Cancer Treatment-Induced Bone Loss: Role of Denosumab in Non-Metastatic Breast Cancer

References

• Ghoncheh M, Pournamdar Z, Salehiniya H. Incidence and mortality and epidemiology of breast cancer in the world. Asian Pac J Cancer Prev. 2016;17(S3):43–46. doi:10.7314/APJCP.2016.17.S3.43
   PubMedGoogle Scholar
• Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424. doi:10.3322/caac.21492
   PubMed Web of Science ®Google Scholar
• World Health Organization. International agency for research on cancer. The Global Cancer Observatory (Globocan 2020). World; 2021. Available from: https://gco.iarc.fr/today/data/factsheets/populations/900-world-fact-sheets.pdf. Accessed June 28, 2022.
   Google Scholar
• World Health Organization. International agency for research on cancer. The Global Cancer Observatory (Globocan 2020). India; 2021. Available from: https://gco.iarc.fr/today/data/factsheets/populations/356-india-fact-sheets.pdf. Accessed June 28, 2022.
   Google Scholar
• Chen Z, Maricic M, Aragaki AK, et al. Fracture risk increases after diagnosis of breast or other cancers in postmenopausal women: results from the Women’s Health Initiative. Osteoporos Int. 2009;20(4):527–536. doi:10.1007/s00198-008-0721-0
   PubMed Web of Science ®Google Scholar
• Lipton A, Smith MR, Ellis GK, et al. Treatment-induced bone loss and fractures in cancer patients undergoing hormone ablation therapy: efficacy and safety of denosumab. Clin Med Insights Oncol. 2012;6:287–303. doi:10.4137/CMO.S8511
   PubMedGoogle Scholar
• Winer EP. Optimizing endocrine therapy for breast cancer. J Clin Oncol. 2005;23(8):1609–1610. doi:10.1200/JCO.2005.01.005
   PubMed Web of Science ®Google Scholar
• Patnayak R, Jena A, Rukmangadha N, et al. Hormone receptor status (estrogen receptor, progesterone receptor), human epidermal growth factor-2 and p53 in South Indian breast cancer patients: a tertiary care center experience. Indian J Med Paediatr Oncol. 2015;36(2):117–122. doi:10.4103/0971-5851.158844
   PubMedGoogle Scholar
• Chatterjee K, Bhaumik G, Chattopadhyay B. Estrogen receptor and progesterone receptor status of breast cancer patients of eastern India: a multi-institutional study. South Asian J Cancer. 2018;7(1):5–6. doi:10.4103/sajc.sajc_60_17
   PubMed Web of Science ®Google Scholar
• Desai SB, Moonim MT, Gill AK, et al. Hormone receptor status of breast cancer in India: a study of 798 tumours. Breast. 2000;9(5):267–270. doi:10.1054/brst.2000.0134
   PubMed Web of Science ®Google Scholar
• Burstein HJ, Lacchetti C, Anderson H, et al. Adjuvant endocrine therapy for women with hormone receptor–positive breast cancer: American society of clinical oncology clinical practice guideline update on ovarian suppression. J Clin Oncol. 2016;34(14):1689–1701. doi:10.1200/JCO.2015.65.9573
   PubMed Web of Science ®Google Scholar
• Senkus E, Kyriakides S, Ohno S, et al. Primary breast cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2015;26(Suppl 5):v8–v30. doi:10.1093/annonc/mdv298
   PubMed Web of Science ®Google Scholar
• Winer EP, Hudis C, Burstein HJ, et al. American Society of Clinical Oncology technology assessment on the use of aromatase inhibitors as adjuvant therapy for postmenopausal women with hormone receptor-positive breast cancer: status report 2004. J Clin Oncol. 2005;23(3):619–629. doi:10.1200/JCO.2005.09.121
   PubMed Web of Science ®Google Scholar
• Moser K, Patnick J, Beral V. Do women know that the risk of breast cancer increases with age? Br J Gen Pract. 2007;57(538):404–406.
