Skip to main content
Top
Published in: Cancer Causes & Control 2/2016

01-02-2016 | Original paper

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

Authors: Melanie Ruszczyk, Gary Zirpoli, Shicha Kumar, Elisa V. Bandera, Dana H. Bovbjerg, Lina Jandorf, Thaer Khoury, Helena Hwang, Gregory Ciupak, Karen Pawlish, Pepper Schedin, Patricia Masso-Welch, Christine B. Ambrosone, Chi-Chen Hong

Published in: Cancer Causes & Control | Issue 2/2016

Login to get access

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.
Appendix
Available only for authorised users
Literature
1.
go back to reference Wellings SR, Jensen HM (1973) On the origin and progression of ductal carcinoma in the human breast. J Natl Cancer Inst 50:1111–1118PubMed Wellings SR, Jensen HM (1973) On the origin and progression of ductal carcinoma in the human breast. J Natl Cancer Inst 50:1111–1118PubMed
2.
go back to reference 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 14:370–378PubMedCrossRef 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 14:370–378PubMedCrossRef
3.
go back to reference Schedin P, Elias A (2004) Multistep tumorigenesis and the microenvironment. Breast Cancer Res 126:93–101CrossRef Schedin P, Elias A (2004) Multistep tumorigenesis and the microenvironment. Breast Cancer Res 126:93–101CrossRef
4.
go back to reference 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 130:725–734PubMedCrossRef 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 130:725–734PubMedCrossRef
5.
go back to reference 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 91:2020–2028PubMedCrossRef 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 91:2020–2028PubMedCrossRef
6.
go back to reference 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 102:1391–1396PubMedPubMedCentralCrossRef 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 102:1391–1396PubMedPubMedCentralCrossRef
7.
go back to reference Silverberg SG, Chitale AR (1973) Assessment of significance of proportions of intraductal and infiltrating tumor growth in ductal carcinoma of the breast. Cancer 32:830–837PubMedCrossRef Silverberg SG, Chitale AR (1973) Assessment of significance of proportions of intraductal and infiltrating tumor growth in ductal carcinoma of the breast. Cancer 32:830–837PubMedCrossRef
8.
go back to reference 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 35:913–919PubMedCrossRef 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 35:913–919PubMedCrossRef
9.
go back to reference 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) PubMedCrossRef 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) PubMedCrossRef
10.
go back to reference 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 31:2327–2334PubMed 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 31:2327–2334PubMed
11.
go back to reference 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 29:1536–1542PubMedCrossRef 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 29:1536–1542PubMedCrossRef
12.
go back to reference 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 13:385–391PubMedCrossRef 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 13:385–391PubMedCrossRef
13.
go back to reference 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:R87PubMedPubMedCentralCrossRef 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:R87PubMedPubMedCentralCrossRef
15.
go back to reference Barsky SH, Karlin NJ (2006) Mechanisms of disease: breast tumor pathogenesis and the role of the myoepithelial cell. Nat Clin Pract Oncol 3:138–151PubMedCrossRef Barsky SH, Karlin NJ (2006) Mechanisms of disease: breast tumor pathogenesis and the role of the myoepithelial cell. Nat Clin Pract Oncol 3:138–151PubMedCrossRef
16.
go back to reference 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 78:778–788PubMedCrossRef 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 78:778–788PubMedCrossRef
17.
go back to reference 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 20:213–217PubMedCrossRef 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 20:213–217PubMedCrossRef
18.
go back to reference 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):1719–1723PubMed 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):1719–1723PubMed
19.
go back to reference 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 41:980–989PubMedCrossRef 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 41:980–989PubMedCrossRef
20.
go back to reference 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 35:443–455PubMedCrossRef 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 35:443–455PubMedCrossRef
21.
go back to reference 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 38:305–311PubMedCrossRef 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 38:305–311PubMedCrossRef
22.
go back to reference 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 13:1558–1568PubMed 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 13:1558–1568PubMed
23.
go back to reference 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 17:1723–1730PubMedPubMedCentralCrossRef 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 17:1723–1730PubMedPubMedCentralCrossRef
24.
go back to reference 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 152:514–527PubMedCrossRef 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 152:514–527PubMedCrossRef
25.
go back to reference Mahoney MC, Bevers T, Linos E, Willett WC (2008) Opportunities and strategies for breast cancer prevention through risk reduction. CA Cancer J Clin 58:347–371PubMedCrossRef Mahoney MC, Bevers T, Linos E, Willett WC (2008) Opportunities and strategies for breast cancer prevention through risk reduction. CA Cancer J Clin 58:347–371PubMedCrossRef
26.
go back to reference 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 2009:871250PubMedPubMedCentralCrossRef 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 2009:871250PubMedPubMedCentralCrossRef
27.
go back to reference 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 34:287–291PubMedPubMedCentralCrossRef 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 34:287–291PubMedPubMedCentralCrossRef
28.
go back to reference 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 13:71-2288-13-71CrossRef 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 13:71-2288-13-71CrossRef
29.
go back to reference 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 109:123–139PubMedPubMedCentralCrossRef 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 109:123–139PubMedPubMedCentralCrossRef
30.
go back to reference 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 93:364–371PubMedPubMedCentralCrossRef 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 93:364–371PubMedPubMedCentralCrossRef
31.
go back to reference 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 161:40–51PubMedCrossRef 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 161:40–51PubMedCrossRef
32.
go back to reference 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 23:755–764PubMedPubMedCentralCrossRef 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 23:755–764PubMedPubMedCentralCrossRef
33.
go back to reference 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:djv048PubMedPubMedCentralCrossRef 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:djv048PubMedPubMedCentralCrossRef
34.
