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Breast cancer risk factor associations differ for pure versus invasive carcinoma with an in situ component in case–control and case–case analyses

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Abstract

Purpose

Invasive ductal carcinoma (IDC) is diagnosed with or without a ductal carcinoma in situ (DCIS) component. Previous analyses have found significant differences in tumor characteristics between pure IDC lacking DCIS and mixed IDC with DCIS. We will test our hypothesis that pure IDC represents a form of breast cancer with etiology and risk factors distinct from mixed IDC/DCIS.

Methods

We compared reproductive risk factors for breast cancer risk, as well as family and smoking history between 831 women with mixed IDC/DCIS (n = 650) or pure IDC (n = 181), and 1,620 controls, in the context of the Women’s Circle of Health Study (WCHS), a case–control study of breast cancer in African-American and European-American women. Data on reproductive and lifestyle factors were collected during interviews, and tumor characteristics were abstracted from pathology reports. Case–control and case–case analyses were conducted using unconditional logistic regression.

Results

Most risk factors were similarly associated with pure IDC and mixed IDC/DCIS. However, among postmenopausal women, risk of pure IDC was lower in women with body mass index (BMI) 25 to <30 [odds ratio (OR) 0.66; 95 % confidence interval (CI) 0.35–1.23] and BMI ≥ 30 (OR 0.33; 95 % CI 0.18–0.67) compared to women with BMI < 25, with no associations with mixed IDC/DCIS. In case–case analyses, women who breastfed up to 12 months (OR 0.55; 95 % CI 0.32–0.94) or longer (OR 0.47; 95 % CI 0.26–0.87) showed decreased odds of pure IDC than mixed IDC/DCIS compared to those who did not breastfeed.

Conclusions

Associations with some breast cancer risk factors differed between mixed IDC/DCIS and pure IDC, potentially suggesting differential developmental pathways. These findings, if confirmed in a larger study, will provide a better understanding of the developmental patterns of breast cancer and the influence of modifiable risk factors, which in turn could lead to better preventive measures for pure IDC, which have worse disease prognosis compared to mixed IDC/DCIS.

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Abbreviations

IDC:

Invasive ductal carcinoma

DCIS:

Ductal carcinoma in situ

AA:

African-American

WCHS:

Women’s Circle of Health Study

EA:

European-American

BMI:

Body mass index

OR:

Odds ratio

CI:

Confidence interval

ER:

Estrogen receptor

HER2:

Human epidermal growth factor 2

LN:

Lymph node

RPCI:

Roswell Park Cancer Institute

CINJ:

Rutgers Cancer Institute of New Jersey

ISMMSS:

Icahn School of Medicine at Mount Sinai School

OC:

Oral contraceptive

MHT:

Menopausal hormone therapy

HAMLET:

Human milk complex of alpha-lactalbumin and oleic acid

References

  1. Wellings SR, Jensen HM (1973) On the origin and progression of ductal carcinoma in the human breast. J Natl Cancer Inst 50:1111–1118

    PubMed  CAS  Google Scholar 

  2. Allred DC, Wu Y, Mao S, Nagtegaal ID, Lee S, Perou CM, Mohsin SK, O’Connell P, Tsimelzon A, Medina D (2008) Ductal carcinoma in situ and the emergence of diversity during breast cancer evolution. Clin Cancer Res 14:370–378

    Article  PubMed  CAS  Google Scholar 

  3. Schedin P, Elias A (2004) Multistep tumorigenesis and the microenvironment. Breast Cancer Res 126:93–101

    Article  Google Scholar 

  4. Esserman LJ, Shieh Y, Rutgers EJ, Knauer M, Retel VP, Mook S, Glas AM, Moore DH, Linn S, van Leeuwen FE, van ‘t Veer LJ (2011) Impact of mammographic screening on the detection of good and poor prognosis breast cancers. Breast Cancer Res Treat 130:725–734

    Article  PubMed  Google Scholar 

  5. Porter PL, El-Bastawissi AY, Mandelson MT, Lin MG, Khalid N, Watney EA, Cousens L, White D, Taplin S, White E (1999) Breast tumor characteristics as predictors of mammographic detection: comparison of interval- and screen-detected cancers. J Natl Cancer Inst 91:2020–2028

    Article  PubMed  CAS  Google Scholar 

  6. Wong H, Lau S, Yau T, Cheung P, Epstein RJ (2010) Presence of an in situ component is associated with reduced biological aggressiveness of size-matched invasive breast cancer. Br J Cancer 102:1391–1396

