Skip to main content

Advertisement

Log in

Changes in the Degree of Mineralization with Osteoporosis and its Treatment

  • Bone Quality in Osteoporosis (MD Grynpas and JS Nyman, Section Editors)
  • Published:
Current Osteoporosis Reports Aims and scope Submit manuscript

Abstract

The diagnosis of osteoporosis is based on low bone mineral density (BMD) and/or the occurrence of fragility fractures. The majority of patients, however, have also abnormally low bone matrix mineralization. The latter is indicative of alterations in bone turnover rates and/or in kinetics of mineral accumulation within the newly formed bone matrix. Osteoporosis therapies can alter the bone matrix mineralization according to their action on bone turnover and/or mineralization kinetics. Antiresorptives, including the most widely used bisphosphonates, reduce the bone turnover rate resulting in a decrease in heterogeneity and an increase in the degree of mineralization toward to or even beyond normal values. Anabolic agents increase the bone volume and the amount of newly formed bone resulting in a likely transient decrease in mean degree and homogeneity of mineralization. Hence, the measurement of bone matrix mineralization is a sensitive tool to evaluate the response to therapy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Blake GM, Fogelman I. Role of dual-energy X-ray absorptiometry in the diagnosis and treatment of osteoporosis. J Clin Densitom. 2007;10:102–10.

    PubMed  Google Scholar 

  2. Kanis JA, Burlet N, Cooper C, Delmas PD, Reginster JY, Borgstrom F, et al. European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporos Int. 2008;19:399–428.

    CAS  PubMed Central  PubMed  Google Scholar 

  3. Seeman E. Bone quality: the material and structural basis of bone strength. J Bone Miner Metab. 2008;26:1–8.

    PubMed  Google Scholar 

  4. Fratzl P, Roschger P, Fratzl-Zelman N, Paschalis EP, Phipps R, Klaushofer K. Evidence that treatment with risedronate in women with postmenopausal osteoporosis affects bone mineralization and bone volume. Calcif Tissue Int. 2007;81:73–80.

    CAS  PubMed  Google Scholar 

  5. Rauch F, Schoenau E. Changes in bone density during childhood and adolescence: an approach based on bone's biological organization. J Bone Miner Res. 2001;16(4):597–604.

    CAS  PubMed  Google Scholar 

  6. Scheiner S, Pivonka P, Smith DW, Dunstan CR, Hellmich C. Mathematical modeling of postmenopausal osteoporosis and its treatment by the anti-catabolic drug denosumab. Int J Numer Method Biomed Eng. 2013. doi:10.1002/cnm.2584.

    PubMed  Google Scholar 

  7. Fratzl-Zelman N, Roschger P, Fisher JE, le Duong T, Klaushofer K. Effects of odanacatib on bone mineralization density distribution in thoracic spine and femora of ovariectomized adult rhesus monkeys: a quantitative backscattered electron imaging study. Calcif Tissue Int. 2013;92(3):261–9. doi:10.1007/s00223-012-9673-7.

    CAS  PubMed  Google Scholar 

  8. Sinder BP, Eddy MM, Ominsky MS, Caird MS, Marini JC, Kozloff KM. Sclerostin antibody improves skeletal parameters in a Brtl/+mouse model of osteogenesis imperfecta. J Bone Miner Res. 2013;28(1):73–80. doi:10.1002/jbmr.1717.

    CAS  PubMed Central  PubMed  Google Scholar 

  9. Ross RD, Edwards LH, Acerbo AS, Ominsky MS, Virdi AS, Sena K, et al. Bone matrix quality following sclerostin antibody treatment. J Bone Miner Res. 2014. doi:10.1002/jbmr.2188.

    Google Scholar 

  10. 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.

    CAS  Google Scholar 

  11. Fratzl P, Gupta HS, Roschger P, Klaushofer K. Bone nanostructure and its relevance for mechanical performance, disease and treatment. In: Nanotechnology, Volume 5: Nanomedicine. Viola Vogel, editor. Copyright WILEY-VCH Verlag GMBH and Co. KGaA. Germany: Weinheim; 2009. p. 345–60. ISBN: 978-3-527-31736-3.

  12. Siris ES, Chen YT, Abbott TA, Barrett-Connor E, Miller PD, Wehren LE, et al. Bone mineral density thresholds for pharmacological intervention to prevent fractures. Arch Intern Med. 2004;164(10):1108–12.

