Skip to main content
Top
Published in: Breast Cancer Research and Treatment 2/2019

01-04-2019 | Epidemiology

The mammography screening detection of ductal carcinoma in situ and invasive breast cancer according to women’s characteristics: is it the same?

Authors: Isabelle Théberge, Nathalie Vandal, Marie-Hélène Guertin, Linda Perron

Published in: Breast Cancer Research and Treatment | Issue 2/2019

Login to get access

Abstract

Purpose

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.

Methods

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.

Results

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).

Conclusion

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.
Literature
1.
go back to reference Wiechmann L, Kuerer HM (2008) The molecular journey from ductal carcinoma in situ to invasive breast cancer. Cancer 112(10):2130–2142PubMedCrossRef Wiechmann L, Kuerer HM (2008) The molecular journey from ductal carcinoma in situ to invasive breast cancer. Cancer 112(10):2130–2142PubMedCrossRef
2.
go back to reference 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):859–869PubMedPubMedCentralCrossRef 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):859–869PubMedPubMedCentralCrossRef
3.
go back to reference Allred DC (2010) Ductal carcinoma in situ: terminology, classification, and natural history. J Natl Cancer Inst Monogr 41:134–138CrossRef Allred DC (2010) Ductal carcinoma in situ: terminology, classification, and natural history. J Natl Cancer Inst Monogr 41:134–138CrossRef
4.
go back to reference Casasent AK, Edgerton M, Navin NE (2017) Genome evolution in ductal carcinoma in situ: invasion of the clones. J Pathol 241(2):208–218PubMedCrossRef Casasent AK, Edgerton M, Navin NE (2017) Genome evolution in ductal carcinoma in situ: invasion of the clones. J Pathol 241(2):208–218PubMedCrossRef
5.
go back to reference Leonard GD, Swain SM (2004) Ductal carcinoma in situ, complexities and challenges. J Natl Cancer Inst 96(12):906–920PubMedCrossRef Leonard GD, Swain SM (2004) Ductal carcinoma in situ, complexities and challenges. J Natl Cancer Inst 96(12):906–920PubMedCrossRef
6.
go back to reference 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 31:274–283PubMedCrossRef 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 31:274–283PubMedCrossRef
7.
go back to reference deGelder R, Heijnsdijk EAM, vanRavesteyn NT, Fracheboud J, Draisma G, deKoning HJ (2011) Interpreting overdiagnosis estimates in population-based mammography screening. Epidemiol Rev 33:111–121PubMedPubMedCentralCrossRef deGelder R, Heijnsdijk EAM, vanRavesteyn NT, Fracheboud J, Draisma G, deKoning HJ (2011) Interpreting overdiagnosis estimates in population-based mammography screening. Epidemiol Rev 33:111–121PubMedPubMedCentralCrossRef
8.
go back to reference 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):R35PubMedPubMedCentralCrossRef 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):R35PubMedPubMedCentralCrossRef
9.
go back to reference 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):1329–1340PubMedPubMedCentralCrossRef 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):1329–1340PubMedPubMedCentralCrossRef
10.
go back to reference 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):930–937PubMedCrossRef 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):930–937PubMedCrossRef
11.
go back to reference 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):65–77PubMedCrossRef 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):65–77PubMedCrossRef
12.
go back to reference 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):76–82PubMedCrossRef 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):76–82PubMedCrossRef
13.
go back to reference 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 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
14.
go back to reference 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 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
15.
go back to reference Miglioretti DL, Heagerty PJ (2004) Marginal modeling of multilevel binary data with time-varying covariates. Biostatistics 5(3):381–398PubMedCrossRef Miglioretti DL, Heagerty PJ (2004) Marginal modeling of multilevel binary data with time-varying covariates. Biostatistics 5(3):381–398PubMedCrossRef
16.
go back to reference Muller CJ, MacLehose RF (2014) Estimating predicted probabilities from logistic regression: different methods correspond to different target populations. Int J Epidemiol 43(3):962–970PubMedPubMedCentralCrossRef Muller CJ, MacLehose RF (2014) Estimating predicted probabilities from logistic regression: different methods correspond to different target populations. Int J Epidemiol 43(3):962–970PubMedPubMedCentralCrossRef
17.
go back to reference 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 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
18.
go back to reference Australian Insitute of Health and Welfare (2017) BreastScreen Australia monitoring report 2014–2015. Cancer series no. 106. Cat. No. CAN 105. AIHW, Canberra Australian Insitute of Health and Welfare (2017) BreastScreen Australia monitoring report 2014–2015. Cancer series no. 106. Cat. No. CAN 105. AIHW, Canberra
19.
go back to reference 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):424–432PubMedCrossRef 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):424–432PubMedCrossRef