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  7. Silverberg SG, Chitale AR (1973) Assessment of significance of proportions of intraductal and infiltrating tumor growth in ductal carcinoma of the breast. Cancer 32:830–837

    Article  PubMed  CAS  Google Scholar 

  8. Logullo AF, Godoy AB, Mourao-Neto M, Simpson AJ, Nishimoto IN, Brentani MM (2002) Presence of ductal carcinoma in situ confers an improved prognosis for patients with T1N0M0 invasive breast carcinoma. Braz J Med Biol Res 35:913–919

    Article  PubMed  CAS  Google Scholar 

  9. Chagpar AB, McMasters KM, Sahoo S, Edwards MJ (2009) Does ductal carcinoma in situ accompanying invasive carcinoma affect prognosis? Surgery 146:561–567 (discussion 567–568)

    Article  PubMed  Google Scholar 

  10. Jiang L, Ma T, Moran MS, Kong X, Li X, Haffty BG, Yang Q (2011) Mammographic features are associated with clinicopathological characteristics in invasive breast cancer. Anticancer Res 31:2327–2334

    PubMed  CAS  Google Scholar 

  11. Wong H, Lau S, Leung R, Chiu J, Cheung P, Wong TT, Liang R, Epstein RJ, Yau T (2012) Coexisting ductal carcinoma in situ independently predicts lower tumor aggressiveness in node-positive luminal breast cancer. Med Oncol 29:1536–1542

    Article  PubMed  CAS  Google Scholar 

  12. Kim JY, Han W, Moon HG, Park IA, Ahn SK, Kim J, Lee JW, Kim T, Kim MK, Noh DY (2013) Grade of ductal carcinoma in situ accompanying infiltrating ductal carcinoma as an independent prognostic factor. Clin Breast Cancer 13:385–391

    Article  PubMed  Google Scholar 

  13. Castro NP, Osorio CA, Torres C, Bastos EP, Mourao-Neto M, Soares FA, Brentani HP, Carraro DM (2008) Evidence that molecular changes in cells occur before morphological alterations during the progression of breast ductal carcinoma. Breast Cancer Res 10:R87

    Article  PubMed  PubMed Central  Google Scholar 

  14. Lakhani SR, O’Hare MJ (2001) The mammary myoepithelial cell—cinderella or ugly sister? Breast Cancer Res 3:1–4

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  15. Barsky SH, Karlin NJ (2006) Mechanisms of disease: breast tumor pathogenesis and the role of the myoepithelial cell. Nat Clin Pract Oncol 3:138–151

    Article  PubMed  CAS  Google Scholar 

  16. Black MM, Zachrau RE, Hankey BF, Feuer EJ (1996) Prognostic significance of in situ carcinoma associated with invasive breast carcinoma. A natural experiment in cancer immunology? Cancer 78:778–788

    Article  PubMed  CAS  Google Scholar 

  17. Carabias-Meseguer P, Zapardiel I, Cusidó-Gimferrer M, Godoy-Tundidor S, Tresserra-Casas F, Rodriguez-García I, Fábregas-Xauradó R, Xercavins-Montosa J (2013) Influence of the in situ component in 389 infiltrating ductal breast carcinomas. Breast Cancer 20:213–217

    Article  PubMed  Google Scholar 

  18. Mylonas I, Makovitzky J, Jeschke U, Briese V, Friese K, Gerber B (2005) Expression of Her2/neu, steroid receptors (ER and PR), Ki67 and p53 in invasive mammary ductal carcinoma associated with ductal carcinoma in situ (DCIS) versus invasive breast cancer alone. Anticancer Res 25(3A):1719–1723

    PubMed  CAS  Google Scholar 

  19. Gonzalez LO, Junquera S, del Casar JM, Gonzalez L, Marin L, Gonzalez-Reyes S, Andicoechea A, Gonzalez-Fernandez R, Gonzalez JM, Perez-Fernandez R, Vizoso FJ (2010) Immunohistochemical study of matrix metalloproteinases and their inhibitors in pure and mixed invasive and in situ ductal carcinomas of the breast. Hum Pathol 41:980–989

    Article  PubMed  CAS  Google Scholar 

  20. Lebeau A, Muller-Aufdemkamp C, Allmacher C, Sauer U, Nerlich A, Lichtinghagen R, Lohrs U (2004) Cellular protein and mRNA expression patterns of matrix metalloproteinases-2, -3 and -9 in human breast cancer: correlation with tumour growth. J Mol Histol 35:443–455

