Micro-morphological properties of osteons reveal changes in cortical bone stability during aging, osteoporosis, and bisphosphonate treatment in women

Osteoporosis International

Volumn 24, Issue 10, 2013, Pages 2671-2680

  Bernhard, A ^a   Milovanovic, P ^a,b   Zimmermann, E A ^a,c   Hahn, M ^a   Djonic, D ^b   Krause, M ^a   Breer, S ^a   Puschel K ^a   Djuric, M ^b   Amling, M ^a   Busse, B ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF BELGRADE   (Serbia)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cortical bone; Femur; Individual osteon's stability; Osteocyte lacunae; Osteonal morphometry

Indexed keywords

BISPHOSPHONIC ACID DERIVATIVE;

ACCIDENT; ADULT; AGED; AGING; ARTICLE; ASSAULT; AUTOPSY; BONE DENSITY; BONE REMODELING; BONE STRENGTH; CADAVER DONOR; COMPRESSION; CONTROLLED STUDY; CORTICAL BONE; DIAPHYSIS; DUAL ENERGY X RAY ABSORPTIOMETRY; FEMALE; FRACTURE; HAVERSIAN CANAL; HUMAN; HUMAN CELL; MORPHOLOGICAL TRAIT; OSTEOCYTE; OSTEOPOROSIS; PRIORITY JOURNAL; TRAFFIC ACCIDENT;

ADULT; AGED; AGED, 80 AND OVER; AGING; BONE DENSITY CONSERVATION AGENTS; BONE REMODELING; DIPHOSPHONATES; FEMALE; FEMUR; HAVERSIAN SYSTEM; HUMANS; OSTEOCYTES; OSTEOPOROSIS, POSTMENOPAUSAL; SPECIMEN HANDLING; STRESS, MECHANICAL;

EID: 84885425357     PISSN: 0937941X     EISSN: 14332965     Source Type: Journal    
DOI: 10.1007/s00198-013-2374-x     Document Type: Article

References (60)

