Calcified Tissue International

, Volume 87, Issue 6, pp 469–484 | Cite as

Impact of Treatments for Postmenopausal Osteoporosis (Bisphosphonates, Parathyroid Hormone, Strontium Ranelate, and Denosumab) on Bone Quality: A Systematic Review

REVIEW

Abstract

The objective of this systematic review was to examine the influence of treatments for postmenopausal osteoporosis (parathyroid hormone [PTH], bisphosphonates, strontium ranelate, and denosumab) on bone quality and discuss the clinical implications. Most bone-quality data for PTH is from teriparatide. Teriparatide results in a rapid increase in bone-formation markers, followed by increases in bone-resorption markers, opening an “anabolic window,” a period of time when PTH is maximally anabolic. Teriparatide reverses the structural damage seen in osteoporosis and restores the structure of trabecular bone. It has a positive effect on cortical bone, and any early increases in cortical porosity appear to be offset by increases in cortical thickness and diameter. Bisphosphonates are antiresorptive agents which reduce bone turnover, improve trabecular microarchitecture, and mineralization. Concerns have been raised that the prolonged antiresorptive action of bisphosphonates may lead to failure to repair microdamage, resulting in microcracks and atypical fragility. Strontium ranelate is thought to have a mixed mode of action, increasing bone formation and decreasing bone resorption. Strontium ranelate improves cortical thickness, trabecular number, and connectivity, with no change in cortical porosity. Denosumab exerts rapid, marked, and sustained effects on bone resorption, resulting in falls in the markers of bone turnover. Evidence from bone-quality studies suggests that treatment-naive women, aged 60–65 years, with very low BMD T scores may benefit from PTH as primary therapy to improve bone substrate and build bone. Post-PTH treatment with bisphosphonates will maintain improvements in bone quality and reduce the risk of fracture.

Keywords

Bone quality Osteoporosis Teriparatide Bisphosphonate Strontium ranelate Denosumab 

Notes

Acknowledgment

This study was supported by Eli-Lilly and Co., which provided a fee for one of the authors (T. D.).

