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Skeletal Manifestations of Treatment of Breast Cancer

  • Osteoporosis and Cancer (P Taxel, Section Editor)
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Abstract

Breast cancer and osteoporosis are common diagnoses in women. Breast cancer survival has improved due to earlier detection and improved treatments. As most breast cancers are estrogen receptor positive, treatment is often aimed at altering the hormonal environment. Both pre and postmenopausal women undergoing these therapies are at risk for bone loss. The patient’s health care team ought to have an awareness of the potential for breast cancer treatments to accelerate bone loss. Women with early stage breast cancer are treated with curative intent and, therefore, maintaining bone health is important and is part of the survivorship care to ensure an optimal quality of life.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. US National Institutes of Health. Surveillance Epidemiology and End Results Cancer Statistics Review: lifetime risk. Available at: http://seer.cancer.gov/csr/1975_2009_pops09/ Lifetime Risk. Accessed July 29, 2013.

  2. Brewster AM, Hortobagyi GN, Broglio KR, Kau SW, Santa-Maria CA, Arun B, et al. Residual risk of breast cancer recurrence 5 years after adjuvant therapy. J Natl Cancer Res. 2008;100:1179–83.

    Google Scholar 

  3. Center for Disease Control FastStats. Osteoporosis. http://www.cdc.gov/nchs/fastats/osteoporosis.htm. Accessed Aug 26 2013.

  4. Nordin C. Screening for osteoporosis: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med. 2011;155:276–7.

    Article  PubMed  Google Scholar 

  5. Ribot C, Pouilles J, Bonneu M, Tremollieres F. Assessment of the risk of post-menopausal osteoporosis using clinical factors. Clin Endocrinol. 1992;36(3):225–8.

    Article  CAS  Google Scholar 

  6. Cauley JA, Robbins J, Chen Z, Cummings SR, Jackson RD, LaCroix AZ, et al. Effects of estrogen plus progestin on risk of fracture and bone mineral density: the women’s health initiative randomized trial. JAMA. 2003;290(13):1729–38.

    Article  PubMed  CAS  Google Scholar 

  7. Tamimi RM, Byrne C, Colditz GA, Hankinson SE. Endogenous hormone levels, mammographic density, and subsequent risk of breast cancer in post-menopausal women. J Natl Cancer Inst. 2007;99:1178–87.

    Google Scholar 

  8. Kerlikowske K, Cook AJ, Buist DS, Cummings SR, Vachon C, Vacek P, et al. Breast cancer risk by breast density, menopause, and postmenopausal hormone therapy use. J Clin Oncol. 2010;28(24):3830–7.

    Article  PubMed  Google Scholar 

  9. American Cancer Society. Breast cancer facts & figures 2011–2012. Atlanta: American Cancer Society; 2011.

    Google Scholar 

  10. Zhang Y, Kiel DP, Kreger BE, Cupples LA, Ellison RC, Dorgan JF, et al. Bone mass and the risk of breast cancer among postmenopausal women. N Engl J Med. 1997;336:611–7.

    Google Scholar 

  11. Qu X, Zhang X, Qin A, Liu G, Zhai Z, Hao Y, et al. Bone mineral density and risk of breast cancer in postmenopausal women. Breast Cancer Res Treat. 2013;138:261–71.

    Google Scholar 

  12. Hofbauer LC, Schoppet MS. Clinical implications of the Osteoprotegerin/RANKL/RANK system for bone and vascular diseases. JAMA. 2004;292:490–5.

    Article  PubMed  CAS  Google Scholar 

  13. Manolagas SC, Kousteni S, Jilka RL. Sex steroids and bone. Recent Prog Horm Res. 2002;57:385–409.

    Google Scholar 

  14. Michaud LB, Goodin S. Cancer-treatment-induced bone loss, parts 1 and 2. Am J Health Syst Pharm. 2006;63:419–30, 534–46.

    Google Scholar 

  15. Violet JA, Harmer C. Breast cancer: improving outcome following adjuvant radiotherapy. Br J Radiol. 2004;77:811–20.

    Google Scholar 

  16. Pierce SM, Recht A, Lingos TI, Abner A, Vicini F, Silver B, et al. Long term radiation complications following conservative surgery and radiation therapy in patients with early stage breast cancer. Int J Radiat Oncol Biol Phys. 1992;23:915–23.

