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Calcified Tissue International

, Volume 101, Issue 4, pp 396–403 | Cite as

Effects of Teriparatide and Sequential Minodronate on Lumbar Spine Bone Mineral Density and Microarchitecture in Osteoporosis

  • Daichi Miyaoka
  • Yasuo Imanishi
  • Masaya Ohara
  • Noriyuki Hayashi
  • Yuki Nagata
  • Shinsuke Yamada
  • Katsuhito Mori
  • Masanori Emoto
  • Masaaki Inaba
Original Research

Abstract

The trabecular bone score (TBS) is a new surrogate for trabecular bone microarchitecture assessment, independent of bone mineral density (BMD), calculated from pixel gray-level variations in the lumbar spine (LS) dual-energy X-ray absorptiometry (DXA) image. Although Teriparatide (TPTD) increased LS-BMD as well as TBS in 2 years, the precise time-course of these parameters was not well known. The aim of this study was to determine the changes in LS-BMD and the TBS in osteoporotic patients treated with TPTD, followed by minodronate (MINO). Primary osteoporotic patients with a low LS-BMD (T-score < −2.5) and/or at least one vertebral fracture were treated with TPTD subcutaneously at 20 µg/day for 12–24 months, followed by MINO (orally at 50 mg/once monthly) for 12 months. LS-BMD and the TBS were measured at 0, 3, 6, 12, and 24 months after the initiation of TPTD treatment, and 12 months after the initiation of MINO. The increments of LS-BMD, significant at 6 months, increased until 12 months, whereas the increments of TBS, significant at 3 months (0.035 ± 0.011; p = 0.045 vs. the baseline), stabilized until 12 months. TPTD treatment, followed by 12 months of MINO, maintained both BMD and the TBS. Comparing the increments of the TBS to those of LS-BMD, our results indicate that TPTD treatment improved trabecular microarchitecture faster than mineralization. TPTD treatment, followed by MINO, can maintain both BMD and the TBS.

Keywords

Osteoporosis Teriparatide Minodronate Bone mineral density Trabecular bone score 

Notes

Acknowledgements

DM contributed to the acquisition, analysis, and interpretation of the data. YI, ME, and MI contributed to the conception and design of the study. MO, NH, YN, SY, and KM contributed to the acquisition of the data. DM took responsibility for the integrity of the data analysis. All authors participated in drafting or revising the manuscript and approved the final version of the manuscript for submission.

Funding

MI received grant support and lecture fees from Eli Lilly Japan K.K. and Ono Pharmaceutical Co., LTD. YI and KM received lecture fees from Eli Lilly Japan K.K. and Ono Pharmaceutical Co., LTD.

Compliance with Ethical Standards

Conflicts of interest

Daichi Miyaoka, Masaya Ohara, Noriyuki Hayashi, Yuki Nagata, Shinsuke Yamada, and Masanori Emoto have no conflicts of interest.

Human and Animal Rights

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed Consent

Informed consent was obtained from all individual participants included in the study, which received institutional ethics committee approval (Osaka City University Graduate School of Medicine, registration number 1775).