References

  1. 1.
    Delmas PD, Seeman E (2004) Changes in bone mineral density explain little of the reduction in vertebral or nonvertebral fracture risk with antiresorptive therapy. Bone 34:599–604CrossRefPubMedGoogle Scholar
  2. 2.
    Siris ES, Chen YT, Abbott TA, Barrett-Connor E, Miller PD, Wehren LE et al (2004) Bone mineral density thresholds for pharmacological intervention to prevent fractures. Arch Intern Med 164:1108–1112CrossRefPubMedGoogle Scholar
  3. 3.
    Chen P, Miller PD, Recker R, Resch H, Rana A, Pavo I et al (2007) Increases in BMD correlate with improvements in bone microarchitecture with teriparatide treatment in postmenopausal women with osteoporosis. J Bone Miner Res 22:1173–1180CrossRefPubMedGoogle Scholar
  4. 4.
    Stepan JJ, Burr DB, Pavo I, Sipos A, Michalska D, Li J et al (2007) Low bone mineral density is associated with bone microdamage accumulation in postmenopausal women with osteoporosis. Bone 41:378–385CrossRefPubMedGoogle Scholar
  5. 5.
    Kwek EB, Goh SK, Koh JS, Png MA, Howe TS (2008) An emerging pattern of subtrochanteric stress fractures: a long-term complication of alendronate therapy? Injury 39:224–231CrossRefPubMedGoogle Scholar
  6. 6.
    Odvina CV, Zerwekh JE, Rao DS, Maalouf N, Gottschalk FA, Pak CY (2005) Severely suppressed bone turnover: a potential complication of alendronate therapy. J Clin Endocrinol Metab 90:1294–1301CrossRefPubMedGoogle Scholar
  7. 7.
    Visekruna M, Wilson D, McKiernan FE (2008) Severely suppressed bone turnover and atypical skeletal fragility. J Clin Endocrinol Metab 93:2948–2952CrossRefPubMedGoogle Scholar
  8. 8.
    Khan AA, Sándor GK, Dore E, Morrison AD, Alsahli M, Amin F, Canadian Taskforce on Osteonecrosis of the Jaw et al (2009) Bisphosphonate associated osteonecrosis of the jaw. J Rheumatol 36:478–490CrossRefPubMedGoogle Scholar
  9. 9.
    Khan A (2010) Osteonecrosis of the jaw and bisphosphonates. BMJ 340:c246CrossRefPubMedGoogle Scholar
  10. 10.
    Khosla S, Burr D, Cauley J, Dempster DW, Ebeling PR, Felsenberg D, American Society for Bone and Mineral Research et al (2007) Bisphosphonate-associated osteonecrosis of the jaw: report of a task force of the American Society for Bone and Mineral Research. J Bone Miner Res 22:1479–1491CrossRefPubMedGoogle Scholar
  11. 11.
    Szulc P, Seeman E (2009) Thinking inside and outside the envelopes of bone: dedicated to PDD. Osteoporos Int 20:1281–1288CrossRefPubMedGoogle Scholar
  12. 12.
    Compston JE (2007) Skeletal actions of intermittent parathyroid hormone: effects on bone remodeling and structure. Bone 40:1447–1452CrossRefPubMedGoogle Scholar
  13. 13.
    Reszka AA, Rodan GA (2003) Bisphosphonate mechanism of action. Curr Rheumatol Rep 5:65–74CrossRefPubMedGoogle Scholar
  14. 14.
    Brown JP, Prince RL, Deal C, Recker RR, Kiel DP, de Gregorio LH et al (2009) Comparison of the effect of denosumab and alendronate on BMD and biochemical markers of bone turnover in postmenopausal women with low bone mass: a randomized, blinded, phase 3 trial. J Bone Miner Res 24:153–161CrossRefPubMedGoogle Scholar
  15. 15.
    Marie PJ (2006) Strontium ranelate: a dual mode of action rebalancing bone turnover in favour of bone formation. Curr Opin Rheumatol 18(Suppl 1):S11–S15CrossRefPubMedGoogle Scholar
  16. 16.
    Meunier PJ, Roux C, Seeman E, Ortolani S, Badurski JE, Spector TD et al (2004) The effects of strontium ranelate on the risk of vertebral fracture in women with postmenopausal osteoporosis. N Engl J Med 350:459–468CrossRefPubMedGoogle Scholar
  17. 17.
