The role of osteocytes and bone microstructure in preventing osteoporotic fractures

Osteoporosis International

Volumn 18, Issue 1, 2007, Pages 1-8

  Hazenberg, Jan G ^a   Taylor, David ^b   Lee, T Clive ^a,b  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Bone adaptation; Microdamage; Osteocytes; Osteoporotic fracture; RANKL

Indexed keywords

BIOCHEMISTRY; BONE DENSITY; BONE INJURY; BONE METABOLISM; BONE REMODELING; BONE STRUCTURE; FRAGILITY FRACTURE; HUMAN; OSTEOCYTE; PRIORITY JOURNAL; REVIEW; SCANNING ELECTRON MICROSCOPY; SIGNAL TRANSDUCTION;

BONE AND BONES; BONE REMODELING; FRACTURES, BONE; HUMANS; OSTEOCYTES; OSTEOPOROSIS; SIGNAL TRANSDUCTION;

EID: 33845426897     PISSN: 0937941X     EISSN: 14332965     Source Type: Journal    
DOI: 10.1007/s00198-006-0222-y     Document Type: Review

References (89)

1. Wenzel TE, Schaffler MB, Fyhrie DP (1996) In vivo trabecular microcracks in human vertebral bone. Bone 19:89-95
2. Aloia JF, Vaswani A, Delerme-Pagan C, Flaster E (1998) Discordance between ultrasound of the calcaneus and bone mineral density in black and white women. Calcif Tissue Int 62:481-485
3. Seeman E, Bianchi G, Adami S, Kanis J, Khosla S, Orwoll E (2004) Osteoporosis in men-consensus is premature. Calcif Tissue Int 75:120-122
4. Lewiecki EM (2004) Management of osteoporosis. Clin Mol Allergy 2:9
5. Riggs BL, Melton LJ 3rd (1995) The worldwide problem of osteoporosis: insights afforded by epidemiology. Bone 17:505S-511S
6. Frost HM (1960) Presence of microscopic cracks in vivo in bone. Henry Ford Hosp Bull 8:25-35
7. Burr DB, Stafford T (1990) Validity of the bulk-staining technique to separate artifactual from in vivo bone microdamage. Clin Orthop 305-308
8. Lee TC, Myers ER, Hayes WC (1998) Fluorescence-aided detection of microdamage in compact bone. J Anat 193(Pt 2):179-184
9. O'Brien FJ, Taylor D, Dickson GR, Lee TC (2000) Visualisation of three-dimensional microcracks in compact bone. J Anat 197 (Pt 3):413-420
10. Norman TL, Vashishth D, Burr DB (1995) Fracture toughness of human bone under tension. J Biomech 28:309-320
11. Yeni YN, Brown CU, Wang Z, Norman TL (1997) The influence of bone morphology on fracture toughness of the human femur and tibia. Bone 21:453-459
12. Feng Z, Rou J, Han S, Ziv I (2000) Orientation and loading condition dependence of fracture toughness in cortical bone. Mater Sci Eng C 11:41-46
13. Zioupos P, X TW, Currey JD (1996) The accumulation of fatigue microdamage in human cortical bone of two different ages in vitro. Clin Biomech (Bristol, Avon) 11:365-375
14. Lee TC, Arthur TL, Gibson LJ, Hayes WC (2000) Sequential labelling of microdamage in bone using chelating agents. J Orthop Res 18:322-325
15. O'Brien FJ, Taylor D, Lee TC (2003) Microcrack accumulation at different intervals during fatigue testing of compact bone. J Biomech 36:973-980
16. Burr DB, Martin RB (1993) Calculating the probability that microcracks initiate resorption spaces. J Biomech 26:613-616
17. Reilly GC, Currey JD (1999) The development of microcracking and failure in bone depends on the loading mode to which it is adapted. J Exp Biol 202(Pt 5):543-552
18. Reilly GC (2000) Observations of microdamage around osteocyte lacunae in bone. J Biomech 33:1131-1134
19. Carter DR, Hayes WC (1977) Compact bone fatigue damage: a microscopic examination. Clin Orthop 265-274
20. Vashishth D, Behiri JC, Bonfield W (1997) Crack growth resistance in cortical bone: concept of microcrack toughening. J Biomech 30:763-769
21. Mohsin S, O'Brien FJ, Lee TC (2006) Osteonal crack barriers in ovine compact bone. J Anat 208:81-89
22. Schaffler MB, Choi K, Milgrom C (1995) Aging and matrix microdamage accumulation in human compact bone. Bone 17:521-525
