Abstract
Purpose
Histopathologic grade provides an integrated measure of biologic features which affects cancer prognosis. In invasive ductal breast cancer (IDBC), the grade of the ductal carcinoma in situ (DCIS) and invasive components are usually concordant, suggesting grade is established early in tumorigenesis and may be linked to etiologic factors. In this study, we used prospectively collected data from postmenopausal women in the Cancer Prevention Study-II (CPS-II) Nutrition Cohort to compare risk factor associations among low-grade and high-grade DCIS, as well as low-grade and high-grade IDBC.
Methods
Among 73,825 cancer-free women at enrollment in the CPS-II Nutrition Cohort in 1992–1993 (mean age: 62.1 years), we verified 802 diagnosed with DCIS (C50 8500/2; n = 430 low-grade and 372 high-grade) and 3,125 with IDBC (C50 8500/3; n = 2,221 low-grade and 904 high-grade) through June 2013. Person-time contribution was conditional on screening mammograms self-reported on biennial surveys. Multivariable-adjusted joint Cox proportional hazards regression models were used to estimate hazard ratios (HR) and 95% confidence intervals (CI).
Results
A personal history of benign breast disease was more strongly associated with higher risk of low-grade DCIS (HR = 2.20, 95% CI 1.81–2.67; p for heterogeneity = 0.0004) than high-grade DCIS. Consumption of two or more alcoholic drinks/day was only associated with a higher risk of low-grade IDBC (HR = 1.58, 95% CI 1.33–1.88; p for heterogeneity = 0.005).
Conclusions
These results suggest heterogeneity by grade for breast cancer etiology. Identification of potential risk factor differences among low-grade and high-grade DCIS and IDBC may help to clarify associations, and ultimately, improve breast cancer risk prediction models.
Similar content being viewed by others
References
Siegel RL, Miller KD, Jemal A (2019) Cancer statistics, 2019. CA Cancer J Clin 69:7–34
Virnig BA, Wang SY, Shamilyan T, Kane RL, Tuttle TM (2010) Ductal carcinoma in situ: risk factors and impact of screening. J Natl Cancer Inst. Monogr 2010:113–116
Gorringe KL, Fox SB (2017) Ductal carcinoma in situ biology, biomarkers, and diagnosis. Front Oncol 7:248
Wärnberg F, Yuen J, Holmberg L (2000) Risk of subsequent invasive breast cancer after breast carcinoma in situ. Lancet 355:724–725
Franceschi S, Levi F, La Vecchia C, Randimbison L, Te VC (1998) Second cancers following in situ carcinoma of the breast. Int J Cancer 77:392–395
Kerlikowske K (2010) Epidemiology of ductal carcinoma in situ. J Natl Cancer Inst Monogr 2010:139–141
Bleyer A, Welch HG (2012) Effect of three decades of screening mammography on breast-cancer incidence. N Engl J Med 367:1998–2005
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68:394–424
Ziegler RG, Hoover RN, Pike MC et al (1993) Migration patterns and breast cancer risk in Asian-American women. J Natl Cancer Inst 85:1819–1827
John EM, Phipps AI, Davis A, Koo J (2005) Migration history, acculturation, and breast cancer risk in Hispanic women. Cancer Epidemiol Biomarkers Prev 14:2905–2913
Brinton LG, Gierach GL (2017) Breast cancer. In: Thun MJ, Linet MS, Cerhan JR, Haiman C, Schottenfeld D (eds) Cancer epidemiology and prevention. Oxford University Press, Oxford, pp 861–888
Kerlikowske K, Molinaro A, Cha I et al (2003) Characteristics associated with recurrence among women with ductal carcinoma in situ treated by lumpectomy. J Natl Cancer Inst 95:1692–1702
Narod SA, Iqbal J, Giannakeas V, Sopik V, Sun P (2015) Breast cancer mortality after a diagnosis of ductal carcinoma in situ. JAMA Oncol 1:888–896
Elston CW, Ellis IO (1991) Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology 19:403–410
Douglas-Jones AG, Gupta SK, Attanoos RL, Morgan JM, Mansel RE (1996) A critical appraisal of six modern classifications of ductal carcinoma in situ of the breast (DCIS): correlation with grade of associated invasive carcinoma. Histopathology 29:397–409
Lopez-Garcia MA, Geyer FC, Lacroix-Triki M, Marchio C, Reis-Filho JS (2010) Breast cancer precursors revisited: molecular features and progression pathways. Histopathology 57:171–192
Wohlfahrt J, Rank F, Kroman N, Melbye M (2004) A comparison of reproductive risk factors for CIS lesions and invasive breast cancer. Int J Cancer 108:750–753
Millikan RC, Schroeder JC, Barnholtz-Sloan JS, Levine BJ (2009) Reproductive and hormonal risk factors for ductal carcinoma in situ of the breast. Cancer Epidemiol Biomarkers Prev 18:1507–1514
Kabat GC, Kim M, Kakani C et al (2010) Cigarette smoking in relation to risk of ductal carcinoma in situ of the breast in a cohort of postmenopausal women. Am J Epidemiol 172:591–599
Abubakar M, Chang-Claude J, Ali HR et al (2018) Etiology of hormone receptor positive breast cancer differs by levels of histologic grade and proliferation. Int J Cancer 143:746–757
