Animal models for the study of tendinopathy

British Journal of Sports Medicine

Volumn 41, Issue 4, 2007, Pages 232-240

  Warden, S J ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLINICAL FEATURE; EX VIVO STUDY; FLEXOR TENDON; HISTOPATHOLOGY; HUMAN; IN VIVO STUDY; MEDICAL RESEARCH; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATELLA TENDON; PATHOGENESIS; REVIEW; RISK FACTOR; SPECIES COMPARISON; TENDINITIS; TISSUE CHARACTERIZATION; TISSUE DIFFERENTIATION; TREADMILL EXERCISE; ACHILLES TENDON; ANIMAL; ANIMAL MODEL; MOUSE; PATELLA; PATHOLOGY; RABBIT; RAT;

ACHILLES TENDON; ANIMALS; HUMANS; MAGNETIC RESONANCE IMAGING; MICE; MODELS, ANIMAL; PATELLA; RABBITS; RATS; RISK FACTORS; TENDINOPATHY;

EID: 34250617042     PISSN: 03063674     EISSN: None     Source Type: Journal    
DOI: 10.1136/bjsm.2006.032342     Document Type: Review

References (101)

1. Lian ØB, Engebretsen L, Bahr R. Prevalence of jumper's knee among elite athletes from different sports: a cross-sectional study. Am J Sports Med 2005;33:561-7.
2. Khan KM, Cook JL, Bonar F, et al. Histopathology of common tendinopathies: update and implications for clinical management. Sports Med 1999;27:393-408.
3. Khan KM, Bonar F, Desmond PM, et al. Patellar tendinosis (jumper's knee): findings at histopathologic examination, US, and MR imaging. Victorian Institute of Sport Tendon Study Group. Radiology 1996;200:821-7.
4. Movin T, Gad A, Reinholt FP, et al. Tendon pathology in long-standing achillodynia. Biopsy findings in 40 patients. Acta Orthop Scand 1997;68:170-5.
5. Riley GP, Goddard MJ, Hazleman BL. Histopathological assessment and pathological significance of matrix degeneration in supraspinatus tendons. Rheumatology 2001;40:229-30.
6. Cook JL, Khan KM. What is the most appropriate treatment for patellar tendinopathy? Br J Sports Med 2001;35:291-4.
7. Anonymous. The importance of animals in biomedical and behavioral research (a statement from the Public Health Service). Physiologist 1994;37:107.
8. Movin T, Guntner P, Gad A, et al. Ultrasonography-guided percutaneous core biopsy in Achilles tendon disorder. Scand J Med Sci Sports 1997;7:244-8.
9. Kannus P, Jozsa L. Histopathological changes preceding spontaneous rupture of a tendon. A controlled study of 891 patients. J Bone Joint Surg [Am] 1991;73:1507-25.
10. Alfredson H, Forsgren S, Thorsen K, et al. In vivo microdialysis and immunohistochemical analyses of tendon tissue demonstrated high amounts of free glutamate and glutamate NMDAR1 receptors, but no signs of inflammation, in Jumper's knee. J Orthop Res 2001;19:881-6.
11. Dalton S, Cawston TE, Riley GP, et al. Human shoulder tendon biopsy samples in organ culture produce procollagenase and tissue inhibitor of metalloproteinases. Ann Rheum Dis 1995;54:571-7.
12. Manske PR, Lesker PA, Gelberman RH, et al. Intrinsic restoration of the flexor tendon surface in the nonhuman primate. J Hand Surg [Am] 1985;10:632-7.
13. Singer DI, Morrison WA, Gumley GJ, et al. Comparative study of vascularized and nonvascularized tendon grafts for reconstruction of flexor tendons in zone 2: an experimental study in primates. J Hand Surg [Am] 1989;14:55-63.
14. Dahlgren LA, van der Meulen MC, Bertram JE, 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;20:910-9.
15. Williams IF, McCullagh KG, Goodship AE, et al. Studies on the pathogenesis of equine tendonitis following collagenase injury. Res Vet Sci 1984;36:326-38.
