The Korean journal of internal medicine

The Korean Association of Internal Medicine (대한내과학회)
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Cancer treatment-induced bone loss

  • Yong Jun Choi (Department of Endocrinology and Metabolism, Ajou University School of Medicine)
  • Received : 2023.09.12
  • Accepted : 2023.11.27
  • Published : 2024.09.01
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Abstract

Cancer treatment-induced bone loss (CTBL) is associated with anti-tumor treatments, including endocrine therapies, chemotherapeutic treatments, radiotherapy, glucocorticoids, and tyrosine kinase inhibitors. Osteoporosis, characterized by the loss of bone mass, can increase the risk of fractures, leading to mortality and long-term disability, even after cancer remission. Cancer and osteoporosis have marked clinical and pathogenetic similarities. Both have a multifactorial etiology, affect the geriatric population, and markedly influence quality of life. Lifestyle management, including calcium and vitamin D supplementation, is recommended but the supporting evidence is limited. Oral and injectable bisphosphonates are effective for osteoporosis and malignant bone disease. Bisphosphonates increase bone mineral density (BMD) in patients with CTBL. Denosumab is also used in the management of CTBL; in clinical trials, it improved BMD and reduced the risk of fracture. Currently, there are no bone anabolic therapies for patients with cancer. Appropriate therapies are necessary to maintain optimal bone health, particularly in patients at heightened risk.

Keywords

Acknowledgement

This study was supported by grants from the National Research Foundation, Korea (NRF-2022R1C1C1006818).

References

  1. D'Oronzo S, Stucci S, Tucci M, Silvestris F. Cancer treatment-induced bone loss (CTIBL): pathogenesis and clinical implications. Cancer Treat Rev 2015;41:798-808. 
  2. Rachner TD, Coleman R, Hadji P, Hofbauer LC. Bone health during endocrine therapy for cancer. Lancet Diabetes Endocrinol 2018;6:901-910. 
  3. Hadji P, Aapro MS, Body JJ, et al. Management of Aromatase Inhibitor-Associated Bone Loss (AIBL) in postmenopausal women with hormone sensitive breast cancer: Joint position statement of the IOF, CABS, ECTS, IEG, ESCEO IMS, and SIOG. J Bone Oncol 2017;7:1-12. 
  4. den Uyl D, Bultink IE, Lems WF. Advances in glucocorticoid-induced osteoporosis. Curr Rheumatol Rep 2011;13:233-240. 
  5. Greenfield DM, Walters SJ, Coleman RE, et al. Prevalence and consequences of androgen deficiency in young male cancer survivors in a controlled cross-sectional study. J Clin Endocrinol Metab 2007;92:3476-3482. 
  6. Emens LA, Ascierto PA, Darcy PK, et al. Cancer immunotherapy: opportunities and challenges in the rapidly evolving clinical landscape. Eur J Cancer 2017;81:116-129. 
  7. Postow MA, Sidlow R, Hellmann MD. Immune-related adverse events associated with immune checkpoint blockade. N Engl J Med 2018;378:158-168. 
  8. Pantano F, Tramontana F, Iuliani M, et al. Changes in bone turnover markers in patients without bone metastases receiving immune checkpoint inhibitors: an exploratory analysis. J Bone Oncol 2022;37:100459. 
  9. Johnell O, Kanis JA. An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int 2006;17:1726-1733. 
  10. Khan MN, Khan AA. Cancer treatment-related bone loss: a review and synthesis of the literature. Curr Oncol 2008;15(Suppl 1):S30-S40. 
  11. Raisz LG. Physiology and pathophysiology of bone remodeling. Clin Chem 1999;45(8 Pt 2):1353-1358. 
  12. You L, Temiyasathit S, Lee P, et al. Osteocytes as mechanosensors in the inhibition of bone resorption due to mechanical loading. Bone 2008;42:172-179. 
