Skip to main content

Advertisement

Log in

Assessment of cancer screening effectiveness in the era of screening programs

  • ESSAY
  • Published:
European Journal of Epidemiology Aims and scope Submit manuscript

Abstract

Whilst the benefit of detecting and removing cancer precursors in the cervix and the large bowel is unequivocally documented, the balance between benefit and harm due to screening for early detection of breast and prostate cancer remains uncertain after 30–50 years of randomized control trials (RCTs). Concomitantly, traditional RCTs become increasingly unfeasible due to low compliance, contamination of control groups, difficulties to enroll screening naïve individuals, and prohibitively high costs. Therefore, we have systematically reviewed pros and cons with alternative study designs to quantify screening effectiveness. Whilst traditional RCTs should remain gold standard whenever feasible, observational cohort and case–control studies are unlikely to provide the valid evidence needed for health policy decisions. Instead, we advocate two methodological approaches that are novel in assessment of cancer screening effectiveness. One—the difference-in-difference design, well established in health policy and public health research—has a sophisticated ecologic design which unfortunately is feasible only in few countries. Another implies that sequential RCTs become embedded whenever population-based screening programs are implemented.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Laara E, Day NE, Hakama M. Trends in mortality from cervical cancer in the Nordic countries: association with organised screening programmes. Lancet. 1987;1(8544):1247–9.

    Article  CAS  Google Scholar 

  2. Gustafsson L, Ponten J, Zack M, Adami HO. International incidence rates of invasive cervical cancer after introduction of cytological screening. Cancer Causes Control. 1997;8(5):755–63.

    Article  CAS  Google Scholar 

  3. Adami HO, Baron JA, Rothman KJ. Ethics of a prostate cancer screening trial. Lancet. 1994;343(8903):958–60.

    Article  CAS  Google Scholar 

  4. Bretthauer M, Kaminski MF, Loberg M, et al. Population-based colonoscopy screening for colorectal cancer: a randomized clinical trial. JAMA Intern Med. 2016;176(7):894–902.

    Article  Google Scholar 

  5. Autier P, Boniol M. Mammography screening: a major issue in medicine. Eur J Cancer. 2018;90:34–62.

    Article  Google Scholar 

  6. Andriole GL, Crawford ED, Grubb RL 3rd, et al. Prostate cancer screening in the randomized prostate, lung, colorectal, and ovarian cancer screening trial: mortality results after 13 years of follow-up. J Natl Cancer Inst. 2012;104(2):125–32.

    Article  Google Scholar 

  7. Holme Ø, Kalager M, Bretthauer M, Adami HO, Helsingen L, Løberg M. Ongoing trials will not determine the comparative effectiveness of colorectal cancer screening tests. Gastroenterology. 2020. https://doi.org/10.1053/j.gastro.2020.02.071.

    Article  PubMed  Google Scholar 

  8. Kalager M, Tamimi RM, Bretthauer M, Adami HO. Prognosis in women with interval breast cancer: population based observational cohort study. BMJ. 2012;345:e7536.

    Article  Google Scholar 

  9. Holmberg LH, Tabar L, Adami HO, Bergstrom R. Survival in breast cancer diagnosed between mammographic screening examinations. Lancet. 1986;8497(2):27–30.

    Article  Google Scholar 

  10. Andrae B, Andersson TM, Lambert PC, et al. Screening and cervical cancer cure: population based cohort study. BMJ. 2012;344:e900.

    Article  Google Scholar 

  11. Jodal H, Løberg M, Holme O, et al. Mortality from post-screening (interval) colorectal cancers is comparable to cancers from unscreened patients: a randomized sigmoidoscopy trial. Gastroenterology. 2018;155(1787–94):e3.

    Google Scholar 

  12. Adami HO, Csermely P, Veres DV, et al. Are rapidly growing cancers more lethal? Eur J Cancer. 2017;72:210–4.

    Article  Google Scholar 

  13. Gustafsson L, Adami HO. Natural history of cervical neoplasia: consistent results obtained by an identification technique. Br J Cancer. 1989;60(1):132–41.

    Article  CAS  Google Scholar 

  14. Loberg M, Kalager M, Holme O, Hoff G, Adami HO, Bretthauer M. Long-term colorectal-cancer mortality after adenoma removal. N Engl J Med. 2014;371(9):799–807.

