The British Columbia Mammography Screening Program: Evaluation of the First 15

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1 45 Linda J. Warren Burhenne1 T. Gregory Hislop2 H. Joachim Burhenn& Received April 22, : accepted after revision July 19, Presented at the annual meeting of the Society of Breast Imaging, Chicago, IL, November I Department of Radiology, University of British Columbia and vancouver General Hospital, vancouver, B.C., Canada 5Z 1 Mg. Address reprint requests to L. J. Warren Burhenne, 750 W. Broadway, #505, Vancouver, B.C., Canada V5Z 1E7. 2 Division of Epidemiology, British Columbia Cancer Agency, Vancouver, B.C., Canada V5Z 4E X/92/ American Roentgen Ray Society The British Columbia Mammography Screening Program: Evaluation of the First 15 Months We report our experiences in the first 15 months of a government-funded pilot project begun in 1988 to study the feasibility of rapid throughput, low-cost screening mammography in British Columbia. The primary goals of the project were (1) to determine the unit cost of screening mammography within the context of the program; (2) to design and put into operation a centralized system of data collection, analysis, and quality control to enable calculations of cancer detection rates, biopsy rates, biopsy yield ratios, staging, and other specific cancer characteristics; and (3) to study compliance in the community where the program was offered. A total of I 1,824 women had mammography at a unit cost of U.S.$ Computerized analysis revealed that (1) 1 1% of women had known primary risk factors; (2) findings on mammograms were interpreted as abnormal in 9% of screening examinations; (3) breast cancers were confirmed in 47 (22%) of 211 patients who had biopsies, and 87% of these were stage 0-I. The overall cancer detection rate was four per 1000, with five per 1000 for women who had not had mammography in the preceding 2 years and one per 1000 for women who had had mammography in the past 2 years. The results show that screening mammography can be conducted at low cost. Data collection and analysis and compliance were sufficiently convincing to initiate provincewide expansion. AJR 158:45-49, January 1992 The acknowledgment that mammography screening is the best single method to reduce mortality rates from breast cancer has had a potent influence on medical practice, and numerous national and international organizations have issued recommendations for screening mammography [1-3]. Cost-control concepts and strategies have been invoked by the American Cancer Society [4, 5], and cost control has been demonstrated by projects in Sweden, the Netherlands, and North America [6-1 3]. It has been continually emphasized that screening mammography can be provided at a cost significantly lower than the cost for radiologic evaluation of symptomatic patients. Residents of British Columbia are insured with the plan administered by the provincial government, which funds all required medical services. Definite potential exists for the public as a whole to benefit from the establishment of a successful low-cost screening program. The Screening Mammography Program of British Columbia pilot project was established with three primary goals: (1 ) to determine the unit cost of screening mammography; (2) to design and put into operation a centralized system of data collection, analysis, and quality control so that program results could be compared with those of other similar studies; and (3) to study compliance and acceptance of the project by women in the community where the service is provided. Subjects and Methods Advertising, using various communications media, public presentations, and mailings to family physicians, is directed to asymptomatic women 40 years old and over; women less

2 46 WARREN BURHENNE ET AL. AJR:158, January 1992 than 40 years old are accepted by special request if they have a strong family history of breast cancer. Women are invited to participate either with or without a formal physician s referral, and they are required to give the name of a family physician. If they do not have a family physician, they are requested to find one before the screening can be done, because it is the family physician who is expected to manage the patient if an abnormality is found at screening mammography. Registration and a brief interview for epidemiologic data are conducted by clerical staff. Women with breast symptoms are not screened but are directed to theirfamily physicians, who are expected to arrange for diagnostic mammography, which can be conducted at any one of numerous hospitals and clinics in the community. Therefore, only asymptomatic women are considered eligible for the program. Before taking the mammogram, the mammography technologists inspect the breasts for scars and skin lesions and record any abnormality, although they do not actively palpate the breasts. Standard mediolateral oblique and craniocaudal views are obtained with no film monitoring on a CGR 500T unit, with Kodak Mm-RE film, Mm-A medium screens, and