    Article  PubMed  CAS  Google Scholar 

  21. Lambe M, Hsieh CC, Chan HW, Ekbom A, Trichopoulos D, Adami HO (1996) Parity, age at first and last birth, and risk of breast cancer: a population-based study in Sweden. Breast Cancer Res Treat 38:305–311

    Article  PubMed  CAS  Google Scholar 

  22. 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 

  23. Lord SJ, Bernstein L, Johnson KA, Malone KE, McDonald JA, Marchbanks PA, Simon MS, Strom BL, Press MF, Folger SG, Burkman RT, Deapen D, Spirtas R, Ursin G (2008) Breast cancer risk and hormone receptor status in older women by parity, age of first birth, and breastfeeding: a case-control study. Cancer Epidemiol Biomarkers Prev 17:1723–1730

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  24. Van Den Brandt PA, Spiegelman D, Yaun SS, Adami HO, Beeson L, Folsom AR, Fraser G, Goldbohm RA, Graham S, Kushi L, Marshall JR, Miller AB, Rohan T, Smith-Warner SA, Speizer FE, Willett WC, Wolk A, Hunter DJ (2000) Pooled analysis of prospective cohort studies on height, weight, and breast cancer risk. Am J Epidemiol 152:514–527

    Article  PubMed  Google Scholar 

  25. Mahoney MC, Bevers T, Linos E, Willett WC (2008) Opportunities and strategies for breast cancer prevention through risk reduction. CA Cancer J Clin 58:347–371

    Article  PubMed  Google Scholar 

  26. Ambrosone CB, Ciupak GL, Bandera EV, Jandorf L, Bovbjerg DH, Zirpoli G, Pawlish K, Godbold J, Furberg H, Fatone A, Valdimarsdottir H, Yao S, Li Y, Hwang H, Davis W, Roberts M, Sucheston L, Demissie K, Amend KL, Tartter P, Reilly J, Pace BW, Rohan T, Sparano J, Raptis G, Castaldi M, Estabrook A, Feldman S, Weltz C, Kemeny M (2009) Conducting molecular epidemiological research in the age of HIPAA: a multi-institutional case-control study of breast cancer in African-American and European-American women. J Oncol 2009:871250

    Article  PubMed  PubMed Central  Google Scholar 

  27. Ruiz-Narvaez EA, Rosenberg L, Yao S, Rotimi CN, Cupples AL, Bandera EV, Ambrosone CB, Adams-Campbell LL, Palmer JR (2013) Fine-mapping of the 6q25 locus identifies a novel SNP associated with breast cancer risk in African-American women. Carcinogenesis 34:287–291

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  28. Bandera EV, Chandran U, Zirpoli G, McCann SE, Ciupak G, Ambrosone CB (2013) Rethinking sources of representative controls for the conduct of case-control studies in minority populations. BMC Med Res Methodol 13:71-2288-13-71

    Article  Google Scholar 

  29. Millikan RC, Newman B, Tse CK, Moorman PG, Conway K, Dressler LG, Smith LV, Labbok MH, Geradts J, Bensen JT, Jackson S, Nyante S, Livasy C, Carey L, Earp HS, Perou CM (2008) Epidemiology of basal-like breast cancer. Breast Cancer Res Treat 109:123–139

    Article  PubMed  PubMed Central  Google Scholar 

  30. Ursin G, Bernstein L, Lord SJ, Karim R, Deapen D, Press MF, Daling JR, Norman SA, Liff JM, Marchbanks PA, Folger SG, Simon MS, Strom BL, Burkman RT, Weiss LK, Spirtas R (2005) Reproductive factors and subtypes of breast cancer defined by hormone receptor and histology. Br J Cancer 93:364–371

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  31. Hall IJ, Moorman PG, Millikan RC, Newman B (2005) Comparative analysis of breast cancer risk factors among African-American women and White women. Am J Epidemiol 161:40–51

    Article  PubMed  Google Scholar 

  32. Beaber EF, Malone KE, Tang MT, Barlow WE, Porter PL, Daling JR, Li CI (2014) Oral contraceptives and breast cancer risk overall and by molecular subtype among young women. Cancer Epidemiol Biomarkers Prev 23:755–764

