1983.. Vet Rec 1985 Jan 19;116(3):66-9.
    doi: 10.1136/vr.116.3.66pubmed: 3976145google scholar: lookup
  3. Castro Martins M, Peffers MJ, Lee K, Rubio-Martinez LM. Effects of stanozolol on normal and IL-1β-stimulated equine chondrocytes in vitro.. BMC Vet Res 2018 Mar 20;14(1):103.
    doi: 10.1186/s12917-018-1426-zpmc: PMC5859414pubmed: 29554899google scholar: lookup
  4. Machado TSL, Massoco CO, Silva LCLC, Fülber J, Moreira JJ, Baccarin RYA. Effects of blood-derived products and sodium hyaluronate on equine synovial fluid cells and on synovial fluid from osteochondrotic joints of horses after arthroscopy and administration of treatment.. Am J Vet Res 2019 Jul;80(7):646-656.
    doi: 10.2460/ajvr.80.7.646pubmed: 31246124google scholar: lookup
  5. Spadari A, Rinnovati R, Babbini S, Romagnoli N. Clinical evaluation of intra-articular administration of stanozolol to manage lameness associated with acute and chronic osteoarthritis in horses.. J Equine Vet Sci 2015;35(2):105–110.
  6. Perrone G, Lastra Y, González C, Caggiano N, Giménez R, Pareja R, De Simone E. Treatment With Platelet Lysate Inhibits Proteases of Synovial Fluid in Equines With Osteoarthritis.. J Equine Vet Sci 2020 May;88:102952.
    doi: 10.1016/j.jevs.2020.102952pubmed: 32303304google scholar: lookup
  7. Gilbertie JM, Long JM, Schubert AG, Berglund AK, Schaer TP, Schnabel LV. Pooled Platelet-Rich Plasma Lysate Therapy Increases Synoviocyte Proliferation and Hyaluronic Acid Production While Protecting Chondrocytes From Synoviocyte-Derived Inflammatory Mediators.. Front Vet Sci 2018;5:150.
    doi: 10.3389/fvets.2018.00150pmc: PMC6039577pubmed: 30023361google scholar: lookup
  8. Fu X, Lin L, Zhang J, Yu C. Assessment of the efficacy of joint lavage in rabbits with osteoarthritis of the knee.. J Orthop Res 2009 Jan;27(1):91-6.
    doi: 10.1002/jor.20720pubmed: 18655133google scholar: lookup
  9. Cokelaere S, Malda J, van Weeren R. Cartilage defect repair in horses: Current strategies and recent developments in regenerative medicine of the equine joint with emphasis on the surgical approach.. Vet J 2016 Aug;214:61-71.
    doi: 10.1016/j.tvjl.2016.02.005pubmed: 27387728google scholar: lookup
  10. Cousty M, David Stack J, Tricaud C, David F. Effect of arthroscopic lavage and repeated intra-articular administrations of antibiotic in adult horses and foals with septic arthritis.. Vet Surg 2017 Oct;46(7):1008-1016.
    doi: 10.1111/vsu.12696pubmed: 28771839google scholar: lookup
  11. Baldwin CM, Smith MRW, Allen S, Wright IM. Radiographic and arthroscopic features of third carpal bone slab fractures and their impact on racing performance following arthroscopic repair in a population of racing Thoroughbreds in the UK.. Equine Vet J 2020 Mar;52(2):213-218.
    doi: 10.1111/evj.13155pubmed: 31356679google scholar: lookup
  12. Henderson E, Clements DN, Johnson CI. An in vitro study of the effect of the optimal irrigation solution conditions during canine articular surgery.. Vet Res Commun 2020 Feb;44(1):1-7.
    doi: 10.1007/s11259-019-09765-9pubmed: 31788728google scholar: lookup
  13. Teeple E, Karamchedu NP, Larson KM, Zhang L, Badger GJ, Fleming BC, Jay GD. Arthroscopic irrigation of the bovine stifle joint increases cartilage surface friction and decreases superficial zone lubricin.. J Biomech 2016 Sep 6;49(13):3106-3110.
