Affiliations of authors: J. G. Elmore, C. Y. Nakano, L. M. Desnick (Department of Medicine), T. D. Koepsell (Department of Health Services and Epidemiology), University of Washington, Seattle; C. J. DOrsi, Department of Radiology, Emory University, Atlanta, GA; D. F. Ransohoff, Department of Medicine, University of North Carolina at Chapel Hill.
Correspondence to: J. G. Elmore, MD, MPH, Department of Medicine, Division of General Internal Medicine, Harborview Medical Center, 325 Ninth Ave., Box 359780, Seattle, WA 98104-2499 (e-mail: jelmore{at}u.washington.edu).
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ABSTRACT |
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INTRODUCTION |
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Variability in screening mammography interpretations may have important clinical and economic implications. Although clinicians do not wish to miss breast cancers, it is important to minimize unnecessary follow-up diagnostic procedures, costs, and patient anxiety associated with false-positive screening mammograms.
In this article, we compare published data from community-based mammography screening programs in North America with similar screening programs in other countries to address two important questions: 1) To what extent is variability in mammographic interpretation in community-based screening mammography programs observed between programs in North America and other countries? and 2) Is variability in mammographic interpretation associated with different intermediate measures of breast cancer outcome (i.e., percentage of breast cancer cases with ductal carcinoma in situ [DCIS] and/or minimal disease)? Based on our findings, we discuss possible explanations for variability in mammography interpretations and of the implications that this variability might have on future research, health policy, and patient care.
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METHODS |
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A MEDLINE search identified 227 English and nonEnglish language candidate publications between January 1, 1985, and June 15, 2002. Search terms included 1) mammography, 2) mass screening, and 3) biopsy. In addition, the references cited within these publications were searched for any publications that may fit the study inclusion criteria. To be included in this study, a publication had to report results of screening mammography performed in or after 1985. Screening mammograms were defined as mammograms obtained on women with no known breast-related symptoms or abnormalities and no known breast cancer at the time of the screen. In addition, at least two of the three measures of physicians interpretation (i.e., percentage of mammograms judged to be abnormal, positive predictive value of an abnormal mammogram [PPVA], and PPVB) and at least one of the two intermediate breast cancer outcomes (i.e., percentage of breast cancer cases with DCIS or percentage with minimal disease) had to be available. For breast cancer screening programs that had published more than one article, we attempted to select the most recent data covering the largest geographic area and the largest number of women. Results from randomized clinical trials and casecontrol studies were excluded from this study because data from research settings may have less generalizability to current community-based practice.
A total of 32 published articles met the study inclusion criteria. Each of these final publications was reviewed independently by at least two authors (J. G. Elmore, L. Desnick, and C. Y. Nakano) to determine if it met the study inclusion criteria. When information was not clear from the publication, the authors of the article were contacted to obtain that information (see supplemental information available at http://jncicancerspectrum.oupjournals.org/jnci/content/vol95issue18/). When disagreements between the text of an article and the data presented in the tables were noted, we chose to use the data from the tables. Information on the characteristics of the population screened, features of the mammogram examination, and outcome of readings were abstracted from each publication that met the study inclusion criteria.
Characteristics of the Population Screened
Age of the women screened was abstracted from each article because mammography sensitivity, specificity, and positive predictive value have been found to increase in older women (9). Each article was also classified as including initial screens only, subsequent screens only, or mixed screens (i.e., both initial and subsequent). Results from first-time (e.g., initial) mammographic screening include prevalent cancers, so the percentage of mammograms judged to be abnormal and cancer rates may be expected to be higher than in subsequent screens of the same woman (9).
Features of the Mammogram Examination
The number of views taken of each breast was noted (mediolateral oblique and craniocaudal views versus a single-view mammogram). The use of two-view mammography improves sensitivity and specificity and reduces the percentage of mammograms judged to be abnormal (10,11). The year in which the mammograms were performed (not the year of publication) was also abstracted because possible improvements in the quality of mammograms over time and secular trends toward an increasing false-positive rate have been noted in the United States (12).
The mammographic interpretive process in each publication was categorized as involving a single radiologist versus separate readings by two radiologists, because double reading of mammograms has been associated with improved accuracy (13,14). If the interpretive process was not stated explicitly, we relied on the use of the term "radiologist" (i.e., singular) in the published literature to imply single-reader interpretation. Although single-reader interpretation is the standard-of-care in most North American screening programs, in other countries, interpretation is often performed by two radiologists (15). The actual method of double reading of mammograms was not stated in most of the publications we studied, but it presumably included two radiologists interpreting each film independently (e.g., blinded), with disagreements decided by consensus or by two radiologists reading each film together.
