Are animal models useful for studying human disc disorders/degeneration?

European Spine Journal

Volumn 17, Issue 1, 2008, Pages 2-19

  Alini, Mauro ^a   Eisenstein, Stephen M ^b   Ito, Keita ^a   Little, Christopher ^c   Kettler, A Annette ^d   Masuda, Koichi ^e   Melrose, James ^c   Ralphs, Jim ^f   Stokes, Ian ^g   Wilke, Hans Joachim ^d  

^a AO RESEARCH INSTITUTE   (Switzerland)

^b ROBERT JONES AND AGNES HUNT ORTHOPAEDIC HOSPITAL   (United Kingdom)

^c ROYAL NORTH SHORE HOSPITAL   (Australia)

^d UNIVERSITY OF ULM   (Germany)

^e RUSH MEDICAL COLLEGE   (United States)

^f CARDIFF UNIVERSITY   (United Kingdom)

^g UNIVERSITY OF VERMONT   (United States)

Author keywords

Animal models; In vitro; In vivo; Intervertebral disc degeneration

Indexed keywords

CHONDROITIN 6 SULFATE; GELATIN; HYALURONIC ACID; METALLOPROTEINASE;

AGING; AMINO ACID SEQUENCE; APOPTOSIS; BABOON; CALF (BOVINE); CELL CULTURE; CHICKEN; DISEASE COURSE; DNA MODIFICATION; DOG; ENZYME ACTIVITY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INNERVATION; INTERVERTEBRAL DISK DEGENERATION; INTERVERTEBRAL DISK HERNIA; LOW BACK PAIN; LUMBAR SPINE; NONHUMAN; NUCLEUS PULPOSUS; PATHOPHYSIOLOGY; PRACTICE GUIDELINE; PRIORITY JOURNAL; RABBIT; REVIEW; SHEEP; SPECIES DIFFERENCE; SPINAL CORD; SPINAL CORD NERVE CELL; SPINE STABILIZATION; SWINE; SYMPTOM; TREATMENT INDICATION;

AGE FACTORS; ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; INTERVERTEBRAL DISK; INTERVERTEBRAL DISK DISPLACEMENT; SPECIES SPECIFICITY; WEIGHT-BEARING;

EID: 38649097225     PISSN: 09406719     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00586-007-0414-y     Document Type: Review

References (161)