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  33. Kohler BA, Sherman RL, Howlader N, Jemal A, Ryerson AB, Henry KA, Boscoe FP, Cronin KA, Lake A, Noone AM, Henley SJ, Eheman CR, Anderson RN, Penberthy L (2015) Annual report to the nation on the status of cancer, 1975–2011, featuring incidence of breast cancer subtypes by race/ethnicity, poverty, and state. J Natl Cancer Inst 107:djv048

    Article  PubMed  PubMed Central  Google Scholar 

  34. Starks AM, Martin DN, Dorsey TH, Boersma BJ, Wallace TA, Ambs S (2013) Household income is associated with the p53 mutation frequency in human breast tumors. PLoS ONE 8:e57361

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  35. Vona-Davis L, Rose DP, Hazard H, Howard-McNatt M, Adkins F, Partin J, Hobbs G (2008) Triple-negative breast cancer and obesity in a rural Appalachian population. Cancer Epidemiol Biomarkers Prev 17:3319–3324

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  36. Key T, Appleby P, Barnes I, Reeves G (2002) Endogenous Hormones and Breast Cancer Collaborative Group. Endogenous sex hormones and breast cancer in postmenopausal women: reanalysis of nine prospective studies. J Natl Cancer Inst 94:606–616

    Article  PubMed  CAS  Google Scholar 

  37. Kaaks R, Rinaldi S, Key TJ, Berrino F, Peeters PH, Biessy C, Dossus L, Lukanova A, Bingham S, Khaw KT, Allen NE, Bueno-de-Mesquita HB, van Gils CH, Grobbee D, Boeing H, Lahmann PH, Nagel G, Chang-Claude J, Clavel-Chapelon F, Fournier A, Thiebaut A, Gonzalez CA, Quiros JR, Tormo MJ, Ardanaz E, Amiano P, Krogh V, Palli D, Panico S, Tumino R, Vineis P, Trichopoulou A, Kalapothaki V, Trichopoulos D, Ferrari P, Norat T, Saracci R, Riboli E (2005) Postmenopausal serum androgens, oestrogens and breast cancer risk: the European prospective investigation into cancer and nutrition. Endocr Relat Cancer 12:1071–1082

    Article  PubMed  CAS  Google Scholar 

  38. Cheraghi Z, Poorolajal J, Hashem T, Esmailnasab N, Doosti Irani A (2012) Effect of body mass index on breast cancer during premenopausal and postmenopausal periods: a meta-analysis. PLoS ONE 7:e51446

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  39. Suzuki R, Rylander-Rudqvist T, Ye W, Saji S, Wolk A (2006) Body weight and postmenopausal breast cancer risk defined by estrogen and progesterone receptor status among Swedish women: a prospective cohort study. Int J Cancer 119:1683–1689

    Article  PubMed  CAS  Google Scholar 

  40. Kawai M, Kakugawa Y, Nishino Y, Hamanaka Y, Ohuchi N, Minami Y (2013) Anthropometric factors, physical activity, and breast cancer risk in relation to hormone receptor and menopausal status in Japanese women: a case-control study. Cancer Causes Control 24:1033–1044

    Article  PubMed  Google Scholar 

  41. Bao PP, Shu XO, Gao YT, Zheng Y, Cai H, Deming SL, Ruan ZX, Su Y, Gu K, Lu W, Zheng W (2011) Association of hormone-related characteristics and breast cancer risk by estrogen receptor/progesterone receptor status in the Shanghai breast cancer study. Am J Epidemiol 174:661–671

    Article  PubMed  PubMed Central  Google Scholar 

  42. Canchola AJ, Anton-Culver H, Bernstein L, Clarke CA, Henderson K, Ma H, Ursin G, Horn-Ross PL (2012) Body size and the risk of postmenopausal breast cancer subtypes in the California teachers study cohort. Cancer Causes Control 23:473–485

    Article  Google Scholar 

  43. Phipps AI, Chlebowski RT, Prentice R, McTiernan A, Stefanick ML, Wactawski-Wende J, Kuller LH, Adams-Campbell LL, Lane D, Vitolins M, Kabat GC, Rohan TE, Li CI (2011) Body size, physical activity, and risk of triple-negative and estrogen receptor-positive breast cancer. Cancer Epidemiol Biomarkers Prev 20:454–463

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  44. Palmer JR, Adams-Campbell LL, Boggs DA, Wise LA, Rosenberg L (2007) A prospective study of body size and breast cancer in Black women. Cancer Epidemiol Biomarkers Prev 16:1795–1802

