Abstract
Purpose
Women with benign breast disease (BBD) have an increased risk of subsequent breast cancer. However, whether conventional breast cancer risk factors influence risk of breast cancer among women with BBD is unclear. In this study, we investigated the associations of lifestyle, menstrual/reproductive, and histological factors with risk of breast cancer among women biopsied for BBD.
Methods
We conducted a case–control study, nested within a cohort of 15,395 women biopsied for BBD at Kaiser Permanente Northwest between 1971 and 2006. Cases were women who developed a subsequent invasive breast cancer during follow-up; controls were individually matched to cases on age at BBD diagnosis. A total of 526 case–control pairs were included in the study. We calculated crude and multivariable OR and 95% CI for the associations between lifestyle, menstrual/reproductive, and histological factors and breast cancer risk using conditional logistic regression.
Results
Compared to premenopausal women, postmenopausal women had reduced risk of subsequent breast cancer (OR 0.60; 95% CI 0.39–0.94), whereas women who ever used hormone replacement therapy (HRT) had increased risk (OR 3.61; 95% CI 1.68–7.75), as did women whose BBD lesion showed atypical hyperplasia (OR 5.56; 95% CI 2.05–15.06). Smoking, BMI, early menarche, multiparity (≥4), history of oophorectomy, and extent of lobular involution were not associated with risk of breast cancer.
Conclusion
This study suggests that use of HRT and having atypical hyperplasia are associated with increased risk of breast cancer among women with BBD, while postmenopausal women with BBD have a reduced risk.
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Change history
11 April 2018
The third category for extent of involution in Table 4 was published incorrectly in the original publication. The correct classification is ≥ 75% and the corrected Table 4 is given in the Correction article.
References
Goldacre MJ, Abisgold JD, Yeates DGR, Vessey MP (2010) Benign breast disease and subsequent breast cancer: English record linkage studies. J Public Health Med 32:565–571. doi:10.1093/pubmed/fdq001
Tice JA, O’Meara ES, Weaver DL, Vachon C, Ballard-Barbash R, Kerlikowske K (2013) Benign breast disease, mammographic breast density, and the risk of breast cancer. J Natl Cancer Inst 105:1043–1049. doi:10.1093/jnci/djt124
Cuzick J, Sestak I, Thorat MA (2015) Impact of preventive therapy on the risk of breast cancer among women with benign breast disease. Breast 24(Supp 2):S51–S55. doi:10.1016/j.breast.2015.07.013
Dupont WD, Page DL (1987) Breast cancer risk associated with proliferative disease, age at first birth, and a family history of breast cancer. Am J Epidemiol 125:769–779. doi:10.1093/oxfordjournals.aje.a114594
Kabat GC, Jones JG, Olson N, Negassa A, Duggan C, Ginsberg M et al (2010) Risk factors for breast cancer in women biopsied for benign breast disease: a nested case-control study. Cancer Epidemiol 34:34–39. doi:10.1016/j.canep.2009.12.005
Thomas DB, Persing JP, Hutchinson WB (1982) Exogenous estrogens and other risk factors for breast cancer in women with benign breast diseases. J Natl Cancer Inst 69:1017–1025. doi:10.1093/jnci/69.5.1017
Byrne C, Connolly JL, Colditz GA, Schnitt SJ (2000) Biopsy confirmed benign breast disease, postmenopausal use of exogenous female hormones, and breast carcinoma risk. Cancer 89:2046–2052. doi:10.1002/1097-0142(20001115)89:10<2046:aid-cncr3>3.0.co;2-f
Horn-Ross P, Canchola AJ, West DW, Stewart SL, Bernstein L, Deapen D et al (2004) Patterns of alcohol consumption and breast cancer risk in the california teachers study cohort. Cancer Epidemiol Biomarkers Prev 13:405
van den Brandt P, Goldbohm RA, van ‘t Veer P (1995) Alcohol and breast cancer: results from the Netherlands cohort study. Am J Epidemiol 141:907–915. doi:10.1093/oxfordjournals.aje.a117357
Milanese TR, Hartmann LC, Sellers TA, Frost MH, Vierkant RA, Maloney SD et al (2006) Age-related lobular involution and risk of breast cancer. J Natl Cancer Inst 98:1600–1607. doi:10.1093/jnci/djj439
Radisky DC, Visscher DW, Frank RD, Vierkant RA, Winham S, Stallings-Mann M et al (2016) Natural history of age-related lobular involution and impact on breast cancer risk. Breast Cancer Res Treat 155:423–430. doi:10.1007/s10549-016-3691-5
