Skip to main content

Advertisement

SpringerLink
Log in

Is bone quality associated with collagen age?

  • Review
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

The World Health Organization defines osteoporosis as a systemic disease characterized by decreased bone tissue mass and microarchitectural deterioration, resulting in increased fracture risk. Since this statement, a significant amount of data has been generated showing that these two factors do not cover all risks for fracture. Other independent clinical factors, such as age, as well as aspects related to qualitative changes in bone tissue, are believed to play an important role. The term “bone quality” encompasses a variety of parameters, including the extent of mineralization, the number and distribution of microfractures, the extent of osteocyte apoptosis, and changes in collagen properties. The major mechanism controlling these qualitative factors is bone remodeling, which is tightly regulated by the osteoclast/osteoblast activity. We focus on the relationship between bone remodeling and changes in collagen properties, especially the extent of one posttranslational modification. In vivo, measurements of the ratio between native and isomerized C-telopeptides of type I collagen provides an index of bone matrix age. Current preclinical and clinical studies suggests that this urinary ratio provides information about bone strength and fracture risk independent of bone mineral density and that it responds differently according to the type of therapy regulating bone turnover.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Anonymous (1997) Who are candidates for prevention and treatment for osteoporosis? Osteoporos Int 7:1–6

    Google Scholar 

  2. Kanis JA (1993) Osteoporosis and its consequences. Osteoporosis. Blackwell Science, London, p 18

    Google Scholar 

  3. Siris ES, Miller PD, Barrett-Connor E, Faulkner KG, Wehren LE, Abbott TA, Berger ML, Santora AC, Sherwood LM (2001) Identification and fracture outcomes of undiagnosed low bone mineral density in postmenopausal women: results from the National Osteoporosis Risk Assessment. JAMA 286:2815–2822

    Article  PubMed  CAS  Google Scholar 

  4. Miller PD, Siris ES, Barrett-Connor E, Faulkner KG, Wehren LE, Abbott TA, Chen YT, Berger ML, Santora AC, Sherwood LM (2002) Prediction of fracture risk in postmenopausal white women with peripheral bone densitometry: evidence from the National Osteoporosis Risk Assessment. J Bone Miner Res 17:2222–2230

    Article  PubMed  Google Scholar 

  5. Hochberg MC, Ross PD, Black D, Cummings SR, Genant HK, Nevitt MC, Barrett-Connor E, Musliner T, Thompson D (1999) Larger increases in bone mineral density during alendronate therapy are associated with a lower risk of new vertebral fractures in women with postmenopausal osteoporosis. Fracture Intervention Trial Research Group. Arthritis Rheum 42:1246–1254

    Article  PubMed  CAS  Google Scholar 

  6. Cummings SR, Karpf DB, Harris F, Genant HK, Ensrud K, LaCroix AZ, Black DM (2002) Improvement in spine bone density and reduction in risk of vertebral fractures during treatment with antiresorptive drugs. Am J Med 112:281–289

    Article  PubMed  CAS  Google Scholar 

  7. Sarkar S, Mitlak BH, Wong M, Stock JL, Black DM, Harper KD (2002) Relationships between bone mineral density and incident vertebral fracture risk with raloxifene therapy. J Bone Miner Res 17:1–10

    Article  PubMed  CAS  Google Scholar 

  8. Watts NB, Cooper C, Lindsay R, Eastell R, Manhart MD, Barton IP, van Staa TP, Adachi JD (2004) Relationship between changes in bone mineral density and vertebral fracture risk associated with risedronate: greater increases in bone mineral density do not relate to greater decreases in fracture risk. J Clin Densitom 7:255–261

    Article  PubMed  Google Scholar 

  9. Kanis JA, McCloskey EV, Johansson H, Strom O, Borgstrom F, Oden A (2008) Case finding for the management of osteoporosis with FRAX—assessment and intervention thresholds for the UK. Osteoporos Int 19:1395–1408

