Skip to main content
Top
Published in: Breast Cancer Research 1/2021

01-12-2021 | Breast Disease | Research article

Risk factors for breast cancer development by tumor characteristics among women with benign breast disease

Authors: Jonine D. Figueroa, Gretchen L. Gierach, Máire A. Duggan, Shaoqi Fan, Ruth M. Pfeiffer, Yihong Wang, Roni T. Falk, Olivier Loudig, Mustapha Abubakar, Mindy Ginsberg, Teresa M. Kimes, Kathryn Richert-Boe, Andrew G. Glass, Thomas E. Rohan

Published in: Breast Cancer Research | Issue 1/2021

Login to get access

Abstract

Background

Among women diagnosed with invasive breast cancer, 30% have a prior diagnosis of benign breast disease (BBD). Thus, it is important to identify factors among BBD patients that elevate invasive cancer risk. In the general population, risk factors differ in their associations by clinical pathologic features; however, whether women with BBD show etiologic heterogeneity in the types of breast cancers they develop remains unknown.

Methods

Using a nested case-control study of BBD and breast cancer risk conducted in a community healthcare plan (Kaiser Permanente Northwest), we assessed relationships of histologic features in BBD biopsies and patient characteristics with subsequent breast cancer risk and tested for heterogeneity of associations by estrogen receptor (ER) status, tumor grade, and size. The study included 514 invasive breast cancer cases (median follow-up of 9 years post-BBD diagnosis) and 514 matched controls, diagnosed with proliferative or non-proliferative BBD between 1971 and 2006, with follow-up through mid-2015. Odds ratios (ORs) and 95% confidence intervals (CIs) were obtained using multivariable polytomous logistic regression models.

Results

Breast cancers were predominantly ER-positive (86%), well or moderately differentiated (73%), small (74% < 20 mm), and stage I/II (91%). Compared to patients with non-proliferative BBD, proliferative BBD with atypia conferred increased risk for ER-positive cancer (OR = 5.48, 95% CI = 2.14–14.01) with only one ER-negative case, P-heterogeneity = 0.45. The presence of columnar cell lesions (CCLs) at BBD diagnosis was associated with a 1.5-fold increase in the risk of both ER-positive and ER-negative tumors, with a 2-fold increase (95% CI = 1.21–3.58) observed among postmenopausal women (56%), independent of proliferative BBD status with and without atypia. We did not identify statistically significant differences in risk factor associations by tumor grade or size.

