Breast Cancer Research and Treatment

, Volume 92, Issue 2, pp 107–114 | Cite as

An ecological study of the association of environmental chemicals on breast cancer incidence in Texas

  • Yvonne M. CoyleEmail author
  • Linda S. Hynan
  • David M. Euhus
  • Abu T.M. Minhajuddin


Purpose. To investigate the role of environment in breast cancer development, we conducted an ecological study to examine the association of releases for selected industrial chemicals with breast cancer incidence in Texas.

Methods. During 1995–2000, 54,487 invasive breast cancer cases were reported in Texas. We identified 12 toxicants released into the environment by industry that: (1) were positively associated with breast cancer in epidemiological studies, (2) were Environmental Protection Agency (EPA) Toxics Release Inventory (TRI) chemicals designated as carcinogens or had estrogenic effects associated with breast cancer risk, and (3) had releases consistently reported to EPA TRI for multiple Texas counties during 1988–2000. We performed univariate, and multivariate analyses adjusted for race and ethnicity to examine the association of releases for these toxicants during 1988–2000 with the average annual age-adjusted breast cancer rate at the county level.

Results. Univariate analysis indicated that formaldehyde, methylene chloride, styrene, tetrachloroethylene, trichloroethylene, chromium, cobalt, copper, and nickel were positively associated with the breast cancer rate. Multivariate analyses indicated that styrene was positively associated with the breast cancer rate in women and men (β = 0.219, p =0.004), women (β = 0.191, p=0.002), and women ≥ 50 years old (β = 0.187, p=0.002).

Conclusion. Styrene was the most important environmental toxicant positively associated with invasive breast cancer incidence in Texas, likely involving women and men of all ages. Styrene may be an important breast carcinogen due to its widespread use for food storage and preparation, and its release from building materials, tobacco smoke, and industry.