  14. McIlwraith CW, Nixon AJ, Wright IM. Diagnostic and surgical arthroscopy in the horse.. 4 2015.
  15. Rossetti RB, Massoco Cde O, Penna AC, Silva LC. An experimental study to compare inflammatory response due to liquid or gas joint distension in horses submitted to arthroscopy.. Acta Cir Bras 2012 Dec;27(12):848-54.
  16. Das S, Banquy X, Zappone B, Greene GW, Jay GD, Israelachvili JN. Synergistic interactions between grafted hyaluronic acid and lubricin provide enhanced wear protection and lubrication.. Biomacromolecules 2013 May 13;14(5):1669-77.
    doi: 10.1021/bm400327apubmed: 23560944google scholar: lookup
  17. Musumeci G, Trovato FM, Loreto C, Leonardi R, Szychlinska MA, Castorina S, Mobasheri A. Lubricin expression in human osteoarthritic knee meniscus and synovial fluid: a morphological, immunohistochemical and biochemical study.. Acta Histochem 2014 Jun;116(5):965-72.
    doi: 10.1016/j.acthis.2014.03.011pubmed: 24932985google scholar: lookup
  18. Jay GD, Waller KA. The biology of lubricin: near frictionless joint motion.. Matrix Biol 2014 Oct;39:17-24.
    pubmed: 25172828doi: 10.1016/j.matbio.2014.08.008google scholar: lookup
  19. Svala E, Jin C, Rüetschi U, Ekman S, Lindahl A, Karlsson NG, Skiöldebrand E. Characterisation of lubricin in synovial fluid from horses with osteoarthritis.. Equine Vet J 2017 Jan;49(1):116-123.
    doi: 10.1111/evj.12521pubmed: 26507102google scholar: lookup
  20. Feeney E, Peal BT, Inglis JE, Su J, Nixon AJ, Bonassar LJ, Reesink HL. Temporal changes in synovial fluid composition and elastoviscous lubrication in the equine carpal fracture model.. J Orthop Res 2019 May;37(5):1071-1079.
    pmc: PMC6768400pubmed: 30859611doi: 10.1002/jor.24281google scholar: lookup
  21. Waller KA, Zhang LX, Elsaid KA, Fleming BC, Warman ML, Jay GD. Role of lubricin and boundary lubrication in the prevention of chondrocyte apoptosis.. Proc Natl Acad Sci U S A 2013 Apr 9;110(15):5852-7.
    doi: 10.1073/pnas.1219289110pmc: PMC3625316pubmed: 23530215google scholar: lookup
  22. Mathies B. Effects of Viscoseal, a synovial fluid substitute, on recovery after arthroscopic partial meniscectomy and joint lavage.. Knee Surg Sports Traumatol Arthrosc 2006 Jan;14(1):32-9.
    doi: 10.1007/s00167-005-0625-xpubmed: 15918064google scholar: lookup
  23. Hempfling H. Intra-articular hyaluronic acid after knee arthroscopy: a two-year study.. Knee Surg Sports Traumatol Arthrosc 2007 May;15(5):537-46.
    doi: 10.1007/s00167-006-0260-1pubmed: 17187274google scholar: lookup
  24. Sellam J, Berenbaum F. The role of synovitis in pathophysiology and clinical symptoms of osteoarthritis.. Nat Rev Rheumatol 2010 Nov;6(11):625-35.
    doi: 10.1038/nrrheum.2010.159pubmed: 20924410google scholar: lookup
  25. Hawkins DL, MacKay RJ, Gum GG, Colahan PT, Meyer JC. Effects of intra-articularly administered endotoxin on clinical signs of disease and synovial fluid tumor necrosis factor, interleukin 6, and prostaglandin E2 values in horses.. Am J Vet Res 1993 Mar;54(3):379-86.
    pubmed: 8498739
  26. Palmer JL, Bertone AL. Experimentally-induced synovitis as a model for acute synovitis in the horse.. Equine Vet J 1994 Nov;26(6):492-5.