    Article  PubMed  CAS  Google Scholar 

  10. Peel N, Eastell R (1993) Measurement of bone mass and turnover. Baillieres Clin Rheumatol 7:479–498

    Article  PubMed  CAS  Google Scholar 

  11. Christiansen C (1995) Osteoporosis: diagnosis and management today and tomorrow. Bone 17:513S–516S

    Article  PubMed  CAS  Google Scholar 

  12. Schuit SC, van der Klift M, Weel AE, de Laet CE, Burger H, Seeman E, Hofman A, Uitterlinden AG, van Leeuwen JP, Pols HA (2004) Fracture incidence and association with bone mineral density in elderly men and women: the Rotterdam Study. Bone 34:195–202

    Article  PubMed  CAS  Google Scholar 

  13. Kanis JA (2002) Diagnosis of osteoporosis and assessment of fracture risk. Lancet 359:1929–1936

    Article  PubMed  Google Scholar 

  14. Sornay-Rendu E, Munoz F, Garnero P, Duboeuf F, Delmas PD (2005) Identification of osteopenic women at high risk of fracture: the OFELY study. J Bone Miner Res 20:1813–1819

    Article  PubMed  Google Scholar 

  15. Chesnut CHIII, Silverman S, Andriano K, Genant H, Gimona A, Harris S, Kiel D, LeBoff M, Maricic M, Miller P, Moniz C, Peacock M, Richardson P, Watts N, Baylink D (2000) A randomized trial of nasal spray salmon calcitonin in postmenopausal women with established osteoporosis: the prevent recurrence of osteoporotic fractures study. PROOF Study Group. Am J Med 109:267–276

    Article  PubMed  CAS  Google Scholar 

  16. Chen P, Miller PD, Delmas PD, Misurski DA, Krege JH (2006) Change in lumbar spine BMD and vertebral fracture risk reduction in teriparatide-treated postmenopausal women with osteoporosis. J Bone Miner Res 21:1785–1790

    Article  PubMed  CAS  Google Scholar 

  17. Seeman E, Delmas PD (2006) Bone quality—the material and structural basis of bone strength and fragility. N Engl J Med 354:2250–2261

    Article  PubMed  CAS  Google Scholar 

  18. Viguet-Carrin S, Garnero P, Delmas PD (2006) The role of collagen in bone strength. Osteoporos Int 17:319–336

    Article  PubMed  CAS  Google Scholar 

  19. O'Brien FJ, Brennan O, Kennedy OD, Lee TC (2005) Microcracks in cortical bone: how do they affect bone biology? Curr Osteoporos Rep 3:39–45

    Article  PubMed  Google Scholar 

  20. Karsdal MA, Qvist P, Christiansen C, Tanko LB (2006) Optimising antiresorptive therapies in postmenopausal women: why do we need to give due consideration to the degree of suppression? Drugs 66:1909–1918

    Article  PubMed  Google Scholar 

  21. Compston J (2006) Bone quality: what is it and how is it measured? Arq Bras Endocrinol Metabol 50:579–585

    PubMed  Google Scholar 

  22. Viguet-Carrin S, Roux JP, Arlot ME, Merabet Z, Leeming DJ, Byrjalsen I, Delmas PD, Bouxsein ML (2006) Contribution of the advanced glycation end product pentosidine and of maturation of type I collagen to compressive biomechanical properties of human lumbar vertebrae. Bone 39:1073–1079

    Article  PubMed  CAS  Google Scholar 

  23. Byrjalsen I, Leeming DJ, Qvist P, Christiansen C, Karsdal MA (2008) Bone turnover and bone collagen maturation in osteoporosis: effects of antiresorptive therapies. Osteoporos Int 19:339–348

    Article  PubMed  CAS  Google Scholar 

  24. Ammann P, Badoud I, Barraud S, Dayer R, Rizzoli R (2007) Strontium ranelate treatment improves trabecular and cortical intrinsic bone tissue quality, a determinant of bone strength. J Bone Miner Res 22:1419–1425