1. Adams MA, Roughley PJ (2006) What is intervertebral disc degeneration, and what causes it? Spine 31:2151-2161
2. Aguiar DJ, Johnson SL, Oegema TR (1999) Notochordal cells interact with nucleus pulposus cells: regulation of proteoglycan synthesis. Exp Cell Res 246:129-137
3. Anderson GD, Li X, Tannoury T, Beck G, Balian G (2003) A fibronectin fragment stimulates intervertebral disc degeneration in vivo. Spine 28:2338-2345
4. Ando T, Kato F, Mimatsu K, Iwata H (1995) Effects of chondroitinase ABC on degenerative intervertebral discs. Clin Orthop Relat Res 318:214-221
5. Ariga K, Miyamoto S, Nakase T, Okuda S, Meng WX, Yonenobu K, Yoshikawa H (2001) The relationship between apoptosis of endplate chondrocytes and aging and degeneration of the intervertebral disc. Spine 26:2414-2420
6. Ariga K, Yonenobu K, Nakase T, Hosono N, Okuda S, Meng WX, Tamura Y, Yoshikawa H (2003) Mechanical stress-induced apoptosis of endplate chondrocytes in organ-cultured mouse intervertebral discs-an ex vivo study. Spine 28:1528-1533
7. Aszodi A, Chan D, Hunziker E, Bateman JF, Fassler R (1998) Collagen II is essential for the removal of the notochord and the formation of intervertebral discs. J Cell Biol 143:1399-1412
8. Bailey AS, Adler F, Min LS, Asher MA (2001) A comparison between bipedal and quadrupedal rats: do bipedal rats actually assume an upright posture? Spine 26:E308-E313
9. Barry FP, Neame PJ, Sasse J, Pearson D (1994) Length variation in the keratan sulfate domain of mammalian aggrecan. Matrix Biol 14:323-328
10. Battie MC, Videman T, Parent E (2004) Lumbar disc degeneration: epidemiology and genetic influences. Spine 29:2679-2690
11. Bayliss MT, Johnstone B, O'Brien JP (1988) 1988 Volvo award in basic science. Proteoglycan synthesis in the human intervertebral disc. Variation with age, region and pathology. Spine 13:972-981
12. Behrens A, Haigh J, Mechta-Grigoriou F, Nagy A, Yaniv M, Wagner EF (2003) Impaired intervertebral disc formation in the absence of Jun. Development 130:103-109
13. Benneker LM, Heini PF, Alini M, Anderson SE, Ito K (2005) 2004 Young Investigator Award Winner: vertebral endplate marrow contact channel occlusions and intervertebral disc degeneration. Spine 30:167-173
14. Bernick S, Cailliet R (1982) Vertebral end-plate changes with aging of human vertebrae. Spine 7:97-102
15. Berry RJ (1960) Genetical studies on the skeleton of the mouse 26. Pintail. Genet Res 1:439-451
16. Boszczyk BM, Boszczyk AA, Putz R (2001) Comparative and functional anatomy of the mammalian lumbar spine. Anat Rec 264:157-168
17. Braund KG (1974) Some aspects of structure and function of the canine intervertebral disc. Ph.D. thesis, University of Sydney
18. Bruehlmann SB, Matyas JR, Duncan NA (2004) ISSLS prize winner: collagen fibril sliding governs cell mechanics in the anulus fibrosus: an in situ confocal microscopy study of bovine discs. Spine 29:2612-2620
19. Bushell GR, Ghosh DP, Taylor TK, Sutherland JM, Braund KG (1978) The effect of spinal fusion on the collagen and proteoglycans of the canine intervertebral disc. J Surg Res 25:61-69
20. Bushell GR, Ghosh P, Taylor TK, Sutherland JM (1979) The collagen of the intervertebral disc in adolescent idiopathic scoliosis. J Bone Joint Surg Br 61-B:501-508
21. Butler WF (1988) Comparative anatomy and development of the mammalian disc. In: Ghosh P (eds) The biology of the intervertebral disc. CRC, Boca Raton, FL, pp 83-108
22. Cassidy JD, Yong-Hing K, Kirkaldy-Willis WH, Wilkinson AA (1988) A study of the effects of bipedism and upright posture on the lumbosacral spine and paravertebral muscles of the Wistar rat. Spine 13:301-308
23. Cheung KM, Lu DS, Poon AM, Wang T, Luk KD, Leong JC (2003) Effect of melatonin suppression on scoliosis development in chickens by either constant light or surgical pinealectomy. Spine 28:1941-1944
24. Cheung KM, Wang T, Poon AM, Carl A, Tranmer B, Hu Y, Luk KD, Leong JC (2005) The effect of pinealectomy on scoliosis development in young nonhuman primates. Spine 30:2009-2013
25. Chiba K, Andersson GB, Masuda K, Momohara S, Williams JM, Thonar EJ (1998) A new culture system to study the metabolism of the intervertebral disc in vitro. Spine 23:1821-1827
26. Ching CT, Chow DH, Yao FY, Holmes AD (2003) The effect of cyclic compression on the mechanical properties of the inter-vertebral disc: an in vivo study in a rat tail model. Clin Biomech 18:182-189
