Document Type : Original Article
Authors
- Mohammad Hazhir Alaei 1
- Rahim Mohammadi 1
- Seyed Mohammad Hashemi-Asl 1
- Siamak Asri-Rezaei 2
- Mehdi Behfar 1
- Ali Asghar Tehrani 3
1 Department of Surgery and Diagnostic Imaging, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran.
2 Department of Internal Medicine and Clinical Pathology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran.
3 Department of Pathobiology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran.
Abstract
Injuries to tendons are among the most common injuries in competition horses and represent a significant cause of morbidity and mortality. The present study aimed at an eight -week period ultrasonographic and biomechanical assessments of collagenase induced tendinitis in forelimb superficial digital flexor tendon (SDFT) in donkeys. Four healthy male donkeys were used. 1000 U collagenase type I from Clostridium histolyticum was injected in the center of the SDFT guided by ultrasonography. Ultrasonographical images of the SDFT were recorded prior to injury and 8 weeks after confirmation of tendinitis on a weekly basis. Images were digitized and lesion area to cross-sectional tendon area ratio (LA/TA ratios) was measured. At the end of the study period, the animals underwent tenectomy and tendon samples were evaluated biomechanically. Collagenase induced tendinitis was confirmed ultrasonographically 10 days post-injection. The animals showed swelling and response to palpation, however, no lameness was found in animals within the study period. There were significant differences between the first and the fifth weeks in operated limbs ultrasonographically (p < 0.05). The eight-week period is sufficient to assess the effect of various modalities in tendon healing in the collagenase-induced model in the donkey. The development and expansion of collagenase induced tendinitis until week six after confirmation of tendinitis may disturb findings of the healing effect of various modalities in the tendon, in which tendinitis is still expanding and may mask the healing effect of the modalities used.
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Main Subjects
- Williams RB, Harkins LS, Hammond CJ, Wood JL. Racehorse injuries, clinical problems and fatalities recorded on British racecourses from flat racing and National Hunt racing during 1996, 1997 and 1998. Equine Veterinary Journal, 2001; 33: 478-486.
- Ely ER, Avella CS, Price JS, Smith RK, Wood JL, Verheyen KL. Descriptive epidemiology of fracture, tendon and suspensory ligament injuries in National Hunt racehorses in training. Equine Veterinary Journal, 2009; 41: 372-378.
- Dyson SJ. Treatment of superficial digital flexor tendinitis: a comparison of conservative management, sodium hyaluronate, and glycosaminoglycan polysulfate, in Proceedings. 43rd American Association of Equine Practitioners, 1997; 43: 297–300.
- Dyson SJ. Medical management of superficial digital flexor tendonitis: a comparative study in 219 horses (1992–2000). Equine Veterinary Journal, 2004; 36: 415–419.
- Stanley RL, Goodship AE, Edwards B, Firth EC, Patterson-Kane JC. Effects of exercise on tenocyte cellularity and tenocyte nuclear morphology in immature and mature equine digital tendons. Equine Veterinary Journal, 2008; 40: 141-146
- Stromberg B. Morphologic, thermographic and 133Xe clearance studies on normal and diseased superficial digital flexor tendons in race horses. Equine Veterinary Journal, 1973; 5: 156-161.
- El-Shafaey EA, Karrouf GI, Zaghloul AE. Clinical and biomechanical evaluation of three bioscaffold augmentation devices used for superficial digital flexor tenorrhaphy indonkeys (Equus asinus): an experimental study. Journal of Advanced Research, 2013; 4: 103–113.
- Geburek F, Roggel F, van Schie HTM, Beineke A, Estrada R, Weber K. Effect of single intralesional treatment of surgically induced equine superficial digital flexor tendon core lesions with adipose-derived mesenchymal stromal cells: A controlled experimental trial. Stem Cell Research and Thereputics, 2017; 8: 129.
- Bertone AL, Stashak TS, Smith FW, Norrdin RW. A comparison of repair methods for gap healing in equine flexor tendon. Veterinary Surgery, 1990; 19: 254-265.
- Nixon AJ, Dahlgren LA, Haupt JL, Yeager AE, Ward DL. Effect of adipose-derived nucleated cell fractions on tendon repair in horses with collagenase induced tendinitis. American Journal of Veterinary Research, 2008; 69(7): 928-937.