    Article  PubMed  CAS  Google Scholar 

  25. Garnero P, Borel O, Gineyts E, Duboeuf F, Solberg H, Bouxsein ML, Christiansen C, Delmas PD (2006) Extracellular post-translational modifications of collagen are major determinants of biomechanical properties of fetal bovine cortical bone. Bone 38:300–309

    Article  PubMed  CAS  Google Scholar 

  26. Garnero P, Cloos P, Sornay-Rendu E, Qvist P, Delmas PD (2002) Type I collagen racemization and isomerization and the risk of fracture in postmenopausal women: the OFELY prospective study. J Bone Miner Res 17:826–833

    Article  PubMed  CAS  Google Scholar 

  27. Karsdal MA, Byrjalsen I, Leeming DJ, Delmas PD, Christiansen C (2007) The effects of oral calcitonin of bone collagen maturation: Implications for bone turnover and quality. Osteoporos Int 19:1355–1361

    Article  CAS  Google Scholar 

  28. Donahue SW, Galley SA (2006) Microdamage in bone: implications for fracture, repair, remodeling, and adaptation. Crit Rev Biomed Eng 34:215–271

    PubMed  Google Scholar 

  29. Burr DB (2002) Targeted and nontargeted remodeling. Bone 30:2–4

    Article  PubMed  CAS  Google Scholar 

  30. Benhamou CL (2007) Effects of osteoporosis medications on bone quality. Joint Bone Spine 74:39–47

    Article  PubMed  CAS  Google Scholar 

  31. Henriksen K, Leeming DJ, Byrjalsen I, Nielsen RH, Sorensen MG, Dziegiel MH, Martin TJ, Christiansen C, Qvist P, Karsdal MA (2007) Osteoclasts prefer aged bone. Osteoporos Int 18:751–759

    Article  PubMed  CAS  Google Scholar 

  32. Davison KS, Siminoski K, Adachi JD, Hanley DA, Goltzman D, Hodsman AB, Josse R, Kaiser S, Olszynski WP, Papaioannou A, Ste-Marie LG, Kendler DL, Tenenhouse A, Brown JP (2006) The effects of antifracture therapies on the components of bone strength: assessment of fracture risk today and in the future. Semin Arthritis Rheum 36:10–21

    Article  PubMed  CAS  Google Scholar 

  33. Davison KS, Siminoski K, Adachi JD, Hanley DA, Goltzman D, Hodsman AB, Josse R, Kaiser S, Olszynski WP, Papaioannou A, Ste-Marie LG, Kendler DL, Tenenhouse A, Brown JP (2006) Bone strength: the whole is greater than the sum of its parts. Semin Arthritis Rheum 36:22–31

    Article  PubMed  Google Scholar 

  34. Hernandez CJ (2008) How can bone turnover modify bone strength independent of bone mass? Bone 42:1014–1020

    Article  PubMed  CAS  Google Scholar 

  35. Ruppel ME, Miller LM, Burr DB (2008) The effect of the microscopic and nanoscale structure on bone fragility. Osteoporos Int 19:1251–1265

    Article  PubMed  CAS  Google Scholar 

  36. Hernandez CJ, Beaupre GS, Marcus R, Carter DR (2001) A theoretical analysis of the contributions of remodeling space, mineralization, and bone balance to changes in bone mineral density during alendronate treatment. Bone 29:511–516

    Article  PubMed  CAS  Google Scholar 

  37. Wasserman N, Yerramshetty J, Akkus O (2005) Microcracks colocalize within highly mineralized regions of cortical bone tissue. Eur J Morphol 42:43–51

    Article  PubMed  Google Scholar 

  38. Mori S, Harruff R, Ambrosius W, Burr DB (1997) Trabecular bone volume and microdamage accumulation in the femoral heads of women with and without femoral neck fractures. Bone 21:521–526

    Article  PubMed  CAS  Google Scholar 

  39. Schaffler MB, Choi K, Milgrom C (1995) Aging and matrix microdamage accumulation in human compact bone. Bone 17:521–525

