Abstract
Recent evidence confirms the superiority of osteoanabolic therapy compared to anti-remodeling drugs for rapid improvement in bone density and fracture risk reduction, providing strong justification for the use of these anabolic agents as the initial therapy in high-risk patients, to be followed by anti-remodeling therapy. This review will highlight the results of recent studies and define the current status of osteoanabolic therapy for osteoporosis.
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References
Compston JE, McClung MR, Leslie WD (2019) Osteoporosis. The Lancet 393:364–376
Kanis JA, Cooper C, Rizzoli R et al (2019) European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporos Int 30:3–44
Camacho PM, Petak SM, Binkley N et al (2020) American Association of Clinical Endocrinologists/American College of Endocrinology Clinical Practice Guidelines for the diagnosis and treatment of postmenopausal osteoporosis—2020 Update. Endocr Pract 26:1–46
Cosman F, Nieves JW, Dempster DW (2017) Treatment sequence matters: anabolic and antiresorptive therapy for osteoporosis. J Bone Miner Res 32:198–202
McClung MR (2017) Using osteoporosis therapies in combination. Curr Osteoporos Rep 15:343–352
Cummings SR, Black DM, Nevitt MC et al (1993) Bone density at various sites for prediction of hip fractures. The study of osteoporotic fractures research group. Lancet (London, England) 341:72–75
Ferrari S, Libanati C, Lin CJF et al (2019) Relationship between bone mineral density T-score and nonvertebral fracture risk over 10 years of denosumab treatment. J Bone Miner Res 34:1033–1040
Cosman F, Lewiecki EM, Ebeling PR et al (2020) T-Score as an Indicator of Fracture Risk During Treatment With Romosozumab or Alendronate in the ARCH Trial. J Bone Miner Res. 35:1333–1342
Bouxsein ML, Eastell R, Lui LY et al (2019) Change in bone density and reduction in fracture risk: a meta-regression of published trials. J Bone Miner Res 34:632–642
Kanis JA, Harvey NC, McCloskey E et al (2020) Algorithm for the management of patients at low, high and very high risk of osteoporotic fractures. Osteoporos Int 31:1–12
Kanis JA, Harvey NC, Johansson H et al (2020) A decade of FRAX: how has it changed the management of osteoporosis? Aging Clin Exp Res 32:187–196
Minisola S, Cipriani C, Grotta GD et al (2019) Update on the safety and efficacy of teriparatide in the treatment of osteoporosis. Ther Adv Musculoskelet Dis 11:1759720
Sleeman A, Clements JN (2019) Abaloparatide: a new pharmacological option for osteoporosis. Am J Health Syst Pharm 76:130–135
McClung MR (2018) Romosozumab for the treatment of osteoporosis. Osteoporos Sarcopenia 4:11–15
Kaveh S, Hosseinifard H, Ghadimi N et al (2020) Efficacy and safety of Romosozumab in treatment for low bone mineral density: a systematic review and meta-analysis. Clin Rheumatol. https://doi.org/10.1007/s10067-020-04948-1
Hodsman AB, Bauer DC, Dempster DW 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 26:688–703
Marcus R (2011) Present at the beginning: a personal reminiscence on the history of teriparatide. Osteoporos Int 22:2241–2248
Dobnig H, Turner RT (1997) The effects of programmed administration of human parathyroid hormone fragment (1-34) on bone histomorphometry and serum chemistry in rats. Endocrinology 138:4607–4612
Jilka RL (2007) Molecular and cellular mechanisms of the anabolic effect of intermittent PTH. Bone 40:1434–1446
Silva BC, Costa AG, Cusano NE et al (2011) Catabolic and anabolic actions of parathyroid hormone on the skeleton. J Endocrinol Invest 34:801–810
Bellido T, Saini V, Pajevic PD (2013) Effects of PTH on osteocyte function. Bone 54:250–257
Reeve J, Hesp R, Williams D et al (1976) Anabolic effect of low doses of a fragment of human parathyroid hormone on the skeleton in postmenopausal osteoporosis. Lancet (London, England) 1:1035–1038
