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Mammography Versus Clinical Examination of the Breasts

Mammography Versus Clinical Examination of the Breasts Abstract Using published data from screening trials, this article compares two-modality (mammography and clinical examination) and single-modality (clinical examination alone) screening by evaluating cancer detection rates, program sensitivities, mode of cancer detection in two-modality screening, nodal status at time of detection, survival 10 years postdiagnosis, and breast cancer mortality 10 years after entry. Consistently, two-modality screening achieved higher cancer detection rates and program sensitivity estimates than either modality alone; mammography alone achieved higher rates than clinical examination alone; interval cancer detection rates between screening examinations were higher following clinical examination alone than mammography alone; single-modality screening with mammography failed to detect breast cancers identified by clinical examination alone; the sensitivity of mammography was lower in younger than older women, while the reverse was true for clinical examination; and mammography identified a higher proportion of node-negative breast cancer than clinical examination. We conclude that combining clinical breast examination with mammography is desirable for women age 40-49 because mammography is less sensitive in younger than older women. Careful training and monitoring are, however, as essential with clinical examiners as with mammographers. In countries where breast cancer is not a major priority and where funding for and expertise in screening mammography are scarce, clinical examination of the breasts as a single screening modality unquestionably deserves consideration. However, in North America, where breast cancer is a priority and mammography is relatively accessible, the real issue is not “screening mammography versus clinical examination,” but rather “screening mammography with clinical examination versus screening mammography without clinical examination.” Unfortunately, this issue is rarely addressed, probably due to two major factors: pervasive confidence in technology as a solution for most problems facing society; and the population's generally inflated view of the risks of getting breast cancer, of dying from breast cancer and, in particular, of benefiting from mammographic screening (1,2). Furthermore, when clinical breast examination is considered for inclusion in a mammography screening program, it is often dismissed for economic reasons. In general, mammography gets much attention and clinical breast examination is usually given short shrift, just as chest x-rays and electrocardiograms have diminished reliance on percussion and auscultation of the chest. Several years ago, at a meeting on breast cancer, a speaker commented that “in an era when modern mammography is available, the use of clinical breast examination in screening is unethical and irrational.” He raised an important issue. What is the role of clinical breast examination in screening for breast cancer? Is it dispensable? Answering these questions is difficult because there are few opportunities allowing valid comparisons of two-modality screening (mammography and clinical breast examination) with single-modality screening (clinical breast examination alone). The question may be particularly important for women age 40 to 49, for whom there is widespread controversy about the efficacy of mammography screening. Data Sources Of eight randomized controlled trials (RCTs) of breast cancer screening reported to date (3), the four Swedish RCTs used only mammography, leaving four that incorporated clinical breast examination in their protocol, namely the New York Health Insurance Plan (HIP) Study (4), the Edinburgh RCT (5), and the Canadian National Breast Screening Studies (CNBSS) I (6) and II (7) (Table 11). The manner in which these RCTs differed from each other must be understood. Respective ages at entry were 40-64 years, 45-64 years, 40-49 years, and 50-59 years. The intervention group in the HIP study and both CNBSS trials received annual two-view mammography and clinical breast examination. In the Edinburgh trial, the intervention group received two-view mammography with clinical breast examination at the first screen visit, one-view mammography with clinical breast examination at the third, fifth, and seventh screens, and clinical breast examination alone at the second, fourth, and sixth screens. Control groups in the HIP and Edinburgh trials received no screening at all. In CNBSS-I, the control group received a