    Article  PubMed  CAS  Google Scholar 

  40. Sobelman OS, Gibeling JC, Stover SM, Hazelwood SJ, Yeh OC, Shelton DR, Martin RB (2004) Do microcracks decrease or increase fatigue resistance in cortical bone? J Biomech 37:1295–1303

    Article  PubMed  CAS  Google Scholar 

  41. Danova NA, Colopy SA, Radtke CL, Kalscheur VL, Markel MD, Vanderby R, McCabe RP, Escarcega AJ, Muir P (2003) Degradation of bone structural properties by accumulation and coalescence of microcracks. Bone 33:197–205

    Article  PubMed  CAS  Google Scholar 

  42. Diab T, Sit S, Kim D, Rho J, Vashishth D (2005) Age-dependent fatigue behaviour of human cortical bone. Eur J Morphol 42:53–59

    Article  PubMed  CAS  Google Scholar 

  43. Martin TJ, Seeman E (2007) New mechanisms and targets in the treatment of bone fragility. Clin Sci (Lond) 112:77–91

    CAS  Google Scholar 

  44. Karsdal MA, Martin TJ, Bollerslev J, Christiansen C, Henriksen K (2007) Are nonresorbing osteoclasts sources of bone anabolic activity? J Bone Miner Res 22:487–494

    Article  PubMed  CAS  Google Scholar 

  45. Allen MR, Gineyts E, Leeming DJ, Burr DB, Delmas PD (2008) Bisphosphonates alter trabecular bone collagen cross-linking and isomerization in beagle dog vertebra. Osteoporos Int 19:329–337

    Article  PubMed  CAS  Google Scholar 

  46. Allen MR, Iwata K, Phipps R, Burr DB (2006) Alterations in canine vertebral bone turnover, microdamage accumulation, and biomechanical properties following 1-year treatment with clinical treatment doses of risedronate or alendronate. Bone 39:872–879

    Article  PubMed  CAS  Google Scholar 

  47. Tang SY, Allen MR, Phipps R, Burr DB, Vashishth D (2008) Changes in non-enzymatic glycation and its association with altered mechanical properties following 1-year treatment with risedronate or alendronate. Osteoporos Int doi:10.1007/s00198-008-0754-4

  48. Avery NC, Bailey AJ (2005) Enzymic and non-enzymic cross-linking mechanisms in relation to turnover of collagen: relevance to aging and exercise. Scand J Med Sci Sports 15:231–240

    Article  PubMed  CAS  Google Scholar 

  49. Wang X, Shen X, Li X, Agrawal CM (2002) Age-related changes in the collagen network and toughness of bone. Bone 31:1–7

    Article  PubMed  Google Scholar 

  50. Bonde M, Qvist P, Fledelius C, Riis BJ, Christiansen C (1994) Immunoassay for quantifying type I collagen degradation products in urine evaluated. Clin Chem 40:2022–2025

    PubMed  CAS  Google Scholar 

  51. Cloos PA, Christgau S (2004) Post-translational modifications of proteins: implications for aging, antigen recognition, and autoimmunity. Biogerontology 5:139–158

    Article  PubMed  CAS  Google Scholar 

  52. Fledelius C, Johnsen AH, Cloos PA, Bonde M, Qvist P (1997) Characterization of urinary degradation products derived from type I collagen. Identification of a beta-isomerized Asp-Gly sequence within the C-terminal telopeptide (alpha1) region. J Biol Chem 272:9755–9763

    Article  PubMed  CAS  Google Scholar 

  53. Cloos PA, Fledelius C (2000) Collagen fragments in urine derived from bone resorption are highly racemized and isomerized: a biological clock of protein aging with clinical potential. Biochem J 345(Pt 3):473–480

    Article  PubMed  CAS  Google Scholar 

  54. Garnero P, Delmas PD (2004) Contribution of bone mineral density and bone turnover markers to the estimation of risk of osteoporotic fracture in postmenopausal women. J Musculoskelet Neuronal Interact 4:50–63