Reeve J, Meunier PJ, Parsons JA et al (1980) Anabolic effect of human parathyroid hormone fragment on trabecular bone in involutional osteoporosis: a multicentre trial. BMJ 280:1340–1344
Slovik DM, Neer RM, Potts JT Jr (1981) Short-term effects of synthetic human parathyroid hormone (1-34) administration on bone mineral metabolism in osteoporotic patients. J Clin Invest 68:1261–1271
Cosman F, Shen V, Xie F et al (1993) Estrogen protection against bone resorbing effects of parathyroid hormone infusion Assessment by use of biochemical markers. Ann Intern Med 118:337–343
Lindsay R, Nieves J, Formica C et al (1997) Randomised controlled study of effect of parathyroid hormone on vertebral-bone mass and fracture incidence among postmenopausal women on oestrogen with osteoporosis. Lancet 350:550–555
Lane NE, Sanchez S, Modin GW et al (1998) Parathyroid hormone treatment can reverse corticosteroid-induced osteoporosis. Results of a randomized controlled clinical trial. J Clin Invest 102:1627–1633
Neer RM, Arnaud CD, Zanchetta JR et al (2001) Effect of parathyroid hormone (1-34) on fractures and bone mineral density in postmenopausal women with osteoporosis. New Engl J Med 344:1434–1441
Lindsay R, Scheele WH, Neer R et al (2004) Sustained vertebral fracture risk reduction after withdrawal of teriparatide in postmenopausal women with osteoporosis. Arch Intern Med 164:2024–2030
Prince R, Sipos A, Hossain A et al (2005) Sustained nonvertebral fragility fracture risk reduction after discontinuation of teriparatide treatment. J Bone Miner Res 20:1507–1513
Silverman S, Miller P, Sebba A et al (2013) The direct assessment of nonvertebral fractures in community experience (DANCE) study: 2-year nonvertebral fragility fracture results. Osteoporos Int 24:2309–2317
Cosman F, Nieves JW, Zion M et al (2009) Retreatment with teriparatide one year after the first teriparatide course in patients on continued long-term alendronate. J Bone Miner Res 24:1110–1115
Finkelstein JS, Wyland JJ, Leder BZ et al (2009) Effects of teriparatide retreatment in osteoporotic men and women. J Clin Endocrinol Metab 94:2495–2501
Mana DL, Zanchetta MB, Zanchetta JR (2017) Retreatment with teriparatide: our experience in three patients with severe secondary osteoporosis. Osteoporos Int 28:1491–1494
Jiang Y, Zhao JJ, Mitlak BH et al (2003) Recombinant human parathyroid hormone (1-34) [teriparatide] improves both cortical and cancellous bone structure. J Bone Miner Res 18:1932–1941
Miller PD, Hattersley G, Riis BJ et al (2016) Effect of abaloparatide vs placebo on new vertebral fractures in postmenopausal women with osteoporosis: a randomized clinical trial. JAMA 316:722–733
Moreira CA, Fitzpatrick LA, Wang Y et al (2016) Effects of abaloparatide-SC (BA058) on bone histology and histomorphometry: the ACTIVE phase 3 trial. Bone 97:314–319
Dempster DW, Zhou H, Recker RR et al (2018) Remodeling- and modeling-based bone formation with teriparatide versus denosumab: a longitudinal analysis from baseline to 3 months in the AVA study. J Bone Miner Res 33:298–306
Arlot M, Meunier PJ, Boivin G et al (2005) Differential effects of teriparatide and alendronate on bone remodeling in postmenopausal women assessed by histomorphometric parameters. J Bone Miner Res 20:1244–1253
Gatti D, Viapiana O, Idolazzi L et al (2011) The waning of teriparatide effect on bone formation markers in postmenopausal osteoporosis is associated with increasing serum levels of DKK1. J Clin Endocrinol Metab 96:1555–1559
Jolette J, Attalla B, Varela A et al (2017) Comparing the incidence of bone tumors in rats chronically exposed to the selective PTH type 1 receptor agonist abaloparatide or PTH(1-34). Regul Toxicol Pharmacol 86:356–365
Andrews EB, Gilsenan AW, Midkiff K et al (2012) The US postmarketing surveillance study of adult osteosarcoma and teriparatide: study design and findings from the first 7 years. J Bone Miner Res 27:2429–2437