  27. Palmer JL, Bertone AL, Malemud CJ, Mansour J. Biochemical and biomechanical alterations in equine articular cartilage following an experimentally-induced synovitis.. Osteoarthritis Cartilage 1996 Jun;4(2):127-37.
    doi: 10.1016/S1063-4584(05)80321-8pubmed: 8806114google scholar: lookup
  28. Todhunter PG, Kincaid SA, Todhunter RJ, Kammermann JR, Johnstone B, Baird AN, Hanson RR, Wright JM, Lin HC, Purohit RC. Immunohistochemical analysis of an equine model of synovitis-induced arthritis.. Am J Vet Res 1996 Jul;57(7):1080-93.
    pubmed: 8807026
  29. Ludwig EK, Brandon Wiese R, Graham MR, Tyler AJ, Settlage JM, Werre SR, Petersson-Wolfe CS, Kanevsky-Mullarky I, Dahlgren LA. Serum and Synovial Fluid Serum Amyloid A Response in Equine Models of Synovitis and Septic Arthritis.. Vet Surg 2016 Oct;45(7):859-867.
    doi: 10.1111/vsu.12531pubmed: 27580707google scholar: lookup
  30. Colbath AC, Dow SW, Hopkins LS, Phillips JN, McIlwraith CW, Goodrich LR. Induction of Synovitis Using Interleukin-1 Beta: Are There Differences in the Response of Middle Carpal Joint Compared to the Tibiotarsal Joint?. Front Vet Sci 2018;5:208.
    doi: 10.3389/fvets.2018.00208pmc: PMC6127273pubmed: 30234134google scholar: lookup
  31. Nelson BB, King MR, Frisbie DD. Assessment of a novel equine tarsocrural experimental joint disease model using recombinant interleukin-1β and arthroscopic articular sampling of the medial malleolus of the tibia on the standing sedated horse.. Vet J 2017 Nov;229:54-59.
    doi: 10.1016/j.tvjl.2017.10.021pubmed: 29183574google scholar: lookup
  32. Ross TN, Kisiday JD, Hess T, McIlwraith CW. Evaluation of the inflammatory response in experimentally induced synovitis in the horse: a comparison of recombinant equine interleukin 1 beta and lipopolysaccharide.. Osteoarthritis Cartilage 2012 Dec;20(12):1583-90.
    doi: 10.1016/j.joca.2012.08.008pubmed: 22917743google scholar: lookup
  33. Scott I, Midha A, Rashid U, Ball S, Walding A, Kerry P, Delaney S, Cruwys S. Correlation of gene and mediator expression with clinical endpoints in an acute interleukin-1beta-driven model of joint pathology.. Osteoarthritis Cartilage 2009 Jun;17(6):790-7.
    doi: 10.1016/j.joca.2008.09.016pubmed: 19010066google scholar: lookup
  34. Jay GD, Elsaid KA, Zack J, Robinson K, Trespalacios F, Cha CJ, Chichester CO. Lubricating ability of aspirated synovial fluid from emergency department patients with knee joint synovitis.. J Rheumatol 2004 Mar;31(3):557-64.
    pubmed: 14994405
  35. Irwin RM, Feeney E, Secchieri C, Galesso D, Cohen I, Oliviero F, Ramonda R, Bonassar LJ. Distinct tribological endotypes of pathological human synovial fluid reveal characteristic biomarkers and variation in efficacy of viscosupplementation at reducing local strains in articular cartilage.. Osteoarthritis Cartilage 2020 Apr;28(4):492-501.
    pmc: PMC7707424pubmed: 32105835doi: 10.1016/j.joca.2020.02.029google scholar: lookup
  36. Bertuglia A, Pagliara E, Grego E, Ricci A, Brkljaca-Bottegaro N. Pro-inflammatory cytokines and structural biomarkers are effective to categorize osteoarthritis phenotype and progression in Standardbred racehorses over five years of racing career.. BMC Vet Res 2016 Nov 8;12(1):246.
    doi: 10.1186/s12917-016-0873-7pmc: PMC5100096pubmed: 27821120google scholar: lookup
  37. Ma TW, Li Y, Wang GY, Li XR, Jiang RL, Song XP, Zhang ZH, Bai H, Li X, Gao L. Changes in Synovial Fluid Biomarkers after Experimental Equine Osteoarthritis.. J Vet Res 2017 Dec;61(4):503-508.
