Breast cancer screening: Evidence of benefit depends on the method used

BMC Medicine

Volumn 10, Issue , 2012, Pages

  Autier, Philippe ^a   Boniol, Mathieu ^a  

^a INTERNATIONAL PREVENTION RESEARCH INSTITUTE   (France)

Author keywords

breast cancer; case control; effectiveness; epidemiology; incidence; mortality; screening

Indexed keywords

ADVANCED CANCER; ARTICLE; BREAST CANCER; CANCER INCIDENCE; CANCER MORTALITY; CANCER SCREENING; CASE CONTROL STUDY; CLINICAL EFFECTIVENESS; DENMARK; ECOLOGY; HUMAN; INCIDENCE BASED MORTALITY; BREAST NEOPLASMS; EARLY DIAGNOSIS; FEMALE; PROCEDURES;

BREAST NEOPLASMS; CASE-CONTROL STUDIES; EARLY DETECTION OF CANCER; FEMALE; HUMANS;

EID: 84870887110     PISSN: None     EISSN: 17417015     Source Type: Journal    
DOI: 10.1186/1741-7015-10-163     Document Type: Article

References (59)

1. Tabár L, Fagerberg CJ, Gad A, Baldetorp L, Holmberg LH, Gröntoft O, Ljungquist U, Lundström B, Månson JC, Eklund G, Day NE, Pettersson F. Reduction in mortality from breast cancer after mass screening with mammography. Randomised trial from the Breast Cancer Screening Working Group of the Swedish National Board of Health and Welfare. Lancet 1985, 1:829-832.
2. Andersson I, Aspegren K, Janzon L, Landberg T, Lindholm K, Linell F, Ljungberg O, Ranstam J, Sigfússon B. Mammographic screening and mortality from breast cancer: the Malmo mammographic screening trial. BMJ 1988, 297:943-948. 10.1136/bmj.297.6654.943, 1834636, 3142562.
3. Frisell J, Lidbrink E, Hellström L, Rutqvist LE. Follow-up after 11 years - update of mortality results in the Stockholm mammographic screening trial. Breast Cancer Res Treat 1997, 45:263-270. 10.1023/A:1005872617944, 9386870.
4. Bjurstam N, Björneld L, Warwick J, Sala E, Duffy SW, Nyström L, Walker N, Cahlin E, Eriksson O, Hafström LO, Lingaas H, Mattsson J, Persson S, Rudenstam CM, Salander H, Säve-Söderbergh J, Wahlin T. The Gothenburg breast screening trial. Cancer 2003, 97:2387-2396. 10.1002/cncr.11361, 12733136.
5. Perry N, Broeders M, de Wolf C, Törnberg S, Holland R, von Karsa L. European guidelines for quality assurance in breast cancer screening and diagnosis. Ann Oncol 2008, 19:614-622.
6. Smith-Bindman R, Chu PW, Miglioretti DL, Sickles EA, Blanks R, Ballard-Barbash R, Bobo JK, Lee NC, Wallis MG, Patnick J, Kerlikowske K. Comparison of screening mammography in the United States and the United Kingdom. JAMA 2003, 290:2129-2137. 10.1001/jama.290.16.2129, 14570948.
7. Fletcher SW. Breast cancer screening: a 35-year perspective. Epidemiol Rev 2011, 33:165-175. 10.1093/epirev/mxr003, 21697257.
8. Dick JF, Gallagher TH, Brenner RJ, Yi JP, Reisch LM, Abraham L, Miglioretti DL, Carney PA, Cutter GR, Elmore JG. Predictors of radiologists' perceived risk of malpractice lawsuits in breast imaging. AJR Am J Roentgenol 2009, 192:327-333. 10.2214/AJR.07.3346, 3138733, 19155390.
9. Amir E, Bedard PL, Ocana A, Seruga B. Benefits and harms of detecting clinically occult breast cancer. J Natl Cancer Inst 2012, 104:1542-1547. 10.1093/jnci/djs394, 22988040.
10. Puliti D, Zappa M. Breast cancer screening: are we seeing the benefit?. BMC Med 2012, 10:106. 10.1186/1741-7015-10-106, 3447729, 22995098.
11. Sasco AJ, Day NE, Walter SD. Case-control studies for the evaluation of screening. J Chron Dis 1986, 39:399-405. 10.1016/0021-9681(86)90126-8, 3700581.
12. Cronin KA, Weed DL, Connor RJ, Prorok PC. Case-control studies of cancer screening: theory and practice. J Natl Cancer Inst 1998, 90:498-504. 10.1093/jnci/90.7.498, 9539244.