27. Ching CT, Chow DH, Yao FY, Holmes AD (2004) Changes in nuclear composition following cyclic compression of the intervertebral disc in an in vivo rat-tail model. Med Eng Phys 26:587-594
28. Cole TC, Burkhardt D, Frost L, Ghosh P (1985) The proteoglycans of the canine intervertebral disc. Biochim Biophys Acta 839:127-138
29. Cole TC, Burkhardt D, Ghosh P, Ryan M, Taylor T (1985) Effects of spinal fusion on the proteoglycans of the canine intervertebral disc. J Orthop Res 3:277-291
30. Cole TC, Ghosh P, Hannan NJ, Taylor TK, Bellenger CR (1987) The response of the canine intervertebral disc to immobilization produced by spinal arthrodesis is dependent on constitutional factors. J Orthop Res 5:337-347
31. Cole TC, Ghosh P, Taylor TK (1986) Variations of the proteoglycans of the canine intervertebral disc with ageing. Biochim Biophys Acta 880:209-219
32. Court C, Colliou OK, Chin JR, Liebenberg E, Bradford DS, Lotz JC (2001) The effect of static in vivo bending on the murine intervertebral disc. Spine J 1:239-245
33. Demers CN, Antoniou J, Mwale F (2004) Value and limitations of using the bovine tail as a model for the human lumbar spine. Spine 29:2793-2799
34. Elliott DM, Sarver JJ (2004) Young investigator award winner: validation of the mouse and rat disc as mechanical models of the human lumbar disc. Spine 29:713-722
35. Fazzalari NL, Costi JJ, Hearn TC, Fraser RD, Vernon-Roberts B, Hutchinson J, Manthey BA, Parkinson IH, Sinclair C (2001) Mechanical and pathologic consequences of induced concentric anular tears in an ovine model. Spine 26:2575-2581
36. Flannery CR, Little CB, Caterson B (1998) Molecular cloning and sequence analysis of the aggrecan interglobular domain from porcine, equine, bovine and ovine cartilage: comparison of proteinase-susceptible regions and sites of keratan sulfate substitution. Matrix Biol 16:507-511
37. Foster MR, Allen MJ, Schoonmaker JE, Yuan HA, Kanazawa A, Park SA, Liu B (2002) Characterization of a developing lumbar arthrodesis in a sheep model with quantitative instability. Spine J 2:244-250
38. Furuya S, Ohtsuki T, Yabe Y, Hosoda Y (2000) Ultrastructural study on calcification of cartilage: comparing ICR and twy mice. J Bone Miner Metab 18:140-147
39. Gantenbein B, Grünhagen T, Lee CR, van Donkelaar CC, Alini M, Ito K (2006) An in vitro organ culturing system for intervertebral disc explants with vertebral endplates: a feasibility study with ovine caudal discs. Spine 31:2665-2673
40. Ghosh P, Bushell GR, Taylor TK, Pearce RH, Grimmer BJ (1980) Distribution of glycosaminoglycans across the normal and the scoliotic disc. Spine 5:310-317
41. Ghosh P, Melrose J, Cole TC, Taylor T (1992) A comparison of the high buoyant density proteoglycans isolated from the intervertebral discs of chondrodystrophoid and non-chondrodystrophoid dogs. Matrix 12:148-155
42. Ghosh P, Taylor TK, Braund KG (1977) The variation of the glycosaminoglycans of the canine intervertebral disc with ageing. I. Chondrodystrophoid breed. Gerontology 23:87-98
43. Ghosh P, Taylor TK, Braund KG (1977) Variation of the glycosaminoglycans of the intervertebral disc with ageing. II. Non-chondrodystrophoid breed. Gerontology 23:99-109
44. Ghosh P, Taylor TK, Braund KG, Larsen LH (1976) The collagenous and non-collagenous protein of the canine intervertebral disc and their variation with age, spinal level and breed. Gerontology 22:124-134
45. Gillett NA, Gerlach R, Cassidy JJ, Brown SA (1988) Age-related changes in the beagle spine. Acta Orthop Scand 59:503-507
46. Glant TT, Mikecz K, Arzoumanian A, Poole AR (1987) Proteoglycan-induced arthritis in BALB/c mice. Clinical features and histopathology. Arthritis Rheum 30:201-212
47. Hadjipavlou AG, Simmons JW, Yang JP, Bi LX, Ansari GA, Kaphalia BS, Simmons DJ, Nicodemus CL, Necessary JT, Lane R, Esch O (1998) Torsional injury resulting in disc degeneration: I. An in vivo rabbit model. J Spinal Disord 11:312-317
48. Hammer RE, Maika SD, Richardson JA, Tang JP, Taurog JD (1990) Spontaneous inflammatory disease in transgenic rats expressing HLA-B27 and human beta 2m: an animal model of HLA-B27-associated human disorders. Cell 63:1099-1112
49. Hamrick MW, Pennington C, Byron CD (2003) Bone architecture and disc degeneration in the lumbar spine of mice lacking GDF-8 (myostatin). J Orthop Res 21:1025-1032