   PubMed Web of Science ®Google Scholar
• Planas Morin J, Morote Robles J. Skeletal complications of ADT: disease burden and treatment options. Asian J Androl. 2012;14(5):670–675. doi:10.1038/aja.2012.70
   PubMed Web of Science ®Google Scholar
• Kalder M, Hadji P. Breast cancer and osteoporosis - management of cancer treatment-induced bone loss in postmenopausal women with breast cancer. Breast Care. 2014;9(5):312–317. doi:10.1159/000368843
   PubMed Web of Science ®Google Scholar
• Boskey AL, Coleman R. Aging and bone. J Dent Res. 2010;89(12):1333–1348. doi:10.1177/0022034510377791
   PubMed Web of Science ®Google Scholar
• Delmas PD, Fontana A. Bone loss induced by cancer treatment and its management. Eur J Cancer. 1998;34(2):260–262. doi:10.1016/S0959-8049(97)10135-6
   PubMed Web of Science ®Google Scholar
• Hadji P, Gottschalk M, Ziller V, et al. Bone mass and the risk of breast cancer: the influence of cumulative exposure to oestrogen and reproductive correlates. Results of the Marburg breast cancer and osteoporosis trial (MABOT). Maturitas. 2007;56(3):312–321. doi:10.1016/j.maturitas.2006.09.005
   PubMed Web of Science ®Google Scholar
• Ramaswamy B, Shapiro CL. Osteopenia and osteoporosis in women with breast cancer. Semin Oncol. 2003;30(6):763–775. doi:10.1053/j.seminoncol.2003.08.028
   PubMed Web of Science ®Google Scholar
• Agostini D, Zeppa Donati S, Lucertini F, et al. Muscle and bone health in postmenopausal women: role of protein and Vitamin D supplementation combined with exercise training. Nutrients. 2018;10(8):1103. doi:10.3390/nu10081103
   PubMed Web of Science ®Google Scholar
• Taxel P, Faircloth E, Idrees S, et al. Cancer treatment-induced bone loss in women with breast cancer and men with prostate cancer. J Endocr Soc. 2018;2(7):574–588. doi:10.1210/js.2018-00052
   PubMed Web of Science ®Google Scholar
• Robertson JF, Blamey RW. The use of gonadotrophin-releasing hormone (GnRH) agonists in early and advanced breast cancer in pre- and perimenopausal women. Eur J Cancer. 2003;39(7):861–869. doi:10.1016/S0959-8049(02)00810-9
   PubMed Web of Science ®Google Scholar
• Sverrisdóttir A, Fornander T, Jacobsson H, et al. Bone mineral density among premenopausal women with early breast cancer in a randomized trial of adjuvant endocrine therapy. J Clin Oncol. 2004;22(18):3694–3699. doi:10.1200/JCO.2004.08.148
   PubMed Web of Science ®Google Scholar
• Dowsett M, Forbes JF, Bradley R, et al. Aromatase inhibitors versus tamoxifen in early breast cancer: patient-level meta-analysis of the randomised trials. Lancet. 2015;386(10001):1341–1352. doi:10.1016/S0140-6736(15)61074-1
   PubMed Web of Science ®Google Scholar
• 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(31):2916–2946. doi:10.1200/JCO.19.01696
   PubMed Web of Science ®Google Scholar
• 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(7):1051–1057. doi:10.1200/JCO.2007.11.0726
   PubMed Web of Science ®Google Scholar
• Gnant MF, Mlineritsch B, Luschin-Ebengreuth G, et al. Zoledronic acid prevents cancer treatment-induced bone loss in premenopausal women receiving adjuvant endocrine therapy for hormone-responsive breast cancer: a report from the Austrian Breast and Colorectal Cancer Study Group. J Clin Oncol. 2007;25(7):820–828. doi:10.1200/JCO.2005.02.7102
