Subchondral bone in osteoarthritis: Insight into risk factors and microstructural changes

Arthritis Research and Therapy

Volumn 15, Issue 6, 2013, Pages

  Li, Guangyi ^a,b   Yin, Jimin ^a   Gao, Junjie ^b   Cheng, Tak S ^b   Pavlos, Nathan J ^b   Zhang, Changqing ^a   Zheng, Ming H ^b  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AGING; ARTICULAR CARTILAGE; BONE; BONE CYST; BONE MARROW EDEMA; BONE NECROSIS; BONE STRUCTURE; CARTILAGE; GENETIC PREDISPOSITION; HISTOPATHOLOGY; HUMAN; JOINT; JOINT INJURY; KNEE; NONHUMAN; OBESITY; OSTEOARTHRITIS; OSTEOSCLEROSIS; PATHOGENESIS; PHYSICAL ACTIVITY; REVIEW; RISK FACTOR; SUBCHONDRAL BONE; SUBCHONDRAL BONE PLATE; PATHOLOGY;

BONE AND BONES; HUMANS; OSTEOARTHRITIS; RISK FACTORS;

EID: 84889670489     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar4405     Document Type: Review

References (125)

1. Grynpas MD, Alpert B, Katz I, Lieberman I, Pritzker KP. Subchondral bone in osteoarthritis. Calcif Tissue Int 1991, 49:20-26. 10.1007/BF02555898, 1893292.
2. Suri S, Walsh DA. Osteochondral alterations in osteoarthritis. Bone 2012, 51:204-211. 10.1016/j.bone.2011.10.010, 22023932.
3. Madry H, van Dijk CN, Mueller-Gerbl M. The basic science of the subchondral bone. Knee Surg Sports Traumatol Arthrosc 2010, 18:419-433. 10.1007/s00167-010-1054-z, 20119671.
4. Burr DB, Gallant MA. Bone remodelling in osteoarthritis. Nat Rev Rheumatol 2012, 8:665-673. 10.1038/nrrheum.2012.130, 22868925.
5. Henrotin Y, Pesesse L, Sanchez C. Subchondral bone and osteoarthritis: biological and cellular aspects. Osteoporos Int 2012, 23:S847-S851. 10.1007/s00198-012-2162-z, 23179567.
6. Bettica P, Cline G, Hart DJ, Meyer J, Spector TD. Evidence for increased bone resorption in patients with progressive knee osteoarthritis: longitudinal results from the Chingford study. Arthritis Rheum 2002, 46:3178-3184. 10.1002/art.10630, 12483721.
7. McErlain DD, Ulici V, Darling M, Gati JS, Pitelka V, Beier F, Holdsworth DW. An in vivo investigation of the initiation and progression of subchondral cysts in a rodent model of secondary osteoarthritis. Arthritis Res Ther 2012, 14:R26. 10.1186/ar3727, 3392819, 22304985.
8. Felson DT, McLaughlin S, Goggins J, LaValley MP, Gale ME, Totterman S, Li W, Hill C, Gale D. Bone marrow edema and its relation to progression of knee osteoarthritis. Ann Intern Med 2003, 139:330-336. 10.7326/0003-4819-139-5_Part_1-200309020-00008, 12965941.
9. Burr DB, Radin EL. Microfractures and microcracks in subchondral bone: are they relevant to osteoarthrosis?. Rheum Dis Clin North Am 2003, 29:675-685. 10.1016/S0889-857X(03)00061-9, 14603577.
10. Castaneda S, Roman-Blas JA, Largo R, Herrero-Beaumont G. Subchondral bone as a key target for osteoarthritis treatment. Biochem Pharmacol 2012, 83:315-323. 10.1016/j.bcp.2011.09.018, 21964345.
11. Goldring M, Goldring S. Articular cartilage and subchondral bone in the pathogenesis of osteoarthritis. Ann NY Acad Sci 2010, 1192:230-237. 10.1111/j.1749-6632.2009.05240.x, 20392241.
12. Milz S, Putz R. Quantitative morphology of the subchondral plate of the tibial plateau. J Anat 1994, 185:103-110. 1166819, 7559105.
13. Holmdahl DE, Ingelmark BE. The contact between the articular cartilage and the medullary cavities of the bone. Acta Orthop Scand 1950, 20:156-165. 10.3109/17453675009043414, 14868441.
14. Holopainen JT, Brama PA, Halmesmaki E, Harjula T, Tuukkanen J, van Weeren PR, Helminen HJ, Hyttinen MM. Changes in subchondral bone mineral density and collagen matrix organization in growing horses. Bone 2008, 43:1108-1114. 10.1016/j.bone.2008.07.254, 18757048.
