Bone micromechanical properties are compromised during long-term alendronate therapy independently of mineralization

Journal of Bone and Mineral Research

Volumn 27, Issue 4, 2012, Pages 825-834

  Bala, Yohann ^a,b   Depalle, Baptiste ^a,b   Farlay, Delphine ^a,b   Douillard, Thierry ^b,c   Meille, Sylvain ^b,c   Follet, Helene ^a,b   Chapurlat, Roland ^a,b   Chevalier, Jérème ^b,c   Boivin, Georges ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ DE LYON   (France)

^c UNIVERSITÉ DE LYON   (France)

Author keywords

Bone quality; fourier transform infrared microspectroscopy; long term alendronate; nanoindentation; postmenopausal osteoporosis

Indexed keywords

ALENDRONIC ACID; COLLAGEN;

AGED; ANALYTIC METHOD; ARTICLE; BIOMECHANICS; BONE BIOPSY; BONE MATRIX; BONE MATURATION; BONE MINERAL; BONE MINERALIZATION; BONE STRUCTURE; CLINICAL ARTICLE; CONTROLLED STUDY; CORTICAL BONE; CRYSTALLIZATION; DISEASE ASSOCIATION; EX VIVO STUDY; FEMALE; HARDNESS; HUMAN; HUMAN TISSUE; ILIAC BONE; INFRARED SPECTROSCOPY; LONG TERM CARE; MICRORADIOGRAPHY; NANOINDENTATION; POSTMENOPAUSE OSTEOPOROSIS; QUANTITATIVE ANALYSIS; TREATMENT DURATION; YOUNG MODULUS;

AGED; ALENDRONATE; BIOMECHANICS; BIOPSY; BONE AND BONES; CALCIFICATION, PHYSIOLOGIC; FEMALE; HUMANS; POSTMENOPAUSE; REGRESSION ANALYSIS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; TIME FACTORS; WEIGHT-BEARING;

EID: 84858717807     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.1501     Document Type: Article

References (63)

