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Vet Comp Orthop Traumatol 2014; 27(05): 358-365
DOI: 10.3415/VCOT-13-11-0136
Original Research
Schattauer GmbH

Comparison of healing in forelimb and hindlimb surgically induced core lesions of the equine superficial digital flexor tendon

R. J. Estrada
1   Equine Clinic, School of Veterinary Medicine, Free University of Berlin, Berlin, Germany
2   Large Animal Hospital, School of Veterinary Medicine, National University, Heredia, Costa Rica
,
P. R. Van Weeren
3   Department of Equine Sciences, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands
,
C. H. A. Van de Lest
3   Department of Equine Sciences, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands
4   Department of Biochemistry and Cell Biology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands
,
J. Boere
3   Department of Equine Sciences, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands
,
M. Reyes
5   Department of Orthopaedics, Erasmus MC, University Medical Center, Rotterdam, The Netherlands
,
J. C. Ionita
6   Large Animal Clinic for Surgery, Faculty of Veterinary Medicine, University of Leipzig, Leipzig, Germany
,
M. Estrada
2   Large Animal Hospital, School of Veterinary Medicine, National University, Heredia, Costa Rica
,
C. J. Lischer
1   Equine Clinic, School of Veterinary Medicine, Free University of Berlin, Berlin, Germany
› Author Affiliations
Further Information

Publication History

Received: 13 November 2013

Accepted: 07 July 2014

Publication Date:
22 December 2017 (online)

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Summary

Objective: Even though equine multi-limb tendinopathy models have been reported, it is unknown if fore- and hindlimb tendon healing behave similarly. The aim of this study was to compare the healing process of surgically induced superficial digital flexor tendon (SDFT) core lesions of fore- and hindlimbs in horses.

Methods: Tendon core lesions were surgically induced in the SDFT of both fore- and hindlimbs in eight horses. One randomly assigned forelimb and one randomly assigned hindlimb were injected with saline one and two weeks post-surgery. The healing process was monitored clinically and ultrasonographically. After 24 weeks, the tendons were harvested and biochemical, biomechanical and histological parameters were evaluated.

Results: Twenty-four weeks post-surgery, the forelimb SDFT lesions had a significantly higher colour Doppler ultrasound vascularization score (p = 0.02) and glycosaminoglycan concentration (p = 0.04) and a significantly lower hydroxylysylpyridinoline content (p = 0.03).

Clinical relevance: Our results indicate that fore- and hindlimb SDFT surgically induced lesions exhibit significant differences in several important parameters of tendon healing 24 weeks post-surgery. These differences create significant challenges in using all four limbs and accurately interpreting the results that one might generate. Therefore these findings do not support the use of four-limb models for study of tendon injury until the reasons for these differences are much better understood.

