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The epidemiology of triple-negative breast cancer, including race

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Abstract

Objective

Predictors of intrinsic breast cancer subtypes, including the triple-negative (TN) subtype, are largely unknown. We evaluated whether anthropometrics, demographics, and reproductive history were associated with distinct breast cancer subtypes.

Methods

Invasive breast tumors from a population-based case–control study of 476 (116 black and 360 white) Atlanta women aged 20–54, diagnosed between 1990 and 1992, were centrally reviewed and immunohistochemically analyzed for estrogen receptor (ER), progesterone receptor (PR) and human epidermal growth factor receptor 2 (HER2); then grouped [TN (ER−PR−HER2−); ER−PR−HER2+; ER/PR+HER2+; ER/PR+HER2− (case-only reference group)]. Data were from interviews and anthropometric measurements; adjusted odds ratios (OR) and 95% confidence intervals (CI) were estimated using logistic regression, including both case-only and case-control comparisons.

Results

From the case-only analyses and compared with the ER/PR+HER2− subtype, women with TN tumors were more likely to be obese than normal/underweight [OR = 1.89 (95% CI = 1.22, 2.92)]. Regardless of HER2 status, ER−PR− tumors were associated with black race, young age at first birth, having a recent birth, and being overweight.

Conclusions

Distinct breast cancer subtypes have unique sociodemographic, anthropometric and reproductive characteristics and possibly different pathways for development.

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Abbreviations

TN:

Triple negative

ER:

Estrogen receptor

PR:

Progesterone receptor

HER2:

Human epidermal growth factor receptor 2

WHR:

Waist to hip ratio

BMI:

Body mass index

SES:

Socioeconomic status

SEER:

Surveillance, Epidemiology and End Results

IHC:

Immunohistochemical

References

  1. Sorlie T, Perou CM, Tibshirani R et al (2001) Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A 98:10869–10874. doi:10.1073/pnas.191367098

    Article  PubMed  CAS  Google Scholar 

  2. Sotiriou C, Neo SY, McShane LM et al (2003) Breast cancer classification and prognosis based on gene expression profiles from a population-based study. Proc Natl Acad Sci U S A 100:10393–10398. doi:10.1073/pnas.1732912100

    Article  PubMed  CAS  Google Scholar 

  3. Sorlie T, Wang Y, Xiao C et al (2006) Distinct molecular mechanisms underlying clinically relevant subtypes of breast cancer: gene expression analyses across three different platforms. BMC Genomics 7:127. doi:10.1186/1471-2164-7-127

    Article  PubMed  CAS  Google Scholar 

  4. Carey LA, Perou CM, Livasy CA et al (2006) Race, breast cancer subtypes, and survival in the Carolina breast cancer study. JAMA 295:2492–2502. doi:10.1001/jama.295.21.2492

    Article  PubMed  CAS  Google Scholar 

  5. Perou CM, Sorlie T, Eisen MB et al (2000) Molecular portraits of human breast tumours. Nature 406:747–752. doi:10.1038/35021093

    Article  PubMed  CAS  Google Scholar 

  6. Sotiriou C, Wirapati P, Loi S et al (2006) Gene expression profiling in breast cancer: understanding the molecular basis of histologic grade to improve prognosis. J Natl Cancer Inst 98:262–272

    Article  PubMed  CAS  Google Scholar 

  7. Yang XR, Sherman ME, Rimm DL et al (2007) Differences in risk factors for breast cancer molecular subtypes in a population-based study. Cancer Epidemiol Biomarkers Prev 16:439–443. doi:10.1158/1055-9965.EPI-06-0806

    Article  PubMed  CAS  Google Scholar 

  8. Rakha EA, El-Rehim DA, Paish C et al (2006) Basal phenotype identifies a poor prognostic subgroup of breast cancer of clinical importance. Eur J Cancer 42:3149–3156. doi:10.1016/j.ejca.2006.08.015

    Article  PubMed  CAS  Google Scholar 

  9. Rakha EA, El-Sayed ME, Green AR, Lee AHS, Robertson JF, Ellis IO (2007) Prognostic markers in triple-negative breast cancer. Cancer 109:25–32. doi:10.1002/cncr.22381

