Environmental exposures during windows of susceptibility for breast cancer: A framework for prevention research

Mary Beth Terry, Karin B. Michels, Julia Green Brody, Celia Byrne, Shiuan Chen, D. Joseph Jerry, Kristen M.C. Malecki, Mary Beth Martin, Rachel L. Miller, Susan L. Neuhausen, Kami Silk, Amy Trentham-Dietz*, Jasmine McDonald, Sabine Oskar, Julia Knight, Rosario Toro-Campos, Xiaomei Cai, Camella J. Rising, Dasha Afanaseva, Michaela Devyn MullisMary Pat Berry, Jennifer Bird, Christopher Bradfield, Ronald Gangnon, Michael Gould, John Hampton, Sara Lindberg, Sarah Luongo, Betsy Rolland, James Shull, Mia Gaudet, Mark Thornquist, Mark D. Aupperlee, Sandra Z. Haslam, Reyhane Hoshyar, Anastasia Kariagina, Juliana R. Lopes, Karen J. Miller, Olena Morozova, Cathy J. Newkirk, Richard C. Schwartz, Brandon Thomas, Daniel Totzkay, Fang Xie, Kami J. Silk, Frank M. Biro, Cecily S. Fassler, Courtney M. Giannini, Susan Pinney, Melissa A. Troester, Kimberly Burke, Julie Herbstman, Rebecca Kehm, Logthar Lilge, Frederica Perera, Debeshish Sahay, Parisa Tehranifar, Desiree Walker, Nur Zeinomar, Milagros De Hoz, Peggy Shepard, Alexandra Binder, Vincent Bessonneau, Vanessa De La Rosa, Jennifer Ohayon, Ruthann Rudel, Camila Corvalan, Ana Pereira, Julia Pereira, Jose Russo, Su Yanrong, John Shepherd, Lucile Adams-Campbell, Chiranjeev Dash, Bassem Haddad, Rhonda Hamilton, Brenda Richardson, Hristina Denic-Roberts, Gregory Chang, Yuan Chun Ding, Noriko Kanaya, Michele Rakoff, Kohei Saeki, Mayra Serrano, Peggy Reynolds, Karen Dunphy, Joseph Jerry, Anna Symington, Laura Vandenberg, Sallie Schneider, Swann Arp Adams, Heather M. Brandt, Daniela Friedman, Jamie R. Lead, Gary Kreps, Kevin Wright, Amelia Burke-Garcia, Carla Fisher

*Corresponding author for this work

Research output: Contribution to journalReview articlepeer-review

139 Scopus citations


Background: The long time from exposure to potentially harmful chemicals until breast cancer occurrence poses challenges for designing etiologic studies and for implementing successful prevention programs. Growing evidence from animal and human studies indicates that distinct time periods of heightened susceptibility to endocrine disruptors exist throughout the life course. The influence of environmental chemicals on breast cancer risk may be greater during several windows of susceptibility (WOS) in a woman's life, including prenatal development, puberty, pregnancy, and the menopausal transition. These time windows are considered as specific periods of susceptibility for breast cancer because significant structural and functional changes occur in the mammary gland, as well as alterations in the mammary micro-environment and hormone signaling that may influence risk. Breast cancer research focused on these breast cancer WOS will accelerate understanding of disease etiology and prevention. Main text: Despite the plausible heightened mechanistic influences of environmental chemicals on breast cancer risk during time periods of change in the mammary gland's structure and function, most human studies of environmental chemicals are not focused on specific WOS. This article reviews studies conducted over the past few decades that have specifically addressed the effect of environmental chemicals and metals on breast cancer risk during at least one of these WOS. In addition to summarizing the broader evidence-base specific to WOS, we include discussion of the NIH-funded Breast Cancer and the Environment Research Program (BCERP) which included population-based and basic science research focused on specific WOS to evaluate associations between breast cancer risk and particular classes of endocrine-disrupting chemicals - including polycyclic aromatic hydrocarbons, perfluorinated compounds, polybrominated diphenyl ethers, and phenols - and metals. We outline ways in which ongoing transdisciplinary BCERP projects incorporate animal research and human epidemiologic studies in close partnership with community organizations and communication scientists to identify research priorities and effectively translate evidence-based findings to the public and policy makers. Conclusions: An integrative model of breast cancer research is needed to determine the impact and mechanisms of action of endocrine disruptors at different WOS. By focusing on environmental chemical exposure during specific WOS, scientists and their community partners may identify when prevention efforts are likely to be most effective.

Original languageEnglish
Article number96
JournalBreast Cancer Research
Issue number1
StatePublished - 20 Aug 2019
Externally publishedYes


  • Breast neoplasms
  • Environment
  • Menopause
  • Pregnancy
  • Puberty


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