15. Walker WT, Kawcak CE, Hill AE. Medial femoral condyle morphometrics and subchondral bone density patterns in thoroughbred racehorses. Am J Vet Res 2013, 74:691-699. 10.2460/ajvr.74.5.691, 23627381.
16. Goldring SR. Alterations in periarticular bone and cross talk between subchondral bone and articular cartilage in osteoarthritis. Ther Adv Musculoskelet Dis 2012, 4:249-258. 10.1177/1759720X12437353, 3403248, 22859924.
17. Pan J, Zhou X, Li W, Novotny JE, Doty SB, Wang L. In situ measurement of transport between subchondral bone and articular cartilage. J Orthop Res 2009, 27:1347-1352. 10.1002/jor.20883, 2748158, 19360842.
18. Lyons TJ, McClure SF, Stoddart RW, McClure J. The normal human chondro-osseous junctional region: evidence for contact of uncalcified cartilage with subchondral bone and marrow spaces. BMC Musculoskelet Disord 2006, 7:52. 10.1186/1471-2474-7-52, 1550228, 16787529.
19. Imhof H, Breitenseher M, Kainberger F, Rand T, Trattnig S. Importance of subchondral bone to articular cartilage in health and disease. Top Magn Reson Imaging 1999, 10:180-192. 10.1097/00002142-199906000-00002, 10565710.
20. Goldring SR. Role of bone in osteoarthritis pathogenesis. Med Clin North Am 2009, 93:25-35. xv, 10.1016/j.mcna.2008.09.006, 19059019.
21. Neogi T, Nevitt M, Niu J, Sharma L, Roemer F, Guermazi A, Lewis CE, Torner J, Javaid K, Felson D. Subchondral bone attrition may be a reflection of compartment-specific mechanical load: the MOST Study. Ann Rheum Dis 2010, 69:841-844. 10.1136/ard.2009.110114, 2891513, 19762366.
22. Lajeunesse D, Reboul P. Subchondral bone in osteoarthritis: a biologic link with articular cartilage leading to abnormal remodeling. Curr Opin Rheumatol 2003, 15:628-633. 10.1097/00002281-200309000-00018, 12960492.
23. Bellido M, Lugo L, Roman-Blas JA, Castaneda S, Caeiro JR, Dapia S, Calvo E, Largo R, Herrero-Beaumont G. Subchondral bone microstructural damage by increased remodelling aggravates experimental osteoarthritis preceded by osteoporosis. Arthritis Res Ther 2010, 12:R152. 10.1186/ar3103, 2945051, 20678201.
24. Brandt KD, Dieppe P, Radin E. Etiopathogenesis of osteoarthritis. Med Clin North Am 2009, 93:1-24. xv, 10.1016/j.mcna.2008.08.009, 19059018.
25. Chapman K, Valdes AM. Genetic factors in OA pathogenesis. Bone 2012, 51:258-264. 10.1016/j.bone.2011.11.026, 22178404.
26. Spector TD, Cicuttini F, Baker J, Loughlin J, Hart D. Genetic influences on osteoarthritis in women: a twin study. BMJ 1996, 312:940-943. 10.1136/bmj.312.7036.940, 2350783, 8616305.
27. Bijkerk C, Houwing-Duistermaat JJ, Valkenburg HA, Meulenbelt I, Hofman A, Breedveld FC, Pols HA, van Duijn CM, Slagboom PE. Heritabilities of radiologic osteoarthritis in peripheral joints and of disc degeneration of the spine. Arthritis Rheum 1999, 42:1729-1735. 10.1002/1529-0131(199908)42:8<1729::AID-ANR23>3.0.CO;2-H, 10446874.
28. Jordan JM, Kraus VB, Hochberg MC. Genetics of osteoarthritis. Curr Rheumatol Rep 2004, 6:7-13. 10.1007/s11926-004-0078-0, 14713397.
29. Doherty M. How important are genetic factors in osteoarthritis?. J Rheumatol Suppl 2004, 70:22-27.
30. Sandell LJ. Etiology of osteoarthritis: genetics and synovial joint development. Nat Rev Rheumatol 2012, 8:77-89.
31. Fries CL, Remedios AM. The pathogenesis and diagnosis of canine hip dysplasia: a review. Can Vet J 1995, 36:494-502. 1687006, 7585436.