single clinical breast examination and thereafter depended on “usual care” in the community. They were followed annually by mailed questionnaire. In CNBSS-II, the control group received annual clinical breast examinations. In addition to results from screening trials, clinical breast examination has been evaluated in case series (8) and in screening projects (9,10), all disadvantaged by the lack of an appropriate comparison group. In contrast to the case series, two screening projects—the Breast Cancer Detection Demonstration Project (BCDDP) (9) in the United States and the DOM Project in Utrecht (10), both of which used two-modality screening—do provide useful data on clinical breast examination for comparison purposes with the RCTs. The quality of the breast examination is also an important issue. Clearly, high performance standards are as important for clinical examination as for mammography. The CNBSS has established what competent clinical breast examination alone can achieve in terms of cancer detection (11). Recent research on the efficacy of breast self-examination (BSE) also reinforces the importance of high standards: benefit from BSE seems to be restricted to competent practitioners (12,13). We are not aware of any published document describing training, monitoring, or routine evaluation of clinical examiners in the HIP study, the BCDDP, or the Edinburgh trial. In the Utrecht Project, the clinical examination was performed by the radiological technologist at the time of mammography, and she used a cupped hand to palpate four quadrants of each breast (personal communication). This is in marked contrast to the method applied in the CNBSS, where the examiners were trained to visually examine the breasts, to palpate the whole breast (not just the cone), to use a systematic search pattern, and to apply the pads of their fingers. Women were examined both sitting up and lying down (11). Overall, the standards achieved by CNBSS clinical breast examination were high. Approaches to Analysis The constraints on evaluation of clinical breast examination arising from the various study designs are apparent in Table 11. Even so, the four RCTs and the two screening projects that combined clinical breast examination with mammography allow several approaches to evaluating the role of the former: cancer detection rates, program sensitivities, mode of cancer detection, nodal status at time of cancer detection, survival 10 years postdiagnosis, and breast cancer mortality 10 years after entry. a) Cancer detection: Only the CNBSS allows detection rates to be compared for combined versus single-modality screening, since in the other two RCTs the comparison was screening versus no screening, and in the screening projects there were no control groups. In CNBSS-I, for women 40-49 years on entry, two-modality screening can be compared with clinical examination alone, but only for cancers detected at the first screening visit and up to 12 months thereafter. (Because intervention women received their second screening examination 12 months after the first, subsequent comparisons on the role of clinical breast examination are not possible; one can only compare program outcomes with respect to breast cancer incidence and breast cancer mortality.) In contrast, in CNBSS-II, for women 50-59 years on entry, two-modality screening can be compared with clinical examination alone for four or five successive annual screening examinations. Not only can breast cancer be detected as a direct consequence of a screening examination, it can also be detected in the interval between screening visits. Such “interval cancers” may only become detectable after the screening examination, or they may be missed by the screening process (in both cases, the screens are said to be “false negative”). Any evaluation of clinical breast examination must consider interval cancer rates. b) Program sensitivities (detection method): Only the CNBSS studies yield sensitivity estimates for a screening protocol that includes clinical examination alone. c) Mode of cancer detection: For women receiving two-modality screening, the proportions of breast cancer detected by mammography alone, by clinical examination alone, and by both simultaneously can be documented. This is possible within the intervention arm in the four RCTs and in the two screening projects. d) Nodal status at time of detection: This offers yet another way to evaluate clinical examination. With the data available, comparisons of nodal status are possible according to both mode of detection within the intervention arms in all four RCTs and intervention versus control