  13. Roodman GD. Mechanisms of bone metastasis. N Engl J Med 2004;350:1655-1664. 
  14. Goltzman D, Mannstadt M, Marcocci C. Physiology of the calcium-parathyroid hormone-vitamin D axis. Front Horm Res 2018;50:1-13. 
  15. Higano CS. Androgen-deprivation-therapy-induced fractures in men with nonmetastatic prostate cancer: what do we really know? Nat Clin Pract Urol 2008;5:24-34. 
  16. Ginaldi L, Di Benedetto MC, De Martinis M. Osteoporosis, inflammation and ageing. Immun Ageing 2005;2:14. 
  17. Buckley L, Humphrey MB. Glucocorticoid-induced osteoporosis. N Engl J Med 2018;379:2547-2556. 
  18. Takahashi S. Management of cancer treatment-induced bone loss (CTIBL) in patients with breast cancer or prostate cancer. J Bone Miner Metab 2023;41:307-316. 
  19. Gradishar WJ, Moran MS, Abraham J, et al. NCCN Guidelines® Insights: breast cancer, version 4.2023. J Natl Compr Canc Netw 2023;21:594-608. 
  20. Spring LM, Wander SA, Andre F, Moy B, Turner NC, Bardia A. Cyclin-dependent kinase 4 and 6 inhibitors for hormone receptor-positive breast cancer: past, present, and future. Lancet 2020;395:817-827. 
  21. Harbeck N, Rastogi P, Martin M, et al. Adjuvant abemaciclib combined with endocrine therapy for high-risk early breast cancer: updated efficacy and Ki-67 analysis from the monarchE study. Ann Oncol 2021;32:1571-1581. 
  22. Powles TJ, Hickish T, Kanis JA, Tidy A, Ashley S. Effect of tamoxifen on bone mineral density measured by dual-energy x-ray absorptiometry in healthy premenopausal and postmenopausal women. J Clin Oncol 1996;14:78-84. 
  23. Stumpf U, Kostev K, Kyvernitakis J, Bocker W, Hadji P. Incidence of fractures in young women with breast cancer - a retrospective cohort study. J Bone Oncol 2019;18:100254. 
  24. Dowsett M, Cuzick J, Ingle J, et al. Meta-analysis of breast cancer outcomes in adjuvant trials of aromatase inhibitors versus tamoxifen. J Clin Oncol 2010;28:509-518. 
  25. Pagani O, Regan MM, Walley BA, et al. Adjuvant exemestane with ovarian suppression in premenopausal breast cancer. N Engl J Med 2014;371:107-118. 
  26. Hadji P. Aromatase inhibitor-associated bone loss in breast cancer patients is distinct from postmenopausal osteoporosis. Crit Rev Oncol Hematol 2009;69:73-82. 
  27. Eastell R, Adams JE, Coleman RE, et al. Effect of anastrozole on bone mineral density: 5-year results from the anastrozole, tamoxifen, alone or in combination trial 18233230. J Clin Oncol 2008;26:1051-1057. 
  28. BIG 1-98 Collaborative Group; Mouridsen H, Giobbie-Hurder A, Goldhirsch A, et al. Letrozole therapy alone or in sequence with tamoxifen in women with breast cancer. N Engl J Med 2009;361:766-776. 
  29. Coleman RE, Banks LM, Girgis SI, et al. Skeletal effects of exemestane on bone-mineral density, bone biomarkers, and fracture incidence in postmenopausal women with early breast cancer participating in the Intergroup Exemestane Study (IES): a randomised controlled study. Lancet Oncol 2007;8:119-127. 
  30. Amir E, Seruga B, Niraula S, Carlsson L, Ocana A. Toxicity of adjuvant endocrine therapy in postmenopausal breast cancer patients: a systematic review and meta-analysis. J Natl Cancer Inst 2011;103:1299-1309. 
  31. Lee YK, Lee EG, Kim HY, et al. Osteoporotic fractures of the spine, hip, and other locations after adjuvant endocrine therapy with aromatase inhibitors in breast cancer patients: a meta-analysis. J Korean Med Sci 2020;35:e403. 