16. Fealy S, Rodeo SA, MacGillivray JD, et al. Biomechanical evaluation of the relation between number of suture anchors and strength of the bone-tendon interface in a goat rotator cuff model. Arthroscopy 2006;22:595-602.
17. Cohen MS, Turner TM, Urban RM. Effects of implant material and plate design on tendon function and morphology. Clin Orthop 2006;445:81-90.
18. Shakibaei M, de Souza P, van Sickle D, et al. Biochemical changes in Achilles tendon from juvenile dogs after treatment with ciprofloxacin or feeding a magnesium-deficient diet. Arch Toxicol 2001;75:369- 74.
19. Juncosa-Melvin N, Boivin GP, Gooch C, et al. The effect of autologous mesenchymal stem cells on the biomechanics and histology of gel-collagen sponge constructs used for rabbit patellar tendon repair. Tissue Eng 2006;12:369-79.
20. Kobayashi M, Itoi E, Minagawa H, et al. Expression of growth factors in the early phase of supraspinatus tendon healing in rabbits. J Shoulder Elbow Surg 2006;15:371-7.
21. Soslowsky LJ, Carpenter JE, DeBano CM, et al. Development and use of an animal model for investigations on rotator cuff disease. J Shoulder Elbow Surg 1996;5:383-92.
22. Soslowsky LJ, Thomopoulos S, Esmail A, et al. Rotator cuff tendinosis in an animal model: role of extrinsic and overuse factors. Ann Biomed Eng 2002;30:1057-63.
23. Palmes D, Spiegel HU, Schneider TO, et al. Achilles tendon healing: long-term biomechanical effects of postoperative mobilization and immobilization in a new mouse model. J Orthop Res 2002;20:939-46.
24. Zantop T, Gilbert TW, Yoder MC, et al. Extracellular matrix scaffolds are repopulated by bone marrow-derived cells in a mouse model of Achilles tendon reconstruction. J Orthop Res 2006;24:1299-309.
25. Fransson BA, Gavin PR, Lahmers KK. Supraspinatus tendinosis associated with biceps brachii tendon displacement in a dog. J Am Vet Med Assoc. 2005;227:1429-33, 1416.
26. Kasashima Y, Takahashi T, Smith RK, et al. Prevalence of superficial digital flexor tendonitis and suspensory desmitis in Japanese Thoroughbred flat racehorses in 1999. Equine Vet J 2004;36:346-50.
27. Fox RR. The rabbit as a research subject. Physiologist 1984;27:393-402.
28. Lander ES, Linton LM, Birren B, et al. Initial sequencing and analysis of the human genome. Nature 2001;409:860-921.
29. Venter JC, Adams MD, Myers EW, et al. The sequence of the human genome. Science 2001;291:1304-51.
30. Waterston RH, Lindblad-Toh K, Birney E, et al. Initial sequencing and comparative analysis of the mouse genome. Nature 2002;420:520-62.
31. Gibbs RA, Weinstock GM, Metzker ML, et al. Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 2004;428:493-521.
32. Abbott A. Laboratory animals: the Renaissance rat. Nature 2004;428:464-6.
33. Lin TW, Cardenas L, Glaser DL, et al. Tendon healing in interleukin-4 and interleukin-6 knockout mice. J Biomech 2006;39:61-9.
34. Mikic B, Bierwert L, Tsou D. Achilles tendon characterization in GDF-7 deficient mice. J Orthop Res 2006;24:831-41.
35. Perez AV, Perrine M, Brainard N, et al. Scleraxis (Scx) directs lacZ expression in tendon of transgenic mice. Mech Dev 2003;120:1153-63.
36. Robinson PS, Lin TW, Reynolds PR, et al. Strain-rate sensitive mechanical properties of tendon fascicles from mice with genetically engineered alterations in collagen and decorin. J Biomech Eng 2004;126:252-7.
37. Xia W, Wang Y, Appleyard RC, et al. Spontaneous recovery of injured Achilles tendon in inducible nitric oxide synthase gene knockout mice. Inflamm Res 2006;55:40-5.
38. Lee H, Wang VM, Laudier DM, et al. A novel in vivo model of tendon fatigue damage accumulation. Trans Orthop Res Soc 2006;31:1058.