    PubMed  Google Scholar 

  13. Roschger P, Paschalis EP, Fratzl P, Klaushofer K. Bone mineralization density distribution in health and disease. Bone. 2008;42:456–66.

    CAS  PubMed  Google Scholar 

  14. Ruffoni D, Fratzl P, Roschger P, Klaushofer K, Weinkamer R. The bone mineralization density distribution as a fingerprint of the mineralization process. Bone. 2007;40(5):1308–19 [Epub Jan 25, 2007].

    CAS  PubMed  Google Scholar 

  15. Recker RR, Kimmel DB, Dempster D, Weinstein RS, Wronski TJ, Burr DB. Issues in modern bone histomorphometry. Bone. 2011;49:955–64.

    CAS  PubMed Central  PubMed  Google Scholar 

  16. Eriksen EF, Gundersen HJ, Melsen F, Mosekilde L. Reconstruction of the formative site in iliac trabecular bone in 20 normal individuals employing a kinetic model for matrix and mineral apposition. Metab Bone Dis Rela t Res. 1984;5(5):243–52.

    CAS  Google Scholar 

  17. Boivin G, Meunier PJ. The mineralization of bone tissue: a forgotten dimension in osteoporosis research. Osteoporos Int. 2003;14 Suppl 3:S19–24.

    PubMed  Google Scholar 

  18. Fuchs RK, Faillace ME, Allen MR, Phipps RJ, Miller LM, Burr DB. Bisphosphonates do not alter the rate of secondary mineralization. Bone. 2011;49(4):701–5. doi:10.1016/j.bone.2011.05.009. This is an important contribution to the understanding of the time sequence of the mineral accumulation within the newly formed bone matrix in general and in particular under alendronate or risedronate treatment.

    CAS  PubMed  Google Scholar 

  19. Fuchs RK, Allen MR, Ruppel ME, Diab T, Phipps RJ, Miller LM, et al. In situ examination of the time-course for secondary mineralization of Haversian bone using synchrotron Fourier transform infrared microspectroscopy. Matrix Biol. 2008;27(1):34–41.

    CAS  PubMed  Google Scholar 

  20. Bala Y, Farlay D, Chapurlat RD, Boivin G. Modifications of bone material properties in postmenopausal osteoporotic women long-term treated with alendronate. Eur J Endocrinol. 2011;165:647–55.

    CAS  PubMed  Google Scholar 

  21. Akkus O, Polyakova-Akkus A, Adar F, Schaffler MB. Aging of microstructural compartments in human compact bone. J Bone Miner Res. 2003;18(6):1012–9.

    CAS  PubMed  Google Scholar 

  22. Bala Y, Farlay D, Boivin G. Bone mineralization: from tissue to crystal in normal and pathologic contexts. Osteoporos Int. 2013;24(8):2153–66. doi:10.1007/s00198-012-2228-y.

    CAS  PubMed  Google Scholar 

  23. Roschger P, Gupta HS, Berzlanovich A, Ittner G, Dempster DW, Fratzl P, et al. Constant mineralization density distribution in cancellous human bone. Bone. 2003;32:316–23.

    CAS  PubMed  Google Scholar 

  24. Skedros JG, Bloebaum RD, Bachus KN, Boyce TM, Constantz B. Influence of mineral content and composition on gray levels in backscattered electron images of bone. J Biomed Mater Res. 1993;27:57–64.

    CAS  PubMed  Google Scholar 

  25. Grynpas M. Age and disease-related changes in the mineral of bone. Calcif Tissue Int. 1993;53 Suppl 1:S57–64.

    PubMed  Google Scholar 

  26. Akesson K, Grynpas MD, Hancock RG, Odselius R, Obrant KJ. Energy-dispersive X-ray microanalysis of the bone mineral content in human trabecular bone: a comparison with ICPES and neutron activation analysis. Calcif Tissue Int. 1994;55:236–9.

    CAS  PubMed  Google Scholar 

  27. Bang S, Baud CA. Topographical distribution of fluoride in iliac bone of a fluoride-treated osteoporotic patient. J Bone Miner Res. 1990;5 Suppl 1:S87–9.

    PubMed  Google Scholar 

  28. Zoeger N, Streli C, Wobrauschek P, Jakubonis C, Pepponi G, Roschger P, et al. Determination of the elemental distribution in human joint bones by SR micro XRF. X-Ray Spectrom. 2008;37:3–11.