50. Higuchi M, Abe K, Kaneda K (1983) Changes in the nucleus pulposus of the intervertebral disc in bipedal mice. A light and electron microscopic study. Clin Orthop Relat Res 175:251-257
51. Holm S, Holm AK, Ekström L, Karladani A, Hansson T (2004) Experimental disc degeneration due to endplate injury. J Spinal Disord Tech 17:64-71
52. Horner HA, Roberts S, Bielby RC, Menage J, Evans H, Urban JPG (2002) Cells from different regions of the intervertebral disc-effect of culture system on matrix expression and cell phenotype. Spine 27:1018-1028
53. Horner HA, Urban JPG (2001) 2001 Volvo award winner in basic science studies: effect of nutrient supply on the viability of cells from the nucleus pulposus of the intervertebral disc. Spine 26:2543-2549
54. Hunter CJ, Matyas JR, Duncan NA (2003) The notochordal cell in the nucleus pulposus: a review in the context of tissue engineering. Tissue Eng 9:667-677
55. Hunter CJ, Matyas JR, Duncan NA (2004) Cytomorphology of notochordal and chondrocytic cells from the nucleus pulposus: a species comparison. J Anat 205:357-362
56. Hutton WC, Murakami H, Li A, Elmer WA, Yoon ST, Minamide A, Akamaru T, Tomita K (2004) The effect of blocking a nutritional pathway to the intervertebral disc in the dog model. J Spinal Disord Tech 17:53-63
57. Iatridis JC, MacLean JJ, Roughley PJ, Alini M (2006) Effects of mechanical loading on intervertebral disc metabolism in vivo. J Bone Joint Surg Am 88(Suppl 2):41-46
58. Iatridis JC, Mente PL, Stokes IA, Aronsson DD, Alini M (1999) Compression-induced changes in intervertebral disc properties in a rat tail model. Spine 24:996-1002
59. Johnson WEB, Menage J, Evans H, Gaguilo B, Roberts S, Eisenstein SM (2004) Serum-deprivation is associated with decreased cellularity and a loss of proteoglycan in organ cultures of bovine intervertebral discs. In: Proceedings of the 30th annual meeting, 5-5-1930, Porto, p 223
60. Kaapa E, Han X, Holm S, Peltonen J, Takala T, Vanharanta H (1995) Collagen synthesis and types I, III, IV, and VI collagens in an animal model of disc degeneration. Spine 20:59-66
61. Kaapa E, Holm S, Han X, Takala T, Kovanen V, Vanharanta H (1994) Collagens in the injured porcine intervertebral disc. J Orthop Res 12:93-102
62. Kaigle AM, Holm SH, Hansson TH (1995) Experimental instability in the lumbar spine. Spine 20:421-430
63. Kaigle AM, Holm SH, Hansson TH (1997) 1997 Volvo Award winner in biomechanical studies. Kinematic behavior of the porcine lumbar spine: a chronic lesion model. Spine 22:2796-2806
64. Kanemura T, Kawakami N, Deguchi M, Mimatsu K, Iwata H (1997) Natural course of experimental scoliosis in pinealectomized chickens. Spine 22:1563-1567
65. Key JA, Ford LT (1948) Experimental intervertebral disc lesions. J Bone Joint Surg Am 30A:621
66. Kim KS, Yoon ST, Li J, Park JS, Hutton WC (2005) Disc degeneration in the rabbit: a biochemical and radiological comparison between four disc injury models. Spine 30:33-37
67. Kim KW, Ha KY, Park JB, Woo YK, Chung HN, An HS (2005) Expressions of membrane-type I matrix metalloproteinase, Ki-67 protein, and type II collagen by chondrocytes migrating from cartilage endplate into nucleus pulposus in rat intervertebral discs: a cartilage endplate-fracture model using an intervertebral disc organ culture. Spine 30:1373-1378
68. Kim KW, Lim TH, Kim JG, Jeong ST, Masuda K, An HS (2003) The origin of chondrocytes in the nucleus pulposus and histologic findings associated with the transition of a notochordal nucleus pulposus to a fibrocartilaginous nucleus pulposus in intact rabbit intervertebral discs. Spine 28:982-990
69. Kimura T, Nakata K, Tsumaki N, Miyamoto S, Matsui Y, Ebara S, Ochi T (1996) Progressive degeneration of articular cartilage and intervertebral discs. An experimental study in transgenic mice bearing a type IX collagen mutation. Int Orthop 20:177-181
70. Kluba T, Niemeyer T, Gaissmaier C, Grunder T (2005) Human anulus fibrosis and nucleus pulposus cells of the intervertebral disc: effect of degeneration and culture system on cell phenotype. Spine 30:2743-2748
71. Krebs J, Ferguson SJ, Goss BG, Aebli N (2006) Degenerative changes of intervertebral discs after vertebroplasty. In: Proceedings of the 33rd annual meeting of the international society for the study of the lumbar spine, Bergen, p 31