1. Rho JY, Kuhn-Spearing L, Zioupos P,. Mechanical properties and the hierarchical structure of bone. Med Eng Phys. 1998; 20 (2): 92-102. (Pubitemid 28318322)
2. Bouxsein ML,. Determinants of skeletal fragility. Best Pract Res Clin Rheumatol. 2005; 19 (6): 897-11.
3. Seeman E, Delmas PD,. Bone quality-the material and structural basis of bone strength and fragility. N Engl J Med. 2006; 354 (21): 2250-61.
4. Fratzl P, Weinkamer R,. Nature's hierarchical materials. Prog Mater Sci. 2007; 52: 1263-334. (Pubitemid 47374755)
5. Jepsen KJ,. Functional interactions among morphologic and tissue quality traits define bone quality. Clin Orthop Relat Res. 2011; 469 (8): 2150-9.
6. Zebaze RM, Ghasem-Zadeh A, Bohte A, Iuliano-Burns S, Mirams M, Price RI, Mackie EJ, Seeman E,. Intracortical remodelling and porosity in the distal radius and post-mortem femurs of women: a cross-sectional study. Lancet. 2010; 375 (9727): 1729-36.
7. Black DM, Cummings SR, Karpf DB, Cauley JA, Thompson DE, Nevitt MC, Bauer DC, Genant HK, Haskell WL, Marcus R, Ott SM, Torner JC, Quandt SA, Reiss TF, Ensrud KE,. Randomised trial of effect of alendronate on risk of fracture in women with existing vertebral fractures. Fracture Intervention Trial Research Group. Lancet. 1996; 348 (9041): 1535-41. (Pubitemid 26411651)
8. Black DM, Thompson DE, Bauer DC, Ensrud K, Musliner T, Hochberg MC, Nevitt MC, Suryawanshi S, Cummings SR,. Fracture risk reduction with alendronate in women with osteoporosis: the Fracture Intervention Trial. FIT Research Group. J Clin Endocrinol Metab. 2000; 85 (11): 4118-24. (Pubitemid 32055362)
9. Cummings SR, Black DM, Thompson DE, Applegate WB, Barrett-Connor E, Musliner TA, Palermo L, Prineas R, Rubin SM, Scott JC, Vogt T, Wallace R, Yates AJ, LaCroix AZ,. Effect of alendronate on risk of fracture in women with low bone density but without vertebral fractures: results from the Fracture Intervention Trial. JAMA. 1998; 280 (24): 2077-82. (Pubitemid 29014065)
10. Liberman UA, Weiss SR, Broll J, Minne HW, Quan H, Bell NH, Rodriguez-Portales J, Downs RW Jr, Dequeker J, Favus M,. Effect of oral alendronate on bone mineral density and the incidence of fractures in postmenopausal osteoporosis. The Alendronate Phase III Osteoporosis Treatment Study Group. N Engl J Med. 1995; 333 (22): 1437-43.
11. Boivin GY, Chavassieux PM, Santora AC, Yates J, Meunier PJ,. Alendronate increases bone strength by increasing the mean degree of mineralization of bone tissue in osteoporotic women. Bone. 2000; 27 (5): 687-94.
12. Roschger P, Rinnerthaler S, Yates J, Rodan GA, Fratzl P, Klaushofer K,. Alendronate increases degree and uniformity of mineralization in cancellous bone and decreases the porosity in cortical bone of osteoporotic women. Bone. 2001; 29 (2): 185-91. (Pubitemid 32737191)
13. Boskey AL, Spevak L, Weinstein RS,. Spectroscopic markers of bone quality in alendronate-treated postmenopausal women. Osteoporos Int. 2009; 20 (5): 793-800.
14. Allen MR, Iwata K, Phipps R, Burr DB,. Alterations in canine vertebral bone turnover, microdamage accumulation, and biomechanical properties following 1-year treatment with clinical treatment doses of risedronate or alendronate. Bone. 2006; 39 (4): 872-9. (Pubitemid 44311727)
15. Mashiba T, Hirano T, Turner CH, Forwood MR, Johnston CC, Burr DB,. Suppressed bone turnover by bisphosphonates increases microdamage accumulation and reduces some biomechanical properties in dog rib. J Bone Miner Res. 2000; 15 (4): 613-20. (Pubitemid 30174014)