dedicated processing. Movable grids are used routinely. The entire visit in the screening center averages less than 30mm. Screening examinations are batch reported by one of a team of five screening radiologists, the films having been mounted by technologists on a multiviewer. The members of the screening team were chosen from a group of nearly 30 applicants, the choice made by the steering committee after assessment of documented mammographic experience both in screening and diagnosis, as well as contribution to mammographic education in the community and to the scientific literature. A standardized test based on documented cases was devised as a means to assess the expertise of future screeners; individual abnormal interpretation rates and cancer detection rates are assessed on a monthly basis. Reporting is currently done by using a check-off form in which the results are designated as either normal or abnormal. A handwritten note describing the finding is added by the radiologist in abnormal cases. Previous films, if done at the screening center, are always provided for comparison. The screening radiologist decides whether or not a technical error requires the examination to be repeated; under these circumstances, women are asked to return for further films, and no interpretation is rendered until the examination is considered complete. The patient s physician and the patient receive a letter with results for all examinations. In cases with abnormal findings, the physician receives a written report generated from the check-off interpretation form that describes the abnormality and its location, together with brief but specific recommendations for diagnostic workup. Letters to both physicians and patients include a recommendation that physical examination of the breast be done. The Section of General Practice of the British Columbia Medical Association has undertaken to ensure that the patient is instructed in breast self-examination during the same visit to the physician s office. All procedures for registration, recording of mammography results, printing of reports and letters, handling of return screening visits, follow-up of patients with abnormal findings, and recording of outcome data are fully centralized. Specifically, at the head office, a team of three, headed by a program evaluator, is responsible to ensure that complete follow-up on all women with abnormal findings is documented. Documentation of diagnostic workup is requested by mail from the patients physicians. It has been possible to complete follow-up documentation on all patients with abnormal interpretations within 6 months of the screening visit. The British Columbia Cancer Registry records all cancers diagnosed in British Columbia. By means of computer linkage with the Cancer Registry we are able to identify subsequent breast cancers in patients who were screened but whose cancers were not detected by the screening mammogram. Therefore we can document all interval cancers diagnosed in the province. For our program, the recommended screening interval is 1 year; therefore, interval cancers are defined as those diagnosed within 1 year of the most recent screening mammography examination. All biopsy specimens generated by the screening program undergo a formal review by the senior pathologist of the British Columbia Cancer Agency. Results The unit cost per screening during the first 1 5 months of operation was Can$3755 (U.S.$32.66). The unit operating cost includes an interpretation fee of $5.00 per mammogram and an administrative fee of $1.00 per mammogram. This unit cost does not include an additional unit cost of $1.25 for rental of office space and $5.32 for equipment. These additional costs have been built into the current budget because they will be incurred in a noninstitutional setting and do not apply to the pilot center. Overall, the cost breakdown was salaries and benefits, 56%; professional fees, 1 0%; nonprofessional expenses, including supplies, data processing, and equipment maintenance, 34%. During the first 1 5 months of operation, women were screened. Forty percent of the women attending were less than 50 years old and 33% were premenopausal. Only 18% were nulliparous, 21 % reported late age at first parity (i.e., 30 years and over), and 1 1 % had a family history of breast cancer (Table 1 ). Seventy-five percent regularly prac- TABLE 1: Distribution of Demographic Characteristics in 11,824 Women Participating in Mammography Screening Program Characteristic No. (%) Age (yr) <40 76 (1) (40) (31) (22) (6) Menopausal status Premenopausal 3926 (33) Postmenopausal 6576 (56) Education Did not graduate 2413 (20) High school graduate 2691 (23) Postsecondary 6547 (55) Parity Nulliparous 2150 (18) Parous (80) Age at first delivery (yr) < (8) (58) (21) Family history No (88) Yes, unilateral and post- 737 (6) menopausal Yes, bilateral or premeno- 626 (5) pausal Note-Some participants did not answer all questions; therefore, numbers do not add up. Percentages, however, relate to total number of women (1 1, 824).