- Hast MW, Zuskov A, Soslowsky LJ. The role of animal models in tendon research. Bone and Joint Research, 2014; 3: 193-202.
- Crass JR, Genovese RL, Render JA, Bellon EM. Magnetic resonance, ultrasound and histopathologic correlation of acute and healing equine tendon injuries. Veterinary Radiology and Ultrasound, 2005; 33(4): 206-216.
- Schie HV, Bakker EM, Jonker AM, Weeren PRV. Efficacy of computerized discrimination between structure-related and non-structure-related echoes in ultrasonographic images for the quantitative evaluation of the structural integrity of superficial digital flexor tendons in horses. American Journal of Veterinary Research, 2001; 62(7): 1159-1166.
- Smith R, Schramme M. Tendon injury in the horse: Current theories and therapies. In Practice, 2003; 529-539.
- Alzola Domingo R, Riggs CM, Gardner DS, Freeman SL. Ultrasonographic scoring system for superficial digital flexor tendon injuries in horses: intra- and inter-rater variability. Veterinary Record, 2017; 181: 655.
- De Lacerda Neto JC, De Freitas JMR, Poggiani FM, Dias DPM, Gravena K, Bernadi NS, Ribeiro G, Palmeira-Borges V. Serial superficial digital flexor tendon biopsies for diagnosing and monitoring collagenase-induced tendonitis in horses. Pesquisa Veterinária Brasileira, 2013; 33: 710-718.
- Thorpe CT, Stark RJ, Goodship AE, Birch HL. Mechanical properties of the equine superficial digital flexor tendon relate to specific collagen cross-link levels. Equine Veterinary Journal, 2010; 38: 538-543.
- Johnson S, Symons J. Measuring volumetric changes of equine distal limbs: A pilot study examining jumping exercise. Animals (Basel), 2019; 9: 751.
- Reis A, Baccarin R. The cross-sectional area of the superficial digital flexor tendon of trained and untrained Thoroughbred racehorses. Ciência Rural, 2010; 40: 1786-1790.
- James R, Kesturu G, Balian G, Chhabra B. Tendon: Biology, biomechanics, repair, growth factors, and evolving treatment options. Journal of Hand Surgery, 2008; 33A: 102–112.
- Asahara H, Inui M, Lotz MK. Tendons and ligaments: Connecting developmental biology to musculoskeletal disease pathogenesis. Journal of Bone and Mineral Research, 2017; 32: 1773‐1782.
- Oakes BW, Singleton C, Haut RC. Correlation of collagen fibril morphology and tensile modulus in the repairing and normal rabbit patella tendon. Transactions of the Orthopedic Research Society, 1998; 23: 24.
- Sensini A, Cristofolini L. Biofabrication of electrospun scaffolds for the regeneration of tendons and ligaments. Materials (Basel), 2018; 11: 1963.
- Zitnay JL, Weiss JA. Load transfer, damage, and failure in ligaments and tendons. Journal of Orthopedic Research, 2018; 36: 3093‐3104.
- Cadby JA, David F, Van De Lest C, Bosch G, Van Weeren PR, Snedeker JG, van Schie HTM. Further characterisation of an experimental model of tendinopathy in the horse. Equine Veterinary Journal, 2013; 45: 642-648.
- De Cesar Netto C, Godoy-Santos AL, Augusto Pontin P, Natalino RJM, Pereira CAM, Lima FDO, da Fonseca LF, Staggers JR, Cavinatto LM, Schon LC, de Camargo OP, Fernandes TD. Novel animal model for Achilles tendinopathy: Controlled experimental study of serial injections of collagenase in rabbits. PLoS One, 2018; 13: e0192769.
- Ueda Y, Inui A, Mifune Y, Takase F, Kataoka T, Kurosawa T, Yamaura K, Kokubu T, Kuroda R. Molecular changes to tendons after collagenase-induced acute tendon injury in a senescence-accelerated mouse model. BMC Musculoskeletal Disorders, 2019; 20: 120.