16. Chapurlat RD, Arlot M, Burt-Pichat B, Chavassieux P, Roux JP, Portero-Muzy N, Delmas PD,. Microcrack frequency and bone remodeling in postmenopausal osteoporotic women on long-term bisphosphonates: a bone biopsy study. J Bone Miner Res. 2007; 22 (10): 1502-9. (Pubitemid 351229320)
17. Stepan JJ, Burr DB, Pavo I, Sipos A, Michalska D, Li J, Fahrleitner-Pammer A, Petto H, Westmore M, Michalsky D, Sato M, Dobnig H,. Low bone mineral density is associated with bone microdamage accumulation in postmenopausal women with osteoporosis. Bone. 2007; 41 (3): 378-85. (Pubitemid 47199146)
18. Allen MR, Burr DB,. Bisphosphonate effects on bone turnover, microdamage, and mechanical properties: what we think we know and what we know that we don't know. Bone. 2011; 49 (1): 56-65.
19. Roschger P, Lombardi A, Misof BM, Maier G, Fratzl-Zelman N, Fratzl P, Klaushofer K,. Mineralization density distribution of postmenopausal osteoporotic bone is restored to normal after long-term alendronate treatment: qBEI and sSAXS data from the fracture intervention trial long-term extension (FLEX). J Bone Miner Res. 2010; 25 (1): 48-55.
20. Allen MR, Gineyts E, Leeming DJ, Burr DB, Delmas PD,. Bisphosphonates alter trabecular bone collagen cross-linking and isomerization in beagle dog vertebra. Osteoporos Int. 2008; 19 (3): 329-37.
21. Tang SY, Allen MR, Phipps R, Burr DB, Vashishth D,. Changes in non-enzymatic glycation and its association with altered mechanical properties following 1-year treatment with risedronate or alendronate. Osteoporos Int. 2009; 20 (6): 887-94.
22. Tang SY, Zeenath U, Vashishth D,. Effects of non-enzymatic glycation on cancellous bone fragility. Bone. 2007; 40 (4): 1144-51. (Pubitemid 46386561)
23. Viguet-Carrin S, Garnero P, Delmas PD,. The role of collagen in bone strength. Osteoporos Int. 2006; 17 (3): 319-36.
24. Yerramshetty JS, Akkus O,. The associations between mineral crystallinity and the mechanical properties of human cortical bone. Bone. 2008; 42 (3): 476-82.
25. Khosla S, Burr D, Cauley J, Dempster DW, Ebeling PR, Felsenberg D, Gagel RF, Gilsanz V, Guise T, Koka S, McCauley LK, McGowan J, McKee MD, Mohla S, Pendrys DG, Raisz LG, Ruggiero SL, Shafer DM, Shum L, Silverman SL, Van Poznak CH, Watts N, Woo SB, Shane E,. Bisphosphonate-associated osteonecrosis of the jaw: report of a task force of the American Society for Bone and Mineral Research. J Bone Miner Res. 2007; 22 (10): 1479-91. (Pubitemid 351229318)
26. Odvina CV, Zerwekh JE, Rao DS, Maalouf N, Gottschalk FA, Pak CY,. Severely suppressed bone turnover: a potential complication of alendronate therapy. J Clin Endocrinol Metab. 2005; 90 (3): 1294-301. (Pubitemid 40463979)
27. Shane E, Burr D, Ebeling PR, Abrahamsen B, Adler RA, Brown TD, Cheung AM, Cosman F, Curtis JR, Dell R, Dempster D, Einhorn TA, Genant HK, Geusens P, Klaushofer K, Koval K, Lane JM, McKiernan F, McKinney R, Ng A, Nieves J, O'Keefe R, Papapoulos S, Sen HT, van der Meulen MC, Weinstein RS, Whyte M,. Atypical subtrochanteric and diaphyseal femoral fractures: report of a task force of the American Society for Bone and Mineral Research. J Bone Miner Res. 2010; 25 (11): 2267-94.
28. Gamsjaeger S, Buchinger B, Zwettler E, Recker R, Black D, Gasser JA, Eriksen EF, Klaushofer K, Paschalis EP,. 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. 2011; 26 (1): 12-8.
29. Ott SM, Oleksik A, Lu Y, Harper K, Lips P,. Bone histomorphometric and biochemical marker results of a 2-year placebo-controlled trial of raloxifene in postmenopausal women. J Bone Miner Res. 2002; 17 (2): 341-8. (Pubitemid 34087667)
30. Boivin G, Bala Y, Doublier A, Farlay D, Ste-Marie LG, Meunier PJ, Delmas PD,. The role of mineralization and organic matrix in the microhardness of bone tissue from controls and osteoporotic patients. Bone. 2008; 43 (3): 532-8.