  32. Cuzick J, Sestak I, Baum M, et al. Effect of anastrozole and tamoxifen as adjuvant treatment for early-stage breast cancer: 10-year analysis of the ATAC trial. Lancet Oncol 2010;11:1135-1141. 
  33. Goldvaser H, Barnes TA, Seruga B, et al. Toxicity of extended adjuvant therapy with aromatase inhibitors in early breast cancer: a systematic review and meta-analysis. J Natl Cancer Inst 2018;110:31-39. 
  34. Sverrisdottir A, Fornander T, Jacobsson H, von Schoultz E, Rutqvist LE. Bone mineral density among premenopausal women with early breast cancer in a randomized trial of adjuvant endocrine therapy. J Clin Oncol 2004;22:3694-3699. 
  35. Kalder M, Kyvernitakis I, Albert US, Baier-Ebert M, Hadji P. Effects of zoledronic acid versus placebo on bone mineral density and bone texture analysis assessed by the trabecular bone score in premenopausal women with breast cancer treatment-induced bone loss: results of the ProBONE II substudy. Osteoporos Int 2015;26:353-360. 
  36. Gnant M, Mlineritsch B, Luschin-Ebengreuth G, et al. Adjuvant endocrine therapy plus zoledronic acid in premenopausal women with early-stage breast cancer: 5-year follow-up of the ABCSG-12 bone-mineral density substudy. Lancet Oncol 2008;9:840-849. 
  37. Yoneda K, Tanji Y, Okishiro M, Taguchi T, Tamaki Y, Noguchi S. Influence of adjuvant anastrozole on bone mineral density in Japanese postmenopausal breast cancer patients: is there a racial difference? Ann Oncol 2006;17:1175-1176. 
  38. Iuliani M, Simonetti S, Ribelli G, et al. Biological effects of cyclin-dependent kinase inhibitors ribociclib, palbociclib and abemaciclib on breast cancer bone microenvironment. Int J Mol Sci 2022;23:2477. 
  39. Mitsiades N, Kaochar S. Androgen receptor signaling inhibitors: post-chemotherapy, pre-chemotherapy and now in castration-sensitive prostate cancer. Endocr Relat Cancer 2021;28:T19-T38. 
  40. Mohamad NV, Soelaiman IN, Chin KY. A concise review of testosterone and bone health. Clin Interv Aging 2016;11:1317-1324. 
  41. Kiratli BJ, Srinivas S, Perkash I, Terris MK. Progressive decrease in bone density over 10 years of androgen deprivation therapy in patients with prostate cancer. Urology 2001;57:127-132. 
  42. Shahinian VB, Kuo YF, Freeman JL, Goodwin JS. Risk of fracture after androgen deprivation for prostate cancer. N Engl J Med 2005;352:154-164. 
  43. Wallander M, Axelsson KF, Lundh D, Lorentzon M. Patients with prostate cancer and androgen deprivation therapy have increased risk of fractures-a study from the fractures and fall injuries in the elderly cohort (FRAILCO). Osteoporos Int 2019;30:115-125. 
  44. Smith MR, Lee WC, Brandman J, Wang Q, Botteman M, Pashos CL. Gonadotropin-releasing hormone agonists and fracture risk: a claims-based cohort study of men with nonmetastatic prostate cancer. J Clin Oncol 2005;23:7897-7903. 
  45. Morgans AK, Fan KH, Koyama T, et al. Bone complications among prostate cancer survivors: long-term follow-up from the prostate cancer outcomes study. Prostate Cancer Prostatic Dis 2014;17:338-342. 
  46. Iuliani M, Pantano F, Buttigliero C, et al. Biological and clinical effects of abiraterone on anti-resorptive and anabolic activity in bone microenvironment. Oncotarget 2015;6:12520-12528. 
  47. Nakajima S, Inoue T, Huang M, et al. Does the addition of abiraterone to castration affect the reduction in bone mineral density? In Vivo 2020;34:3291-3299. 