Conclusion

Most tumors that developed after a BBD diagnosis in this cohort were highly treatable low-stage ER-positive tumors. CCL in BBD biopsies may be associated with moderately increased risk, independent of BBD histology, and irrespective of ER status.
Appendix
Available only for authorised users
Literature
1.
go back to reference Dupont WD, Page DL. Risk factors for breast cancer in women with proliferative breast disease. N Engl J Med. 1985;312(3):146–51.PubMedCrossRef Dupont WD, Page DL. Risk factors for breast cancer in women with proliferative breast disease. N Engl J Med. 1985;312(3):146–51.PubMedCrossRef
2.
go back to reference Allison KH, Abraham LA, Weaver DL, Tosteson AN, Nelson HD, Onega T, Geller BM, Kerlikowske K, Carney PA, Ichikawa LE, Buist DS, Elmore JG. Trends in breast biopsy pathology diagnoses among women undergoing mammography in the United States: a report from the Breast Cancer Surveillance Consortium. Cancer. 2015;121(9):1369–78. https://doi.org/10.1002/cncr.29199. Allison KH, Abraham LA, Weaver DL, Tosteson AN, Nelson HD, Onega T, Geller BM, Kerlikowske K, Carney PA, Ichikawa LE, Buist DS, Elmore JG. Trends in breast biopsy pathology diagnoses among women undergoing mammography in the United States: a report from the Breast Cancer Surveillance Consortium. Cancer. 2015;121(9):1369–78. https://​doi.​org/​10.​1002/​cncr.​29199.
3.
go back to reference Neal L, Sandhu NP, Hieken TJ, Glazebrook KN, Mac Bride MB, Dilaveri CA, Wahner-Roedler DL, Ghosh K, Visscher DW. Diagnosis and management of benign, atypical, and indeterminate breast lesions detected on core needle biopsy. Mayo Clin Proc. 2014;89(4):536–47.PubMedCrossRef Neal L, Sandhu NP, Hieken TJ, Glazebrook KN, Mac Bride MB, Dilaveri CA, Wahner-Roedler DL, Ghosh K, Visscher DW. Diagnosis and management of benign, atypical, and indeterminate breast lesions detected on core needle biopsy. Mayo Clin Proc. 2014;89(4):536–47.PubMedCrossRef
4.
go back to reference Hartmann LC, Degnim AC, Santen RJ, Dupont WD, Ghosh K. Atypical hyperplasia of the breast--risk assessment and management options. N Engl J Med. 2015;372(1):78–89.PubMedPubMedCentralCrossRef Hartmann LC, Degnim AC, Santen RJ, Dupont WD, Ghosh K. Atypical hyperplasia of the breast--risk assessment and management options. N Engl J Med. 2015;372(1):78–89.PubMedPubMedCentralCrossRef
5.
go back to reference Cuzick J, Sestak I, Thorat MA. Impact of preventive therapy on the risk of breast cancer among women with benign breast disease. Breast. 2015;24(Suppl 2):S51–5.PubMedPubMedCentralCrossRef Cuzick J, Sestak I, Thorat MA. Impact of preventive therapy on the risk of breast cancer among women with benign breast disease. Breast. 2015;24(Suppl 2):S51–5.PubMedPubMedCentralCrossRef
6.
go back to reference Pankratz VS, Degnim AC, Frank RD, Frost MH, Visscher DW, Vierkant RA, Hieken TJ, Ghosh K, Tarabishy Y, Vachon CM, Radisky DC, Hartmann LC. Model for individualized prediction of breast cancer risk after a benign breast biopsy. J Clin Oncol. 2015;33(8):923–9.PubMedPubMedCentralCrossRef Pankratz VS, Degnim AC, Frank RD, Frost MH, Visscher DW, Vierkant RA, Hieken TJ, Ghosh K, Tarabishy Y, Vachon CM, Radisky DC, Hartmann LC. Model for individualized prediction of breast cancer risk after a benign breast biopsy. J Clin Oncol. 2015;33(8):923–9.PubMedPubMedCentralCrossRef
7.
go back to reference Arthur R, Wang Y, Ye K, Glass AG, Ginsberg M, Loudig O, Rohan T. Association between lifestyle, menstrual/reproductive history, and histological factors and risk of breast cancer in women biopsied for benign breast disease. Breast Cancer Res Treat. 2017;165(3):623–31.PubMedPubMedCentralCrossRef Arthur R, Wang Y, Ye K, Glass AG, Ginsberg M, Loudig O, Rohan T. Association between lifestyle, menstrual/reproductive history, and histological factors and risk of breast cancer in women biopsied for benign breast disease. Breast Cancer Res Treat. 2017;165(3):623–31.PubMedPubMedCentralCrossRef