Keywords

Horse - superficial digital flexor tendon - tendinopathy - model - healing
 

  • References

  • 1 Murray RC, Dyson SJ, Tranquille C. et al Association of type of sport and performance level with anatomical site of orthopaedic injury diagnosis. Equine Vet J Suppl 2006; 36: 411-416.
    PubMedSearch in Google Scholar
  • 2 Ely ER, Avella CS, Price JS. et al Descriptive epidemiology of fracture, tendon and suspensory ligament injuries in National Hunt racehorses in training. Equine Vet J 2009; 41: 372-378.
    CrossrefPubMedSearch in Google Scholar
  • 3 Singer ER. et al Injuries in the event horse: training versus competition. Vet J 2008; 175: 76-81.
    CrossrefPubMedSearch in Google Scholar
  • 4 Kasashima Y, Takahashi T. et al Prevalence of superficial digital flexor tendonitis and suspensory desmitis in Japanese Thoroughbred flat racehorses in 1999. Equine Vet J 2004; 36: 346-350.
    PubMedSearch in Google Scholar
  • 5 Back W, Schamhardt HC, Hartman W. et al Kinematic differences between the distal portions of the forelimbs and hind limbs of horses at the trot. Am J Vet Res 1995; 56: 1522-1528.
    PubMedSearch in Google Scholar
  • 6 Merkens HW, Schamhardt HC. et al Ground reaction force patterns of Dutch Warmbloods at the canter. Am J Vet Res 1993; 54: 670-674.
    PubMedSearch in Google Scholar
  • 7 Merkens HW, Schamhardt HC. Evaluation of equine locomotion during different degrees of experimentally induced lameness. I: Lameness model and quantification of ground reaction force patterns of the limbs. Equine Vet J Suppl 1988; 6: 99-106.
    PubMedSearch in Google Scholar
  • 8 Merkens HW, Schamhardt HC. Evaluation of equine locomotion during different degrees of experimentally induced lameness. II: Distribution of ground reaction force patterns of the concurrently loaded limbs. Equine Vet J Suppl 1988; 6: 107-112.
    PubMedSearch in Google Scholar
  • 9 David F. et al Short-term cast immobilisation is effective in reducing lesion propagation in a surgical model of equine superficial digital flexor tendon injury. Equine Vet J 2012; 44: 570-575.
    CrossrefPubMedSearch in Google Scholar
  • 10 Cadby JA, David F. et al Further characterisation of an experimental model of tendinopathy in the horse. Equine Vet J 2013; 45: 642-648.
    CrossrefPubMedSearch in Google Scholar
  • 11 Schramme M, Hunter S. et al A surgical tendonitis model in horses: technique, clinical, ultrasonographic and histological characterisation. Vet Comp Orthop Traumatol 2010; 23: 231-239.
    Thieme ConnectPubMedSearch in Google Scholar
  • 12 Watkins JP, Auer JA, Gay S. et al Healing of surgically created defects in the equine superficial digital flexor tendon: collagen-type transformation and tissue morphologic reorganization. Am J Vet Res 1985; 46: 2091-2096.
    PubMedSearch in Google Scholar
  • 13 Williams IF, McCullagh KG. et al Studies on the pathogenesis of equine tendonitis following collagenase injury. Res Vet Sci 1984; 36: 326-338.
    PubMedSearch in Google Scholar
  • 14 Bosch G, van Schie HT. et al Effects of plateletrich plasma on the quality of repair of mechanically induced core lesions in equine superficial digital flexor tendons: A placebo-controlled experimental study. J Orthop Res 2010; 28: 211-217.
    PubMedSearch in Google Scholar
  • 15 Dahlgren LA. et al Insulin-like growth factor-I improves cellular and molecular aspects of healing in a collagenase-induced model of flexor tendinitis. J Orthop Res 2002; 20: 910-919.
    CrossrefPubMedSearch in Google Scholar
  • 16 Keg PR, Barneveld A, Schamhardt HC. et al Clinical and force plate evaluation of the effect of a high plantar nerve block in lameness caused by induced mid-metatarsal tendinitis. Vet Q. 1994; 2: 70-75.
    PubMedSearch in Google Scholar
  • 17 Crovace A, Lacitignola L. et al Histological and immunohistochemical evaluation of autologous cultured bone marrow mesenchymal stem cells and bone marrow mononucleated cells in collagenase-induced tendinitis of equine superficial digital flexor tendon. Vet Med Int 2010 2010; 250978.
    PubMedSearch in Google Scholar
  • 18 Estrada RJ, Van Weeren PR, Van de Lest CHA. et al Effects of leukocyte-reduced platelet concentrate on the repair of surgically induced core lesions in equine superficial digital flexor tendon. BMC Vet Res 2014 Submitted for Publication
    PubMedSearch in Google Scholar
  • 19 American Association of Equine Practitioners. Definition and classification of lameness. In: Guide for Veterinary Service and Judging of Equestrian Events. Lexington, KY, USA; American Association of Equine Practitioners, 1991
    PubMed
  • 20 Rantanen NW, Jorgensen JS, Genovese RL. Ultrasonographic Evaluation of the Equine Limb: Technique. In Dyson S Ross. editors Diagnosis and Management of Lameness in the Horse. Vol 2. Missouri: Elsevier Saunders; 2011: 183-205.