31. Oliver WC, Pharr GM,. An improved technique for determining hardness and elastic modulus. J Mater Res. 1992; 7 (6): 1564-83.
32. Sakai M,. The Meyer Hardness: A measure for plasticity?. J Mater Res. 1999; 14 (9): 3630-9.
33. Oyen ML,. Nanoindentation hardness of mineralized tissues. J Biomech. 39 (14): 2699-702.
34. Bala Y, Depalle B, Douillard T, Meille S, Clément P, Follet H, Chevalier J, Boivin G,. Respective roles of organic and mineral components of human cortical bone matrix in micromechanical behavior: an instrumented study. J Biomechan Behav Biomed Mater. 2011; 4: 1473-82.
35. Farlay D, Duclos M-E, Gineyts E, Bertholon C, Viguet-Carrin S, Nallala J, Sockalingum G, Bertrand D, Roger T, Hartmann DJ, Chapurlat R, Boivin G,. The ratio 1660/1690cm-1 measured by Infrared Microspectroscopy is not specific of enzymatic collagen cross-links in bone tissue. PLoS ONE. 2011; 6 (12): e2873.
36. Farlay D, Panczer G, Rey C, Delmas PD, Boivin G,. Mineral maturity and crystallinity index are distinct characteristics of bone mineral. J Bone Miner Metab. 2010; 28 (4): 433-45.
37. Bala Y, Farlay D, Chapurlat R, Boivin G,. Modifications of bone material properties in postmenopausal osteoporotic women long-term treated with alendronate. Eur J Endocrinol. 2011; 165 (4): 647-55.
38. Borah B, Ritman EL, Dufresne TE, Jorgensen SM, Liu S, Sacha J, Phipps RJ, Turner RT,. The effect of risedronate on bone mineralization as measured by micro-computed tomography with synchrotron radiation: correlation to histomorphometric indices of turnover. Bone. 2005; 37 (1): 1-9. (Pubitemid 40848411)
39. Seeman E,. Bone morphology in response to alendronate as seen by high-resolution computed tomography: through a glass darkly. J Bone Miner Res. 2010; 25 (12): 2553-7.
40. Chavassieux PM, Arlot ME, Reda C, Wei L, Yates AJ, Meunier PJ,. Histomorphometric assessment of the long-term effects of alendronate on bone quality and remodeling in patients with osteoporosis. J Clin Invest. 1997; 100 (6): 1475-80. (Pubitemid 27425772)
41. Recker RR, Weinstein RS, Chesnut CH 3rd, Schimmer RC, Mahoney P, Hughes C, Bonvoisin B, Meunier PJ,. Histomorphometric evaluation of daily and intermittent oral ibandronate in women with postmenopausal osteoporosis: results from the BONE study. Osteoporos Int. 2004; 15 (3): 231-7. (Pubitemid 38391539)
42. Recker RR, Delmas PD, Halse J, Reid IR, Boonen S, Garcia-Hernandez PA, Supronik J, Lewiecki EM, Ochoa L, Miller P, Hu H, Mesenbrink P, Hartl F, Gasser J, Eriksen EF,. Effects of intravenous zoledronic acid once yearly on bone remodeling and bone structure. J Bone Miner Res. 2008; 23 (1): 6-16.
43. Fuchs RK, Faillace ME, Allen MR, Phipps R, Miller LM, Burr D,. Bisphosphonates do not alter the rate of the secondary mineralization. Bone. 2011; 49 (4): 701-5.
44. Durchschlag E, Paschalis EP, Zoehrer R, Roschger P, Fratzl P, Recker R, Phipps R, Klaushofer K,. Bone material properties in trabecular bone from human iliac crest biopsies after 3- and 5-year treatment with risedronate. J Bone Miner Res. 2006; 21 (10): 1581-90. (Pubitemid 44484603)
45. Byrjalsen I, Leeming DJ, Qvist P, Christiansen C, Karsdal MA,. Bone turnover and bone collagen maturation in osteoporosis: effects of antiresorptive therapies. Osteoporos Int. 2008; 19 (3): 339-48. (Pubitemid 351199183)
46. Sroga GE, Vashishth D,. UPLC methodology for identification and quantitation of naturally fluorescent crosslinks in proteins: a study of bone collagen. J Chromatogr B Anal Technol Biomed Life Sci. 2011; 879 (5-6): 379-85.