23. Norman TL, Wang Z (1997) Microdamage of human cortical bone: incidence and morphology in long bones. Bone 20:375-379
24. O'Brien FJ, Taylor D, Lee TC (2002) An improved labelling technique for monitoring microcrack growth in compact bone. J Biomech 35:523-526
25. Martin RB, Burr DB (1982) A hypothetical mechanism for the stimulation of osteonal remodelling by fatigue damage. J Biomech 15:137-139
26. Akkus O, Rimnac CM (2001) Cortical bone tissue resists fatigue fracture by deceleration and arrest of microcrack growth. J Biomech 34:757-764
27. Hazenberg JG, Taylor D, Lee TC (2006) Mechanisms of short crack growth at constant stress in bone. Biomaterials 27:2114-2122
28. Nalla RK, Kinney JH, Ritchie RO (2003) Effect of orientation on the in vitro fracture toughness of dentin: the role of toughening mechanisms. Biomaterials 24:3955-3968
29. Nalla RK, Kinney JH, Ritchie RO (2003) Mechanistic fracture criteria for the failure of human cortical bone. Nat Mater 2:164-168
30. Nalla RK, Kruzic JJ, Ritchie RO (2004) On the origin of the toughness of mineralized tissue: microcracking or crack bridging? Bone 34:790-798
31. Malik CL, Stover SM, Martin RB, Gibeling JC (2003) Equine cortical bone exhibits rising R-curve fracture mechanics. J Biomech 36:191-198
32. Nalla RK, Kruzic JJ, Kinney JH, Ritchie RO (2005) Mechanistic aspects of fracture and R-curve behavior in human cortical bone. Biomaterials 26:217-231
33. Vashishth D, Koontz J, Qiu SJ, Lundin-Cannon D, Yeni YN, Schaffler MB, Fyhrie DP (2000) In vivo diffuse damage in human vertebral trabecular bone. Bone 26:147-152
34. Vashishth D, Tanner KE, Bonfield W (2003) Experimental validation of a microcracking-based toughening mechanism for cortical bone. J Biomech 36:121-124
35. Vashishth D (2004) Rising crack-growth-resistance behavior in cortical bone: implications for toughness measurements. J Biomech 37:943-946
36. Ritchie RO (1988) Mechanisms of fatigue crack propagation in metals, ceramics and composites: role of crack-tip shielding. Mater Sci Eng A 103:15-28
37. Yeni YN, Fyhrie DP (2003) A rate-dependent microcrackbridging model that can explain the strain rate dependency of cortical bone apparent yield strength. J Biomech 36:1343-1353
38. Hazenberg JG, Taylor D, Clive Lee T (2006) Mechanisms of short crack growth at constant stress in bone. Biomaterials 27:2114-2122
39. Frost HM (1987) Bone "mass" and the "mechanostat": a proposal. Anat Rec 219:1-9
40. Palumbo C, Palazzini S, Marotti G (1990) Morphological study of intercellular junctions during osteocyte differentiation. Bone 11:401-406
41. Viceconti M, Seireg A (1990) A generalized procedure for predicting bone mass regulation by mechanical strain. Calcif Tissue Int 47:296-301
42. Prendergast PJ, Taylor D (1994) Prediction of bone adaptation using damage accumulation. J Biomech 27:1067-1076
43. Martin RB, Stover SM, Gibson VA, Gibeling JC, Griffin LV (1996) In vitro fatigue behaviour of the equine third metacarpus: remodeling and microcrack damage analysis. J Orthop Res 14:794-801
44. Burr DB, Forwood MR, Fyhrie DP, Martin RB, Schaffler MB, Turner CH (1997) Bone microdamage and skeletal fragility in osteoporotic and stress fractures. J Bone Miner Res 12:6-15
45. Bentolila V, Boyce TM, Fyhrie DP, Drumb R, Skerry TM, Schaffler MB (1998) Intracortical remodeling in adult rat long bones after fatigue loading. Bone 23:275-281
46. Sissons HA, O'Connor P (1977) Quantitative histology of osteocyte lacunae in normal human cortical bone. Calcif Tissue Res 22 (Suppl):530-533
47. Qin L, Mak AT, Cheng CW, Hung LK, Chan KM (1999) Histomorphological study on pattern of fluid movement in cortical bone in goats. Anat Rec 255:380-387
