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  • Research Article
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Human breast biomonitoring and environmental chemicals: use of breast tissues and fluids in breast cancer etiologic research

Abstract

Extensive research indicates that the etiology of breast cancer is complex and multifactorial and may include environmental risk factors. Breast cancer etiology and exposure to xenobiotic compounds, diet, electromagnetic fields, and lifestyle have been the subject of numerous scientific inquiries, but research has yielded inconsistent results. Biomonitoring has been used to explore associations between breast cancer and levels of environmental chemicals in the breast. Research using breast tissues and fluids to cast light on the etiology of breast cancer is, for the most part, predicated on the assumption that the tissue or fluid samples either contain measurable traces of the environmental agent(s) associated with the cancer or that they retain biological changes that are biomarkers of such exposure or precursors of carcinogenic effect. In this paper, we review breast cancer etiology research utilizing breast biomonitoring. We first provide a brief synopsis of the current state of understanding of associations between exposure to environmental chemicals and breast cancer etiology. We then describe the published breast cancer research on tissues and fluids, which have been used for biomonitoring, specifically human milk and its components, malignant and benign breast tissue, nipple aspirate fluid (NAF) and breast cyst fluid. We conclude with a discussion on recommendations for biomonitoring of breast tissues and fluids in future breast cancer etiology research. Both human milk and NAF fluids, and the cells contained therein, hold promise for future biomonitoring research into breast cancer etiology, but must be conducted with carefully delineated hypotheses and a scientifically supportable epidemiological approach.

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Abbreviations

PhIP:

2-Amino-1-methyl-6-phenylimidazo[4,5-b]pyridine

B[a]P:

Benzo[a]pyrene

DDD:

1,1-Dichloro-2,2-bis(p-chlorophenyl)ethane

DDE:

1,1-Dichloro-2,2- bis(p-chlorophenyl)ethylene

DDT:

dichloro-diphenyl-trichloroethane

ER:

estrogen receptor

HCB:

hexachlorobenzene

HCH:

hexachorocyclohexane

8-OHdG:

8-hydroxy-2′-deoxyguanosine

NAF:

Nipple aspirate fluid

PCBs:

Polychlorinated biphenyls

PAHs:

polycyclic aromatic hydrocarbons

PR:

progesterone receptor

References

  • Adami H.-O., Signorello L.B., and Trichopolous D. Towards an understanding of breast cancer etiology. Cancer Biol 1998: 8: 255–262.

    Article  CAS  Google Scholar 

  • Archibeque-Engle S.L., Tessari J.D., Winn D.T., Keefe T.J., Nett T.M., and Zheng T. Comparison of organochlorine pesticide and polychlorinated biphenyl residues in human breast adipose tissue and serum. J Toxicol Environ Health 1997: 52: 285–293.

    Article  PubMed  Google Scholar 

  • Aronson K.J., Miller A.B., Woolcott C.G., Sterns E.E., McCready D.R., Lickley L.A., Fish E.B., Hiraki G.Y., Holloway C., Ross T., Hanna W.M., SenGupta S.K., and Weber J.-P. Breast adipose tissue concentrations of polychlorinated biphenyls and other organochlorines and breast cancer risk. Cancer Epidem Bio Prev 2000: 9: 55–63.

    CAS  Google Scholar 

  • Bagga D., Anders K.H., Wang H.-J., Roberts E., and Glaspy J.A. Organochlorine pesticide content of breast adipose tissue from women with breast cancer and control subjects. J Natl Canc Inst 2000: 92: 750–753.

    Article  CAS  Google Scholar 

  • Bates M.N., Selevan S.G., Ellerbee S.M., and Gartner L.M. Reporting needs for studies of environmental chemicals in human milk. J Toxicol Environ Health Part A 2002: 65: 1867–1880.

    Article  CAS  Google Scholar 

  • Biggs P.J., Warren W., Venitt S., and Stratton M.R. Does a genotoxic carcinogen contribute to human breast cancer? The value of mutational spectra in unravelling the aetiology of cancer. Mutagenesis 1993: 8: 275–283.

    Article  CAS  PubMed  Google Scholar 

  • Birnbaum L.S., and Fenton S.E. Cancer and developmental exposure to endocrine disruptors. Environ Health Perspect 2003: 111: 389–394.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blackwood A., Wolff M., Rundle A., Estabrook A., Schnabel F., Mooney L.A., Rivera M., Channing K.M., and Perera F.P. Organochlorine compounds (DDE and PCB) in plasma and breast cyst fluid of women with benign breast disease. Cancer Epidemiol Biomarkers Prev 1998: 7: 579–583.