    doi: 10.1515/jvetres-2017-0056pmc: PMC5937351pubmed: 29978116google scholar: lookup
  38. Luster AD. Chemokines--chemotactic cytokines that mediate inflammation.. N Engl J Med 1998 Feb 12;338(7):436-45.
    doi: 10.1056/NEJM199802123380706pubmed: 9459648google scholar: lookup
  39. Zlotnik A, Yoshie O. The chemokine superfamily revisited.. Immunity 2012 May 25;36(5):705-16.
  40. David KS, Oliveira ERA, Horta BAC, Valente AP, de Paula VS. Insights into CC Chemokine Ligand 2/Chemokine Receptor 2 Molecular Recognition: A Step Forward toward Antichemotactic Agents.. Biochemistry 2017 Jun 27;56(25):3197-3210.
    doi: 10.1021/acs.biochem.7b00129pubmed: 28570817google scholar: lookup
  41. Hosokawa Y, Hosokawa I, Ozaki K, Matsuo T. Transforming growth factor-β1 increases C-C chemokine ligand 11 production in interleukin 4-stimulated human periodontal ligament cells.. Cell Biol Int 2018 Sep;42(10):1395-1400.
    doi: 10.1002/cbin.11030pubmed: 29993161google scholar: lookup
  42. Haringman JJ, Ludikhuize J, Tak PP. Chemokines in joint disease: the key to inflammation?. Ann Rheum Dis 2004 Oct;63(10):1186-94.
    doi: 10.1136/ard.2004.020529pmc: PMC1754785pubmed: 15082471google scholar: lookup
  43. Schnabel CL, Wemette M, Babasyan S, Freer H, Baldwin C, Wagner B. C-C motif chemokine ligand (CCL) production in equine peripheral blood mononuclear cells identified by newly generated monoclonal antibodies.. Vet Immunol Immunopathol 2018 Oct;204:28-39.
    doi: 10.1016/j.vetimm.2018.09.003pubmed: 30596378google scholar: lookup
  44. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization.. Trends Immunol 2004 Dec;25(12):677-86.
    doi: 10.1016/j.it.2004.09.015pubmed: 15530839google scholar: lookup
  45. Kindstedt E, Holm CK, Sulniute R, Martinez-Carrasco I, Lundmark R, Lundberg P. CCL11, a novel mediator of inflammatory bone resorption.. Sci Rep 2017 Jul 13;7(1):5334.
    doi: 10.1038/s41598-017-05654-wpmc: PMC5509729pubmed: 28706221google scholar: lookup
  46. Endres M, Andreas K, Kalwitz G, Freymann U, Neumann K, Ringe J, Sittinger M, Häupl T, Kaps C. Chemokine profile of synovial fluid from normal, osteoarthritis and rheumatoid arthritis patients: CCL25, CXCL10 and XCL1 recruit human subchondral mesenchymal progenitor cells.. Osteoarthritis Cartilage 2010 Nov;18(11):1458-66.
    doi: 10.1016/j.joca.2010.08.003pubmed: 20709179google scholar: lookup
  47. Peal BT, Gagliardi R, Su J, Fortier LA, Delco ML, Nixon AJ, Reesink HL. Synovial fluid lubricin and hyaluronan are altered in equine osteochondral fragmentation, cartilage impact injury, and full-thickness cartilage defect models.. J Orthop Res 2020 Aug;38(8):1826-1835.
    pmc: PMC7354223pubmed: 31965593doi: 10.1002/jor.24597google scholar: lookup
  48. Reesink HL, Watts AE, Mohammed HO, Jay GD, Nixon AJ. Lubricin/proteoglycan 4 increases in both experimental and naturally occurring equine osteoarthritis.. Osteoarthritis Cartilage 2017 Jan;25(1):128-137.
    doi: 10.1016/j.joca.2016.07.021pmc: PMC5489058pubmed: 27498214google scholar: lookup
  49. Antonacci JM, Schmidt TA, Serventi LA, Cai MZ, Shu YL, Schumacher BL, McIlwraith CW, Sah RL. Effects of equine joint injury on boundary lubrication of articular cartilage by synovial fluid: role of hyaluronan.. Arthritis Rheum 2012 Sep;64(9):2917-26.