status in the two CNBSS trials. The latter is of greater relevance in evaluating clinical breast examination. e) Survival postdiagnosis: For this approach, data from the three North American studies—CNBSS, HIP, BCDDP—relate survival to mode of detection for two-modality screening. Additionally, in the CNBSS, survival associated with single-modality screening can be reported. f) Mortality from breast cancer 10 years after entry: CNBSS-I breast cancer mortality in cases with year-one screen and interval detections will be described because it offers the only opportunity to compare mortality following a single episode of two-modality screening to mortality following a single episode of single-modality nonmammographic screening in women age 40-49. What Can Screening With Clinical Breast Examination Achieve? a) Cancer detection: Unfortunately, there are only three trials in which clinical breast examination was conducted in the absence of mammography: the Edinburgh trial (5) and CNBSS I and II (6,7). It is clear from Table 22 that two-modality screening will detect more breast cancer than clinical examination alone. Edinburgh detection rates for clinical examination at screening rounds 2, 4, and 6 were lower than the rates observed in the CNBSS for women age 50-59 (7). However, the Edinburgh women received mammography in rounds 1, 3, 5, and 7, and this may have depleted the breast cancers available for diagnosis by clinical examination in the following years. The rates might also be lower because the quality of the clinical examination did not match that in the CNBSS. A straightforward comparison of the Edinburgh and Canadian trials is clearly impossible. The CNBSS-I detection rate for women age 40-49 screened with clinical examination alone at the first screening round was 2.46/1,000 (6), a rate exceeding the rates reported for the Swedish two-county and Stockholm mammography-alone trials, which were 2.09/1,000 and 2.06/1,000, respectively, in women age 40-49 at entry (3). Interval cancer rates can be expected to be higher following screening with clinical breast examination alone compared to screening with mammography. At the first screen, for those age 40-49 at entry, CNBSS interval cancer rates were higher in women allocated to receive clinical breast examination only (1.11/1,000 women) than in those receiving two-modality screening (0.75/1,000 women). Given that CNBSS mammography achieves detection rates and sensitivity estimates that match other trials (3), it cannot be suggested that the comparison of CNBSS interval rates is unduly favorable to clinical examination. For women age 40-49, this raises the question, How important is the difference between interval rates in the two groups being compared? b) Program sensitivity (detection method): Sensitivity estimates are higher for two-modality screening than for single-modality with mammography. For women age 40-49 on entry, the sensitivity of two-modality screening with two-view mammography was much higher in the CNBSS (81%) compared to single-modality with single-view mammography in the two-county study (62%) and in the first screen of the Stockholm study (53%) (3). Only the CNBSS trials can compare the sensitivity of mammographic screening with screening by clinical breast examination alone (11). Comparing CNBSS sensitivity rates for two-modality screening to single modality with clinical breast examination in the two age groups, 40-49 at entry and 50-59 at entry, four observations can be made. First, two-modality screening achieved a higher sensitivity in older (88%) than younger (81%) women. Secondly, sensitivity estimates for clinical examination alone were slightly higher in younger women (68% vs. 63%). Thirdly, two-modality screening achieved a higher sensitivity in both older and younger women than single-modality screening with clinical breast examination. Fourth, in the CNBSS, the observed sensitivity for clinical examination alone in women age 40-49 is of the same order of magnitude (68%) as that observed in the two-county and Stockholm mammography-alone trials (62% and 53%, respectively) (3). However, the fact remains that mammography achieves higher detection rates than clinical examination alone (Table 33). It may be advisable to use 1) two-modality screening for women age 40-49, based on lower mammography and higher clinical examination sensitivity estimates for this age group compared to older women and 2) single-modality, two-view mammographic screening for women 50 years and over, based on higher mammography sensitivity estimates and lower estimates for clinical examination for older women relative to younger