    CAS  PubMed  Google Scholar 

  • Brinton L.A., Potischman N.A., Swanson C.A., Schoenberg J.B., Coates R.J., Gammon M.D., Malone K.E., Stanford J.L., and Daling J.R. Breastfeeding and breast cancer risk. Cancer Causes Control 1995: 6: 199–208.

    Article  CAS  PubMed  Google Scholar 

  • Brody J.G., and Rudel R.A. Environmental pollutants and breast cancer. Environ Health Perspect 2003: 111: 1007–1019.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bucalossi P., and Veronesi U. Some observations on cancer of the breast in mothers and daughters. Br J Cancer 1957: 11: 337–347.

    Article  CAS  PubMed  Google Scholar 

  • State of California. California Senate Bill SB 689. April 22, 2003. http://info.sen.ca.gov/pub/bill/sen/sb_0651-0700/sb_689_bill_20030422_amended_sen.pdf, 2003.

  • Carmichael P.L., Stone E.M., Grover P.L., Gusterson B.A., and Phillips D.H. Metabolic activation and DNA binding of food mutagens and other environmental carcinogens in human mammary epithelial cells. Carcinogenesis 1996: 17: 1769–1772.

    Article  CAS  PubMed  Google Scholar 

  • Charles M.J., Schell M.J., Willman E., Gross H.B., Lin Y., Sonnenberg S., and Graham M.L. Organochlorines and 8-hydroxy-2′-deoxyguanosine (8-OHdG) in cancerous and noncancerous breast tissue: Do the data support the hypothesis that oxidative DNA damage caused by organochlorines affects breast cancer? Arch Environ Contam Toxicol 2001: 41: 386–395.

    Article  CAS  PubMed  Google Scholar 

  • Clark P. Ductal Lavage: A New Look Inside The Breast. Cancernews, Available: www.cancernews.com/category.asp?cat=3&aid=223[accessed 4 March 2006].

  • Collaborative Group on Hormonal Factors in Breast Cancer. Breast cancer and breastfeeding: collaborative reanalysis of individual data from 47 epidemiological studies in 30 countries, including 50302 women with breast cancer and 96973 women without the disease. Lancet 2002: 360: 187–195.

    Article  Google Scholar 

  • Darbre P.D., Aljarrah A., Miller W.R., Coldham N.G., Sauer M.J., and Pope G.S. Concentrations of parabens in human breast tumors. J Appl Toxicol 2004: 24: 5–13.

    Article  CAS  PubMed  Google Scholar 

  • Davis M. Review of the evidence for an association between infant feeding and childhood cancer. Int J Cancer Suppl 1998: 11: 29–33.

    Article  CAS  PubMed  Google Scholar 

  • DeBruin L.S., and Josephy P.D. Perspectives on the chemical etiology of breast cancer. Environ Health Perspect 2002: 110 (Supp 1): 119–128.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DeBruin L.S., Pawliszyn J.B., and Josephy P.D. Detection of monocyclic aromatic amines, possible mammary carcinogens, in human milk. Chem Res Toxicol 1999: 12: 78–82.

    Article  CAS  PubMed  Google Scholar 

  • DeBruin L.S., Martos P.A., and Josephy P.D. Detection of PhIP (2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine) in the milk of healthy women. Chem Res Toxicol 2001: 14: 1523–1528.

    Article  CAS  PubMed  Google Scholar 

  • De Stefani E., Ronco A., Mendilaharsu M., Guidobono M., and Deneo-Pellegrini H. Meat intake, heterocyclic amines, and risk of breast cancer: a case–control study in Uruguay. Cancer Epidemiol Biomarkers Prev 1997: 6: 573–581.

    CAS  PubMed  Google Scholar 

  • Dos Santos Silva I., Mangtani P., McCormack V., Bhakta D., Sevak L., and McMichael A.J. Lifelong vegetarianism and risk of breast cancer: a population-based case–control study among South Asian migrant women living in England. Int J Cancer 2002: 99: 238–244.

    Article  CAS  PubMed  Google Scholar 

  • Edwards B.K., Brown M.L., Wingo P.A., Howe H.L., Ward E., Ries L.A.G., Schrag D., Jamison P.M., Jemal A., Wu X.C., Friedman C., Harlan L., Warren J., Anderson R.N., and Pickle L.W. Annual Report to the Nation on the Status of Cancer, 1975–2002, Featuring Population-Based Trends in Cancer Treatment. J Natl Cancer Inst 2005: 97: 1407–1427.