39. Fu SC, Wang W, Pau HM, et al. Increased expression of transforming growth factor-beta1 in patellar tendinosis. Clin Orthop 2002:174-83.
40. Maffulli N, Testa V, Capasso G, et al. Similar histopathological picture in males with Achilles and patellar tendinopathy. Med Sci Sports Exerc 2004;36:1470-5.
41. Yu JS, Popp JE, Kaeding CC, et al. Correlation of MR imaging and pathologic findings in athletes undergoing surgery for chronic patellar tendinitis. AJR Am J Roentgenol 1995;165:115-8.
42. Rees JD, Wilson AM, Wolman RL. Current concepts in the management of tendon disorders. Rheumatology 2006;45:508-21.
43. Rolf CG, Fu BS, Pau A, et al. Increased cell proliferation and associated expression of PDGFRbeta causing hypercellularity in patellar tendinosis. Rheumatology 2001;40:256-61.
44. Popp JE, Yu JS, Kaeding CC. Recalcitrant patellar tendinitis. Magnetic resonance imaging, histologic evaluation, and surgical treatment. Am J Sports Med 1997;25:218-22.
45. Griffiths GP, Selesnick FH. Operative treatment and arthroscopic findings in chronic patellar tendinitis. Arthroscopy 1998;14:836- 9.
46. Kraushaar BS, Nirschl RP. Tendinosis of the elbow (tennis elbow). Clinical features and findings of histological, immunohistochemical, and electron microscopy studies. J Bone Joint Surg [Am] 1999;81:259- 78.
47. Cook JL, Feller JA, Bonar SF, et al. Abnormal tenocyte morphology is more prevalent than collagen disruption in asymptomatic athletes' patellar tendons. J Orthop Res 2004;22:334-8.
48. Matthews TJ, Hand GC, Rees JL, et al. Pathology of the torn rotator cuff tendon. Reduction in potential for repair as tear size increases. J Bone Joint Surg [Br] 2006;88:489-95.
49. Rosenberg JM, Whitaker JH. Bilateral infrapatellar tendon rupture in a patient with jumper's knee. Am J Sports Med 1991;19:94-5.
50. Cetti R, Junge J, Vyberg M. Spontaneous rupture of the Achilles tendon is preceded by widespread and bilateral tendon damage and ipsilateral inflammation: a clinical and histopathologic study of 60 patients. Acta Orthop Scand 2003;74:78-84.
51. Maffulli N, Barrass V, Ewen SW. Light microscopic histology of Achilles tendon ruptures. A comparison with unruptured tendons. Am J Sports Med 2000;28:857-63.
52. Tallon C, Maffulli N, Ewen SW. Ruptured Achilles tendons are significantly more degenerated than tendinopathic tendons. Med Sci Sports Exerc 2001;33:1983-90.
53. Riley GP. Gene expression and matrix turnover in overused and damaged tendons. Scand J Med Sci Sports 2005;15:241-51.
54. Kettunen JA, Kujala UM, Kaprio J, et al. Health of master track and field athletes: a 16-year follow-up study. Clin J Sport Med 2006;16:142-8.
55. Stenlund B, Goldie I, Hagberg M, et al. Shoulder tendinitis and its relation to heavy manual work and exposure to vibration. Scand J Work Environ Health 1993;19:43-9.
56. Cook JL, Kiss ZS, Khan KM, et al. Anthropometry, physical performance, and ultrasound patellar tendon abnormality in elite junior basketball players: a cross-sectional study. Br J Sports Med 2004;38:206-9.
57. Mahieu NN, Witvrouw E, Stevens V, et al. Intrinsic risk factors for the development of Achilles tendon overuse injury: a prospective study. Am J Sports Med 2006;34:226-35.
58. Mokone GG, Schwellnus MP, Nookes TD, et al. The COL5A1 gene and Achilles tendon pathology. Scand J Med Sci Sports 2006;16:19-26.
59. Witvrouw E, Bellemans J, Lysens R, et al. Intrinsic risk factors for the development of patellar tendinitis in an athletic population. A two-year prospective study. Am J Sports Med 2001;29:190-5.