women. c) Mode of cancer detection: Table 33 displays the mode of cancer detection (for screen-detected tumors) in the intervention arms of the four RCTs and the two screening projects. The proportions detected by clinical breast examination alone vary from 3.3% in Edinburgh (5) to 44.7% in the HIP study (15). If one looks at the proportion of all clinically positive screening examinations, it varies from 44% for Utrecht to 74% for Edinburgh. The usefulness of clinical breast examination is demonstrated by the fact that there is no trial in which mammography identified all breast cancers. Although Edinburgh comes close at 96%, its provision of mammography every second year precludes results that can truly evaluate the role of clinical breast examination. The data in Table 33 reinforce the advisability of adding clinical breast examination to mammography screening in younger women. In the CNBSS, for women age 40-49 allocated to mammography, clinical examination alone was the mode of cancer detection in 23.5%, compared to only 12% for women age 50-59 allocated to mammography. d) Nodal status: Mammographically detected cancers are more likely to be node negative than those detected by clinical examination. Table 44 reveals not only that single-modality screening in CNBSS-I detected fewer cancers (55) at the first screening round than two-modality (86), but also that the latter is associated with a higher proportion of node-negative invasive tumors and a marginally higher proportion of node-positive tumors. Since equal numbers of women were assigned to the intervention and control arms, 25,214 and 25,216, respectively, it is appropriate to show frequencies rather than rates. e) Survival postdiagnosis: Table 55 compares survival at 10 years postdiagnosis according to mode of detection for women with screen-detected breast cancer. Lead-time bias is not an issue here because what is being described are the survival rates associated with the three modes of detection possible in two-modality screening. The comparisons across these North American screening studies are impeded by unmatched age groupings for the cohorts, with younger women having a lower risk of breast cancer than older. CNBSS-I has the youngest cohort (age 40-49) (6) compared with the HIP Study (age 40-64) (14) and the BCDDP (age 34-74) (9). The highest survival rates are observed in the CNBSS for every mode of detection in women who received combined mammography and clinical examination. Because the CNBSS is the most recently conducted study of the three displayed, one contributing element may be better mammographic technology in the CNBSS compared to the two older trials. CNBSS 10-year survival postdiagnosis for women assigned to receive a single clinical examination matched that observed for women in the mammography arm who were detected by clinical examination only. Although the survival rates associated with detection by mammography alone in all three studies exceed those for the other two modes of detection, this is insufficient to prove that mortality from breast cancer has been reduced. The major conclusion of the Boston case series (8), implausibly endorsed in the journal Science (15), was that five-year survival postdiagnosis was excellent at 95% for women whose breast cancers were detected by mammography alone, while that for women whose breast cancer was physically palpable was much lower at 74%. The usefulness of such case series, however, is limited by the lack of an appropriate comparison group, lead-time bias, and selection bias. Indeed, in CNBSS-1, seven-year survival for breast cancer patients age 40-49 detected by mammography alone was 95%, while that for women who did not receive mammography was 91% (6). f) Deaths 10 years after entry: Much concern has been expressed about the asymmetric distribution of advanced breast cancer in CNBSS-I at the first screening round in women age 40-49 on entry (16,17), namely an excess of advanced breast cancer detected in the two-modality arm of the trial compared to the control arm. Table 66 displays the distribution of deaths that have occurred approximately 10 years after entry, in CNBSS-I women who had breast cancer detected either at the first screening round or in the first 12 months thereafter. For two-modality and single-modality groups, the distribution of breast cancer deaths in cases detected in the first year is now 21 versus 19, respectively, compared to 16 versus 10 at the seven-year follow-up (6). Including deaths in women with breast cancer due to other causes [all causes of death in breast cancer patients are verified by external panel review (18)], the