Bisphosphonates and primary breast cancer risk: an updated systematic review and meta-analysis involving 963,995 women

References

• Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018. doi:10.3322/caac.21492
   PubMed Web of Science ®Google Scholar
• Ferlay J, Soerjomataram I, Ervik M, et al. GLOBOCAN 2012 V1.1, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet]. Lyon, France: International Agency for Research on Cancer; 2014 Available from: http://globocan.iarc.fr, Accessed January 16, 2018
   Google Scholar
• Rosen CJ. Clinical practice. Postmenopausal osteoporosis. N Engl J Med. 2005;353(6):595–603. doi:10.1056/NEJMcp04380116093468
   PubMed Web of Science ®Google Scholar
• Watts NB, Lewiecki EM, Miller PD, Baim S. National osteoporosis foundation 2008 clinician’s guide to prevention and treatment of osteoporosis and the world health organization Fracture Risk Assessment Tool (FRAX): what they mean to the bone densitometrist and bone technologist. J Clin Densitom. 2008;11(4):473–477. doi:10.1016/j.jocd.2008.04.00318562228
   PubMed Web of Science ®Google Scholar
• Bedard PL, Body JJ, Piccart-Gebhart MJ. Sowing the soil for cure? Results of the ABCSG-12 trial open a new chapter in the evolving adjuvant bisphosphonate story in early breast cancer. J Clin Oncol. 2009;27(25):4043–4046. doi:10.1200/JCO.2008.21.490819652062
   PubMed Web of Science ®Google Scholar
• Green JR. Antitumor effects of bisphosphonates. Cancer. 2003;97(3 Suppl):840–847. doi:10.1002/cncr.1112812548584
   PubMed Web of Science ®Google Scholar
• Wiemer AJ, Hohl RJ, Wiemer DF. The intermediate enzymes of isoprenoid metabolism as anticancer targets. Anticancer Agents Med Chem. 2009;9(5):526–542.19519294
   PubMed Web of Science ®Google Scholar
• Santini D, Vincenzi B, Galluzzo S, et al. Repeated intermittent low-dose therapy with zoledronic acid induces an early, sustained, and long-lasting decrease of peripheral vascular endothelial growth factor levels in cancer patients. Clin Cancer Res. 2007;13(15 Pt 1):4482–4486. doi:10.1158/1078-0432.CCR-07-055117671133
   PubMed Web of Science ®Google Scholar
• Stresing V, Fournier PG, Bellahcene A, et al. Nitrogen-containing bisphosphonates can inhibit angiogenesis in vivo without the involvement of farnesyl pyrophosphate synthase. Bone. 2011;48(2):259–266. doi:10.1016/j.bone.2010.09.03520920623
   PubMed Web of Science ®Google Scholar
• Dieli F, Gebbia N, Poccia F, et al. Induction of gammadelta T-lymphocyte effector functions by bisphosphonate zoledronic acid in cancer patients in vivo. Blood. 2003;102(6):2310–2311. doi:10.1182/blood-2003-05-165512959943
   PubMed Web of Science ®Google Scholar
• Benzaid I, Monkkonen H, Stresing V, et al. High phosphoantigen levels in bisphosphonate-treated human breast tumors promote Vgamma9Vdelta2 T-cell chemotaxis and cytotoxicity in vivo. Cancer Res. 2011;71(13):4562–4572. doi:10.1158/0008-5472.CAN-10-386221646473
   PubMed Web of Science ®Google Scholar
• Winter MC, Holen I, Coleman RE. Exploring the anti-tumour activity of bisphosphonates in early breast cancer. Cancer Treat Rev. 2008;34(5):453–475. doi:10.1016/j.ctrv.2008.02.00418423992
   PubMed Web of Science ®Google Scholar
• Clezardin P. Bisphosphonates’ antitumor activity: an unravelled side of a multifaceted drug class. Bone. 2011;48(1):71–79. doi:10.1016/j.bone.2010.07.01620655399
