Interpreting overdiagnosis estimates in population-based mammography screening

Abstract

Estimates of overdiagnosis in mammography screening range from 1% to 54%. This review explains such variations using gradual implementation of mammography screening in the Netherlands as an example. Breast cancer incidence without screening was predicted with a micro-simulation model. Observed breast cancer incidence (including ductal carcinoma in situ and invasive breast cancer) was modeled and compared with predicted incidence without screening during various phases of screening program implementation. Overdiagnosis was calculated as the difference between the modeled number of breast cancers with and the predicted number of breast cancers without screening. Estimating overdiagnosis annually between 1990 and 2006 illustrated the importance of the time at which overdiagnosis is measured. Overdiagnosis was also calculated using several estimators identified from the literature. The estimated overdiagnosis rate peaked during the implementation phase of screening, at 11.4% of all predicted cancers in women aged 0-100 years in the absence of screening. At steady-state screening, in 2006, this estimate had decreased to 2.8%. When different estimators were used, the overdiagnosis rate in 2006 ranged from 3.6% (screening age or older) to 9.7% (screening age only). The authors concluded that the estimated overdiagnosis rate in 2006 could vary by a factor of 3.5 when different denominators were used. Calculations based on earlier screening program phases may overestimate overdiagnosis by a factor 4. Sufficient follow-up and agreement regarding the chosen estimator are needed to obtain reliable estimates.

Figure 1.

Stages at which overdiagnosis can occur: A) When preclinical ductal carcinoma in situ (DCIS), detected by screening, would have regressed if no screening had taken place; B) when preclinical DCIS, detected by screening, would not have progressed to invasive cancer during a woman's lifetime if no screening had taken place; C) when preclinical DCIS, detected by screening, would have progressed to invasive cancer but would not have become symptomatic during a woman's lifetime if no screening had taken place; and D) when preclinical invasive breast cancer, detected by screening, would not have become symptomatic during a woman's lifetime if no screening had taken place. Dot-filled boxes; stage at which a breast cancer is screen detected; grey-shaded boxes: stages of the natural history of the tumor averted by screen detection; crosses: death from causes other than breast cancer.

Figure 2.

Observed and modeled breast cancer incidence per 100,000 woman-years in the presence and absence of screening between 1990 and 2006 (values after years indicate percentage of the target population aged 49–69 years invited, fraction of prevalent screenings). A) 1990: 9.2%, 74%; B) 1992: 47.4%, 77%; C) 1994: 74.3%, 49%; D) 1996: 92.0%, 39%; E) 1998: 80.8%, 20%; F) 1999: 91.8%, 19%; G) 2000: 94.4%, 18%; H) 2002: 96.1%, 14%; I) 2004: 95.8%, 14%; J) 2006: 92.2%, 13%. Solid lines, modeled with screening; dashed lines, modeled without screening; triangles, observed.