    CAS  Google Scholar 

  29. Gomes S, Rizzo R, Pozzi-Mucelli M, Bonucci E, Vittur F. Zinc mapping in bone tissues by histochemistry and synchrotron radiation–induced x-ray emission: correlation with the distribution of alkaline phosphatase. Bone. 1999;25:33–8.

    Google Scholar 

  30. Zoeger N, Roschger P, Hoefstaetter JG, Jokubonis C, Pepponi G, Falkenberg G, et al. Lead accumulation in the tidemark of articular cartilage. Osteoarthr Cartil. 2006;14:906–13.

    CAS  PubMed  Google Scholar 

  31. Henss A, Rohnke M, El Khassawna T, Govindarajan P, Schlewitz G, Heiss C, et al. Applicability of ToF-SIMS for monitoring compositional changes in bone in a long-term animal model. J R Soc Interface. 2013;10:20130332. doi:10.1098/rsif.2013.0332.

    PubMed  Google Scholar 

  32. Boivin G, Meunier PJ. The degree of mineralization of bone tissue measured by computerized quantitative contact microradiography. Calcif Tissue Int. 2002;70:503–11.

    CAS  PubMed  Google Scholar 

  33. Eschberger J, Eschberger DJ. Microradiography. In: von Recum FA, editor. Handbook of biomaterials evaluation. New York: Macmillan Publishing Company; 1986. p. 491–500.

    Google Scholar 

  34. Borah B, Dufresne TE, Ritman EL, Jorgensen SM, Liu S, Chmielewski PA, et al. Long-term risedronate treatment normalizes mineralization and continues to preserve trabecular architecture: sequential triple biopsy studies with micro-computed tomography. Bone. 2006;39:345–52.

    CAS  PubMed  Google Scholar 

  35. Nuzzo S, Lafage-Proust MH, Martin-Badosa E, Boivin G, Thomas T, Alexandre C, et al. Synchrotron radiation microtomography allows the analysis of three-dimensional microarchitecture and degree of mineralization of human iliac crest biopsy specimens: effects of etidronate treatment. J Bone Miner Res. 2002;17:1372–82.

    CAS  PubMed  Google Scholar 

  36. Cheng Z, Yao W, Zimmermann EA, Busse C, Ritchie RO, Lane NE. Prolonged treatments with antiresorptive agents and PTH have different effects on bone strength and the degree of mineralization in old estrogen-deficient osteoporotic rats. J Bone Miner Res. 2009;24(2):209–20.

    CAS  PubMed Central  PubMed  Google Scholar 

  37. Recker RR, Delmas PD, Halse J, Reid IR, Boonen S, García-Hernandez PA, et al. Effects of intravenous zoledronic acid once yearly on bone remodeling and bone structure. J Bone Miner Res. 2008;23(1):6–16.

    CAS  PubMed  Google Scholar 

  38. Nazarian A, Snyder BD, Zurakowski D, Müller R. Quantitative micro-computed tomography: a non-invasive method to assess equivalent bone mineral density. Bone. 2008;43:302–11.

    PubMed  Google Scholar 

  39. Boyde A, Jones SJ. Backscattered electron imaging of skeletal tissues. Metab Bone Dis Rel Res. 1983;5:145–50.

    Google Scholar 

  40. Roschger P, Fratzl P, Eschberger J, Klaushofer K. Validation of quantitative backscattered electron imaging for the measurement of mineral density distribution in human bone biopsies. Bone. 1998;23:319–26.

    CAS  PubMed  Google Scholar 

  41. Bloebaum RD, Skedros JG, Vajda EG, Bachus KN, Constantz BR. Determining mineral content variations in bone using backscattered electron imaging. Bone. 1997;20:485–90.

    CAS  PubMed  Google Scholar 

  42. Busse B, Jobke B, Hahn M, Priemel M, Niecke M, Seitz S, et al. Effects of strontium ranelate administration on bisphosphonate-altered hydroxyapatite: matrix incorporation of strontium is accompanied by changes in mineralization and microstructure. Acta Biomater. 2010;6(12):4513–21. doi:10.1016/j.actbio.2010.07.019.