    PubMed  CAS  Google Scholar 

  55. Cremers S, Garnero P (2006) Biochemical markers of bone turnover in the clinical development of drugs for osteoporosis and metastatic bone disease: potential uses and pitfalls. Drugs 66:2031–2058

    Article  PubMed  CAS  Google Scholar 

  56. Tolar J, Teitelbaum SL, Orchard PJ (2004) Osteopetrosis. N Engl J Med 351:2839–2849

    Article  PubMed  Google Scholar 

  57. Chavassieux P, Seeman E, Delmas PD (2007) Insights into material and structural basis of bone fragility from diseases associated with fractures: how determinants of the biomechanical properties of bone are compromised by disease. Endocr Rev 28:151–164

    Article  PubMed  CAS  Google Scholar 

  58. Balemans W, Patel N, Ebeling M, Van HE, Wuyts W, Lacza C, Dioszegi M, Dikkers FG, Hildering P, Willems PJ, Verheij JB, Lindpaintner K, Vickery B, Foernzler D, Van HW (2002) Identification of a 52 kb deletion downstream of the SOST gene in patients with van Buchem disease. J Med Genet 39:91–97

    Article  PubMed  CAS  Google Scholar 

  59. Balemans W, Ebeling M, Patel N, Van HE, Olson P, Dioszegi M, Lacza C, Wuyts W, Van Den EJ, Willems P, Paes-Alves AF, Hill S, Bueno M, Ramos FJ, Tacconi P, Dikkers FG, Stratakis C, Lindpaintner K, Vickery B, Foernzler D, Van HW (2001) Increased bone density in sclerosteosis is due to the deficiency of a novel secreted protein (SOST). Hum Mol Genet 10:537–543

    Article  PubMed  CAS  Google Scholar 

  60. Gardner JC, van Bezooijen RL, Mervis B, Hamdy NA, Lowik CW, Hamersma H, Beighton P, Papapoulos SE (2005) Bone mineral density in sclerosteosis; affected individuals and gene carriers. J Clin Endocrinol Metab 90:6392–6395

    Article  PubMed  CAS  Google Scholar 

  61. Ellies DL, Viviano B, McCarthy J, Rey JP, Itasaki N, Saunders S, Krumlauf R (2006) Bone density ligand, Sclerostin, directly interacts with LRP5 but not LRP5G171V to modulate Wnt activity. J Bone Miner Res 21:1738–1749

    Article  PubMed  CAS  Google Scholar 

  62. Van WL, Cleiren E, Gram J, Beals RK, Benichou O, Scopelliti D, Key L, Renton T, Bartels C, Gong Y, Warman ML, De Vernejoul MC, Bollerslev J, Van HW (2003) Six novel missense mutations in the LDL receptor-related protein 5 (LRP5) gene in different conditions with an increased bone density. Am J Hum Genet 72:763–771

    Article  Google Scholar 

  63. Boyden LM, Mao J, Belsky J, Mitzner L, Farhi A, Mitnick MA, Wu D, Insogna K, Lifton RP (2002) High bone density due to a mutation in LDL-receptor-related protein 5. N Engl J Med 346:1513–1521

    Article  PubMed  CAS  Google Scholar 

  64. Bollerslev J, Mosekilde L, Nielsen HK, Mosekilde L (1989) Biomechanical competence of iliac crest trabecular bone in autosomal dominant osteopetrosis type I. Bone 10:159–164

    Article  PubMed  CAS  Google Scholar 

  65. Alexandersen P, Peris P, Guanabens N, Byrjalsen I, Alvarez L, Solberg H, Cloos PA (2005) Non-isomerized C-telopeptide fragments are highly sensitive markers for monitoring disease activity and treatment efficacy in Paget's disease of bone. J Bone Miner Res 20:588–595