    Article  PubMed  CAS  Google Scholar 

  10. Sorlie T (2004) Molecular portraits of breast cancer: tumour subtypes as distinct disease entities. Eur J Cancer 40:2667–2675. doi:10.1016/j.ejca.2004.08.021

    Article  PubMed  CAS  Google Scholar 

  11. Bertucci F, Finetti P, Cervera N et al (2008) How basal are triple-negative breast cancers? Int J Cancer 123:236–240. doi:10.1002/ijc.23518

    Article  PubMed  CAS  Google Scholar 

  12. Lund MJ, Trivers KF, Porter PL et al (2009) Race and triple negative threats to breast cancer survival: a population-based study in Atlanta, GA. Breast Cancer Res Treat 113:357–370. doi:10.1007/s10549-008-9926-3

    Article  PubMed  Google Scholar 

  13. Bauer KR, Brown M, Cress RD, Parise CR, Caggiano V (2007) Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the so-called triple-negative phenotype: a population-based study from the California Cancer Registry. Cancer 109:1721–1728. doi:10.1002/cncr.22618

    Article  PubMed  Google Scholar 

  14. Millikan RC, Newman B, Tse CK et al (2008) Epidemiology of basal-like breast cancer. Breast Cancer Res Treat 109:123–139. doi:10.1007/s10549-007-9632-6

    Article  PubMed  Google Scholar 

  15. Morris GJ, Naidu S, Topham AK et al (2007) Differences in breast carcinoma characteristics in newly diagnosed African–American and Caucasian patients: a single-institution compilation compared with the National Cancer Institute’s surveillance, epidemiology, and end results database. Cancer 110:876–884. doi:10.1002/cncr.22836

    Article  PubMed  Google Scholar 

  16. Stark A, Kapke A, Schultz D, Brown R, Linden M, Raju U (2008) Advanced stages and poorly differentiated grade are associated with an increased risk of HER2/neu positive breast carcinoma only in white women: findings from a prospective cohort study of African–American and white-American women. Breast Cancer Res Treat 107:405–414. doi:10.1007/s10549-007-9560-5

    Article  PubMed  CAS  Google Scholar 

  17. Lund MJ, Butler EN, Bumpers HL et al (2008) High prevalence of triple-negative tumors in an urban cancer center. Cancer 113:608–615. doi:10.1002/cncr.23569

    Article  PubMed  Google Scholar 

  18. Bowen RL, Duffy SW, Ryan DA, Hart IR, Jones JL (2008) Early onset of breast cancer in a group of British black women. Br J Cancer 98:277–281. doi:10.1038/sj.bjc.6604174

    Article  PubMed  CAS  Google Scholar 

  19. Phipps AI, Malone KE, Porter PL, Daling JR, Li CI (2008) Reproductive and hormonal risk factors for postmenopausal luminal, HER-2-overexpressing, and triple-negative breast cancer. Cancer 113:1521–1526. doi:10.1002/cncr.23786

    Article  PubMed  Google Scholar 

  20. Phipps AI, Malone KE, Porter PL, Daling JR, Li CI (2008) Body size and risk of luminal, HER2-overexpressing, and triple-negative breast cancer in postmenopausal women. Cancer Epidemiol Biomarkers Prev 17:2078–2086. doi:10.1158/1055-9965.EPI-08-0206

    Article  PubMed  CAS  Google Scholar 

  21. Brinton LA, Daling JR, Liff JM et al (1995) Oral contraceptives and breast cancer risk among younger women. J Natl Cancer Inst 87:827–835. doi:10.1093/jnci/87.11.827

    Article  PubMed  CAS  Google Scholar 

  22. National Heart Blood Lung Institute (NHLBI) expert panel on the identification, evaluation, treatment of overweight, obesity in adults (1998) Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults: the evidence report. Obes Res 6(suppl 2):51S–209S

    Google Scholar 

  23. Gwyn K, Bondy ML, Cohen DS et al (2004) Racial differences in diagnosis, treatment, and clinical delays in a population-based study of patients with newly diagnosed breast carcinoma. Cancer 1008:1595–1604. doi:10.1002/cncr.20169

    Article  Google Scholar 

  24. American Joint Committee on Cancer (1988) Manual for staging of cancer, 3rd edn. JB Lippincott Company, Philladelphia

    Google Scholar 

  25. Porter PL, Lund MJ, Lin MG et al (2004) Racial differences in expression of cell cycle regulatory proteins in breast cancer: study of young African American and white women in Atlanta. Cancer 100:2533–2542. doi:10.1002/cncr.20279