References

  1. 1.
    Hans D, Goertzen AL, Krieg MA, Leslie WD (2011) Bone microarchitecture assessed by TBS predicts osteoporotic fractures independent of bone density: the Manitoba study. J Bone Miner Res 26:2762–2769CrossRefPubMedGoogle Scholar
  2. 2.
    McCloskey EV, Oden A, Harvey NC, Leslie WD, Hans D, Johansson H, Barkmann R, Boutroy S, Brown J, Chapurlat R, Elders PJ, Fujita Y, Gluer CC, Goltzman D, Iki M, Karlsson M, Kindmark A, Kotowicz M, Kurumatani N, Kwok T, Lamy O, Leung J, Lippuner K, Ljunggren O, Lorentzon M, Mellstrom D, Merlijn T, Oei L, Ohlsson C, Pasco JA, Rivadeneira F, Rosengren B, Sornay-Rendu E, Szulc P, Tamaki J, Kanis JA (2016) A meta-analysis of trabecular bone score in fracture risk prediction and its relationship to FRAX. J Bone Miner Res 31:940–948CrossRefPubMedGoogle Scholar
  3. 3.
    Hans D, Barthe N, Boutroy S, Pothuaud L, Winzenrieth R, Krieg MA (2011) Correlations between trabecular bone score, measured using anteroposterior dual-energy X-ray absorptiometry acquisition, and 3-dimensional parameters of bone microarchitecture: an experimental study on human cadaver vertebrae. J Clin Densitom 14:302–312CrossRefPubMedGoogle Scholar
  4. 4.
    Roux JP, Wegrzyn J, Boutroy S, Bouxsein ML, Hans D, Chapurlat R (2013) The predictive value of trabecular bone score (TBS) on whole lumbar vertebrae mechanics: an ex vivo study. Osteoporos Int 24:2455–2460CrossRefPubMedGoogle Scholar
  5. 5.
    Silva BC, Boutroy S, Zhang C, McMahon DJ, Zhou B, Wang J, Udesky J, Cremers S, Sarquis M, Guo XD, Hans D, Bilezikian JP (2013) Trabecular bone score (TBS)—a novel method to evaluate bone microarchitectural texture in patients with primary hyperparathyroidism. J Clin Endocrinol Metab 98:1963–1970CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Silva BC, Walker MD, Abraham A, Boutroy S, Zhang C, McMahon DJ, Liu G, Hans D, Bilezikian JP (2013) Trabecular bone score is associated with volumetric bone density and microarchitecture as assessed by central QCT and HRpQCT in Chinese American and White women. J Clin Densitom 16:554–561CrossRefPubMedGoogle Scholar
  7. 7.
    Muschitz C, Kocijan R, Haschka J, Pahr D, Kaider A, Pietschmann P, Hans D, Muschitz GK, Fahrleitner-Pammer A, Resch H (2015) TBS reflects trabecular microarchitecture in premenopausal women and men with idiopathic osteoporosis and low-traumatic fractures. Bone 79:259–266CrossRefPubMedGoogle Scholar
  8. 8.
    Dufour R, Winzenrieth R, Heraud A, Hans D, Mehsen N (2013) Generation and validation of a normative, age-specific reference curve for lumbar spine trabecular bone score (TBS) in French women. Osteoporos Int 24:2837–2846CrossRefPubMedGoogle Scholar
  9. 9.
    Simonelli C, Leib E, Mossman N, Winzenrieth R, Hans D, McClung M (2014) Creation of an age-adjusted, dual-energy X-ray absorptiometry-derived trabecular bone score curve for the lumbar spine in non-Hispanic US White women. J Clin Densitom 17:314–319CrossRefPubMedGoogle Scholar
  10. 10.
    Iki M, Tamaki J, Sato Y, Winzenrieth R, Kagamimori S, Kagawa Y, Yoneshima H (2015) Age-related normative values of trabecular bone score (TBS) for Japanese women: the Japanese Population-based Osteoporosis (JPOS) study. Osteoporos Int 26:245–252CrossRefPubMedGoogle Scholar
  11. 11.
    Iki M, Tamaki J, Kadowaki E, Sato Y, Dongmei N, Winzenrieth R, Kagamimori S, Kagawa Y, Yoneshima H (2014) Trabecular bone score (TBS) predicts vertebral fractures in Japanese women over 10 years independently of bone density and prevalent vertebral deformity: the Japanese Population-Based Osteoporosis (JPOS) cohort study. J Bone Miner Res 29:399–407CrossRefPubMedGoogle Scholar
  12. 12.
    Neer RM, Arnaud CD, Zanchetta JR, Prince R, Gaich GA, Reginster JY, Hodsman AB, Eriksen EF, Ish-Shalom S, Genant HK, Wang O, Mitlak BH (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
  13. 13.
