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Published in: BMC Cancer 1/2018

Open Access 01-12-2018 | Research article

The impact of mammography screening programmes on incidence of advanced breast cancer in Europe: a literature review

Authors: M. J. M. Broeders, P. Allgood, S. W. Duffy, S. Hofvind, I. D. Nagtegaal, E. Paci, S. M. Moss, L. Bucchi

Published in: BMC Cancer | Issue 1/2018

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Abstract

Background

Observational studies have reported conflicting results on the impact of mammography service screening programmes on the advanced breast cancer rate (ABCR), a correlation that was firmly established in randomized controlled trials. We reviewed and summarized studies of the effect of service screening programmes in the European Union on ABCR and discussed their limitations.

Methods

The PubMed database was searched for English language studies published between 01-01-2000 and 01–06-2018. After inspection of titles and abstracts, 220 of the 8644 potentially eligible papers were considered relevant. Their abstracts were reviewed by groups of two authors using predefined criteria. Fifty studies were selected for full paper review, and 22 of these were eligible. A theoretical framework for their review was developed. Review was performed using a ten-point checklist of the methodological caveats in the analysis of studies of ABCR and a standardised assessment form designed to extract quantitative and qualitative information.

Results

Most of the evaluable studies support a reduction in ABCR following the introduction of screening. However, all studies were challenged by issues of design and analysis which could at least potentially cause bias, and showed considerable variation in the estimated effect. Problems were observed in duration of follow-up time, availability of reliable reference ABCR, definition of advanced stage, temporal variation in the proportion of unknown-stage cancers, and statistical approach.

Conclusions

We conclude that much of the current controversy on the impact of service screening programmes on ABCR is due to observational data that were gathered and/or analysed with methodological approaches which could not capture stage effects in full. Future research on this important early indicator of screening effectiveness should focus on establishing consensus in the correct methodology.
Appendix
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Literature
1.
go back to reference Autier P, Héry C, Haukka J, Boniol M, Byrnes G. Advanced breast cancer and breast cancer mortality in randomized controlled trials on mammography screening. J Clin Oncol. 2009;27:5915–23.CrossRef Autier P, Héry C, Haukka J, Boniol M, Byrnes G. Advanced breast cancer and breast cancer mortality in randomized controlled trials on mammography screening. J Clin Oncol. 2009;27:5915–23.CrossRef
2.
go back to reference Tabar L, Fagerberg G, Duffy SW, Day NE, Gad A, Grontoft O. Update of the Swedish two-county program of mammographic screening for breast cancer. Radiol Clin N Am. 1992;30:187–210.PubMed Tabar L, Fagerberg G, Duffy SW, Day NE, Gad A, Grontoft O. Update of the Swedish two-county program of mammographic screening for breast cancer. Radiol Clin N Am. 1992;30:187–210.PubMed
3.
go back to reference Tabár L, Yen AM, Wu WY, Chen SL, Chiu SY, Fann JC, et al. Insights from the breast cancer screening trials: how screening affects the natural history of breast cancer and implications for evaluating service screening programs. Breast J. 2015;21:13–20.CrossRefPubMed Tabár L, Yen AM, Wu WY, Chen SL, Chiu SY, Fann JC, et al. Insights from the breast cancer screening trials: how screening affects the natural history of breast cancer and implications for evaluating service screening programs. Breast J. 2015;21:13–20.CrossRefPubMed
4.
go back to reference Nagtegaal ID, Duffy SW. Reduction in rate of node metastases with breast screening: consistency of association with tumor size. Breast Cancer Res Treat. 2013;137:653–63.CrossRefPubMed Nagtegaal ID, Duffy SW. Reduction in rate of node metastases with breast screening: consistency of association with tumor size. Breast Cancer Res Treat. 2013;137:653–63.CrossRefPubMed
5.
go back to reference Autier P, Boniol M, Middleton R, Doré JF, Héry C, Zheng T, et al. Advanced breast cancer incidence following population-based mammographic screening. Ann Oncol. 2011;22:1726–35.CrossRefPubMedPubMedCentral Autier P, Boniol M, Middleton R, Doré JF, Héry C, Zheng T, et al. Advanced breast cancer incidence following population-based mammographic screening. Ann Oncol. 2011;22:1726–35.CrossRefPubMedPubMedCentral
6.
go back to reference Bleyer A, Welch HG. Effect of three decades of screening mammography on breast-cancer incidence. N Engl J Med. 2012;367:1998–2005.CrossRefPubMed Bleyer A, Welch HG. Effect of three decades of screening mammography on breast-cancer incidence. N Engl J Med. 2012;367:1998–2005.CrossRefPubMed
7.
go back to reference Welch HG, Prorok PC, O'Malley AJ, Kramer BS. Breast-cancer tumor size, overdiagnosis, and mammography screening effectiveness. N Engl J Med. 2016;375:1438–47.CrossRefPubMed Welch HG, Prorok PC, O'Malley AJ, Kramer BS. Breast-cancer tumor size, overdiagnosis, and mammography screening effectiveness. N Engl J Med. 2016;375:1438–47.CrossRefPubMed
8.
go back to reference Jørgensen KJ, Gøtzsche PC, Kalager M, Zahl P-H. Breast cancer screening in Denmark. A cohort study of tumor size and overdiagnosis. Ann Intern Med. 2017;166:313–23.CrossRefPubMed Jørgensen KJ, Gøtzsche PC, Kalager M, Zahl P-H. Breast cancer screening in Denmark. A cohort study of tumor size and overdiagnosis. Ann Intern Med. 2017;166:313–23.CrossRefPubMed
9.
go back to reference Ernst MF, Voogd AC, Coebergh JW, Roukema JA. Breast carcinoma diagnosis, treatment, and prognosis before and after the introduction of mass mammographic screening. Cancer. 2004;100:1337–44.CrossRefPubMed Ernst MF, Voogd AC, Coebergh JW, Roukema JA. Breast carcinoma diagnosis, treatment, and prognosis before and after the introduction of mass mammographic screening. Cancer. 2004;100:1337–44.CrossRefPubMed
10.
go back to reference Hofvind S, Lee CI, Elmore JG. Stage-specific breast cancer incidence rates among participants and non-participants of a population-based mammographic screening program. Breast Cancer Res Treat. 2012;135:291–9.CrossRefPubMedPubMedCentral Hofvind S, Lee CI, Elmore JG. Stage-specific breast cancer incidence rates among participants and non-participants of a population-based mammographic screening program. Breast Cancer Res Treat. 2012;135:291–9.CrossRefPubMedPubMedCentral
11.
go back to reference Mook S, Van ‘t Veer LJ, Rutgers EJ, Ravdin PM, Van de Velde AO, Van Leeuwen FE, et al. Independent prognostic value of screen detection in invasive breast cancer. J Natl Cancer Inst. 2011;103:585–97.CrossRefPubMed Mook S, Van ‘t Veer LJ, Rutgers EJ, Ravdin PM, Van de Velde AO, Van Leeuwen FE, et al. Independent prognostic value of screen detection in invasive breast cancer. J Natl Cancer Inst. 2011;103:585–97.CrossRefPubMed
12.
go back to reference Nederend J, Duijm LE, Voogd AC, Groenewoud JH, Jansen FH, Louwman MW. Trends in incidence and detection of advanced cancer at biennial screening mammography in the Netherlands: a population based study. Breast Cancer Res. 2012;14:R10.CrossRefPubMedPubMedCentral Nederend J, Duijm LE, Voogd AC, Groenewoud JH, Jansen FH, Louwman MW. Trends in incidence and detection of advanced cancer at biennial screening mammography in the Netherlands: a population based study. Breast Cancer Res. 2012;14:R10.CrossRefPubMedPubMedCentral
13.
go back to reference Autier P, Boniol M. The incidence of advanced breast cancer in the west midlands. United Kingdom Eur J Cancer Prev. 2012;21:217–21.CrossRefPubMed Autier P, Boniol M. The incidence of advanced breast cancer in the west midlands. United Kingdom Eur J Cancer Prev. 2012;21:217–21.CrossRefPubMed
14.
go back to reference Fracheboud J, Otto SJ, Van Dijck JAAM, Broeders MJ, Verbeek AL, de Koning HJ, et al. Decreased rates of advanced breast cancer due to mammography screening in the Netherlands. Br J Cancer. 2004;91:861–7.CrossRefPubMedPubMedCentral Fracheboud J, Otto SJ, Van Dijck JAAM, Broeders MJ, Verbeek AL, de Koning HJ, et al. Decreased rates of advanced breast cancer due to mammography screening in the Netherlands. Br J Cancer. 2004;91:861–7.CrossRefPubMedPubMedCentral
15.
go back to reference Foca F, Mancini S, Bucchi L, Zappa M, Naldoni C, Falcini F, et al. Decreasing incidence of late-stage breast cancer after the introduction of organized mammographic screening in Italy. Cancer. 2013;119:2022–8.CrossRefPubMed Foca F, Mancini S, Bucchi L, Zappa M, Naldoni C, Falcini F, et al. Decreasing incidence of late-stage breast cancer after the introduction of organized mammographic screening in Italy. Cancer. 2013;119:2022–8.CrossRefPubMed
16.
go back to reference Paci E. EUROSCREEN working group. Summary of the evidence of breast cancer service screening outcomes in Europe and first estimate of the benefit and harm balance sheet. J Med Screen. 2012;19(Suppl 1):5–13.CrossRefPubMed Paci E. EUROSCREEN working group. Summary of the evidence of breast cancer service screening outcomes in Europe and first estimate of the benefit and harm balance sheet. J Med Screen. 2012;19(Suppl 1):5–13.CrossRefPubMed
17.
go back to reference UICC. TNM classification of malignant tumours. 7th ed. New York: Wiley-Blackwell; 2009. UICC. TNM classification of malignant tumours. 7th ed. New York: Wiley-Blackwell; 2009.
18.
go back to reference Maaskant AJ, van de Poll-Franse LV, Voogd AC, Coebergh JW, Tutein Nolthenius-Puylaert MBCJE, Nieuwenhuijzen GAP. Stage migration due to introduction of the sentinel node procedure: a population-based study. Breast Cancer Res Treat. 2009;113:173–9.CrossRefPubMed Maaskant AJ, van de Poll-Franse LV, Voogd AC, Coebergh JW, Tutein Nolthenius-Puylaert MBCJE, Nieuwenhuijzen GAP. Stage migration due to introduction of the sentinel node procedure: a population-based study. Breast Cancer Res Treat. 2009;113:173–9.CrossRefPubMed
19.
go back to reference Larsen IK, Myklebust TÅ, Johannesen TB, Møller B, Hofvind S. Stage-specific incidence and survival of breast cancer in Norway: the implications of changes in coding and classification practice. Breast. 2018;38:107–13.CrossRefPubMed Larsen IK, Myklebust TÅ, Johannesen TB, Møller B, Hofvind S. Stage-specific incidence and survival of breast cancer in Norway: the implications of changes in coding and classification practice. Breast. 2018;38:107–13.CrossRefPubMed
20.
go back to reference Miller AB, Wall C, Baines CJ, Sun P, To T, Narod SA. Twenty five year follow-up for breast cancer incidence and mortality of the Canadian National Breast Screening Study: a randomised screening trial. BMJ. 2014;348:g366.CrossRefPubMedPubMedCentral Miller AB, Wall C, Baines CJ, Sun P, To T, Narod SA. Twenty five year follow-up for breast cancer incidence and mortality of the Canadian National Breast Screening Study: a randomised screening trial. BMJ. 2014;348:g366.CrossRefPubMedPubMedCentral
21.
go back to reference Bucchi L, Barchielli A, Ravaioli A, Frederico M, De Lisi V, Ferretti S, et al. Screen-detected vs clinical breast cancer: the advantage in the relative risk of lymph node metastases decreases with increasing tumor size. Br J Cancer. 2005;92:156–61.CrossRefPubMed Bucchi L, Barchielli A, Ravaioli A, Frederico M, De Lisi V, Ferretti S, et al. Screen-detected vs clinical breast cancer: the advantage in the relative risk of lymph node metastases decreases with increasing tumor size. Br J Cancer. 2005;92:156–61.CrossRefPubMed
22.
go back to reference Anttila A, Läärä E. Cervix cancer: geographical correlations. In: Sankila R, Démaret E, Hakama M, Lynge E, Schouten LJ, Parkin DM, editors. Evaluation and monitoring of screening programmes. Luxembourg: Office for Official Publications of the European Communities; 2001. p. 77–98. Anttila A, Läärä E. Cervix cancer: geographical correlations. In: Sankila R, Démaret E, Hakama M, Lynge E, Schouten LJ, Parkin DM, editors. Evaluation and monitoring of screening programmes. Luxembourg: Office for Official Publications of the European Communities; 2001. p. 77–98.
23.
go back to reference Coburn NG, Chung MA, Fulton J, Cady B. Decreased breast cancer tumor size, stage, and mortality in Rhode Island: an example of a well-screened population. Cancer Control. 2004;11:222–30.CrossRefPubMed Coburn NG, Chung MA, Fulton J, Cady B. Decreased breast cancer tumor size, stage, and mortality in Rhode Island: an example of a well-screened population. Cancer Control. 2004;11:222–30.CrossRefPubMed
24.
go back to reference Escobedo LG, Zhong Z, Key C. Breast and cervical cancer screening and disease incidence and stage in New Mexico. Cancer Causes Control. 2002;13:137–45.CrossRefPubMed Escobedo LG, Zhong Z, Key C. Breast and cervical cancer screening and disease incidence and stage in New Mexico. Cancer Causes Control. 2002;13:137–45.CrossRefPubMed
25.
go back to reference Harmer C, Staples M, Kavanagh AM. Evaluation of breast cancer incidence: is the increase due entirely to mammographic screening? Cancer Causes Control. 1999;10:333–7.CrossRefPubMed Harmer C, Staples M, Kavanagh AM. Evaluation of breast cancer incidence: is the increase due entirely to mammographic screening? Cancer Causes Control. 1999;10:333–7.CrossRefPubMed
26.
go back to reference Kricker A, Farac K, Smith D, Sweeny A, McCredie M, Armstrong BK. Breast cancer in New South Wales in 1972-1995: tumor size and the impact of mammographic screening. Int J Cancer. 1999;81:877–80.CrossRefPubMed Kricker A, Farac K, Smith D, Sweeny A, McCredie M, Armstrong BK. Breast cancer in New South Wales in 1972-1995: tumor size and the impact of mammographic screening. Int J Cancer. 1999;81:877–80.CrossRefPubMed
27.
go back to reference Broeders M, Moss S, Nyström L, Njor S, Jonsson H, Paap E, et al. The impact of mammographic screening on breast cancer mortality in Europe: a review of observational studies. J Med Screen. 2012;19(Suppl 1):14–25.CrossRefPubMed Broeders M, Moss S, Nyström L, Njor S, Jonsson H, Paap E, et al. The impact of mammographic screening on breast cancer mortality in Europe: a review of observational studies. J Med Screen. 2012;19(Suppl 1):14–25.CrossRefPubMed
28.
go back to reference Moss SM, Nyström L, Jonsson H, Paci E, Lynge E, Njor S, et al. The impact of mammographic screening on breast cancer mortality in Europe: a review of trend studies. J Med Screen. 2012;19(Suppl 1):26–32.CrossRefPubMed Moss SM, Nyström L, Jonsson H, Paci E, Lynge E, Njor S, et al. The impact of mammographic screening on breast cancer mortality in Europe: a review of trend studies. J Med Screen. 2012;19(Suppl 1):26–32.CrossRefPubMed
29.
go back to reference Barchielli A, Paci E. Trends in breast cancer mortality, incidence, and survival, and mammographic screening in Tuscany. Italy Cancer Causes Control. 2001;12:249–55.CrossRefPubMed Barchielli A, Paci E. Trends in breast cancer mortality, incidence, and survival, and mammographic screening in Tuscany. Italy Cancer Causes Control. 2001;12:249–55.CrossRefPubMed
30.
go back to reference Paci E, Duffy SW, Giorgi D, Zappa M, Crocetti E, Vezzosi V, et al. Quantification of the effect of mammographic screening on fatal breast cancers: the Florence Programme 1990-96. Br J Cancer. 2002;87:65–9.CrossRefPubMedPubMedCentral Paci E, Duffy SW, Giorgi D, Zappa M, Crocetti E, Vezzosi V, et al. Quantification of the effect of mammographic screening on fatal breast cancers: the Florence Programme 1990-96. Br J Cancer. 2002;87:65–9.CrossRefPubMedPubMedCentral
31.
go back to reference Schouten LJ, de Rijke JM, Huveneers JA, Verbeek ALM. Rising incidence of breast cancer after completion of the first prevalent round of the breast cancer screening programme. J Med Screen. 2002;9:120–4.CrossRefPubMed Schouten LJ, de Rijke JM, Huveneers JA, Verbeek ALM. Rising incidence of breast cancer after completion of the first prevalent round of the breast cancer screening programme. J Med Screen. 2002;9:120–4.CrossRefPubMed
32.
go back to reference Buiatti E, Barchielli A, Bartolacci S, Federico M, De Lisi V, Bucchi L, et al. The impact of organised screening programmes on the stage-specific incidence of breast cancer in some Italian areas. Eur J Cancer. 2003;39:1776–82.CrossRefPubMed Buiatti E, Barchielli A, Bartolacci S, Federico M, De Lisi V, Bucchi L, et al. The impact of organised screening programmes on the stage-specific incidence of breast cancer in some Italian areas. Eur J Cancer. 2003;39:1776–82.CrossRefPubMed
33.
go back to reference Swedish Organised Service Screening Evaluation Group. Effect of mammographic service screening on stage at presentation of breast cancers in Sweden. Cancer. 2007;109:2205–12.CrossRef Swedish Organised Service Screening Evaluation Group. Effect of mammographic service screening on stage at presentation of breast cancers in Sweden. Cancer. 2007;109:2205–12.CrossRef
34.
go back to reference Anttila A, Sarkeala T, Hakulinen T, Heinävaara S. Impacts of the Finnish service screening programme on breast cancer rates. BMC Public Health. 2008;8:38.CrossRefPubMedPubMedCentral Anttila A, Sarkeala T, Hakulinen T, Heinävaara S. Impacts of the Finnish service screening programme on breast cancer rates. BMC Public Health. 2008;8:38.CrossRefPubMedPubMedCentral
35.
go back to reference Hofvind S, Sørum R, Thoresen S. Incidence and tumor characteristics of breast cancer diagnosed before and after implementation of a population-based screening program. Acta Oncol. 2008;47:225–31.CrossRefPubMed Hofvind S, Sørum R, Thoresen S. Incidence and tumor characteristics of breast cancer diagnosed before and after implementation of a population-based screening program. Acta Oncol. 2008;47:225–31.CrossRefPubMed
36.
go back to reference Kalager M, Adami HO, Bretthauer M, Tamimi RM. Overdiagnosis of invasive breast cancer due to mammography screening: results from the Norwegian screening program. Ann Intern Med. 2012;156:491–9.CrossRefPubMed Kalager M, Adami HO, Bretthauer M, Tamimi RM. Overdiagnosis of invasive breast cancer due to mammography screening: results from the Norwegian screening program. Ann Intern Med. 2012;156:491–9.CrossRefPubMed
37.
go back to reference Christiansen P, Vejborg I, Kroman N, Holten I, Garne JP, Vedsted P, et al. Position paper: breast cancer screening, diagnosis, and treatment in Denmark. Acta Oncol. 2014;53:433–44.CrossRefPubMed Christiansen P, Vejborg I, Kroman N, Holten I, Garne JP, Vedsted P, et al. Position paper: breast cancer screening, diagnosis, and treatment in Denmark. Acta Oncol. 2014;53:433–44.CrossRefPubMed
38.
go back to reference Lousdal ML, Kristiansen IS, Møller B, Støvring H. Trends in breast cancer stage distribution before, during and after introduction of a screening programme in Norway. Eur J Pub Health. 2014;24:1017–22.CrossRef Lousdal ML, Kristiansen IS, Møller B, Støvring H. Trends in breast cancer stage distribution before, during and after introduction of a screening programme in Norway. Eur J Pub Health. 2014;24:1017–22.CrossRef
39.
go back to reference Lousdal ML, Kristiansen IS, Møller B, Støvring H. Effect of organised mammography screening on stage-specific incidence in Norway: population study. Br J Cancer. 2016;114:590–6.CrossRefPubMedPubMedCentral Lousdal ML, Kristiansen IS, Møller B, Støvring H. Effect of organised mammography screening on stage-specific incidence in Norway: population study. Br J Cancer. 2016;114:590–6.CrossRefPubMedPubMedCentral
40.
go back to reference Simbrich A, Wellmann I, Heidrich J, Heidinger O, Hense HW. Trends in advanced breast cancer incidence rates after implementation of a mammography screening program in a German population. Cancer Epidemiol. 2016;44:44–51.CrossRefPubMed Simbrich A, Wellmann I, Heidrich J, Heidinger O, Hense HW. Trends in advanced breast cancer incidence rates after implementation of a mammography screening program in a German population. Cancer Epidemiol. 2016;44:44–51.CrossRefPubMed
41.
go back to reference Autier P, Boniol M, Koechlin A, Pizot C, Boniol M. Effectiveness of and overdiagnosis from mammography screening in the Netherlands: population based study. BMJ. 2017;359:j5224.CrossRefPubMedPubMedCentral Autier P, Boniol M, Koechlin A, Pizot C, Boniol M. Effectiveness of and overdiagnosis from mammography screening in the Netherlands: population based study. BMJ. 2017;359:j5224.CrossRefPubMedPubMedCentral
42.
go back to reference Hanley JA, Hannigan A, O’Brien KM. Mortality reductions due to mammography screening: contemporary population-based data. PLoS One. 2017;12:e0188947.CrossRefPubMedPubMedCentral Hanley JA, Hannigan A, O’Brien KM. Mortality reductions due to mammography screening: contemporary population-based data. PLoS One. 2017;12:e0188947.CrossRefPubMedPubMedCentral
43.
go back to reference Molinié F, Delacour-Billon S, Tretarre B, Delafosse P, Seradour B, Colonna M. Breast cancer incidence: decreasing trend in large tumours in women aged 50-74. J Med Screen. 2017;24:189–94.CrossRefPubMed Molinié F, Delacour-Billon S, Tretarre B, Delafosse P, Seradour B, Colonna M. Breast cancer incidence: decreasing trend in large tumours in women aged 50-74. J Med Screen. 2017;24:189–94.CrossRefPubMed
44.