8.
go back to reference Kabat GC, Jones JG, Olson N, Negassa A, Duggan C, Ginsberg M, Kandel RA, Glass AG, Rohan TE. A multi-center prospective cohort study of benign breast disease and risk of subsequent breast cancer. Cancer Causes Control. 2010;21(6):821–8.PubMedPubMedCentralCrossRef Kabat GC, Jones JG, Olson N, Negassa A, Duggan C, Ginsberg M, Kandel RA, Glass AG, Rohan TE. A multi-center prospective cohort study of benign breast disease and risk of subsequent breast cancer. Cancer Causes Control. 2010;21(6):821–8.PubMedPubMedCentralCrossRef
9.
go back to reference Palmer JR, Boggs DA, Wise LA, Ambrosone CB, Adams-Campbell LL, Rosenberg L. Parity and lactation in relation to estrogen receptor negative breast cancer in African American women. Cancer Epidemiol Biomark Prev. 2011;20(9):1883–91.CrossRef Palmer JR, Boggs DA, Wise LA, Ambrosone CB, Adams-Campbell LL, Rosenberg L. Parity and lactation in relation to estrogen receptor negative breast cancer in African American women. Cancer Epidemiol Biomark Prev. 2011;20(9):1883–91.CrossRef
11.
go back to reference Sighoko D, Ogundiran T, Ademola A, Adebamowo C, Chen L, Odedina S, Anetor I, Ndom P, Gakwaya A, Ojengbede O, Huo D, Olopade OI. Breast cancer risk after full-term pregnancies among African women from Nigeria, Cameroon, and Uganda. Cancer. 2015;121(13):2237–43. https://doi.org/10.1002/cncr.29305. Sighoko D, Ogundiran T, Ademola A, Adebamowo C, Chen L, Odedina S, Anetor I, Ndom P, Gakwaya A, Ojengbede O, Huo D, Olopade OI. Breast cancer risk after full-term pregnancies among African women from Nigeria, Cameroon, and Uganda. Cancer. 2015;121(13):2237–43. https://​doi.​org/​10.​1002/​cncr.​29305.
12.
go back to reference Yang XR, Chang-Claude J, Goode EL, Couch FJ, Nevanlinna H, Milne RL, Gaudet M, Schmidt MK, Broeks A, Cox A, Fasching PA, Hein R, Spurdle AB, Blows F, Driver K, Flesch-Janys D, Heinz J, Sinn P, Vrieling A, Heikkinen T, Aittomaki K, Heikkila P, Blomqvist C, Lissowska J, Peplonska B, Chanock S, Figueroa J, Brinton L, Hall P, Czene K, Humphreys K, Darabi H, Liu J, Van ‘t Veer LJ, van Leeuwen FE, Andrulis IL, Glendon G, Knight JA, Mulligan AM, O’Malley FP, Weerasooriya N, John EM, Beckmann MW, Hartmann A, Weihbrecht SB, Wachter DL, Jud SM, Loehberg CR, Baglietto L, English DR, Giles GG, McLean CA, Severi G, Lambrechts D, Vandorpe T, Weltens C, Paridaens R, Smeets A, Neven P, Wildiers H, Wang X, Olson JE, Cafourek V, Fredericksen Z, Kosel M, Vachon C, Cramp HE, Connley D, Cross SS, Balasubramanian SP, Reed MW, Dork T, Bremer M, Meyer A, Karstens JH, Ay A, Park-Simon TW, Hillemanns P, Arias Perez JI, Menendez Rodriguez P, Zamora P, Benitez J, Ko YD, Fischer HP, Hamann U, Pesch B, Bruning T, Justenhoven C, Brauch H, Eccles DM, Tapper WJ, Gerty SM, Sawyer EJ, Tomlinson IP, Jones A, Kerin M, Miller N, McInerney N, Anton-Culver H, Ziogas A, et al. Associations of breast cancer risk factors with tumor subtypes: a pooled analysis from the Breast Cancer Association Consortium studies. J Natl Cancer Inst. 2011;103(3):250–63.PubMedCrossRef Yang XR, Chang-Claude J, Goode EL, Couch FJ, Nevanlinna H, Milne RL, Gaudet M, Schmidt MK, Broeks A, Cox A, Fasching PA, Hein R, Spurdle AB, Blows F, Driver K, Flesch-Janys D, Heinz J, Sinn P, Vrieling A, Heikkinen T, Aittomaki K, Heikkila P, Blomqvist C, Lissowska J, Peplonska B, Chanock S, Figueroa J, Brinton L, Hall P, Czene K, Humphreys K, Darabi H, Liu J, Van ‘t Veer LJ, van Leeuwen FE, Andrulis IL, Glendon G, Knight JA, Mulligan AM, O’Malley