    Search in Google Scholar
  • 21 Bosch G. et al The effect of plateletrich plasma on the neovascularization of surgically created equine superficial digital flexor tendon lesions. Scand J Med Sci Sports 2011; 21: 554-561.
    CrossrefPubMedSearch in Google Scholar
  • 22 Farndale RW, Sayers CA, Barrett AJ. A direct spectrophotometric microassay for sulphated glycosaminoglycans in cartilage cultures. Connect Tissue Res 1982; 9: 247-248.
    CrossrefPubMedSearch in Google Scholar
  • 23 Kim YJ, Sah RL, Doong JY. et al Fluorometric assay of DNA in cartilage explants using Hoechst 33258. Anal Biochem 1988; 174: 168-176.
    CrossrefPubMedSearch in Google Scholar
  • 24 Lin YL, Brama PA, Kiers GH. et al Functional adaptation through changes in regional biochemical characteristics during maturation of equine superficial digital flexor tendons. Am J Vet Res 2005; 66: 1623-1629.
    CrossrefPubMedSearch in Google Scholar
  • 25 Reddy GK, Enwemeka CS. A simplified method for the analysis of hydroxyproline in biological tissues. Clin Biochem 1996; 29: 225-229.
    CrossrefPubMedSearch in Google Scholar
  • 26 Thorpe CT, Stark RJ, Goodship AE. et al Mechanical properties of the equine superficial digital flexor tendon relate to specific collagen cross-link levels. Equine Vet J Suppl 2010; 38: 538-543.
    PubMedSearch in Google Scholar
  • 27 Jensen EC. Quantitative analysis of histological staining and fluorescence using ImageJ. Anat Rec (Hoboken) 2013; 296: 378-381.
    CrossrefPubMedSearch in Google Scholar
  • 28 Silver IA. et al A clinical and experimental study of tendon injury, healing and treatment in the horse. Equine Vet J Suppl 1983; 1: 1-43.
    PubMedSearch in Google Scholar
  • 29 Tsuzaki M, Yamauchi M, Banes AJ. Tendon collagens: extracellular matrix composition in shear stress and tensile components of flexor tendons. Connect Tissue Res 1993; 29: 141-152.
    CrossrefPubMedSearch in Google Scholar
  • 30 Parry DA. The molecular and fibrillar structure of collagen and its relationship to the mechanical properties of connective tissue. Biophys Chem 1988; 29: 195-209.
    CrossrefPubMedSearch in Google Scholar
  • 31 Eyre DR, Koob TJ, Van Ness KP. Quantitation of hydroxypyridinium crosslinks in collagen by high-performance liquid chromatography. Anal Biochem 1984; 137: 380-388.
    CrossrefPubMedSearch in Google Scholar
  • 32 Williams IF, Heaton A, McCullagh KG. Cell morphology and collagen types in equine tendon scar. Res Vet Sci 1980; 28: 302-310.
    PubMedSearch in Google Scholar
  • 33 Bank RA, Te Koppele JM, Oostingh G. et al Lysylhydroxylation and non-reducible cross-linking of human supraspinatus tendon collagen: changes with age and in chronic rotator cuff tendinitis. Ann Rheum Dis 1999; 58: 35-41.
    CrossrefPubMedSearch in Google Scholar
  • 34 Birch HL, Bailey AJ. et al Macroscopic ‘degeneration' of equine superficial digital flexor tendon is accompanied by a change in extracellular matrix composition. Equine Vet J 1998; 30: 534-539.
    CrossrefPubMedSearch in Google Scholar
  • 35 Esko JD. Proteoglycans and Glycosaminoglycans. In Varki A, Cummings R, Esko JD. editors Essentials of Glycobiology [eBook]. Vol 2. New York: Cold Spring Harbor Laboratory Press; 1999. Available from http://www.ncbi.nlm.nih.gov/books/NBK20693/
    Search in Google Scholar
  • 36 Cribb AM, Scott JE. Tendon response to tensile stress: an ultrastructural investigation of collagen: proteoglycan interactions in stressed tendon. J Anat 1995; 187: 423-428.
    PubMedSearch in Google Scholar
  • 37 Parkinson J, Samiric T, Ilic MZ. et al Involvement of Proteoglycans in Tendinopathy. J Musculoskelet Neuronal Interact 2011; 11: 86-93.
    PubMedSearch in Google Scholar
  • 38 Parkinson J, Samiric T, Ilic MZ. et al Change in Proteoglycan Metabolism Is a Characteristic of Human Patellar Tendinopathy. Arthritis Rheum 2010; 62: 3028-3035.
    CrossrefPubMedSearch in Google Scholar
  • 39 Halper J, Kim B, Khan A. et al Degenerative suspensory ligament desmitis as a systemic disorder characterized by proteoglycan accumulation. BMC Vet Res 2006; 2: 12.
    CrossrefPubMedSearch in Google Scholar
  • 40 Yang X, Coleman DP, Pugh ND. et al The volume of the neovascularity and its clinical implications in achilles tendinopathy. Ultrasound Med Biol 2012; 38: 1887-1895.
    CrossrefPubMedSearch in Google Scholar
  • 41 Kristoffersen M, Ohberg L, Johnston C. et al Neovascularisation in chronic tendon injuries detected with colour Doppler ultrasound in horse and man: implications for research and treatment. Knee Surg Sports Traumatol Arthrosc 2005; 13: 505-508.
    CrossrefPubMedSearch in Google Scholar
  • 42 Murata D, Misumi K, Fujiki M. A preliminary study of diagnostic color Doppler ultrasonography in equine superficial digital flexor tendonitis. J Vet Med Sci 2012; 74: 1639-1642.
    CrossrefPubMedSearch in Google Scholar