    Google Scholar 

  17. • Bellon JR, Harris EE, Arthur DW, Bailey L, Carey L, Goyal S, et al. American College of Radiology Appropriateness Criteria conservative surgery and radiation—stage I and II breast carcinoma: expert panel on radiation oncology: breast. Breast J. 2011;17:448–55. This article discusses the effects of breast cancer radiation treatment and its effects on skeletal health.

  18. Smith GL, Xu Y, Buchholz TA, Giordano SH, Jiang J, Shih YC, et al. Association between treatment with brachytherapy vs whole-breast irradiation and subsequent mastectomy, complications, and survival among older women with invasive breast cancer. JAMA. 2012;307:1827–37.

    Google Scholar 

  19. Wang TM, Shih C. Study of histomorphometric changes of the mandibular condyles in neonatal and juvenile rats after administration of cyclophosphamide. Acta Anat. 1986;127:93–9.

    Google Scholar 

  20. Wheeler DL, Vander Griend RA, Wronski TJ, Miller GJ, Keith EE, Graves JE. The short- and long-term effects of methotrexate on the rat skeleton. Bone. 1995;16:215–21.

    Google Scholar 

  21. Bines J, Oleske DM, Cobleigh MA. Ovarian function in pre-menopausal women treated with adjuvant chemotherapy for breast cancer. J Clin Oncol. 1996;14:1718–29.

    PubMed  CAS  Google Scholar 

  22. Vehmanen L, Saarto T, Elomaa I, Makela P, Valimaki M, Blomqvist C. Long-term impact of chemotherapy-induced ovarian failure on bone mineral density (BMD) in premenopausal breast cancer patients. The effect of adjuvant clodronate treatment. Eur J Cancer. 2001;37:2372–8.

    Article  Google Scholar 

  23. Partridge AH, Burstein HF, Winer EP. Side effects of chemotherapy and combined chemohormonal therapy in women with early-stage breast cancer. J Nat Cancer Res Monogr. 2001;30:135–42.

    Article  Google Scholar 

  24. 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;19:3306–11.

    PubMed  CAS  Google Scholar 

  25. Fuleihan GH, Salamoun M, Mourad YA, et al. Pamidronate in the prevention of chemotherapy-induced bone loss in premenopausal women with breast cancer: a randomized controlled trial. J Clin Endocrinol Metab. 2005;90:3209–14.

    Article  Google Scholar 

  26. Body J-J. Increased fracture rate in women with breast cancer: a review of the hidden risk. BMC Cancer. 2011;11:384–92.

    Article  PubMed  Google Scholar 

  27. Lipton A, Smith MR, Ellis GK, Goessl C. Treatment-induced bone loss and fractures in cancer patients undergoing hormone ablation therapy: efficacy and safety of denosumab. Clin Med Insights Oncol. 2012;6:287–99.

    Article  PubMed  CAS  Google Scholar 

  28. Burstein GH, Prestrud AA, Seidenfeld J, Anderson H, Buchholz TA, et al. American Society of Clinical Oncology Clinical Practice Guideline: update on adjuvant endocrine therapy for women with hormone receptor-positive breast cancer. J Clin Oncol. 2010;28(23):3784–96.

    Article  PubMed  Google Scholar 

  29. 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;23:619–29.

    Article  PubMed  CAS  Google Scholar 

  30. Love RR, Barden HS, Mazess RB, Epstein S, Chappell RJ. Effect of tamoxifen on lumbar spine bone mineral density in postmenopausal women after 5 years. Arch Intern Med. 1994;22:2585–8.

    Article  Google Scholar 

  31. 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.

    PubMed  CAS  Google Scholar 

  32. Geisler J, Haynes B, Anker G, Dowsett M, Lonning PE. Influence of letrozole (Femara) and anastrozole (Arimedex) on total body aromatization and plasma estrogen levels in postmenopausal breast cancer patients evaluated in a randomized, crossover-designed study. J Clin Oncol. 2002;20:751–7.