   PubMed Web of Science ®Google Scholar
• Shapiro CL, Manola J, Leboff M. Ovarian failure after adjuvant chemotherapy is associated with rapid bone loss in women with early-stage breast cancer. J Clin Oncol. 2001;19(14):3306–3311. doi:10.1200/JCO.2001.19.14.3306
   PubMed Web of Science ®Google Scholar
• Maillefert JF, Sibilia J, Michel F, et al. Bone mineral density in men treated with synthetic gonadotropin-releasing hormone agonists for prostatic carcinoma. J Urol. 1999;161(4):1219–1222. doi:10.1016/S0022-5347(01)61639-2
   PubMed Web of Science ®Google Scholar
• 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. doi:10.6004/jnccn.2013.0215
   PubMed Web of Science ®Google Scholar
• Coleman RE. Effect of anastrozole on bone mineral density: 5-year results from the ’Arimidex’, Tamoxifen, Alone or in Combination (ATAC) trial. J Clin Oncol. 2006;24(18_suppl):511. doi:10.1200/jco.2006.24.18_suppl.511
   Web of Science ®Google Scholar
• Hamilton A, Piccart M. The third-generation non-steroidal aromatase inhibitors: a review of their clinical benefits in the second-line hormonal treatment of advanced breast cancer. Ann Oncol. 1999;10(4):377–384. doi:10.1023/A:1008368300827
   PubMed Web of Science ®Google Scholar
• Mincey BA, Duh MS, Thomas SK, et al. Risk of cancer treatment-associated bone loss and fractures among women with breast cancer receiving aromatase inhibitors. Clin Breast Cancer. 2006;7(2):127–132. doi:10.3816/CBC.2006.n.021
   PubMed Web of Science ®Google Scholar
• Hadji P. Aromatase inhibitor-associated bone loss in breast cancer patients is distinct from postmenopausal osteoporosis. Crit Rev Oncol Hematol. 2009;69(1):73–82. doi:10.1016/j.critrevonc.2008.07.013
   PubMed Web of Science ®Google Scholar
• Bruning PF, Pit MJ, de Jong-Bakker M, et al. Bone mineral density after adjuvant chemotherapy for premenopausal breast cancer. Br J Cancer. 1990;61(2):308–310. doi:10.1038/bjc.1990.58
   PubMed Web of Science ®Google Scholar
• Bines J, Oleske DM, Cobleigh MA. Ovarian function in premenopausal women treated with adjuvant chemotherapy for breast cancer. J Clin Oncol. 1996;14(5):1718–1729. doi:10.1200/JCO.1996.14.5.1718
   PubMed Web of Science ®Google Scholar
• Saarto T, Blomqvist C, Välimäki M, et al. Chemical castration induced by adjuvant cyclophosphamide, methotrexate, and fluorouracil chemotherapy causes rapid bone loss that is reduced by clodronate: a randomized study in premenopausal breast cancer patients. J Clin Oncol. 1997;15(4):1341–1347. doi:10.1200/JCO.1997.15.4.1341
   PubMed Web of Science ®Google Scholar
• Greep NC, Giuliano AE, Hansen NM, et al. The effects of adjuvant chemotherapy on bone density in postmenopausal women with early breast cancer. Am J Med. 2003;114(8):653–659. doi:10.1016/S0002-9343(03)00127-X
   PubMed Web of Science ®Google Scholar
• Fontanges E, Fontana A, Delmas P. Osteoporosis and breast cancer. Joint Bone Spine. 2004;71(2):102–110. doi:10.1016/j.jbspin.2003.02.001
   PubMed Web of Science ®Google Scholar
• Overgaard M. Spontaneous radiation-induced rib fractures in breast cancer patients treated with postmastectomy irradiation. A clinical radiobiological analysis of the influence of fraction size and dose-response relationships on late bone damage. Acta Oncol. 1988;27(2):117–122. doi:10.3109/02841868809090331