3 AJA:158, January 1992 BRITISH COLUMBIA MAMMOGRAPHY SCREENING PROGRAM 47 TABLE 2: Distribution of Prior Breast Examination in 11,824 Women Participating in Mammography Screening Program Examination No. (%) Breast self-examination No 2868 (24) Yes 8859 (75) Breast physical examination No 3825 (32) Yes 7883 (67) Mammography No 8716 (74) Yes 3029 (26) Breast biopsy No (86) Yes 1603 (14) Note-See footnote to Table 1. TABLE 3: Subsequent Diagnostic Tests Performed on 1031 Women with Abnormal Findings on Mammograms Diagnostic Investigation No. (%) Diagnostic mammography 816 (79) Sonography 242 (24) Fluid aspiration 74 (7) Tissue aspiration 1 1 (1) Wire localization and biopsy 149 (14) Biopsy (other) 62 (6) ticed breast self-examination, and 67% had had physical examination of the breast within the past year. Twenty-six percent had had mammography before, and 14% had had a breast biopsy with benign results before (Table 2); women with previous diagnoses of breast malignancy were not accepted for the program. All patients with abnormal mammographic interpretations were followed up through diagnosis. The overall abnormal interpretation rate was 9%, with a range from 8% to 9% by individual screening radiologists. The call-back rate because of technically unsatisfactory films was 0.5%. The kinds of subsequent diagnostic tests performed on women with abnormal findings on mammograms are summarized in Table 3. Under the current protocol, only patients regarded as having a negligible risk of malignancy are assigned to early follow-up mammography at 4-6 months, and therefore an early follow-up category has not been included in the list of diagnostic investigations. This policy is currently under review, pending analysis of the basic assumption. Forty-seven cancers were diagnosed on the basis of 211 biopsies, for an overall cancer-to-biopsy ratio of 22%. As there is neither a review clinic nor a community standard for the number and order of diagnostic tests, this biopsy yield is therefore a manifestation of the various diagnostic practices within this medical community. Certain patterns of delay from the screening center visit to referral for diagnostic investigation emerged. A mean delay of 25 days occurred from the time of the screening mammograms to when diagnostic mammography was performed, and a mean delay of 29 days occurred between diagnostic mammography and biopsy. Delays were generally shorter in women ultimately diagnosed with breast cancer. The cancer detection rate for women with prevalent cancers (no mammography in the preceding 2 years) was five per 1 000; that for incident cancers (mammography during the preceding 2 years) one per The overall cancer detection rate was four per The breast cancer detection rate was age dependent: for women less than 50 years old, 1.7 per 1 000; for women 70 years old or more, 9.2 per Detection rates for breast cancer relative to mammographic proportion of dense tissue were 4.8/1 000 for women with less than 50% dense tissue and 2.6/1 000 for women with more than 50% dense tissue (Table 4). Thirteen (28%) of the 47 cancers were ductal carcinoma in situ; 33 (70%) were invasive ductal carcinoma, the remaining one (2%) was lobular invasive carcinoma. The tumor sizes are shown in Table 5. Twenty-eight (60%) of 47 cancers measured 1 0 mm or less, and nine of these were in situ. Axillary nodes were not dissected in five women with in situ lesions; one additional woman with invasive disease declined recommended dissection. For the remaining 41 cases, five showed involvement of axillary lymph nodes; in only one of these was the involvement more significant than that of micrometastasis. Cancers were staged according to the current criteria of the American Joint Committee on Cancer. TABLE 4: Cancer Detection Rates by Subgroups of Participants Age N f N Cancer Subgroup Women wh Screened Cancer (yr) < Family history of breast cancer (first degree relative) No Yes, lower riska Yes, higher riskb Prior mammography in preceding 2 years No Yes Mammographic proportion of dense tissue (D) <50% >50% Total a Lower risk: unilateral disease, age >50 years. b Higher risk: bilateral disease, age <50 years. TABLE 5: Size of Breast Cancers LesknSize Intraductal Invasive Total > Note-Sizes of 24 of the 47 tumors were available from the pathology report; the remainder were measured on the mammograms.