1. Cooper C, Campion G, Melton LJ (1992) Hip fractures in the elderly: a world-wide projection. Osteoporos Int 2:285-289
2. Cole Z, Dennison E, Cooper C (2008) Osteoporosis epidemiology update. Curr Rheum Rep 10:92-96
3. Burge R, Dawson-Hughes B, Solomon DH, Wong JB, King A, Tosteson A (2007) Incidence and economic burden of osteoporosis-related fractures in the United States, 2005-2025. J Bone Miner Res 22:465-475
4. Milovanovic P, Djonic D, Marshall RP, Hahn M, Nikolic S, Zivkovic V, Amling M, Djuric M (2012) Micro-structural basis for particular vulnerability of the superolateral neck trabecular bone in the postmenopausal women with hip fractures. Bone 50:63-68
5. Mayhew PM, Thomas CD, Clement JG, Loveridge N, Beck TJ, Bonfield W, Burgoyne CJ, Reeve J (2005) Relation between age, femoral neck cortical stability, and hip fracture risk. Lancet 366:129-135
6. Busse B, Hahn M, Schinke T, Püschel K, Duda GN, Amling M (2010) Reorganization of the femoral cortex due to age-, sex-, and endoprosthetic- related effects emphasized by osteonal dimensions and remodeling. J Biomed Mater Res A 92A:1440-1451
7. Currey JD (2002) Bones: structure and mechanics. Princeton University Press, Princeton
8. Skedros JG, Clark GC, Sorenson SM, Taylor KW, Qiu S (2011) Analysis of the effect of osteon diameter on the potential relationship of osteocyte lacuna density and osteon wall thickness. Anat Rec A 294:1472-1485
9. Rauch F, Travers R, Glorieux FH (2007) Intracortical remodeling during human bone development - a histomorphometric study. Bone 40:274-280
10. Metz LN, Martin RB, Turner AS (2003) Histomorphometric analysis of the effects of osteocyte density on osteonal morphology and remodeling. Bone 33:753-759
11. Thomas CDL, Stein MS, Feik SA, Wark JD, Clement JG (2000) Determination of age at death using combined morphology and histology of the femur. J Anat 196:463-471
12. Ascenzi M-G, Liao VP, Lee BM, Billi F, Zhou H, Lindsay R, Cosman F, Nieves J, Bilezikian JP, Dempster DW (2012) Parathyroid hormone treatment improves the cortical bone microstructure by improving the distribution of type I collagen in postmenopausal women with osteoporosis. J Bone Miner Res 27:702-712
13. Britz HM, Thomas CDL, Clement JG, Cooper DML (2009) The relation of femoral osteon geometry to age, sex, height and weight. Bone 45:77-83
14. Barth RW, Williams JL, Kaplan FS (1992) Osteon morphometry in females with femoral neck fractures. Clin Orthop Relat Res 283:178-186
15. Beck TJ, Looker AC, Ruff CB, Sievanen H, Wahner HW (2000) Structural trends in the aging femoral neck and proximal shaft: analysis of the Third National Health and Nutrition Examination Survey dual-energy X-ray absorptiometry data. J Bone Miner Res 15:2297-2304
16. Beck TJ, Ruff CB, Warden KE, Scott WW Jr, Rao GU (1990) Predicting femoral neck strength from bone mineral data. A structural approach. Invest Radiol 25:6-18
17. Seeman E (2008) Structural basis of growth-related gain and age-related loss of bone strength. Rheumatology 47:iv2-iv8
18. Marotti G (1996) The structure of bone tissues and the cellular control of their deposition. Ital J Anat Embryol 101:25-79
19. Power J, Doube M, van Bezooijen RL, Loveridge N, Reeve J (2012) Osteocyte recruitment declines as the osteon fills in: interacting effects of osteocytic sclerostin and previous hip fracture on the size of cortical canals in the femoral neck. Bone 50:1107-1114
20. Qiu S, Rao DS, Palnitkar S, Parfitt AM (2010) Dependence of bone yield (volume of bone formed per unit of cement surface area) on resorption cavity size during osteonal remodeling in human rib: implications for osteoblast function and the pathogenesis of age-related bone loss. J Bone Miner Res 25:423-430
21. Skedros JG, Kiser CJ, Keenan KE, Thomas SC (2011) Analysis of osteon morphotype scoring schemes for interpreting load history: evaluation in the chimpanzee femur. J Anat 218:480-499
22. Hahn M, Vogel M, Delling G (1991) Undecalcified preparation of bone tissue: report of technical experience and development of new methods. Virchows Arch A Pathol Anat Histopathol 418:1-7
23. Donath K, Breuner G (1982) A method for the study of undecalcified bones and teeth with attached soft tissues. The Säge-Schliff (sawing and grinding) technique. J Oral Pathol 11:318-326
24. Busse B, Djonic D, Milovanovic P, Hahn M, Püschel K, Ritchie RO, Djuric M, Amling M (2010) Decrease in the osteocyte lacunar density accompanied by hypermineralized lacunar occlusion reveals failure and delay of remodeling in aged human bone. Aging Cell 9:1065-1075
25. Bell KL, Loveridge N, Jordan GR, Power J, Constant CR, Reeve J (2000) A novel mechanism for induction of increased cortical porosity in cases of intracapsular hip fracture. Bone 27:297-304
26. Jordan GR, Loveridge N, Bell KL, Power J, Rushton N, Reeve J (2000) Spatial clustering of remodeling osteons in the femoral neck cortex: a cause of weakness in hip fracture? Bone 26:305-313
27. Dempster DW, Compston JE, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR, Parfitt AM (2013) Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 28:2-17
28. Currey J (2012) The structure and mechanics of bone. J Mater Sci 47:41-54
29. Guo XE, Liang LC, Goldstein SA (1998) Micromechanics of osteonal cortical bone fracture. J Biomech Eng 120:112-117
30. Bigley RF, Griffin LV, Christensen L, Vandenbosch R (2006) Osteon interfacial strength and histomorphometry of equine cortical bone. J Biomech 39:1629-1640
31. Chavassieux PM, Arlot ME, Reda C, Wei L, Yates AJ, Meunier PJ (1997) Histomorphometric assessment of the long-term effects of alendronate on bone quality and remodeling in patients with osteoporosis. J Clin Invest 100:1475-1480
32. Burr DB, Diab T, Koivunemi A, Koivunemi M, Allen MR (2009) Effects of 1 to 3 years' treatment with alendronate on mechanical properties of the femoral shaft in a canine model: implications for subtrochanteric femoral fracture risk. J Orthop Res 27:1288-1292