    Google Scholar 

  33. Geisler J, King N, Dowsett M, Ottestad L, Lundgren S, Walton P, et al. Influence of anastrazole (Arimidex), a selective, non-steroidal aromatase inhibitor, on in vivo aromatization and plasma estrogen levels in postmenopausal women with breast cancer. Br J Cancer. 1996;74:1286–91.

    Google Scholar 

  34. Geisler J, Ekse D, Duong NK, Evens DB, Nordbo Y, Aas T, et al. In vivo inhibition of aromatization by exemestane, a novel irreversible aromatase inhibitor, in postmenopausal breast cancer patients. Clin Cancer Res. 1998;4:2089–93.

    PubMed  CAS  Google Scholar 

  35. Eastell R, Adams JE, Coleman RE, Howell A, Hannon RA, Cuzick J, 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;26:1051–7.

    Article  PubMed  CAS  Google Scholar 

  36. • Eastell R, Adams J, Clack G, Howell A, Cuzick J, Mackey J, et al. Long-term effects of anastrozole on bone mineral density: 7-year results from the ATAC trial. Ann Oncol. 2011;22:857–62. This study evaluated the effects of long term anastrazole on bone mineral density and improvement at the lumbar spine following discontinuation of anastrazole.

    Article  PubMed  CAS  Google Scholar 

  37. Geisler J, Lønning PE, Krag LE, Løkkevik E, Risberg T, Hagen AI, et al. Changes in bone and lipid metabolism in postmenopausal women with early breast cancer after terminating 2-year treatment with exemestane: a randomized, placebo-controlled study. Eur J Cancer. 2006;42:2968–75.

    Article  PubMed  CAS  Google Scholar 

  38. Weinstein RS, Jilka RL, Parfitt AM, et al. Inhibition of osteoblastogenesis and promotion of apoptosis of osteoblasts and osteocytes by glucocorticoids: potential mechanisms of the deleterious effects on bone. J Clin Invest. 1998;102:274–82.

    Article  PubMed  CAS  Google Scholar 

  39. Davidge-Pitts CJ. Update on medications with adverse skeletal effects, a concise review for clinicians. Mayo Clin Proc. 2011;86:338–43.

    Article  PubMed  Google Scholar 

  40. Cummings SR, Browner WS, Bauer D, Stone K, Ensrud K, et al. Endogenous hormones and the risk of hip and vertebral fractures among older women. Study of Osteoporotic Fractures Research Group. N Engl J Med. 1998;339:733–8.

    Article  PubMed  CAS  Google Scholar 

  41. Chen Z, Maricic M, Aragaki AK, Mouton C, Arendell L, Lopez AM, 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;20:527–36.

    Article  PubMed  CAS  Google Scholar 

  42. Bliuc D, Nguyen ND, Milch VE, Nguyen TV, Eisman JA, Center JR. Mortality risk associated with low-trauma osteoporotic fracture and subsequent fracture in men and women. JAMA. 2009;301:513–21.

    Article  PubMed  CAS  Google Scholar 

  43. Chen Z. Fracture risk among breast cancer survivors. Arch Intern Med. 2005;165:332–8.

    Article  Google Scholar 

  44. Bruning PF, Pit MJ, de Jong-Bakker M, van den Ende A, Hart A, van Enk A. Bone mineral density after adjuvant chemotherapy for premenopausal breast cancer. Br J Cancer. 1990;61:308–10.

    Article  PubMed  CAS  Google Scholar 

  45. Forbes JF, Cuzick J, Buzdar A, Howell A, Tobias JS, Baum M. Arimidex, Tamoxifen, Alone or in Combination (ATAC) Trialists’ Group, effect of anastrozole and tamoxifen as adjuvant treatment for early-stage breast cancer: 100-month analysis of the ATAC trial. Lancet Oncol. 2008;9:45–53.

    Article  PubMed  Google Scholar 

  46. •• Goss PE, Ingle JN, Pritchard KI, Ellis MJ, Sledge GW, Budd GT, et al. Exemestane versus anastrozole in postmenopausal women with early breast cancer: NCIC CTG MA.27—a randomized controlled phase III trial. J Clin Oncol. 2013;31:1398–404. This study compares the two AIs exemestane and anastrazole and the self-reported new diagnoses of osteoporosis after treatment.