4 48 WARREN BURHENNE ET AL. AJA:158, January 1992 Twenty-one percent were stage 0, 64% stage I, 1 3% stage II, and 2% stage Ill. Overall, 85% were stage 0 to I. If the criteria of Martin and Gallager [1 4] are applied, 36% of the cancers detected were in the minimal category; 67% would be minimal if the expanded criteria (including invasive carcinomas 1 0 mm or less) were used [15]. The false-negative rate was measured through linkage with the cancer registry. Breast cancer was diagnosed in seven of our patients within 1 year after a normal mammographic result at the screening center, an interval cancer rate of 5.9 per 1 0,000 patients. On review, only one of the patients with interval cancers had radiologic signs suggestive of neoplasm. The rest of the interval cancers were in dense breasts and were radiologically occult. A detailed analysis of all interval cancers will be the subject of a subsequent report. The true sensitivity of the screening mammograms therefore was 87% (47/54), specificity was 92% (1 0786/ ), and positive predictive value of an abnormal interpretation was 5% (47/ 1 031), ranging among radiologists from 3% to 6%. Discussion The acknowledgment of the proved benefit of screening mammography from the earliest results of the Health Insurance Plan of New York study [1 6, 1 7] and the subsequent confirmation based on the trials from Sweden and the Netherlands [1 8, 19] resulted in American Cancer Society Guidelines for Cancer Related Check-ups with specific recommendations for breast cancer in 1980 [20]. Subsequently, studies such as those performed by the American Cancer Society in [4] and in 1989 [5] confirmed that the guidelines were not being adhered to and that mammography was being generally underused in the United States. In British Columbia, the situation is not analogous to either the patient-funded system prevalent in the United States or the public-funded systems of Sweden and the Netherlands [9-1 3, 21, 22]. Similarly, it is not analogous to the two-tiered funding system of Great Britain. In the Canadian system, in which essentially all citizens are insured publicly, and mammography of asymptomatic women is available in approximately 30 facilities in the Vancouver area, whether screening mammography is offered free at the Screening Mammography Pilot Project is not of concern to women who are informed enough to present for screening. It is for this reason that barriers to screening mammography cited by Gold et al. [23], involving the attitudes of patients and physicians, become more relevant. Despite the fact that average attendance (825 per month) was less than the expected 1 000, the unit cost for screening of Can$37.55 (U.S.$32.66), excluding equipment, compares quite closely with the results from both fixed centers (Bird and McLelland [1 1 ], U.S.$27.00) and mobile facilities (Sickles et al. [9], US$25.00 and Rubin et al. [13], U.S.$55.00) in the United States, and with the Swedish program s unit cost of US.$24.00 [3]. The unit cost, calculated after the first 1 5 months, included, inevitably, costs for development of the central computer system and programs for analysis. Although these development costs cannot be regarded as purely related to the screening examination, they cannot be separated from the screening center s costs at a time when only one screening center was in operation. We anticipate that as the program expands, even without an increased volume of patients, the cost per screening will decrease as development costs dedine. This phenomenon is addressed by Van der Maas et al. [24] of the Netherlands, who in preparing estimates for the unit cost at different stages of their program, predict a drop from U.S.$86.00 to U.S.$35.50 throughout the planned 27- year course of the program. The daily screening volume dropped after 9 months of operation by an average of five screenings per day. Unit cost increased from Can$33.81 for the first 9 months to Can$3755 for the total 15-month period, reflecting primarily reduction in the daily volume of patients. McLelland and Sickles [25] emphasize the need for education on the benefits of early detection and acceptance of screening by both patients and physicians to ensure compliance. Having established an acceptable unit cost at current average daily volume, we expect that our future challenges will include maintenance of the volumes at the current centers and ensuring adequate volume at the newer developing centers. Success in these areas will clearly depend on the effectiveness of educational techniques. The central computerization system has been developed in an ongoing fashion based on three consecutive projects: the first comprised the elements necessary for registration and recording and printing of interpretation; the second provided the capacity to handle annual return visits, to follow-up abnormalities and analyze