- Petermann U. Treatment of 29 case of acute and chronic equine tendonitis with local laser therapy and laser acupuncture. American Journal of Traditional Chinese Veterinary Medicine, 2016; 11: 43-51.
- Jean-François K, Antoine S, Jean-Michel C. Hyaluronic acid and tendon lesions. Muscle, Ligaments and Tendons Journal, 2015; 5: 264–269.
- Maffulli N, Longo UG, Loppini M, Spiezia F, Denaro V. New options in the management of tendinopathy. Open Access Journal of Sports Medicine, 2010; 1: 29-37.
- Oloumi MM, Vosough D, Derakhshanfar A, Nematollahi MH. The healing potential of Plantago lanceolata ointment on collagenase-induced tendinitis in burros (Equus asinus). Journal of Equine Veterinary Science, 2011; 31: 470-474.
- Bazzano M, Piccione G, Giannetto C, Tosto F, Di Pietro S, Giudice E. PRP intralesional injection as bedside therapy for tendinitis in athletic horse. Acta Scientiae Veterinariae, 2013; 41(1): 1-7.
- Whitcomb MB. Ultrasonographic evaluation of the metacarpus, metatarsus, and pastern. Clinical Techniques in Equine Practice, 2004; 3: 238-255.
- Kasashima Y, Takahashi T, Smith RK, Goodship AE, Kuwano A, Ueno T, Hirano S. Prevalence of superficial digital flexor tendonitis and suspensory desmitis in Japanese Thoroughbred flat racehorses in 1999. Equine Veterinary Journal, 2004; 36, 346-350.
- Ely ER, Verheyen KL, Wood JL. Fractures and tendon injuries in National Hunt horses in training in the UK: A pilot study. Equine Veterinary Journal, 2004; 36: 365-367.
- Lam KH, Parkin TD, Riggs CM, Morgan KL. Descriptive analysis of retirement of Thoroughbred racehorses due to tendon injuries at the Hong Kong Jockey Club (1992-2004). Equine Veterinary Journal, 2007; 39: 143-148.
- Alexander RM. Energy-saving mechanisms in walking and running. Journal of Experimental Biology, 1991; 160: 55-69.
- Birch HL. Tendon matrix composition and turnover in relation to functional requirements. International Journal of Experimental Pathology, 2007; 88: 241-248.
- Batson EL, Paramour RJ, Smith TJ, Birch HL, Patterson-Kane JC, Goodship AE. Are the material properties and matrix composition of equine flexor and extensor tendons determined by their functions? Equine Veterinary Journal, 2003; 35: 314-318.
- Dowling BA, Dart AJ, Hodgson DR, Rose RJ, Walsh WR. Recombinant equine growth hormone does not affect the in vitro biomechanical properties of equine superficial digital flexor tendon. Veterinary Surgery, 2002; 31: 325-330.
- Gerard MP, Hodgson DR, Rose RJ, Walsh WR. Effects of recombinant equine growth hormone on in vitro biomechanical properties of the superficial digital flexor tendon of Standardbred yearlings in training. Veterinary Surgery, 2005; 34: 253-259.
- Behfar M, Sarrafzadeh-Rezaei F, Hobbenaghi R, Delirezh N, Dalir-Naghadeh B. Enhanced mechanical properties of rabbit flexor tendons in response to intratendinous injection of adipose derived stromal vascular fraction. Curr Stem Cell Research and Therapy, 2012; 7: 173-178.
- Sleutjens J, Serra Bragança FM, van Empelen MW, Ten Have RE, de Zwaan J, Roelfsema E, Oosterlinck M, Back W. Mouldable, thermoplastic, glue-on frog-supportive shoes change hoof kinetics in normal and obese Shetland ponies. Equine Veterinary Journal, 2018; 50: 684‐689.
- Sharifi D, Kazemi D, Latifi H. Evaluation of tensile strength of the superficial flexor tendon in horses subjected to transcutaneous electrical neural stimulation therapeutic regimen. American Journal of Applied Sciences, 2009; 5: 703–706.
- Takahashi T, Mukai K, Ohmura H, Aida H, Hiraga A. In vivo measurements of flexor tendon and suspensory ligament forces during trotting using the thoroughbred forelimb model. Journal of Equine Science, 2014; 25: 15‐22.
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