20.
go back to reference 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):307–314PubMedCrossRef 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):307–314PubMedCrossRef
21.
go back to reference 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):821PubMedPubMedCentralCrossRef 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):821PubMedPubMedCentralCrossRef
22.
go back to reference 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):1179–1189PubMedPubMedCentralCrossRef 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):1179–1189PubMedPubMedCentralCrossRef
23.
go back to reference 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):343–348PubMedCrossRef 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):343–348PubMedCrossRef
24.
go back to reference 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):R30PubMedPubMedCentralCrossRef 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):R30PubMedPubMedCentralCrossRef
25.
go back to reference 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):750–753PubMedCrossRef 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):750–753PubMedCrossRef
26.
go back to reference 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 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
27.
go back to reference 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 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
28.
go back to reference 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):2091–2097PubMedCrossRef 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):2091–2097PubMedCrossRef
29.
go back to reference 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):559–568PubMedCrossRef 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):559–568PubMedCrossRef
30.
go back to reference Claus EB, Stowe M, Carter D (2001) Breast carcinoma in situ: risk factors and screening patterns. J Natl Cancer Inst 93(23):1811–1817PubMedCrossRef Claus EB, Stowe M, Carter D (2001) Breast carcinoma in situ: risk factors and screening patterns. J Natl Cancer Inst 93(23):1811–1817PubMedCrossRef
31.
go back to reference 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):R4PubMedPubMedCentralCrossRef 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):R4PubMedPubMedCentralCrossRef
32.
go back to reference 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):113–116PubMedPubMedCentralCrossRef 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):113–116PubMedPubMedCentralCrossRef
33.
go back to reference 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):956–969PubMedPubMedCentralCrossRef 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):956–969PubMedPubMedCentralCrossRef
34.
go back to reference Nazari SS, Mukherjee P (2018) An overview of mammographic density and its association with breast cancer. Breast Cancer Tokyo Jpn25(3):259–267CrossRef Nazari SS, Mukherjee P (2018) An overview of mammographic density and its association with breast cancer. Breast Cancer Tokyo Jpn25(3):259–267CrossRef
36.
go back to reference 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):168–175PubMedCrossRef 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):168–175PubMedCrossRef
37.
go back to reference 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):1060–1064CrossRef 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):1060–1064CrossRef
38.
go back to reference 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):30–37PubMedCrossRef 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):30–37PubMedCrossRef
39.
go back to reference 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):5140–5146PubMedPubMedCentralCrossRef 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):5140–5146PubMedPubMedCentralCrossRef
40.
go back to reference 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):1335–1339PubMedCrossRef 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):1335–1339PubMedCrossRef
41.
go back to reference 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):1038–1048CrossRef 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):1038–1048CrossRef
42.
go back to reference 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):481–487PubMedCrossRef 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):481–487PubMedCrossRef
43.
go back to reference O’Grady S, Morgan MP (2018) Microcalcifications in breast cancer: from pathophysiology to diagnosis and prognosis. Biochim Biophys Acta 1869(2):310–320 O’Grady S, Morgan MP (2018) Microcalcifications in breast cancer: from pathophysiology to diagnosis and prognosis. Biochim Biophys Acta 1869(2):310–320
44.
go back to reference 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):17PubMedPubMedCentralCrossRef 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):17PubMedPubMedCentralCrossRef
Metadata
Title
The mammography screening detection of ductal carcinoma in situ and invasive breast cancer according to women’s characteristics: is it the same?
Authors
Isabelle Théberge
Nathalie Vandal
Marie-Hélène Guertin
Linda Perron
Publication date
01-04-2019
Publisher
Springer US
Published in
Breast Cancer Research and Treatment / Issue 2/2019
Print ISSN: 0167-6806
Electronic ISSN: 1573-7217
DOI
https://doi.org/10.1007/s10549-018-05095-7

Other articles of this Issue 2/2019

Breast Cancer Research and Treatment 2/2019 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