    Senn C, Gunther B, Popp AW, Perrelet R, Hans D, Lippuner K (2014) Comparative effects of teriparatide and ibandronate on spine bone mineral density (BMD) and microarchitecture (TBS) in postmenopausal women with osteoporosis: a 2 year open-label study. Osteoporos Int 25:1945–1951CrossRefPubMedGoogle Scholar
  14. 14.
    Kurland ES, Heller SL, Diamond B, McMahon DJ, Cosman F, Bilezikian JP (2004) The importance of bisphosphonate therapy in maintaining bone mass in men after therapy with teriparatide [human parathyroid hormone (1–34)]. Osteoporos Int 15:992–997CrossRefPubMedGoogle Scholar
  15. 15.
    Kaufman JM, Orwoll E, Goemaere S, San Martin J, Hossain A, Dalsky GP, Lindsay R, Mitlak BH (2005) Teriparatide effects on vertebral fractures and bone mineral density in men with osteoporosis: treatment and discontinuation of therapy. Osteoporos Int 16:510–516CrossRefPubMedGoogle Scholar
  16. 16.
    Adami S, San Martin J, Munoz-Torres M, Econs MJ, Xie L, Dalsky GP, McClung M, Felsenberg D, Brown JP, Brandi ML, Sipos A (2008) Effect of raloxifene after recombinant teriparatide [hPTH(1–34)] treatment in postmenopausal women with osteoporosis. Osteoporos Int 19:87–94CrossRefPubMedGoogle Scholar
  17. 17.
    Eastell R, Nickelsen T, Marin F, Barker C, Hadji P, Farrerons J, Audran M, Boonen S, Brixen K, Gomes JM, Obermayer-Pietsch B, Avramidis A, Sigurdsson G, Gluer CC (2009) Sequential treatment of severe postmenopausal osteoporosis after teriparatide: final results of the randomized, controlled European Study of Forsteo (EUROFORS). J Bone Miner Res 24:726–736CrossRefPubMedGoogle Scholar
  18. 18.
    Ebina K, Hashimoto J, Kashii M, Hirao M, Kaneshiro S, Noguchi T, Tsukamoto Y, Yoshikawa H (2017) The effects of switching daily teriparatide to oral bisphosphonates or denosumab in patients with primary osteoporosis. J Bone Miner Metab 35:91–98CrossRefPubMedGoogle Scholar
  19. 19.
    Riggs BL, Parfitt AM (2005) Drugs used to treat osteoporosis: the critical need for a uniform nomenclature based on their action on bone remodeling. J Bone Miner Res 20:177–184CrossRefPubMedGoogle Scholar
  20. 20.
    Dunford JE, Thompson K, Coxon FP, Luckman SP, Hahn FM, Poulter CD, Ebetino FH, Rogers MJ (2001) Structure-activity relationships for inhibition of farnesyl diphosphate synthase in vitro and inhibition of bone resorption in vivo by nitrogen-containing bisphosphonates. J Pharmacol Exp Ther 296:235–242PubMedGoogle Scholar
  21. 21.
    Hagino H, Nishizawa Y, Sone T, Morii H, Taketani Y, Nakamura T, Itabashi A, Mizunuma H, Ohashi Y, Shiraki M, Minamide T, Matsumoto T (2009) A double-blinded head-to-head trial of minodronate and alendronate in women with postmenopausal osteoporosis. Bone 44:1078–1084CrossRefPubMedGoogle Scholar
  22. 22.
    Okazaki R, Hagino H, Ito M, Sone T, Nakamura T, Mizunuma H, Fukunaga M, Shiraki M, Nishizawa Y, Ohashi Y, Matsumoto T (2012) Efficacy and safety of monthly oral minodronate in patients with involutional osteoporosis. Osteoporos Int 23:1737–1745CrossRefPubMedGoogle Scholar
  23. 23.
    Genant HK, Jergas M, Palermo L, Nevitt M, Valentin RS, Black D, Cummings SR (1996) Comparison of semiquantitative visual and quantitative morphometric assessment of prevalent and incident vertebral fractures in osteoporosis. The study of osteoporotic fractures research group. J Bone Miner Res 11:984–996CrossRefPubMedGoogle Scholar
  24. 24.
    Imai E, Horio M, Nitta K, Yamagata K, Iseki K, Tsukamoto Y, Ito S, Makino H, Hishida A, Matsuo S (2007) Modification of the modification of diet in renal disease (MDRD) study equation for Japan. Am J Kidney Dis 50:927–937CrossRefPubMedGoogle Scholar
  25. 25.
    Gao P, Scheibel S, D’Amour P, John MR, Rao SD, Schmidt-Gayk H, Cantor TL (2001) Development of a novel immunoradiometric assay exclusively for biologically active whole parathyroid hormone 1–84: implications for improvement of accurate assessment of parathyroid function. J Bone Miner Res 16:605–614CrossRefPubMedGoogle Scholar