  48. Wu J, Moverare-Skrtic S, Borjesson AE, et al. Enzalutamide reduces the bone mass in the axial but not the appendicular skeleton in male mice. Endocrinology 2016;157:969-977. 
  49. Smith MR, Saad F, Chowdhury S, et al. Apalutamide treatment and metastasis-free survival in prostate cancer. N Engl J Med 2018;378:1408-1418. 
  50. Fizazi K, Shore N, Tammela TL, et al. Darolutamide in nonmetastatic, castration-resistant prostate cancer. N Engl J Med 2019;380:1235-1246. 
  51. Hussain M, Fizazi K, Saad F, et al. Enzalutamide in men with nonmetastatic, castration-resistant prostate cancer. N Engl J Med 2018;378:2465-2474. 
  52. Swaminathan R. Magnesium metabolism and its disorders. Clin Biochem Rev 2003;24:47-66. 
  53. Stavraka C, Maclaran K, Gabra H, et al. A study to evaluate the cause of bone demineralization in gynecological cancer survivors. Oncologist 2013;18:423-429. 
  54. Hu XC, Zhang J, Xu BH, et al. Cisplatin plus gemcitabine versus paclitaxel plus gemcitabine as first-line therapy for metastatic triple-negative breast cancer (CBCSG006): a randomised, open-label, multicentre, phase 3 trial. Lancet Oncol 2015;16:436-446. 
  55. Stava CJ, Jimenez C, Hu MI, Vassilopoulou-Sellin R. Skeletal sequelae of cancer and cancer treatment. J Cancer Surviv 2009;3:75-88. 
  56. Pfeilschifter J, Diel IJ. Osteoporosis due to cancer treatment: pathogenesis and management. J Clin Oncol 2000;18:1570-1593. 
  57. Rana T, Chakrabarti A, Freeman M, Biswas S. Doxorubicin-mediated bone loss in breast cancer bone metastases is driven by an interplay between oxidative stress and induction of TGFβ. PLoS One 2013;8:e78043. 
  58. Soleimani R, Heytens E, Darzynkiewicz Z, Oktay K. Mechanisms of chemotherapy-induced human ovarian aging: double strand DNA breaks and microvascular compromise. Aging (Albany NY) 2011;3:782-793. 
  59. Georgiou KR, Scherer MA, Fan CM, et al. Methotrexate chemotherapy reduces osteogenesis but increases adipogenic potential in the bone marrow. J Cell Physiol 2012;227:909-918. 
  60. Georgiou KR, King TJ, Scherer MA, et al. Attenuated Wnt/β-catenin signalling mediates methotrexate chemotherapy-induced bone loss and marrow adiposity in rats. Bone 2012;50:1223-1233. 
  61. Shandala T, Shen Ng Y, Hopwood B, et al. The role of osteocyte apoptosis in cancer chemotherapy-induced bone loss. J Cell Physiol 2012;227:2889-2897. 
  62. King TJ, Georgiou KR, Cool JC, et al. Methotrexate chemotherapy promotes osteoclast formation in the long bone of rats via increased pro-inflammatory cytokines and enhanced NF-κB activation. Am J Pathol 2012;181:121-129. 
  63. Meier L, van Tuyll van Sersooskerken AM, Liberton E, et al. Fractures of the proximal tibia associated with longterm use of methotrexate: 3 case reports and a review of literature. J Rheumatol 2010;37:2434-2438. 
  64. Aksnes LH, Bruland OS. Some musculo-skeletal sequelae in cancer survivors. Acta Oncol 2007;46:490-496. 
  65. Mori G, D'Amelio P, Faccio R, Brunetti G. Bone-immune cell crosstalk: bone diseases. J Immunol Res 2015;2015:108451. 
  66. Dietrich J, Rao K, Pastorino S, Kesari S. Corticosteroids in brain cancer patients: benefits and pitfalls. Expert Rev Clin Pharmacol 2011;4:233-242. 