    Article  PubMed  CAS  Google Scholar 

  47. McCloskey EV, Hannon RA, Lakner G, Fraser WD, Clack G, Miyamoto A, et al. Effects of third generation aromatase inhibitors on bone health and other safety parameters: results of an open, randomized, multi-center study of letrozole, exemestane and anastrozole in healthy postmenopausal women. Eur J Cancer. 2007;43:2523–31.

    Article  PubMed  CAS  Google Scholar 

  48. Hillner BE, Ingle JN, Chlebowski RT, et al. American Society of Clinical Oncology 2003 update on the role of bisphosphonates and bone health issues in women with breast cancer. J Clin Oncol. 2003;21:4042–57.

    Article  PubMed  CAS  Google Scholar 

  49. Reid DM, Doughty J, Eastell R, Heys SD, Howell A, McCloskey EV, 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.

    Article  PubMed  CAS  Google Scholar 

  50. Kanis JA, Oden A, Johnell O, Johansson H, De Laet C, Brown J, et al. The use of clinical risk factors enhances the performance of BMD in the prediction of hip and osteoporotic fractures in men and women. Osteoporos Int. 2007;18:1033–46.

    Article  PubMed  CAS  Google Scholar 

  51. Kanis J. FRAX WHO Fracture Risk Assessment Tool. http://www.shef.ac.uk/FRAX. Accessed Sep 1 2013.

  52. Kelley GA, Kelley KS, Tran ZV. Exercise and lumbar spine bone mineral density in postmenopausal women: a meta-analysis of individual patient data. J Gerontol A Biol Sci Med Sci. 2002;57:M599–604.

    Article  PubMed  Google Scholar 

  53. Kelley GA, Kelley KS. Efficacy of resistance exercise on lumbar spine and femoral neck bone mineral density in premenopausal women: a meta-analysis of individual patient data. J Women’s Health. 2004;13:293–300.

    Article  Google Scholar 

  54. Wolff I, Croonenberg JJ, Kemper HC, Kostense PJ, Twisk JW. The effect of exercise training programs on bone mass: a meta-analysis of published controlled trials in pre- and postmenopausal women. Osteoporos Int. 1999;9:1–12.

    Article  PubMed  CAS  Google Scholar 

  55. Kam D, Smulders E, Weerdesteyn V, Smits-Engelsman BC. Exercise interventions to reduce fall-related fractures and their risk factors in individuals with low bone density: a systematic review of randomized controlled trials. Osteoporos Int. 2009;20:2111–25.

    Article  PubMed  Google Scholar 

  56. Kannus P, Sievanen H, Palvanen M, Jarvinen T, Parkkari J. Prevention of falls and consequent injuries in elderly people. Lancet. 2005;366:1885–93.

    Article  PubMed  Google Scholar 

  57. Tinetti ME, Kumar C. The patient who falls: it’s always a trade-off. JAMA. 2010;3:258–66.

    Article  Google Scholar 

  58. Maurel DB, Boisseau N, Benhamou CL, Jaffre C. Alcohol and bone: review of dose effects and mechanisms. Osteoporos Int. 2012;23:1–16.

    Article  PubMed  CAS  Google Scholar 

  59. Kanis JA, Johansson H, Johnell O, Oden A, De Laet C, Eisman JA, et al. Alcohol intake as a risk factor for fracture. Osteoporos Int. 2005;16:737–42.

    Article  PubMed  Google Scholar 

  60. Kanis JA, Johnell O, Oden A, Johansson H, De Laet C, Eisman JA, et al. Smoking and fracture risk: a meta-analysis. Osteoporos Int. 2005;16:155–62.

    Article  PubMed  CAS  Google Scholar 

  61. Reid IR, Mason B, Horne A, Ames R, Reid HE, Bava U, et al. Randomized controlled trial of calcium in healthy older women. Am J Med. 2006;119:777–85.

    Article  PubMed  CAS  Google Scholar 

  62. Tang BMP, Eslick GD, Nowson C, Smith C, Bensoussan A. Use of calcium or calcium in combination with vitamin D supplementation to prevent fractures and bone loss in people aged 50 years and older: a meta-analysis. Lancet. 2007;370:657–66.