  26. 26.
    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
  27. 27.
    Graeff C, Timm W, Nickelsen TN, Farrerons J, Marin F, Barker C, Gluer CC, Group EHRCTS (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
  28. 28.
    Jobke B, Muche B, Burghardt AJ, Semler J, Link TM, Majumdar S (2011) Teriparatide in bisphosphonate-resistant osteoporosis: microarchitectural changes and clinical results after 6 and 18 months. Calcif Tissue Int 89:130–139CrossRefPubMedGoogle Scholar
  29. 29.
    Misof BM, Roschger P, Cosman F, Kurland ES, Tesch W, Messmer P, Dempster DW, Nieves J, Shane E, Fratzl P, Klaushofer K, Bilezikian J, Lindsay R (2003) Effects of intermittent parathyroid hormone administration on bone mineralization density in iliac crest biopsies from patients with osteoporosis: a paired study before and after treatment. J Clin Endocrinol Metab 88:1150–1156CrossRefPubMedGoogle Scholar
  30. 30.
    Boytsov N, Zhang X, Sugihara T, Taylor K, Swindle R (2015) Osteoporotic fractures and associated hospitalizations among patients treated with teriparatide compared to a matched cohort of patients not treated with teriparatide. Curr Med Res Opin 31:1665–1675CrossRefPubMedGoogle Scholar
  31. 31.
    Di Gregorio S, Del Rio L, Rodriguez-Tolra J, Bonel E, Garcia M, Winzenrieth R (2015) Comparison between different bone treatments on areal bone mineral density (aBMD) and bone microarchitectural texture as assessed by the trabecular bone score (TBS). Bone 75:138–143CrossRefPubMedGoogle Scholar
  32. 32.
    Saag KG, Agnusdei D, Hans D, Kohlmeier LA, Krohn KD, Leib ES, MacLaughlin EJ, Alam J, Simonelli C, Taylor KA, Marcus R (2016) Trabecular bone score in patients with chronic glucocorticoid therapy-induced osteoporosis treated with alendronate or teriparatide. Arthritis Rheumatol 68:2122–2128CrossRefPubMedGoogle Scholar
  33. 33.
    Weinstein RS (2011) Clinical practice. Glucocorticoid-induced bone disease. N Engl J Med 365:62–70CrossRefPubMedGoogle Scholar
  34. 34.
    Saag KG, Shane E, Boonen S, Marin F, Donley DW, Taylor KA, Dalsky GP, Marcus R (2007) Teriparatide or alendronate in glucocorticoid-induced osteoporosis. N Engl J Med 357:2028–2039CrossRefPubMedGoogle Scholar
  35. 35.
    McClung MR, San Martin J, Miller PD, Civitelli R, Bandeira F, Omizo M, Donley DW, Dalsky GP, Eriksen EF (2005) Opposite bone remodeling effects of teriparatide and alendronate in increasing bone mass. Arch Intern Med 165:1762–1768CrossRefPubMedGoogle Scholar
  36. 36.
    Saag KG, Zanchetta JR, Devogelaer JP, Adler RA, Eastell R, See K, Krege JH, Krohn K, Warner MR (2009) Effects of teriparatide versus alendronate for treating glucocorticoid-induced osteoporosis: thirty-six-month results of a randomized, double-blind, controlled trial. Arthritis Rheum 60:3346–3355CrossRefPubMedGoogle Scholar
  37. 37.
    Black DM, Bilezikian JP, Ensrud KE, Greenspan SL, Palermo L, Hue T, Lang TF, McGowan JA, Rosen CJ, Pa THSI (2005) One year of alendronate after one year of parathyroid hormone (1–84) for osteoporosis. N Engl J Med 353:555–565CrossRefPubMedGoogle Scholar
  38. 38.
    Krieg MA, Aubry-Rozier B, Hans D, Leslie WD, Manitoba Bone Density P (2013) Effects of anti-resorptive agents on trabecular bone score (TBS) in older women. Osteoporos Int 24:1073–1078CrossRefPubMedGoogle Scholar
  39. 39.
    Popp AW, Guler S, Lamy O, Senn C, Buffat H, Perrelet R, Hans D, Lippuner K (2013) Effects of zoledronate versus placebo on spine bone mineral density and microarchitecture assessed by the trabecular bone score in postmenopausal women with osteoporosis: a three-year study. J Bone Miner Res 28:449–454CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Department of Metabolism, Endocrinology and Molecular MedicineOsaka City University Graduate School of MedicineAbeno-kuJapan

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