    Article  PubMed  Google Scholar 

  • Ekbom A., Hsieh C.-C., Trichopoulos D., Yen Y.-Y., Petridou E., and Adami H.-O. Breast-feeding and breast cancer in the offspring. Br J Cancer 1993: 67: 842–845.

    Article  CAS  PubMed  Google Scholar 

  • El-Bayoumy K. Environmental carcinogens that may be involved in human breast cancer etiology. Chem Res Toxicol 1992: 5: 585–590.

    Article  CAS  PubMed  Google Scholar 

  • Falck F., Ricci A., Wolff M.S., Godbold J., and Deckers P. Pesticides and polychlorinated biphenyl residues in human breast lipid and their relation to breast cancer. Arch Env Health 1992: 47: 143–146.

    Google Scholar 

  • Felton J.S., Knize M.G., Salmon C.P., Malfatti M.A., and Kulp K.S. Human exposure to heterocyclic amine food mutagens/carcinogens: relevance to breast cancer. Environ Mol Mutagen 2002: 39: 112–118.

    Article  CAS  PubMed  Google Scholar 

  • Fraumeni J.F., and Miller R.W. Breast cancer from breast-feeding. Lancet 1971: 2: 1196–1197.

    Article  PubMed  Google Scholar 

  • Freudenheim J.L., Marshall J.R., Graham S., Laughlin R., Vena J.E., Bandera E., Muti P., Swanson M., and Nemoto T. Exposure to breastmilk in infancy and the risk of breast cancer. Epidemiol 1994: 5: 324–331.

    Article  CAS  Google Scholar 

  • Gorlewska-Roberts K., Green B., Fares M., Ambrosone C.B., and Kadlubar F.F. Carcinogen-DNA adducts in human breast epithelial cells. Environ Mol Mutagen 2002: 39: 184–192.

    Article  CAS  PubMed  Google Scholar 

  • Güttes S., Failing K., Neumann J., Kleinstein J., Georgii S., and Brunn H. Chororganic pesticides and polychlorinated biphenyls in breast tissue of women with benign and malignant breast disease. Arch Environ Contam Toxicol 1998: 35: 140–147.

    Article  PubMed  Google Scholar 

  • Henderson B.E., and Fiegelson H.S. Hormonal carcinogenesis. Carcinogenesis 2000: 21: 427–433.

    Article  CAS  PubMed  Google Scholar 

  • Henderson B.E., Powell D., Rosario I., Keys C., Hanisch R., Young M., Casagrande J., Gerkins V., and Pike M.C. An epidemiologic study of breast cancer. J Natl Cancer Inst 1974: 53: 609–614.

    Article  CAS  PubMed  Google Scholar 

  • Hindle W.H. Hormone alterations in breast cancer: examining the hypotheses. Medscape Womens Health eJournal 1999: 4 (1): 4.

    CAS  Google Scholar 

  • Hu Y.F., Russo I.H., Zalipsky U., Lynch H.T., and Russo J. Environmental chemical carcinogens induce transformation of breast epithelial cells from women with familial history of breast cancer. In Vitro Cell Dev Biol Anim 1997: 33: 495–498.

    Article  CAS  PubMed  Google Scholar 

  • Jeffy B.D., Chirnomas R.B., and Romagnolo D.F. Epigenetics of breast cancer: polycyclic aromatic hydrocarbons as risk factors. Environ Mol Mutagen 2002: 39: 235–244.

    Article  CAS  PubMed  Google Scholar 

  • Jensen A.A., and Slorach S.A., (Eds.) Chemical Contaminants in Human Milk. CRC Press, Boca Raton, FL, 1991.

    Google Scholar 

  • Jernström H., Lubinski J., Lynch H.T., Ghadirian P., Neuhausen S., Isaacs C., Weber B.L., Horsman D., Rosen B., Foulkes W.D., Friedman E., Gershoni-Baruch R., Ainsworth P., Daly M., Garber J., Olsson H., Sun P., and Narod S.A. Breast-feeding and the Risk of Breast Cancer in BRCA1 and BRCA2 Mutation Carriers. J Natl Cancer Inst 2004: 96: 1094–1098.

    Article  PubMed  CAS  Google Scholar 

  • Johnson K.C. Accumulating evidence on passive and active smoking and breast cancer risk. Int J Cancer 2005: 117: 619–628.

    Article  CAS  PubMed  Google Scholar 

  • Kelsey J.L., Gammon M.D., and John E.M. Reproductive and other factors and links to breast cancer. Epidemiol Rev 1993: 15: 36–47.