Cosman F, Lane NE, Bolognese MA et al (2010) Effect of transdermal teriparatide administration on bone mineral density in postmenopausal women. J Clin Endocrinol Metab 95:151–158
Pearson RG, Masud T, Blackshaw E et al (2019) Nasal administration and plasma pharmacokinetics of parathyroid hormone peptide PTH 1-34 for the treatment of osteoporosis. Pharmaceutics 11:265
Nakamura T, Sugimoto T, Nakano T et al (2012) Randomized teriparatide [human parathyroid hormone (PTH) 1-34] once-weekly efficacy research (TOWER) trial for examining the reduction in new vertebral fractures in subjects with primary osteoporosis and high fracture risk. J Clin Endocrinol Metab 97:3097–3106
Nakano T, Shiraki M, Sugimoto T et al (2014) Once-weekly teriparatide reduces the risk of vertebral fracture in patients with various fracture risks: subgroup analysis of the Teriparatide Once-Weekly Efficacy Research (TOWER) trial. J Bone Min Metab 32:441–446
Hagino H, Narita R, Yokoyama Y et al (2019) A multicenter, randomized, rater-blinded, parallel-group, phase 3 study to compare the efficacy, safety, and immunogenicity of biosimilar RGB-10 and reference once-daily teriparatide in patients with osteoporosis. Osteoporos Int 30:2027–2037
Pfenex. FDA Approves Bonsity (teriparatide injection) to Treat Osteoporosis (2019). https://www.drugs.com/newdrugs/fda-approves-bonsity-teriparatide-osteoporosis-5072.html. Accessed June 29, 2020
Company ELa. FORTEO Presecribing Information (2020). https://uspl.lilly.com/forteo/forteo.html#pi. Accessed June 29, 2020
Greenspan SL, Bone HG, Ettinger MP et al (2007) Effect of recombinant human parathyroid hormone (1-84) on vertebral fracture and bone mineral density in postmenopausal women with osteoporosis: a randomized trial. Ann Intern Med 146:326–339
Agency EM. Preotact (2014) [updated 02/07/2014. https://www.ema.europa.eu/en/medicines/human/EPAR/preotact. Accessed August 25, 2020
Hattersley G, Dean T, Corbin BA et al (2016) Binding selectivity of abaloparatide for PTH-Type-1-receptor conformations and effects on downstream signaling. Endocrinology 157:141–149
Bahar H, Gallacher K, Downall J et al (2016) Six weeks of daily abaloparatide treatment increased vertebral and femoral bone mineral density, microarchitecture and strength in ovariectomized osteopenic rats. Calcif Tissue Int 99:489–499
Varela A, Chouinard L, Lesage E et al (2017) One year of abaloparatide, a selective activator of the PTH1 receptor, increased bone formation and bone mass in osteopenic ovariectomized rats without increasing bone resorption. J Bone Miner Res 32:24–33
Doyle N, Varela A, Haile S et al (2018) Abaloparatide, a novel PTH receptor agonist, increased bone mass and strength in ovariectomized cynomolgus monkeys by increasing bone formation without increasing bone resorption. Osteoporos Int 29:685–697
Leder BZ, O’Dea LS, Zanchetta JR et al (2015) Effects of abaloparatide, a human parathyroid hormone-related peptide analog, on bone mineral density in postmenopausal women with osteoporosis. J Clin Endocrinol Metab 100:697–706
Cosman F, Hattersley G, Hu MY et al (2017) Effects of abaloparatide-sc on fractures and bone mineral density in subgroups of postmenopausal women with osteoporosis and varying baseline risk factors. J Bone Miner Res 32:17–23
Bilezikian JP, Hattersley G, Mitlak BH et al (2019) Abaloparatide in patients with mild or moderate renal impairment: results from the ACTIVE phase 3 trial. Curr Med Res Opin 35:2097–2102
McClung MR, Williams GC, Hattersley G et al (2018) Geography of fracture incidence in postmenopausal women with osteoporosis treated with abaloparatide. Calcif Tissue Int 102:627–633
Dhaliwal R, Hans D, Hattersley G et al (2020) Abaloparatide in postmenopausal women with osteoporosis and type 2 diabetes: a post hoc analysis of the ACTIVE study. JBMR Plus 4:e10346