    doi: 10.1002/art.34520pmc: PMC3424370pubmed: 22605527google scholar: lookup
  50. Sotelo EDP, Vendruscolo CP, Fülber J, Seidel SRT, Jaramillo FM, Agreste FR, Silva LCLCD, Baccarin RYA. Effects of Joint Lavage with Dimethylsulfoxide on LPS-Induced Synovitis in Horses-Clinical and Laboratorial Aspects.. Vet Sci 2020 Apr 30;7(2).
    pmc: PMC7356314pubmed: 32365982doi: 10.3390/vetsci7020057google scholar: lookup
  51. Blewis ME, Nugent-Derfus GE, Schmidt TA, Schumacher BL, Sah RL. A model of synovial fluid lubricant composition in normal and injured joints.. Eur Cell Mater 2007 Mar 6;13:26-39.
    doi: 10.22203/eCM.v013a03pubmed: 17340555google scholar: lookup
  52. Neuenschwander HM, Moreira JJ, Vendruscolo CP, Fülber J, Seidel SRT, Michelacci YM, Baccarin RYA. Hyaluronic acid has chondroprotective and joint-preserving effects on LPS-induced synovitis in horses.. J Vet Sci 2019 Nov;20(6):e67.
    doi: 10.4142/jvs.2019.20.e67pmc: PMC6883190pubmed: 31775194google scholar: lookup
  53. Jin C, Ekwall AK, Bylund J, Björkman L, Estrella RP, Whitelock JM, Eisler T, Bokarewa M, Karlsson NG. Human synovial lubricin expresses sialyl Lewis x determinant and has L-selectin ligand activity.. J Biol Chem 2012 Oct 19;287(43):35922-33.
    doi: 10.1074/jbc.M112.363119pmc: PMC3476260pubmed: 22930755google scholar: lookup
  54. Wanderling C, Liles J, Davis E, Schmitt D, Statz S, Guler N, Hoppensteadt D, Fareed J, Hopkinson W. Levels of Matrix-Degrading Enzymes and Lubricin in Patients With Degenerative Joint Disease Requiring Arthroplasty.. Clin Appl Thromb Hemost 2018 Jan;24(1):41-46.
    doi: 10.1177/1076029617724231pmc: PMC6709591pubmed: 28877607google scholar: lookup
  55. Elsaid KA, Jay GD, Warman ML, Rhee DK, Chichester CO. Association of articular cartilage degradation and loss of boundary-lubricating ability of synovial fluid following injury and inflammatory arthritis.. Arthritis Rheum 2005 Jun;52(6):1746-55.
    doi: 10.1002/art.21038pubmed: 15934070google scholar: lookup
  56. Menarim BC, Gillis KH, Oliver A, Mason C, Werre SR, Luo X, Byron CR, Kalbfleisch TS, MacLeod JN, Dahlgren LA. Inflamed synovial fluid induces a homeostatic response in bone marrow mononuclear cells in vitro: Implications for joint therapy.. FASEB J 2020 Mar;34(3):4430-4444.
    doi: 10.1096/fj.201902698Rpubmed: 32030831google scholar: lookup
  57. Bertone AL, Palmer JL, Jones J. Synovial fluid cytokines and eicosanoids as markers of joint disease in horses.. Vet Surg 2001 Nov-Dec;30(6):528-38.
    doi: 10.1053/jvet.2001.28430pubmed: 11704948google scholar: lookup
  58. Ross-Jones TN, McIlwraith CW, Kisiday JD, Hess TM, Hansen DK, Black J. Influence of an n-3 long-chain polyunsaturated fatty acid-enriched diet on experimentally induced synovitis in horses.. J Anim Physiol Anim Nutr (Berl) 2016 Jun;100(3):565-77.
    doi: 10.1111/jpn.12359pubmed: 26189710google scholar: lookup
  59. Kamm JL, Nixon AJ, Witte TH. Cytokine and catabolic enzyme expression in synovium, synovial fluid and articular cartilage of naturally osteoarthritic equine carpi.. Equine Vet J 2010 Nov;42(8):693-9.