    Article  PubMed  Google Scholar 

  26. Cattoretti G, Becker MH, Key G et al (1992) Monoclonal antibodies against recombinant parts of the Ki-67 antigen (MIB 1 and MIB 3) detect proliferating cells in microwave-processed formalin-fixed paraffin sections. J Pathol 168:357–363. doi:10.1002/path.1711680404

    Article  PubMed  CAS  Google Scholar 

  27. Gerdes J, Becker MH, Key G, Cattoretti G (1992) Immunohistological detection of tumour growth fraction (Ki-67 antigen) in formalin-fixed and routinely processed tissues (see comment). J Pathol 168:85–86. doi:10.1002/path.1711680114

    Article  PubMed  CAS  Google Scholar 

  28. Hsu SM, Raine L, Fanger H (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures (see comment). J Histochem Cytochem 29:577–580

    PubMed  CAS  Google Scholar 

  29. Hsu SM, Soban E (1982) Color modification of diaminobenzidine (DAB) precipitation by metallic ions and its application for double immunohistochemistry. J Histochem Cytochem 30:1079–1082

    PubMed  CAS  Google Scholar 

  30. Taylor CR, Shi SR, Chaiwun B, Young L, Imam SA, Cote RJ (1994) Strategies for improving the immunohistochemical staining of various intranuclear prognostic markers in formalin-paraffin sections: androgen receptor, estrogen receptor, progesterone receptor, p53 protein, proliferating cell nuclear antigen, and Ki-67 antigen revealed by antigen retrieval techniques (see comment). Hum Pathol 25:263–270. doi:10.1016/0046-8177(94)90198-8

    Article  PubMed  CAS  Google Scholar 

  31. Andersen J, Poulsen HS (1989) Immunohistochemical estrogen receptor determination in paraffin-embedded tissue. Prediction of response to hormonal treatment in advanced breast cancer. Cancer 64:1901–1908. doi:10.1002/1097-0142(19891101)64:9<1901::AID-CNCR2820640924>3.0.CO;2-W

    Article  PubMed  CAS  Google Scholar 

  32. Parl FF, Posey YF (1988) Discrepancies of the biochemical and immunohistochemical estrogen receptor assays in breast cancer. Hum Pathol 19:960–966. doi:10.1016/S0046-8177(88)80013-3

    Article  PubMed  CAS  Google Scholar 

  33. Shousha S, Stamp T, James K, Alaghband-Zadeh J (1990) Immunohistochemical study of oestrogen receptors in breast carcinomas that are biochemically receptor negative. J Clin Pathol 43:239–242. doi:10.1136/jcp.43.3.239

    Article  PubMed  CAS  Google Scholar 

  34. Giri D, Goepel J, Rogers K (1988) Immunohistological demonstration of progesterone receptor in breast carninomas: correlation with radioligand binding assays and oestrogen receptor negative. J Clin Pathol 41:444–447. doi:10.1136/jcp.41.4.444

    Article  PubMed  CAS  Google Scholar 

  35. Press MF, Hung G, Godolphin W, Slamon DJ (1994) Sensitivity of HER-2/neu antibodies in archival tissue samples: potential source of error in immunohistochemical studies of oncogene expression. Cancer Res 54:2771–2777

    PubMed  CAS  Google Scholar 

  36. Birner P, Oberhuber G, Stani J et al (2001) Evaluation of the United States Food and Drug Administration-approved scoring and test system of HER-2 protein expression in breast cancer. Clin Cancer Res 7:1669–1675

    PubMed  CAS  Google Scholar 

  37. Begg CB, Zhang ZF (1994) Statistical analysis of molecular epidemiology studies employing case-series. Cancer Epidemiol Biomarkers Prev 3:173–175

    PubMed  CAS  Google Scholar 

  38. Cheang MC, Voduc D, Bajdik C et al (2008) Basal-like breast cancer defined by five biomarkers has superior prognostic value than triple-negative phenotype. Clin Cancer Res 14:1368–1376. doi:10.1158/1078-0432.CCR-07-1658