totals are 22 and 21 for the two groups, respectively. This near equalization in distribution should lessen the persuasiveness of criticism directed at the CNBSS (16,17), especially in light of similar patterns of mortality observed in other trials (18). The CNBSS mortality results are compatible with conclusions reached from meta-analyses, namely that benefit from screening women age 40-49 is slow to appear. The recently published external review of CNBSS randomization (19) by forensic experts found no evidence of subversion in CNBSS randomization procedures. An accompanying editorial (20) includes factual inaccuracies that have recently been corrected (21). This is not the first time that factual inaccuracies have been published (18). Conclusions Proponents of mammography screening in women age 40-49 have rightly said it is inappropriate to recommend clinical breast examination for screening in the absence of evidence. Certainly evidence from an RCT in North America comparing screening with clinical breast examination to no screening will never be available. Therefore, evidence on clinical breast examination from existing trials and projects must be examined. In fact, only the CNBSS allows comparative evaluation of clinical breast examination, and the comparison is with two-modality screening, not “no screening.” Because proponents of mammography have repeatedly called the CNBSS mammography “flawed” (16,17), the question arises, Are the achievements of clinical breast examination in the CNBSS enhanced because of “flawed mammography”? As has been reported before (18), there is much evidence to answer “no.” The CNBSS has achieved results equal to or better than other RCTs with respect to successful randomization (which cannot be similarly documented for any other trial), cancer detection rates, prevalence/incidence ratio, and survival. In short, there is no persuasive evidence that “flawed” mammography enhanced the achievements of clinical breast examination observed in the CNBSS. Unquestionably, by any of the parameters examined, screening with mammography, alone or in combination with clinical exam, performs better than clinical breast examination alone. The differences described may be smaller and possibly less important than many would predict, with one major exception: cancer detection rates. These are always considerably higher when mammography is used. Nevertheless, this may not be an unqualified benefit given the likelihood of overdiagnosis (22,23). Because two-modality screening out-performs mammography alone, there is a role for clinical breast examination in breast screening if women are to gain the most benefit from screening. It has long been known that biopsy of a palpable mass should not be deferred because of negative mammograms (24). With mammography alone, lumps will be overlooked, especially in younger women. As with mammography, breast examination technique must be excellent in order to be useful. And excellence can be achieved. It has been demonstrated that medical school curricula could be revised to enhance clinical breast examination competence among medical students (25) and that educational programs can effectively improve examination competence among health professionals (26). The need to achieve excellence should not be a deterrent to clinical breast examination any more than it has been to mammography. If clinical breast examination is to be employed in screening, examiners will need to be carefully trained and monitored. If the costs of a screening program must be limited, one could recommend that clinical breast examination should, at the very least, be part of the screening protocol for women under age 50 because, at that age, the sensitivity of mammography is lower than in later years. Table 1. Available data sources for evaluating clinical breast examination* Source (start date)   Design   Age at entry (year)   Study intervention   Frequency   Control intervention   HIP (1963) (4)  RCT  40-64  MA + CBE  q l y  No screening  Edinburgh (1979) (5)  RCT  45-64  MA + CBE  q 2 y  No screening        (Rounds 1, 3, 5, 7)        CBE  q 2 y  No screening        (Rounds 2, 4, 6)  CNBSS-I (1980) (6)  RCT  40-49  MA + CBE  q 1 y  Single CBE  CNBSS-II (1980) (7)  RCT  50-59  MA + CBE  q l y  Annual CBE  BCDDP (1972) (9)  Project  37-74  MA + CBE  q 1 y  NA  Utrecht (1975) (10)  Project  50-64  MA + CBE  Variable  NA  Source (start date)   Design   Age at entry (year)   Study intervention   Frequency   Control intervention   HIP (1963) (4)  RCT  40-64  MA + CBE  q l y  No screening  Edinburgh (1979) (5)  RCT  45-64  MA + CBE  q 2 y  No screening        (Rounds 1, 3, 5, 7)        CBE  q 2 y  No screening        (Rounds 2, 4, 6)  CNBSS-I (1980) (6)  RCT  40-49  MA + CBE  q 1 y  Single CBE  CNBSS-II (1980) (7)  RCT  50-59  MA + CBE  q l y  Annual CBE  BCDDP (1972) (9)  Project  37-74  MA + CBE  q 1 y  NA  Utrecht (1975) (10)  Project  50-64  MA + CBE  Variable  NA  * MA = mammography; CBE = clinical breast examination; q 1 y = annually; q 2 y = every two years. View Large Table 2. Screen detection rates/1000: two- versus single-modality screening*   CNBSS   Edinburgh (5)   Trial age intervention rounds   40-49 (6)   50-59 (7)   45-64   MA + CBE   CBE   MA + CBE   CBE   MA + CBE   CBE   1  3.89  2.46  7.20  3.45  6.15  —  2  1.74  —  3.74  1.95  —  1.75  3  1.99  —  2.48  1.28  3.15  —  4  2.38  —  3.14  0.89  —  0.85  5  1.84  —  2.84  1.64  3.33  —  6  —  —  —  —  —  1.03  7  —  —  —  —  3.08  —    CNBSS   Edinburgh (5)   Trial age intervention rounds   40-49 (6)   50-59 (7)   45-64   MA + CBE   CBE   MA + CBE   CBE   MA + CBE   CBE   1  3.89  2.46  7.20  3.45  6.15  —  2  1.74  —  3.74  1.95  —  1.75  3  1.99  —  2.48  1.28  3.15  —  4  2.38  —  3.14  0.89  —  0.85  5  1.84  —  2.84  1.64  3.33  —  6  —  —  —  —  —  1.03  7  —  —  —  —  3.08  —  * MA = mammography; CBE = clinical breast examination. View Large Table 3. Mode of cancer detection with two-modality screening* Study   Age (year)   n   Percent detected at screening   MA only   CBE only   MA + CBE   HIP (1988) (14)  40-64  132  33.3  44.7  22.0  BCDDP (1987)† (9)  37-74  3548  35.5  7.9  53.3  Edinburgh (1990)‡ (5)  45-64  88  22.7  3.4  73.9  CNBSS† (6)  40-49  255  40.4  23.5  36.1  CNBS† (7)  50-59  325  53.2  12.0  34.8  Utrecht (1984)‡ (10)  50-69  196  55.6  9.7  34.6  Study   Age (year)   n   Percent detected at screening   MA only   CBE only   MA + CBE   HIP (1988) (14)  40-64  132  33.3  44.7  22.0  BCDDP (1987)† (9)  37-74  3548  35.5  7.9  53.3  Edinburgh (1990)‡ (5)  45-64  88  22.7  3.4  73.9  CNBSS† (6)  40-49  255  40.4  23.5  36.1  CNBS† (7)  50-59  325  53.2  12.0  34.8  Utrecht (1984)‡ (10)  50-69  196  55.6  9.7  34.6  * MA = mammography; CBE = clinical breast examination. † All cancers. ‡ Invasive cancers. View Large Table 4. Screen-1 nodal status of invasive cancers in patients age 40-49 from CNBSS* Allocation nodal status   Annual MA + CBE   Single CBE   n   (%)   n   (%)   Node-negative  52  (60)  30  (54)  Node-positive  33  (38)  20  (36)  Status unknown  1  (2)  5  (10)    Total  86  (100)  55  (100)  Allocation nodal status   Annual MA + CBE   Single CBE   n   (%)   n   (%)   Node-negative  52  (60)  30  (54)  Node-positive  33  (38)  20  (36)  Status unknown  1  (2)  5  (10)    Total  86  (100)  55  (100)  * MA = mammography; CBE = clinical breast examination. View Large Table 5. Survival at 10 years by mode of detection—screen cancers only (%)*   Study (age, year)   Mode of detection   HIP (40-64) (4)   BCDDP (34-74) (9)   CNBSS (40-49) (6)   MA + CBE   MA + CBE   MA + CBE   Single CBE   MA only  77  85  93  NA  CBE only  59  76  84  86  MA + CBE  55  77  81  NA    Study (age, year)   Mode of detection   HIP (40-64) (4)   BCDDP (34-74) (9)   CNBSS (40-49) (6)   MA + CBE   MA + CBE   MA + CBE   Single CBE   MA only  77  85  93  NA  CBE only  59  76  84  86  MA + CBE  55  77  81  NA  * MA = mammography; CBE = clinical breast examination. View Large Table 6. Deaths due to invasive breast cancer 10 years* after entry among CNBSS subjects aged 40-49† Allocation   MA + CBE   CBE only   Screen-1  15  9  Interval-1  6  10  Deaths due to other causes  1  2    Total  22  21  Allocation   MA + CBE   CBE only   Screen-1  15  9  Interval-1  6  10  Deaths due to other causes  1  2    Total  22  21  * One CBE screen death occurred at 10 y 3 m and one at 10 y 16 d. † MA = mammography; CBE = clinical breast examination. View Large References (1) Black WC, Nease RF Jr, Tosteson AN. Perceptions of breast cancer risk and screening effectiveness in women younger than 50 years of age. J Natl Cancer Inst  1995; 87: 720-31. Google Scholar (2) Baines CJ. Women and breast cancer: is it really possible for the public to be well informed? [editorial]. Can Med Assoc J  1992; 146: 2147-8. Google Scholar (3) Fletcher SW, Black W, Harris R, Rimer BK, Shapiro S. Report of the International Workshop on Screening for Breast Cancer. J Natl Cancer Inst  1993; 85: 1644-56. Google Scholar (4) Shapiro S, Venet W, Strax P, Venet L, Roescer R. Ten- to fourteen-year effect of screening on breast cancer mortality. J Natl Cancer Inst  1982; 69: 349-55. Google Scholar (5) Roberts MM, Alexander FE, Anderson I, Chetly U, Donnan PT, Forrest P, et al. Edinburgh trial of screening for