   PubMed Web of Science ®Google Scholar
• Hue TF, Cummings SR, Cauley JA, et al. Effect of bisphosphonate use on risk of postmenopausal breast cancer: results from the randomized clinical trials of alendronate and zoledronic Acid. JAMA Intern Med. 2014;174(10):1550–1557. doi:10.1001/jamainternmed.2014.363425111880
   PubMed Web of Science ®Google Scholar
• Liu Y, Zhao S, Chen W, et al. Bisphosphonate use and the risk of breast cancer: a meta-analysis of published literature. Clin Breast Cancer. 2012;12(4):276–281. doi:10.1016/j.clbc.2012.04.00322622199
   PubMed Web of Science ®Google Scholar
• Chiang CH, Huang CC, Chan WL, et al. Oral alendronate use and risk of cancer in postmenopausal women with osteoporosis: anationwide study. J Bone Miner Res. 2012;27(9):1951–1958. doi:10.1002/jbmr.164522532232
   PubMed Web of Science ®Google Scholar
• Cardwell CR, Abnet CC, Veal P, Hughes CM, Cantwell MM, Murray LJ. Exposure to oral bisphosphonates and risk of cancer. Int J Cancer. 2012;131(5):E717–E725. doi:10.1002/ijc.2738922161552
   PubMed Web of Science ®Google Scholar
• Fournier A, Mesrine S, Gelot A, et al. Use of bisphosphonates and risk of breast cancer in a French cohort of postmenopausal women. J Clin Oncol. 2017;35(28):3230–3239. doi:10.1200/JCO.2016.71.433728708471
   PubMed Web of Science ®Google Scholar
• Vinogradova Y, Coupland C, Hippisley-Cox J. Exposure to bisphosphonates and risk of common non-gastrointestinal cancers: series of nested case-control studies using two primary-care databases. Br J Cancer. 2013;109(3):795–806. doi:10.1038/bjc.2013.38323868009
   PubMed Web of Science ®Google Scholar
• Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151(4):264–269.19622511
   PubMed Web of Science ®Google Scholar
• Voskuil DW, Monninkhof EM, Elias SG, Vlems FA, van Leeuwen FE. Physical activity and endometrial cancer risk, a systematic review of current evidence. Cancer Epidemiol Biomarkers Prev. 2007;16(4):639–648. doi:10.1158/1055-9965.EPI-06-074217416752
   PubMed Web of Science ®Google Scholar
• Jadad AR, Moore RA, Carroll D, et al. Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials. 1996;17(1):1–12.8721797
   PubMedGoogle Scholar
• Higgins JP, Altman DG, Gotzsche PC, et al. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. Bmj. 2011;343:d5928. doi:10.1136/bmj.d592822008217
   PubMed Web of Science ®Google Scholar
• Vestergaard P, Fischer L, Mele M, Mosekilde L, Christiansen P. Use of bisphosphonates and risk of breast cancer. Calcif Tissue Int. 2011;88(4):255–262. doi:10.1007/s00223-011-9463-721253712
   PubMed Web of Science ®Google Scholar
• Chlebowski RT, Chen Z, Cauley JA, et al. Oral bisphosphonate use and breast cancer incidence in postmenopausal women. J Clin Oncol. 2010;28(22):3582–3590. doi:10.1200/JCO.2010.28.209520567009
   PubMed Web of Science ®Google Scholar
• Sun K, Liu JM, Sun HX, Lu N, Ning G. Bisphosphonate treatment and risk of esophageal cancer: a meta-analysis of observational studies. Osteoporos Int. 2013;24(1):279–286. doi:10.1007/s00198-012-2158-823052941
   PubMed Web of Science ®Google Scholar
• Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539–1558. doi:10.1002/sim.118612111919
   PubMed Web of Science ®Google Scholar
• Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. Bmj. 2003;327(7414):557–560. doi:10.1136/bmj.327.7414.55712958120
   PubMed Web of Science ®Google Scholar