    Article  PubMed  CAS  Google Scholar 

  66. Martin TJ, Sims NA (2005) Osteoclast-derived activity in the coupling of bone formation to resorption. Trends Mol Med 11:76–81

    Article  PubMed  CAS  Google Scholar 

  67. Li J, Mashiba T, Burr DB (2001) Bisphosphonate treatment suppresses not only stochastic remodeling but also the targeted repair of microdamage. Calcif Tissue Int 69:281–286

    Article  PubMed  CAS  Google Scholar 

  68. Compston J (2007) Over-suppression of bone turnover: does it exist? Curr Osteoporos Rep 5:179–185

    Article  PubMed  Google Scholar 

  69. Rosen CJ, Chesnut CHIII, Mallinak NJ (1997) The predictive value of biochemical markers of bone turnover for bone mineral density in early postmenopausal women treated with hormone replacement or calcium supplementation. J Clin Endocrinol Metab 82:1904–1910

    Article  PubMed  CAS  Google Scholar 

  70. Fall PM, Kennedy D, Smith JA, Seibel MJ, Raisz LG (2000) Comparison of serum and urine assays for biochemical markers of bone resorption in postmenopausal women with and without hormone replacement therapy and in men. Osteoporos Int 11:481–485

    Article  PubMed  CAS  Google Scholar 

  71. Lindsay R, Gallagher JC, Kleerekoper M, Pickar JH (2005) Bone response to treatment with lower doses of conjugated estrogens with and without medroxyprogesterone acetate in early postmenopausal women. Osteoporos Int 16:372–379

    Article  PubMed  CAS  Google Scholar 

  72. Cauley JA, Robbins J, Chen Z, Cummings SR, Jackson RD, LaCroix AZ, LeBoff M, Lewis CE, McGowan J, Neuner J, Pettinger M, Stefanick ML, Wactawski-Wende J, Watts NB (2003) Effects of estrogen plus progestin on risk of fracture and bone mineral density: the Women's Health Initiative randomized trial. JAMA 290:1729–1738

    Article  PubMed  CAS  Google Scholar 

  73. Ettinger B, Black DM, Mitlak BH, Knickerbocker RK, Nickelsen T, Genant HK, Christiansen C, Delmas PD, Zanchetta JR, Stakkestad J, Gluer CC, Krueger K, Cohen FJ, Eckert S, Ensrud KE, Avioli LV, Lips P, Cummings SR (1999) Reduction of vertebral fracture risk in postmenopausal women with osteoporosis treated with raloxifene: results from a 3-year randomized clinical trial. Multiple Outcomes of Raloxifene Evaluation (MORE) Investigators. JAMA 282:637–645

    Article  PubMed  CAS  Google Scholar 

  74. Lufkin EG, Whitaker MD, Nickelsen T, Argueta R, Caplan RH, Knickerbocker RK, Riggs BL (1998) Treatment of established postmenopausal osteoporosis with raloxifene: a randomized trial. J Bone Miner Res 13:1747–1754

    Article  PubMed  CAS  Google Scholar 

  75. Johnell O, Kanis JA, Black DM, Balogh A, Poor G, Sarkar S, Zhou C, Pavo I (2004) Associations between baseline risk factors and vertebral fracture risk in the Multiple Outcomes of Raloxifene Evaluation (MORE) Study. J Bone Miner Res 19:764–772

    Article  PubMed  CAS  Google Scholar 

  76. Delmas PD, Recker RR, Chesnut CHIII, Skag A, Stakkestad JA, Emkey R, Gilbride J, Schimmer RC, Christiansen C (2004) Daily and intermittent oral ibandronate normalize bone turnover and provide significant reduction in vertebral fracture risk: results from the BONE study. Osteoporos Int 15:792–798

    Article  PubMed  CAS  Google Scholar 

  77. 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 (1996) Randomised trial of effect of alendronate on risk of fracture in women with existing vertebral fractures. Fracture Intervention Trial Research Group. Lancet 348:1535–1541