    Neer RM, Arnaud CD, Zanchetta JR, Prince R, Gaich GA, Reginster JY et al (2001) Effect of parathyroid hormone (1–34) on fractures and bone mineral density in postmenopausal women with osteoporosis. N Engl J Med 344:1434–1441CrossRefPubMedGoogle Scholar
  18. 18.
    Dobnig H, Sipos A, Jiang Y, Fahrleitner-Pammer A, Ste-Marie LG, Gallagher JC et al (2005) Early changes in biochemical markers of bone formation correlate with improvements in bone structure during teriparatide therapy. J Clin Endocrinol Metab 90:3970–3977CrossRefPubMedGoogle Scholar
  19. 19.
    Bilezikian JP (2008) Combination anabolic and antiresorptive therapy for osteoporosis: opening the anabolic window. Curr Osteoporos Rep 6:24–30CrossRefPubMedGoogle Scholar
  20. 20.
    Hodsman AB, Kisiel M, Adachi JD, Fraher LJ, Watson PH (2000) Histomorphometric evidence for increased bone turnover without change in cortical thickness or porosity after 2 years of cyclical hPTH(1–34) therapy in women with severe osteoporosis. Bone 27:311–318CrossRefPubMedGoogle Scholar
  21. 21.
    Ma YL, Zeng Q, Donley DW, Ste-Marie LG, Gallagher JC, Dalsky GP et al (2006) Teriparatide increases bone formation in modeling and remodeling osteons and enhances IGF-II immunoreactivity in postmenopausal women with osteoporosis. J Bone Miner Res 21:855–864CrossRefPubMedGoogle Scholar
  22. 22.
    Lindsay R, Zhou H, Cosman F, Nieves J, Dempster DW, Hodsman AB (2007) 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 22:495–502CrossRefPubMedGoogle Scholar
  23. 23.
    Anastasilakis AD, Goulis DG, Polyzos SA, Gerou S, Pavlidou V, Koukoulis G et al (2008) Acute changes in serum osteoprotegerin and receptor activator for nuclear factor-kappaB ligand levels in women with established osteoporosis treated with teriparatide. Eur J Endocrinol 158:411–415CrossRefPubMedGoogle Scholar
  24. 24.
    Jiang Y, Zhao JJ, Mitlak BH, Wang O, Genant HK, Eriksen EF (2003) Recombinant human parathyroid hormone (1–34) [teriparatide] improves both cortical and cancellous bone structure. J Bone Miner Res 18:1932–1941CrossRefPubMedGoogle Scholar
  25. 25.
    Graeff C, Timm W, Nickelsen TN, Farrerons J, Marín F, Barker C, EUROFORS High Resolution Computed Tomography Substudy Group et al (2007) Monitoring teriparatide-associated changes in vertebral microstructure by high-resolution CT in vivo: results from the EUROFORS study. J Bone Miner Res 22:1426–1433CrossRefPubMedGoogle Scholar
  26. 26.
    Recker RR, Bare SP, Smith SY, Varela A, Miller MA, Morris SA (2009) Cancellous and cortical bone architecture and turnover at the iliac crest of postmenopausal osteoporotic women treated with parathyroid hormone 1–84. Bone 44:113–119CrossRefPubMedGoogle Scholar
  27. 27.
    Hodsman AB, Bauer DC, Dempster DW, Dian L, Hanley DA, Harris ST et al (2005) Parathyroid hormone and teriparatide for the treatment of osteoporosis: a review of the evidence and suggested guidelines for its use. Endocr Rev 26:688–703CrossRefPubMedGoogle Scholar
  28. 28.
    Hyldstrup L, Jorgensen JT, Gaich G (2002) Assessment of effects of ly333334 [recombinant human parathyroid hormone (1–34)] on cortical bone using digital X-ray radiogrammetry. Bone 28:S97Google Scholar
  29. 29.
    Borggrefe J, Graeff C, Nickelsen TN, Marin F, Glüer CC (2009) Quantitative computed tomography assessment of the effects of 24 months of teriparatide treatment on 3-D femoral neck bone distribution, geometry and bone strength: results from the EUROFORS study. J Bone Miner Res 25:472–481CrossRefGoogle Scholar
  30. 30.
    Paschalis EP, Glass EV, Donley DW, Eriksen EF (2005) Bone mineral and collagen quality in iliac crest biopsies of patients given teriparatide: new results from the fracture prevention trial. J Clin Endocrinol Metab 90:4644–4649CrossRefPubMedGoogle Scholar