FP, Weerasooriya N, John EM, Beckmann MW, Hartmann A, Weihbrecht SB, Wachter DL, Jud SM, Loehberg CR, Baglietto L, English DR, Giles GG, McLean CA, Severi G, Lambrechts D, Vandorpe T, Weltens C, Paridaens R, Smeets A, Neven P, Wildiers H, Wang X, Olson JE, Cafourek V, Fredericksen Z, Kosel M, Vachon C, Cramp HE, Connley D, Cross SS, Balasubramanian SP, Reed MW, Dork T, Bremer M, Meyer A, Karstens JH, Ay A, Park-Simon TW, Hillemanns P, Arias Perez JI, Menendez Rodriguez P, Zamora P, Benitez J, Ko YD, Fischer HP, Hamann U, Pesch B, Bruning T, Justenhoven C, Brauch H, Eccles DM, Tapper WJ, Gerty SM, Sawyer EJ, Tomlinson IP, Jones A, Kerin M, Miller N, McInerney N, Anton-Culver H, Ziogas A, et al. Associations of breast cancer risk factors with tumor subtypes: a pooled analysis from the Breast Cancer Association Consortium studies. J Natl Cancer Inst. 2011;103(3):250–63.PubMedCrossRef
13.
go back to reference Hartmann LC, Sellers TA, Frost MH, Lingle WL, Degnim AC, Ghosh K, Vierkant RA, Maloney SD, Pankratz VS, Hillman DW, Suman VJ, Johnson J, Blake C, Tlsty T, Vachon CM, Melton LJ 3rd, Visscher DW. Benign breast disease and the risk of breast cancer. N Engl J Med. 2005;353(3):229–37.PubMedCrossRef Hartmann LC, Sellers TA, Frost MH, Lingle WL, Degnim AC, Ghosh K, Vierkant RA, Maloney SD, Pankratz VS, Hillman DW, Suman VJ, Johnson J, Blake C, Tlsty T, Vachon CM, Melton LJ 3rd, Visscher DW. Benign breast disease and the risk of breast cancer. N Engl J Med. 2005;353(3):229–37.PubMedCrossRef
14.
go back to reference Tamimi RM, Rosner B, Colditz GA. Evaluation of a breast cancer risk prediction model expanded to include category of prior benign breast disease lesion. Cancer. 2010;116(21):4944–53.PubMedPubMedCentralCrossRef Tamimi RM, Rosner B, Colditz GA. Evaluation of a breast cancer risk prediction model expanded to include category of prior benign breast disease lesion. Cancer. 2010;116(21):4944–53.PubMedPubMedCentralCrossRef
15.
go back to reference Rothman KGS, Lash T. Modern epidemiology. Philadelphia: Lippincott Williams & Wilkins; 2008. Rothman KGS, Lash T. Modern epidemiology. Philadelphia: Lippincott Williams & Wilkins; 2008.
16.
go back to reference Glass AG, Lacey JV Jr, Carreon JD, Hoover RN. Breast cancer incidence, 1980-2006: combined roles of menopausal hormone therapy, screening mammography, and estrogen receptor status. J Natl Cancer Inst. 2007;99(15):1152–61.PubMedCrossRef Glass AG, Lacey JV Jr, Carreon JD, Hoover RN. Breast cancer incidence, 1980-2006: combined roles of menopausal hormone therapy, screening mammography, and estrogen receptor status. J Natl Cancer Inst. 2007;99(15):1152–61.PubMedCrossRef
17.
go back to reference Ali AM, Dawson SJ, Blows FM, Provenzano E, Ellis IO, Baglietto L, Huntsman D, Caldas C, Pharoah PD. Comparison of methods for handling missing data on immunohistochemical markers in survival analysis of breast cancer. Br J Cancer. 2011;104(4):693–9.PubMedPubMedCentralCrossRef Ali AM, Dawson SJ, Blows FM, Provenzano E, Ellis IO, Baglietto L, Huntsman D, Caldas C, Pharoah PD. Comparison of methods for handling missing data on immunohistochemical markers in survival analysis of breast cancer. Br J Cancer. 2011;104(4):693–9.PubMedPubMedCentralCrossRef
18.
go back to reference Moons KG, Donders RA, Stijnen T, Harrell FE Jr. Using the outcome for imputation of missing predictor values was preferred. J Clin Epidemiol. 2006;59(10):1092–101.PubMedCrossRef Moons KG, Donders RA, Stijnen T, Harrell FE Jr. Using the outcome for imputation of missing predictor values was preferred. J Clin Epidemiol. 2006;59(10):1092–101.PubMedCrossRef
19.