Rothman K, Greenland S, Lash T (2008) Modern epidemiology. Lippincott Williams & Wilkins, Philadelphia
Hartmann LC, Sellers TA, Frost MH, Lingle WL, Degnim AC, Ghosh K et al (2005) Benign breast disease and the risk of breast cancer. N Engl J Med 353:229–237. doi:10.1056/NEJMoa044383
Page OL, Anderson TJ (1987) Diagnostic histopathology of the breast. Churchill Livingstone, Edinburgh
Page DL, Rogers LW (1992) Combined histologic and cytologic criteria for the diagnosis of mammary atypical ductal hyperplasia. Hum Pathol 23:1095–1097. doi:10.1016/0046-8177(92)90026-Y
Page DL, Schuyler PA, Dupont WD, Jensen RA, Plummer WD Jr, Simpson JF (2003) Atypical lobular hyperplasia as a unilateral predictor of breast cancer risk: a retrospective cohort study. Lancet 361:125–129. doi:10.1016/S0140-6736(03)12230-1
Collins LC, Baer HJ, Tamimi RM, Connolly JL, Colditz GA, Schnitt SJ (2006) The influence of family history on breast cancer risk in women with biopsy-confirmed benign breast disease. Cancer 107:1240–1247. doi:10.1002/cncr.22136
Zhou W, Xue D, Liu X, Ding Q, Wang S (2011) The influence of family history and histological stratification on breast cancer risk in women with benign breast disease: a meta-analysis. J Cancer Res Clin Oncol 137:1053–1060. doi:10.1007/s00432-011-0979-z
Catsburg C, Miller AB, Rohan TE (2015) Active cigarette smoking and risk of breast cancer. Int J Cancer 136:2204–2209. doi:10.1002/ijc.29266
Dossus L, Boutron-Ruault M, Kaaks R, Gram IT, Vilier A, Fervers B et al (2014) Active and passive cigarette smoking and breast cancer risk: results from the EPIC cohort. Int J Cancer 134:1871–1888. doi:10.1002/ijc.28508
Johnson KC, Miller AB, Collishaw NE, Palmer JR, Hammond SK, Salmon AG et al (2011) Active smoking and secondhand smoke increase breast cancer risk: the report of the Canadian expert panel on tobacco smoke and breast cancer risk (2009). Tob Control 20:e2. doi:10.1136/tc.2010.035931
McPherson K, Steel CM, Dixon JM (2000) Breast cancer- Epidemiology, risk factors, and genetics. BMJ 321:624–628. doi:10.1136/bmj.321.7261.624
Hulka BS, Moorman PG (2008) Reprint of Breast cancer: hormones and other risk factors. Maturitas 61:203–213. doi:10.1016/j.maturitas.2008.11.016
Kyrgiou M, Kalliala I, Markozannes G, Gunter MJ, Paraskevaidis E, Gabra H et al (2017) Adiposity and cancer at major anatomical sites: umbrella review of the literature. BMJ. doi:10.1136/bmj.j477
Degnim AC, Visscher DW, Berman HK, Frost MH, Sellers TA, Vierkant RA et al (2007) Stratification of breast cancer risk in women with atypia: a mayo cohort study. J Clin Oncol 25:2671–2677. doi:10.1200/JCO.2006.09.0217
Webb PM, Byrne C, Schnitt SJ, Connolly JL, Jacobs T, Peiro G et al (2002) Family history of breast cancer, age and benign breast disease. Int J Cancer 100:375–378. doi:10.1002/ijc.10490
Castells X, Domingo L, Corominas JM, Torá-Rocamora I, Quintana MJ, Baré M et al (2015) Breast cancer risk after diagnosis by screening mammography of nonproliferative or proliferative benign breast disease: a study from a population-based screening program. Breast Cancer Res Treat 149:237–244. doi:10.1007/s10549-014-3208-z
Kapil U, Bhadoria AS, Sareen N, Singh P, Dwivedi SN (2014) Reproductive factors and risk of breast cancer: a Review. Indian J Cancer 51:571–576. doi:10.4103/0019-509X.175345
Monninkhof EM, van der Schouw YT, Peeters PHM (1999) Early age at menopause and breast cancer: are leaner women more protected? A prospective analysis of the Dutch DOM cohort. Breast Cancer Res Treat 55:285–291. doi:10.1023/A:1006277207963
Folkerd E, Dowsett M (2013) Sex hormones and breast cancer risk and prognosis. Breast. doi:10.1016/j.breast.2013.07.007
Dupont WD, Page DL (1991) Menopausal estrogen replacement therapy and breast cancer. Arch Intern Med 151:67–72. doi:10.1001/archinte.1991.00400010089011
McDonald JA, Weiss NS, Daling JR, Francis AM, Polissar L (1986) Menopausal estrogen use and the risk of breast cancer. Breast Cancer Res Treat 7:193–199. doi:10.1007/BF01806250
Gambrel RJ, Maier R, Sanders B (1983) Decreased incidence of breast cancer in postmenopausal estrogen-progestogen users. Obstet Gynecol 62:435–443