    CAS  PubMed  Google Scholar 

  43. Sutton-Smith P, Beard H, Fazzalari N. Quantitative backscattered electron imaging of bone in proximal femur fragility fracture and medical illness. J Microsc. 2008;229(Pt 1):60–6.

    CAS  PubMed  Google Scholar 

  44. Pritchard JM, Papaioannou A, Tomowich C, Giangregorio LM, Atkinson SA, Beattie KA, et al. Bone mineralization is elevated and less heterogeneous in adults with type 2 diabetes and osteoarthritis compared with controls with osteoarthritis alone. Bone. 2013;54(1):76–82.

    CAS  PubMed  Google Scholar 

  45. Paschalis EP, Betts F, DiCarlo E, Mendelsohn R, Boskey AL. FTIR microspectroscopic analysis of human cortical and trabecular bone. Bone Calcif Tissue Int. 1997;61:480–6.

    CAS  Google Scholar 

  46. Gamsjäger S, Kazanci M, Paschalis E, Fratzl P. Raman application in Bone Imaging. In: Amer M, editor. Raman spectroscopy for soft matter applications. Hoboken: Wiley; 2009. p. 227–69.

    Google Scholar 

  47. Zoehrer R, Roschger P, Fratzl P, Durchschlag E, Paschalis E, Phipps R, et al. Effects of 3- and 5-year treatment with Risedronate on the bone mineral density distribution of cancellous bone in human iliac crest biopsies. J Bone Miner Res. 2006;21:1106–12.

    CAS  PubMed  Google Scholar 

  48. Misof BM, Paschalis EP, Blouin S, Fratzl-Zelman N, Klaushofer K, Roschger P. Effects of 1 year of daily teriparatide treatment on iliacal bone mineralization density distribution (BMDD) in postmenopausal osteoporotic women previously treated with alendronate or risedronate. J Bone Miner Res. 2010;25(11):2297–303. doi:10.1002/jbmr.198.

    CAS  PubMed  Google Scholar 

  49. Hofstetter B, Gamsjaeger S, Phipps RJ, Recker RR, Ebetino FH, Klaushofer K, et al. Effects of alendronate and risedronate on bone material properties in actively forming trabecular bone surfaces. J Bone Miner Res. 2012;27(5):995–1003. doi:10.1002/jbmr.1572.

    CAS  PubMed  Google Scholar 

  50. Gamsjaeger S, Buchinger B, Zwettler E, Recker R, Black D, Gasser JA, et al. 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. doi:10.1002/jbmr.180. This is the first report showing evidence for changes in the proteoglycan density together with increased mineral per matrix in bone formed under zoledronic acid therapy, which point toward changes in the mineralization kinetics due to this treatment.

    CAS  PubMed  Google Scholar 

  51. Gamsjaeger S, Hofstetter B, Zwettler E, Recker R, Gasser JA, Eriksen EF, et al. Effects of 3 years treatment with once-yearly zoledronic acid on the kinetics of bone matrix maturation in osteoporotic patients. Osteoporos Int. 2013;24(1):339–47.

    CAS  PubMed  Google Scholar 

  52. 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.

    CAS  PubMed  Google Scholar 

  53. 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;27:687–94.

    CAS  PubMed  Google Scholar 

  54. Boskey AL, Spevak L, Weinstein RS. Spectroscopic markers of bone quality in alendronate-treated postmenopausal women. Osteoporos Int. 2009;20(5):793–800. doi:10.1007/s00198-008-0725-9.

    CAS  PubMed Central  PubMed  Google Scholar 

  55. Roschger P, Lombardi A, Misof BM, Maier G, Fratzl-Zelman N, Kimmel D, et al. 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;25:48–55. This work revealed that patients after long-term alendronate therapy had normal bone mineralization patterns, comparably to those from patients who stopped alendronate after 5 years and continued with placebo.

    CAS  PubMed  Google Scholar 

  56. Misof BM, Roschger P, Gabriel D, Paschalis EP, Eriksen EF, Recker RR, et al. Annual intravenous zoledronic acid for three years increased cancellous bone matrix mineralization beyond normal values in the HORIZON biopsy cohort. J Bone Miner Res. 2013;28(3):442–8.

    CAS  PubMed  Google Scholar 

  57. Boivin G, Vedi S, Purdie DW, Compston JE, Meunier PJ. Influence of estrogen therapy at conventional and high doses on the degree of mineralization of iliac bone tissue: a quantitative microradiographic analysis in postmenopausal women. Bone. 2005;3:562–7.