13. Otto SJ, Fracheboud J, Verbeek AL, Boer R, Reijerink-Verheij JC, Otten JD, Broeders MJ, de Koning HJ, . National Evaluation Team for Breast Cancer Screening Mammography screening and risk of breast cancer death: a population-based case-control study. Cancer Epidemiol Biomarkers Prev 2012, 21:66-73. 10.1158/1055-9965.EPI-11-0476, 22147362, National Evaluation Team for Breast Cancer Screening.
14. Duffy SW, Tabár L, Fagerberg G, Gad A, Gröntoft O, South MC, Day NE. Breast screening, prognostic factors and survival - results from the Swedish two county study. Br J Cancer 1991, 64:1133-1138. 10.1038/bjc.1991.477, 1977849, 1764377.
15. Aarts MJ, Voogd AC, Duijm LE, Coebergh JW, Louwman WJ. Socioeconomic inequalities in attending the mass screening for breast cancer in the south of the Netherlands--associations with stage at diagnosis and survival. Breast Cancer Res Treat 2011, 128:517-525. 10.1007/s10549-011-1363-z, 21290176.
16. Mook S, Van 't Veer LJ, Rutgers EJ, Ravdin PM, van de Velde AO, van Leeuwen FE, Visser O, Schmidt MK. Independent prognostic value of screen detection in invasive breast cancer. J Natl Cancer Inst 2011, 103:585-597. 10.1093/jnci/djr043, 21350218.
17. Biesheuvel C, Czene K, Orgeás CC, Hall P. The role of mammography screening attendance and detection mode in predicting breast cancer survival - is there added prognostic value?. Cancer Epidemiol 2011, 35:545-550. 10.1016/j.canep.2011.02.008, 21470933.
18. Duffy SW, Cuzick J, Tabár L, Vitak B, Hsiu-His Chen T, Yen MF, Smith RA. Correcting for non-compliance bias in case-control studies to evaluate cancer screening programmes. Appl Statist 2002, 51(Part 2):235-243.
19. Flamant C, Gauthier E, Clavel-Chapelon F. Determinants of non-compliance to recommendations on breast cancer screening among women participating in the French E3N cohort study. Eur J Cancer Prev 2006, 15:27-33. 10.1097/01.cej.0000180666.11958.60, 2756596, 16374226.
20. Ferrante JM, Chen PH, Crabtree BF, Wartenberg D. Cancer screening in women: BMI and adherence to physician recommendations. Am J Prev Med 2007, 32:525-531. 10.1016/j.amepre.2007.02.004, 1986842, 17533069.
21. La Vecchia C, Giordano SH, Hortobagyi GN, Chabner B. Overweight, obesity, diabetes, and risk of breast cancer: interlocking pieces of the puzzle. Oncologist 2011, 16:726-729. 10.1634/theoncologist.2011-0050, 3228228, 21632448.
22. International Agency for Research on Cancer IARC/WHOH Handbooks of Cancer Prevention vol. 7: Breast Cancer Screening 2002, Lyon: IARC Press, International Agency for Research on Cancer.
23. Sant M, Minicozzi P, Allemani C, Cirilli C, Federico M, Capocaccia R, Budroni M, Candela P, Crocetti E, Falcini F, Ferretti S, Fusco M, Giacomin A, La Rosa F, Mangone L, Natali M, Leon MP, Traina A, Tumino R, Zambon P. Regional inequalities in cancer care persist in Italy and can influence survival. Cancer Epidemiol 2012, 36:541-547. 10.1016/j.canep.2012.06.006, 22770694.
24. Wilking U, Jönsson B, Wilking N, Bergh J. Trastuzumab use in breast cancer patients in the six health care regions in Sweden. Acta Oncol 2010, 49:844-850. 10.3109/0284186X.2010.492790, 20615172.
25. Ess S, Savidan A, Frick H, Rageth C, Vlastos G, Lütolf U, Thürlimann B. Geographic variation in breast cancer care in Switzerland. Cancer Epidemiol 2010, 34:116-121. 10.1016/j.canep.2010.01.008, 20185382.
26. Boscoe FP, Johnson CJ, Henry KA, Goldberg DW, Shahabi K, Elkin EB, Ballas LK, Cockburn M. Geographic proximity to treatment for early stage breast cancer and likelihood of mastectomy. Breast 2011, 20:324-328. 10.1016/j.breast.2011.02.020, 21440439.