    Article  PubMed  Google Scholar 

  45. Shetty PS, Soares MJ, James WP (1994) Body mass index: its relationship to basal metabolic rates and energy requirements. Eur J Clin Nutr 48:S28–S37

    PubMed  Google Scholar 

  46. Budczies J, Denkert C, Muller BM, Brockmoller SF, Klauschen F, Gyorffy B, Dietel M, Richter-Ehrenstein C, Marten U, Salek RM, Griffin JL, Hilvo M, Oresic M, Wohlgemuth G, Fiehn O (2012) Remodeling of central metabolism in invasive breast cancer compared to normal breast tissue—a GC-TOFMS based metabolomics study. BMC Genom 13:334-2164-13-334

    Article  Google Scholar 

  47. Berrino F, Villarini A, Traina A, Bonanni B, Panico S, Mano MP, Mercandino A, Galasso R, Barbero M, Simeoni M, Bassi MC, Consolaro E, Johansson H, Zarcone M, Bruno E, Gargano G, Venturelli E, Pasanisi P (2014) Metabolic syndrome and breast cancer prognosis. Breast Cancer Res Treat 147:159–165

    Article  PubMed  Google Scholar 

  48. Collaborative Group on Hormonal Factors in Breast Cancer (2002) 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 360(187–195):41

    Google Scholar 

  49. Yang L, Jacobsen KH (2008) A systematic review of the association between breastfeeding and breast cancer. J Womens Health (Larchmt) 17:1635–1645

    Article  Google Scholar 

  50. Faupel-Badger JM, Arcaro KF, Balkam JJ, Eliassen AH, Hassiotou F, Lebrilla CB, Michels KB, Palmer JR, Schedin P, Stuebe AM, Watson CJ, Sherman ME (2013) Postpartum remodeling, lactation, and breast cancer risk: summary of a National Cancer Institute-sponsored workshop. J Natl Cancer Inst 105:166–174

    Article  PubMed  PubMed Central  Google Scholar 

  51. Shinde SS, Forman MR, Kuerer HM, Yan K, Peintinger F, Hunt KK, Hortobagyi GN, Pusztai L, Symmans WF (2010) Higher parity and shorter breastfeeding duration: association with triple-negative phenotype of breast cancer. Cancer 116:4933–4943

    Article  PubMed  Google Scholar 

  52. 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

    Article  PubMed  PubMed Central  Google Scholar 

  53. Palmer JR, Boggs DA, Wise LA, Ambrosone CB, Adams-Campbell LL, Rosenberg L (2011) Parity and lactation in relation to estrogen receptor negative breast cancer in African American women. Cancer Epidemiol Biomarkers Prev 20:1883–1891

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  54. Ambrosone CB, Zirpoli G, Ruszczyk M, Shankar J, Hong CC, Roberts M, Yao S, McCann SE, Ciupak G, Hwang H, Khoury T, Jandorf L, Bovbjerg DH, Pawlish K, Bandera EV (2014) Parity and breastfeeding among African-American women: differential effects on breast cancer risk by estrogen and progesterone receptor status in the Women’s Circle of Health Study. Cancer Causes Control 25:259–265

    Article  PubMed  PubMed Central  Google Scholar 

  55. Martinez ME, Wertheim BC, Natarajan L, Schwab R, Bondy M, Daneri-Navarro A, Meza-Montenegro MM, Gutierrez-Milan LE, Brewster A, Komenaka IK, Thompson PA (2013) Reproductive factors, heterogeneity, and breast tumor subtypes in women of Mexican descent. Cancer Epidemiol Biomarkers Prev 22:1853–1861

    Article  PubMed  PubMed Central  Google Scholar 

  56. Clavel-Chapelon F, E3 N Group (2002) Cumulative number of menstrual cycles and breast cancer risk: results from the E3 N cohort study of French women. Cancer Causes Control 13:831–838

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  57. Gray RH, Campbell OM, Apelo R, Eslami SS, Zacur H, Ramos RM, Gehret JC, Labbok MH (1990) Risk of ovulation during lactation. Lancet 335:25–29

    Article  PubMed  CAS  Google Scholar 

  58. Russo J, Mailo D, Hu YF, Balogh G, Sheriff F, Russo IH (2005) Breast differentiation and its implication in cancer prevention. Clin Cancer Res 11:931s–936s