go back to reference 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:e57361PubMedPubMedCentralCrossRef 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:e57361PubMedPubMedCentralCrossRef
35.
go back to reference 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 17:3319–3324PubMedPubMedCentralCrossRef 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 17:3319–3324PubMedPubMedCentralCrossRef
36.
go back to reference 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 94:606–616PubMedCrossRef 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 94:606–616PubMedCrossRef
37.
go back to reference 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 12:1071–1082PubMedCrossRef 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 12:1071–1082PubMedCrossRef
38.
go back to reference 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:e51446PubMedPubMedCentralCrossRef 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:e51446PubMedPubMedCentralCrossRef
39.
go back to reference 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 119:1683–1689PubMedCrossRef 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 119:1683–1689PubMedCrossRef
40.
go back to reference 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 24:1033–1044PubMedCrossRef 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 24:1033–1044PubMedCrossRef
41.
go back to reference 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 174:661–671PubMedPubMedCentralCrossRef 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 174:661–671PubMedPubMedCentralCrossRef
42.
go back to reference 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 23:473–485CrossRef 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 23:473–485CrossRef
43.
go back to reference 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 20:454–463PubMedPubMedCentralCrossRef 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 20:454–463PubMedPubMedCentralCrossRef
44.
go back to reference 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 16:1795–1802PubMedCrossRef 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 16:1795–1802PubMedCrossRef
45.
go back to reference 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–S37PubMed 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–S37PubMed
46.
go back to reference 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 13:334-2164-13-334CrossRef 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 13:334-2164-13-334CrossRef
47.
go back to reference 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 147:159–165PubMedCrossRef 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 147:159–165PubMedCrossRef
48.
go back to reference 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 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
49.
go back to reference Yang L, Jacobsen KH (2008) A systematic review of the association between breastfeeding and breast cancer. J Womens Health (Larchmt) 17:1635–1645CrossRef Yang L, Jacobsen KH (2008) A systematic review of the association between breastfeeding and breast cancer. J Womens Health (Larchmt) 17:1635–1645CrossRef
50.
go back to reference 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 105:166–174PubMedPubMedCentralCrossRef 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 105:166–174PubMedPubMedCentralCrossRef
51.
go back to reference 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 116:4933–4943PubMedCrossRef 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 116:4933–4943PubMedCrossRef
52.
go back to reference 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 113:1521–1526PubMedPubMedCentralCrossRef 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 113:1521–1526PubMedPubMedCentralCrossRef
53.
go back to reference 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 20:1883–1891PubMedPubMedCentralCrossRef 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 20:1883–1891PubMedPubMedCentralCrossRef
54.
go back to reference 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 25:259–265PubMedPubMedCentralCrossRef 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 25:259–265PubMedPubMedCentralCrossRef
55.
go back to reference 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 22:1853–1861PubMedPubMedCentralCrossRef 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 22:1853–1861PubMedPubMedCentralCrossRef
56.
go back to reference 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 13:831–838PubMedPubMedCentralCrossRef 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 13:831–838PubMedPubMedCentralCrossRef
57.
go back to reference Gray RH, Campbell OM, Apelo R, Eslami SS, Zacur H, Ramos RM, Gehret JC, Labbok MH (1990) Risk of ovulation during lactation. Lancet 335:25–29PubMedCrossRef Gray RH, Campbell OM, Apelo R, Eslami SS, Zacur H, Ramos RM, Gehret JC, Labbok MH (1990) Risk of ovulation during lactation. Lancet 335:25–29PubMedCrossRef
58.
go back to reference 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–936sPubMed 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–936sPubMed
59.
go back to reference 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 135:1299–1303PubMed 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 135:1299–1303PubMed
60.
go back to reference 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 13:5327–5332PubMedCrossRef 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 13:5327–5332PubMedCrossRef
62.
go back to reference Amend K, Hicks D, Ambrosone CB (2006) Breast cancer in African-American women: differences in tumor biology from European-American women. Cancer Res 66:8327–8330PubMedCrossRef Amend K, Hicks D, Ambrosone CB (2006) Breast cancer in African-American women: differences in tumor biology from European-American women. Cancer Res 66:8327–8330PubMedCrossRef
63.
go back to reference 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 101:984–992PubMedPubMedCentralCrossRef 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 101:984–992PubMedPubMedCentralCrossRef
64.
go back to reference 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 101:993–1000PubMedPubMedCentralCrossRef 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 101:993–1000PubMedPubMedCentralCrossRef
65.
go back to reference 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 20:1071–1082PubMedCrossRef 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 20:1071–1082PubMedCrossRef
66.
go back to reference 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 27:4515–4521PubMedPubMedCentralCrossRef 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 27:4515–4521PubMedPubMedCentralCrossRef
Metadata
Title
Breast cancer risk factor associations differ for pure versus invasive carcinoma with an in situ component in case–control and case–case analyses
Authors
Melanie Ruszczyk
Gary Zirpoli
Shicha Kumar
Elisa V. Bandera
Dana H. Bovbjerg
Lina Jandorf
Thaer Khoury
Helena Hwang
Gregory Ciupak
Karen Pawlish
Pepper Schedin
Patricia Masso-Welch
Christine B. Ambrosone
Chi-Chen Hong
Publication date
01-02-2016
Publisher
Springer International Publishing
Published in
Cancer Causes & Control / Issue 2/2016
Print ISSN: 0957-5243
Electronic ISSN: 1573-7225
DOI
https://doi.org/10.1007/s10552-015-0696-z

Other articles of this Issue 2/2016

Cancer Causes & Control 2/2016 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine