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

  • Epidemiology
  • Published:
Breast Cancer Research and Treatment Aims and scope Submit manuscript

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.

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Abbreviations

BMI:

Body mass index

CDR:

Cancer detection rate

CI:

Confidence interval

CR:

Computed radiography

DCIS:

Ductal carcinoma in situ

DR:

Direct radiography

GEE:

Generalized estimating equations

HRT:

Hormone replacement therapy

IBC:

Invasive breast cancer

ICD-9:

International Classification of Diseases, 9th edition

ICD-10:

International Classification of Diseases, 10th edition

OR:

Odds ratio

PQDCS:

Programme québécois de dépistage du cancer du sein (Quebec Breast Cancer Screening Program)

References

  1. Wiechmann L, Kuerer HM (2008) The molecular journey from ductal carcinoma in situ to invasive breast cancer. Cancer 112(10):2130–2142

    Article  PubMed  Google Scholar 

  2. 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

    Article  PubMed  PubMed Central  Google Scholar 

  3. Allred DC (2010) Ductal carcinoma in situ: terminology, classification, and natural history. J Natl Cancer Inst Monogr 41:134–138

    Article  Google Scholar 

  4. Casasent AK, Edgerton M, Navin NE (2017) Genome evolution in ductal carcinoma in situ: invasion of the clones. J Pathol 241(2):208–218

    Article  PubMed  Google Scholar 

  5. Leonard GD, Swain SM (2004) Ductal carcinoma in situ, complexities and challenges. J Natl Cancer Inst 96(12):906–920

    Article  PubMed  Google Scholar 

  6. 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

    Article  PubMed  Google Scholar 

  7. 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

    Article  PubMed  PubMed Central  Google Scholar 

  8. 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

    Article  PubMed  PubMed Central  Google Scholar 

  9. 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

    Article  PubMed  PubMed Central  Google Scholar 

  10. 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

    Article  CAS  PubMed  Google Scholar 

  11. 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

    Article  CAS  PubMed  Google Scholar 

  12. 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

    Article  CAS  PubMed  Google Scholar 

  13. 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. 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. Miglioretti DL, Heagerty PJ (2004) Marginal modeling of multilevel binary data with time-varying covariates. Biostatistics 5(3):381–398

    Article  PubMed  Google Scholar 

  16. 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

    Article  PubMed  PubMed Central  Google Scholar 

  17. 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. Australian Insitute of Health and Welfare (2017) BreastScreen Australia monitoring report 2014–2015. Cancer series no. 106. Cat. No. CAN 105. AIHW, Canberra

    Google Scholar 

  19. 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

    Article  PubMed  Google Scholar 

  20. 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

    Article  PubMed  Google Scholar 

  21. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. 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

    Article  PubMed  PubMed Central  Google Scholar 

  23. 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

    Article  PubMed  Google Scholar 

  24. 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

    Article  PubMed  PubMed Central  Google Scholar 

  25. 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

    Article  CAS  PubMed  Google Scholar 

  26. 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

    CAS  Google Scholar 

  27. 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

    CAS  Google Scholar 

  28. 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

    Article  CAS  PubMed  Google Scholar 

  29. 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

    Article  PubMed  Google Scholar 

  30. Claus EB, Stowe M, Carter D (2001) Breast carcinoma in situ: risk factors and screening patterns. J Natl Cancer Inst 93(23):1811–1817

    Article  CAS  PubMed  Google Scholar 

  31. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. 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

    Article  PubMed  PubMed Central  Google Scholar 

  33. 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

    Article  PubMed  PubMed Central  Google Scholar 

  34. Nazari SS, Mukherjee P (2018) An overview of mammographic density and its association with breast cancer. Breast Cancer Tokyo Jpn25(3):259–267

    Article  Google Scholar 

  35. Vinnicombe SJ (2018) Breast density: why all the fuss?Clin Radiol 73(4):334–357

    Article  CAS  PubMed  Google Scholar 

  36. 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

    Article  PubMed  Google Scholar 

  37. 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

    Article  CAS  Google Scholar 

  38. 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

    Article  CAS  PubMed  Google Scholar 

  39. 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

    Article  PubMed  PubMed Central  Google Scholar 

  40. 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

    Article  PubMed  Google Scholar 

  41. 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

    Article  CAS  Google Scholar 

  42. 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

    Article  PubMed  Google Scholar 

  43. O’Grady S, Morgan MP (2018) Microcalcifications in breast cancer: from pathophysiology to diagnosis and prognosis. Biochim Biophys Acta 1869(2):310–320

    Google Scholar 

  44. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Weigelt B, Geyer FC, Reis-Filho JS (2010) Histological types of breast cancer: how special are they? Mol Oncol 4(3):192–208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This study was financially supported by the Direction générale de cancérologie of the Quebec Ministry of Health and Social Services.

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Authors and Affiliations

  1. Institut national de santé publique du Québec, 945, Av. Wolfe, Quebec City, G1V 5B3, Canada

    Isabelle Théberge, Nathalie Vandal, Marie-Hélène Guertin & Linda Perron

  2. Département de médecine sociale et préventive, Faculté de Médecine, Université Laval, Quebec City, Canada

    Isabelle Théberge & Linda Perron

  3. Département de santé publique et médecine préventive, CHU de Québec-Université Laval, Hôpital Saint-François d’Assise, Quebec City, Canada

    Linda Perron

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  1. Isabelle Théberge
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  2. Nathalie Vandal
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  4. Linda Perron
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Correspondence to Isabelle Théberge.

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Conflict of interest

All authors declare that they have no conflicts of interest.

Ethical approval

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, MH. 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

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  • DOI: https://doi.org/10.1007/s10549-018-05095-7

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