• Greenland S. Quantitative methods in the review of epidemiologic literature. Epidemiol Rev. 1987;9:1–30. doi:10.1093/oxfordjournals.epirev.a0362983678409
   PubMed Web of Science ®Google Scholar
• VanderWeele TJ, Ding P. Sensitivity analysis in observational research: introducing the E-value. Ann Intern Med. 2017;167(4):268–274. doi:10.7326/M16-260728693043
   PubMed Web of Science ®Google Scholar
• Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. Bmj. 1997;315(7109):629–634. doi:10.1136/bmj.315.7109.6299310563
   PubMed Web of Science ®Google Scholar
• Duval S, Tweedie R. Trim and fill: asimple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics. 2000;56(2):455–463.10877304
   PubMed Web of Science ®Google Scholar
• Newcomb PA, Trentham-Dietz A, Hampton JM. Bisphosphonates for osteoporosis treatment are associated with reduced breast cancer risk. Br J Cancer. 2010;102(5):799–802. doi:10.1038/sj.bjc.660555520160722
   PubMed Web of Science ®Google Scholar
• Rennert G, Pinchev M, Rennert HS. Use of bisphosphonates and risk of postmenopausal breast cancer. J Clin Oncol. 2010;28(22):3577–3581. doi:10.1200/JCO.2010.28.111320567021
   PubMed Web of Science ®Google Scholar
• Monsees GM, Malone KE, Tang MT, Newcomb PA, Li CI. Bisphosphonate use after estrogen receptor-positive breast cancer and risk of contralateral breast cancer. J Natl Cancer Inst. 2011;103(23):1752–1760. doi:10.1093/jnci/djr39922021667
   PubMedGoogle Scholar
• Kwan ML, Shi JM, Habel LA, et al. Effectiveness of bisphosphonate use and risk of contralateral breast cancer and recurrence in women with early-stage breast cancer treated with tamoxifen. Breast Cancer Res Treat. 2016;156(2):379–389. doi:10.1007/s10549-016-3763-627002508
   PubMed Web of Science ®Google Scholar
• Korde LA, Doody DR, Hsu L, Porter PL, Malone KE. Bisphosphonate use and risk of recurrence, second primary breast cancer, and breast cancer mortality in a population-based cohort of breast cancer patients. Cancer Epidemiol Biomarkers Prev. 2018;27(2):165–173. doi:10.1158/1055-9965.EPI-17-055629254937
   PubMed Web of Science ®Google Scholar
• Wiseman M. The second world cancer research fund/american institute for cancer research expert report. Food, nutrition, physical activity, and the prevention of cancer: a global perspective. Proc Nutr Soc. 2008;67(3):253–256. doi:10.1017/S002966510800712X18452640
   PubMed Web of Science ®Google Scholar
• Coleman RE, Rathbone E, Brown JE. Management of cancer treatment-induced bone loss. Nat Rev Rheumatol. 2013;9(6):365–374. doi:10.1038/nrrheum.2013.3623507900
   PubMed Web of Science ®Google Scholar
• Ou YJ, Chiu HF, Wong YH, Yang CC, Yang YH. Bisphosphonate use and the risk of breast cancer: a meta-analysis of observational studies. Pharmacoepidemiol Drug Saf. 2017;26(10):1286–1295. doi:10.1002/pds.430228857419
   PubMed Web of Science ®Google Scholar
• Dreyfuss JH. Oral bisphosphonate use associated with a decreased risk of breast cancer. CA Cancer J Clin. 2010;60(6):343–344. doi:10.3322/caac.2009120959402
   PubMed Web of Science ®Google Scholar
• Black DM, Delmas PD, Eastell R, et al. Once-yearly zoledronic acid for treatment of postmenopausal osteoporosis. N Engl J Med. 2007;356(18):1809–1822. doi:10.1056/NEJMoa06731217476007
   PubMed Web of Science ®Google Scholar
