Breast Cancer Research and Treatment

, Volume 120, Issue 1, pp 149–160

Urban–rural differences in breast cancer incidence by hormone receptor status across 6 years in Egypt

  • Subhojit Dey
  • Amr S. Soliman
  • Ahmad Hablas
  • Ibrahim A. Seifeldin
  • Kadry Ismail
  • Mohamed Ramadan
  • Hesham El-Hamzawy
  • Mark L. Wilson
  • Mousumi Banerjee
  • Paolo Boffetta
  • Joe Harford
  • Sofia D. Merajver
Epidemiology

Abstract

Breast cancer incidence is higher in developed countries with higher rates of estrogen receptor positive (ER+) tumors. ER+ tumors are caused by estrogenic exposures although known exposures explain approximately 50% of breast cancer risk. Unknown risk factors causing high breast cancer incidence exist that are estrogenic and development-related. Xenoestrogens are such risk factors but are difficult to study since developed countries lack unexposed populations. Developing countries have urban–rural populations with differential exposure to xenoestrogens. This study assessed urban–rural breast cancer incidence classified by hormone receptor status using data from Gharbiah population-based cancer registry in Egypt from 2001 to 2006. Urban ER+ incidence rate (per 100,000 women) was 2–4 times (IRR = 3.36, 95% CI = 4.84, 2.34) higher than rural incidence rate. ER−incidence rate was 2–3 times (IRR = 1.86, 95% CI = 2.38, 1.45) higher in urban areas than in rural areas. Our findings indicate that urban women may probably have a higher exposure to xenoestrogens.

Keywords

Breast cancer incidence Hormone receptor status Mammary stem cells Xenoestrogens Egypt 