    Article  CAS  PubMed  Google Scholar 

  • Key T.J., Fraser G.E., Thorogood M., Appleby P.N., Beral V., Reeves G., Burr M.L., Chang-Claude J., Frentzel-Beyme R., Kuzma J.W., Mann J., and McPherson K. Mortality in vegetarians and nonvegetarians: detailed findings from a collaborative analysis of 5 prospective studies. Am J Clin Nutr 1999: 70 (Suppl): 516S–524S.

    Article  CAS  PubMed  Google Scholar 

  • King B.L., Love S.M., Rochman S., and Kim J.A. The Fourth International Symposium on the Intraductal Approach to Breast Cancer, Santa Barbara, California, 10–13 March 2005. Breast Cancer Res 2005: 7: 198–204.

    Article  PubMed  PubMed Central  Google Scholar 

  • Klein P., Glaser E., Grogan L., Keane M., Lipkowitz S., Soballe P., Brooks L., Jenkins J., Steinberg S.M., DeMarini D.M., and Kirsch I. Biomarker assays in nipple aspirate fluid. Breast J 2001: 7: 378–387.

    Article  CAS  PubMed  Google Scholar 

  • Klein P.M., and Lawrence J.A. Lavage and nipple aspiration of breast ductal fluids: a source of biomarkers for environmental mutagenesis. Environ Mol Mutagen 2002: 39: 127–133.

    Article  CAS  PubMed  Google Scholar 

  • Kreuzer P.E., Csanády G.A., Baur C., Kessler W., Päpke O., Greim H., and Filser J.G. TCDD and congeners in infants. A toxicokinetic model of human lifetime body burden by TCDD with as special emphasis on its uptake by nutrition. Arch Toxicol 1997: 71: 383–400.

    Article  CAS  PubMed  Google Scholar 

  • Labrèche F.P., and Goldberg M.S. Exposure to organic solvents and breast cancer in women: a hypothesis. Am J Ind Med 1997: 32: 1–14.

    Article  PubMed  Google Scholar 

  • Laden F., and Hunter D.J. Environmental risk factors and female breast cancer. Annu Rev Public Health 1998: 19: 101–123.

    Article  CAS  PubMed  Google Scholar 

  • Laden F., Collman G., Iwamoto K., Alberg A.J., Berkowitz G.S., Freudenheim J.L., Hankinson S.E., Helzlsouer K.J., Holford T.R., Huang H.-Y., Moysich K.B., Tessari J.D., Wolff M.S., Zheng T., and Hunter D.J. 1,1-dichloro-2,2-bis(p-chlorophenyl)ethylene and polychlorinated biphenyls and breast cancer: combined analysis of five US studies. J Natl Cancer Inst 2001: 93: 768–775.

    Article  CAS  PubMed  Google Scholar 

  • LaKind J.S. Recent global trends and physiologic origins of dioxins and furans in human milk. J Expo Sci Environ Epidemiol 2007 Jan 24; [Epub ahead of print].

  • LaKind J.S., (Ed.) Technical Workshop on Human Milk Surveillance and Research on Environmental Chemicals in the United States. J Toxicol Env Health Part A 2002: 65 (22): 1827–1935.

    Article  CAS  Google Scholar 

  • LaKind J.S., (Ed.) Technical workshop on human milk surveillance and biomonitoring for environmental chemicals in the United States. J Toxicol Env Health Part A 2005: 68 (20): 1681–1831.

    Article  CAS  Google Scholar 

  • LaKind J.S., Berlin C., and Naiman D.Q. Infant exposure to chemicals in breast milk in the United States: what we need to learn from a breast milk monitoring program. Environ Health Perspect 2001: 109: 75–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • LaKind J.S., Bates M.N., and Wilkins A.A. How useful is measurement of environmental chemicals in human milk in investigations of breast cancer etiology? Organohalogen Compounds 2003: 65: 346–349.

    Google Scholar 

  • LaKind J.S., Berlin C.M., Park C.N., Naiman D.Q., and Gudka N.J. Methodology for characterizing distributions of incremental body burdens of 2,3,7,8-TCDD and DDE from breast milk in North American nursing infants. J Toxicol Env Health Part A 2000: 60: 101–135.

    Article  Google Scholar 

  • LaKind J.S., Wilkins A.A., and Berlin C.M. Environmental chemicals in human milk: a review of concentrations, determinants, infant exposures and health, and guidance for future research. Toxicol Applied Pharmacol 2004: 198: 184–208.