breast neoplasms environment metals organic chemicals risk factors 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Parkin, DM, Pisani, P, Ferlay, J 1999Estimates of worldwide incidence of 25 major cancers in 1990Int J Cancer80827841Google Scholar
  2. 2.
    Landis, SH, Murray, T, Bolden, S, Wingo, PA 1998Cancer statistics in 1998CA Cancer J Clin48629Google Scholar
  3. 3.
    Lacey, JV, Devesa, SS, Brinton, LA 2002Recent trends in breast cancer incidence and mortalityEnviron Mol Mutagen398288Google Scholar
  4. 4.
    Key, TJ, Verkasalo, PK, Banks, E 2001Epidemiology of breast cancerLancet2133140Google Scholar
  5. 5.
    Madigan, MP, Ziegler, RG, Benichou, J, Byrne, C, Hoover, RN 1995Proportion of breast cancer cases in the United States explained by well-established risk factorsJ Natl Cancer Inst8716811685Google Scholar
  6. 6.
    Rockhill, B, Weinberg, CR, Newman, B 1998Population attributable fraction estimation for established breast cancer risk factors: Considering the issues of high prevalence and unmodifiabilityAm J Epidemiol147826833Google Scholar
  7. 7.
    Evans, JS, Wennberg, JE, McNeil, BJ 1986The influence of diagnostic radiography on the incidence of breast cancer and leukemiaN␣Engl J Med315810815Google Scholar
  8. 8.
    Thomas, DB, Jimenez, LM, McTiernen, A, Rosenblatt, K, Stalsberg, H, Stemhagen, A, Thompson, WD, Curnen, MG, Satariano, W, Austin, DF, Greenberg, RS, Key, C, Kolonel, LN, West, DW 1992Breast cancer in men: risk factors with hormonal implicationsAm J Epidemiol135734748Google Scholar
  9. 9.
    Hsing, AW, McLaughlin, JK, Cocco, P, Co, Chein , Fraumeni, JF,Jr. 1998Risk factors for male breast cancer (United States)Cancer Causes Control9269275Google Scholar
  10. 10.
    Sorenson, HT, Friis, S, Olsen, JH, Thulstrup, AM, Mellemkjaer, L, Linet, M, Trichopoulos, D, Vistrup, H, Olsen, J 1998Risk of breast cancer in men with liver cirrhosisAm J Gastroenterol93231233Google Scholar
  11. 11.
    Giordano, SH, Buzdar, AU, Hortobagyi, GN 2002Breast cancer in menAnn Intern Med137678687Google Scholar
  12. 12.
    National Research Council: Hormonally Active Agents in the Environment. National Academy Press, Washington, DC, 1999Google Scholar
  13. 13.
    Russo, J, Hu, YF, Yang, X, Russo, IH 2000Chapter 1: developmental, cellular, and molecular basis of human cancerJ Natl Cancer Inst Monogr271737Google Scholar
  14. 14.
    Sturgeon, SR, Schairer, C, Gail, M, McAdams, M, Brinton, LA, Hoover, RN 1995Geographic variation in mortality from breast cancer among white women in the United StatesJ Natl Cancer Inst8718461853Google Scholar
  15. 15.
    Robbins, AS, Brescianini, S, Kelsey JL,  1997Regional differences in known risk factors and the higher incidence of breast cancer in San FranciscoJ Natl Cancer Inst89960965Google Scholar
  16. 16.
    Laden, F, Spiegleman, D, Neas, LM, Colditz, GA, Hankinson, SE, Manson, JE, Byrne, C, Rosner, BA, Speizer, FE, Hunter, DJ 1997Geographic variation in breast cancer incidence rates in a cohort of US womenJ Natl Cancer Inst8913731378Google Scholar
  17. 17.
    Prehn, AW, West, DW 1998Evaluating local differences in breast cancer incidence rates: a census-based methodology (United States)Cancer Causes Control9511517Google Scholar
  18. 18.
    Reynolds, P, Hurley, S, Goldberg, DE, Anton-Culver, H, Bernstein, L, Deapen, D, Horn-Ross, PL, Peel, D, Pinder, R, Ross, RK, West, D, Wright, WE, Ziogas, A 2004Regional variations in breast cancer among California teachersEpidemiology15746754Google Scholar
  19. 19.
    U.S. Environmental Protection Agency. What is the Toxics Release Inventory (TRI) Program. http://www.epa./gov/tri/what is. htm (23 November 2004)
  20. 20.
    U.S. Environmental Protection Agency. Toxics Release Inventory Program. (23 November 2004)
  21. 21.
    Chakraborty, J 2004The geographic distribution of potential risks posed by industrial toxic emissions in the USJ Environ Sci Health Part A Tox Hazard Subst Environ Eng39559575Google Scholar
  22. 22.
    Wunderlich, L 1995An Overview of the Uses of the Toxics Release Inventory Data in the U.SUS Environmental Protection Agency (US. EPA), Office of Pollution Prevention and Toxics (OPPT)Washington, DCGoogle Scholar
  23. 23.
    Dent, AL, Fowler, BM, Kaplan, GM, Zarus, GM, Henriques, WD 2000Using GIS to study the health impact of air emissionsDrug Chem Toxicol23161178Google Scholar
  24. 24.
    Neumann, CM, Forman, DL, Rothlein, JE 1998Hazard screening of chemical releases and environmental equity analysis of populations proximate to toxic release inventory facilities in OregonEnviron Health Perspect106217226Google Scholar