    Article  PubMed  CAS  Google Scholar 

  63. Bolland MJ, Barber PA, Doughty RN, Mason B, Horne A, Ames R. Vascular events in healthy older women receiving calcium supplementation: randomized controlled trial. BMJ. 2008;336:262–6.

    Article  PubMed  CAS  Google Scholar 

  64. •• Bolland MJ, Grey A, Gamble GD. Calcium and vitamin D supplements and health outcomes: a re-analysis of the Women’s Health Initiative limited-access dataset. Am J Clin Nutr. 2011;94:1144–9. This study evaluates the cardiovascular risk of calcium supplementation. The optimal vitamin D intake in adult is debated.

    Article  PubMed  CAS  Google Scholar 

  65. Ross AC, Manson JE, Abrams SA, et al. The 2011 report on dietary reference intakes for calcium and vitamin D from the Institute of Medicine: what clinicians need to know. J Clin Endocrinol Metab. 2011;96:53–8.

    Article  PubMed  CAS  Google Scholar 

  66. American Society for Bone and Mineral Research. American Society for Bone and Mineral Research. New recommendations for calcium and vitamin D intake: Institute of Medicine Report includes significant evidence on bone health. http://www.asbmr.org/about/pressreleases/detail.aspx?cid=4a1e3f7d-9193-4c11-a2ba-61edb4c31432. Accessed Aug 26 2013.

  67. Holick MF, Binkley NC, Bischoff-Ferrari HA, Gordon CM, Hanley DA, Heaney RP, et al. Endocrine Society. Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2011;96:1911–30.

    Article  PubMed  CAS  Google Scholar 

  68. Greenspan SL, Brufsky A, Lembersky BC, et al. Risedronate prevents bone loss in breast cancer survivors: a 2-year, randomized, double-blind, placebo-controlled clinical trial. J Clin Oncol. 2008;28:967–75.

    Google Scholar 

  69. Hines SL, Mincey B, Dentchev T, et al. Immediate versus delayed zoledronic acid for prevention of bone loss in postmenopausal women with breast cancer starting letrozole after tamoxifen-N03CC. Breast Cancer Res Treat. 2009;117:603–9.

    Article  PubMed  CAS  Google Scholar 

  70. Llombart A, Frassoldati A, Paija O, et al. Zoledronic acid prevents aromatase inhibitor-associated bone loss in postmenopausal women with early breast cancer receiving adjuvant letrozole: E-ZO-FAST 36-month follow-up (Abstract 213). American Society of Clinical Oncology 2009 Breast Cancer Symposium; San Francisco, CA; 2009.

  71. Eidtmann H, de Boer R, Bundred N, et al. Efficacy of zoledronic acid in postmenopausal women with early breast cancer receiving adjuvant letrozole: 36-month results of the ZO-FAST study. Ann Oncol. 2010;21:2188–94.

    Article  PubMed  CAS  Google Scholar 

  72. Markopoulos C, Tzoracoleftherakis E, Polychronis A, et al. Management of anastrozole-induced bone loss in breast cancer patients with oral risedronate: results from the ARBI prospective clinical trial. Breast Cancer Res. 2010;12:R24.

    Article  PubMed  Google Scholar 

  73. 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;14:6336–42.

    Article  PubMed  CAS  Google Scholar 

  74. Confavreux CB, Fontana A, Guastalla JP, et al. Estrogen-dependent increase in bone turnover and bone loss in postmenopausal women with breast cancer treated with anastrozole. Prevention with bisphosphonates. Bone. 2007;41:346–52.

    Article  PubMed  CAS  Google Scholar 

  75. •• Brufsky AM, Harker WG, Beck JT, Bosserman L, Vogel C, Seidler C, 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;118:1192–201. This study gives us the 5-year data on the effects of zoledronic acid in preserving bone mass in postmenopausal women on an AI.

    Article  PubMed  CAS  Google Scholar 

  76. 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;28:967–75.

    Article  PubMed  Google Scholar 

  77. Van Poznak C, Souter SP. Clinical management of osteoporosis in women with a history of breast carcinoma. Cancer. 2005;104:443–56.

