Detection of ductal carcinoma in situ (DCIS) has increased with the mammography dissemination. Given the potential role of DCIS as a precursor of invasive breast cancer (IBC), we aimed to assess whether women’s characteristics have a different effect on the DCIS compared to IBC detection rate.
This study included 3,609,569 screening mammograms performed from 2002 to 2015 in our organized breast cancer screening program, which actively invites women 50–69 years of age. The association between women’s characteristics and the DCIS detection rate, the IBC detection rate and the odds ratio of DCIS among screen-detected cancers was assessed by logistic regression and generalized estimating equations with independent correlation matrix and sandwich estimator.
A total of 4173 DCIS and 15,136 IBC were screen-detected. Increasing women’s age, current hormone replacement therapy use and higher body mass index were less associated with the DCIS than with IBC detection rates (p value for the odds of DCIS among screen-detected cancers of, respectively, < 0.0001, 0.0244 and < 0.0001). In contrast, having a previous breast aspiration or biopsy and increasing breast density were more strongly associated with DCIS than with IBC detection rates (p value of, respectively, 0.0050 and < 0.0001).
The results suggest that some women’s characteristics could be playing a role in the initiation and other in the progression from in situ to invasive breast cancer. These characteristics can also affect the screening sensitivity, and this effect may differ depending on whether screen-detected cases were DCIS or IBC.
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Body mass index
Cancer detection rate
Ductal carcinoma in situ
Generalized estimating equations
Hormone replacement therapy
Invasive breast cancer
International Classification of Diseases, 9th edition
International Classification of Diseases, 10th edition
Programme québécois de dépistage du cancer du sein (Quebec Breast Cancer Screening Program)
Wiechmann L, Kuerer HM (2008) The molecular journey from ductal carcinoma in situ to invasive breast cancer. Cancer 112(10):2130–2142
Cowell CF, Weigelt B, Sakr RA, Ng CKY, Hicks J, King TA et al (2013) Progression from ductal carcinoma in situ to invasive breast cancer: revisited. Mol Oncol 7(5):859–869
Allred DC (2010) Ductal carcinoma in situ: terminology, classification, and natural history. J Natl Cancer Inst Monogr 41:134–138
Casasent AK, Edgerton M, Navin NE (2017) Genome evolution in ductal carcinoma in situ: invasion of the clones. J Pathol 241(2):208–218
Leonard GD, Swain SM (2004) Ductal carcinoma in situ, complexities and challenges. J Natl Cancer Inst 96(12):906–920
Groen EJ, Elshof LE, Visser LL, Rutgers EJT, Winter-Warnars HAO, Lips EH et al (2017) Finding the balance between over- and under-treatment of ductal carcinoma in situ (DCIS). Breast 31:274–283
deGelder R, Heijnsdijk EAM, vanRavesteyn NT, Fracheboud J, Draisma G, deKoning HJ (2011) Interpreting overdiagnosis estimates in population-based mammography screening. Epidemiol Rev 33:111–121
Ma H, Henderson KD, Sullivan-Halley J, Duan L, Marshall SF, Ursin G et al (2010) Pregnancy-related factors and the risk of breast carcinoma in situ and invasive breast cancer among postmenopausal women in the California Teachers Study cohort. Breast Cancer Res 12(3):R35
Mullooly M, Khodr ZG, Dallal CM, Nyante SJ, Sherman ME, Falk R 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(12):1329–1340
Reeves GK, Pirie K, Green J, Bull D, Beral V, Million Women Study Collaborators (2012) Comparison of the effects of genetic and environmental risk factors on in situ and invasive ductal breast cancer. Int J Cancer 131(4):930–937
Millikan R, Dressler L, Geradts J, Graham M (1995) The need for epidemiologic studies of in-situ carcinoma of the breast. Breast Cancer Res Treat 35(1):65–77