72. Kroeber M, Unglaub F, Guehring T, Nerlich A, Hadi T, Lotz J, Carstens C (2005) Effects of controlled dynamic disc distraction on degenerated intervertebral discs: an in vivo study on the rabbit lumbar spine model. Spine 30:181-187
73. Kroeber MW, Unglaub F, Wang HL, Schmid C, Thomsen M, Nerlich A, Richter W (2002) New in vivo animal model to create intervertebral disc degeneration and to investigate the effects of therapeutic strategies to stimulate disc regeneration. Spine 27:2684-2690
74. Latorre A, Albareda J, Castiella T, Lasierra JM, Seral F (1998) Experimental model of multidirectional disc hernia in rats. Int Orthop 22:44-48
75. Lauerman WC, Platenberg RC, Cain JE, Deeney VF (1992) Age-related disk degeneration: preliminary report of a naturally occurring baboon model. J Spinal Disord 5:170-174
76. Lee CR, Grad S, MacLean JJ, Iatridis JC, Alini M (2005) Effect of mechanical loading on mRNA levels of common endogenous controls in articular chondrocytes and intervertebral disk. Anal Biochem 341:372-375
77. Lee CR, Iatridis JC, Poveda L, Alini M (2006) In vitro organ culture of the bovine intervertebral disc: effects of vertebral endplate and potential for mechanobiology studies. Spine 31:515-522
78. Lindblom K (1957) Intervertebral-disc degeneration considered as a pressure atrophy. J Bone Joint Surg Am 39-A:933-945
79. Lipson SJ, Muir H (1980) Vertebral osteophyte formation in experimental disc degeneration. Morphologic and proteoglycan changes over time. Arthritis Rheum 23:319-324
80. Lipson SJ, Muir H (1981) 1980 Volvo award in basic science. Proteoglycans in experimental intervertebral disc degeneration. Spine 6:194-210
81. Lotz JC (2004) Animal models of intervertebral disc degeneration: lessons learned. Spine 29:2742-2750
82. Lotz JC, Colliou OK, Chin JR, Duncan NA, Liebenberg E (1998) 1998 Volvo Award winner in biomechanical studies-compression- induced degeneration of the intervertebral disc: an in vivo mouse model and finite-element study. Spine 23:2493-2506
83. Lundin O, Ekstrom L, Hellstrom M, Holm S, Sward L (1998) Injuries in the adolescent porcine spine exposed to mechanical compression. Spine 23:2574-2579
84. Lundin O, Ekstrom L, Hellstrom M, Holm S, Sward L (2000) Exposure of the porcine spine to mechanical compression: differences in injury pattern between adolescents and adults. Eur Spine J 9:466-471
85. Machida M, Dubousset J, Imamura Y, Iwaya T, Yamada T, Kimura J (1993) An experimental study in chickens for the pathogenesis of idiopathic scoliosis. Spine 18:1609-1615
86. Machida M, Dubousset J, Imamura Y, Iwaya T, Yamada T, Kimura J (1995) Role of melatonin deficiency in the development of scoliosis in pinealectomised chickens. J Bone Joint Surg Br 77:134-138
87. Machida M, Murai I, Miyashita Y, Dubousset J, Yamada T, Kimura J (1999) Pathogenesis of idiopathic scoliosis. Experimental study in rats. Spine 24:1985-1989
88. Machida M, Saito M, Dubousset J, Yamada T, Kimura J, Shibasaki K (2005) Pathological mechanism of idiopathic scoliosis: experimental scoliosis in pinealectomized rats. Eur Spine J 14:843-848
89. Maeda S, Kokubun S (2000) Changes with age in proteoglycan synthesis in cells cultured in vitro from the inner and outer rabbit annulus fibrosus. Responses to interleukin-1 and interleukin-1 receptor antagonist protein. Spine 25:166-169
90. Maldonado BA, Oegema TR Jr (1992) Initial characterization of the metabolism of intervertebral disc cells encapsulated in microspheres. J Orthop Res 10:677-690
91. Mason RM, Palfrey AJ (1984) Intervertebral disc degeneration in adult mice with hereditary kyphoscoliosis. J Orthop Res 2:333-338
92. Masuda K, Aota Y, Muehleman C, Imai Y, Okuma M, Thonar EJ, Andersson GB, An HS (2005) A novel rabbit model of mild, reproducible disc degeneration by an anulus needle puncture: correlation between the degree of disc injury and radiological and histological appearances of disc degeneration. Spine 30:5-14
93. Melrose J, Ghosh P, Taylor TK, Hall A, Osti OL, Vernon-Roberts B, Fraser RD (1992) A longitudinal study of the matrix changes induced in the intervertebral disc by surgical damage to the annulus fibrosus. J Orthop Res 10:665-676