60. Reeves ND. Adaptation of the tendon to mechanical usage. J Musculoskelet Neuronal Interact 2006;6:174-80.
61. Frost HM. Skeletal structural adaptations to mechanical usage (SATMU): 4. Mechanical influences on intact fibrous tissues. Anat Rec 1990;226:433-9.
62. Mackley JR, Ando J, Herzyk P, et al. Phenotypic responses to mechanical stress in fibroblasts from tendon, cornea and skin. Biochem J 2006;396:307-16.
63. Scott A, Khan KM, Heer J, et al. High strain mechanical loading rapidly induces tendon apoptosis: an ex vivo rat tibialis anterior model. Br J Sports Med 2005;39:e25.
64. Li Z, Yang G, Khan M, et al. Inflammatory response of human tendon fibroblasts to cyclic mechanical stretching. Am J Sports Med 2004;32:435-40.
65. Wang JH, Li Z, Yang G, et al. Repetitively stretched tendon fibroblasts produce inflammatory mediators. Clin Orthop 2004:243-50.
66. Cilli F, Khan M, Fu F, et al. Prostaglandin E2 affects proliferation and collagen synthesis by human patellar tendon fibroblasts. Clin J Sport Med 2004;14:232-6.
67. Yuan J, Murrell GA, Trickett A, et al. Overexpression of antioxidant enzyme peroxiredoxin 5 protects human tendon cells against apoptosis and loss of cellular function during oxidative stress. Biochim Biophys Acta 2004;1693:37-45.
68. Archambault JM, Elfervig-Wall MK, Tsuzaki M, et al. Rabbit tendon cells produce MMP-3 in response to fluid flow without significant calcium transients. J Biomech 2002;35:303-9.
69. Huang TF, Perry SM, Soslowsky LJ. The effect of overuse activity on Achilles tendon in an animal model: a biomechanical study. Ann Biomed Eng 2004;32:336-41.
70. Archambault JM, Hart DA, Herzog W. Response of rabbit Achilles tendon to chronic repetitive loading. Connect Tissue Res 2001;42:13-23.
71. Backman C, Boquist L, Friden J, et al. Chronic Achilles paratenonitis with tendinosis: an experimental model in the rabbit. J Orthop Res 1990;8:541-7.
72. Messner K, Wei Y, Andersson B, et al. Rat model of Achilles tendon disorder. A pilot study. Cells Tissues Organs 1999;165:30-9.
73. Nakama LH, King KB, Abrahamsson S, et al. Evidence of tendon microtears due to cyclical loading in an in vivo tendinopathy model. J Orthop Res 2005;23:1199-205.
74. Wisloff U, Helgerud J, Kemi OJ, et al. Intensity-controlled treadmill running in rats: VO(2 max) and cardiac hypertrophy. Am J Physiol Heart Circ Physiol 2001;280:H1301-10.
75. Russell JC, Epling WF, Pierce D, et al. Induction of voluntary prolonged running by rats. J Appl Physiol 1987;63:2549- 53.
76. Carlson KM, Wagner GC. Voluntary exercise and tail shock have differential effects on amphetamine-induced dopaminergic toxicity in adult BALB/c mice. Behav Pharmacol 2006;17:475-84.
77. Moraska A, Deak T, Spencer RL, et al. Treadmill running produces both positive and negative physiological adaptations in Sprague-Dawley rats. Am J Physiol Regul Integr Comp Physiol 2000;279:R1321-9.
78. Soslowsky LJ, Thomopoulos S, Tun S, et al. Overuse activity injures the supraspinatus tendon in an animal model: a histologic and biomechanical study. J Shoulder Elbow Surg 2000;9:79-84.
79. Marsolais D, Cote CH, Frenette J. Neutrophils and macrophages accumulate sequentially following Achilles tendon injury. J Orthop Res 2001;19:1203-9.
80. Hsu RW, Hsu WH, Tai CL, et al. Effect of shock-wave therapy on patellar tendinopathy in a rabbit model. J Orthop Res 2004;22:221-7.