48. Marotti G, Ferretti M, Muglia MA, Palumbo C, Palazzini S (1992) A quantitative evaluation of osteoblast-osteocyte relationships on growing endosteal surface of rabbit tibiae. Bone 13:363-368
49. Martin RB (2000) Does osteocyte formation cause the nonlinear refilling of osteons? Bone 26:71-78
50. Metz LN, Martin RB, Turner AS (2003) Histomorphometric analysis of the effects of osteocyte density on osteonal morphology and remodeling. Bone 33:753-759
51. Kusuzaki K, Kageyama N, Shinjo H, Takeshita H, Murata H, Hashiguchi S, Ashihara T, Hirasawa Y (2000) Development of bone canaliculi during bone repair. Bone 27:655-659
52. Parfitt AM (1984) The cellular basis of bone remodeling: the quantum concept reexamined in light of recent advances in the cell biology of bone. Calcif Tissue Int 36(Suppl 1):S37-S45
53. Hernandez CJ, Majeska RJ, Schaffler MB (2004) Osteocyte density in woven bone. Bone 35:1095-1099
54. Tanaka-Kamioka K, Kamioka H, Ris H, Lim SS (1998) Osteocyte shape is dependent on actin filaments and osteocyte processes are unique actin-rich projections. J Bone Miner Res 13:1555-1568
55. Kamioka H, Honjo T, Takano-Yamamoto T (2001) A three-dimensional distribution of osteocyte processes revealed by the combination of confocal laser scanning microscopy and differential interference contrast microscopy. Bone 28:145-149
56. Sugawara Y, Kamioka H, Honjo T, Tezuka K, Takano-Yamamoto T (2005) Three-dimensional reconstruction of chick calvarial osteocytes and their cell processes using confocal microscopy. Bone 36:877-883
57. You LD, Weinbaum S, Cowin SC, Schaffler MB (2004) Ultrastructure of the osteocyte process and its pericellular matrix. Anat Rec 278A:505-513
58. Cho H, Stout SD, Madsen RW, Streeter MA (2002) Population-specific histological age-estimating method: a model for known African-American and European-American skeletal remains. J Forensic Sci 47:12-18
59. Qiu S, Rao DS, Palnitkar S, Parfitt AM (2005) Differences in osteocyte and lacunar density between Black and White American women. Bone
60. Beck TJ, Ruff CB, Shaffer RA, Betsinger K, Trone DW, Brodine SK (2000) Stress fracture in military recruits: gender differences in muscle and bone susceptibility factors. Bone 27:437-444
61. Martin RB (1995) Mathematical model for repair of fatigue damage and stress fracture in osteonal bone. J Orthop Res 13:309-316
62. Qiu S, Sudhaker Rao D, Fyhrie DP, Palnitkar S, Parfitt AM (2005) The morphological association between microcracks and osteocyte lacunae in human cortical bone. Bone 37:10-15
63. Hsieh YF, Turner CH (2001) Effects of loading frequency on mechanically induced bone formation. J Bone Miner Res 16:918-924
64. Lee KC, Maxwell A, LE Lanyon (2002) Validation of a technique for studying functional adaptation of the mouse ulna in response to mechanical loading. Bone 31:407-412
65. Turner CH, Owan I, Takano Y (1995) Mechanotransduction in bone: role of strain rate. Am J Physiol 269:E438-E442
66. Taylor D, Hazenberg JG, Lee TC (2003) The cellular transducer in damage-stimulated bone remodelling: a theoretical investigation using fracture mechanics. J Theor Biol 225:65-75
67. Noble BS, Reeve J (2000) Osteocyte function, osteocyte death and bone fracture resistance. Mol Cell Endocrinol 159:7-13
68. Verborgt O, Gibson GJ, Schaffler MB (2000) Loss of osteocyte integrity in association with microdamage and bone remodeling after fatigue in vivo. J Bone Miner Res 15:60-67
69. Noble BS, Peet N, Stevens HY, Brabbs A, Mosley JR, Reilly GC, Reeve J, Skerry TM, Lanyon LE (2003) Mechanical loading: biphasic osteocyte survival and targeting of osteoclasts for bone destruction in rat cortical bone. Am J Physiol Cell Physiol 284:C934-C943