94. Melrose J, Ghosh P, Taylor TK, Latham J, Moore R (1997) Topographical variation in the catabolism of aggrecan in an ovine annular lesion model of experimental disc degeneration. J Spinal Disord 10:55-67
95. Melrose J, Ghosh P, Taylor TK, McAuley L (1994) Variation in the composition of the ovine intervertebral disc with spinal level and in its constituent proteoglycans. Vet Comp Orthop Traumatol 7:70-76
96. Melrose J, Ghosh P, Taylor TK, Vernon-Roberts B, Latham J, Moore R (1997) Elevated synthesis of biglycan and decorin in an ovine annular lesion model of experimental disc degeneration. Eur Spine J 6:376-384
97. Melrose J, Gurr KR, Cole TC, Darvodelsky A, Ghosh P, Taylor TK (1991) The influence of scoliosis and ageing on proteoglycan heterogeneity in the human intervertebral disc. J Orthop Res 9:68-77
98. Melrose J, Hall A, Macpherson C, Bellenger CR, Ghosh P (1995) Evaluation of digestive proteinases from the Antarctic krill Euphasia superba as potential chemonucleolytic agents. In vitro and in vivo studies. Arch Orthop Trauma Surg 114:145-152
99. Melrose J, Roberts S, Smith S, Menage J, Ghosh P (2002) Increased nerve and blood vessel ingrowth associated with proteoglycan depletion in an ovine anular lesion model of experimental disc degeneration. Spine 27:1278-1285
100. Melrose J, Smith S, Little CB, Kitson J, Hwa SY, Ghosh P (2002) Spatial and temporal localization of transforming growth factor-beta, fibroblast growth factor-2, and osteonectin, and identification of cells expressing alpha-smooth muscle actin in the injured anulus fibrosus: implications for extracellular matrix repair. Spine 27:1756-1764
101. Melrose J, Taylor TK, Ghosh P (1996) Variation in intervertebral disc serine proteinase inhibitory proteins with ageing in a chondrodystrophoid (beagle) and a non-chondrodystrophoid (greyhound) canine breed. Gerontology 42:322-329
102. Melrose J, Taylor TK, Ghosh P (1997) The serine proteinase inhibitory proteins of the chondrodystrophoid (beagle) and non-chondrodystrophoid (greyhound) canine intervertebral disc. Electrophoresis 18:1059-1063
103. Melrose J, Taylor TK, Ghosh P, Holbert C, Macpherson C, Bellenger CR (1996) Intervertebral disc reconstitution after chemonucleolysis with chymopapain is dependent on dosage. Spine 21:9-17
104. Mente PL, Aronsson DD, Stokes IAF, Iatridis JC (1999) Mechanical modulation of growth for the correction of vertebral wedge deformities. J Orthop Res 17:518-524
105. Mikecz K, Glant TT, Poole AR (1987) Immunity to cartilage proteoglycans in BALB/c mice with progressive polyarthritis and ankylosing spondylitis induced by injection of human cartilage proteoglycan. Arthritis Rheum 30:306-318
106. Moore RJ, Crotti TN, Osti OL, Fraser RD, Vernon-Roberts B (1999) Osteoarthrosis of the facet joints resulting from anular rim lesions in sheep lumbar discs. Spine 24:519-525
107. Moore RJ, Osti OL, Vernon-Roberts B, Fraser RD (1992) Changes in endplate vascularity after an outer anulus tear in the sheep. Spine 17:874-878
108. Moore RJ, Vernon-Roberts B, Osti OL, Fraser RD (1996) Remodeling of vertebral bone after outer anular injury in sheep. Spine 21:936-940
109. Moskowitz RW, Ziv I, Denko CW, Boja B, Jones PK, Adler JH (1990) Spondylosis in sand rats: a model of intervertebral disc degeneration and hyperostosis. J Orthop Res 8:401-411
110. Neufeld JH, Machado T, Margolin L (1991) Variables affecting disc size in the lumbar spine of rabbits: anesthesia, paralysis, and disc injury. J Orthop Res 9:104-112
111. Norcross JP, Lester GE, Weinhold P, Dahners LE (2003) An in vivo model of degenerative disc disease. J Orthop Res 21:183-188
112. O'Kelly C, Wang X, Raso J, Moreau M, Mahood J, Zhao J, Bagnall K (1999) The production of scoliosis after pinealectomy in young chickens, rats, and hamsters. Spine 24:35-43
113. Oegema TR, Johnson SL, Aguiar DJ, Ogilvie JW (2000) Fibronectin and its fragments increase with degeneration in the human intervertebral disc. Spine 25:2742-2747
114. Olsewski JM, Schendel MJ, Wallace LJ, Ogilvie JW, Gundry CR (1996) Magnetic resonance imaging and biological changes in injured intervertebral discs under normal and increased mechanical demands. Spine 21:1945-1951
115. Oshima H, Ishihara H, Urban JP, Tsuji H (1993) The use of coccygeal discs to study intervertebral disc metabolism. J Orthop Res 11:332-338