References

  1. 1.
    Parkin DM, Fernandez LMG (2006) Use of statistics to assess the global burden of breast cancer. Breast J 12:S70–S80. doi:10.1111/j.1075-122X.2006.00205.x CrossRefPubMedGoogle Scholar
  2. 2.
    Colditz GA, Rosner BA, Chen WY et al (2004) Risk factors for breast cancer according to estrogen and progesterone receptor status. J Natl Cancer Inst 96:218–228PubMedGoogle Scholar
  3. 3.
    Chen WY, Colditz GA (2007) Risk factors and hormone-receptor status: epidemiology, risk-prediction models and treatment implications for breast cancer. Nat Clin Pract Oncol 4(7):415–423. doi:10.1038/ncponc0851 CrossRefPubMedGoogle Scholar
  4. 4.
    Hess KR, Pusztai L, Buzdar AU, Hortobagyi GN (2003) Estrogen receptors and distinct patterns of breast cancer relapse. Breast Cancer Res Treat 78(1):105–118. doi:10.1023/A:1022166517963 CrossRefPubMedGoogle Scholar
  5. 5.
    Huang W, Newman B, Millikan RC, Schell MJ, Hulka BS, Moorman PG (2000) Hormone-related factors and risk of breast cancer in relation to estrogen receptor and progesterone receptor status. Am J Epidemiol 151:703–714PubMedGoogle Scholar
  6. 6.
    Althuis MD, Fergenbaum JH, Garcia-Closas M, Brinton LA, Madigan MP, Sherman ME (2004) Etiology of hormone receptor defined breast cancer: a systematic review of the literature. Cancer Epidemiol Biomarkers Prev 13(10):1558–1568PubMedGoogle Scholar
  7. 7.
    Manjer J, Malina J, Berglund G, Bondeson L, Garne JP, Janzon L (2001) Smoking associated with hormone receptor negative breast cancer. Int J Cancer 91:580–584. doi:10.1002/1097-0215(200002)9999:9999<::AID-IJC1091>3.0.CO;2-V CrossRefPubMedGoogle Scholar
  8. 8.
    Bray F, McCarron P, Parkin DM (2004) The changing global patterns of female breast cancer incidence and mortality. Breast Cancer Res 6:229–239. doi:10.1186/bcr932 CrossRefPubMedGoogle Scholar
  9. 9.
    Anderson WF, Chu KC, Chatterjee N, Brawley O, Brinton LA (2001) Tumor variants by hormone receptor expression in white patients with node-negative breast cancer from the surveillance, epidemiology, and end results database. J Clin Oncol 19:18–27PubMedGoogle Scholar
  10. 10.
    Li CI, Malone KE, Daling JR (2002) Differences in breast cancer hormone receptor status and histology by race and ethnicity among women 50 years of age and older. Cancer Epidemiol Biomarkers Prev 11(7):601–607PubMedGoogle Scholar
  11. 11.
    Chlebowski RT, Chen Z, Anderson GL et al (2005) Ethnicity and breast cancer: factors influencing differences in incidence and outcome. J Natl Cancer Inst 97:439–448PubMedGoogle Scholar
  12. 12.
    Parkin DM, Whelan SL, Ferlay J, Teppo L, Thomas TB (eds) (2002) Cancer incidence in five continents, vol VIII. IARC Sc. Publns No.155, LyonGoogle Scholar
  13. 13.
    Desai SB, Moonim MT, Gill AK, Punia RS, Naresh KN, Chinoy RF (2000) Hormone receptor status of breast cancer in India: a study of 798 tumors. Breast 9:267–270. doi:10.1054/brst.2000.0134 CrossRefPubMedGoogle Scholar
  14. 14.
    Li CI, Daling JR, Malone KE (2003) Incidence of invasive breast cancer by hormone receptor status from 1992 to 1998. J Clin Oncol 21(1):28–34. doi:10.1200/JCO.2003.03.088 CrossRefPubMedGoogle Scholar
  15. 15.
    Madigan MP, Zeigler RG, Benichou J, Byrne C, Hoover RN (1995) Proportion of breast cancer cases in the United States explained by well-established risk factors. J Natl Cancer Inst 87:1681–1685. doi:10.1093/jnci/87.22.1681 CrossRefPubMedGoogle Scholar
  16. 16.
    Rockhill B, Weinberg CR, Newman B (1998) Population attributable fraction estimation for estimation for established breast cancer risk factors: considering the issues of high prevalence and un-modifiability. Am J Epidemiol 147:826–833PubMedGoogle Scholar
  17. 17.
    Gray J, Evans N, Taylor B, Rizzo J, Walker M (2009) State of the evidence: the connection between breast cancer and the environment. Int J Occup Environ Health 15(1):43–78PubMedGoogle Scholar
  18. 18.