Outcome of Mammographic Readings
Most published studies during this time period (i.e., between January 1, 1985, and June 15, 2002) did not describe screening mammography program results using standardized methods (e.g., Breast Imaging Reporting and Data System [BI-RADS] classification) (16). Instead, most studies used descriptive prose to define the percentage of mammograms judged to be abnormal and for the measures of accuracy (e.g., PPVs). Because cancer mortality was not an available outcome in these studies, intermediate outcomes of several types were used, as defined below.
The percentage of mammograms judged to be abnormal was defined as the percentage of screening mammograms that the radiologist believed required further diagnostic evaluation, which is also sometimes referred to as the callback or recall rate. For the purposes of this study, our definition included short-interval follow-up diagnostic mammogram within 12 months, additional immediate mammographic views, follow-up with a clinician for physical examination correlation (i.e., follow-up on an abnormality), ultrasound, and fine-needle aspiration or core biopsy. This broad definition corresponds to the use of BI-RADS classifications 0, 3, 4, and 5 indicating the positivity of an initial screening mammogram (16). Although a short-interval follow-up is not considered to be a recall according to the American College of Radiology recommendations (16), we included it in our definition because of the variability of the published reportsthat is, some reports included short-interval follow-up in their definition of the percentage of mammograms judged to be abnormal, whereas other reports did not or were not clear in their definition.
PPVA was defined as the percentage of women with abnormal screening mammograms (i.e., those with a recall) that ultimately received a diagnosis of breast cancer. PPVA is roughly equivalent to the American College of Radiology PPV1 classification (16). However, as noted above, we also included short-interval follow-up (i.e., BI-RADS classification 3).
PPVB was defined as the percentage of women undergoing biopsy as a result of an abnormal screening mammogram who ultimately received a diagnosis of breast cancer. PPVB is roughly equivalent to the American College of Radiology PPV3 classification. However, it is important to note that data on biopsy outcomes in the published articles included fine-needle aspiration, open and core biopsies, and combinations thereof. Because many articles did not specify the type of biopsy performed, we could not stratify or interpret by biopsy type.
Few published studies from community-based settings reported breast cancer mortality results because of the difficulty in tracking patients and the requirements for long-term follow-up. For these reasons, intermediate endpoints were used to assess the clinical outcomes of a screening program. Although tumornodemetastasis (TNM) staging was not available for most articles, the percentage of women with minimal disease at the time of diagnosis and the percentage of women with DCIS at the time of diagnosis were commonly noted. Minimal disease was defined as invasive breast cancer that was less than or equal to 10 mm in diameter and/or DCIS at the time of the diagnosis (17).
Statistical Analysis
To model the proportion of mammograms judged to be abnormal in relation to other study characteristics, we used meta-regression analysis, a form of regression analysis that extends random effects meta-analysis (1820). Meta-regression analysis assumes that, after accounting for within-study variance in the outcome of interest, the remaining between-study variance can be divided into systematic and random components. The systematic component is modeled using regression analysis on study-level covariates. Restricted maximum likelihood was used to estimate the residual random component of the between-study variance. The within-study variance was specified as p(1 - p)/n, where p = the proportion of subjects experiencing the outcome of interest in a given study and n = the number of subjects on which p was based. All meta-regressions were conducted using the metareg procedure in Stata 7.0 (Stata Corp., College Station, TX). P values were obtained by dividing the appropriate regression coefficient by its estimated standard error and then treating the quotient as a standard normal deviate. All statistical tests were two-sided.
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RESULTS |
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The percentage of cancer cases with DCIS at the time of diagnosis ranged from 4.3% to 68.1% (Table 2). Four of eight of the North American screening programs, but only four of the 24 programs from other countries, reported more than 20% of cases with DCIS. The percentage of cases with minimal disease at the time of diagnosis ranged from 30.6% to 80.6% in North American programs and from 14.0% to 55.7% in programs from other countries (Table 2
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To evaluate the strength of the association between the percentage of mammograms judged to be abnormal and the six screening outcomes, the scatter plots shown in Fig. 3 were constructed. The plotting symbol area for each study is proportional to the number of screening mammograms in the audit. The percentage of mammograms judged to be abnormal had a strong negative association with PPVA and PPVB, both of which were highly statistically significant (P<.001). In contrast, the proportion of mammograms judged to be abnormal had a strong positive association with the proportion of DCIS cases among women diagnosed with breast cancer (P = .008) and the number of DCIS cases diagnosed per 1000 screens (P = .024). However, no consistent association was observed between the percentage of mammograms judged to be abnormal and either the proportion of breast cancer diagnoses reported as having minimal disease (P = .21) or the number of breast cancer cases diagnosed per 1000 screens (P = .48).