   PubMed Web of Science ®Google Scholar
• Mavrogenis AF, Pala E, Romantini M, et al. Side effects of radiation in musculoskeletal oncology: clinical evaluation of radiation-induced fractures. Int J Immunopathol Pharmacol. 2011;24(1_suppl2):29–37. doi:10.1177/03946320110241S207
   PubMed Web of Science ®Google Scholar
• Alouani E, Parent L, Massabeau C, et al. [Rib fracture following intra-operative radiotherapy for breast cancer. Case Report and local experience]. Cancer Radiother. 2020;24(1):64–66. French. doi:10.1016/j.canrad.2019.10.005
   PubMed Web of Science ®Google Scholar
• Salcedo MP, Sood AK, Jhingran A, et al. Pelvic fractures and changes in bone mineral density after radiotherapy for cervical, endometrial, and vaginal cancer: a prospective study of 239 women. Cancer. 2020;126(11):2607–2613. doi:10.1002/cncr.32807
   PubMed Web of Science ®Google Scholar
• Dybvik E, Furnes O, Fosså SD, et al. Pelvic irradiation does not increase the risk of Hip replacement in patients with gynecological cancer. A cohort study based on 8507 patients. Acta orthopaedica. 2014;85(6):652–656. doi:10.3109/17453674.2014.963784
   PubMed Web of Science ®Google Scholar
• Wissing MD. Chemotherapy- and irradiation-induced bone loss in adults with solid tumors. Curr Osteoporos Rep. 2015;13(3):140–145. doi:10.1007/s11914-015-0266-z
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1016/j.ctrv.2008.03.007
   PubMed Web of Science ®Google Scholar
• Novak S. [Antiresorptive agents in the treatment of osteoporosis]. Reumatizam. 2014;61(2):89–94. Croatian.
   PubMedGoogle Scholar
• Deal C. Osteoporosis therapies Bisphosphonates, SERMs, PTH, and new therapies. Clin Rev Bone Miner Metab. 2005;3(2):125–141. doi:10.1385/BMM:3:2:125
   Google Scholar
• Prolia (denosumab). Prescribing information. Accessed from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2020/125320s205lbl.pdf. Accessed July 21, 2020.
   Google Scholar
• Hadji P, Aapro MS, Body -J-J, 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. doi:10.1016/j.jbo.2017.03.001
   PubMed Web of Science ®Google Scholar
• Coleman R, Hadji P, Body JJ, et al. Bone health in cancer: ESMO clinical practice guidelines†. Ann Oncol. 2020;31(12):1650–1663. doi:10.1016/j.annonc.2020.07.019
   PubMed Web of Science ®Google Scholar
• Balic M, Thomssen C, Würstlein R, et al. Gallen/Vienna 2019: a brief summary of the consensus discussion on the optimal primary breast cancer treatment. Breast Care. 2019;14(2):103–110. doi:10.1159/000499931
   PubMed Web of Science ®Google Scholar
• Lewiecki EM. Denosumab in postmenopausal osteoporosis: what the clinician needs to know. Ther Adv Musculoskelet Dis. 2009;1(1):13–26. doi:10.1177/1759720X09343221
   PubMedGoogle Scholar
• Cummings SR, Martin JS, McClung MR, et al. Denosumab for prevention of fractures in postmenopausal women with osteoporosis. N Engl J Med. 2009;361(8):756–765. doi:10.1056/NEJMoa0809493
   PubMed Web of Science ®Google Scholar
• Bone HG, Wagman RB, Brandi ML, et al. 10 years of denosumab treatment in postmenopausal women with osteoporosis: results from the Phase 3 randomised FREEDOM trial and open-label extension. Lancet Diabetes Endocrinol. 2017;5(7):513–523. doi:10.1016/S2213-8587(17)30138-9
   PubMed Web of Science ®Google Scholar
• 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(30):4875–4882. doi:10.1200/JCO.2008.16.3832