  60. Rubartelli A, Bajetto A, Allavena G, Cozzolino F, Sitia R. Post-translational regulation of interleukin 1 beta secretion.. Cytokine 1993 Mar;5(2):117-24.
    doi: 10.1016/1043-4666(93)90050-Fpubmed: 8334227google scholar: lookup
  61. Wahl K, Adams SB, Moore GE. Contamination of joints with tissue debris and hair after arthrocentesis: the effect of needle insertion angle, spinal needle gauge, and insertion of spinal needles with and without a stylet.. Vet Surg 2012 Apr;41(3):391-8.
  62. Hunt CL, Leatherwood JL, Coverdale JA, Sigler DL, Vogelsang MM, Arnold CE. Effects of repeated arthrocentesis on systemic cytokine expression and leukocyte population in young horses challenged with intra-articular lipopolysaccharide.. J Anim Sci 2019 Jan 1;97(1):184-191.
    doi: 10.1093/jas/sky423pmc: PMC6313106pubmed: 30423145google scholar: lookup
  63. van den Boom R, Brama PA, Kiers GH, DeGroot J, Barneveld A, van Weeren RR. The influence of repeated arthrocentesis and exercise on matrix metalloproteinase and tumour necrosis factor alpha activities in normal equine joints.. Equine Vet J 2004 Mar;36(2):155-9.
    doi: 10.2746/0425164044868602pubmed: 15038439google scholar: lookup
  64. Brama PA, van den Boom R, DeGroott J, Kiers GH, van Weeren PR. Collagenase-1 (MMP-1) activity in equine synovial fluid: influence of age, joint pathology, exercise and repeated arthrocentesis.. Equine Vet J 2004 Jan;36(1):34-40.
    doi: 10.2746/0425164044864705pubmed: 14756369google scholar: lookup
  65. Francoz D, Desrochers A, Latouche JS. Effect of repeated arthrocentesis and single joint lavage on cytologic evaluation of synovial fluid in 5 young calves.. Can J Vet Res 2007 Apr;71(2):129-34.
    pmc: PMC1829182pubmed: 17479776
  66. White KK, Hodgson DR, Hancock D, Parry BW, Cordell C. Changes in equine carpal joint synovial fluid in response to the injection of two local anesthetic agents.. Cornell Vet 1989 Jan;79(1):25-38.
    pubmed: 2912672
  67. Berg RI, Sykes JE, Kass PH, Vernau W. Effect of repeated arthrocentesis on cytologic analysis of synovial fluid in dogs.. J Vet Intern Med 2009 Jul-Aug;23(4):814-7.
  68. Wisniewski HG, Hua JC, Poppers DM, Naime D, Vilcek J, Cronstein BN. TNF/IL-1-inducible protein TSG-6 potentiates plasmin inhibition by inter-alpha-inhibitor and exerts a strong anti-inflammatory effect in vivo.. J Immunol 1996 Feb 15;156(4):1609-15.
    pubmed: 8568267
  69. Nishida Y, Knudson CB, Nietfeld JJ, Margulis A, Knudson W. Antisense inhibition of hyaluronan synthase-2 in human articular chondrocytes inhibits proteoglycan retention and matrix assembly.. J Biol Chem 1999 Jul 30;274(31):21893-9.
    doi: 10.1074/jbc.274.31.21893pubmed: 10419509google scholar: lookup
  70. Elsaid KA, Jay GD, Chichester CO. Detection of collagen type II and proteoglycans in the synovial fluids of patients diagnosed with non-infectious knee joint synovitis indicates early damage to the articular cartilage matrix.. Osteoarthritis Cartilage 2003 Sep;11(9):673-80.
    doi: 10.1016/S1063-4584(03)00151-1pubmed: 12954238google scholar: lookup
  71. Elsaid KA, Machan JT, Waller K, Fleming BC, Jay GD. 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.. Arthritis Rheum 2009 Oct;60(10):2997-3006.