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DISCUSSION |
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The impact of wide variability on the percentage of mammograms judged to be abnormal involves trade-offs between benefits and risks of mammography screening. On one hand, a low percentage of mammograms judged to be abnormal (i.e., <2%) may reflect decreased sensitivity and missed breast cancers or delay in diagnosis, potentially resulting in more advanced disease. On the other hand, a high percentage of mammograms judged to be abnormal (i.e., >10%) might reflect an increased false-positive rate or over-reading of mammographic films. Indeed, the percentage of mammograms judged to be abnormal can be shown algebraically (see below) to be a weighted average of the true-positive rate (i.e., sensitivity) and the false-positive rate (1 - specificity)that is, the percentage of mammograms judged to be abnormal = sensitivity x prevalence + (1 - specificity) x (1 - prevalence). Because the vast majority of women screened do not have breast cancer, (1 - prevalance) will normally be much greater than the prevalence. Hence, the percentage of mammograms judged to be abnormal will depend more on the false-positive rate than on the true-positive rate.
False-positive mammograms can lead to unnecessary diagnostic evaluations and high medical costs, anxiety for women receiving follow-up evaluations and even, in rare cases, morbidity (e.g., infections from biopsies, scars) (12,53). False-positive results do not have a negative impact on subsequent breast cancer screening behavior (54,55). It is estimated that 50% of women will have at least one false-positive mammogram after 10 screening examinations (12). In the United States, this false-positive rate translates into a substantial annual financial burden (12). For example, an additional $750 000 000 might be spent on diagnostic evaluations each year in the United States if the percentage of mammograms judged to be abnormal were 10% instead of 5% [an estimated 30 million women are screened annually at an average cost of $500 per false-positive episode (56)]. Conversely, it is possible that diagnosing women with earlier stage breast cancer can obtain financial savings (57). It is important, therefore, to learn how clinical benefit, as well as financial cost and possible harm, is associated with variability in mammography interpretation.
In this descriptive study, marked heterogeneity between the screening studies was noted. This finding is to be expected in view of differences in characteristics of the population screened, features of the mammogram examination, and definitions used (e.g., what constitutes an abnormal mammogram). Although we attempted to deal with this heterogeneity in the selection of the studies and we applied statistical tests designed for this type of meta-analysis, interpretation of a possible difference in mammography interpretation between North American screening programs and those from other countries must be made with caution. In addition, only aggregate-level measures of demographic and mammography characteristics were available, rather than data for individual women. Hence, the circumstances of data collection (e.g., relying on what is available in the published literature) weaken any statistical conclusions.
Possible Explanations for the Variability Noted
The question that is implicitly raised by our results is, Why are North American radiologists calling for further evaluations of so many more women, most of whom turn out to have false-positive mammograms, than radiologists from other countries? Given the extent of variability in mammographic interpretation noted in the studies we examined and its potential clinical importance, it is worthwhile discussing the possible sources of this variability and the implications that these findings might have on future research and health policy. The variation in mammographic interpretation noted in the published articles that we studied is likely due to multiple factors as reviewed below and summarized in Table 3.
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Differences in the number of women undergoing their first or initial screening mammogram within each screening program could also explain some of the variability in the interpretation of mammograms. The percentage of mammograms judged to be abnormal generally decreases with subsequent screening examinations because comparison films establish stability of any abnormalities and because the number of incident cancers in a screened population should be lower than in a non-screened population (9). It is interesting that many of the screening programs that had the lowest percentage of mammograms judged to be abnormal and the highest positive predictive value were pilot projects in European countries where screening mammograms had previously been limited, so a high rate of abnormalities in those locations might be expected. In addition, if cancers were being routinely missed in these programs because of the low percentage of mammograms judged to be abnormal, one might also expect more late-stage cancers to become apparent; however, no association was observed between the percentage of mammograms judged to be abnormal and the proportion of cancers reported as having minimal disease.
It is possible that the populations screened differ in regard to the presence of breast cancer risk factors, ethnic groups, presence of known breast cancer symptoms at the time of the mammogram, and the referral status of the woman; however, data for these variables were not available.