    Article  PubMed  Google Scholar 

  78. Eastell R, Walsh JS, Watts NB, Siris E. Bisphosphonates for postmenopausal osteoporosis. Bone. 2011;49:82–8.

    Article  PubMed  CAS  Google Scholar 

  79. Taxel P, Choksi P, Van Poznak C. The management of osteoporosis in breast cancer survivors. Maturitas. 2012;73:275–9.

    Google Scholar 

  80. Cummings SR, San Martin J, McClung MR, et al. Denosumab for prevention of fractures in postmenopausal women with osteoporosis. N Engl J Med. 2009;361:756–65.

    Article  PubMed  CAS  Google Scholar 

  81. Ellis GK, Bone HJ, Chlebowski R, et al. Randomized trial of denosumab in patients receiving adjuvant aromatase inhibitors for nonmetastatic breast cancer. J Clin Oncol. 2008;26:4875–82.

    Article  PubMed  CAS  Google Scholar 

  82. Shane E, Burr D, Ebeling PR, et al. Atypical subtrochanteric and diaphyseal femoral fractures: report of a task force of the American Society for Bone and Mineral Research. J Bone Miner Res. 2010;25:2267–94.

    Article  PubMed  Google Scholar 

  83. Prolia (denosumab) product information. http://pi.amgen.com/united_states/prolia/prolia_pi.pdf. Accessed Aug 26 2013.

  84. Medication Instructions, Zometa. http://www.pharma.us.novartis.com/product/pi/pdf/Zometa.pdf.

  85. Berry DA, Cronin KA, Plevritis SK, Fryback DG, Clarke L, Zelen M, et al. Effect of screening and adjuvant therapy on mortality from breast cancer. N Engl J Med. 2005;353:1784–92.

    Google Scholar 

  86. National Osteoporosis Foundation. Medicines that May Cause Bone Loss. Available at: http://www.nof.org/articles/6. Accessed Aug 26, 2013.

  87. Snyder CF, Frick KD, Kantsiper ME, Peairs KS, Herbert RJ, Blackford AL, et al. Prevention, screening, and surveillance care for breast cancer survivors compared with controls: changes from 1998 to 2002. J Clin Oncol. 2009;27:1054–61.

    Article  PubMed  Google Scholar 

  88. Earle CC, Burstein HJ, Winer EP, Weeks JC. Quality of non-breast cancer health maintenance among elderly breast cancer survivors. J Clin Oncol. 2003;21:1447–51.

    Article  PubMed  Google Scholar 

  89. Lester JE, Dodwell D, Horsman JM, Mori S, Coleman RE. Current management of treatment-induced bone loss in women with breast cancer treated in the United Kingdom. Br J Cancer. 2006;94:30–5.

    Article  PubMed  CAS  Google Scholar 

  90. Coleman RE, Marshall H, Cameron D, et al. Breast cancer adjuvant therapy with zoledronic acid. N Engl J Med. 2011;365:1396.

    Article  PubMed  CAS  Google Scholar 

  91. Gnant M, Mlineritsch B, Stoeger H, Luschin-Ebengreuth G, Heck D, Menzel C, et al. Adjuvant endocrine therapy plus zoledronic acid in premenopausal women with early-stage breast cancer: 62–month follow-up from the ABCSG-12 randomized trial 631. Lancet Oncol. 2011;12:631–41.

    Google Scholar 

  92. Paterson AH, Anderson SJ, Lembersky BC, et al. Oral clodronate for adjuvant treatment of operable breast cancer (National Surgical Adjuvant Breast and Bowel Project) protocol B-34; a multi-center, placebo-controlled, randomized trial. Lancet Oncol. 2012;13:734–42.

    Article  PubMed  CAS  Google Scholar 

  93. Mobus V, Diel IJ, Elling D, et al. GAIN Study: a phase III trial to compare ETC vs EC-TX and ibandronate vs observation in patients with node-positive primary breast cancer—1st interim efficacy analysis, Abstract S2–S4. CTRC-AACR San Antonio Breast Cancer Symposium; 2011.