32. Kannu P, Bateman JF, Belluoccio D, Fosang AJ, Savarirayan R. Employing molecular genetics of chondrodysplasias to inform the study of osteoarthritis. Arthritis Rheum 2009, 60:325-334. 10.1002/art.24251, 19180483.
33. Saamanen AK, Salminen HJ, Dean PB, De Crombrugghe B, Vuorio EI, Metsaranta MP. Osteoarthritis-like lesions in transgenic mice harboring a small deletion mutation in type II collagen gene. Osteoarthritis Cartilage 2000, 8:248-257. 10.1053/joca.2000.0298, 10903878.
34. Salminen H, Perala M, Lorenzo P, Saxne T, Heinegard D, Saamanen AM, Vuorio E. Up-regulation of cartilage oligomeric matrix protein at the onset of articular cartilage degeneration in a transgenic mouse model of osteoarthritis. Arthritis Rheum 2000, 43:1742-1748. 10.1002/1529-0131(200008)43:8<1742::AID-ANR10>3.0.CO;2-U, 10943864.
35. Allen KD, Griffin TM, Rodriguiz RM, Wetsel WC, Kraus VB, Huebner JL, Boyd LM, Setton LA. Decreased physical function and increased pain sensitivity in mice deficient for type IX collagen. Arthritis Rheum 2009, 60:2684-2693. 10.1002/art.24783, 2760314, 19714629.
36. Wilson MG, Michet CJ, Ilstrup DM, Melton LJ. Idiopathic symptomatic osteoarthritis of the hip and knee: a population-based incidence study. Mayo Clin Proc 1990, 65:1214-1221. 10.1016/S0025-6196(12)62745-1, 2402161.
37. McAlindon TE, Snow S, Cooper C, Dieppe PA. Radiographic patterns of osteoarthritis of the knee joint in the community: the importance of the patellofemoral joint. Ann Rheum Dis 1992, 51:844-849. 10.1136/ard.51.7.844, 1004766, 1632657.
38. Oliveria SA, Felson DT, Reed JI, Cirillo PA, Walker AM. Incidence of symptomatic hand, hip, and knee osteoarthritis among patients in a health maintenance organization. Arthritis Rheum 1995, 38:1134-1141. 10.1002/art.1780380817, 7639811.
39. Wluka AE, Cicuttini FM, Spector TD. Menopause, oestrogens and arthritis. Maturitas 2000, 35:183-199. 10.1016/S0378-5122(00)00118-3, 10936736.
40. Nevitt MC, Felson DT. Sex hormones and the risk of osteoarthritis in women: epidemiological evidence. Ann Rheum Dis 1996, 55:673-676. 10.1136/ard.55.9.673, 1010275, 8882148.
41. Zhang Y, McAlindon TE, Hannan MT, Chaisson CE, Klein R, Wilson PW, Felson DT. Estrogen replacement therapy and worsening of radiographic knee osteoarthritis: the Framingham Study. Arthritis Rheum 1998, 41:1867-1873. 10.1002/1529-0131(199810)41:10<1867::AID-ART20>3.0.CO;2-W, 9778229.
42. Sniekers YH, Weinans H, Bierma-Zeinstra SM, van Leeuwen JP, van Osch GJ. Animal models for osteoarthritis: the effect of ovariectomy and estrogen treatment - a systematic approach. Osteoarthritis Cartilage 2008, 16:533-541. 10.1016/j.joca.2008.01.002, 18280756.
43. Yang JH, Woo DG, Tyagi V, Oh KJ. Architectural changes in subchondral bone and its compliance in response to estrogen and progesterone: a micro-computed tomography study. Tissue Eng Regener Med 2011, 8:380-389.
44. Sniekers YH, Weinans H, van Osch GJ, van Leeuwen JP. Oestrogen is important for maintenance of cartilage and subchondral bone in a murine model of knee osteoarthritis. Arthritis Res Ther 2010, 12:R182. 10.1186/ar3148, 2991014, 20923566.
45. Ham KD, Carlson CS. Effects of estrogen replacement therapy on bone turnover in subchondral bone and epiphyseal metaphyseal cancellous bone of ovariectomized cynomolgus monkeys. J Bone Miner Res 2004, 19:823-829. 10.1359/jbmr.040309, 15068506.
46. Carbone LD, Nevitt MC, Wildy K, Barrow KD, Harris F, Felson D, Peterfy C, Visser M, Harris TB, Wang BW, Kritchevsky SB, Health, Aging and Body Composition Study The relationship of antiresorptive drug use to structural findings and symptoms of knee osteoarthritis. Arthritis Rheum 2004, 50:3516-3525. 10.1002/art.20627, 15529367, Health, Aging and Body Composition Study.