47. Viguet-Carrin S, Gineyts E, Bertholon C, Delmas PD,. Simple and sensitive method for quantification of fluorescent enzymatic mature and senescent crosslinks of collagen in bone hydrolysate using single-column high performance liquid chromatography. J Chromatogr B Anal Technol Biomed Life Sci. 2009; 877 (1-2): 1-7.
48. Nancollas GH, Tang R, Phipps RJ, Henneman Z, Gulde S, Wu W, Mangood A, Russell RG, Ebetino FH,. Novel insights into actions of bisphosphonates on bone: differences in interactions with hydroxyapatite. Bone. 2006; 38 (5): 617-27.
49. Ebetino FH, Barnett BL, Russell RG,. A computational model delineates differences in hydroxyapatite binding affinities of bisphosphonates in clinical use. J Bone Miner Res. 2005; 20 (Suppl 1): S259.
50. Russell RG, Watts NB, Ebetino FH, Rogers MJ,. Mechanisms of action of bisphosphonates: similarities and differences and their potential influence on clinical efficacy. Osteoporos Int. 2008; 19 (6): 733-59.
51. Li ZY, Lam WM, Yang C, Xu B, Ni GX, Abbah SA, Cheung KM, Luk KD, Lu WW,. Chemical composition, crystal size and lattice structural changes after incorporation of strontium into biomimetic apatite. Biomaterials. 2007; 28 (7): 1452-60. (Pubitemid 44959038)
52. Wu W, Gerard DE, Nancollas GH,. Nucleation at surfaces: the importance of interfacial energy. J Am Soc Nephrol. 1999; 10 (Suppl 14): S355-8. (Pubitemid 29498580)
53. Wang X, Shanbhag AS, Rubash HE, Agrawal CM,. Short-term effects of bisphosphonates on the biomechanical properties of canine bone. J Biomed Mater Res. 1999; 44 (4): 456-60. (Pubitemid 29031129)
54. Fratzl P, Gupta HS, Paschalis EP, Roschger P,. Structure and mechanical quality of the collagen-mineral nano-composite in bone. J Mater Chem. 2004; 14: 2115-23.
55. Gourion-Arsiquaud S, Burket JC, Havill LM, DiCarlo E, Doty SB, Mendelsohn R, van der Meulen MC, Boskey AL,. Spatial variation in osteonal bone properties relative to tissue and animal age. J Bone Miner Res. 2009; 24 (7): 1271-81.
56. Isaksson H, Malkiewicz M, Nowak R, Helminen HJ, Jurvelin JS,. Rabbit cortical bone tissue increases its elastic stiffness but becomes less viscoelastic with age. Bone. 2010; 47 (6): 1030-8.
57. Svensson RB, Hassenkam T, Hansen P, Peter Magnusson S,. Viscoelastic behavior of discrete human collagen fibrils. J Mech Behav Biomed Mater. 2010; 3 (1): 112-5.
58. van der Rijt JA, van der Werf KO, Bennink ML, Dijkstra PJ, Feijen J,. Micromechanical testing of individual collagen fibrils. Macromol Biosci. 2006; 6 (9): 697-702.
59. Oyen ML, Ko CC,. Examination of local variations in viscous, elastic, and plastic indentation responses in healing bone. J Mater Sci Mater Med. 2007; 18 (4): 623-8. (Pubitemid 46876376)
60. Hengsberger S, Ammann P, Legros B, Rizzoli R, Zysset P,. Intrinsic bone tissue properties in adult rat vertebrae: modulation by dietary protein. Bone. 2005; 36 (1): 134-41. (Pubitemid 40136588)
61. Allen MR, Reinwald S, Burr DB,. Alendronate reduces bone toughness of ribs without significantly increasing microdamage accumulation in dogs following 3 years of daily treatment. Calcif Tissue Int. 2008; 82 (5): 354-60.
62. Ziv V, Wagner HD, Weiner S,. Microstructure-microhardness relations in parallel-fibered and lamellar bone. Bone. 1996; 18 (5): 417-28. (Pubitemid 26152304)
63. Bone HG, Hosking D, Devogelaer JP, Tucci JR, Emkey RD, Tonino RP, Rodriguez-Portales JA, Downs RW, Gupta J, Santora AC, Liberman UA,. Ten years' experience with alendronate for osteoporosis in postmenopausal women. N Engl J Med. 2004; 350 (12): 1189-99. (Pubitemid 38339363)