go back to reference Baer HJ, Collins LC, Connolly JL, Colditz GA, Schnitt SJ, Tamimi RM. Lobule type and subsequent breast cancer risk: results from the Nurses’ Health Studies. Cancer. 2009;115(7):1404–11.PubMedPubMedCentralCrossRef Baer HJ, Collins LC, Connolly JL, Colditz GA, Schnitt SJ, Tamimi RM. Lobule type and subsequent breast cancer risk: results from the Nurses’ Health Studies. Cancer. 2009;115(7):1404–11.PubMedPubMedCentralCrossRef
20.
go back to reference Lee A, Mavaddat N, Wilcox AN, Cunningham AP, Carver T, Hartley S, Babb de Villiers C, Izquierdo A, Simard J, Schmidt MK, Walter FM, Chatterjee N, Garcia-Closas M, Tischkowitz M, Pharoah P, Easton DF, Antoniou AC. BOADICEA: a comprehensive breast cancer risk prediction model incorporating genetic and nongenetic risk factors. Genet Med. 2019;21(8):1708–18.PubMedPubMedCentralCrossRef Lee A, Mavaddat N, Wilcox AN, Cunningham AP, Carver T, Hartley S, Babb de Villiers C, Izquierdo A, Simard J, Schmidt MK, Walter FM, Chatterjee N, Garcia-Closas M, Tischkowitz M, Pharoah P, Easton DF, Antoniou AC. BOADICEA: a comprehensive breast cancer risk prediction model incorporating genetic and nongenetic risk factors. Genet Med. 2019;21(8):1708–18.PubMedPubMedCentralCrossRef
21.
go back to reference Mavaddat N, Rebbeck TR, Lakhani SR, Easton DF, Antoniou AC. Incorporating tumour pathology information into breast cancer risk prediction algorithms. Breast Cancer Res. 2010;12(3):R28.PubMedPubMedCentralCrossRef Mavaddat N, Rebbeck TR, Lakhani SR, Easton DF, Antoniou AC. Incorporating tumour pathology information into breast cancer risk prediction algorithms. Breast Cancer Res. 2010;12(3):R28.PubMedPubMedCentralCrossRef
22.
go back to reference Gaudet MM, Press MF, Haile RW, Lynch CF, Glaser SL, Schildkraut J, Gammon MD, Douglas Thompson W, Bernstein JL. Risk factors by molecular subtypes of breast cancer across a population-based study of women 56 years or younger. Breast Cancer Res Treat. 2011;130(2):587–97.PubMedPubMedCentralCrossRef Gaudet MM, Press MF, Haile RW, Lynch CF, Glaser SL, Schildkraut J, Gammon MD, Douglas Thompson W, Bernstein JL. Risk factors by molecular subtypes of breast cancer across a population-based study of women 56 years or younger. Breast Cancer Res Treat. 2011;130(2):587–97.PubMedPubMedCentralCrossRef
23.
go back to reference Boulos FI, Dupont WD, Simpson JF, Schuyler PA, Sanders ME, Freudenthal ME, Page DL. Histologic associations and long-term cancer risk in columnar cell lesions of the breast: a retrospective cohort and a nested case-control study. Cancer. 2008;113(9):2415–21.PubMedPubMedCentralCrossRef Boulos FI, Dupont WD, Simpson JF, Schuyler PA, Sanders ME, Freudenthal ME, Page DL. Histologic associations and long-term cancer risk in columnar cell lesions of the breast: a retrospective cohort and a nested case-control study. Cancer. 2008;113(9):2415–21.PubMedPubMedCentralCrossRef
24.
go back to reference Fitzgibbons PL, Henson DE, Hutter RV. Benign breast changes and the risk for subsequent breast cancer: an update of the 1985 consensus statement. Cancer Committee of the College of American Pathologists. Arch Pathol Lab Med. 1998;122(12):1053–5.PubMed Fitzgibbons PL, Henson DE, Hutter RV. Benign breast changes and the risk for subsequent breast cancer: an update of the 1985 consensus statement. Cancer Committee of the College of American Pathologists. Arch Pathol Lab Med. 1998;122(12):1053–5.PubMed
25.
go back to reference Lopez-Garcia MA, Geyer FC, Natrajan R, Kreike B, Mackay A, Grigoriadis A, Reis-Filho JS, Weigelt B. Transcriptomic analysis of tubular carcinomas of the breast reveals similarities and differences with molecular subtype-matched ductal and lobular carcinomas. J Pathol. 2010;222(1):64–75.PubMed Lopez-Garcia MA, Geyer FC, Natrajan R, Kreike B, Mackay A, Grigoriadis A, Reis-Filho JS, Weigelt B. Transcriptomic analysis of tubular carcinomas of the breast reveals similarities and differences with molecular subtype-matched ductal and lobular carcinomas. J Pathol. 2010;222(1):64–75.PubMed