47. Shane Anderson A, Loeser RF. Why is osteoarthritis an age-related disease?. Best Pract Res Clin Rheumatol 2010, 24:15-26. 10.1016/j.berh.2009.08.006, 2818253, 20129196.
48. Ding M, Odgaard A, Linde F, Hvid I. Age-related variations in the microstructure of human tibial cancellous bone. J Orthop Res 2002, 20:615-621. 10.1016/S0736-0266(01)00132-2, 12038639.
49. Crane GJ, Fazzalari NL, Parkinson IH, Vernon-Roberts B. Age-related changes in femoral trabecular bone in arthrosis. Acta Orthop Scand 1990, 61:421-426. 10.3109/17453679008993554, 2239166.
50. Perilli E, Baleani M, Ohman C, Baruffaldi F, Viceconti M. Structural parameters and mechanical strength of cancellous bone in the femoral head in osteoarthritis do not depend on age. Bone 2007, 41:760-768. 10.1016/j.bone.2007.07.014, 17707709.
51. Martin B. Aging and strength of bone as a structural material. Calcif Tissue Int 1993, 53:S34-S39. discussion S39-S40, 10.1007/BF01673400, 8275378.
52. Lohmander LS. Gerhardsson de Verdier M, Rollof J, Nilsson PM, Engstrom G: Incidence of severe knee and hip osteoarthritis in relation to different measures of body mass: a population-based prospective cohort study. Ann Rheum Dis 2009, 68:490-496. 10.1136/ard.2008.089748, 18467514.
53. Lievense AM, Bierma-Zeinstra SM, Verhagen AP, van Baar ME, Verhaar JA, Koes BW. Influence of obesity on the development of osteoarthritis of the hip: a systematic review. Rheumatology (Oxford) 2002, 41:1155-1162.
54. Grotle M, Hagen KB, Natvig B, Dahl FA, Kvien TK. Obesity and osteoarthritis in knee, hip and/or hand: an epidemiological study in the general population with 10 years follow-up. BMC Musculoskelet Disord 2008, 9:132. 10.1186/1471-2474-9-132, 2573886, 18831740.
55. Guilak F, Fermor B, Keefe FJ, Kraus VB, Olson SA, Pisetsky DS, Setton LA, Weinberg JB. The role of biomechanics and inflammation in cartilage injury and repair. Clin Orthop Relat Res 2004, 423:17-26.
56. Killock D. Osteoarthritis: the influence of obesity on OA - does size matter or is metabolic dysfunction more important?. Nat Rev Rheumatol 2012, 8:61.
57. Mooney RA, Sampson ER, Lerea J, Rosier RN, Zuscik MJ. High-fat diet accelerates progression of osteoarthritis after meniscal/ligamentous injury. Arthritis Res Ther 2011, 13:R198. 10.1186/ar3529, 3334649, 22152451.
58. Sornay-Rendu E, Boutroy S, Vilayphiou N, Claustrat B, Chapurlat RD. In obese postmenopausal women, bone microarchitecture and strength are not commensurate to greater body weight: the Os des Femmes de Lyon (OFELY) study. J Bone Miner Res 2013, 28:1679-1687. 10.1002/jbmr.1880, 23371055.
59. Cao JJ. Effects of obesity on bone metabolism. J Orthop Surg Res 2011, 6:30. 10.1186/1749-799X-6-30, 3141563, 21676245.
60. Dequeker J, Goris P, Uytterhoeven R. Osteoporosis and osteoarthritis (osteoarthrosis). Anthropometric distinctions. JAMA 1983, 249:1448-1451. 10.1001/jama.1983.03330350024020, 6827721.
61. Wijayaratne SP, Teichtahl AJ, Wluka AE, Hanna F, Bell R, Davis SR, Adams J, Cicuttini FM. The determinants of change in patella cartilage volume - a cohort study of healthy middle-aged women. Rheumatology (Oxford) 2008, 47:1426-1429.
62. Sun HB. Mechanical loading, cartilage degradation, and arthritis. Ann N Y Acad Sci 2010, 1211:37-50. 10.1111/j.1749-6632.2010.05808.x, 21062294.
63. Wilks DC, Winwood K, Gilliver SF, Kwiet A, Chatfield M, Michaelis I, Sun LW, Ferretti JL, Sargeant AJ, Felsenberg D, Rittweger J. Bone mass and geometry of the tibia and the radius of master sprinters, middle and long distance runners, race-walkers and sedentary control participants: a pQCT study. Bone 2009, 45:91-97. 10.1016/j.bone.2009.03.660, 2832729, 19332164.
64. Oettmeier R, Arokoski J, Roth AJ, Helminen HJ, Tammi M, Abendroth K. Quantitative study of articular cartilage and subchondral bone remodeling in the knee joint of dogs after strenuous running training. J Bone Miner Res 1992, 7:S419-S424. 10.1002/jbmr.5650071410, 1485550.
65. Young DR, Richardson DW, Markel MD, Nunamaker DM. Mechanical and morphometric analysis of the third carpal bone of thoroughbreds. Am J Vet Res 1991, 52:402-409.
66. Helminen HJ, Hyttinen MM, Lammi MJ, Arokoski JP, Lapvetelainen T, Jurvelin J, Kiviranta I, Tammi MI. Regular joint loading in youth assists in the establishment and strengthening of the collagen network of articular cartilage and contributes to the prevention of osteoarthrosis later in life: a hypothesis. J Bone Miner Metab 2000, 18:245-257. 10.1007/PL00010638, 10959613.
67. Burr DB, Schaffler MB. The involvement of subchondral mineralized tissues in osteoarthrosis: quantitative microscopic evidence. Microsc Res Tech 1997, 37:343-357. 10.1002/(SICI)1097-0029(19970515)37:4<343::AID-JEMT9>3.0.CO;2-L, 9185156.
68. Radin EL, Burr DB, Fyhrie D, Brown TD, Boyd RD. Characteristics of joint loading as it applies to osteoarthrosis. Biomechanics of Diarthrodial Joints, Volume 1 1990, 437-451. New York: Springer New York, Ratcliffe A, Woo SLY, Mow VC.
69. Colon JL, Bramlage LR, Hance SR, Embertson RM. Qualitative and quantitative documentation of the racing performance of 461 thoroughbred racehorses after arthroscopic removal of dorsoproximal first phalanx osteochondral fractures (1986-1995). Equine Vet J 2000, 32:475-481.
70. Parente EJ, Richardson DW, Spencer P. Basal sesamoidean fractures in horses: 57 cases (1980-1991). J Am Vet Med Assoc 1993, 202:1293-1297.
71. Gelber AC, Hochberg MC, Mead LA, Wang NY, Wigley FM, Klag MJ. Joint injury in young adults and risk for subsequent knee and hip osteoarthritis. Ann Intern Med 2000, 133:321-328. 10.7326/0003-4819-133-5-200009050-00007, 10979876.
72. Furman BD, Strand J, Hembree WC, Ward BD, Guilak F, Olson SA. Joint degeneration following closed intraarticular fracture in the mouse knee: a model of posttraumatic arthritis. J Orthop Res 2007, 25:578-592. 10.1002/jor.20331, 17266145.
73. Mrosek EH, Lahm A, Erggelet C, Uhl M, Kurz H, Eissner B, Schagemann JC. Subchondral bone trauma causes cartilage matrix degeneration: an immunohistochemical analysis in a canine model. Osteoarthritis Cartilage 2006, 14:171-178. 10.1016/j.joca.2005.08.004, 16242359.
74. Hayami T, Pickarski M, Zhuo Y. Characterization of articular cartilage and subchondral bone changes in the rat anterior cruciate ligament transection and meniscectomized models of osteoarthritis. Bone 2006, 38:234-243. 10.1016/j.bone.2005.08.007, 16185945.
75. Boyd SK, Muller R, Leonard T, Herzog W. Long-term periarticular bone adaptation in a feline knee injury model for post-traumatic experimental osteoarthritis. Osteoarthritis Cartilage 2005, 13:235-242. 10.1016/j.joca.2004.11.004, 15727890.
76. Lo GH, Niu J, McLennan CE, Kiel DP, McLean RR, Guermazi A, Genant HK, McAlindon TE, Hunter DJ. Meniscal damage associated with increased local subchondral bone mineral density: a Framingham study. Osteoarthritis Cartilage 2008, 16:261-267. 10.1016/j.joca.2007.07.007, 2278381, 17825586.
77. Wang Y, Wluka AE, Pelletier JP, Martel-Pelletier J, Abram F, Ding C, Cicuttini FM. Meniscal extrusion predicts increases in subchondral bone marrow lesions and bone cysts and expansion of subchondral bone in osteoarthritic knees. Rheumatology (Oxford) 2010, 49:997-1004.