  25. 25.
    Cantor, KP, Stewart, PA, Brinton, LA, Dosemeci, M 1995Occupational exposures and female breast cancer mortality in the United StatesJ Occup Environ Med37336348Google Scholar
  26. 26.
    Hansen, J 1999Breast cancer risk among relatively young women employed in solvent-using industriesAm J Ind Med364347Google Scholar
  27. 27.
    Band, PR, Le, ND, Fang, R, Deschamps, M, Yang, P 2000Identification of occupational cancer risks in British Columbia. A population-based case–control study of 995 incident breast cancer cases by menopausal status, controlling for confounding factorsJ Occup Environ Med42284310Google Scholar
  28. 28.
    U.S. Environmental Protection Agency. EPA TRI. OSHA Carcinogens. http// (23 November 2004)Google Scholar
  29. 29.
    Martin, MB, Reiter, R, Pham, T, Allellanet, YR, Camara, J, Lahm, M, Pentecost, L, Pratap, K, Gilmore, BA, Divekar, S, Daguta, RS, Bull, JL, Stoica, A 2003Estrogen-like activity of metals in mcf-7 breast cancer cellsEndocrinology14424252436Google Scholar
  30. 30.
    Jia, ZG 1991Analysis of serum levels of selenium, zinc, and copper in 132 patients with malignant tumorsZhonghua Yu Fang Yi Xue Za Zhi25205207Google Scholar
  31. 31.
    Capel, ID, Pinnock, MH, Williams, DC, Hanham, IW 1982The serum levels of some trace and bulk elements in cancer patientsOncology393841Google Scholar
  32. 32.
    Margalioth EJ, Schenker JG, Chevron M: Copper and zinc levels in normal and malignant tissues. Cancer 52: 868–872, 1983Google Scholar
  33. 33.
    Vaidya, SM, Kamalakar, PL 1998Copper and ceruloplasmin levels in serum of women with breast cancerInd J Med Sci52184187Google Scholar
  34. 34.
    Garofalo, JA, Ashkari, H, Lesser, ML, Menendez-Botet, C, Cunningham-Rundels, S, Schwartz, MK, Good, RA 1980Serum zinc, copper, and CU/Zn ratio in patients with benign and malignant breast lesionsCancer4626822685Google Scholar
  35. 35.
    Gupta, SK, Shukla, VK, Naidya, MP, Roay, SK, Gupta, S 1991Serum trace elements and Cu/Zn ratio in breast cancerJ Surg Oncol46178181Google Scholar
  36. 36.
    Yenisey, C, Fadilogu, M, Onvural, B 1996Serum copper and ceruloplasmin concentrations in patients with primary breast cancerBiochem Soc Trans24321SGoogle Scholar
  37. 37.
    National Toxicology Program. National Toxicology Program Annual Plan 2002 (NIH Publication No. 03–5309). U.S. Department of Health and Human Services, Rockville, MD, 2002Google Scholar
  38. 38.
    International Agency for Research on Cancer. IARC’s Mission. Cancer Research for Cancer Control. (23 November 2004)
  39. 39.
    Agricultural Health Study. Study Background. http://www. (2 December 2004)
  40. 40.
    Gammon, MD, Wolff, MS, Neugut, AI, Eng, SM, Teitelbaum, SL, Britton, JA, Terry, MB, Levin, B, Stellman, SD, Kabat, GC, Hatch, M, Senie, R, Berkowitz, G, Bradlow, HL, Garbowski, G, Maffeao, C, Montalvan, P, Kemeny, M, Citron, M, Schnabel, F, Schuss, A, Hajdu, S, Vinceguerra, V, Niguidula, N, Ireland, K, Santella, RM 2002Environmental toxins and breast cancer on Long Island. II. Organochlorine compound levels in bloodCancer Epidemiol Biomark Prev11686697Google Scholar
  41. 41.
    Texas Department of Health: change in population standard for age-adjusted rates. Dis Prev News 60(5): 1–5, 2001Google Scholar
  42. 42.
    Anderson, RN, Rosenberg, HM 1998Age standardization of death rates: implementation of the year 2000 standardNational Center for Health StatisticsHyattsville, MDGoogle Scholar
  43. 43.
    The North American Association of Central Cancer Registries. Cancer in North America Publications. NAACCR Combined Incidence Rates. & Col_ContentID=50 (7 December 2004)
  44. 44.
    United States Census 2000. Texas QuickFacts from the US Census Bureau. (23 November 2004)
  45. 45.
    The North American Association of Central Cancer Registries. Cancer in North America Publications. Section III: Age-adjusted Cancer Incidence for the NAACCR (U.S.) Combined by Sex and Hispanic/Latino Ethnicity, 1995–2000. & Col_ContentID=50 (7 December 2004)
  46. 46.
    United States Census 2000. Census 2000. Urban and Rural Classification. (23 November 2004)
  47. 47.
    United States Environmental Protection Agency. How Are the Toxics Release Inventory Data Used? (EPA-260-R-002–004), Office of Information Analysis and Access, Washington D.C, 2003Google Scholar
  48. 48.
    U.S. Environmental Protection Agency. Toxics Release Inventory Program. 2002 TRI Press Materials. TRI Total Disposal or Other Releases, 1988–2002. (23 November 2004)