81. Sullo A, Maffulli N, Capasso G, et al. The effects of prolonged peritendinous administration of PGE1 to the rat Achilles tendon: a possible animal model of chronic Achilles tendinopathy. J Orthop Sci 2001;6:349-57.
82. Khan MH, Li Z, Wang JH. Repeated exposure of tendon to prostaglandin-E2 leads to localized tendon degeneration. Clin J Sport Med 2005;15:27-33.
83. Tatari H, Kosay C, Baran O, et al. Deleterious effects of local corticosteroid injections on the Achilles tendon of rats. Arch Orthop Trauma Surg 2001;121:333-7.
84. Stone D, Green C, Rao U, et al. Cytokine-induced tendinitis: a preliminary study in rabbits. J Orthop Res 1999;17:168-77.
85. Fu SC, Chan BP, Wang W, et al. Increased expression of matrix metalloproteinase 1 (MMP1) in 11 patients with patellar tendinosis. Acta Orthop Scand 2002;73:658-62.
86. Wetzel BJ, Nindl G, Swez JA, et al. Quantitative characterization of rat tendinitis to evaluate the efficacy of therapeutic interventions. Biomed Sci Instrum 2002;38:157-62.
87. Carpenter JE, Flanagan CL, Thomopoulos S, et al. The effects of overuse combined with intrinsic or extrinsic alterations in an animal model of rotator cuff tendinosis. Am J Sports Med 1998;26:801-7.
88. Foster FS, Zhang MY, Zhou YQ, et al. A new ultrasound instrument for in vivo microimaging of mice. Ultrasound Med Biol 2002;28:1165-72.
89. Pautler RG. Mouse MRI: concepts and applications in physiology. Physiology 2004;19:168-75.
90. Wang Y-XJ, Bradley DP, Kuribayashi H, et al. Some aspects of rat femorotibial joint microanatomy as demonstrated by high-resolution magnetic resonance imaging. Lab Anim 2006;40(3):288-95.
91. Crevier-Denoix N, Ruel Y, Dardillat C, et al. Correlations between mean echogenicity and material properties of normal and diseased equine superficial digital flexor tendons: an in vitro segmental approach. J Biomech 2005;38:2212-20.
92. Wang VM, Banack TM, Tsai CW, et al. Variability in tendon and knee joint biomechanics among inbred mouse strains. J Orthop Res 2006;24:1200-7.
93. Provenzano PP, Vanderby R Jr. Collagen fibril morphology and organization: implications for force transmission in ligament and tendon. Matrix Biol 2006;25:71-84.
94. Doroski DM, Brink KS, Temenoff JS. Techniques for biological characterization of tissue-engineered tendon and ligament. Biomaterials 2007;28:187-202.
95. Molloy T, Kemp M, Wang Y, et al. Microarray analysis of the tendinopathic rat supraspinatus tendon: glutamate signalling and its potential role in tendon degeneration. J Appl Physiol 2006;101:1702-9.
96. Szomor ZL, Appleyard RC, Murrell GA. Overexpression of nitric oxide synthases in tendon overuse. J Orthop Res 2006;24:80-6.
97. Flatow EL, Wang VM, Rajan L, et al. How does tendon damage initiate? In: Woo SL-Y, Abramowitch SD, Miura K, eds. International Symposium on Ligaments and Tendons - V. Washington, DC, 2005:12.
98. Flatow EL, Nasser P, Lee L, et al. Overestimation of the degradation state in fatigue loaded tendon due to transient effects. Trans Orthop Res Soc 2002;27:621.
99. Wang VM, Laudier D, Tsai CW, et al. Imaging normal and damaged tendons: development and application of novel tissue processing techniques. Trans Orthop Res Soc 2005;30:321.
100. Nakama LH, King KB, Abrahamsson S, et al. VEGF, VEGFR-1, and CTGF cell densities in tendon are increased with cyclical loading: An in vivo tendinopathy model. J Orthop Res 2006;24:393-400.
101. Bebarta V, Luyten D, Heard K. Emergency medicine animal research: does use of randomization and blinding affect the results? Acad Emerg Med 2003;10:684-7.