26.
go back to reference Page DL, Dupont WD, Rogers LW, Rados MS. Atypical hyperplastic lesions of the female breast. A long-term follow-up study. Cancer. 1985;55(11):2698–708.PubMedCrossRef Page DL, Dupont WD, Rogers LW, Rados MS. Atypical hyperplastic lesions of the female breast. A long-term follow-up study. Cancer. 1985;55(11):2698–708.PubMedCrossRef
27.
go back to reference Cuzick J, Sestak I, Cawthorn S, Hamed H, Holli K, Howell A, Forbes JF, Investigators I-I. Tamoxifen for prevention of breast cancer: extended long-term follow-up of the IBIS-I breast cancer prevention trial. Lancet Oncol. 2015;16(1):67–75.PubMedPubMedCentralCrossRef Cuzick J, Sestak I, Cawthorn S, Hamed H, Holli K, Howell A, Forbes JF, Investigators I-I. Tamoxifen for prevention of breast cancer: extended long-term follow-up of the IBIS-I breast cancer prevention trial. Lancet Oncol. 2015;16(1):67–75.PubMedPubMedCentralCrossRef
28.
go back to reference Holm J, Eriksson L, Ploner A, Eriksson M, Rantalainen M, Li J, Hall P, Czene K. Assessment of breast cancer risk factors reveals subtype heterogeneity. Cancer Res. 2017;77(13):3708–17.PubMedCrossRef Holm J, Eriksson L, Ploner A, Eriksson M, Rantalainen M, Li J, Hall P, Czene K. Assessment of breast cancer risk factors reveals subtype heterogeneity. Cancer Res. 2017;77(13):3708–17.PubMedCrossRef
29.
go back to reference Aroner SA, Collins LC, Connolly JL, Colditz GA, Schnitt SJ, Rosner BA, Hankinson SE, Tamimi RM. Radial scars and subsequent breast cancer risk: results from the Nurses’ Health Studies. Breast Cancer Res Treat. 2013;139(1):277–85.PubMedPubMedCentralCrossRef Aroner SA, Collins LC, Connolly JL, Colditz GA, Schnitt SJ, Rosner BA, Hankinson SE, Tamimi RM. Radial scars and subsequent breast cancer risk: results from the Nurses’ Health Studies. Breast Cancer Res Treat. 2013;139(1):277–85.PubMedPubMedCentralCrossRef
30.
go back to reference Allred DC, Mohsin SK, Fuqua SA. Histological and biological evolution of human premalignant breast disease. Endocr Relat Cancer. 2001;8(1):47–61.PubMedCrossRef Allred DC, Mohsin SK, Fuqua SA. Histological and biological evolution of human premalignant breast disease. Endocr Relat Cancer. 2001;8(1):47–61.PubMedCrossRef
31.
32.
go back to reference Lee S, Medina D, Tsimelzon A, Mohsin SK, Mao S, Wu Y, Allred DC. Alterations of gene expression in the development of early hyperplastic precursors of breast cancer. Am J Pathol. 2007;171(1):252–62.PubMedPubMedCentralCrossRef Lee S, Medina D, Tsimelzon A, Mohsin SK, Mao S, Wu Y, Allred DC. Alterations of gene expression in the development of early hyperplastic precursors of breast cancer. Am J Pathol. 2007;171(1):252–62.PubMedPubMedCentralCrossRef
33.
go back to reference Simpson PT, Gale T, Reis-Filho JS, Jones C, Parry S, Sloane JP, Hanby A, Pinder SE, Lee AH, Humphreys S, Ellis IO, Lakhani SR. Columnar cell lesions of the breast: the missing link in breast cancer progression? A morphological and molecular analysis. Am J Surg Pathol. 2005;29(6):734–46.PubMedCrossRef Simpson PT, Gale T, Reis-Filho JS, Jones C, Parry S, Sloane JP, Hanby A, Pinder SE, Lee AH, Humphreys S, Ellis IO, Lakhani SR. Columnar cell lesions of the breast: the missing link in breast cancer progression? A morphological and molecular analysis. Am J Surg Pathol. 2005;29(6):734–46.PubMedCrossRef
34.
go back to reference Sinn HP. Breast cancer precursors: lessons learned from molecular genetics. J Mol Med (Berl). 2009;87(2):113–5.CrossRef Sinn HP. Breast cancer precursors: lessons learned from molecular genetics. J Mol Med (Berl). 2009;87(2):113–5.CrossRef