  94. Southwest Oncology Group. NCT00127205 S0307 Zoledronate, clodronate, or ibandronate in treating women who have undergone surgery for stage I, stage II, or stage III breast cancer. http://clinicaltrials.gov/ct2/show/NCT00127205?term=NCT00127205&rank=1. Accessed 10/8/2013.

  95. Study of Denosumab as Adjuvant Treatment for Women With High Risk Early Breast Cancer Receiving Neoadjuvant or Adjuvant Therapy (D-CARE) NCT01077154. http://clinicaltrials.gov/ct2/show/NCT01077154?term=NCT01077154.&rank=1. Accessed 10/8/2013.

  96. Efficacy and safety of odanocatinib in postmenopausal women previously treated with oral bisophosphonate NCT01803607. May 2013. http://clinicaltrials.gov/ct2/show/NCT01803607?term=NCT01803607&rank=1. Accessed 10/8/2013.

  97. Vitamin D and Physical Activity on Bone Health NCT01419730. http://clinicaltrials.gov/ct2/show/NCT01419730?term=NCT01419730&rank=1. Accessed 10/8/2013.

  98. Cholecalciferol in Improving Survival in Patients With Newly Diagnosed Cancer With Vitamin D Insufficiency NCT01787409. http://clinicaltrials.gov/ct2/show/NCT01787409?term=NCT01787409.&rank=1. Accessed 10/8/2013.

  99. Braun S, Pantel K, Muller P, Janni W, Hepp F, Kentenich CRM, et al. Cytokeratin-positive cells in the bone marrow and survival of patients with stage I, II, or III breast cancer. N Engl J Med. 2000;342:525–33.

    Article  PubMed  CAS  Google Scholar 

  100. Lucci A, Hall CS, Lodhi AK, Bhattacharyya A, Anderson AE, Xiao L, et al. Circulating tumor cells in non-metastatic breast cancer: a prospective study. Lancet Oncol. 2012;13:688–95.

    Google Scholar 

  101. Wiedswang G, Borgen E, Kåresen R, Qvist H, Janbu J, Kvalheim G, et al. Isolated tumor cells in bone marrow three years after diagnosis in disease-free breast cancer patients predict unfavorable clinical outcome. Clin Cancer Res. 2004;10:5342–8.

    Google Scholar 

  102. Janni W, Vogl FD, Wiedswang G, et al. Persistence of disseminated tumor cells in the bone marrow of breast cancer patients predicts increased risk for relapse—a European pooled analysis. Clin Cancer Res. 2011;17:2967–76.

    Article  PubMed  Google Scholar 

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Acknowledgments

Catherine Van Poznak is supported by the NIDCR grant 5K23DE020197. The authors would like to thank Alonso Molina-Gomez for his help with the Figure on estrogen mechanism.

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Conflict of Interest

P Choksi declares that she has no conflicts of interest.

M Williams declares that she has no conflicts of interest.

PM Clark declares that she has no conflicts of interest.

C Van Poznak declares that she has no conflicts of interest.

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Authors and Affiliations

  1. Division of Metabolism, Endocrinology and Diabetes, Department of Internal Medicine, University of Michigan Health System, 24 Frank Lloyd Wright Drive, Lobby C, Ann Arbor, MI, 48106, USA

    Palak Choksi

  2. Department of Internal Medicine, 3116G Taubman Center, University of Michigan Health System, SPC 5368, Ann Arbor, MI, 48109, USA

    Margaret Williams

  3. University of Michigan Comprehensive Cancer Center, Building 16, Room G036E, 2800 Plymouth Road, Ann Arbor, MI, 48109-2800, USA

    Patricia M. Clark

  4. Division of Hematology and Oncology, Cancer Center, Floor 1, 1500 E Medical Center Dr, SPC 5916, Ann Arbor, MI, 48109, USA

    Catherine Van Poznak

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  1. Palak Choksi
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Choksi, P., Williams, M., Clark, P.M. et al. Skeletal Manifestations of Treatment of Breast Cancer. Curr Osteoporos Rep 11, 319–328 (2013). https://doi.org/10.1007/s11914-013-0179-7

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  • DOI: https://doi.org/10.1007/s11914-013-0179-7

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