  67. Paccou J, Merlusca L, Henry-Desailly I, et al. Alterations in bone mineral density and bone turnover markers in newly diagnosed adults with lymphoma receiving chemotherapy: a 1-year prospective pilot study. Ann Oncol 2014;25:481-486. 
  68. Aggarwal S. Targeted cancer therapies. Nat Rev Drug Discov 2010;9:427-428. 
  69. Sawyers C. Targeted cancer therapy. Nature 2004;432:294-297. 
  70. Arora A, Scholar EM. Role of tyrosine kinase inhibitors in cancer therapy. J Pharmacol Exp Ther 2005;315:971-979. 
  71. Druker BJ. David A. Karnofsky Award lecture. Imatinib as a paradigm of targeted therapies. J Clin Oncol 2003;21(23 Suppl):239s-245s. 
  72. Capdeville R, Buchdunger E, Zimmermann J, Matter A. Glivec (STI571, imatinib), a rationally developed, targeted anticancer drug. Nat Rev Drug Discov 2002;1:493-502. 
  73. Reichardt P, Blay JY, Boukovinas I, et al. Adjuvant therapy in primary GIST: state-of-the-art. Ann Oncol 2012;23:2776-2781. 
  74. Patel S. Long-term efficacy of imatinib for treatment of metastatic GIST. Cancer Chemother Pharmacol 2013;72:277-286. 
  75. Vandyke K, Fitter S, Dewar AL, Hughes TP, Zannettino AC. Dysregulation of bone remodeling by imatinib mesylate. Blood 2010;115:766-774. 
  76. Fitter S, Dewar AL, Kostakis P, et al. Long-term imatinib therapy promotes bone formation in CML patients. Blood 2008;111:2538-2547. 
  77. O'Sullivan S, Naot D, Callon KE, et al. Imatinib mesylate does not increase bone volume in vivo. Calcif Tissue Int 2011;88:16-22. 
  78. Berman E, Nicolaides M, Maki RG, et al. Altered bone and mineral metabolism in patients receiving imatinib mesylate. N Engl J Med 2006;354:2006-2013. 
  79. Berman E, Girotra M, Cheng C, et al. Effect of long term imatinib on bone in adults with chronic myelogenous leukemia and gastrointestinal stromal tumors. Leuk Res 2013;37:790-794. 
  80. Aleman JO, Farooki A, Girotra M. Effects of tyrosine kinase inhibition on bone metabolism: untargeted consequences of targeted therapies. Endocr Relat Cancer 2014;21:R247-R259. 
  81. Gnant M, Baselga J, Rugo HS, et al. Effect of everolimus on bone marker levels and progressive disease in bone in BOLERO-2. J Natl Cancer Inst 2013;105:654-663. 
  82. Kneissel M, Luong-Nguyen NH, Baptist M, et al. Everolimus suppresses cancellous bone loss, bone resorption, and cathepsin K expression by osteoclasts. Bone 2004;35:1144-1156. 
  83. Moseley KF, Naidoo J, Bingham CO, et al. Immune-related adverse events with immune checkpoint inhibitors affecting the skeleton: a seminal case series. J Immunother Cancer 2018;6:104. 
  84. Filippini DM, Gatti M, Di Martino V, et al. Bone fracture as a novel immune-related adverse event with immune checkpoint inhibitors: case series and large-scale pharmacovigilance analysis. Int J Cancer 2021;149:675-683. 
  85. Chandra A, Lin T, Tribble MB, et al. PTH1-34 alleviates radiotherapy-induced local bone loss by improving osteoblast and osteocyte survival. Bone 2014;67:33-40. 
  86. Baxter NN, Habermann EB, Tepper JE, Durham SB, Virnig BA. Risk of pelvic fractures in older women following pelvic irradiation. JAMA 2005;294:2587-2593. 