Albrektsen G, Heuch I, Thoresen SO (2010) Histological type and grade of breast cancer tumors by parity, age at birth, and time since birth: a register-based study in Norway. BMC Cancer 10:226
Santa-Maria CA, Yan J, Xie XJ, Euhus DM (2015) Aggressive estrogen-receptor-positive breast cancer arising in patients with elevated body mass index. Int J Clin Oncol 20:317–323
Yanai A, Miyagawa Y, Murase K et al (2014) Influence of body mass index on clinicopathological factors including estrogen receptor, progesterone receptor, and Ki67 expression levels in breast cancers. Int J Clin Oncol 19:467–472
Veneroso C, Siegel R, Levine PH (2008) Early age at first childbirth associated with advanced tumor grade in breast cancer. Cancer Detect Prev 32:215–223
Largent JA, Ziogas A, Anton-Culver H (2005) Effect of reproductive factors on stage, grade and hormone receptor status in early-onset breast cancer. Breast Cancer Res 7:R541–R544
Shen S, Zhong S, Xiao G, Zhou H, Huang W (2017) Parity association with clinicopathological factors in invasive breast cancer: a retrospective analysis. OncoTargets Ther 10:477–481
Butt S, Borgquist S, Anagnostaki L, Landberg G, Manjer J (2014) Breastfeeding in relation to risk of different breast cancer characteristics. BMC Res Notes 7:216
White E, Lee CY, Kristal AR (1990) Evaluation of the increase in breast cancer incidence in relation to mammography use. J Natl Cancer Inst 82:1546–1552
Calle EE, Rodriguez C, Jacobs EJ et al (2002) The American Cancer Society Cancer Prevention Study II Nutrition Cohort: rationale, study design, and baseline characteristics. Cancer 94:2490–2501
Garfinkel L (1985) Selection, follow-up, and analysis in the American Cancer Society prospective studies. Natl Cancer Inst Monogr 67:49–52
Xue X, Kim MY, Gaudet MM et al (2013) A comparison of the polytomous logistic regression and joint cox proportional hazards models for evaluating multiple disease subtypes in prospective cohort studies. Cancer Epidemiol Biomarkers Prev 22:275–285
Mullooly M, Khodr ZG, Dallal CM et al (2017) Epidemiologic risk factors for in situ and invasive breast cancers among postmenopausal women in the National Institutes of Health-AARP Diet and Health Study. Am J Epidemiol 186:1329–1340
Reeves GK, Pirie K, Green J, Bull D, Beral V (2012) Comparison of the effects of genetic and environmental risk factors on in situ and invasive ductal breast cancer. Int J Cancer 131:930–937
Garcia-Closas M, Berrington de Gonzalez A (2015) Invited commentary: screening and the elusive etiology of prostate cancer. Am J Epidemiol 182:390–393
Jung S, Wang M, Anderson K et al (2016) Alcohol consumption and breast cancer risk by estrogen receptor status: in a pooled analysis of 20 studies. Int J Epidemiol 45:916–928
World Cancer Research Fund/American Institute for Cancer Research (2018) Continuous Update Project Expert Report 2018. Alcoholic drinks and the risk of cancer
Sprague BL, Trentham-Dietz A, Cronin KA (2012) A sustained decline in postmenopausal hormone use: results from the National Health and Nutrition Examination Survey, 1999–2010. Obstet Gynecol 120:595–603
Sherman ME, Ichikawa L, Pfeiffer RM et al (2016) Relationship of predicted risk of developing invasive breast cancer, as assessed with three models, and breast cancer mortality among breast cancer patients. PLoS ONE 11:e0160966
Acknowledgments
The authors express sincere appreciation to all Cancer Prevention Study participants, and to each member of the study and biospecimen management group. The authors would like to acknowledge the contribution to this study from central cancer registries supported through the Centers for Disease Control and Prevention's National Program of Cancer Registries and cancer registries supported by the National Cancer Institute's Surveillance Epidemiology and End Results Program.
Disclaimer
The views expressed here are those of the authors and do not necessarily represent the American Cancer Society or the American Cancer Society—Cancer Action Network.
Funding
Dr. Puvanesarajah was supported by the American Cancer Society’s Cancer Prevention Studies Post-Doctoral Fellowship Program. The American Cancer Society funds the creation, maintenance, and updating of the Cancer Prevention Study-II cohort.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All aspects of the CPS-II Nutrition Cohort have been reviewed and approved by the Emory University Institutional Review Board.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Puvanesarajah, S., Gapstur, S.M., Gansler, T. et al. Epidemiologic risk factors for in situ and invasive ductal breast cancer among regularly screened postmenopausal women by grade in the Cancer Prevention Study-II Nutrition Cohort. Cancer Causes Control 31, 95–103 (2020). https://doi.org/10.1007/s10552-019-01253-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10552-019-01253-4