    Article  PubMed  CAS  Google Scholar 

  39. Tworoger SS, Eliassen AH, Missmer SA et al (2006) Birthweight and body size throughout life in relation to sex hormones and prolactin concentrations in premenopausal women. Cancer Epidemiol Biomarkers Prev 15:2494–2501. doi:10.1158/1055-9965.EPI-06-0671

    Article  PubMed  CAS  Google Scholar 

  40. Sherman ME, Rimm DL, Yang XR et al (2007) Variation in breast cancer hormone receptor and HER2 levels by etiologic factors: a population-based analysis. Int J Cancer 121:1079–1085. doi:10.1002/ijc.22812

    Article  PubMed  CAS  Google Scholar 

  41. 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 13:1558–1568

    PubMed  CAS  Google Scholar 

  42. Trivers KF, Gammon MD, Abrahamson PE et al (2007) Association between reproductive factors and breast cancer survival in younger women. Breast Cancer Res Treat 103:93–102. doi:10.1007/s10549-006-9346-1

    Article  PubMed  Google Scholar 

  43. Whiteman MK, Hillis SD, Curtis KM, McDonald JA, Wingo PA, Marchbanks PA (2004) Reproductive history and mortality after breast cancer diagnosis. Obstet Gynecol 104:146–154

    PubMed  Google Scholar 

  44. Whiteman MK, Hillis SD, Curtis KM, McDonald JA, Wingo PA, Marchbanks PA (2005) Body mass and mortality after breast cancer diagnosis. Cancer Epidemiol Biomarkers Prev 14(8):2009–2014. doi:10.1158/1055-9965.EPI-05-0106

    Article  PubMed  Google Scholar 

  45. Abrahamson PE, Gammon MD, Lund MJ et al (2006) General and abdominal obesity and survival among young women with breast cancer. Cancer Epidemiol Biomarkers Prev 15:1871–1877. doi:10.1158/1055-9965.EPI-06-0356

    Article  PubMed  Google Scholar 

  46. Ioannidis JP (2005) Why most published research findings are false. PLoS Med 2(8):e124

    Article  PubMed  Google Scholar 

  47. Ries LAG, Melbert D, Krapcho M et al (2006) SEER cancer statistics review, 1975–2004. National Cancer Institute, Bethesda

    Google Scholar 

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Acknowledgments

Supported in part by awards RO1CA64292 (R.J.C., E.W.F., J.W.E., M.J.L.), RO1CA71735 (P.L.P.), the Avon Foundation (M.J.L., P.L.P.), the Glenn Foundation (M.J.L.), the Sindab Endowment (M.J.L.) and the Oak Ridge Institute for Science & Education Research Participation Program at CDC (M.J.L., K.F.T).

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Author notes

  1. Elaine W. Flagg

    Present address: Division of HIV/AIDS Prevention, National Center for HIV/AIDS, Viral Hepatitis, STD and TB Prevention, Centers for Disease Control and Prevention, Atlanta, GA, USA

Authors and Affiliations

  1. Division of Cancer Prevention and Control, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, 4770 Buford Highway, NE, MS K-55, Atlanta, GA, 30341, USA

    Katrina F. Trivers

  2. Department of Epidemiology, Rollins School of Public Health, Emory University, Atlanta, GA, USA

    Mary Jo Lund & Jonathan M. Liff

  3. Hematology and Oncology, Emory University School of Medicine, Atlanta, GA, USA

    Mary Jo Lund & J. William Eley

  4. Winship Cancer Institute, Emory University School of Medicine, Atlanta, GA, USA

    Mary Jo Lund & J. William Eley

  5. Georgia Cancer Center for Excellence at Grady, Emory University, Atlanta, GA, USA

    Mary Jo Lund

  6. Division of Human Biology, Fred Hutchinson Cancer Research Center, Seattle, WA, USA

    Peggy L. Porter

  7. Division of General Medicine, Emory University School of Medicine, Atlanta, GA, USA

    Elaine W. Flagg

  8. National Office of Public Health Genomics, Centers for Disease Control and Prevention, Atlanta, GA, USA

    Ralph J. Coates

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  1. Katrina F. Trivers
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Correspondence to Katrina F. Trivers.

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The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.

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Trivers, K.F., Lund, M.J., Porter, P.L. et al. The epidemiology of triple-negative breast cancer, including race. Cancer Causes Control 20, 1071–1082 (2009). https://doi.org/10.1007/s10552-009-9331-1

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