70. Shimizu H, Sakamoto M, Sakamoto S (1990) Bone resorption by isolated osteoclasts in living versus devitalized bone: differences in mode and extent and the effects of human recombinant tissue inhibitor of metalloproteinases. J Bone Miner Res 5:411-418
71. Maejima-Ikeda A, Aoki M, Tsuritani K, Kamioka K, Hiura K, Miyoshi T, Hara H, Takano-Yamamoto T, Kumegawa M (1997) Chick osteocyte-derived protein inhibits osteoclastic bone resorption. Biochem J 322(Pt 1):245-250
72. Plotkin LI, Weinstein RS, Parfitt AM, Roberson PK, Manolagas SC, Bellido T (1999) Prevention of osteocyte and osteoblast apoptosis by bisphosphonates and calcitonin. J Clin Invest 104:1363-1374
73. Kogianni G, Mann V, Ebetino F, Nuttall M, Nijweide P, Simpson H, Noble B (2004) Fas/CD95 is associated with glucocorticoid-induced osteocyte apoptosis. Life Sci 75:2879-2895
74. Liu Y, Porta A, Peng X, Gengaro K, Cunningham EB, Li H, Dominguez LA, Bellido T, Christakos S (2004) Prevention of glucocorticoid-induced apoptosis in osteocytes and osteoblasts by calbindin-D28k. J Bone Miner Res 19:479-490
75. Gu G, Mulari M, Peng Z, Hentunen TA, Vaananen HK (2005) Death of osteocytes turns off the inhibition of osteoclasts and triggers local bone resorption. Biochem Biophys Res Commun 335:1095-1101
76. Hazenberg JG, Freeley M, Foran E, Lee TC, Taylor D (2005) Microdamage: A cell transducing mechanism based on ruptured osteocyte processes. J Biomech
77. Bonewald LF (1999) Establishment and characterization of an osteocyte-like cell line, MLO-Y4. J Bone Miner Metab 17:61-65
78. Simmons ED Jr, Pritzker KP, Grynpas MD (1991) Age-related changes in the human femoral cortex. J Orthop Res 9:155-167
79. Machwate M, Zerath E, Holy X, Pastoureau P, Marie PJ (1994) Insulin-like growth factor-I increases trabecular bone formation and osteoblastic cell proliferation in unloaded rats. Endocrinology 134:1031-1038
80. Burger EH, Klein-Nulend J (1999) Mechanotransduction in bone: role of the lacuno-canalicular network. FASEB J 13(Suppl):S101-S112
81. Pensler JM, Patel PK, Langman CB (1997) Osteoblast-directed osteoclast metabolism from patients with premature coronal synostosis. Plast Reconstr Surg 99:1518-1521
82. Gay CV, Gilman VR, Sugiyama T (2000) Perspectives on osteoblast and osteoclast function. Poult Sci 79:1005-1008
83. Shimoaka T, Ogasawara T, Yonamine A, Chikazu D, Kawano H, Nakamura K, Itoh N, Kawaguchi H (2002) Regulation of osteoblast, chondrocyte, and osteoclast functions by fibroblast growth factor (FGF)-18 in comparison with FGF-2 and FGF-10. J Biol Chem 277:7493-7500
84. Phan TC, Xu J, Zheng MH (2004) Interaction between osteoblast and osteoclast: impact in bone disease. Histol Histopathol 19:1325-1344
85. Horowitz MC, Bothwell AL, Hesslein DG, Pflugh DL, Schatz DG (2005) B cells and osteoblast and osteoclast development. Immunol Rev 208:141-153
86. Kurata K, Heino HJ, Higaki H, Vaananen HK (2006) Bone marrow cell differentiation induced by mechanically damaged osteocytes in 3D gel-embedded culture. J Biomed Mater Res 21:616-625
87. Currey JD, Brear K, Zioupos P (1996) The effects of ageing and changes in mineral content in degrading the toughness of human femora. J Biomech 29:257-260
88. Burr DB, Milgrom C, Boyd RD, Higgins WL, Robin G, Radin EL (1990) Experimental stress fractures of the tibia. Biological and mechanical aetiology in rabbits. J Bone Joint Surg Br 72:370-375
89. Hazenberg JG, Freeley M, Foran E, Lee TC, Taylor D (2006) Microdamage: a cell transducing mechanism based on ruptured osteocyte processes. J Biomech 39:2096-2103