   PubMed Web of Science ®Google Scholar
• 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(9992):433–443. doi:10.1016/S0140-6736(15)60995-3
   PubMed Web of Science ®Google Scholar
• Gnant M, Pfeiler G, Steger GG, et al. Adjuvant denosumab in postmenopausal patients with hormone receptor-positive breast cancer (ABCSG-18): disease-free survival results from a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol. 2019;20(3):339–351. doi:10.1016/S1470-2045(18)30862-3
   PubMed Web of Science ®Google Scholar
• Nakatsukasa K, Koyama H, Ouchi Y, et al. Effect of denosumab administration on low bone mineral density (T-score −1.0 to −2.5) in postmenopausal Japanese women receiving adjuvant aromatase inhibitors for non-metastatic breast cancer. J Bone Miner Metab. 2018;36(6):716–722. doi:10.1007/s00774-017-0884-x
   PubMed Web of Science ®Google Scholar
• Nakatsukasa K, Koyama H, Ouchi Y, et al. Effect of denosumab on bone mineral density in Japanese women with osteopenia treated with aromatase inhibitors for breast cancer: subgroup analyses of a Phase II study. Ther Clin Risk Manag. 2018;14:1213–1218. doi:10.2147/TCRM.S167579
   PubMed Web of Science ®Google Scholar
• Nakatsukasa K, Koyama H, Ouchi Y, et al. Effects of denosumab on bone mineral density in Japanese women with osteoporosis treated with aromatase inhibitors for breast cancer. J Bone Miner Metab. 2019;37(2):301–306. doi:10.1007/s00774-018-0917-0
   PubMed Web of Science ®Google Scholar
• Nakatsukasa K, Koyama H, Ouchi Y, et al. Effect of denosumab on low bone mineral density in postmenopausal Japanese women receiving adjuvant aromatase inhibitors for non-metastatic breast cancer: 24-month results. Breast Cancer. 2019;26(1):106–112. doi:10.1007/s12282-018-0896-y
   PubMed Web of Science ®Google Scholar
• Scaturro D, de Sire A, Terrana P, et al. Early Denosumab for the prevention of osteoporotic fractures in breast cancer women undergoing aromatase inhibitors: a case-control retrospective study. J Back Musculoskelet Rehabil. 2022;35(1):207–212. doi:10.3233/BMR-210012
   PubMed Web of Science ®Google Scholar
• Poon Y, Pechlivanoglou P, Alibhai SMH, et al. Systematic review and network meta-analysis on the relative efficacy of osteoporotic medications: men with prostate cancer on continuous androgen-deprivation therapy to reduce risk of fragility fractures. BJU Int. 2018;121(1):17–28. doi:10.1111/bju.14015
   PubMed Web of Science ®Google Scholar
• Khan AA, Morrison A, Hanley DA, et al. Diagnosis and management of osteonecrosis of the jaw: a systematic review and international consensus. J Bone Miner Res. 2015;30(1):3–23. doi:10.1002/jbmr.2405
   PubMed Web of Science ®Google Scholar
• Stopeck AT, Lipton A, Body JJ, et al. Denosumab compared with zoledronic acid for the treatment of bone metastases in patients with advanced breast cancer: a randomized, double-blind study. J Clin Oncol. 2010;28(35):5132–5139. doi:10.1200/JCO.2010.29.7101
   PubMed Web of Science ®Google Scholar
• Doria C, Leali PT, Solla F, et al. Denosumab is really effective in the treatment of osteoporosis secondary to hypogonadism in prostate carcinoma patients? A prospective randomized multicenter international study. Clin Cases Miner Bone Metab. 2016;13(3):195–199. doi:10.11138/ccmbm/2016.13.3.195