  31. 31.
    Uusi-Rasi K, Semanick LM, Zanchetta JR, Bogado CE, Eriksen EF, Sato M et al (2005) Effects of teriparatide [rhPTH (1–34)] treatment on structural geometry of the proximal femur in elderly osteoporotic women. Bone 36:948–958CrossRefPubMedGoogle Scholar
  32. 32.
    Zanchetta JR, Bogado CE, Ferretti JL, Wang O, Wilson MG, Sato M et al (2003) Effects of teriparatide [recombinant human parathyroid hormone (1–34)] on cortical bone in postmenopausal women with osteoporosis. J Bone Miner Res 18:539–543CrossRefPubMedGoogle Scholar
  33. 33.
    Xiong Y, Yang HJ, Feng J, Shi ZL, Wu LD (2009) Effects of alendronate on the proliferation and osteogenic differentiation of MG-63 cells. J Int Med Res 37:407–416PubMedGoogle Scholar
  34. 34.
    Wells GA, Cranney A, Peterson J, Boucher M, Shea B, Welch V et al (2008) Alendronate for the primary and secondary prevention of osteoporotic fractures in postmenopausal women. Cochrane Database Syst Rev 1:CD001155. doi: 10.1002/14651858.CD001155.pub2
  35. 35.
    Wells GA, Cranney A, Peterson J, Boucher M, Shea B, Welch V et al (2008) Risedronate for the primary and secondary prevention of osteoporotic fractures in postmenopausal women. Cochrane Database Syst Rev 1: CD004523. doi: 10.1002/14651858.CD004523.pub3
  36. 36.
    Black DM, Delmas PD, Eastell R, Reid IR, Boonen S, Cauley JA, for HORIZON Pivotal Fracture Trial et al (2007) Once-yearly zoledronic acid for treatment of postmenopausal osteoporosis. N Engl J Med 356:1809–1822CrossRefPubMedGoogle Scholar
  37. 37.
    Chesnut CH III, Skag A, Christiansen C, Recker R, Stakkestad JA, Hoiseth A, for the Oral Ibandronate Osteoporosis Vertebral Fracture Trial in North America, Europe (BONE) et al (2004) Effects of oral ibandronate administered daily or intermittently on fracture risk in postmenopausal osteoporosis. J Bone Miner Res 19:1241–1249CrossRefGoogle Scholar
  38. 38.
    Seeman E (2009) To stop or not to stop, that is the question. Osteoporos Int 20:187–195CrossRefPubMedGoogle Scholar
  39. 39.
    Recker R, Masarachia P, Santora A, Howard T, Chavassieux P, Arlot M et al (2005) Trabecular bone microarchitecture after alendronate treatment of osteoporotic women. Curr Med Res Opin 21:185–194CrossRefPubMedGoogle Scholar
  40. 40.
    Dufresne TE, Chmielewski PA, Manhart MD, Johnson TD, Borah B (2003) Risedronate preserves bone architecture in early postmenopausal women in 1 year as measured by three-dimensional microcomputed tomography. Calcif Tissue Int 73:423–432CrossRefPubMedGoogle Scholar
  41. 41.
    Durchschlag E, Paschalis EP, Zoehrer R, Roschger P, Fratzl P, Recker R et al (2006) Bone material properties in trabecular bone from human iliac crest biopsies after 3- and 5-year treatment with risedronate. J Bone Miner Res 21:1581–1590CrossRefPubMedGoogle Scholar
  42. 42.
    Borah B, Dufresne TE, Chmielewski PA, Johnson TD, Chines A, Manhart MD (2004) Risedronate preserves bone architecture in postmenopausal women with osteoporosis as measured by three-dimensional microcomputed tomography. Bone 34:736–746CrossRefPubMedGoogle Scholar
  43. 43.
    Roschger P, Rinnerthaler S, Yates J, Rodan GA, Fratzl P, Klaushofer K (2001) Alendronate increases degree and uniformity of mineralization in cancellous bone and decreases the porosity in cortical bone of osteoporotic women. Bone 29:185–191CrossRefPubMedGoogle Scholar
  44. 44.
    Recker RR, Delmas PD, Halse J, Reid IR, Boonen S, García-Hernandez PA et al (2008) Effects of intravenous zoledronic acid once yearly on bone remodeling and bone structure. J Bone Miner Res 23:6–16CrossRefPubMedGoogle Scholar
  45. 45.