    Article  CAS  Google Scholar 

  • Laug E.P., Kunze F.M., and Prickett C.S. Occurrence of DDT in human fat and milk. Arch Ind Hyg 1951: 3: 245–246.

    CAS  Google Scholar 

  • Lee S.Y., Kim M.T., Kim S.W., Song M.S., and Yoon S.J. Effect of lifetime lactation on breast cancer risk: a Korean women's cohort study. Int J Cancer 2003: 105: 390–393.

    Article  CAS  PubMed  Google Scholar 

  • Li D., Wang M., Dhingra K., and Hittelman W.N. Aromatic DNA adducts in adjacent tissues of breast cancer patients: clues to breast cancer etiology. Cancer Res 1996: 56: 287–293.

    CAS  PubMed  Google Scholar 

  • Lightfoot T.J., Coxhead J.M., Cupid B.C., Nicholson S., and Garner R.C. Analysis of DNA adducts by accelerator mass spectrometry in human breast tissue after administration of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine and benzo[a]pyrene. Mutat Res 2000: 472: 119–127.

    Article  CAS  PubMed  Google Scholar 

  • Lipworth L., Bailey L.R., and Trichopoulos D. History of breast-feeding in relation to breast cancer risk: a review of the epidemiologic literature. J Natl Cancer Inst 2000: 92: 302–312.

    Article  CAS  PubMed  Google Scholar 

  • Lorber M., and Phillips L. Infant exposure to dioxin-like compounds in breast milk. Environ Health Perspect 2002: 110: A325–A332.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Madigan M.P., Ziegler R.G., Benichou J., Byrne C., and Hoover R.N. Proportion of breast cancer cases in the United States explained by well-established risk factors. J Natl Cancer Inst 1995: 87: 1681–1685.

    Article  CAS  PubMed  Google Scholar 

  • Magnusson C., Colditz G., Rosner B., Bergström R., and Persson I. Association of family history and other risk factors with breast cancer risk (Sweden). Cancer Causes Control 1998: 9: 259–267.

    Article  CAS  PubMed  Google Scholar 

  • Malatesta M., Mannello F., Bianchi G., Sebastiani M., and Gazzanelli G. Biochemical and ultrastrucural features of human milk and nipple aspirate fluids. J Clin Lab Anal 2000: 14: 330–335.

    Article  CAS  PubMed  Google Scholar 

  • Martin F.L., Carmichael P.L., Crofton-Sleigh C., Venitt S., Phillips D.H., and Grover P.L. Genotoxicity of human mammary lipid. Cancer Res 1996: 56: 5342–5346.

    CAS  PubMed  Google Scholar 

  • Martin F.L., Cole K.J., Weaver G., Williams J.A., Millar B.C., Grover P.L., and Phillips D.H. Genotoxicity of human milk extracts and detection of DNA damage in exfoliated cells recovered from breast milk. Biochem Biophys Res Comm 1999: 257: 319–326.

    Article  CAS  PubMed  Google Scholar 

  • Martin F.L., Cole K.J, Harvey D., Weaver G., Williams J.A., Millar B.C., Phillips D.H., and Grover P.L. DNA damage in human breast milk cells and its induction by ‘early’ and ‘late’ milk extracts. Carcinogenesis 2000a: 21: 799–804.

    Article  CAS  PubMed  Google Scholar 

  • Martin F.L., Cole K.J., Williams J.A., Millar B.C., Harvey D., Weaver G., Grover P.L., and Phillips D.H. Activation of genotoxins to DNA-damaging species in exfoliated breast milk cells. Mutat Res 2000b: 470: 115–124.

    Article  CAS  PubMed  Google Scholar 

  • Martin F.L., Cole K.J., Weaver G., Hong G.S., Lam B.C., Balaram P., Grover P.L., and Phillips D.H. Genotoxicity of human breast milk from different countries. Mutagenesis 2001: 16: 401–406.

    Article  CAS  PubMed  Google Scholar 

  • Martin R.M., Middleton N., Gunnell D., Owen C.G., and Smith G.D. Breast-feeding and cancer: The Boyd Orr cohort and a systematic review with meta-analysis. J Natl Cancer Inst 2005: 97: 1446–1457.

    Article  PubMed  Google Scholar 

  • McClure G.Y., Thompson P.A., DeMarini D., Brooks L., Green B., Fares M., Stone A., Josephy D., Kadlubar F., and Ambrosone C.B. Evidence for arylamines in human breast carcinogenesis. Proc Am Assoc Cancer Res 1999: 40: 410.