Kerlikowske K, Barclay J, Grady D, Sickles EA, Ernster V (1997) Comparison of risk factors for ductal carcinoma in situ and invasive breast cancer. J Natl Cancer Inst 89(1):76–82
Théberge I, Major D, Langlois A, Brisson J (2003) [Validation de stratégies pour obtenir le taux de détection du cancer, la valeur prédictive positive, la proportion des cancers in situ, la proportion des cancers infiltrants de petite taille et la proportion des cancers infiltrants sans envahissement ganglionnaire dans le cadre des données fournies par le Programme québécois de dépistage du cancer du sein (PQDCS)] [In French]. Institut national de santé publique du Québec. https://www.inspq.qc.ca/publications/201. Accessed 9 Oct 2018
Pelletier E, Major D, Brisson J (2005) [Développement d’algorithmes permettant d’identifier les interventions et les délais liés à l’investigation diagnostique suite à une mammographie de dépistage anormale - Programme québécois de dépistage du cancer du sein (PQDCS)] [In French]. Institut national de santé publique du Québec. https://www.inspq.qc.ca/publications/417. Accessed 9 Oct 2018
Miglioretti DL, Heagerty PJ (2004) Marginal modeling of multilevel binary data with time-varying covariates. Biostatistics 5(3):381–398
Muller CJ, MacLehose RF (2014) Estimating predicted probabilities from logistic regression: different methods correspond to different target populations. Int J Epidemiol 43(3):962–970
Canadian Partnership Against Cancer (2017) Breast cancer screening in Canada: monitoring and evaluation of quality indicators—results report, January 2011 to December 2012. Toronto, Canadian Partnership Against Cancer
Australian Insitute of Health and Welfare (2017) BreastScreen Australia monitoring report 2014–2015. Cancer series no. 106. Cat. No. CAN 105. AIHW, Canberra
Weigel S, Khil L, Hense H-W, Decker T, Wellmann J, Heidrich J et al (2018) Detection rates of ductal carcinoma in situ with biennial digital mammography screening: radiologic findings support pathologic model of tumor progression. Radiology 286(2):424–432
Luiten JD, Voogd AD, Luiten EJT, Duijm EM (2017) Trends in incidence and tumour grade in screen-detected ductal carcinoma in situ and invasive breast cancer. Breast Cancer Res Treat 166(1):307–314
Ko H, Shin J, Lee JE, Nam SJ, Nguyen TL, Hopper JL et al (2017) Comparison of the association of mammographic density and clinical factors with ductal carcinoma in situ versus invasive ductal breast cancer in Korean women. BMC Cancer 17(1):821
Yaghjyan L, Colditz GA, Collins LC, Schnitt SJ, Rosner B, Vachon C et al (2011) Mammographic breast density and subsequent risk of breast cancer in postmenopausal women according to tumor characteristics. J Natl Cancer Inst 103(15):1179–1189
Reinier KS, Vacek PM, Geller BM (2007) Risk factors for breast carcinoma in situ versus invasive breast cancer in a prospective study of pre- and post-menopausal women. Breast Cancer Res Treat 103(3):343–348
Gill JK, Maskarinec G, Pagano I, Kolonel LN (2006) The association of mammographic density with ductal carcinoma in situ of the breast: the Multiethnic Cohort. Breast Cancer Res 8(3):R30
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(5):750–753
Trentham-Dietz A, Newcomb PA, Storer BE, Remington PL (2000) Risk factors for carcinoma in situ of the breast. Cancer Epidemiol Biomark Prev 9(7):697–703
Longnecker MP, Bernstein L, Paganini-Hill A, Enger SM, Ross RK (1996) Risk factors for in situ breast cancer. Cancer Epidemiol Biomark Prev 5(12):961–965
Gapstur SM, Morrow M, Sellers TA (1999) Hormone replacement therapy and risk of breast cancer with a favorable histology: results of the Iowa Women’s Health Study. JAMA 281(22):2091–2097
Granström C, Sundquist J, Hemminki K (2008) Population attributable risks for breast cancer in Swedish women by morphological type. Breast Cancer Res Treat 111(3):559–568