    Article  Google Scholar 

  15. Welch HG, Black WC. Overdiagnosis in cancer. J Natl Cancer Inst. 2010;102(9):605–13.

    Article  Google Scholar 

  16. Adami HO. The prostate cancer pseudo-epidemic. Acta Oncol. 2010;49(3):298–304.

    Article  Google Scholar 

  17. Barratt A. Overdiagnosis in mammography screening: a 45 year journey from shadowy idea to acknowledged reality. BMJ. 2015;350:h867.

    Article  Google Scholar 

  18. 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. https://doi.org/10.1136/bmj.j5224.

    Article  PubMed  PubMed Central  Google Scholar 

  19. 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(7):491–9.

    Article  Google Scholar 

  20. Brawley OW. Accepting the existence of breast cancer overdiagnosis. Ann Intern Med. 2017;166(5):364–5.

    Article  Google Scholar 

  21. IARC. Colorectal cancer screening. Handb Cancer Prev. 2019;17:1–300.

    Google Scholar 

  22. Breast cancer screening. Vainio H, Bianchini F, editors. Lyon: IARC Press; 2002.

  23. Phillips N, Coldman A. Comparison of nonbreast cancer incidence, survival and mortality between breast screening program participants and nonparticipants. Int J Cancer. 2008;122(1):197–201.

    Article  CAS  Google Scholar 

  24. Cuzick J, Edwards R, Segnan N. Adjusting for non-compliance and contamination in randomized clinical trials. Stat Med. 1997;16(9):1017–29.

    Article  CAS  Google Scholar 

  25. Duffy S, Cuzick J, Tabar L, et al. Correcting for non-compliance bias in case–control studies to evaluate cancer screening programmes. J R Stat Soc Ser C Appl Stat. 2008;51:235–43.

    Article  Google Scholar 

  26. Schneeweiss S, Rassen JA, Glynn RJ, Avorn J, Mogun H, Brookhart MA. High-dimensional propensity score adjustment in studies of treatment effects using health care claims data. Epidemiology. 2009;20(4):512–22.

    Article  Google Scholar 

  27. Carter JL, Coletti RJ, Harris RP. Quantifying and monitoring overdiagnosis in cancer screening: a systematic review of methods. BMJ. 2015;350:g7773.

    Article  Google Scholar 

  28. Wing C, Simon K, Bello-Gomez RA. Designing difference in difference studies: best practices for public health policy research. Ann Rev Publ Health. 2018;39:453–69.

    Article  Google Scholar 

  29. Kalager M, Zelen M, Langmark F, Adami HO. Effect of screening mammography on breast-cancer mortality in Norway. N Engl J Med. 2010;363(13):1203–10.

    Article  CAS  Google Scholar 

  30. Olsen AH, Lynge E, Njor SH, et al. Breast cancer mortality in Norway after the introduction of mammography screening. Int J Cancer. 2013;132(1):208–14.

    Article  CAS  Google Scholar 

  31. Kalager M, Bretthauer M. Improving cancer screening programs. Science. 2020;367(6474):143–4.

    CAS  PubMed  Google Scholar 

  32. Hakama M, Pukkala E, Heikkila M, Kallio M. Effectiveness of the public health policy for breast cancer screening in Finland: population based cohort study. BMJ. 1997;314(7084):864–7.

    Article  CAS  Google Scholar 

  33. Pitkaniemi J, Seppa K, Hakama M, et al. Effectiveness of screening for colorectal cancer with a faecal occult-blood test, in Finland. BMJ Open Gastroenterol. 2015;2(1):e000034.

    Article  CAS  Google Scholar 

  34. Cancer Registry of Norway. HPV i primærscreening. Available at: www.kreftregisteret.no/en/screening/Cervical-Cancer-Screening-Programme/Helsepersonell/screeningstrategi-og-nasjonale-retningslinjer/hpv-i-primarscreening/.

  35. Kaminski MF, Kraszewska E, Rupinski M, Laskowska M, Wieszczy P, Regula J. Design of the polish colonoscopy screening program: a randomized health services study. Endoscopy. 2015;47(12):1144–50.

    Article  Google Scholar 

  36. Ioannidis JP. Why most published research findings are false. PLoS Med. 2005;2(8):e124.

    Article  Google Scholar 

Download references

Funding

This manuscript was written without any funding support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hans-Olov Adami.

Ethics declarations

Conflict of interest

The authors declare no conflict of interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Adami, HO., Bretthauer, M. & Kalager, M. Assessment of cancer screening effectiveness in the era of screening programs. Eur J Epidemiol 35, 891–897 (2020). https://doi.org/10.1007/s10654-020-00684-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10654-020-00684-7

Keywords

Navigation