33. Faingold A, Cohen SR, Wagner HD (2012) Nanoindentation of osteonal bone lamellae. J Mech Behav Biomed Mater 9:198-206
34. Wu Y, Bergot C, Jolivet E, Zhou LQ, Laredo J-D, Bousson V (2009) Cortical bone mineralization differences between hip-fractured females and controls. A microradiographic study. Bone 45:207-212
35. Bergot C, Wu Y, Jolivet E, Zhou LQ, Laredo JD, Bousson V (2009) The degree and distribution of cortical bone mineralization in the human femoral shaft change with age and sex in a microradiographic study. Bone 45:435-442
36. Bala Y, Depalle B, Douillard T, Meille S, Clément P, Follet H, Chevalier J, Boivin G (2011) Respective roles of organic and mineral components of human cortical bone matrix in micromechanical behavior: an instrumented indentation study. J Mech Behav Biomed Mater 4:1473-1482
37. Giraud-Guille MM (1988) Twisted plywood architecture of collagen fibrils in human compact bone osteons. Calcif Tissue Int 42:167-180
38. Ascenzi A, Bonucci E (1968) The compressive properties of single osteons. Anat Rec 161:377-391
39. Gamsjaeger S, Buchinger B, Zwettler E, Recker R, Black D, Gasser JA, Eriksen EF, Klaushofer K, Paschalis EP (2011) Bone material properties in actively bone-forming trabeculae in postmenopausal women with osteoporosis after three years of treatment with once-yearly Zoledronic acid. J Bone Miner Res 26:12-18
40. Bala Y, Depalle B, Farlay D, Douillard T, Meille S, Follet H, Chapurlat R, Chevalier J, Boivin G (2012) Bone micromechanical properties are compromised during long-term alendronate therapy independently of mineralization. J Bone Miner Res 27:825-834
41. Hazenberg J, Taylor D, Lee T (2007) The role of osteocytes and bone microstructure in preventing osteoporotic fractures. Osteoporos Int 18:1-8
42. Zimmermann EA, Schaible E, Bale H, Barth HD, Tang SY, Reichert P, Busse B, Alliston T, Ager JW, Ritchie RO (2011) Age-related changes in the plasticity and toughness of human cortical bone at multiple length scales. Proc Natl Acad Sci USA 108:14416-14421
43. Ritchie RO (2011) The conflicts between strength and toughness. Nat Mater 10:817-822
44. Barth HD, Zimmermann EA, Schaible E, Tang SY, Alliston T, Ritchie RO (2011) Characterization of the effects of X-ray irradiation on the hierarchical structure and mechanical properties of human cortical bone. Biomaterials 32:8892-8904
45. Burger EH, Klein-Nulend J (1999) Mechanotransduction in bone - role of the lacuno-canalicular network. FASEB J 13:101-112
46. Vashishth D, Verborgt O, Divine G, Schaffler MB, Fyhrie DP (2000) Decline in osteocyte lacunar density in human cortical bone is associated with accumulation of microcracks with age. Bone 26:375-380
47. Duque G, Troen BR (2008) Understanding the mechanisms of senile osteoporosis: new facts for a major geriatric syndrome. J Am Geriatr Soc 56:935-941
48. Russell RG (2011) Bisphosphonates: the first 40 years. Bone 49:2-19
49. Allen MR, Burr DB (2011) Bisphosphonate effects on bone turnover, microdamage, and mechanical properties: what we think we know and what we know that we don't know. Bone 49:56-65
50. Saag K, Lindsay R, Kriegman A, Beamer E, Zhou W (2007) A single zoledronic acid infusion reduces bone resorption markers more rapidly than weekly oral alendronate in postmenopausal women with low bone mineral density. Bone 40:1238-1243
51. Dempster DW, Zhou H, Recker RR, Brown JP, Bolognese MA, Recknor CP, Kendler DL, Lewiecki EM, Hanley DA, Rao DS, Miller PD, Woodson GC, Lindsay R, Binkley N, Wan X, Ruff VA, Janos B, Taylor KA (2012) Skeletal Histomorphometry in subjects on teriparatide or zoledronic acid therapy (SHOTZ) study: a randomized controlled trial. J Clin Endocrinol Metab 97:2799-2808
52. Black DM, Schwartz AV, Ensrud K, Cauley J, Levis S, Quandt SA, Satterfield S, Wallace RB, Bauer DC, Palermo L, Wehren LE, Lombardi A, Santora AC, Cummings SR (2006) Effects of continuing or stopping alendronate after 5 years of treatment: the fracture intervention trial long-term extension (flex): a randomized trial. J Am Med Assoc 296:2927-2938
53. McClung M, Recker R, Miller P, Fiske D, Minkoff J, Kriegman A, Zhou W, Adera M, Davis J (2007) Intravenous zoledronic acid 5 mg in the treatment of postmenopausal women with low bone density previously treated with alendronate. Bone 41:122-128
54. Devogelaer JP, Broll H, Correa-Rotter R, Cumming DC, Nagant de Deuxchaisnes C, Geusens P, Hosking D, Jaeger P, Kaufman JM, Leite M, Leon J, Liberman U, Menkes CJ, Meunier PJ, Reid I, Rodriguez J, Romanowicz A, Seeman E, Vermeulen A, Hirsch LJ, Lombardi A, Plezia K, Santora AC, Yates AJ, Yuan W (1996) Oral alendronate induces progressive increases in bone mass of the spine, hip, and total body over 3 years in postmenopausal women with osteoporosis. Bone 18:141-150
55. Bone HG, Hosking D, Devogelaer J-P, Tucci JR, Emkey RD, Tonino RP, Rodriguez-Portales JA, Downs RW, Gupta J, Santora AC, Liberman UA (2004) Ten years' experience with alendronate for osteoporosis in postmenopausal women. N Engl J Med 350:1189-1199
56. Martin RB (2000) Toward a unifying theory of bone remodeling. Bone 26:1-6
57. Qiu S, Rao DS, Palnitkar S, Parfitt AM (2002) Relationships between osteocyte density and bone formation rate in human cancellous bone. Bone 31:709-711
58. Pazzaglia UE, Congiu T, Franzetti E, Marchese M, Spagnuolo F, Di Mascio L, Zarattini G (2012) A model of osteoblast-osteocyte kinetics in the development of secondary osteons in rabbits. J Anat 220:372-383
59. Skedros JG, Keenan KE, Williams TJ, Kiser CJ (2013) Secondary osteon size and collagen/lamellar organization ("osteon morphotypes") are not coupled, but potentially adapt independently for local strain mode or magnitude. J Struct Biol 181:95-107
60. Simões JA, Vaz MA, Blatcher S, Taylor M (2000) Influence of head constraint and muscle forces on the strain distribution within the intact femur. Med Eng Phys 22:453-459