Features of the mammography examination. The screening studies we examined covered approximately the same time periods, so mammographic equipment and other technical issues were probably similar. However, all of the North American screening programs used two mammographic views per breast, whereas one or two mammographic views were used for programs from other countries. In addition, double reading of films was more common in screening programs from other countries than it was in programs from North America. Unfortunately, the published articles did not generally describe the specific details regarding how double reading was performed (i.e., two independent blind interpretations versus consensus interpretation). The differences noted between North American programs and programs from other countries persisted after adjustment for calendar year, number of views per breast, and use of single versus double readings.
Features of physicians interpreting the mammogram. Previous research has suggested a positive correlation between a physicians experience and accuracy of mammography interpretations (8,5860), although definitions of experience vary and not all research has shown a statistically significant association (61,62). In addition, whether a physicians personal comfort with ambiguity influences clinical decision-making is an important but understudied area of research (63). It is possible that physicians who are uncomfortable with ambiguity interpret a higher percentage of mammograms as abnormal. Individual physicians have different thresholds for labeling mammograms as abnormal (59); decision-making aids may help in adjusting the thresholds of selected physicians (6467).
Features of the health care system. Malpractice concerns may also be contributing to the high percentage of mammograms judged to be abnormal in some screening programs. For example, physicians in North America might be reluctant to label a mammogram as normal, thus leading to higher percentages of mammograms being judged as abnormal. This higher percentage of mammograms judged to be abnormal would probably lead to more false-positive mammograms and perhaps more true-positive mammograms with better sensitivity. It is interesting that malpractice concerns have been shown to affect physicians ordering of tests and procedures (6875). Failure or delay in cancer diagnosis is the most frequent allegation in medical malpractice claims in the United States (76), with issues related to breast cancer, particularly delay in diagnosis, being the most common cause of malpractice claims for all specialties (77). Malpractice concerns are on physicians minds, and some physicians believe that these concerns influence their clinical practice in a variety of ways, including referring more patients to other physicians and increasing the use of tests and procedures (6870,73,7780). In academic and public screening programs, there is a possible buffer against malpractice concerns in that physicians are rarely responsible for their own malpractice insurance or defense in litigation.
Financial incentives inherent to the health care system can also affect physicians use of health care resources (8183). Physicians in nonprofit mammography programs might differ in their practice patterns compared with physicians who interpret both screening and diagnostic mammograms with an incentive plan for high volume. In addition, academic and public screening programs might be isolated from the confounding issue of benefiting financially from additional diagnostic procedures that may follow an abnormal screening mammogram.
Some screening programs use specialized radiologists and have stated goals to develop high-quality screening programs that minimize false-positive results (11,22,41). These specialized programs monitor outcomes through quality control and self-auditing procedures. Programs that combine clinical breast examination with screening mammography may have higher biopsy rates because of abnormalities noted on the clinical examination and not necessarily on the mammography examination. In contrast, smaller, community-based screening programs may not have access to specialized radiologists.
Finally, national policy regarding desired goals for the percentage of screening mammograms judged to be abnormal varies (84,85) (Table 4). It is possible that physicians interpreting mammograms may, to some degree, simply be responding to those goals. Screening programs may also be using different methods for defining the percentage of mammograms judged to be abnormal and for calculating cancer outcomes. For example, some screening programs categorize short-term follow-up as a positive mammogram, which will elevate the false-positive rate. In addition, some European countries used fine-needle biopsies earlier than they were routinely used in the United States. The screening programs from these European countries do not consider fine-needle aspiration a biopsy; however, they use the aspiration information to decide if an excisional biopsy is warranted, which could well elevate the reported PPVB for these programs.
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The mammography screening programs described in this article are heterogeneous both in the methods of auditing their practice and in factors that may affect the interpretation of results. Currently, it is not possible to determine which features may be most responsible for the variability. To address this problem, we recommend standardized reporting of mammography data in the literature, with results stratified for patient characteristics and features of the examination and data on both process and outcome. We also endorse the new international standards for reporting diagnostic tests evaluation (86,87), which will improve the quality of reporting methods and results. In addition, linkage of screening programs to tumor registries, as is currently being performed in the United States by the Breast Cancer Surveillance Consortium (88), is critical to obtaining outcome data that go beyond intermediary endpoints. Outcome data on breast cancerspecific mortality would be the best comparison but were not available in the published literature. Finally, a better understanding of the sources of variability in mammography may lead to more effective screening programs that have a lower percentage of mammograms judged as abnormal without substantially lowering the cancer detection rate.
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NOTES |
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We appreciate suggestions on early drafts of this work by Drs. Suzanne Fletcher and Patricia A. Carney.
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Manuscript received January 7, 2003; revised July 14, 2003; accepted July 17, 2003.
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