116. Osterman K, Osterman H (1996) Experimental lumbar spondylolisthesis in growing rabbits. Clin Orthop Relat Res 332:274-280
117. Osti OL, Vernon-Roberts B, Fraser RD (1990) 1990 Volvo Award in experimental studies. Anulus tears and intervertebral disc degeneration. An experimental study using an animal model. Spine 15:762-767
118. Park C, Kim YJ, Lee CS, An K, Shin HJ, Lee CH, Kim CH, Shin JW (2005) An in vitro animal study of the biomechanical responses of anulus fibrosus with aging. Spine 30:E259-E265
119. Pedrini-Mille A, Weinstein JN, Found EM, Chung CB, Goel VK (1990) Stimulation of dorsal root ganglia and degradation of rabbit annulus fibrosus. Spine 15:1252-1256
120. Peng BG, Hou SX, Shi Q, Jia LS (2001) The relationship between cartilage end-plate calcification and disc degeneration: an experimental study. Chin Med J 114:308-312
121. Pezowicz CA, Robertson PA, Broom ND (2005) Intralamellar relationships within the collagenous architecture of the annulus fibrosus imaged in its fully hydrated state. J Anat 207:299-312
122. Phillips FM, Reuben J, Wetzel FT (2002) Intervertebral disc degeneration adjacent to a lumbar fusion-an experimental rabbit model. J Bone Joint Surg Br 84B:289-294
123. Puustjarvi K, Lammi M, Helminen H, Inkinen R, Tammi M (1994) Proteoglycans in the intervertebral disc of young dogs following strenuous running exercise. Connect Tissue Res 30:225-240
124. Puustjarvi K, Lammi M, Kiviranta I, Helminen HJ, Tammi M (1993) Proteoglycan synthesis in canine intervertebral discs after long-distance running training. J Orthop Res 11:738-746
125. Rannou F, Poiraudeau S, Foltz V, Boiteux M, Corvol M, Revel M (2000) Monolayer anulus fibrosus cell cultures in a mechanically active environment: local culture condition adaptations and cell phenotype study. J Lab Clin Med 136:412-421
126. Roberts S, Menage J, Eisenstein SM (1993) The cartilage end-plate and intervertebral disc in scoliosis: calcification and other sequelae. J Orthop Res 11:747-757
127. Saamanen AM, Puustjarvi K, Ilves K, Lammi M, Kiviranta I, Jurvelin J, Helminen HJ, Tammi M (1993) Effect of running exercise on proteoglycans and collagen content in the intervertebral disc of young dogs. Int J Sports Med 14:48-51
128. Sahlman J, Inkinen R, Hirvonen T, Lammi MJ, Lammi PE, Nieminen J, Lapvetelainen T, Prockop DJ, Arita M, Li SW, Hyttinen MM, Helminen HJ, Puustjarvi K (2001) Premature vertebral endplate ossification and mild disc degeneration in mice after inactivation of one allele belonging to the Col2a1 gene for Type II collagen. Spine 26:2558-2565
129. Sambrook PN, MacGregor AJ, Spector TD (1999) Genetic influences on cervical and lumbar disc degeneration: a magnetic resonance imaging study in twins. Arthritis Rheum 42:366-372
130. Sarver JJ, Elliott DM (2005) Mechanical differences between lumbar and tail discs in the mouse. J Orthop Res 23:150-155
131. Shi S, Ciurli C, Cartman A, Pidoux I, Poole AR, Zhang Y (2003) Experimental immunity to the G1 domain of the proteoglycan versican induces spondylitis and sacroiliitis, of a kind seen in human spondylarthropathies. Arthritis Rheum 48:2903-2915
132. Smith JW, Walmsley R (1951) Experimental incision of the intervertebral disc. J Bone Joint Surg Br 33-B:612-625
133. Sobajima S, Kompel JF, Kim JS, Wallach CJ, Robertson DD, Vogt MT, Kang JD, Gilbertson LG (2005) A slowly progressive and reproducible animal model of intervertebral disc degeneration characterized by MRI, X-ray, and histology. Spine 30:15-24
134. Stevens JW, Kurriger GL, Carter AS, Maynard JA (2000) CD44 expression in the developing and growing rat intervertebral disc. Dev Dyn 219:381-390
135. Stokes IA, Aronsson DD, Spence H, Iatridis JC (1998) Mechanical modulation of intervertebral disc thickness in growing rat tails. J Spinal Disord 11:261-265
136. Stokes IA, Counts DF, Frymoyer JW (1989) Experimental instability in the rabbit lumbar spine. Spine 14:68-72
137. Stokes IA, Iatridis JC (2004) Mechanical conditions that accelerate intervertebral disc degeneration: overload versus immobilization. Spine 29:2724-2732
138. Suguro T, Oegema TR Jr, Bradford DS (1986) Ultrastructural study of the short-term effects of chymopapain on the intervertebral disc. J Orthop Res 4:281-287
139. Sweet HO, Green MC (1981) Progressive ankylosis, a new skeletal mutation in the mouse. J Hered 72:87-93