  87. Dybvik E, Furnes O, Fossa SD, Trovik C, Lie SA. Pelvic irradiation does not increase the risk of hip replacement in patients with gynecological cancer. A cohort study based on 8,507 patients. Acta Orthop 2014;85:652-656. 
  88. Wilson SD, Doffek KM, Wang TS, Krzywda EA, Evans DB, Yen TW. Primary hyperparathyroidism with a history of head and neck irradiation: the consequences of associated thyroid tumors. Surgery 2011;150:869-877. 
  89. Wasilewski-Masker K, Kaste SC, Hudson MM, Esiashvili N, Mattano LA, Meacham LR. Bone mineral density deficits in survivors of childhood cancer: long-term follow-up guidelines and review of the literature. Pediatrics 2008;121:e705-e713. 
  90. Camacho PM, Petak SM, Binkley N, et al. American Association of Clinical Endocrinologists/American College of Endocrinology clinical practice guidelines for the diagnosis and treatment of postmenopausal osteoporosis-2020 update. Endocr Pract 2020;26(Suppl 1):1-46. 
  91. Kanis JA, Johansson H, Oden A, Cooper C, McCloskey EV. Worldwide uptake of FRAX. Arch Osteoporos 2014;9:166. 
  92. Leslie WD, Morin SN, Lix LM, et al. Performance of FRAX in women with breast cancer initiating aromatase inhibitor therapy: a registry-based cohort study. J Bone Miner Res 2019;34:1428-1435. 
  93. Datta M, Schwartz GG. Calcium and vitamin D supplementation during androgen deprivation therapy for prostate cancer: a critical review. Oncologist 2012;17:1171-1179. 
  94. van Schoor NM, Visser M, Pluijm SM, Kuchuk N, Smit JH, Lips P. Vitamin D deficiency as a risk factor for osteoporotic fractures. Bone 2008;42:260-266. 
  95. Dalla Via J, Daly RM, Fraser SF. The effect of exercise on bone mineral density in adult cancer survivors: a systematic review and meta-analysis. Osteoporos Int 2018;29:287-303. 
  96. Lomax AJ, Yee Yap S, White K, et al. Prevention of aromatase inhibitor-induced bone loss with alendronate in postmenopausal women: the BATMAN Trial. J Bone Oncol 2013;2:145-153. 
  97. Van Poznak C, Hannon RA, Mackey JR, et al. Prevention of aromatase inhibitor-induced bone loss using risedronate: the SABRE trial. J Clin Oncol 2010;28:967-975. 
  98. Brufsky AM, Harker WG, Beck JT, et al. Final 5-year results of Z-FAST trial: adjuvant zoledronic acid maintains bone mass in postmenopausal breast cancer patients receiving letrozole. Cancer 2012;118:1192-1201. 
  99. Coleman R, de Boer R, Eidtmann H, et al. Zoledronic acid (zoledronate) for postmenopausal women with early breast cancer receiving adjuvant letrozole (ZO-FAST study): final 60-month results. Ann Oncol 2013;24:398-405. 
  100. Llombart A, Frassoldati A, Paija O, et al. Immediate administration of zoledronic acid reduces aromatase inhibitor-associated bone loss in postmenopausal women with early breast cancer: 12-month analysis of the E-ZO-FAST trial. Clin Breast Cancer 2012;12:40-48. 
  101. Gnant M, Mlineritsch B, Schippinger W, et al. Endocrine therapy plus zoledronic acid in premenopausal breast cancer. N Engl J Med 2009;360:679-691. 
  102. Hong N, Burm SW, Treece G, et al. Protective effect of bisphosphonate on the cortical bone at key locations of the femur in aromatase inhibitor-associated bone loss: A three-dimensional cortical bone mapping study. J Bone Oncol 2021;32:100409. 
  103. Lester JE, Dodwell D, Purohit OP, et al. Prevention of anastrozole-induced bone loss with monthly oral ibandronate during adjuvant aromatase inhibitor therapy for breast cancer. Clin Cancer Res 2008;14:6336-6342. 