    Brody JG, Rudel RA, Michels KB, Moysich KB, Berstein L, Attfield KR, Gray S (2007) Environmental pollutants, diet, physical activity, body size, and breast cancer. Where do we stand in research to identify opportunities for prevention? Cancer 109(Suppl 12):2627–2634. doi:10.1002/cncr.22656 CrossRefPubMedGoogle Scholar
  19. 19.
    Robison AK, Sirbasku DA, Stancel GM (1985) DDT supports the growth of an estrogen-responsive tumor. Toxicol Lett 27:109–113. doi:10.1016/0378-4274(85)90127-4 CrossRefPubMedGoogle Scholar
  20. 20.
    Dewailly E, Dodin S, Verreault R et al (1994) High organochlorine body burden in women with estrogen receptor-positive breast cancer. J Natl Cancer Inst 86:232–234. doi:10.1093/jnci/86.3.232 CrossRefPubMedGoogle Scholar
  21. 21.
    Woolcott CG, Aronson KJ, Hanna WM et al (2001) Organochlorines and breast cancer risk by receptor status, tumor size, and grade (Canada). Cancer Causes Control 12:395–404. doi:10.1023/A:1011289905751 CrossRefPubMedGoogle Scholar
  22. 22.
    Brody JG, Moysich KB, Humblet O, Attfeild KR, Beehler GP, Rudel RA (2007) Environmental pollutants and breast cancer. Cancer 109(12):2667–2711. doi:10.1002/cncr.22655 CrossRefPubMedGoogle Scholar
  23. 23.
    Calafat AM, Kuklenyik Z, Reidy JA, Caudill SP, Ekong J, Needham LL (2005) Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ Health Perspect 113(4):391–395PubMedCrossRefGoogle Scholar
  24. 24.
    Wittassek M, Wiesmuller GA, Koch HM et al (2007) Internal phthalate exposure over the last two decades—a retrospective human biomonitoring study. Int J Hyg Environ Health 210(3–4):319–333. doi:10.1016/j.ijheh.2007.01.037 CrossRefPubMedGoogle Scholar
  25. 25.
    Gouin T, Jantunen L, Harner T, Blanchard P, Bidleman T (2007) Spatial and temporal trends of chiral organochlorine signatures in Great Lakes air using passive air samplers. Environ Sci Technol 41(11):3877–3883. doi:10.1021/es063015r CrossRefPubMedGoogle Scholar
  26. 26.
    Kitada Y, Kawahata H, Suzuki A, Oomori T (2008) Distribution of pesticides and bisphenol A in sediments collected from rivers adjacent to coral reefs. Chemosphere 71(11):2082–2090. doi:10.1016/j.chemosphere.2008.01.025 CrossRefPubMedGoogle Scholar
  27. 27.
    Zhang H, Chai Z, Sun H (2007) Human hair as a potential biomonitor for assessing persistent organic pollutants. Environ Int 33(5):685–693. doi:10.1016/j.envint.2007.02.003 CrossRefPubMedGoogle Scholar
  28. 28.
    Pentamwa P, Oanh NT (2008) Levels of pesticides and polychlorinated biphenyls in selected homes in the Bangkok metropolitan region, Thailand. Ann N Y Acad Sci 1140:91–112CrossRefPubMedGoogle Scholar
  29. 29.
    Jafari A, Moeckel C, Jones KC (2008) Spatial biomonitoring of persistent organic pollutants in Iran: a study using locally produced butter. J Environ Monit 10(7):861–866. doi:10.1039/b802061b CrossRefPubMedGoogle Scholar
  30. 30.
    Kumari B, Singh J, Singh S, Kathpal TS (2005) Monitoring of butter and ghee (clarified butter fat) for pesticidal contamination from cotton belt of Haryana, India. Environ Monit Assess 105(1–3):111–120. doi:10.1007/s10661-005-3159-2 CrossRefPubMedGoogle Scholar
  31. 31.
    Dey S, Soliman AS, Merajver SD (2009) Xenoestrogens may be the cause of high and increasing rates of hormone receptor positive breast cancer in the world. Med Hyp 72(6):652–656CrossRefGoogle Scholar
  32. 32.
    Freedman LS, Edwards BK, Ries LAG (2006) Young JL Cancer incidence in four member countries (Cyprus, Egypt, Israel, and Jordan) of the Middle East Cancer Consortium (MECC) compared with US SEER. National Cancer Institute, US Department of Health and Human Services, National Institutes of Health, Bethesda, MDGoogle Scholar
  33. 33.
    Cancer in Egypt Gharbiah (2007) Triennial Report of 2000–2002. Gharbiah Population-Based Cancer Registry, EgyptGoogle Scholar
  34. 34.
    ERPR pharm DxTM Interpretation Manual. Dako Inc. www.dako.com
  35. 35.
    CAPMAS Census Reports, 1996 and 2006Google Scholar
  36. 36.
    Kelsey JL, Bernstein L (1996) Epidemiology and prevention of breast cancer. Annu Rev Public Health 17:47–67. doi:10.1146/annurev.pu.17.050196.000403 CrossRefPubMedGoogle Scholar