    Google Scholar 

  • McPhee S.J., Lingappa V.R., Ganong W.F., and Lange J.D. Pathophysiology of Disease: An Introduction to Clinical Medicine, Fifth Edition. Lange Medical Books/McGraw-Hill Medical Publishing Division, New York, 2006.

    Google Scholar 

  • Mussalo-Rauhamaa H., and Pantzar P. Selenium and DDE in breast fat of breast cancer patients: their relationship to hormone receptors in breast tissue (letter). J Natl Cancer Inst 1993: 85: 1964–1965.

    Article  CAS  PubMed  Google Scholar 

  • Neutra R.R., Testimony of Raymond Richard Neutra M.D. Dr.P.H., Chief, Division of Environmental and Occupational Disease Control, California Department of Health Services: Senate Health and Human Services Committee and Assembly Health Committee: Joint Informational Hearing on Breast Cancer and the Environment, October 23, 2002. Available: http://www.breastcancerfund.org/environment_hearing_neutra.htm(accessed 16 September 2003).

  • Perera F.P., Estabrook A., Hewer A., Channing K., Rundle A., Mooney L.A., Whyatt R., and Phillips D.H. Carcinogen-DNA adducts in human breast tissue. Cancer Epidemiol Biomarkers Prev 1995: 4: 233–238.

    CAS  PubMed  Google Scholar 

  • Petrakis N.L. Physiologic, biochemical, and cytologic aspects of nipple aspirate fluid. Breast Cancer Res Treat 1986: 8: 7–19.

    Article  CAS  PubMed  Google Scholar 

  • Petrakis N.L. Nipple aspirate fluid in epidemiologic studies of breast disease. Epidemiol Rev 1993a: 15: 188–195.

    Article  CAS  PubMed  Google Scholar 

  • Petrakis N.L. Studies on the epidemiology and natural history of benign breast disease and breast cancer using nipple aspirate fluid. Cancer Epidemiol Biomarkers Prev 1993b: 3: 3–10.

    Google Scholar 

  • Petrakis N.L., Maack C.A., Lee R.E., and Lyon M. Mutagenic activity in the nipple aspirates of human breast fluid. Cancer Res 1980: 40: 188–189.

    CAS  PubMed  Google Scholar 

  • Petrakis N.L., Gruenke L.D., Beelen T.C., Castagnoli N., and Craig J.C. Nicotine in breast fluid of nonlactating women. Science 1978: 199: 303–305.

    Article  CAS  PubMed  Google Scholar 

  • Petreas M., Smith D., Hurley S., Jeffrey S.S., Gilliss D., and Reynolds P. Distribution of persistent, lipid-soluble chemicals in breast and abdominal adipose tissues: Lessons learned from a breast cancer study. Cancer Epidemiol Biomarkers Prev 2004: 13: 416–424.

    CAS  PubMed  Google Scholar 

  • Phillips D.H., Martin F.L., Williams A., Wheat L.M.C., Nolan L., Cole K.J., and Grover P.L. Mutagens of human breast lipid and milk: the search for environmental agents that initiate breast cancer. Environ Mol Mutagen 2002: 39: 143–149.

    Article  CAS  PubMed  Google Scholar 

  • Potischman N., and Troisi R. In-utero and early life exposures in relation to risk of breast cancer. Cancer Causes Control 1999: 10: 561–573.

    Article  CAS  PubMed  Google Scholar 

  • Raaschou-Nielsen O., Pavuk M., Leblanc A., Dumas P., Weber J.P., Olsen A., Tjonneland A., Overvad K., and Olsen J.H. Adipose organochlorine concentrations and risk of breast cancer among postmenopausal Danish women. Cancer Epidemiol Biomarkers Prev 2005: 14: 67–74.

    CAS  PubMed  Google Scholar 

  • Rundle A., Tang D., Hibshoosh H., Estabrook A., Schnabel F., Cao W., Grumet S., and Perera F.P. The relationship between genetic damage from polycyclic aromatic hydrocarbons in breast tissue and breast cancer. Carcinogenesis 2000: 21: 1281–1289.

    Article  CAS  PubMed  Google Scholar 

  • Rusiecki J.A., Holford T.R., Zahm S.H., and Zheng T. Polychlorinated biphenyls and breast cancer risk by combined estrogen and progesterone receptor status. Eur J Epidemiol 2004: 19: 793–801.

    Article  CAS  PubMed  Google Scholar 

  • Safe S. Is there an association between exposure to environmental estrogens and breast cancer? Environ Health Perspect 1997: 105 (Suppl 3): 675–678.