Watts NB, Hattersley G, Fitzpatrick LA et al (2019) Abaloparatide effect on forearm bone mineral density and wrist fracture risk in postmenopausal women with osteoporosis. Osteoporos Int 30:1187–1194
Reginster J, Bianic F, Campbell R et al (2019) Abaloparatide for risk reduction of nonvertebral and vertebral fractures in postmenopausal women with osteoporosis: a network meta-analysis. Osteoporos Int 30:1465–1473
Cosman F, Miller PD, Williams GC et al (2017) Eighteen months of treatment with subcutaneous abaloparatide followed by 6 months of treatment with alendronate in postmenopausal women with osteoporosis: results of the ACTIVExtend trial. Mayo Clin Proc 92:200–210
Bone HG, Cosman F, Miller PD et al (2018) ACTIVExtend: 24 months of alendronate after 18 months of abaloparatide or placebo for postmenopausal osteoporosis. J Clin Endocrinol Metab 103:2949–2957
Leder B, Zapalowski C, Hu MY et al (2019) Fracture and bone mineral density response by baseline risk in patients treated with abaloparatide followed by alendronate: results from the phase 3 ACTIVExtend Trial. J Bone Miner Res 34:2213–2219
Agency EM. Refusal of the marketing authorisation for Eladynos (abaloparatide) (2017). https://www.ema.europa.eu/en/documents/smop-initial/questions-answers-refusal-marketing-authorisation-eladynos-abaloparatide_en.pdf. Accessed June 29, 2020
Health R. TYMLOS Prescribing Information (2018) https://radiuspharm.com/wp-content/uploads/tymlos/tymlos-prescribing-information.pdf. Accessed June 29, 2020
Shirley M (2017) Abaloparatide: first Global Approval. Drugs 77:1363–1368
Delgado-Calle J, Sato AY, Bellido T (2017) Role and mechanism of action of sclerostin in bone. Bone 96:29–37
Ominsky MS, Niu QT, Li C et al (2014) Tissue-level mechanisms responsible for the increase in bone formation and bone volume by sclerostin antibody. J Bone Miner Res 29:1424–1430
Ominsky MS, Boyce RW, Li X et al (2017) Effects of sclerostin antibodies in animal models of osteoporosis. Bone 96:63–75
Ominsky MS, Boyd SK, Varela A et al (2017) Romosozumab improves bone mass and strength while maintaining bone quality in ovariectomized cynomolgus monkeys. J Bone Miner Res 32:788–801
Padhi D, Jang G, Stouch B et al (2011) Single-dose, placebo-controlled, randomized study of AMG 785, a sclerostin monoclonal antibody. J Bone Miner Res 26:19–26
Padhi D, Allison M, Kivitz AJ et al (2014) Multiple doses of sclerostin antibody romosozumab in healthy men and postmenopausal women with low bone mass: a randomized, double-blind, placebo-controlled study. J Clin Pharmacol 54:168–178
McClung MR, San Martin J, Miller PD et al (2005) Opposite bone remodeling effects of teriparatide and alendronate in increasing bone mass. Arch Intern Med 165:1762–1768
McClung MR, Brown JP, Diez-Perez A et al (2018) Effects of 24 months of treatment with romosozumab followed by 12 months of denosumab or placebo in postmenopausal women with low bone mineral density: a randomized, double-blind, phase 2, parallel group study. J Bone Miner Res 33:1397–1406
Ishibashi H, Crittenden DB, Miyauchi A et al (2017) Romosozumab increases bone mineral density in postmenopausal Japanese women with osteoporosis: a phase 2 study. Bone 103:209–215
Stolina M, Dwyer D, Niu QT et al (2014) Temporal changes in systemic and local expression of bone turnover markers during six months of sclerostin antibody administration to ovariectomized rats. Bone 67:305–313
Boyce RW, Brown D, Felx M et al (2018) Decreased osteoprogenitor proliferation precedes attenuation of cancellous bone formation in ovariectomized rats treated with sclerostin antibody. Bone Rep 8:90–94
Kendler DL, Bone HG, Massari F et al (2019) Bone mineral density gains with a second 12-month course of romosozumab therapy following placebo or denosumab. Osteoporos Int 30:2437–2448
Cosman F, Crittenden DB, Adachi JD et al (2016) Romosozumab treatment in postmenopausal women with osteoporosis. New Engl J Med 375:1532–1543