go back to reference Puliti D, Bucchi L, Mancini S, Paci E, Baracco S, Campari C, et al. Advanced breast cancer rates in the epoch of service screening: the 400,000 women cohort study from Italy. Eur J Cancer. 2017;75:109–16.CrossRefPubMed Puliti D, Bucchi L, Mancini S, Paci E, Baracco S, Campari C, et al. Advanced breast cancer rates in the epoch of service screening: the 400,000 women cohort study from Italy. Eur J Cancer. 2017;75:109–16.CrossRefPubMed
45.
go back to reference Fracheboud J, De Gelder R, Otto SJ, Van Ineveld BM, Otten JDM, Broeders MJM, et al. National evaluation of breast cancer screening in the Netherlands. In: Twelfth evaluation report (in Dutch). XII. Rotterdam: Dept of Public Health, Erasmus University Rotterdam; 1990-2007. p. 2009. Fracheboud J, De Gelder R, Otto SJ, Van Ineveld BM, Otten JDM, Broeders MJM, et al. National evaluation of breast cancer screening in the Netherlands. In: Twelfth evaluation report (in Dutch). XII. Rotterdam: Dept of Public Health, Erasmus University Rotterdam; 1990-2007. p. 2009.
46.
go back to reference Swedish Organised Service Screening Evaluation Group. Reduction in breast cancer mortality from organized service screening with mammography: 1. Further confirmation with extended data. Cancer Epidemiol Biomarkers Prev. 2006;15:45–51.CrossRef Swedish Organised Service Screening Evaluation Group. Reduction in breast cancer mortality from organized service screening with mammography: 1. Further confirmation with extended data. Cancer Epidemiol Biomarkers Prev. 2006;15:45–51.CrossRef
47.
go back to reference Nagtegaal ID, Allgood PC, Duffy SW, Kearins O, Sullivan EO, Tappenden N, et al. Prognosis and pathology of screen-detected carcinomas: how different are they? Cancer. 2011;117:1360–8.CrossRefPubMed Nagtegaal ID, Allgood PC, Duffy SW, Kearins O, Sullivan EO, Tappenden N, et al. Prognosis and pathology of screen-detected carcinomas: how different are they? Cancer. 2011;117:1360–8.CrossRefPubMed
48.
go back to reference Lawrence G, O'Sullivan E, Kearins O, Tappenden N, Martin K, Wallis M. Screening histories of invasive breast cancers diagnosed 1989-2006 in the west midlands, UK: variation with time and impact on 10-year survival. J Med Screen. 2009;16:186–92.CrossRefPubMed Lawrence G, O'Sullivan E, Kearins O, Tappenden N, Martin K, Wallis M. Screening histories of invasive breast cancers diagnosed 1989-2006 in the west midlands, UK: variation with time and impact on 10-year survival. J Med Screen. 2009;16:186–92.CrossRefPubMed
49.
go back to reference Broeders M, Nyström L, Ascunce N, Riza E, Becker N, Törnberg S, et al. Epidemiological guidelines for quality assurance in breast cancer screening. In: Perry N, Broeders M, de Wolf C, Törnberg S, Holland R, von Karsa L, editors. European guidelines for quality assurance in breast cancer screening and diagnosis. Luxembourg: Office for Official Publications of the European Communities; 2006. p. 15–56. Broeders M, Nyström L, Ascunce N, Riza E, Becker N, Törnberg S, et al. Epidemiological guidelines for quality assurance in breast cancer screening. In: Perry N, Broeders M, de Wolf C, Törnberg S, Holland R, von Karsa L, editors. European guidelines for quality assurance in breast cancer screening and diagnosis. Luxembourg: Office for Official Publications of the European Communities; 2006. p. 15–56.
50.
go back to reference Day NE, Williams DRR, Khaw KT. Breast cancer screening programmes: the development of a monitoring and evaluation system. Br J Cancer. 1989;59:954–8.CrossRefPubMedPubMedCentral Day NE, Williams DRR, Khaw KT. Breast cancer screening programmes: the development of a monitoring and evaluation system. Br J Cancer. 1989;59:954–8.CrossRefPubMedPubMedCentral
Metadata
Title
The impact of mammography screening programmes on incidence of advanced breast cancer in Europe: a literature review
Authors
M. J. M. Broeders
P. Allgood
S. W. Duffy
S. Hofvind
I. D. Nagtegaal
E. Paci
S. M. Moss
L. Bucchi
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2018
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-018-4666-1

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