  49. 49.
    SAS Institute Inc.: SAS (Program) Version 9.0. SAS Institute, Cary, NC, 2004Google Scholar
  50. 50.
    Center for Disease Control. Agency for Toxic Substances and Disease Registry. ToxFAQs for Styrene. http://www.atsdr. (26 October 2004)
  51. 51.
    United States Environmental Protection Agency. Technology Transfer Network Air Toxics Website. Styrene. http://www. (26 October 2004)
  52. 52.
    Demole, E, Berthet, D 1979A chemical study of Burley tobacco flavour (Nicotiana tabacum L.) I. Volatile to medium-volatile constituents (b. p. ≤ 84° C/0.001 Torr)Helv Chim Acta5518661882Google Scholar
  53. 53.
    International Agency for Research on Cancer: IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Styrene. IARC, Lyon, 2002Google Scholar
  54. 54.
    Rappaport, SM, Yeowell-O’Connell, K, Bodel, W, Yager, JW, Symanski, E 1996An investigation of multiple biomarkers among workers exposed to styrene and styrene-7,8-oxideCancer Res5654105416Google Scholar
  55. 55.
    Ohno, K, Azuma, Y, Nakano, S, Kobayashi, T, Hirano, S, Nobuhara, Y, Yamada, T 2001Assessment for styrene oligomers eluted from polystyrene-made food containers for estrogenic effects in in vitro assaysFood Chem Toxicol3912331241Google Scholar
  56. 56.
    Wong, O 1990A cohort mortality study and a case–control study of workers potentially exposed to styrene in the reinforced plastics and composites industryBr Ind J Med47753762Google Scholar
  57. 57.
    Matanoski- Francis, M, Correa-Villasenor, A, Elliot, E, Sautos-Burgoa, C, Schwartz, L 1993Cancer epidemiology among styrene- butadiene rubber workersIARC Sci Publ 127363374Google Scholar
  58. 58.
    Wong, O, Lisa, ST, Whorton, MD 1994An updated cohort mortality study of workers exposed to styrene in the reinforced plastics and composites industryOccup Environ Med51386396Google Scholar
  59. 59.
    Kogevinas, M, Ferro, G, Andersen, A, Bellander, T, Biocca, M, Coggon, D, Gennaro, V, Hutchings, S, Kolstad, H, Lundberg, I, Lynge, E, Partanen, T, Saracci, R 1994Cancer mortality in a historical cohort study of workers exposed to styreneScand J Work Environ Health20251261Google Scholar
  60. 60.
    Kolstad, HA, Juel, K, Olsen, J, Lynge, E 1995Exposure to styrene and chronic health effects: mortality and incidence of solid cancers in the Danish reinforced plastics industryOccup Environ Med52320327Google Scholar
  61. 61.
    Ruder, AM, Ward, EM, Dong, M, Okun, AH, Davis-King, K 2004Mortality patterns among workers exposed to styrene in the reinforced plastic boatbuilding industry: an updateAm J Ind Med45165176Google Scholar
  62. 62.
    Darrall, KG, Figgins, JA, Brown, RD, Phillips, GF 1998Determination of benzene and associated volatile compounds in mainstream cigarette smokeAnalyst12310951101Google Scholar
  63. 63.
    Miller, SL, Branoff, S, Nazaroff, WW 1998Exposure to toxic air contaminants in environmental tobacco smoke: an assessment for California based on personal monitoring dataJ Expo Anal Environ Epidemiol8287311Google Scholar
  64. 64.
    Morabia, A 2002Smoking (active and passive) and breast cancer: epidemiologic evidence up to June 2001Environ Mol Mutagen398995Google Scholar
  65. 65.
    Terry, PD, Rohan, TE 2002Cigarette smoking and the risk of breast cancer in women: a review of the literatureCancer Epidemiol Biomarkers Prev11953971Google Scholar
  66. 66.
    Kropp, S, Chang-Claude, J 2002Active and passive smoking and risk of breast cancer by age 50 years among German womenAm J Epidemiol156616626Google Scholar
  67. 67.
    Gordis, L 2000Epidemiology2ndW.B. Saunders CompanyPhiladelphiaGoogle Scholar
  68. 68.
    Colton, T, Greenberg, R, Noller, K, Ressquie, L, Bennekam, C, Heeven, T, Zhang, Y 1993Breast cancer in mothers prescribed diethylstilbesterol in pregnancy. Further follow-upJAMA26920962100Google Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Yvonne M. Coyle
    • 1
    Email author
  • Linda S. Hynan
    • 2
  • David M. Euhus
    • 3
  • Abu T.M. Minhajuddin
    • 2
  1. 1.Department of Internal Medicine, Hamon Center for Therapeutic Oncology ResearchThe University of Texas Southwestern Medical Center at DallasDallas USA
  2. 2.Center for Biostatistics and Clinical ScienceThe University of Texas Southwestern Medical Center at Dallas USA
  3. 3.Department of Surgery, Hamon Center for Therapeutic Oncology ResearchThe University of Texas Southwestern Medical Center at DallasDallas USA

Personalised recommendations