Claus EB, Stowe M, Carter D (2001) Breast carcinoma in situ: risk factors and screening patterns. J Natl Cancer Inst 93(23):1811–1817
Marshall SF, Clarke CA, Deapen D, Henderson K, Largent J, Neuhausen SL et al (2010) Recent breast cancer incidence trends according to hormone therapy use: the California Teachers Study cohort. Breast Cancer Res 12(1):R4
Virnig BA, Wang S-Y, Shamilyan T, Kane RL, Tuttle TM (2010) Ductal carcinoma in situ: risk factors and impact of screening. J Natl Cancer Inst Monogr 2010(41):113–116
Sprague BL, Gangnon RE, Hampton JM, Egan KM, Titus LJ, Kerlikowske K et al (2015) Variation in breast cancer risk factor associations by method of detection: results from a series of case-control studies. Am J Epidemiol 181(12):956–969
Nazari SS, Mukherjee P (2018) An overview of mammographic density and its association with breast cancer. Breast Cancer Tokyo Jpn25(3):259–267
Vinnicombe SJ (2018) Breast density: why all the fuss?Clin Radiol 73(4):334–357
Carney PA, Miglioretti DL, Yankaskas BC, Kerlikowske K, Rosenberg R, Rutter CM et al (2003) Individual and combined effects of age, breast density, and hormone replacement therapy use on the accuracy of screening mammography. Ann Intern Med 138(3):168–175
Kavanagh AM, Cawson J, Byrnes GB, Giles GG, Marr G, Tong B et al (2005) Hormone replacement therapy, percent mammographic density, and sensitivity of mammography. Cancer Epidemiol Biomark Prev 14(5):1060–1064
Greendale GA, Reboussin BA, Slone S, Wasilauskas C, Pike MC, Ursin G (2003) Postmenopausal hormone therapy and change in mammographic density. J Natl Cancer Inst 95(1):30–37
Farhat GN, Walker R, Buist DSM, Onega T, Kerlikowske K (2010) Changes in invasive breast cancer and ductal carcinoma in situ rates in relation to the decline in hormone therapy use. J Clin Oncol 28(35):5140–5146
Kerlikowske K, Miglioretti DL, Buist DSM, Walker R, Carney PA, for the National Cancer Institute (2007) Declines in invasive breast cancer and use of postmenopausal hormone therapy in a screening mammography population. J Natl Cancer Inst 99(17):1335–1339
Santen RJ, Yue W, Heitjan DF (2012) Modeling of the growth kinetics of occult breast tumors: role in interpretation of studies of prevention and menopausal hormone therapy. Cancer Epidemiol Biomark Prev 21(7):1038–1048
Hofvind S, Iversen BF, Eriksen L, Styr BM, Kjellevold K, Kurz KD (2011) Mammographic morphology and distribution of calcifications in ductal carcinoma in situ diagnosed in organized screening. Acta Radiol 52(5):481–487
O’Grady S, Morgan MP (2018) Microcalcifications in breast cancer: from pathophysiology to diagnosis and prognosis. Biochim Biophys Acta 1869(2):310–320
Boyd N, Berman H, Zhu J, Martin LJ, Yaffe MJ, Chavez S et al (2018) The origins of breast cancer associated with mammographic density: a testable biological hypothesis. Breast Cancer Res 20(1):17
Weigelt B, Geyer FC, Reis-Filho JS (2010) Histological types of breast cancer: how special are they? Mol Oncol 4(3):192–208
This study was financially supported by the Direction générale de cancérologie of the Quebec Ministry of Health and Social Services.
Conflict of interest
All authors declare that they have no conflicts of interest.
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. All women included in this analysis signed a consent form agreeing to participate in the PQDCS, which includes transmission of their data to central database for analysis.
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Théberge, I., Vandal, N., Guertin, M. et al. The mammography screening detection of ductal carcinoma in situ and invasive breast cancer according to women’s characteristics: is it the same?. Breast Cancer Res Treat 174, 525–535 (2019). https://doi.org/10.1007/s10549-018-05095-7
- Breast cancer
- Detection rate
- Ductal carcinoma in situ