Collaborative Group on Hormonal Factors in Breast Cancer (1997) Breast cancer and hormone replacement therapy: collaborative reanalysis of data from 51 epidemiological studies of 52 705 women with breast cancer and 108 411 women without breast cancer. Lancet 350:1047–1059. doi:10.1016/S0140-6736(97)08233-0
Chlebowski RT, Anderson GL, Gass M, Lane DS, Aragaki AK, Kuller LH et al (2010) Estrogen plus progestin and breast cancer incidence and mortality in postmenopausal women. J Am Med Assoc 304:1684–1692. doi:10.1001/jama.2010.1500
Thorbjarnardottir T, Olafsdottir EJ, Valdimarsdottir UA, Olafsson O, Tryggvadottir L (2014) Oral contraceptives, hormone replacement therapy and breast cancer risk: a cohort study of 16 928 women 48 years and older. Acta Oncol 53:752–758. doi:10.3109/0284186X.2013.878471
Jones ME, Schoemaker MJ, Wright L, McFadden E, Griffin J, Thomas D et al (2016) Menopausal hormone therapy and breast cancer: what is the true size of the increased risk. Br J Cancer 115:607–615. doi:10.1038/bjc.2016.231
Coombs NJ, Taylor R, Wilcken N, Fiorica J, Boyages J (2005) Hormone replacement therapy and breast cancer risk in California. Breast J 11:410–415. doi:10.1111/j.1075-122X.2005.00132.x
Nandi S, Guzman RC, Yang J (1995) Hormones and mammary carcinogenesis in mice, rats, and humans: a unifying hypothesis. Proc Natl Acad Sci USA 92:3650–3657. doi:10.1073/pnas.92.9.3650
Pike MC, Spicer D, Dahmoush L, Press MF (1993) Estrogens, progestogens, normal breast cell proliferation, and breast cancer risk. Epidemiol Rev 15:17–35. doi:10.1093/oxfordjournals.epirev.a036102
Russo J, Fernandez SV, Russo PA, Fernbaugh R, Sheriff FS, Lareef HM et al (2006) 17-Beta-estradiol induces transformation and tumorigenesis in human breast epithelial cells. FASEB J 20:1622–1634. doi:10.1096/fj.05-5399com
Kabat GC, Jones JG, Olson N, Negassa A, Duggan C, Ginsberg M et al (2010) A multi-center prospective cohort study of benign breast disease and risk of subsequent breast cancer. Cancer Causes Control 21:821–828. doi:10.1007/s10552-010-9508-7
Dyrstad SW, Yan Y, Fowler AM, Colditz GA (2015) Breast cancer risk associated with benign breast disease: systematic review and meta-analysis. Breast Cancer Res Treat 149:569–575. doi:10.1007/s10549-014-3254-6
Hartmann LC, Degnim AC, Santen RJ, Dupont WD, Ghosh K (2015) Atypical hyperplasia of the breast -risk assessment and management options. N Engl J Med 372:78–89. doi:10.1056/NEJMsr1407164
Ma X, Salunga R, Tuggle JT, Gaudet J, Enright E, McQuary P et al (2003) Gene expression profiles of human breast cancer progression. Proc Natl Acad Sci USA 100:5974–5979. doi:10.1073/pnas.0931261100
Ghosh K, Vachon CM, Pankratz VS, Vierkant RA, Anderson SS, Brandt KR et al (2010) Independent association of lobular involution and mammographic breast density with breast cancer risk. J Natl Cancer Inst 102:1716–1723. doi:10.1093/jnci/djq414
Stevens VJ, Wagner EL, Rossner J, Craddick S, Greenlick MR (1988) Validity and usefulness of medical chart weights in the long-term evaluation of weight loss programs. Addict Behav 13:171–175. doi:10.1016/0306-4603(88)90007-X
West CN, Geiger AM, Greene SM, Harris EL, Liu IA, Barton MB et al (2005) Race and ethnicity: comparing medical records to self-reports. J Natl Cancer Inst Monogr 2005:72–74. doi:10.1093/jncimonographs/lgi041
Acknowledgements
This work was supported by NIH/NCI Grant R01CA142942 (to TE Rohan). Drs. Arthur and Rohan are supported by the Breast Cancer Research Foundation. We would particularly like to thank the following staff at the Kaiser Center for Health Research who worked on this project for several years: Nicole Bennett, Kristine Bennett, Donna Gleason, Kathy Pearson, Tracy Dodge, Stacy Harsh, and Kevin Winn.
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Arthur, R., Wang, Y., Ye, K. et al. Association between lifestyle, menstrual/reproductive history, and histological factors and risk of breast cancer in women biopsied for benign breast disease. Breast Cancer Res Treat 165, 623–631 (2017). https://doi.org/10.1007/s10549-017-4347-9
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DOI: https://doi.org/10.1007/s10549-017-4347-9