    Article  PubMed  CAS  Google Scholar 

  78. Bone HG, Hosking D, Devogelaer JP, 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

    Article  PubMed  CAS  Google Scholar 

  79. Lyles KW, Colon-Emeric CS, Magaziner JS, Adachi JD, Pieper CF, Mautalen C, Hyldstrup L, Recknor C, Nordsletten L, Moore KA, Lavecchia C, Zhang J, Mesenbrink P, Hodgson PK, Abrams K, Orloff JJ, Horowitz Z, Eriksen EF, Boonen S (2007) Zoledronic acid and clinical fractures and mortality after hip fracture. N Engl J Med 357:1799–1809

    Article  PubMed  CAS  Google Scholar 

  80. Black DM, Delmas PD, Eastell R, Reid IR, Boonen S, Cauley JA, Cosman F, Lakatos P, Leung PC, Man Z, Mautalen C, Mesenbrink P, Hu H, Caminis J, Tong K, Rosario-Jansen T, Krasnow J, Hue TF, Sellmeyer D, Eriksen EF, Cummings SR (2007) Once-yearly zoledronic acid for treatment of postmenopausal osteoporosis. N Engl J Med 356:1809–1822

    Article  PubMed  CAS  Google Scholar 

  81. Leeming DJ, Alexandersen P, Karsdal MA, Qvist P, Schaller S, Tanko LB (2006) An update on biomarkers of bone turnover and their utility in biomedical research and clinical practice. Eur J Clin Pharmacol 62:781–792

    Article  PubMed  CAS  Google Scholar 

  82. Allen MR, Hogan HA, Hobbs WA, Koivuniemi AS, Koivuniemi MC, Burr DB (2007) Raloxifene enhances material-level mechanical properties of femoral cortical and trabecular bone. Endocrinology 148:3908–3913

    Article  PubMed  CAS  Google Scholar 

  83. Allen MR, Iwata K, Sato M, Burr DB (2006) Raloxifene enhances vertebral mechanical properties independent of bone density. Bone 39:1130–1135

    Article  PubMed  CAS  Google Scholar 

  84. Sato M, Bryant HU, Iversen P, Helterbrand J, Smietana F, Bemis K, Higgs R, Turner CH, Owan I, Takano Y, Burr DB (1996) Advantages of raloxifene over alendronate or estrogen on nonreproductive and reproductive tissues in the long-term dosing of ovariectomized rats. J Pharmacol Exp Ther 279:298–305

    PubMed  CAS  Google Scholar 

  85. Allen MR, Follet H, Khurana M, Sato M, Burr DB (2006) Antiremodeling agents influence osteoblast activity differently in modeling and remodeling sites of canine rib. Calcif Tissue Int 79:255–261

    Article  PubMed  CAS  Google Scholar 

  86. Garnero P, Bauer D, Mareau E, Bilezikian J, Greenspan S, Rosen C, Black D (2008) Effects of parathyroid hormone and alendronate on type I collagen isomerization in postmenopausal women with osteoporosis: the PaTH study. J Bone Miner Res 23:1442–1448

    Article  PubMed  CAS  Google Scholar 

  87. Kung AW, Pasion EG, Sofiyan M, Lau EM, Tay BK, Lam KS, Wilawan K, Ongphiphadhanakul B, Thiebaud D (2006) A comparison of teriparatide and calcitonin therapy in postmenopausal Asian women with osteoporosis: a 6-month study. Curr Med Res Opin 22:929–937

    Article  PubMed  CAS  Google Scholar 

  88. Hwang JS, Tu ST, Yang TS, Chen JF, Wang CJ, Tsai KS (2006) Teriparatide vs. calcitonin in the treatment of Asian postmenopausal women with established osteoporosis. Osteoporos Int 17:373–378

    Article  PubMed  CAS  Google Scholar 

  89. Trovas GP, Lyritis GP, Galanos A, Raptou P, Constantelou E (2002) A randomized trial of nasal spray salmon calcitonin in men with idiopathic osteoporosis: effects on bone mineral density and bone markers. J Bone Miner Res 17:521–527

