Overestimated lead times in cancer screening has led to substantial underestimation of overdiagnosis

British Journal of Cancer

Volumn 109, Issue 7, 2013, Pages 2014-2019

  Zahl, P H ^a   Jorgensen K J ^b   Gotzsche P C ^b  

^a NORWEGIAN INSTITUTE OF PUBLIC HEALTH   (Norway)

^b Rigshospitalet   (Denmark)

Author keywords

lead time; overdiagnosis; screening

Indexed keywords

ADULT; AGED; ARTICLE; BREAST CANCER; CANCER INCIDENCE; CANCER SCREENING; DIAGNOSTIC ERROR; FEMALE; HUMAN; LEAD TIME; MAMMOGRAPHY; PRIORITY JOURNAL; TIME;

AGED; BREAST NEOPLASMS; DIAGNOSTIC ERRORS; EARLY DETECTION OF CANCER; FEMALE; HUMANS; INCIDENCE; MAMMOGRAPHY; MASS SCREENING; MIDDLE AGED;

EID: 84885182193     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2013.427     Document Type: Article

References (35)

1. Andriole GL, Crawford ED, Grubb III RL, Buys SS, Chia D, Church TR, Fouad MN, Isaacs C, Kvale PA, Reding DJ, Weissfeld JL, Yokochi LA, O'Brien B, Ragard LR, Clapp JD, Rathmell JM, Riley TL, Hsing AW, Izmirlian G, Pinsky PF, Kramer BS, Miller AB, Gohagan JK, Prorok PC (2012) Prostate cancer screening in the randomized prostate, lung, colorectal and ovarian cancer screening trial: mortality results after 13 years follow-up. JNCI 104: 125-132.
2. Aoki T, Nakata H, Watanabe H, Nakamura K, Kasai T, Hashimoto H, Yasumoto K, Kido M (2000) Evolution of peripheral lung adenocarcinomas. CT findings correlated with histology and tumor doubling time. Am J Roentgenol 74: 763-876.
3. Bleyer A, Welch GH (2012) Effect of three decades of screening mammography on breast-cancer incidence. N Engl J Med 367: 1998-2005.
4. Boer R, Mamerdam P, de Koning H, van Oortmarssen G (1994) Extra incidence caused by mammographic screening. Lancet 343: 979.
5. Draisma G, Boer R, Otto SJ, van der Cruijsen I, Damhuis RAM, Schröder FH, de Koning HJ (2003) Lead time and overdetection due to prostate-specific antigen screening: estimates from the European randomized study on screening for breast cancer. JNCI 95: 868-878.
6. Draisma G, Etzioni R, Tsodikov A, Mariotto A, Wever E, Guliati R, Feuer E, de Koning H (2009) Lead time and overdiagnosis in prostate-specific antigen screening: importance of methods and context. JNCI 101: 374-383.
7. Duffy SW, Hill C, Chen H-H, Tabar L, Day NE (1995) Estimation of mean sojourn time in breast cancer screening using a Markov chain model of both entry to and exit from the preclinical detectable phase. Stat Med 14: 1531-1543.
8. Esserman L, Shieh Y, Thompson I (2009) Rethinking screening for breast cancer and prostate cancer. JAMA 302: 1685-1692.
9. Falk RS, Hofvind R, Skaane S, Haldorsen T (2013) Overdiagnosis among women attending a population-based mammography screening program. Int J Cancer 133(3): 705-712.
10. Folkman J, Watson K, Ingber D, Hanahan D (1989) Induction of angiogenesis during the transition from hyperplasia to neoplasia. Nature 339: 58-61.
11. Fryback DG, Stout NK, Rosenberg MA, Trentham-Dietz A, Kuruchittham V, Remington PL (2006) The Wisconsin breast cancer epidemiology simulation model. J Natl Cancer Inst Monogr 36: 37-47.
12. Gøtzsche PC. (2012) Mammography Screening: Truth, Lies and Controversy. Radcliffe Publishing: London.
13. Gøtzsche PC, Jørgensen KJ, Zahl P-H, Mæhlen J (2012) Why mammography screening has not lived up to expectations from the randomised trials. Cancer Causes Control 23: 15-21.
14. Jørgensen KJ, Gøtzsche PC (2009) Overdiagnosis in publicly organised mammography screening programmes: systematic review of incidence trends. BMJ 339: b2587.
