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5. Effectiveness of Breast Cancer Screening 5. EFFECTIVENESS OF BREAST CANCER SCREENING This section considers measures of screening Nevertheless, the performance of a screening quality and major beneficial and harmful programme should be monitored to identify and outcomes. Beneficial outcomes include reduc- remedy shortcomings before enough time has tions in deaths from breast cancer and in elapsed to enable observation of mortality effects. advanced-stage disease, and the main example of a harmful outcome is overdiagnosis of breast (a) Screening standards cancer. The absolute reduction in breast cancer The randomized trials performed during mortality achieved by a particular screening the past 30 years have enabled the suggestion programme is the most crucial indicator of of several indicators of quality assurance for a programme’s effectiveness. This may vary screening services (Day et al., 1989; Tabár et according to the risk of breast cancer death in al., 1992; Feig, 2007; Perry et al., 2008; Wilson the target population, the rate of participation & Liston, 2011), including screening participa- in screening programmes, and the time scale tion rates, rates of recall for assessment, rates observed (Duffy et al., 2013). The technical quality of percutaneous and surgical biopsy, and breast of the screening, in both radiographic and radio- cancer detection rates. Detection rates are often logical terms, also has an impact on breast cancer classified by invasive/in situ status, tumour size, mortality. The observational analysis of breast lymph-node status, and histological grade. cancer mortality and of a screening programme’s Table 5.1 and Table 5.2 show selected quality performance may be assessed against several standards developed in England by the National process indicators. The major indicators of both Health Service (NHS) (Wilson & Liston, 2011; the screening process and the clinical outcome, Department of Health, 2013) and in the USA and the associated analytical methodologies, are by the Agency for Health Care Policy and described below. Research and endorsed by the American College of Radiology, respectively (Bassett et al., 1994; 5.1 Indicators for monitoring and D’Orsi et al., 2013). Similar sets of standards exist for screening in Australia, Canada, and Europe evaluating effectiveness (National Quality Management Committee of 5.1.1 Performance indicators BreastScreen Australia, 2008; Perry et al., 2008; CPAC, 2013) (see Section 3.2). The programmes As a general principle, the most important specify standards – related mainly to the indicator of the effectiveness of a screening screening process and not directly to technical programme is its effect on breast cancer mortality. 281 IARC HANDBOOKS OF CANCER PREVENTION – 15 Table 5.1 Minimum quality standards and targets considered in the National Health Service breast screening programme in England Criterion Standard Target Attendance at screening ≥ 70% 80% Invasive cancers detected, prevalent screen ≥ 3.6/1000 ≥ 5.1/1000 Invasive cancers detected, incident screen ≥ 4.1/1000 ≥ 5.7/1000 In situ cancers detected, prevalent screen ≥ 0.5/1000 None specified In situ cancers detected, incident screen ≥ 0.6/1000 None specified Standardized detection ratio ≥ 1.0 ≥ 1.4 Invasive cancers < 15 mm, prevalent screen ≥ 2.0/1000 ≥ 2.8/1000 Invasive cancers < 15 mm, incident screen ≥ 2.3/1000 ≥ 3.1/1000 Mean glandular radiation dose for standard breast ≤ 2.5 mGy None specified Number of repeat examinations (% of total examinations) < 3% < 2% Recall for assessment (% of prevalent screens) < 10% < 7% Recall for assessment (% of incident screens) < 7% < 5% Short-term recall (% of screened women) < 0.25% ≤ 0.12% Non-operative diagnosis (% of cancers) ≥ 90% ≥ 95% Non-operative diagnosis (% of DCIS) ≥ 85% ≥ 90% Benign biopsies (prevalent screens) < 1.5/1000 < 1.0/1000 Benign biopsies (incident screens) < 1.0/1000 < 0.75/1000 Interval cancers within 24 months (screened women) ≤ 1.2/1000 None specified Interval cancers within 25–36 months ≤ 1.4/1000 None specified Percentage rescreened within 36 months ≥ 90% 100% Percentage receiving screening result within 2 weeks ≥ 90% 100% Assessed within 3 weeks (% of total assessed) ≥ 90% 100% Percentage non-operative biopsies with result within 1 week ≥ 90% 100% Percentage referred to surgeon receiving surgical assessment within 1 week ≥ 90% 100% Percentage admitted for treatment within 2 months of referral ≥ 90% 100% DCIS, ductal carcinoma in situ. Adapted from Wilson & Liston (2011) and Department of Health (2013). aspects of image quality – that all units should specified for adverse effects of screening, such as attain, as well as achievable targets at which units radiation dose, and for rates of interval cancers, should aim. repeat examinations, and