    Google Scholar 

  58. Boivin G, Lips P, Ott SM, Harper KD, Sarkar S, Pinette KV, et al. Contribution of raloxifene and calcium and vitamin D3 supplementation to the increase of the degree of mineralization of bone in postmenopausal women. J Clin Endocrinol Metab. 2003;88(9):4199–205.

    CAS  PubMed  Google Scholar 

  59. Faibish D, Ott SM, Boskey AL. Mineral changes in osteoporosis: a review. Clin Orthop Relat Res. 2006;443:28–38.

    PubMed Central  PubMed  Google Scholar 

  60. Paschalis EP, Boskey AL, Kassem M, Eriksen EF. Effect of hormone replacement therapy on bone quality in early postmenopausal women. J Bone Miner Res. 2003;18(6):955–9.

    CAS  PubMed  Google Scholar 

  61. Misof BM, Patsch JM, Roschger P, Muschitz C, Gamsjaeger S, Paschalis EP, et al. Intravenous treatment with ibandronate normalizes bone matrix mineralization and reduces cortical porosity after two years in male osteoporosis: a paired biopsy study. J Bone Miner Res. 2013. doi:10.1002/jbmr.2035.

    PubMed  Google Scholar 

  62. Bala Y, Kohles J, Recker RR, Boivin G. Oral ibandronate in postmenopausal osteoporotic women alters micromechanical properties independently of changes in mineralization. Calcif Tissue Int. 2013;92(1):6–14. doi:10.1007/s00223-012-9658-6. The relationship of local material hardness and degree of mineralization was found altered by bisphosphonate treatment suggesting bone material changes at the organic matrix or mineral compositional level.

    CAS  PubMed  Google Scholar 

  63. Boivin G, Farlay D, Khebbab MT, Jaurand X, Delmas PD, Meunier PJ. In osteoporotic women treated with strontium ranelate, strontium is located in bone formed during treatment with a maintained degree of mineralization. Osteoporos Int. 2010;21:667–77.

    CAS  PubMed  Google Scholar 

  64. Roschger P, Manjubala I, Zoeger N, Meirer F, Simon R, Li C, et al. Bone material quality in transiliac bone biopsies of postmenopausal osteoporotic women after 3 years of strontium ranelate treatment. J Bone Miner Res. 2010;25(4):891–900. doi:10.1359/jbmr.091028.

    PubMed  Google Scholar 

  65. Doublier A, Farlay D, Khebbab MT, Jaurand X, Meunier MJ, Boivin G. Distribution of strontium and mineralization in iliac bone biopsies from osteoporotic women treated long-term with strontium ranelate. Eur J Endocrinol. 2011;165:469–76.

    CAS  PubMed  Google Scholar 

  66. Misof BM, Roschger P, Cosman R, Kurland ES, Tesch W, Messmer P, et al. Effects of intermittent parathyroid hormone administration on bone mineralization density distribution in iliac crest biopsies from patients with osteoporosis: a paired study before and after treatment. J Clin Endocrinol Metab. 2003;88:1150–6.

    CAS  PubMed  Google Scholar 

  67. Paschalis EP, Glass EV, Donley DW, Eriksen EF. Bone mineral and collagen quality in iliac crest biopsies of patients given teriparatide: new results from the fracture prevention trial. J Clin Endocrinol Metab. 2005;90:4644–9.

    CAS  PubMed  Google Scholar 

  68. Gourrier A, Li C, Seigel S, Paris O, Roschger P, Klaushofer K, et al. Scanning small-angle X-ray scattering analysis of the size and organization of the mineral nanoparticles in fluorotic bone using a stack of cards model. J Appl Cryst. 2010;43:1385–92.

    CAS  Google Scholar 

  69. Gamsjaeger S, Buchinger B, Zoehrer R, Phipps R, Klaushofer K, Paschalis EP. Effects of one-year daily teriparatide treatment on trabecular bone material properties in postmenopausal osteoporotic women previously treated with alendronate or risedronate. Bone. 2011;49:1160–5.