78. Meyer EG, Baumer TG, Slade JM, Smith WE, Haut RC. Tibiofemoral contact pressures and osteochondral microtrauma during anterior cruciate ligament rupture due to excessive compressive loading and internal torque of the human knee. Am J Sports Med 2008, 36:1966-1977. 10.1177/0363546508318046, 18490469.
79. Rubin DA, Harner CD, Costello JM. Treatable chondral injuries in the knee: frequency of associated focal subchondral edema. AJR Am J Roentgenol 2000, 174:1099-1106. 10.2214/ajr.174.4.1741099, 10749260.
80. Brouwer GM, van Tol AW, Bergink AP, Belo JN, Bernsen RM, Reijman M, Pols HA, Bierma-Zeinstra SM. Association between valgus and varus alignment and the development and progression of radiographic osteoarthritis of the knee. Arthritis Rheum 2007, 56:1204-1211. 10.1002/art.22515, 17393449.
81. Heijink A, Gomoll AH, Madry H, Drobnic M, Filardo G, Espregueira-Mendes J, Van Dijk CN. Biomechanical considerations in the pathogenesis of osteoarthritis of the knee. Knee Surg Sports Traumatol Arthrosc 2012, 20:423-435. 10.1007/s00167-011-1818-0, 3282009, 22173730.
82. Kraus VB, McDaniel G, Worrell TW, Feng S, Vail TP, Varju G, Coleman RE. Association of bone scintigraphic abnormalities with knee malalignment and pain. Ann Rheum Dis 2009, 68:1673-1679. 10.1136/ard.2008.094722, 3684623, 18981032.
83. Hunter DJ, Zhang Y, Niu J, Goggins J, Amin S, LaValley MP, Guermazi A, Genant H, Gale D, Felson DT. Increase in bone marrow lesions associated with cartilage loss: a longitudinal magnetic resonance imaging study of knee osteoarthritis. Arthritis Rheum 2006, 54:1529-1535. 10.1002/art.21789, 16646037.
84. Baker-LePain JC, Lane NE. Relationship between joint shape and the development of osteoarthritis. Curr Opin Rheumatol 2010, 22:538-543. 10.1097/BOR.0b013e32833d20ae, 20644480.
85. Herrero-Beaumont G, Roman-Blas JA, Castaneda S, Jimenez SA. Primary osteoarthritis no longer primary: three subsets with distinct etiological, clinical, and therapeutic characteristics. Semin Arthritis Rheum 2009, 39:71-80. 10.1016/j.semarthrit.2009.03.006, 19589561.
86. Jacobsen S, Sonne-Holm S. Hip dysplasia: a significant risk factor for the development of hip osteoarthritis. A cross-sectional survey. Rheumatology (Oxford) 2005, 44:211-218.
87. Swieszkowski W, Tuan BH, Kurzydlowski KJ, Hutmacher DW. Repair and regeneration of osteochondral defects in the articular joints. Biomol Eng 2007, 24:489-495. 10.1016/j.bioeng.2007.07.014, 17931965.
88. Chiba K, Nango N, Kubota S, Okazaki N, Taguchi K, Osaki M, Ito M. Relationship between microstructure and degree of mineralization in subchondral bone of osteoarthritis: a synchrotron radiation microCT study. J Bone Miner Res 2012, 27:1511-1517. 10.1002/jbmr.1609, 22434696.
89. Intema F, Hazewinkel HA, Gouwens D, Bijlsma JW, Weinans H, Lafeber FP, Mastbergen SC. In early OA, thinning of the subchondral plate is directly related to cartilage damage: results from a canine ACLT-meniscectomy model. Osteoarthritis Cartilage 2010, 18:691-698. 10.1016/j.joca.2010.01.004, 20175978.
90. Batiste DL, Kirkley A, Laverty S, Thain LM, Spouge AR, Holdsworth DW. Ex vivo characterization of articular cartilage and bone lesions in a rabbit ACL transection model of osteoarthritis using MRI and micro-CT. Osteoarthritis Cartilage 2004, 12:986-996. 10.1016/j.joca.2004.08.010, 15564066.
91. Radin EL, Paul IL, Tolkoff MJ. Subchondral bone changes in patients with early degenerative joint disease. Arthritis Rheum 1970, 13:400-405. 10.1002/art.1780130406, 4246869.
92. Verborgt O, Gibson GJ, Schaffler MB. Loss of osteocyte integrity in association with microdamage and bone remodeling after fatigue in vivo. J Bone Miner Res 2000, 15:60-67. 10.1359/jbmr.2000.15.1.60, 10646115.