15. Kalager M, Adami H-O, Bretthauer M, Tamimi RM (2012) Overdiagnosis of invasive breast cancer due to mammography screening: results from the Norwegian Screening program. Ann Intern Med 156: 491-499.
16. Marmot MG, Altman DG, Cameron DA, Dewar JA, Thompson SG, Wilcox M. Independent UK Panel on Breast Cancer Screening (2012) The benefits and harms of breast cancer screening: an independent review. Lancet 380: 1778-1786.
17. Njor SH, Olsen AH, Blichert-Toft M, Schwartz W, Vejborg I, Lynge E (2013) Overdiagnosis in screening mammography in Denmark: population based cohort study. BMJ 346: f1064.
18. Printz C (2001) Spontaneous regression of melanoma may offer insight into cancer immunology. JNCI 1047-1048.
19. Prorok PC (1976) The theory of periodic screening I: lead time and proportion detected. Adv Appl Probability 8: 127-143.
20. Schilling FH, Spix C, Berthold F, Erttmann R, Fehse N, Hero B, Klein G, Sander J, Schwartz K, Treuner J, Zorn U, Michaelis J (2002) Neuroblastoma screening at one year of age. N Engl J Med 346: 1047-1053.
21. Seigneurin A, Francois O, Labarere J, Oudeville P, Monlong J, Colonna M (2011) Overdiagnosis from non-progressive cancer detected by screening mammography: stochastic simulation study with calibration to population based registry data. BMJ 343: d7017.
22. Smith RA, Duffy SW, Gabe R, Tabar L, Yen AM, Chen TH (2004) The randomized trials of breast cancer screening: what have we learned? Radiol Clin North Am 42: 793-806.
23. Smith-Bindman R, Chu PW, Miglioretti DL, Sickles EA, Blanks R, Ballard-Barbash R, Bobo JK, Lee NC, Wallis MG, Patnick J, Kerlekowske K (2003) Comparison of screening mammography in the United States and the United Kingdom. JAMA 290: 2129-2137.
24. Spratt JA, von Fournier D, Spratt JS, Weber EE (1993) Decelerating growth and human breast cancer. Cancer 71: 2013-2019.
25. Vaidya JS (2004) Women undergoing screening mammography experience a higher incidence of invasive breast cancer, without a corresponding reduction in symptomatic breast cancer. BMJ. Available at http://www.bmj.com/content/339/ bmj.b2587?tab=responses (accessed 20 March 2012).
26. Walter SD, Day NE (1984) Simplified models of screening for chronic disease: estimation procedures from mass screening programmes. Biometrics 40: 1-14.
27. Weedon Fekjær H, Lindquist BH, Allen OO, Vatten LJ, Tretli S (2008) Estimating sojourn time and screening sensitivity using questionnaire data on time since previous screening. J Med Screen 15: 83-90.
28. Welch HG (2006) Ramifications of screening for breast cancer: 1 in 4 cancers detected at mammography screening are pseudocancers. BMJ. Available at http://www.bmj.com/content/332/7543/689?tab=responses (accessed 20 March 2012).
29. Welch HG (2010) Overdiagnosis in cancer. JNCI 102: 605-613.
30. Zackrisson S, Andersson I, Janzon L, Manjer J, Garne JP (2006) Rate of overdiagnosis of breast cancer 15 years after end of Malmö mammographic screening trial: follow-up study. BMJ 332: 689-691.
31. Zahl P-H, Gøtzsche PC, Mæhlen J (2011) Spontaneous regression of screening-detected cancers in the Swedish breast screening program. Lancet Oncol 12: 1118-1124.
32. Zahl P-H, Mæhlen J (2012) [Overdiagnosis of breast cancer after 14 years with screening]. Tidsskr Nor Lægeforen 132: 414-417.
33. Zahl P-H, Mæhlen J, Welch HG (2008) The natural history of invasive breast cancers detected by screening mammography. Arch Intern Med 168: 2311-2316.
34. Zahl P-H, Strand BH, Mæhlen J (2004) Breast cancer incidence in Norway and Sweden during introduction of nation-wide screening: prospective cohort study. BMJ 328: 921-924.
35. Zelen M, Feinleib M (1969) On the theory of screening for chronic diseases. Biometrika 56: 601-613.