outcome data; and the third included elements for ongoing management reporting, quality control, evaluation, and monitoring. Although all projects have been completed to the current requirements, we are still refining the auditing programs for maximum efficiency. The observation that few women had known risk factors is consistent with the work of Seidman et al. [26]. The high proportion of women who had performed self-examination and reported having received a physical examination of the breast in the past year suggests a relatively high degree of health consciousness in the screening population. The percentage of women who had had mammography before (26%) falls between the 33% figure cited by Rubin et al. [1 3] and the 4% figure of Sickles et al. [27]. The high percentage of women in this category, particularly those who had had mammography within the past 2 years, will reduce the total number of prevalent cancers available for detection, and therefore will affect the overall detection rate. Our measured false-negative rate of 59 per 1 0,000 is based on linkage with the British Columbia Registry. It is similar to the rates estimated by Sickles et al. [27] and Bird [1 2] of 4.4 and 5.5 per 1 0,000, respectively. However, because these rates were not based on population-based registries and because of the different means of calculation, these three rates cannot be accurately compared [28]. Further follow-up to determine any additional false-negatives diagnosed more than 1 2 months after the conclusion of the pilot study, as well as ongoing documentation of missed and interval carcinomas, is currently underway. It is of interest that a quality assurance standard of six missed cancers per

5 AJR:158, January 1992 BRITISH COLUMBIA MAMMOGRAPHY SCREENING PROGRAM ,000 within the 1 2 months subsequent to a prevalent screening is one of the criteria set for the British National Health Service Breast Screening Program [29]. The overall cancer detection rate of four per 1 000, with five per in the group not screened in the past two years and one per 1000 in the group screened during this period, is comparable with similar figures cited by Sickles et al. [27] and Bird [12]. Moskowitz [30] predicted a four per 1000 overall detection rate for the National Breast Screening Study Program. Factors such as self-selection, the significant proportion of women less than 50 years old who were examined, and the relatively high number of women who had had mammography before would influence these minor variations between studies. Also, results of various studies need to be compared and contrasted in the broader context of the primary motive for screening-reduction in mortality rate. The detection of 47 cancers, 85% of which were stage 0 to I, 88% of which occurred with normal axillary lymph nodes, and 36% of which were classified as minimal according to Martin and Gallager [14] could reduce the mortality rate due to breast cancer. Analyses of false-positive, false-negative, and positive predictive values provide the basis for the essential quality control of the performance of radiologist screeners. Finally, the confirmation that screening mammography can be conducted at high volume and low cost under circumstances in which there is no specific incentive such as low cost to attract women to attend a high-volume screening center rather than a diagnostic facility suggests that provision of facilities for wider scale screening would succeed here. On the other hand, measures such as mailed invitations to specific groups of women may eventually be necessary to ensure an acceptable average level of attendance. Maintaining compliance will clearly continue to be the ongoing challenge to perpetuate the economic advantages of such a program to the public. Full implementation of the program with its predicted reduction in mortality rate of at least 30% [31 ] here in British Columbia will depend on education, not only of radiologic professionals but also of primary physicians and the public as a whole. REFERENCES 1. American College of Radiology. Breast screening education needed: joint statement on mammography. ACR Bull 1989;45(7): Miller AB, Tsechkovski M. Imaging technologies on breast cancer control: summary of a report of a World Health Organization meeting. AJR 1987;198: Day NE, Baines CJ, Chamberlain J, Hakama M, Miller AB, Prorok P. UICC Project on Screening for Cancer: report of the Workshop on Screening for Breast Cancer. Int J Cancer 1986;38: American Cancer Society. Survey of physicians athtudes and practices in early cancer detection. 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Oak Brook, IL: Radiological Society of North America, 1986: Tabar L. Control of breast cancer through screening mammography. Radiology 1990:174: I The reader s attention is directed to the commentary on this article, which appears on pages 55-57