    CAS  PubMed  Google Scholar 

  70. Tjhia CK, Odvina CV, Rao DS, Stover SM, Wang X, Fyhrie DP. Mechanical property and tissue mineral density differences among severely suppressed bone turnover (SSBT) patients, osteoporotic patients, and normal subjects. Bone. 2011;49:1279–89. This work studies bone material properties at the iliac crest from patients with suppressed bone turnover and atypical femoral fractures in search for evidence in the material for the origin of the occurrence of these fractures.

    PubMed Central  PubMed  Google Scholar 

  71. Boskey AL, DiCarlo E, Paschalis E, West P, Mendelsohn R. Comparison of mineral quality and quantity in iliac crest biopsies from high- and low-turnover osteoporosis: an FT-IR microspectroscopic investigation. Osteoporos Int. 2005;16(12):2031–8.

    CAS  PubMed Central  PubMed  Google Scholar 

  72. Misof B, Gamsjaeger S, Cohen A, Hofstetter B, Roschger P, Stein E, et al. Bone material properties in premenopausal women with idiopathic osteoporosis. J Bone Miner Res. 2012;27(12):2551–61.

    CAS  PubMed Central  PubMed  Google Scholar 

  73. Boivin G, Bala Y, Doublier A, Farlay D, Ste-Marie LG, Meunier PJ, et al. The role of mineralization and organic matrix in the micro-hardness of bone tissue from controls and osteoporotic patients. Bone. 2008;43:532–8.

    CAS  PubMed  Google Scholar 

  74. Fratzl-Zelman N, Roschger P, Misof BM, Nawrot-Wawrzyniak K, Pötter-Lang S, et al. Fragility fractures in men with idiopathic osteoporosis are associated with undermineralization of the bone matrix without evidence of increased bone turnover. Calcif Tissue Int. 2011;88(5):378–87.

    CAS  PubMed  Google Scholar 

  75. Ciarelli TE, Fyhrie DP, Parfitt AM. Effects of vertebral bone fragility and bone formation rate on the mineralization levels of cancellous bone from white females. Bone. 2003;32(3):311–5.

    CAS  PubMed  Google Scholar 

  76. Tamminen IS, Misof BM, Roschger P, Mäyränpää MK, Turunen MJ, Isaksson H, et al. Increased heterogeneity of bone matrix mineralization in pediatric patients prone to fractures: a biopsy study. J Bone Miner Res. 2013. doi:10.1002/jbmr.2124.

    Google Scholar 

  77. Fratzl P. Bone fracture: when the cracks begin to show. Nat Mater. 2008;7(8):610–2.

    CAS  PubMed  Google Scholar 

  78. Koester KJ, Ager III JW, Ritchie RO. The true toughness of human cortical bone measured with realistically short cracks. Nat Mater. 2008;7(8):672–7.

    CAS  PubMed  Google Scholar 

  79. Peterlik H, Roschger P, Klaushofer K, Fratzl P. From brittle to ductile fracture of bone. Nat Mater. 2006;5(1):52–5 [Epub Dec 11, 2005].

    CAS  PubMed  Google Scholar 

  80. Fratzl-Zelman N, Valenta A, Roschger P, Nader A, Gelb BD, Fratzl P, et al. Decreased bone turnover and deterioration of bone structure in two cases of pycnodysostosis. J Clin Endocrinol Metab. 2004;89(4):1538–47.

    CAS  PubMed  Google Scholar 

  81. Yao H, Dao M, Carnelli D, Tai K, Ortiz C. Size-dependent heterogeneity benefits the mechanical performance of bone. J Mech Phys Solids. 2011;59:64–74.

    Google Scholar 

  82. Tai K, Dao M, Suresh S, Plazoglu A, Ortiz C. Nanoscale heterogeneity promotes energy dissipation in bone. Nat Mater. 2007;6:454–62.

    CAS  PubMed  Google Scholar 

  83. Eastell R. Pathogenesis of postmenopausal osteoporosis. In: Favus MJ, editor. Primer on the metabolic bone diseases and disorders of mineral metabolism. Washington, DC: ASBMR; 2006. p. 259–62.

    Google Scholar 

  84. Szulc P, Kaufman JM, Delmas PD. Biochemical assessment of bone turnover and bone fragility in men. Osteoporos Int. 2007;18:1451–61.

    CAS  PubMed  Google Scholar 

  85. Boivin G, Farlay D, Bala Y, Doublier A, Meunier PJ, Delmas PD. Influence of remodeling on the mineralization of bone tissue. Osteoporos Int. 2009;20(6):1023–6. doi:10.1007/s00198-009-0861-x.