93. Luyten FP, Lories RJ, Verschueren P, de Vlam K, Westhovens R. Contemporary concepts of inflammation, damage and repair in rheumatic diseases. Best Pract Res Clin Rheumatol 2006, 20:829-848. 10.1016/j.berh.2006.06.009, 16980209.
94. Ding M. Microarchitectural adaptations in aging and osteoarthrotic subchondral bone issues. Acta Orthop Suppl 2010, 81:1-53.
95. Li B, Aspden RM. Composition and mechanical properties of cancellous bone from the femoral head of patients with osteoporosis or osteoarthritis. J Bone Miner Res 1997, 12:641-651. 10.1359/jbmr.1997.12.4.641, 9101376.
96. Mansell JP, Bailey AJ. Abnormal cancellous bone collagen metabolism in osteoarthritis. J Clin Invest 1998, 101:1596-1603. 10.1172/JCI867, 508740, 9541489.
97. Day J, Ding M, van der Linden J. A decreased subchondral trabecular bone tissue elastic modulus is associated with pre-arthritic cartilage damage. J Orthop Res 2001, 19:914-918. 10.1016/S0736-0266(01)00012-2, 11562141.
98. Karsdal MA, Leeming DJ, Dam EB, Henriksen K, Alexandersen P, Pastoureau P, Altman RD, Christiansen C. Should subchondral bone turnover be targeted when treating osteoarthritis?. Osteoarthritis Cartilage 2008, 16:638-646. 10.1016/j.joca.2008.01.014, 18362080.
99. Link TM, Steinbach LS, Ghosh S, Ries M, Lu Y, Lane N, Majumdar S. Osteoarthritis: MR imaging findings in different stages of disease and correlation with clinical findings. Radiology 2003, 226:373-381. 10.1148/radiol.2262012190, 12563128.
100. Wluka AE, Hanna F, Davies-Tuck M, Wang Y, Bell RJ, Davis SR, Adams J, Cicuttini FM. Bone marrow lesions predict increase in knee cartilage defects and loss of cartilage volume in middle-aged women without knee pain over 2 years. Ann Rheum Dis 2009, 68:850-855. 10.1136/ard.2008.092221, 18625617.
101. Garnero P, Peterfy C, Zaim S, Schoenharting M. Bone marrow abnormalities on magnetic resonance imaging are associated with type II collagen degradation in knee osteoarthritis: a three-month longitudinal study. Arthritis Rheum 2005, 52:2822-2829. 10.1002/art.21366, 16145678.
102. Wilson AJ, Murphy WA, Hardy DC, Totty WG. Transient osteoporosis: transient bone marrow edema?. Radiology 1988, 167:757-760.
103. Lecouvet FE, van de Berg BC, Maldague BE, Lebon CJ, Jamart J, Saleh M, Noel H, Malghem J. Early irreversible osteonecrosis versus transient lesions of the femoral condyles: prognostic value of subchondral bone and marrow changes on MR imaging. AJR Am J Roentgenol 1998, 170:71-77. 10.2214/ajr.170.1.9423603, 9423603.
104. Hunter DJ, Gerstenfeld L, Bishop G, Davis AD, Mason ZD, Einhorn TA, Maciewicz RA, Newham P, Foster M, Jackson S, Morgan EF. Bone marrow lesions from osteoarthritis knees are characterized by sclerotic bone that is less well mineralized. Arthritis Res Ther 2009, 11:R11. 10.1186/ar2601, 2688243, 19171047.
105. Bergman AG, Willen HK, Lindstrand AL, Pettersson HT. Osteoarthritis of the knee: correlation of subchondral MR signal abnormalities with histopathologic and radiographic features. Skeletal Radiol 1994, 23:445-448.
106. Zanetti M, Bruder E, Romero J, Hodler J. Bone marrow edema pattern in osteoarthritic knees: correlation between MR imaging and histologic findings. Radiology 2000, 215:835-840. 10.1148/radiology.215.3.r00jn05835, 10831707.
107. Kazakia GJ, Kuo D, Schooler J, Siddiqui S, Shanbhag S, Bernstein G, Horvai A, Majumdar S, Ries M, Li X. Bone and cartilage demonstrate changes localized to bone marrow edema-like lesions within osteoarthritic knees. Osteoarthritis Cartilage 2013, 21:94-101. 10.1016/j.joca.2012.09.008, 23025926.
108. Nolte-Ernsting CC, Adam G, Buhne M, Prescher A, Gunther RW. MRI of degenerative bone marrow lesions in experimental osteoarthritis of canine knee joints. Skeletal Radiol 1996, 25:413-420. 10.1007/s002560050108, 8837271.