    doi: 10.1002/art.24800pmc: PMC2800051pubmed: 19790069google scholar: lookup
  72. Barton KI, Ludwig TE, Achari Y, Shrive NG, Frank CB, Schmidt TA. Characterization of proteoglycan 4 and hyaluronan composition and lubrication function of ovine synovial fluid following knee surgery.. J Orthop Res 2013 Oct;31(10):1549-54.
    doi: 10.1002/jor.22399pubmed: 23722645google scholar: lookup
  73. Lee HG, Cowman MK. An agarose gel electrophoretic method for analysis of hyaluronan molecular weight distribution.. Anal Biochem 1994 Jun;219(2):278-87.
    doi: 10.1006/abio.1994.1267pubmed: 8080084google scholar: lookup
  74. Nixon AJ, Begum L, Mohammed HO, Huibregtse B, O'Callaghan MM, Matthews GL. Autologous chondrocyte implantation drives early chondrogenesis and organized repair in extensive full- and partial-thickness cartilage defects in an equine model.. J Orthop Res 2011 Jul;29(7):1121-30.
    doi: 10.1002/jor.21366pubmed: 21319216google scholar: lookup
  75. Wagner B, Freer H. Development of a bead-based multiplex assay for simultaneous quantification of cytokines in horses.. Vet Immunol Immunopathol 2009 Feb 15;127(3-4):242-8.
    doi: 10.1016/j.vetimm.2008.10.313pubmed: 19027964google scholar: lookup
  76. Wagner B, Hillegas JM, Babasyan S. Monoclonal antibodies to equine CD23 identify the low-affinity receptor for IgE on subpopulations of IgM+ and IgG1+ B-cells in horses.. Vet Immunol Immunopathol 2012 Apr 15;146(2):125-34.
    doi: 10.1016/j.vetimm.2012.02.007pubmed: 22405681google scholar: lookup
  77. Chan DD, Xiao WF, Li J, de la Motte CA, Sandy JD, Plaas A. Deficiency of hyaluronan synthase 1 (Has1) results in chronic joint inflammation and widespread intra-articular fibrosis in a murine model of knee joint cartilage damage.. Osteoarthritis Cartilage 2015 Nov;23(11):1879-89.
    doi: 10.1016/j.joca.2015.06.021pmc: PMC4630789pubmed: 26521733google scholar: lookup
  78. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method.. Nat Protoc 2008;3(6):1101-8.
    doi: 10.1038/nprot.2008.73pubmed: 18546601google scholar: lookup

Citations

This article has been cited 13 times.
  1. Mustonen AM, Lehmonen N, Oikari S, Capra J, Raekallio M, Mykkänen A, Paakkonen T, Rilla K, Niemelä T, Nieminen P. Counts of hyaluronic acid-containing extracellular vesicles decrease in naturally occurring equine osteoarthritis. Sci Rep 2022 Oct 20;12(1):17550.
    doi: 10.1038/s41598-022-21398-8pubmed: 36266410google scholar: lookup
  2. Miescher I, Wolint P, Opelz C, Snedeker JG, Giovanoli P, Calcagni M, Buschmann J. Impact of High-Molecular-Weight Hyaluronic Acid on Gene Expression in Rabbit Achilles Tenocytes In Vitro. Int J Mol Sci 2022 Jul 18;23(14).
    doi: 10.3390/ijms23147926pubmed: 35887273google scholar: lookup
  3. Botto R, Riccio V, Galosi L, Rossi G, Vincenzetti S, Tambella AM, De Francesco F, Pennasilico L, Riccio M, Salvaggio A, Sassaroli S, Palumbo Piccionello A. Effects of Intra-Articular Autologous Adipose Micrograft for the Treatment of Osteoarthritis in Dogs: A Prospective, Randomized, Controlled Study. Animals (Basel) 2022 Jul 20;12(14).
    doi: 10.3390/ani12141844pubmed: 35883392google scholar: lookup
  4. Korac L, St George L, MacNicol J, McCrae P, Jung L, Golestani N, Karrow N, Cánovas A, Pearson W. Functional and biochemical inflammatory responses to low-dose intra-articular recombinant equine IL-1β: a pilot study. Front Vet Sci 2025;12:1746738.