   PubMedGoogle Scholar
• Hadji P, Kyvernitakis I, Kann PH, et al. GRAND-4: the German retrospective analysis of long-term persistence in women with osteoporosis treated with bisphosphonates or denosumab. Osteoporos Int. 2016;27(10):2967–2978. doi:10.1007/s00198-016-3623-6
   PubMed Web of Science ®Google Scholar
• Imai H, Saijo K, Yamada H, et al. Efficacy and safety of denosumab versus zoledronic acid in delaying skeletal-related events in patients with gastrointestinal cancer, pancreas-biliary system cancer, and other rare cancers. J Bone Oncol. 2017;6:37–40. doi:10.1016/j.jbo.2016.10.002
   Web of Science ®Google Scholar
• Abdel-Rahman O. Denosumab versus zoledronic acid to prevent aromatase inhibitors-associated fractures in postmenopausal early breast cancer; a mixed treatment meta-analysis. Expert Rev Anticancer Ther. 2016;16(8):885–891. doi:10.1080/14737140.2016.1192466
   PubMed Web of Science ®Google Scholar
• Miyashita H, Satoi S, Kuno T, et al. Bone modifying agents for bone loss in patients with aromatase inhibitor as adjuvant treatment for breast cancer; insights from a network meta-analysis. Breast Cancer Res Treat. 2020;181(2):279–289. doi:10.1007/s10549-020-05640-3
   PubMed Web of Science ®Google Scholar
• Deeks ED, Deeks ED. Denosumab: a review in postmenopausal osteoporosis. Drugs Aging. 2018;35(2):163–173. doi:10.1007/s40266-018-0525-7
   PubMed Web of Science ®Google Scholar
• Van den Wyngaert T, Wouters K, Huizing MT, et al. RANK ligand inhibition in bone metastatic cancer and risk of osteonecrosis of the jaw (ONJ): non bis in idem? Support Care Cancer. 2011;19(12):2035–2040. doi:10.1007/s00520-010-1061-0
   PubMed Web of Science ®Google Scholar
• Qaisi M, Hargett J, Loeb M, et al. Denosumab related osteonecrosis of the jaw with spontaneous necrosis of the soft palate: report of a life threatening case. Case Rep Dent. 2016;2016:5070187. doi:10.1155/2016/5070187
   PubMedGoogle Scholar
• Qi WX, Tang LN, He AN, et al. Risk of osteonecrosis of the jaw in cancer patients receiving denosumab: a meta-analysis of seven randomized controlled trials. Int J Clin Oncol. 2014;19(2):403–410. doi:10.1007/s10147-013-0561-6
   PubMed Web of Science ®Google Scholar
• Gonzalez-Rodriguez E, Aubry-Rozier B, Stoll D, et al. Increased risk of multiple spontaneous vertebral fractures at denosumab discontinuation must be taken into account. J Clin Oncol. 2020;38(14):1641–1642. doi:10.1200/JCO.19.02678
   PubMed Web of Science ®Google Scholar
• Tsourdi E, Langdahl B, Cohen-Solal M, et al. Discontinuation of Denosumab therapy for osteoporosis: a systematic review and position statement by ECTS. Bone. 2017;105:11–17. doi:10.1016/j.bone.2017.08.003
   PubMed Web of Science ®Google Scholar
• Ford J, Cummins E, Sharma P, et al. Systematic review of the clinical effectiveness and cost-effectiveness, and economic evaluation, of denosumab for the treatment of bone metastases from solid tumours. Health Technol Assess. 2013;17(29):1–386. doi:10.3310/hta17290
   PubMed Web of Science ®Google Scholar
• Chen H, Chen W, Yuan F, et al. Pharmacokinetics, pharmacodynamics, safety and immunogenicity of CMAB807, a new denosumab biosimilar, in healthy Chinese subjects. Front Pharmacol. 2022;13:821944. doi:10.3389/fphar.2022.821944
   PubMed Web of Science ®Google Scholar