140. Takaishi H, Nemoto O, Shiota M, Kikuchi T, Yamada H, Yamagishi M, Yabe Y (1997) Type-II collagen gene expression is transiently upregulated in experimentally induced degeneration of rabbit intervertebral disc. J Orthop Res 15:528-538
141. Taurog JD, Maika SD, Satumtira N, Dorris ML, McLean IL, Yanagisawa H, Sayad A, Stagg AJ, Fox GM, Le O'Brien A, Rehman M, Zhou M, Weiner AL, Splawski JB, Richardson JA, Hammer RE (1999) Inflammatory disease in HLA-B27 transgenic rats. Immunol Rev 169:209-223
142. Taylor TK, Ghosh P, Braund KG, Sutherland JM, Sherwood AA (1976) The effect of spinal fusion on intervertebral disc composition: an experimental study. J Surg Res 21:91-104
143. Taylor TK, Melrose J, Burkhardt D, Ghosh P, Claes LE, Kettler A, Wilke HJ (2000) Spinal biomechanics and aging are major determinants of the proteoglycan metabolism of intervertebral disc cells. Spine 25:3014-3020
144. Thometz JG, Liu XC, Lyon R (2000) Three-dimensional rotations of the thoracic spine after distraction with and without rib resection: a kinematic evaluation of the apical vertebra in rabbits with induced scoliosis. J Spinal Disord 13:108-112
145. Thompson RE, Pearcy MJ, Barker TM (2004) The mechanical effects of intervertebral disc lesions. Clin Biomech 19:448-455
146. Turgut M, Basaloglu HK, Yenisey C, Ozsunar Y (2006) Surgical pinealectomy accelerates intervertebral disc degeneration process in chicken. Eur Spine J 15:605-612
147. Urayama S (1986) Histological and ultrastructural study of degeneration of the lumbar intervertebral disc in the rabbit following nucleotomy, with special reference to the topographical distribution pattern of the degeneration. Nippon Seikeigeka Gakkai Zasshi 60:649-662
148. van der Werf MJ, Lezuo P, Maissen O, Ito K (2006) Decreased diffusion as a result of perfusion block in the ovine lumbar spine: a future model for disc degeneration. In: Proceedings of the 52nd annual meeting of the orthopaedic research society, Chicago, IL, p 31
149. Walsh AJL, Lotz JC (2004) Biological response of the intervertebral disc to dynamic loading. J Biomech 37:329-337
150. Wang JY, Baer AE, Kraus VB, Setton LA (2001) Intervertebral disc cells exhibit differences in gene expression in alginate and monolayer culture. Spine 26:1747-1751
151. Wang X, Jiang H, Raso J, Moreau M, Mahood J, Zhao J, Bagnall K (1997) Characterization of the scoliosis that develops after pinealectomy in the chicken and comparison with adolescent idiopathic scoliosis in humans. Spine 22:2626-2635
152. Watanabe H, Nakata K, Kimata K, Nakanishi I, Yamada Y (1997) Dwarfism and age-associated spinal degeneration of heterozygote cmd mice defective in aggrecan. Proc Natl Acad Sci USA 94:6943-6947
153. Watanabe H, Yamada Y (2002) Chondrodysplasia of gene knockout mice for aggrecan and link protein. Glycoconj J 19:269-273
154. Weinreich S, Hoebe B, Ivanyi P (1995) Maternal age influences risk for HLA-B27 associated ankylosing enthesopathy in transgenic mice. Ann Rheum Dis 54:754-756
155. Wilke HJ, Kettler A, Claes LE (1997) Are sheep spines a valid biomechanical model for human spines? Spine 22:2365-2374
156. Wilke HJ, Kettler A, Gosh P, Claes L (1999) Is the lumbar sheep spine an adequate model for the human lumbar spine? - a comparison of biomechanical properties, macroscopic and microscopic anatomy and bone mineral density. In: Proceedings of the 26th annual meeting, Hawaii, p 124
157. Wilke HJ, Kettler A, Wenger KH, Claes LE (1997) Anatomy of the sheep spine and its comparison to the human spine. Anat Rec 247:542-555
158. Wilke HJ, Krischak ST, Wenger KH, Claes LE (1997) Load-displacement properties of the thoracolumbar calf spine: experimental results and comparison to known human data. Eur Spine J 6:129-137
159. Wilke HJ, Rohlmann A, Neller S, Graichen F, Claes L, Bergmann G (2003) ISSLS prize winner: a novel approach to determine trunk muscle forces during flexion and extension: a comparison of data from an in vitro experiment and in vivo measurements. Spine 28:2585-2593
160. White AA, Panjabi MM (1990) Clinical Biomechanics of the Spine. 2nd edn. JB Lippincott Company
161. Yamada K, Tanabe S, Eueno H, Oinuma A, Ytakahashi T, Mityauchi S, Shigeno S, Hirose T, Miyahara K, Sato M (2001) Investigation of the short term effect of chemonucleolysis with chondroitinase ABC. J Vet Med Sci 63: 521-525