    doi: 10.3389/fvets.2025.1746738pubmed: 41624292google scholar: lookup
  5. Gao W, Gao Z, Xiao H, Qian Y, Fan R, Li Y, Yang S, Yang Y, Qiao Y. Energy metabolism dysfunction and therapeutic strategies for treating temporomandibular disorders. Front Med (Lausanne) 2025;12:1581446.
    doi: 10.3389/fmed.2025.1581446pubmed: 40641978google scholar: lookup
  6. Roth SP, Liso G, Brehm W, Wagner B, Schnabel CL, Troillet A. Selected cytokine and chemokine concentrations in equine autologous conditioned serum are similar under defined and practically relevant storage conditions. Front Vet Sci 2025;12:1588240.
    doi: 10.3389/fvets.2025.1588240pubmed: 40496923google scholar: lookup
  7. Pietsch W, Schumann T, Safferthal M, Geue N, Pagel K, Götze M. The Road Toward Nanopore Sequencing of Glycosaminoglycans. Handb Exp Pharmacol 2025;288:109-130.
    doi: 10.1007/164_2025_750pubmed: 40442467google scholar: lookup
  8. Moore GE, Leatherwood JL, Glass KG, Arnold CE, Paris BL, Carter MM, George JM, Fontenot AB, Martinez RE, Franklin MA, Norton SA, Bradbery AN, Wickersham TA. Influence of dietary Saccharomyces cerevisiae fermentation product on markers of inflammation and cartilage metabolism in young exercising horses challenged with intra-articular lipopolysaccharide. Transl Anim Sci 2025;9:txaf042.
    doi: 10.1093/tas/txaf042pubmed: 40336821google scholar: lookup
  9. Miescher I, Wolint P, Opelz C, Snedeker JG, Giovanoli P, Calcagni M, Buschmann J. Proliferation and gene expression data of rabbit Achilles tenocyte in vitro culture in the presence of high-molecular weight hyaluronic acid (1.01-1.8 MDa). Data Brief 2025 Jun;60:111459.
    doi: 10.1016/j.dib.2025.111459pubmed: 40206697google scholar: lookup
  10. Terlinden A, Jacquet S, Manivong S, Cullier A, Cassé F, Legendre F, Garcia AA, Roullin G, Moldovan F, Sirois P, Banquy X, Galéra P, Audigié F, Demoor M, Bertoni L. Double-blinded, randomized tolerance study of a biologically enhanced Nanogel with endothelin-1 and bradykinin receptor antagonist peptides via intra-articular injection for osteoarthritis treatment in horses. BMC Vet Res 2024 Dec 4;20(1):547.
    doi: 10.1186/s12917-024-04352-wpubmed: 39633332google scholar: lookup
  11. Vishwanath K, Secor EJ, Watkins A, Reesink HL, Bonassar LJ. Loss of effective lubricating viscosity is the primary mechanical marker of joint inflammation in equine synovitis. J Orthop Res 2024 Jul;42(7):1438-1447.
    doi: 10.1002/jor.25793pubmed: 38291343google scholar: lookup
  12. Erxleben DA, Dodd RJ, Day AJ, Green DE, DeAngelis PL, Poddar S, Enghild JJ, Huebner JL, Kraus VB, Watkins AR, Reesink HL, Rahbar E, Hall AR. Targeted Analysis of the Size Distribution of Heavy Chain-Modified Hyaluronan with Solid-State Nanopores. Anal Chem 2024 Jan 30;96(4):1606-1613.
    doi: 10.1021/acs.analchem.3c04387pubmed: 38215004google scholar: lookup
  13. Canonici F, Cocumelli C, Cersini A, Marcoccia D, Zepparoni A, Altigeri A, Caciolo D, Roncoroni C, Monteleone V, Innocenzi E, Alimonti C, Ghisellini P, Rando C, Pechkova E, Eggenhöffner R, Scicluna MT, Barbaro K. Articular Cartilage Regeneration by Hyaline Chondrocytes: A Case Study in Equine Model and Outcomes. Biomedicines 2023 May 31;11(6).
    doi: 10.3390/biomedicines11061602pubmed: 37371697google scholar: lookup