    Article  PubMed  CAS  Google Scholar 

  90. Karsdal MA, Henriksen K, Arnold M, Christiansen C (2008) Calcitonin: a drug of the past or for the future? Physiologic inhibition of bone resorption while sustaining osteoclast numbers improves bone quality. BioDrugs 22:137–144

    Article  PubMed  CAS  Google Scholar 

  91. Segovia-Silvestre T, Neutzsky-Wulff AV, Sorensen MG, Christiansen C, Bollerslev J, Karsdal MA, Henriksen K (2009) Advances in osteoclast biology resulting from the study of osteopetrotic mutations. Hum Genet 124:561–577

    Article  PubMed  CAS  Google Scholar 

  92. Silverman SL, Watts NB, Delmas PD, Lange JL, Lindsay R (2007) Effectiveness of bisphosphonates on nonvertebral and hip fractures in the first year of therapy: the risedronate and alendronate (REAL) cohort study. Osteoporos Int 18:25–34

    Article  PubMed  CAS  Google Scholar 

  93. Boonen S, Laan RF, Barton IP, Watts NB (2005) Effect of osteoporosis treatments on risk of non-vertebral fractures: review and meta-analysis of intention-to-treat studies. Osteoporos Int 16:1291–1298

    Article  PubMed  Google Scholar 

  94. Hochberg MC, Greenspan S, Wasnich RD, Miller P, Thompson DE, Ross PD (2002) Changes in bone density and turnover explain the reductions in incidence of nonvertebral fractures that occur during treatment with antiresorptive agents. J Clin Endocrinol Metab 87:1586–1592

    Article  PubMed  CAS  Google Scholar 

  95. Reginster J, Minne HW, Sorensen OH, Hooper M, Roux C, Brandi ML, Lund B, Ethgen D, Pack S, Roumagnac I, Eastell R (2000) Randomized trial of the effects of risedronate on vertebral fractures in women with established postmenopausal osteoporosis. Vertebral Efficacy with Risedronate Therapy (VERT) Study Group. Osteoporos Int 11:83–91

    Article  PubMed  CAS  Google Scholar 

  96. Durchschlag E, Paschalis EP, Zoehrer R, Roschger P, Fratzl P, Recker R, Phipps R, Klaushofer K (2006) Bone material properties in trabecular bone from human iliac crest biopsies after 3- and 5-year treatment with risedronate. J Bone Miner Res 21:1581–1590

    Article  PubMed  CAS  Google Scholar 

  97. Reginster JY, Sarkar S, Zegels B, Henrotin Y, Bruyere O, Agnusdei D, Collette J (2004) Reduction in PINP, a marker of bone metabolism, with raloxifene treatment and its relationship with vertebral fracture risk. Bone 34:344–351

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We acknowledge the funding from the Danish “Ministry of Science, Technology and Science”.

Conflicts of interest

Leeming DJ, Henriksen K, Byrjalsen I, Qvist P, Madsen SH, and Karsdal MA are employees of Nordic Bioscience.

Author information

Authors and Affiliations

  1. Nordic Bioscience, Herlev Hovedgade 207, 2730, Herlev, Denmark

    D. J. Leeming, K. Henriksen, I. Byrjalsen, P. Qvist, S. H. Madsen & M. A. Karsdal

  2. CCBR-Synarc, Lyon, France

    P. Garnero

  3. INSERM, Unit 664, Lyon, France

    P. Garnero

Authors
  1. D. J. Leeming
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. Henriksen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. Byrjalsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. Qvist
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. H. Madsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. P. Garnero
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. A. Karsdal
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. J. Leeming.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Leeming, D.J., Henriksen, K., Byrjalsen, I. et al. Is bone quality associated with collagen age?. Osteoporos Int 20, 1461–1470 (2009). https://doi.org/10.1007/s00198-009-0904-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-009-0904-3

Keywords

Search

Navigation