    CAS  PubMed Central  PubMed  Google Scholar 

  86. Roschger P, Dempster DW, Zhou H, Paschalis EP, Silverberg SJ, Shane E, et al. New observations on bone quality in mild primary hyperparathyroidism as determined by quantitative backscattered electron imaging. J Bone Miner Res. 2007;22:717–23.

    PubMed  Google Scholar 

  87. Fratzl-Zelman N, Schmidt I, Roschger P, Glorieux FH, Klaushofer K, Fratzl P, et al. Mineral particle size in children with osteogenesis imperfecta type I is not increased independently of specific collagen mutations. Bone. 2014;60:122–8.

    CAS  PubMed  Google Scholar 

  88. Khosla S, Lufkin EG, Hodgson SF, Fitzpatrick LA, Melton III LJ. Epidemiology and clinical features of osteoporosis in young individuals. Bone. 1994;15:551–5.

    CAS  PubMed  Google Scholar 

  89. Cohen A, Recker RR, Lappe J, Dempster DW, Cremers S, McMahon DJ, et al. Premenopausal women with idiopathic low-trauma fractures and/or low bone mineral density. Osteoporos Int. 2012;23(1):171–82.

    CAS  PubMed Central  PubMed  Google Scholar 

  90. Stewart TL, Roschger P, Misof BM, Mann V, Fratzl P, Klaushofer K, et al. Association of COLIA1 Sp1 alleles with defective bone nodule formation in vitro and abnormal bone mineralization in vivo. Calcif Tissue Int. 2005;77(2):113–8.

    CAS  PubMed  Google Scholar 

  91. Stepan JJ, Alenfeld F, Boivin G, Feyen JH, Lakatos. Mechanisms of action of antiresorptive therapies of postmenopausal osteoporosis. Endocr Regul. 2003;37(4):225–38.

    CAS  PubMed  Google Scholar 

  92. Recker RR, Armas L. The effect of antiresorptives on bone quality. Clin Orthop Relat Res. 2011;469(8):2207–14. doi:10.1007/s11999-011-1909-8.

    PubMed Central  PubMed  Google Scholar 

  93. Borah B, Dufresne T, Nurre J, Phipps R, Chmielewski P, Wagner L, et al. Risedronate reduces intracortical porosity in women with osteoporosis. J Bone Miner Res. 2010;25(1):41–7. This work reports an additional effect of bisphosphonates, the decrease of cortical porosity which might contribute to fracture risk reduction after treatment.

    CAS  PubMed  Google Scholar 

  94. Ebetino FH, Hogan AM, Sun S, Tsoumpra MK, Duan X, Triffitt JT, et al. The relationship between the chemistry and biological activity of the bisphosphonates: review. Bone. 2011;49:20–33.

    CAS  PubMed  Google Scholar 

  95. Shane E, Burr D, Abrahamsen B, Adler RA, Brown TD, Cheung AM, et al. Atypical subtrochanteric and diaphyseal femoral fractures: second report of a task force of the American Society for Bone and Mineral Research. J Bone Miner Res. 2014;29:1–23.

    PubMed  Google Scholar 

  96. Shane E, Burr D, Abrahamsen B, Adler RA, Brown TD, Cheung AM, et al. Atypical subtrochanteric and diaphyseal femoral fractures: second report of a task force of the American Society for Bone and Mineral Research. J Bone Miner Res. 2014;29(1):1–23. doi:10.1002/jbmr.1998.

    PubMed  Google Scholar 

  97. Donnelly E, Meredith DS, Nguyen JT, Gladnick BP, Rebolledo BJ, Shaffer AD, et al. Reduced cortical bone compositional heterogeneity with bisphosphonate treatment in postmenopausal women with intertrochanteric and subtrochanteric fractures. J Bone Miner Res. 2012;27(3):672–8. doi:10.1002/jbmr.560. Bone material heterogeneity seems important for mechanical properties such as crack propagation and initiation. Decreases in the heterogeneity of collagen maturity and mineral crystallinity distributions in cortical bone are reported for patients after bisphosphonate treatment.

    CAS  PubMed  Google Scholar 

  98. van der Meulen MC, Boskey AL. Atypical subtrochanteric femoral shaft fractures: role for mechanics and bone quality. Arthritis Res Ther. 2012;14(4):220.