    Article  PubMed  PubMed Central  Google Scholar 

  • Safe S., and Zacharewski T. Organochlorine exposure and risk for breast cancer. In: Aldaz CM, Gould MN, McLachlan J, Slaga TJ (Eds.). Etiology of Breast and Gynecological Cancers. Wiley-Liss, New York, 1997 pp. 133–145.

    Google Scholar 

  • Scott W.N., and Miller W.R. The mutagenic activity of human breast secretions. J Cancer Res Clin Oncol 1990: 116: 499–502.

    Article  CAS  PubMed  Google Scholar 

  • Scott W.N., and Miller W.R. Mutagens in human breast cyst fluid. J Cancer Res Clin Oncol 1991: 117: 254–258.

    Article  CAS  PubMed  Google Scholar 

  • Shan L., Yu M., Schut H.A.J., and Snyderwine E.G. Susceptibility of rats to mammary gland carcinogenesis by the food-derived carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) varies with age and is associated with the induction of differential gene expression. Am J Pathol 2004: 165: 191–202.

    Article  CAS  PubMed  Google Scholar 

  • Siddiqui M.K.J., Anand M., Mehrotra P.K., Sarangi R., and Mathur N. Biomonitoring of organochlorines in women with benign and malignant breast disease. Environ Res 2005: 98: 250–257.

    Article  CAS  PubMed  Google Scholar 

  • Smith D. Worldwide trends in DDT levels in human breast milk. Int J Epidem 1999: 28: 179–188.

    Article  CAS  Google Scholar 

  • Snedeker S. Pesticides and breast cancer risk: A review of DDT, DDE, and dieldrin. Environ Health Perspect 2001: 109 (Suppl 1): 35–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snedeker S.M. Chemical exposures in the workplace: effect on breast cancer risk among women. AAOHN J 2006: 54: 270–279.

    Article  PubMed  Google Scholar 

  • Snyderwine E.G., Venugopal M., and Yu M. Mammary gland carcinogenesis by food-derived heterocyclic amines and studies on the mechanisms of carcinogenesis of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP). Mutat Res 2002: 506-507: 145–152.

    Article  CAS  PubMed  Google Scholar 

  • Solomon G.M., and Weiss P.M. Chemical contaminants in breast milk: time trends and regional variability. Environ Health Perspect 2002: 110: A339–A347.

    Article  CAS  PubMed  Google Scholar 

  • Sonawane B.R. Chemical contaminants in human milk: an overview. Environ. Health Perspect 1995: 103 (Suppl 6): 197–205.

    Article  CAS  PubMed  Google Scholar 

  • Thompson P.A., Kadlubar F.F., Vena S.M., Hill H.L., McClure G.H.Y., McDaniel L.P., and Ambrosone C.B. Exfoliated ductal epithelial cells in human breast milk: a source of target tissue DNA for molecular epidemiologic studies of breast cancer. Cancer Epidemiol Biomarkers Prev 1998: 7: 37–42.

    CAS  PubMed  Google Scholar 

  • Thompson P.A., DeMarini D.M., Kadlubar F.F., McClure G.Y., Brooks L.R., Green B.L., Fares M.Y., Stone A., Josephy P.D., and Ambrosone C.B. Evidence for the presence of mutagenic arylamines in human breast milk and DNA adducts in exfoliated breast ductal epithelial cells. Environ Mol Mutagen 2002: 39: 134–142.

    Article  CAS  PubMed  Google Scholar 

  • Titus-Ernstoff L., Egan K.M., Newcomb P.A., Baron J.A., Stampfer M., Greenberg E.R., Cole B.F., Ding J., Willett W., and Trichopoulos D. Exposure to breast milk in infancy and adult breast cancer risk. J Natl Cancer Inst 1998: 90: 921–924.

    Article  CAS  PubMed  Google Scholar 

  • Tokuhata G.K. Morbidity and mortality among off-spring of breast cancer mothers. Am J Epidemiol 1969: 89: 139–153.

    Article  CAS  PubMed  Google Scholar 

  • Tsung J.S., Wang T.Y., Wang S.M., and Yang P.S. Cytological and biochemical studies of breast cyst fluid. Breast 2005: 14: 37–41.

    Article  CAS  PubMed  Google Scholar 

  • Unger M., Kiær H., Blichert-Toft M., Olsen J., and Clausen J. Organochlorine compounds in human breast fat from deceased with and without breast cancer and in a biopsy material from newly diagnosed patients undergoing breast surgery. Environ Res 1984: 34: 24–28.