27. Tabár L, Yen MF, Vitak B, Chen HH, Smith RA, Duffy SW. Mammography service screening and mortality in breast cancer patients: 20-year follow-up before and after introduction of screening. Lancet 2003, 361:1405-1410. 10.1016/S0140-6736(03)13143-1, 12727392.
28. Olsen AH, Njor SH, Vejborg I, Schwartz W, Dalgaard P, Jensen MB, Tange UB, Blichert-Toft M, Rank F, Mouridsen H, Lynge E. Breast cancer mortality in Copenhagen after introduction of mammography screening: cohort study. BMJ 2005, 330:220. 10.1136/bmj.38313.639236.82, 546064, 15649904.
29. 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. Swedish Organised Service Screening Evaluation Group.
30. Jonsson H, Bordas P, Wallin H, Nyström L, Lenner P. Service screening with mammography in Northern Sweden: effects on breast cancer mortality - an update. J Med Screen 2007, 14:87-93. 10.1258/096914107781261918, 17626708.
31. 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. 10.1186/1471-2458-8-38, 2254397, 18226204.
32. Hellquist BN, Duffy SW, Abdsaleh S, Björneld L, Bordás P, Tabár L, Viták B, Zackrisson S, Nyström L, Jonsson H. Effectiveness of population-based service screening with mammography for women ages 40 to 49 years: evaluation of the Swedish Mammography Screening in Young Women (SCRY) cohort. Cancer 2011, 117:714-722. 10.1002/cncr.25650, 20882563.
33. Kalager M, Zelen M, Langmark F, Adami HO. Effect of screening mammography on breast-cancer mortality in Norway. N Engl J Med 2010, 363:1203-1210. 10.1056/NEJMoa1000727, 20860502.
34. Olsen AH, Lynge E, Njor SH, Kumle M, Waaseth M, Braaten T, Lund E. Breast cancer mortality in Norway after the introduction of mammography screening. Int J Cancer 2013, 132:208-214. 10.1002/ijc.27609, 22532175.
35. Autier P, Boniol M, LaVecchia C, Vatten L, Gavin A, Héry C, Heanue M. Disparities in breast cancer mortality trends between thirty European countries: retrospective trend analysis of WHO mortality database. BMJ 2010, 341:c3620. 10.1136/bmj.c3620, 2920378, 20702548.
36. Autier P, Koechlin A, Smans M, Vatten L, Boniol M. Mammography screening and breast cancer mortality in Sweden. J Natl Cancer Inst 2012, 104:1080-1093. 10.1093/jnci/djs272, 22811439.
37. Welch HG, Schwartz LM, Woloshin S. Are increasing 5-year survival rates evidence of success against cancer?. JAMA 2000, 283:2975-2978. 10.1001/jama.283.22.2975, 10865276.
38. Olsson S, Andersson I, Karlberg I, Bjurstam N, Frodis E, Håkansson S. Implementation of service screening with mammography in Sweden: from pilot study to nationwide programme. J Med Screen 2000, 7:14-18. 10.1136/jms.7.1.14, 10807141.
39. 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, 156:491-499.
40. Autier P. Mammography screening before introduction of the national breast screening programme in Norway. Int J Cancer 2012, Epub ahead of print.
41. Smith RA, Duffy SW, Gabe R, Tabar L, Yen AMF, Chen THH. The randomized trials of breast cancer screening: what have we learned?. Radiol Clin North Am 2004, 42:793-806. 10.1016/j.rcl.2004.06.014, 15337416.
42. Fracheboud J, Otto SJ, van Dijck JA, Broeders MJ, Verbeek AL, de Koning HJ, . National Evaluation Team for Breast cancer screening (NETB) Decreased rates of advanced breast cancer due to mammography screening in the Netherlands. Br J Cancer 2004, 91:861-867. 2409867, 15292936, National Evaluation Team for Breast cancer screening (NETB).
43. 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, 27:5919-5923. 10.1200/JCO.2009.22.7041, 19884547.
44. Sigurdsson K, Sigvaldason H. Effectiveness of cervical cancer screening in Iceland, 1964-2002: a study on trends in incidence and mortality and the effect of risk factors. Acta Obstet Gynecol Scand 2006, 85:343-349. 10.1080/00016340500432457, 16553184.