  104. Brufsky AM, Bosserman LD, Caradonna RR, et al. Zoledronic acid effectively prevents aromatase inhibitor-associated bone loss in postmenopausal women with early breast cancer receiving adjuvant letrozole: Z-FAST study 36-month follow-up results. Clin Breast Cancer 2009;9:77-85. 
  105. Wilson C, Bell R, Hinsley S, et al. Adjuvant zoledronic acid reduces fractures in breast cancer patients; an AZURE (BIG 01/04) study. Eur J Cancer 2018;94:70-78. 
  106. Valachis A, Polyzos NP, Coleman RE, et al. Adjuvant therapy with zoledronic acid in patients with breast cancer: a systematic review and meta-analysis. Oncologist 2013;18:353-361. 
  107. Israeli RS, Rosenberg SJ, Saltzstein DR, et al. The effect of zoledronic acid on bone mineral density in patients undergoing androgen deprivation therapy. Clin Genitourin Cancer 2007;5:271-277. 
  108. Greenspan SL, Nelson JB, Trump DL, Resnick NM. Effect of once-weekly oral alendronate on bone loss in men receiving androgen deprivation therapy for prostate cancer: a randomized trial. Ann Intern Med 2007;146:416-424. 
  109. Jones C, Sachdeva A, Murphy L, et al. Clinical fracture incidence in metastatic hormone-sensitive prostate cancer (mHSPC) and risk-reduction following addition of zoledronic acid to androgen deprivation therapy (ADT) with or without docetaxel (DOC): long-term results from 2 phase 3 trials from the STAMPEDE platform protocol. J Urol 2023;209(Suppl 4):e129. 
  110. Ellis GK, Bone HG, Chlebowski R, et al. Randomized trial of denosumab in patients receiving adjuvant aromatase inhibitors for nonmetastatic breast cancer. J Clin Oncol 2008;26:4875-4882. 
  111. Gnant M, Pfeiler G, Dubsky PC, et al. Adjuvant denosumab in breast cancer (ABCSG-18): a multicentre, randomised, double-blind, placebo-controlled trial. Lancet 2015;386:433-443. 
  112. Smith MR, Egerdie B, Hernandez Toriz N, et al. Denosumab in men receiving androgen-deprivation therapy for prostate cancer. N Engl J Med 2009;361:745-755. 
  113. Lovato C, Lewiecki EM. Emerging anabolic agents in the treatment of osteoporosis. Expert Opin Emerg Drugs 2017;22:247-257. 
  114. Reid DM, Doughty J, Eastell R, et al. Guidance for the management of breast cancer treatment-induced bone loss: a consensus position statement from a UK Expert Group. Cancer Treat Rev 2008;34 Suppl 1:S3-S18. 
  115. Gralow JR, Biermann JS, Farooki A, et al. NCCN task force report: bone health in cancer care. J Natl Compr Canc Netw 2013;11 Suppl 3:S1-S50; quiz S51. 
  116. Waqas K, Lima Ferreira J, Tsourdi E, Body JJ, Hadji P, Zillikens MC. Updated guidance on the management of cancer treatment-induced bone loss (CTIBL) in pre- and postmenopausal women with early-stage breast cancer. J Bone Oncol 2021;28:100355. 
  117. Shapiro CL, Van Poznak C, Lacchetti C, et al. Management of osteoporosis in survivors of adult cancers with nonmetastatic disease: ASCO clinical practice guideline. J Clin Oncol 2019;37:2916-2946.s 
  118. Fukumoto S, Soen S, Taguchi T, et al. Management manual for cancer treatment-induced bone loss (CTIBL): position statement of the JSBMR. J Bone Miner Metab 2020;38:141-144. 
  119. National Institute for Health and Clinical Excellence (NICE). Prostate cancer: diagnosis and management. Clinical guideline NG 131 [Internet]. London: NICE, c2021 [cited 2023 Sep 24]. Available from: www.nice.org.uk/guidance/ng131.