    Article  CAS  PubMed  Google Scholar 

  • Ward E.M., Schulte P., Grajewski B., Anderson A., Patterson Jr D.G., Turner W., Jellum E., Deddens J., Friedland J., Roeleveld N., Waters M., Butler M., Dipietro E., and Needham L.L. Serum organochlorine levels and breast cancer: a nested case–control study of Norwegian women. Cancer Epidem Biomarkers Prev 2000: 9: 1357–1367.

    CAS  Google Scholar 

  • Wassermann M., Nogueira D.P., Tomatis L., Mirra A.P., Shibata H., Arie G., Cucos S., and Wassermann D. Organochlorine compounds in neoplastic and adjacent apparently normal breast tissue. Bull Environ Contam Toxicol 1976: 15: 478–484.

    Article  CAS  PubMed  Google Scholar 

  • Weiss H.A., Potischman N.A., Brinton L.A., Brogan D., Coates R.J., Gammon M.D., Malone K.E., and Schoenberg J.B. Prenatal and perinatal risk factors for breast cancer in young women. Epidemiol 1997: 8: 181–187.

    Article  CAS  Google Scholar 

  • Wheat L.M.C., Martin F.L., and Phillips D.H. Genotoxic agents in human milk. Proc Am Assoc Cancer Res 2001: 42, Abstract 3233.

  • Wolff M.S., and Berkowitz G.S. Reply. Env Res A 2002: 88: 70–71.

    Article  CAS  Google Scholar 

  • Wolff M.S., and Weston A. Breast cancer risk and environmental exposures. Environ Health Perspect 1997: 105 (Supp 4): 891–896.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Woolcott C.G., Aronson K.J., Hanna W.M., SenGupta S.K., McCready D.R., Sterns E.E., and Miller A.B. Organochlorines and breast cancer risk by receptor status, tumor size, and grade (Canada). Cancer Causes Control 2001: 12: 395–404.

    Article  CAS  PubMed  Google Scholar 

  • Wrensch M.R., Petrakis N., Gruenke L.D., Ernster V.L., Miike R., King E.B., and Hauck W.W. Factors associated with obtaining nipple aspirate fluid: analysis of 1428 women and literature review. Breast Cancer Res Treat 1990: 15: 39–51.

    Article  CAS  PubMed  Google Scholar 

  • Zheng T., Holford T.R., Mayne S.T., Ward B., Carter D., Owens P.H., Dubrow R., Zahm S.H., Boyle P., Archibeque S., and Tessari J. DDE and DDT in breast adipose tissue and risk of female breast cancer. Am J Epidemiol 1999a: 150: 453–458.

    Article  CAS  PubMed  Google Scholar 

  • Zheng T., Holford T.R., Mayne S.T., Owens P.H., Ward B., Carter D., Dubrow R., Zahm S.H., Boyle P., and Tessari J. β-Benzene hexachloride in breast adipose tissue and risk of breast carcinoma. Cancer 1999b: 85: 2212–2218.

    Article  CAS  PubMed  Google Scholar 

  • Zheng T., Duan L., Liu Y., Zhang B., Wang Y., Chen Y., Zhang Y., and Owens P.H. Lactation reduces breast cancer risk in Shandong Province, China. Am J Epidemiol 2000a: 152: 1129–1135.

    Article  CAS  PubMed  Google Scholar 

  • Zheng T., Holford T.R., Tessari J., Mayne S.T., Zahm S.H., Owens P.H., Zhang B., Ward B., Carter D., Zhang Y., Zhang W., Dubrow R., and Boyle P. Oxychlordane and trans-nonachlor in breast adipose tissue and risk of female breast cancer. J Epidemiol Biostat 2000b: 5: 153–160.

    CAS  PubMed  Google Scholar 

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Acknowledgements

The views expressed in this paper are those of the authors and do not necessarily reflect the views or policies of the US Environmental Protection Agency. We acknowledge comments and suggestions from Dr. Suzanne Fenton and Dr. Babasaheb Sonawane. Dr. LaKind consults to both private industry and government, and received funding from the US Environmental Protection Agency for this research.

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Correspondence to Judy S Lakind.

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Lakind, J., Wilkins, A. & Bates, M. Human breast biomonitoring and environmental chemicals: use of breast tissues and fluids in breast cancer etiologic research. J Expo Sci Environ Epidemiol 17, 525–540 (2007). https://doi.org/10.1038/sj.jes.7500548

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