  37. 37.
    El-Zanaty F, Way A (2006) Egypt demographic and health survey 2005. Cairo, Egypt: ministry of health and population, national population council, El-Zanaty and Associates, and ORC MacroGoogle Scholar
  38. 38.
    Soliman AS, Vulimiri SV, Kleiner HE et al (2004) High levels of oxidative DNA damage in lymphocyte DNA of premenopausal breast cancer patients from Egypt. Int J Environ Health Res 14(2):121–134. doi:10.1080/0960312042000209534 CrossRefPubMedGoogle Scholar
  39. 39.
    Fenton SE (2006) Endocrine-disrupting compounds and mammary gland development: early exposure and later life consequences. Endocrinology 147(6):S18–S24. doi:10.1210/en.2005-1131 CrossRefPubMedGoogle Scholar
  40. 40.
    Reya T, Morrison SJ, Clarke MF, Weissman IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414(6859):105–111. doi:10.1038/35102167 CrossRefPubMedGoogle Scholar
  41. 41.
    Marx J (2003) Cancer research. Mutant stem cells may seed cancer. Science 301(5638):1308–1310. doi:10.1126/science.301.5638.1308 CrossRefPubMedGoogle Scholar
  42. 42.
    Singh SK, Clarke ID, Terasaki M et al (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63(18):5821–5828PubMedGoogle Scholar
  43. 43.
    Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100:3983–3988. doi:10.1073/pnas.0530291100 CrossRefPubMedGoogle Scholar
  44. 44.
    Bartow SA (1998) Use of the autopsy to study ontogeny and expression of the estrogen receptor gene in human breast. J Mammary Gland Biol Neoplasia 3:37–48. doi:10.1023/A:1026641401184 CrossRefPubMedGoogle Scholar
  45. 45.
    Keeling JW, Ozere E, King G, Walker F (2000) Oestrogen receptor alpha in female fetal, infant and child mammary tissue. J Pathol 191:449–451. doi:10.1002/1096-9896(2000)9999:9999<::AID-PATH661>3.0.CO;2-# CrossRefPubMedGoogle Scholar
  46. 46.
    Soliman AS, Wang X, DiGiovanni J et al (2003) Serum organochlorine levels and history of lactation in Egypt. Environ Res 92:110–117. doi:10.1016/S0013-9351(02)00056-7 CrossRefPubMedGoogle Scholar
  47. 47.
    Solomon GM, Weiss PM (2002) Chemical contaminants in breast milk: time trends and regional variability. Environ Health Perspect 110:A339–A347PubMedGoogle Scholar
  48. 48.
    LaKind JS, Wilkins AA, Berlin CM (2004) Environmental chemicals in human milk: a review of concentrations, determinants, infant exposures and health, and guidance for future research. Toxicol Appl Pharmacol 198:184–208. doi:10.1016/j.taap.2003.08.021 CrossRefPubMedGoogle Scholar
  49. 49.
    Dontu G, El-Ashry D, Wicha MS (2004) Breast cancer, stem/progenitor cells and the estrogen receptor. Trends Endocrinol Metab 15(5):193–197. doi:10.1016/j.tem.2004.05.011 CrossRefPubMedGoogle Scholar
  50. 50.
    Ciocca DR, Gago FE, Fanelli MA, Calderwood SK (2006) Co-expression of steroid receptors (estrogen receptor alpha and/or progesterone receptors) and Her-2/neu: Clinical implications. J Steroid Biochem Mol Biol 102:32–40. doi:10.1016/j.jsbmb.2006.09.008 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC. 2009

Authors and Affiliations

  • Subhojit Dey
    • 1
  • Amr S. Soliman
    • 1
  • Ahmad Hablas
    • 2
  • Ibrahim A. Seifeldin
    • 3
  • Kadry Ismail
    • 2
  • Mohamed Ramadan
    • 3
  • Hesham El-Hamzawy
    • 3
  • Mark L. Wilson
    • 1
  • Mousumi Banerjee
    • 4
  • Paolo Boffetta
    • 5
  • Joe Harford
    • 6
  • Sofia D. Merajver
    • 7
  1. 1.Department of Epidemiology, School of Public HealthUniversity of MichiganAnn ArborUSA
  2. 2.Gharbiah Cancer SocietyTanta, GharbiahEgypt
  3. 3.Tanta Cancer CenterTanta, GharbiahEgypt
  4. 4.Department of Biostatistics, School of Public HealthUniversity of MichiganAnn ArborUSA
  5. 5.International Agency for Research on CancerLyonFrance
  6. 6.Office of International AffairsNational Cancer InstituteBethesdaUSA
  7. 7.University of Michigan Comprehensive Cancer CenterAnn ArborUSA

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