    Boivin GY, Chavassieux PM, Santora AC, Yates J, Meunier PJ (2000) Alendronate increases bone strength by increasing the mean degree of mineralization of bone tissue in osteoporotic women. Bone 27:687–694CrossRefPubMedGoogle Scholar
  46. 46.
    Borah B, Ritman EL, Dufresne TE, Jorgensen SM, Liu S, Sacha J et al (2005) The effect of risedronate on bone mineralization as measured by micro-computed tomography with synchrotron radiation: correlation to histomorphometric indices of turnover. Bone 37:1–9CrossRefPubMedGoogle Scholar
  47. 47.
    Borah B, Dufresne TE, Ritman EL, Jorgensen SM, Liu S, Chmielewski PA et al (2006) Long-term risedronate treatment normalizes mineralization and continues to preserve trabecular architecture: sequential triple biopsy studies with micro-computed tomography. Bone 39:345–352CrossRefPubMedGoogle Scholar
  48. 48.
    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 100:1475–1480CrossRefPubMedGoogle Scholar
  49. 49.
    Eriksen EF, Melsen F, Sod E, Barton I, Chines A (2002) Effects of long-term risedronate on bone quality and bone turnover in women with postmenopausal osteoporosis. Bone 3:620–625CrossRefGoogle Scholar
  50. 50.
    Zoehrer R, Roschger P, Paschalis EP, Hofstaetter JG, Durchschlag E, Fratzl P et al (2006) Effects of 3- and 5-year treatment with risedronate on bone mineralization density distribution in triple biopsies of the iliac crest in postmenopausal women. J Bone Miner Res 21:1106–1112CrossRefPubMedGoogle Scholar
  51. 51.
    Roschger P, Lombardi A, Misof BM, Maier G, Fratzl-Zelman N, Fratzl P et al (2010) 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 25:48–55CrossRefPubMedGoogle Scholar
  52. 52.
    Recker RR, Weinstein RS, Chesnut CH III, Schimmer RC, Mahoney P, Hughes C et al (2004) Histomorphometric evaluation of daily and intermittent oral ibandronate in women with postmenopausal osteoporosis: results from the BONE study. Osteoporos Int 15:231–237CrossRefPubMedGoogle Scholar
  53. 53.
    McClung M, Recker R, Miller P, Fiske D, Minkoff J, Kriegman A et al (2007) Intravenous zoledronic acid 5 mg in the treatment of postmenopausal women with low bone density previously treated with alendronate. Bone 41:122–128CrossRefPubMedGoogle Scholar
  54. 54.
    Boskey AL, Spevak L, Weinstein RS (2009) Spectroscopic markers of bone quality in alendronate-treated postmenopausal women. Osteoporos Int 20:793–800CrossRefPubMedGoogle Scholar
  55. 55.
    Iba K, Takada J, Hatakeyama N, Ozasa Y, Wada T, Yamashita T (2008) Changes in urinary NTX levels in patients with primary osteoporosis undergoing long-term bisphosphonate treatment. J Orthop Sci 13:438–441CrossRefPubMedGoogle Scholar
  56. 56.
    Chapurlat RD, Arlot M, Burt-Pichat B, Chavassieux P, Roux JP, Portero-Muzy N et al (2007) Microcrack frequency and bone remodeling in postmenopausal osteoporotic women on long-term bisphosphonates: a bone biopsy study. J Bone Miner Res 22:1502–1509CrossRefPubMedGoogle Scholar
  57. 57.
    Chapurlat RD, Delmas PD (2009) Bone microdamage: a clinical perspective. Osteoporos Int 20:1299–1308CrossRefPubMedGoogle Scholar
  58. 58.
    Black DM, Kelly MP, Genant HK, Palermo L, Eastell R, Bucci-Rechtweg C, the Fracture Intervention Trial and HORIZON Pivotal Fracture Trial Steering Committees et al (2010) Bisphosphonates and fractures of the subtrochanteric or diaphyseal femur. N Engl J Med 362:1761–1771CrossRefPubMedGoogle Scholar
  59. 59.
    Shane E (2010) Evolving data about subtrochanteric fractures and bisphosphonates. N Engl J Med 362:1825–1827CrossRefPubMedGoogle Scholar
  60. 60.