    PubMed  CAS  Google Scholar 

  59. Gustafsson L, Hallgren O, Mossberg AK, Pettersson J, Fischer W, Aronsson A, Svanborg C (2005) HAMLET kills tumor cells by apoptosis: structure, cellular mechanisms, and therapy. J Nutr 135:1299–1303

    PubMed  CAS  Google Scholar 

  60. Do Carmo Franca-Botelho A, Ferreira MC, Franca JL, Franca EL, Honorio-Franca AC (2012) Breastfeeding and its relationship with reduction of breast cancer: a review. Asian Pac J Cancer Prev 13:5327–5332

    Article  PubMed  Google Scholar 

  61. Lyons TR, Schedin PJ, Borges VF (2009) Pregnancy and breast cancer: when they collide. J Mammary Gland Biol Neoplasia 14:87–98

    Article  PubMed  PubMed Central  Google Scholar 

  62. Amend K, Hicks D, Ambrosone CB (2006) Breast cancer in African-American women: differences in tumor biology from European-American women. Cancer Res 66:8327–8330

    Article  PubMed  CAS  Google Scholar 

  63. Albain KS, Unger JM, Crowley JJ, Coltman CA Jr, Hershman DL (2009) Racial disparities in cancer survival among randomized clinical trials patients of the Southwest Oncology Group. J Natl Cancer Inst 101:984–992

    Article  PubMed  PubMed Central  Google Scholar 

  64. Menashe I, Anderson WF, Jatoi I, Rosenberg PS (2009) Underlying causes of the black-white racial disparity in breast cancer mortality: a population-based analysis. J Natl Cancer Inst 101:993–1000

    Article  PubMed  PubMed Central  Google Scholar 

  65. Trivers KF, Lund MJ, Porter PL, Liff JM, Flagg EW, Coates RJ, Eley JW (2009) The epidemiology of triple-negative breast cancer, including race. Cancer Causes Control 20:1071–1082

    Article  PubMed  Google Scholar 

  66. Huo D, Ikpatt F, Khramtsov A, Dangou JM, Nanda R, Dignam J, Zhang B, Grushko T, Zhang C, Oluwasola O, Malaka D, Malami S, Odetunde A, Adeoye AO, Iyare F, Falusi A, Perou CM, Olopade OI (2009) Population differences in breast cancer: survey in indigenous African women reveals over-representation of triple-negative breast cancer. J Clin Oncol 27:4515–4521

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by grants from the US Army Medical Research and Material Command (DAMD-17-01-1-0334) (to D.H. Bovbjerg and C.B. Ambrosone), the National Cancer Institute (R03 CA17106 to C.B. Ambrosone; R01 CA100598 to C.B. Ambrosone; P01 CA151135 to C.B. Ambrosone, J.R. Palmer, and A.F. Olshan; K22 CA138563 to E.V. Bandera; P30 CA072720 to Roswell Park Cancer Institute; P30 CA016056 to Rutgers Cancer Institute of NJ), the Breast Cancer Research Foundation (to C.B. Ambrosone), and a gift from the Philip L. Hubbell family (to C.B. Ambrosone). The New Jersey State Cancer Registry (NJSCR) is a participant in the Centers for Disease Control and Prevention’s National Program of Cancer Registries and is a National Cancer Institute’s Surveillance, Epidemiology, and End Results (SEER) Expansion Registry. The NJSCR is supported by the Centers for Disease Control and Prevention under cooperative agreement 5U58DP003931-02 awarded to the New Jersey Department of Health. The collection of New Jersey cancer incidence data is also supported by the National Cancer Institute’s SEER Program under contract N01PC-2013-00021 and the State of New Jersey. The funding agents played no role in the study design, data collection, analysis, and interpretation of data or in the writing of the manuscript for publication.

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Correspondence to Chi-Chen Hong.

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WCHS protocols for agreement to participate and informed consent were approved by the institutional review boards at Roswell Park Cancer Institute (RPCI), Rutgers Cancer Institute of New Jersey (CINJ), Icahn School of Medicine at Mount Sinai School (ISMMSS, formerly the Mount Sinai School of Medicine), and the participating hospitals in NYC in compliance with the Declaration of Helsinki.

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The authors declare that they have no competing interests.

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Ruszczyk, M., Zirpoli, G., Kumar, S. et al. Breast cancer risk factor associations differ for pure versus invasive carcinoma with an in situ component in case–control and case–case analyses. Cancer Causes Control 27, 183–198 (2016). https://doi.org/10.1007/s10552-015-0696-z

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