Lewiecki EM, Dinavahi RV, Lazaretti-Castro M et al (2019) One year of romosozumab followed by two years of denosumab maintains fracture risk reductions: results of the FRAME extension study. J Bone Miner Res 34:419–428
Saag KG, Petersen J, Brandi ML et al (2017) Romosozumab or alendronate for fracture prevention in women with osteoporosis. New Engl J Med 377:1417–1427
Chavassieux P, Chapurlat R, Portero-Muzy N et al (2019) Bone-forming and antiresorptive effects of romosozumab in postmenopausal women with osteoporosis: bone histomorphometry and microcomputed tomography analysis after 2 and 12 months of treatment. J Bone Miner Res 34:1597–1608
McClung MR, Grauer A, Boonen S et al (2014) Romosozumab in postmenopausal women with low bone mineral density. New Engl J Med 370:412–420
Chouinard L, Felx M, Mellal N et al (2016) Carcinogenicity risk assessment of romosozumab: a review of scientific weight-of-evidence and findings in a rat lifetime pharmacology study. Regulat Toxicol Pharmacol 81:212–222
Amgen. Bone, Reproductive and Urologic Drugs Advisory Committee for Romosozumab Briefing Materials (2019). https://www.fda.gov/media/121255/download. Accessed June 29, 2020
Krishna SM, Seto SW, Jose RJ et al (2017) WNT signaling pathway inhibitor sclerostin inhibits angiotensin ii-induced aortic aneurysm and atherosclerosis. Arterioscler Thromb Vasc Biol 37:553–566
Lyles KW, Colon-Emeric CS, Magaziner JS et al (2007) Zoledronic acid and clinical fractures and mortality after hip fracture. New Engl J Med 357:1799–1809
Reid IR, Horne AM, Mihov B et al (2018) Fracture prevention with zoledronate in older women with osteopenia. New Engl J Med 379:2407–2416
Kim DH, Rogers JR, Fulchino LA et al (2015) Bisphosphonates and risk of cardiovascular events: a meta-analysis. PLoS ONE 10:e0122646
Kranenburg G, Bartstra JW, Weijmans M et al (2016) Bisphosphonates for cardiovascular risk reduction: a systematic review and meta-analysis. Atherosclerosis 252:106–115
Food and Drug Administration. Bone Reproductive and Urologic Drugs Advisory Committee (BRUDAC) Meeting, January 29 (2019) https://www.fda.gov/media/112946/download. Accessed June 25, 2020
Cummings SR, McCulloch C (2020) Explanations for the difference in rates of cardiovascular events in a trial of alendronate and romosozumab. Osteoporos Int 31:1019–1021
European Medicines Agency (2019) Human medicine European public assessment report (EPAR): Evenity, pp. 1–263
Amgen. EVENITY Prescribing Information (2019). https://www.pi.amgen.com/~/media/amgen/repositorysites/pi-amgen-com/evenity/evenity_pi_hcp_english.ashx. Accessed June 29, 2020
Imaz I, Zegarra P, González-Enríquez J et al (2010) Poor bisphosphonate adherence for treatment of osteoporosis increases fracture risk: systematic review and meta-analysis. Osteoporos Int 21:1943–1951
Koller G, Goetz V, Vandermeer B et al (2020) Persistence and adherence to parenteral osteoporosis therapies: a systematic review. Osteoporos Int. https://doi.org/10.1007/s00198-020-05507-9
Body JJ, Gaich GA, Scheele WH et al (2002) A randomized double-blind trial to compare the efficacy of teriparatide [recombinant human parathyroid hormone (1-34)] with alendronate in postmenopausal women with osteoporosis. J Clin Endocrinol Metab 87:4528–4535
Hadji P, Zanchetta JR, Russo L et al (2012) The effect of teriparatide compared with risedronate on reduction of back pain in postmenopausal women with osteoporotic vertebral fractures. Osteoporos Int 23:2141–2150
Saag KG, Shane E, Boonen S et al (2007) Teriparatide or alendronate in glucocorticoid-induced osteoporosis. New Engl J Med 357:2028–2039
Cosman F, Eriksen EF, Recknor C et al (2011) Effects of intravenous zoledronic acid plus subcutaneous teriparatide [rhPTH(1-34)] in postmenopausal osteoporosis. J Bone Miner Res 26:503–511