45. Edwards BK, Ward E, Kohler BA, Eheman C, Zauber AG, Anderson RN, Jemal A, Schymura MJ, Lansdorp-Vogelaar I, Seeff LC, van Ballegooijen M, Goede SL, Ries LA. Annual report to the nation on the status of cancer, 1975-2006, featuring colorectal cancer trends and impact of interventions (risk factors, screening, and treatment) to reduce future rates. Cancer 2010, 116:544-573. 10.1002/cncr.24760, 19998273.
46. Autier P, Boniol M, Middleton R, Doré JF, Héry C, Zheng T, Gavin A. Advanced breast cancer incidence following population-based mammographic screening. Ann Oncol 2011, 22:1726-1735. 10.1093/annonc/mdq633, 3144633, 21252058.
47. Esserman L, Shieh Y, Thompson I. Rethinking screening for breast cancer and prostate cancer. JAMA 2009, 302:1685-1692. 10.1001/jama.2009.1498, 19843904.
48. Nederend J, Duijm LE, Voogd AC, Groenewoud JH, Jansen FH, Louwman MW. Trends in incidence and detection of advanced breast cancer at biennial screening mammography in the Netherlands: a population based study. Breast Cancer Research 2012, 14:R10. 10.1186/bcr3091, 3496125, 22230363.
49. Autier P, Boniol M. The incidence of advanced breast cancer in the West Midlands, United Kingdom. Eur J Cancer Prev 2012, 21:217-221. 10.1097/CEJ.0b013e328350b107, 22314850.
50. NETB. National Evaluation Team for Breast Cancer Screening National Evaluation of Breast Cancer Screening in the Netherlands 11th Evaluation Report 2005, Rotterdam and Nijmegen: NETB, NETB. National Evaluation Team for Breast Cancer Screening.
51. Harmer C, Staples M, Kavanagh AM. Evaluation of breast cancer incidence: is the increase due entirely to mammographic screening?. Cancer Causes Control 1999, 10:333-337. 10.1023/A:1008949819969, 10530601.
52. Pell JP, Haw S, Cobbe S, Newby DE, Pell AC, Fischbacher C, McConnachie A, Pringle S, Murdoch D, Dunn F, Oldroyd K, Macintyre P, O'Rourke B, Borland W. Smoke-free legislation and hospitalizations for acute coronary syndrome. New Engl J Med 2008, 359:482-491. 10.1056/NEJMsa0706740, 18669427.
53. Läärä E, Day NE, Hakama M. Trends in mortality from cervical cancer in the Nordic countries: association with organized screening programmes. Lancet 1987, 1:1247-1249.
54. Autier P, Boniol M, Gavin A, Vatten L. Breast cancer mortality in neighbouring European countries with different levels of screening but similar access to treatment: trend analysis of WHO mortality database. BMJ 2011, 343:d4411. 10.1136/bmj.d4411, 3145837, 21798968.
55. Bleyer A. US breast cancer mortality is consistent with European Data. BMJ 2011, 343:d5630. 10.1136/bmj.d5630, 21896600.
56. Otten JD, Broeders MJ, Fracheboud J, Otto SJ, de Koning HJ, Verbeek AL. Impressive time-related influence of the Dutch screening programme on breast cancer incidence and mortality, 1975-2006. Int J Cancer 2008, 123:1929-1934. 10.1002/ijc.23736, 18688863.
57. Blanks RG, Moss SM, McGahan CE, Quinn MJ, Babb PJ. Effect of NHS breast screening programme on mortality from breast cancer in England and Wales, 1990-8: comparison of observed with predicted mortality. BMJ 2000, 321:665-669. 10.1136/bmj.321.7262.665, 27479, 10987769.
58. Thomson CS, Brewster DH, Dewar JA, Twelves CJ. Improvements in survival for women with breast cancer in Scotland between 1987 and 1993: impact of earlier diagnosis and changes in treatment. Eur J Cancer 2004, 40:743-753. 10.1016/j.ejca.2003.08.029, 15010076.
59. Jørgensen KJ, Zahl PH, Gøtzsche PC. Breast cancer mortality in organised mammography screening in Denmark: comparative study. BMJ 2010, 340:c1241. 10.1136/bmj.c1241, 2844939, 20332505.