35.
go back to reference Aroner SA, Collins LC, Schnitt SJ, Connolly JL, Colditz GA, Tamimi RM. Columnar cell lesions and subsequent breast cancer risk: a nested case-control study. Breast Cancer Res. 2010;12(4):R61.PubMedPubMedCentralCrossRef Aroner SA, Collins LC, Schnitt SJ, Connolly JL, Colditz GA, Tamimi RM. Columnar cell lesions and subsequent breast cancer risk: a nested case-control study. Breast Cancer Res. 2010;12(4):R61.PubMedPubMedCentralCrossRef
36.
go back to reference Boulos FI, Dupont WD, Schuyler PA, Sanders ME, Page DL, Fedda FA, Simpson JF. Clinicopathologic characteristics of carcinomas that develop after a biopsy containing columnar cell lesions: evidence against a precursor role. Cancer. 2012;118(9):2372–7.PubMedCrossRef Boulos FI, Dupont WD, Schuyler PA, Sanders ME, Page DL, Fedda FA, Simpson JF. Clinicopathologic characteristics of carcinomas that develop after a biopsy containing columnar cell lesions: evidence against a precursor role. Cancer. 2012;118(9):2372–7.PubMedCrossRef
37.
go back to reference Collins LC. Precursor lesions of the low-grade breast neoplasia pathway. Surg Pathol Clin. 2018;11(1):177–97.PubMedCrossRef Collins LC. Precursor lesions of the low-grade breast neoplasia pathway. Surg Pathol Clin. 2018;11(1):177–97.PubMedCrossRef
38.
go back to reference Jung MM, Colditz GA, Collins LC, Schnitt SJ, Connolly JL, Tamimi RM. Lifetime physical activity and the incidence of proliferative benign breast disease. Cancer Causes Control. 2011;22(9):1297–305.PubMedPubMedCentralCrossRef Jung MM, Colditz GA, Collins LC, Schnitt SJ, Connolly JL, Tamimi RM. Lifetime physical activity and the incidence of proliferative benign breast disease. Cancer Causes Control. 2011;22(9):1297–305.PubMedPubMedCentralCrossRef
39.
go back to reference Meares AL, Frank RD, Degnim AC, Vierkant RA, Frost MH, Hartmann LC, Winham SJ, Visscher DW. Mucocele-like lesions of the breast: a clinical outcome and histologic analysis of 102 cases. Hum Pathol. 2016;49:33–8.PubMedCrossRef Meares AL, Frank RD, Degnim AC, Vierkant RA, Frost MH, Hartmann LC, Winham SJ, Visscher DW. Mucocele-like lesions of the breast: a clinical outcome and histologic analysis of 102 cases. Hum Pathol. 2016;49:33–8.PubMedCrossRef
40.
go back to reference Said SM, Visscher DW, Nassar A, Frank RD, Vierkant RA, Frost MH, Ghosh K, Radisky DC, Hartmann LC, Degnim AC. Flat epithelial atypia and risk of breast cancer: a Mayo cohort study. Cancer. 2015;121(10):1548–55.PubMedPubMedCentralCrossRef Said SM, Visscher DW, Nassar A, Frank RD, Vierkant RA, Frost MH, Ghosh K, Radisky DC, Hartmann LC, Degnim AC. Flat epithelial atypia and risk of breast cancer: a Mayo cohort study. Cancer. 2015;121(10):1548–55.PubMedPubMedCentralCrossRef
41.
go back to reference Verschuur-Maes AH, Moelans CB, de Bruin PC, van Diest PJ. Analysis of gene copy number alterations by multiplex ligation-dependent probe amplification in columnar cell lesions of the breast. Cell Oncol (Dordr). 2014;37(2):147–54.CrossRef Verschuur-Maes AH, Moelans CB, de Bruin PC, van Diest PJ. Analysis of gene copy number alterations by multiplex ligation-dependent probe amplification in columnar cell lesions of the breast. Cell Oncol (Dordr). 2014;37(2):147–54.CrossRef
42.
go back to reference Verschuur-Maes AH, van Gils CH, van den Bosch MA, De Bruin PC, van Diest PJ. Digital mammography: more microcalcifications, more columnar cell lesions without atypia. Modern Pathol. 2011;24(9):1191–7.CrossRef Verschuur-Maes AH, van Gils CH, van den Bosch MA, De Bruin PC, van Diest PJ. Digital mammography: more microcalcifications, more columnar cell lesions without atypia. Modern Pathol. 2011;24(9):1191–7.CrossRef