Leder BZ, Tsai JN, Uihlein AV et al (2014) Two years of Denosumab and teriparatide administration in postmenopausal women with osteoporosis (The DATA Extension Study): a randomized controlled trial. J Clin Endocrinol Metab 99:1694–1700
Kendler DL, Marin F, Zerbini CAF et al (2018) Effects of teriparatide and risedronate on new fractures in post-menopausal women with severe osteoporosis (VERO): a multicentre, double-blind, double-dummy, randomised controlled trial. Lancet (London, England). 391:230–240
Miller PD, Hattersley G, Lau E et al (2019) Bone mineral density response rates are greater in patients treated with abaloparatide compared with those treated with placebo or teriparatide: results from the ACTIVE phase 3 trial. Bone 120:137–140
Genant HK, Engelke K, Bolognese MA et al (2017) Effects of romosozumab compared with teriparatide on bone density and mass at the spine and hip in postmenopausal women with low bone mass. J Bone Miner Res. 32:181–187
Keaveny TM, Crittenden DB, Bolognese MA et al (2017) Greater gains in spine and hip strength for romosozumab compared with teriparatide in postmenopausal women with low bone mass. J Bone Miner Res 32:1956–1962
Langdahl BL, Libanati C, Crittenden DB et al (2017) Romosozumab (sclerostin monoclonal antibody) versus teriparatide in postmenopausal women with osteoporosis transitioning from oral bisphosphonate therapy: a randomised, open-label, phase 3 trial. The Lancet 390:1585–1594
Leder BZ, Tsai JN, Uihlein AV et al (2015) Denosumab and teriparatide transitions in postmenopausal osteoporosis (the DATA-Switch study): extension of a randomised controlled trial. Lancet (London, England). 386:1147–1155
McClung MR, Bolognese MA, Brown JP et al (2020) A single dose of zoledronate preserves bone mineral density for up to 2 years after a second course of romosozumab. Osteoporos Int. https://doi.org/10.1007/s00198-020-05502-0
Cosman F, Crittenden DB, Ferrari S et al (2018) FRAME study: the foundation effect of building bone with 1 year of romosozumab leads to continued lower fracture risk after transition to denosumab. J Bone Miner Res 33:1219–1226
Adami S, San Martin J, Munoz-Torres M et al (2008) Effect of raloxifene after recombinant teriparatide [hPTH(1-34)] treatment in postmenopausal women with osteoporosis. Osteoporos Int 19:87–94
Eastell R, Nickelsen T, Marin F et al (2009) Sequential treatment of severe postmenopausal osteoporosis after teriparatide: final results of the randomized, controlled European Study of Forsteo (EUROFORS). J Bone Miner Res 24:726–736
Minne H, Audran M, Simões ME et al (2008) Bone density after teriparatide in patients with or without prior antiresorptive treatment: one-year results from the EUROFORS study. Curr Med Res Opin 24:3117–3128
Boonen S, Marin F, Obermayer-Pietsch B 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 93:852–860
Obermayer-Pietsch BM, Marin F, McCloskey EV 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 23:1591–1600
Cosman F, Wermers RA, Recknor C et al (2009) Effects of teriparatide in postmenopausal women with osteoporosis on prior alendronate or raloxifene: differences between stopping and continuing the antiresorptive agent. J Clin Endocrinol Metab 94:3772–3780
Langdahl BL, Libanati C, Crittenden DB et al (2017) Romosozumab (sclerostin monoclonal antibody) versus teriparatide in postmenopausal women with osteoporosis transitioning from oral bisphosphonate therapy: a randomised, open-label, phase 3 trial. Lancet (London, England). 390:1585–1594
Ravn P, Clemmesen B, Christiansen C (1999) Biochemical markers can predict the response in bone mass during alendronate treatment in early postmenopausal women. Alendronate osteoporosis prevention study group. Bone. 24:237–244
Greenspan SL, Schneider DL, McClung MR et al (2002) Alendronate improves bone mineral density in elderly women with osteoporosis residing in long-term care facilities. A randomized, double-blind, placebo-controlled trial. Ann Int Med 136:742–746
Chen P, Satterwhite JH, Licata AA et al (2005) Early changes in biochemical markers of bone formation predict BMD response to teriparatide in postmenopausal women with osteoporosis. J Bone Miner Res 20:962–970
Cosman F, Keaveny TM, Kopperdahl D et al (2013) Hip and spine strength effects of adding versus switching to teriparatide in postmenopausal women with osteoporosis treated with prior alendronate or raloxifene. J Bone Miner Res. 28:1328–1336
Stepan JJ, Burr DB, Li J et al (2010) Histomorphometric changes by teriparatide in alendronate-pretreated women with osteoporosis. Osteoporos Int 21:2027–2036
Ma YL, Zeng QQ, Chiang AY et al (2014) Effects of teriparatide on cortical histomorphometric variables in postmenopausal women with or without prior alendronate treatment. Bone 59:139–147
Fahrleitner-Pammer A, Burr D, Dobnig H et al (2016) Improvement of cancellous bone microstructure in patients on teriparatide following alendronate pretreatment. Bone 89:16–24
Miller PD, Bolognese MA, Lewiecki EM et al (2008) Effect of denosumab on bone density and turnover in postmenopausal women with low bone mass after long-term continued, discontinued, and restarting of therapy: a randomized blinded phase 2 clinical trial. Bone 43:222–229
Fogelman I, Fordham JN, Fraser WD et al (2008) Parathyroid hormone(1-84) treatment of postmenopausal women with low bone mass receiving hormone replacement therapy. Calcif Tissue Int 83:85–92
Deal C, Omizo M, Schwartz EN et al (2005) Combination teriparatide and raloxifene therapy for postmenopausal osteoporosis: results from a 6-month double-blind placebo-controlled trial. J Bone Miner Res 20:1905–1911
Tsai JN, Uihlein AV, Lee H et al (2013) Teriparatide and denosumab, alone or combined, in women with postmenopausal osteoporosis: the DATA study randomised trial. Lancet (London, England). 382:50–56
Tsai JN, Uihlein AV, Burnett-Bowie SA et al (2015) Comparative effects of teriparatide, denosumab, and combination therapy on peripheral compartmental bone density, microarchitecture, and estimated strength: the DATA-HRpQCT Study. J Bone Miner Res 30:39–45
Tsai JN, Uihlein AV, Burnett-Bowie SM et al (2016) Effects of two years of teriparatide, denosumab, or both on bone microarchitecture and strength (DATA-HRpQCT study). J Clin Endocrinol Metab 101:2023–2030
Nakamura Y, Suzuki T, Kamimura M et al (2017) Two-year clinical outcome of denosumab treatment alone and in combination with teriparatide in Japanese treatment-naive postmenopausal osteoporotic women. Bone Res 5:16055
Suzuki T, Nakamura Y, Kato H (2019) Efficacy of 4-year denosumab treatment alone or in combination with teriparatide in Japanese postmenopausal osteoporotic women. Mod Rheumatol 29:676–681
Tsai JN, Lee H, David NL et al (2019) Combination denosumab and high dose teriparatide for postmenopausal osteoporosis (DATA-HD): a randomised, controlled phase 4 trial. Lancet Diabetes Endocrinol 7:767–775
Idolazzi L, Rossini M, Viapiana O et al (2016) Teriparatide and denosumab combination therapy and skeletal metabolism. Osteoporos Int 27:3301–3307
Lou S, Lv H, Yin P et al (2019) Combination therapy with parathyroid hormone analogs and antiresorptive agents for osteoporosis: a systematic review and meta-analysis of randomized controlled trials. Osteoporos Int 30:59–70
Albert SG, Reddy S (2017) Clinical evaluation and cost efficacy of drugs for treatment of osteoporosis: a meta-analysis. Endocr Pract 23:841–856
Mori T, Crandall CJ, Ganz DA (2019) Cost-effectiveness of sequential teriparatide/alendronate versus alendronate-alone strategies in highrisk osteoporotic women in the US: analyzing the impact of generic/biosimilar teriparatide. JBMR Plus 3:e10233
Davis S, Simpson E, Hamilton J et al (2020) Denosumab, raloxifene, romosozumab and teriparatide to prevent osteoporotic fragility fractures: a systematic review and economic evaluation. Health Technol Assess 24:1–314
Hiligsmann M, Williams SA, Fitzpatrick LA et al (2020) Cost-effectiveness of sequential treatment with abaloparatide followed by alendronate vs. alendronate monotherapy in women at increased risk of fracture: A US payer perspective. Semin Arthr Rheumat. 50:394–400
Hiligsmann M, Williams SA, Fitzpatrick LA et al (2019) Cost-effectiveness of sequential treatment with abaloparatide vs. teriparatide for United States women at increased risk of fracture. Seminars Arthritis Rheum. 49:184–196
Le QA, Hay JW, Becker R et al (2019) Cost-effectiveness analysis of sequential treatment of abaloparatide followed by alendronate versus teriparatide followed by alendronate in postmenopausal women with osteoporosis in the United States. Ann Pharm 53:134–143
Orwoll ES, Scheele WH, Paul S et al (2003) The effect of teriparatide [human parathyroid hormone (1-34)] therapy on bone density in men with osteoporosis. J Bone Miner Res 18:9–17
Kaufman JM, Orwoll E, Goemaere S et al (2005) Teriparatide effects on vertebral fractures and bone mineral density in men with osteoporosis: treatment and discontinuation of therapy. Osteoporos Int 16:510–516
Lewiecki EM, Blicharski T, Goemaere S et al (2018) A phase III randomized placebo-controlled trial to evaluate efficacy and safety of romosozumab in men with osteoporosis. J Clin Endocrinol Metab 103:3183–3193
Chandler H, Brooks DJ, Hattersley G et al (2019) Abaloparatide increases bone mineral density and bone strength in ovariectomized rabbits with glucocorticoid-induced osteopenia. Osteoporos Int 30:1607–1616
Cohen A, Stein EM, Recker RR et al (2013) Teriparatide for idiopathic osteoporosis in premenopausal women: a pilot study. J Clin Endocrinol Metab 98:1971–1981
Nishiyama KK, Cohen A, Young P et al (2014) Teriparatide increases strength of the peripheral skeleton in premenopausal women with idiopathic osteoporosis: a pilot HR-pQCT study. J Clin Endocrinol Metab 99:2418–2425
Hong N, Kim JE, Lee SJ et al (2018) Changes in bone mineral density and bone turnover markers during treatment with teriparatide in pregnancy- and lactation-associated osteoporosis. Clin Endocrinol 88:652–658
Bernhardsson M, Aspenberg P (2018) Abaloparatide versus teriparatide: a head to head comparison of effects on fracture healing in mouse models. Acta Orthop 89:674–677
Lanske B, Chandler H, Pierce A et al (2019) Abaloparatide, a PTH receptor agonist with homology to PTHrP, enhances callus bridging and biomechanical properties in rats with femoral fracture. J Orthopaed Res 37:812–820
Feng G, Chang-Qing Z, Yi-Min C et al (2015) Systemic administration of sclerostin monoclonal antibody accelerates fracture healing in the femoral osteotomy model of young rats. Int Immunopharmacol 24:7–13
Ominsky MS, Li C, Li X et al (2011) Inhibition of sclerostin by monoclonal antibody enhances bone healing and improves bone density and strength of nonfractured bones. JJ Bone Miner Res 26:1012–1021
Aspenberg P, Genant HK, Johansson T et al (2010) Teriparatide for acceleration of fracture repair in humans: a prospective, randomized, double-blind study of 102 postmenopausal women with distal radial fractures. J Bone Miner Res 25:404–414
Bhandari M, Schemitsch EH, Karachalios T et al (2020) Romosozumab in skeletally mature adults with a fresh unilateral tibial diaphyseal fracture: a randomized phase-2 study. J Bone Joint Surg Am 102:1416–1426
Schemitsch EH, Miclau T, Karachalios T et al (2020) A randomized, placebo-controlled study of romosozumab for the treatment of hip fractures. J Bone Joint Surg Am 102:693–702
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McClung, M.R. Role of bone-forming agents in the management of osteoporosis. Aging Clin Exp Res 33, 775–791 (2021). https://doi.org/10.1007/s40520-020-01708-8
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DOI: https://doi.org/10.1007/s40520-020-01708-8