Breast cancer is the second leading cause of cancer death among American women. Known risk factors account for only approximately one-third of the 182,000 new cases diagnosed each year in the United States. There is both concern and debate over the contribution of environmental exposures related to lifestyle, occupation, and ambient pollution, particularly in high risk areas such as Long Island, NY and the rest of the northeastern United States. Biomarkers such as carcinogen-DNA adducts can help to explore the role of environmental risk factors for breast cancer by documenting DNA damage from specific carcinogens directly in human tissue. In this pilot study, a fetal of 31 breast tissue samples were analyzed by the P-32-postlabeling method for carcinogen-DNA adducts characteristic of complex mixtures of aromatic compounds (such as polycyclic aromatic hydrocarbons) and tobacco smoke. The samples included tumor and tumor-adjacent tissues from 15 women with breast cancer and normal tissue samples from 4 women undergoing breast reduction, Among the breast canter cases, the mean aromatic/hydrophobic-DNA adduct level in all tissues assayed was 5.3 +/- 2.4 (SD) adducts/10(8) 10(8) nucleotides compared to 2.3 +/- 1.5 among the samples from the noncancer patients. Breast tissue (tumor and/or nontumor) from 30% (5 of 15) of women with breast cancer displayed a pattern of adducts (referred to as a diagonal zone of radioactivity) associated previously, in studies of other tissues, with exposure to tobacco smoke. The 5 positive samples were from current smokers; tissue samples from the 8 nonsmoking eases did not show this characteristic pattern (P < 0.01). While the nature of the study precludes an inference of causality, these results demonstrate the presence in human breast cells of DNA damage characteristic of environmental carcinogens (complex mixtures of polycyclic aromatic hydrocarbons and tobacco smoke) to which women are widely exposed. Although limited, our results indicate that biomarkers such as DNA adducts may be useful in investigating specific environmental exposures that may contribute to breast cancer causation as well as the populations and individuals most affected. If so, they might be helpful in suggesting new strategies for prevention of breast cancer.