    Arlot M, Meunier PJ, Boivin G, Haddock L, Tamayo J, Correa-Rotter R et al (2005) Differential effects of teriparatide and alendronate on bone remodeling in postmenopausal women assessed by histomorphometric parameters. J Bone Miner Res 20:1244–1253CrossRefPubMedGoogle Scholar
  61. 61.
    Keaveny TM, Donley DW, Hoffmann PF, Mitlak BH, Glass EV, San Martin JA (2007) Effects of teriparatide and alendronate on vertebral strength as assessed by finite element modeling of QCT scans in women with osteoporosis. J Bone Miner Res 22:149–157CrossRefPubMedGoogle Scholar
  62. 62.
    Fonseca JE (2008) Rebalancing bone turnover in favour of formation with strontium ranelate: implications for bone strength. Rheumatology (Oxford) 47(Suppl 4):iv17–iv19Google Scholar
  63. 63.
    Anastasilakis AD, Goulis DG, Polyzos SA, Gerou S, Ballaouri I, Efstathiadou Z et al (2009) No difference between strontium ranelate (SR) and calcium/vitamin D on bone turnover markers in women with established osteoporosis previously treated with teriparatide: a randomized controlled trial. Clin Endocrinol (Oxf) 70:522–526CrossRefGoogle Scholar
  64. 64.
    Anastasilakis AD, Polyzos SA, Avramidis A, Papatheodorou A, Terpos E (2009) Effect of strontium ranelate on lumbar spine bone mineral density in women with established osteoporosis previously treated with teriparatide. Horm Metab Res 41:559–562CrossRefPubMedGoogle Scholar
  65. 65.
    O’Donnell S, Cranney A, Wells GA, Adachi J, Reginster JY (2006) Strontium ranelate for preventing and treating postmenopausal osteoporosis. Cochrane Database Syst Rev 4:CD005326. doi: 10.1002/14651858.CD005326.pub3
  66. 66.
    Reginster JY, Seeman E, De Vernejoul MC, Adami S, Compston J, Phenekos C et al (2005) Strontium ranelate reduces the risk of nonvertebral fractures in postmenopausal women with osteoporosis: Treatment of Peripheral Osteoporosis (TROPOS) study. J Clin Endocrinol Metab 90:2816–2822CrossRefPubMedGoogle Scholar
  67. 67.
    Arlot ME, Jiang Y, Genant HK, Zhao J, Burt-Pichat B, Roux JP et al (2008) Histomorphometric and microCT analysis of bone biopsies from postmenopausal osteoporotic women treated with strontium ranelate. J Bone Miner Res 23:215–222CrossRefPubMedGoogle Scholar
  68. 68.
    Roschger P, Manjubala I, Zoeger N, Meirer F, Simon R et al (2010) Bone material quality in transiliac bone biopsies of postmenopausal osteoporotic women after 3 years of strontium ranelate treatment. J Bone Miner Res 25:891–900CrossRefPubMedGoogle Scholar
  69. 69.
    Boivin G, Farlay D, Khebbab MT, Jaurand X, Delmas PD, Meunier PJ (2010) In osteoporotic women treated with strontium ranelate, strontium is located in bone formed during treatment with a maintained degree of mineralization. Osteoporos Int 21:667–677CrossRefPubMedGoogle Scholar
  70. 70.
    Tankó LB (2007) Effect of RANKL-specific denosumab on osteoclast number and function: a potential friend or foe? Curr Opin Investig Drugs 8:830–835PubMedGoogle Scholar
  71. 71.
    Cummings SR, San Martin J, McClung MR, Siris ES, Eastell R, Reid IR, FREEDOM Trial et al (2009) Denosumab for prevention of fractures in postmenopausal women with osteoporosis. N Engl J Med 361:756–765CrossRefPubMedGoogle Scholar
  72. 72.
    Beck TJ, Lewiecki EM, Miller PD, Felsenberg D, Liu Y, Ding B (2008) Effects of denosumab on the geometry of the proximal femur in postmenopausal women in comparison with alendronate. J Clin Densitom 11:351–359CrossRefPubMedGoogle Scholar
  73. 73.
    Kendler DL, Roux C, Benhamou CL, Brown JP, Lillestol M, Siddhanti S et al (2009) Effects of denosumab on bone mineral density and bone turnover in postmenopausal women transitioning from alendronate therapy. J Bone Miner Res 25:72–81CrossRefGoogle Scholar