recalls for assessment. Table 5.1 pertains to a programme that In addition, maximum times to events in the targets women aged 50–70 years with a screening, diagnostic, and treatment processes maximum screening interval of 36 months in are specified; these are important for the patient’s high-incidence countries. In the example in experience and quality of life, although they do England, two-view mammography is used, and not necessarily reflect clinical or radiological the programme changed from film to digital quality. mammography during 2010–2014. Some of the criteria and standards are very Minimum standards are specified for specific to the programme. For example, the screening attendance and detection rates, in randomized trials of breast screening observe particular detection rates of small cancers, a higher rate of breast cancer detection at the which are expected to be high in an effective prevalent (first) screen than at incident (subse- screening programme. Maximum standards are quent) screens (see, for example, Tabár et al., 282 Breast cancer screening Table 5.2 Minimum quality standards for mammography in the USAa Criterion Standard Recall rate for assessment (% of screened women) < 10% Cancer detection rate, prevalent screen (per 1000 screened) 6–10 Cancer detection rate, incident screen (per 1000 screened) 2–4 Positive predictive value of recall for assessment 5–10% Positive predictive value of biopsy 25–40% Proportion of screen-detected cancers in situ or TNM stage 0–I > 50% Proportion of screen-detected node-positive cancers < 25% a Values are specified by the United States Agency for Health Care Policy and Research and endorsed by the American College of Radiology. TNM, tumour–node–metastasis staging system of malignant tumours (see Section 1, Table 1.9). Adapted from Bassett et al. (1994) and D’Orsi et al. (2013). 1992). However, the detection rate standards Indicators such as detection rates are typically are expected to be higher for incident screens part of the monitoring system of most screening because these values are based not on observa- programmes, but the actual target values will tions of a cohort recruited at the prevalent screen vary according to the screening regimen, the and followed up thereafter but on a programme target population, the underlying incidence in in which prevalent screens usually take place the programme’s location, and possibly aspects at about age 50 years and incident screens on of the health-care delivery systems and the medi- average at about age 60 years (when the under- colegal environment (Klabunde et al., 2001). lying risk of cancer is higher). Table 5.2 shows selected standards developed Another measure that is used in the United in the USA. These standards include acceptable Kingdom is the standardized detection ratio, ranges for positive predictive values (PPVs) of obtained by comparing the observed detection recall for assessment and for recommendation rates of invasive cancers by age with those of the for biopsy. They specify that the proportion of Swedish Two-County trial (Tabár et al., 1992), cases recalled for assessment that result in diag- on which the United Kingdom breast screening nosis of cancer should be 5–10%, and that the programme was modelled. At present, the proportion of biopsies that result in diagnosis standard is almost invariably exceeded (NHSBSP, of cancer should be 25–40%. These are powerful 2009), probably at least partly due to the fact that measures of the process since they reflect detection breast cancer incidence in the United Kingdom rates, recall rates, and biopsy rates. in the 21st century is higher than that in Sweden in the 1970s and 1980s. This example implies that (b) Screening sensitivity and interval cancers standards should be revised over time, although In a screening setting, the prevalence of it has also been observed that lower standards the disease in screened subjects, expressed as followed by remedial action have conferred a proportion, is usually very low; a very small substantial improvements in programme perfor- number of those screened at each screening mance (Blanks et al., 2002). Wallis et al. (2008) round are diagnosed with cancer, whereas thou- gave a demonstration of how careful surveillance sands of women are screened negative. Typically, of audit standards can lead to changes in prac- in European screening programmes, per 10 000 tice and improved performance at the local and women screened, about 9500 will have a normal national levels. initial result and about 500 will be recalled for further assessment, of whom about 70 will have 283 IARC HANDBOOKS OF CANCER PREVENTION – 15 breast cancer. After the screen, about 10–30 will potential to improve the programme’s ability to present with symptomatic interval cancer. detect
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