109. Baird DK, Hathcock JT, Kincaid SA, Rumph PF, Kammermann J, Widmer WR, Visco D, Sweet D. Low-field magnetic resonance imaging of early subchondral cyst-like lesions in induced cranial cruciate ligament deficient dogs. Vet Radiol Ultrasound 1998, 39:167-173. 10.1111/j.1740-8261.1998.tb00334.x, 9634181.
110. Martig S, Boisclair J, Konar M, Spreng D, Lang J. MRI characteristics and histology of bone marrow lesions in dogs with experimentally induced osteoarthritis. Vet Radiol Ultrasound 2007, 48:105-112. 10.1111/j.1740-8261.2007.00213.x, 17385365.
111. Zhao J, Li X, Bolbos RI, Link TM, Majumdar S. Longitudinal assessment of bone marrow edema-like lesions and cartilage degeneration in osteoarthritis using 3 T MR T1rho quantification. Skeletal Radiol 2010, 39:523-531. 10.1007/s00256-010-0892-6, 2929817, 20195865.
112. Carrino JA, Blum J, Parellada JA, Schweitzer ME, Morrison WB. MRI of bone marrow edema-like signal in the pathogenesis of subchondral cysts. Osteoarthritis Cartilage 2006, 14:1081-1085. 10.1016/j.joca.2006.05.011, 16806996.
113. Tanamas SK, Wluka AE, Pelletier JP, Martel-Pelletier J, Abram F, Wang Y, Cicuttini FM. The association between subchondral bone cysts and tibial cartilage volume and risk of joint replacement in people with knee osteoarthritis: a longitudinal study. Arthritis Res Ther 2010, 12:R58. 10.1186/ar2971, 2888209, 20356405.
114. Plewes LW. Osteo-arthritis of the hip. Br J Surg 1940, 27:682-695.
115. Durr HD, Martin H, Pellengahr C, Schlemmer M, Maier M, Jansson V. The cause of subchondral bone cysts in osteoarthrosis: a finite element analysis. Acta Orthop Scand 2004, 75:554-558. 10.1080/00016470410001411, 15513486.
116. Ondrouch AS. Cyst formation in osteoarthritis. J Bone Joint Surg Br 1963, 45:755-760.
117. Bancroft LW, Peterson JJ, Kransdorf MJ. Cysts, geodes, and erosions. Radiol Clin North Am 2004, 42:73-87. 10.1016/S0033-8389(03)00165-9, 15049524.
118. Resnick D, Niwayama G, Coutts RD. Subchondral cysts (geodes) in arthritic disorders: pathologic and radiographic appearance of the hip joint. AJR Am J Roentgenol 1977, 128:799-806. 10.2214/ajr.128.5.799, 404905.
119. Havdrup T, Hulth A, Telhag H. The subchondral bone in osteoarthritis and rheumatoid arthritis of the knee. A histological and microradiographical study. Acta Orthop Scand 1976, 47:345-350. 10.3109/17453677608992003, 952224.
120. Sabokbar A, Crawford R, Murray DW, Athanasou NA. Macrophage-osteoclast differentiation and bone resorption in osteoarthrotic subchondral acetabular cysts. Acta Orthop Scand 2000, 71:255-261. 10.1080/000164700317411843, 10919296.
121. Vener MJ, Thompson RC, Lewis JL, Oegema TR. Subchondral damage after acute transarticular loading: an in vitro model of joint injury. J Orthop Res 1992, 10:759-765. 10.1002/jor.1100100603, 1403288.
122. Herman BC, Cardoso L, Majeska RJ, Jepsen KJ, Schaffler MB. Activation of bone remodeling after fatigue: differential response to linear microcracks and diffuse damage. Bone 2010, 47:766-772. 10.1016/j.bone.2010.07.006, 2939191, 20633708.
123. Kawcak CE, McIlwraith CW, Norrdin RW, Park RD, James SP. The role of subchondral bone in joint disease: a review. Equine Vet J 2001, 33:120-126.
124. Fazzalari NL, Kuliwaba JS, Forwood MR. Cancellous bone microdamage in the proximal femur: influence of age and osteoarthritis on damage morphology and regional distribution. Bone 2002, 31:697-702. 10.1016/S8756-3282(02)00906-7, 12531564.
125. Vashishth D, Koontz J, Qiu SJ, Lundin-Cannon D, Yeni YN, Schaffler MB, Fyhrie DP. In vivo diffuse damage in human vertebral trabecular bone. Bone 2000, 26:147-152. 10.1016/S8756-3282(99)00253-7, 10678409.