    PubMed Central  PubMed  Google Scholar 

  99. 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;49:56–65.

    CAS  PubMed  Google Scholar 

  100. Li C, Paris O, Siegel S, Roschger P, Paschalis EP, Klaushofer K, et al. Strontium is incorporated into mineral crystals only in newly formed bone during strontium ranelate treatment. J Bone Miner Res. 2010;25(5):968–75. doi:10.1359/jbmr.091038. Knowledge on the incorporation of strontium to the crystal is an important issue in therapy with strontium ranelate. This work revealed that strontium is incorporated into the mineral crystal and is changing its crystal lattice of bone formed under therapy.

    CAS  PubMed  Google Scholar 

  101. Riggs BL, Hodgson SF, O’Fallon WM, Chao EYS, Wahner HW, Muhs JM, et al. Effect of fluoride treatment on the fracture rate in postmenopausal women with osteoporosis. N Engl J Med. 1990;322:802–9.

    CAS  PubMed  Google Scholar 

  102. Meunier PJ, Sebert JL, Reginster JY, Briancon D, Appelboom T, Netter P, et al. Fluoride salts are no better at preventing new vertebral fractures than calcium-vitamin D in postmenopausal osteoporosis: the FAVO Study. Osteoporos Int. 1998;8(1):4–12.

    CAS  PubMed  Google Scholar 

  103. Boivin G, Duriez J, Chapuy MC, Flautre B, Hardouin P, Meunier PJ. Relationship between bone fluoride content and histological evidence of calcification defects in osteoporotic women treated long-term with sodium fluoride. Osteoporos Int. 1993;3(4):204–8.

    CAS  PubMed  Google Scholar 

  104. Fratzl P, Roschger P, Eschberger J, Abendroth B, Klaushofer K. Abnormal bone mineralization after fluoride treatment in osteoporosis: a small-angle x-ray-scattering study. J Bone Miner Res. 1994;9(10):1541–9.

    CAS  PubMed  Google Scholar 

  105. Dempster DW, Cosman F, Kurland ES, Zhou H, Nieves J, Woelfert L, et al. Effects of daily treatment with parathyroid hormone on bone microarchitecture and turnover in patients with osteoporosis: a paired biopsy study. J Bone Miner Res. 2001;16(10):1846–53.

    CAS  PubMed  Google Scholar 

  106. Lindsay R, Zhou H, Cosman F, Nieves J, Dempster DW, Hodsman AB. Effects of a one-month treatment with PTH(1-34) on bone formation on cancellous, endocortical, and periosteal surfaces of the human ilium. J Bone Miner Res. 2007;22(4):495–502.

    CAS  PubMed  Google Scholar 

  107. Dempster DW, Zhou H, Recker RR, Brown JP, Bolognese MA, Recknor CP, et al. Skeletal histomorphometry in subjects on teriparatide or zoledronic acid therapy (SHOTZ) study: a randomized controlled trial. J Clin Endocrinol Metab. 2012;97(8):2799–808. doi:10.1210/jc.2012-1262.

    CAS  PubMed  Google Scholar 

  108. Cohen A, Stein EM, Recker RR, Lappe JM, Dempster DW, Zhou H, et al. Teriparatide for idiopathic osteoporosis in premenopausal women: a pilot study. J Clin Endocrinol Metab. 2013;98(5):1971–81.

    CAS  PubMed Central  PubMed  Google Scholar 

  109. Recker RR, Armas L. The effect of antiresorptives on bone quality. Clin Orthop Relat Res. 2011;469(8):2207–14. doi:10.1007/s11999-011-1909-8.

    PubMed Central  PubMed  Google Scholar 

Download references

Compliance with Ethics Guidelines

Conflict of Interest

P. Roschger, B. Misof, E. Paschalis, P. Fratzl, and K. Klaushofer declare that they have no conflicts of interest.

Human and Animal Rights and Informed Consent

All studies by the authors involving animal and/or human subjects were performed after approval by the appropriate institutional review boards. When required, written informed consent was obtained from all participants.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul Roschger.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Roschger, P., Misof, B., Paschalis, E. et al. Changes in the Degree of Mineralization with Osteoporosis and its Treatment. Curr Osteoporos Rep 12, 338–350 (2014). https://doi.org/10.1007/s11914-014-0218-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11914-014-0218-z

Keywords

Navigation