• Early Breast Cancer Trialists’ Collaborative G. Adjuvant bisphosphonate treatment in early breast cancer: meta-analyses of individual patient data from randomised trials. Lancet. 2015;386(10001):1353–1361. doi:10.1016/S0140-6736(15)60908-426211824
   PubMed Web of Science ®Google Scholar
• Russell RG, Watts NB, Ebetino FH, Rogers MJ. Mechanisms of action of bisphosphonates: similarities and differences and their potential influence on clinical efficacy. Osteoporos Int. 2008;19(6):733–759. doi:10.1007/s00198-007-0540-818214569
   PubMed Web of Science ®Google Scholar
• Licata AA. Discovery, clinical development, and therapeutic uses of bisphosphonates. Ann Pharmacother. 2005;39(4):668–677. doi:10.1345/aph.1E35715755793
   PubMed Web of Science ®Google Scholar
• Hollick RJ, Reid DM. Role of bisphosphonates in the management of postmenopausal osteoporosis: an update on recent safety anxieties. Menopause Int. 2011;17(2):66–72. doi:10.1258/mi.2011.01101421693503
   PubMedGoogle Scholar
• Reid IR, Cornish J. Epidemiology and pathogenesis of osteonecrosis of the jaw. Nat Rev Rheumatol. 2012;8(2):90–96. doi:10.1038/nrrheum.2011.181
   Web of Science ®Google Scholar
• Andrici J, Tio M, Eslick GD. Meta-analysis: oral bisphosphonates and the risk of oesophageal cancer. Aliment Pharmacol Ther. 2012;36(8):708–716. doi:10.1111/apt.1204122966908
   PubMed Web of Science ®Google Scholar
• Oh YH, Yoon C, Park SM. Bisphosphonate use and gastrointestinal tract cancer risk: meta-analysis of observational studies. World J Gastroenterol. 2012;18(40):5779–5788. doi:10.3748/wjg.v18.i40.577923155320
   PubMed Web of Science ®Google Scholar
• Hermann AP, Abrahamsen B. The bisphosphonates: risks and benefits of long term use. Curr Opin Pharmacol. 2013;13(3):435–439. doi:10.1016/j.coph.2013.02.00223434194
   PubMed Web of Science ®Google Scholar
• Dreyfuss JH. Tamoxifen infrequently used by women at risk for breast cancer. CA Cancer J Clin. 2010;60(4):204–206. doi:10.3322/caac.2008020530798
   PubMed Web of Science ®Google Scholar
• Powles TJ. Extended adjuvant tamoxifen for breast cancer – anew era? Lancet. 2013;381(9869):782–783. doi:10.1016/S0140-6736(12)62038-823219287
   PubMed Web of Science ®Google Scholar
• Davies C, Pan H, Godwin J, et al. Long-term effects of continuing adjuvant tamoxifen to 10 years versus stopping at 5 years after diagnosis of oestrogen receptor-positive breast cancer: ATLAS, a randomised trial. Lancet. 2013;381(9869):805–816. doi:10.1016/S0140-6736(12)61963-123219286
   PubMed Web of Science ®Google Scholar
• Waters EA, Cronin KA, Graubard BI, Han PK, Freedman AN. Prevalence of tamoxifen use for breast cancer chemoprevention among U.S. women. Cancer Epidemiol Biomarkers Prev. 2010;19(2):443–446. doi:10.1158/1055-9965.EPI-09-093020142242
   PubMed Web of Science ®Google Scholar
• Kirk R. Oral bisphosphonate use may protect women from breast cancer. Nat Rev Clin Oncol. 2010;7(9):482. doi:10.1038/nrclinonc.2010.126
   Google Scholar
• Coleman R, Gnant M, Morgan G, Clezardin P. Effects of bone-targeted agents on cancer progression and mortality. J Natl Cancer Inst. 2012;104(14):1059–1067. doi:10.1093/jnci/djs26322752060
   PubMedGoogle Scholar
• Gnant M, Clezardin P. Direct and indirect anticancer activity of bisphosphonates: a brief review of published literature. Cancer Treat Rev. 2012;38(5):407–415. doi:10.1016/j.ctrv.2011.09.00321983264
   PubMed Web of Science ®Google Scholar