43.
go back to reference Figueroa JD, Pfeiffer RM, Brinton LA, Palakal M, Degnim AC, Radisky D, Hartmann LC, Frost M, Stallings-Mann ML, DP, Visscher D, Sherman ME. Standardized measures of lobular involution and subsequent breast cancer risk among women with benign breast disease. Breast Cancer Res Treat. 2016;159(1):163–72.PubMedPubMedCentralCrossRef Figueroa JD, Pfeiffer RM, Brinton LA, Palakal M, Degnim AC, Radisky D, Hartmann LC, Frost M, Stallings-Mann ML, DP, Visscher D, Sherman ME. Standardized measures of lobular involution and subsequent breast cancer risk among women with benign breast disease. Breast Cancer Res Treat. 2016;159(1):163–72.PubMedPubMedCentralCrossRef
44.
go back to reference Milanese TR, Hartmann LC, Sellers TA, Frost MH, Vierkant RA, Maloney SD, Pankratz VS, Degnim AC, Vachon CM, Reynolds CA, Thompson RA, Melton LJ 3rd, Goode EL, Visscher DW. Age-related lobular involution and risk of breast cancer. J Natl Cancer Inst. 2006;98(22):1600–7.PubMedCrossRef Milanese TR, Hartmann LC, Sellers TA, Frost MH, Vierkant RA, Maloney SD, Pankratz VS, Degnim AC, Vachon CM, Reynolds CA, Thompson RA, Melton LJ 3rd, Goode EL, Visscher DW. Age-related lobular involution and risk of breast cancer. J Natl Cancer Inst. 2006;98(22):1600–7.PubMedCrossRef
45.
go back to reference Figueroa JD, Pfeiffer RM, Patel DA, Linville L, Brinton LA, Gierach GL, Yang XR, Papathomas D, Visscher D, Mies C, Degnim AC, Anderson WF, Hewitt S, Khodr ZG, Clare SE, Storniolo AM, Sherman ME. Terminal duct lobular unit involution of the normal breast: implications for breast cancer etiology. J Natl Cancer Inst. 2014;106(10). Figueroa JD, Pfeiffer RM, Patel DA, Linville L, Brinton LA, Gierach GL, Yang XR, Papathomas D, Visscher D, Mies C, Degnim AC, Anderson WF, Hewitt S, Khodr ZG, Clare SE, Storniolo AM, Sherman ME. Terminal duct lobular unit involution of the normal breast: implications for breast cancer etiology. J Natl Cancer Inst. 2014;106(10).
46.
go back to reference Roman M, Quintana MJ, Ferrer J, Sala M, Castells X. Cumulative risk of breast cancer screening outcomes according to the presence of previous benign breast disease and family history of breast cancer: supporting personalised screening. Br J Cancer. 2017;116(11):1480–5.PubMedPubMedCentralCrossRef Roman M, Quintana MJ, Ferrer J, Sala M, Castells X. Cumulative risk of breast cancer screening outcomes according to the presence of previous benign breast disease and family history of breast cancer: supporting personalised screening. Br J Cancer. 2017;116(11):1480–5.PubMedPubMedCentralCrossRef
47.
go back to reference Menes TS, Kerlikowske K, Lange J, Jaffer S, Rosenberg R, Miglioretti DL. Subsequent breast cancer risk following diagnosis of atypical ductal hyperplasia on needle biopsy. JAMA Oncol. 2017;3(1):36–41.PubMedPubMedCentralCrossRef Menes TS, Kerlikowske K, Lange J, Jaffer S, Rosenberg R, Miglioretti DL. Subsequent breast cancer risk following diagnosis of atypical ductal hyperplasia on needle biopsy. JAMA Oncol. 2017;3(1):36–41.PubMedPubMedCentralCrossRef
Metadata
Title
Risk factors for breast cancer development by tumor characteristics among women with benign breast disease
Authors
Jonine D. Figueroa
Gretchen L. Gierach
Máire A. Duggan
Shaoqi Fan
Ruth M. Pfeiffer
Yihong Wang
Roni T. Falk
Olivier Loudig
Mustapha Abubakar
Mindy Ginsberg
Teresa M. Kimes
Kathryn Richert-Boe
Andrew G. Glass
Thomas E. Rohan
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Breast Cancer Research / Issue 1/2021
Electronic ISSN: 1465-542X
DOI
https://doi.org/10.1186/s13058-021-01410-1

Other articles of this Issue 1/2021

Breast Cancer Research 1/2021 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