  74. 74.
    Delmas PD, Licata AA, Reginster JY, Crans GG, Chen P, Misurski DA et al (2006) Fracture risk reduction during treatment with teriparatide is independent of pretreatment bone turnover. Bone 39:237–243CrossRefPubMedGoogle Scholar
  75. 75.
    Boonen S, Marin F, Obermayer-Pietsch B, Simoes ME, Barker C, Glass EV et al (2008) Effects of previous antiresorptive therapy on the bone mineral density response to two years of teriparatide treatment in postmenopausal women with osteoporosis. J Clin Endocrinol Metab 93:852–860CrossRefPubMedGoogle Scholar
  76. 76.
    Miller PD, Delmas PD, Lindsay R, Watts NB, Luckey M, Adachi J et al (2008) Early responsiveness of women with osteoporosis to teriparatide after therapy with alendronate or risedronate. J Clin Endocrinol Metab 93:3785–3793CrossRefPubMedGoogle Scholar
  77. 77.
    Middleton ET, Steel SA, Doherty SM (2007) The effect of prior bisphosphonate exposure on the treatment response to teriparatide in clinical practice. Calcif Tissue Int 81:335–340CrossRefPubMedGoogle Scholar
  78. 78.
    Obermayer-Pietsch BM, Marin F, McCloskey EV, Hadji P, Farrerons J, Boonen S, EUROFORS Investigators et al (2008) Effects of two years of daily teriparatide treatment on BMD in postmenopausal women with severe osteoporosis with and without prior antiresorptive treatment. J Bone Miner Res 10:1591–1600CrossRefGoogle Scholar
  79. 79.
    Jobke B, Pfeifer M, Minne HW (2009) Teriparatide following bisphosphonates: initial and long-term effects on microarchitecture and bone remodeling at the human iliac crest. Connect Tissue Res 50:46–54CrossRefPubMedGoogle Scholar
  80. 80.
    Dobnig H, Stepan JJ, Burr DB, Li J, Michalska D, Sipos A et al (2009) Teriparatide reduces bone microdamage accumulation in postmenopausal women previously treated with alendronate. J Bone Miner Res 24:1998–2006CrossRefPubMedGoogle Scholar
  81. 81.
    Leder BZ, Neer RM, Wyland JJ, Lee HW, Burnett-Bowie SA, Finkelstein JS (2009) Effects of teriparatide treatment and discontinuation in postmenopausal women and eugonadal men with osteoporosis. J Clin Endocrinol Metab 94:2915–2921CrossRefPubMedGoogle Scholar
  82. 82.
    Finkelstein JS, Wyland JJ, Leder BZ, Burnett-Bowie SM, Lee H, Jüppner H et al (2009) Effects of teriparatide retreatment in osteoporotic men and women. J Clin Endocrinol Metab 94:2495–2501CrossRefPubMedGoogle Scholar
  83. 83.
    Rittmaster RS, Bolognese M, Ettinger MP, Hanley DA, Hodsman AB, Kendler DL et al (2000) Enhancement of bone mass in osteoporotic women with parathyroid hormone followed by alendronate. J Clin Endocrinol Metab 85:2129–2134CrossRefPubMedGoogle Scholar
  84. 84.
    Black DM, Greenspan SL, Ensrud KE, Palermo L, McGowan JA, Lang TF, PaTH Study Investigators et al (2003) The effects of parathyroid hormone and alendronate alone or in combination in postmenopausal osteoporosis. N Engl J Med 349:1207–1215CrossRefPubMedGoogle Scholar
  85. 85.
    Black DM, Bilezikian JP, Ensrud KE, Greenspan SL, Palermo L, Hue T et al (2005) One year of alendronate after one year of parathyroid hormone (1–84) for osteoporosis. N Engl J Med 353:555–565CrossRefPubMedGoogle Scholar
  86. 86.
    Keaveny TM, Hoffmann PF, Singh M, Palermo L, Bilezikian JP, Greenspan SL et al (2008) Femoral bone strength and its relation to cortical and trabecular changes after treatment with PTH, alendronate, and their combination as assessed by finite element analysis of quantitative CT scans. J Bone Miner Res 23:1974–1982CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Southern General HospitalGlasgowUK
  2. 2.JB Medical, Ltd.SudburyUK

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