breast cancer: mortality at seven years. Lancet  1990; 335: 241-6. Google Scholar (6) Miller AB, Baines CJ, To T, Wall C. Canadian National Breast Screening Study: 1. Breast cancer detection and death rates among women aged 40 to 49 years [published erratum appears in Can Med Assoc J 1993;148:718]. Can Med Assoc J  1992; 147: 1459-76. Google Scholar (7) Miller AB, Baines CJ, To T, Wall C. Canadian National Breast Screening Study: II. Breast cancer detection and death rates among women aged 50-59 years [published erratum appears in Can Med Assoc J 1993;148:718]. Can Med Assoc J  1992; 147: 1477-88. Google Scholar (8) Stacey-Clear A, McCarthy KA, Hall DA, Pile-Spellman E, White G, Hulka C, et al. Breast cancer survival among women under age 50: is mammography detrimental? Lancet  1992; 340: 991-4. Google Scholar (9) Seidman H, Gelb SK, Silverberg E, LaVerda N, Lubera JA. Survival experience in the Breast Cancer Detection Demonstration Project. CA  1987; 37: 258-90. Google Scholar (10) DeWaard EF, Collette HJA, Rombach JJ, Banders-van Halewijn EA, Honing C. The DOM project for the early detection of breast cancer, Utrecht, The Netherlands. J Chron Dis  1984; 37: 1-44. Google Scholar (11) Baines CJ, Miller AB, Bassett AA. Physical examination. Its role as a single screening modality in the Canadian National Breast Screening Study. Cancer  1989; 63: 1816-22. Google Scholar (12) Newcomb PA, Weiss NS, Storer BE, Scholes D, Young BE, Voigt LF. Breast self examination in relation to the occurrence of advanced breast cancer. J Natl Cancer Inst  1 991; 83: 2605. Google Scholar (13) Harvey BJ, Miller AB, Baines CJ, Corey PN. A nested case-control study of breast self examination practice. Can Med Assoc J . In press. Google Scholar (14) Shapiro S, Venet W, Strax P, Venet L. Current results of the breast cancer screening randomized trial: the Health Insurance Plan (HIP) of Greater New York Study. In: Day NE, Miller AB, editors. Screening for Breast Cancer. Toronto: Hans Huber, 1988:3-15. Google Scholar (15) Good news on mammograms. Science  1992 ; 258: 739. Google Scholar (16) Tarone E. The excess of patients with advanced breast cancer in young women screened with mammography in the Canadian National Breast Screening Study. Cancer  1995; 75: 997-1003. Google Scholar (17) Kopans DB, Feig SA. The Canadian National Breast Screening Study: a critical review. AJR Am J Roentgenol  1993; 161: 755-60. Google Scholar (18) Baines CJ. The Canadian National Breast Screening Study: a perspective on criticisms. Ann Int Med  1994; 120: 326-34. Google Scholar (19) Bailar JC III, MacMahon B. Randomization in the CNBSS: a review for evidence of subversion. Can Med Assoc J  1997; 156: 193-9. Google Scholar (20) Boyd NF. The review of randomization in the Canadian National Breast Screening Study. Is the debate over? Can Med Assoc J  1997; 156: 207-9. Google Scholar (21) Cohen M, Kaufert P, MacWilliam L, Tate R. Checking random assignment with claims data. Can Med Assoc J  1997; 156: 1269-70. Google Scholar (22) Fletcher SW. Breast cancer screening among women in their forties: an overview of the issues. Monogr Natl Cancer Inst  1997; 22: 5-9. Google Scholar (23) Andersson I, Janzon L. Reduced breast cancer mortality in women under age 50: Updated results from the Malmö Mammographic Screening Program. Monogr Natl Cancer Inst  1997; 22: 63-7. Google Scholar (24) Winchester DP. Physical examination of the breast. Cancer  1992; 69: 1947-9. Google Scholar (25) Campbell HS, McBean M, Mandin H, Bryant H. Teaching medical students how to perform a clinical breast examination. Acad Med  1994; 69: 993-5. Google Scholar (26) Campbell HS, Pilgrin CA, Fletcher SE, Morgan TM, Lin S. Improving physicians' and nurses' clinical breast examination. A randomized controlled trial. Am J Prev Med  1991; 7: 1-8. Google Scholar Oxford University Press http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png JNCI Monographs Oxford University Press

Mammography Versus Clinical Examination of the Breasts

JNCI Monographs , Volume 1997 (22) – Jan 1, 1997

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References (28)

Publisher
Oxford University Press
Copyright
Oxford University Press
ISSN
1052-6773
eISSN
1745-6614
DOI
10.1093/jncimono/1997.22.125
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See Article on Publisher Site

Abstract

Abstract Using published data from screening trials, this article compares two-modality (mammography and clinical examination) and single-modality (clinical examination alone) screening by evaluating cancer detection rates, program sensitivities, mode of cancer detection in two-modality screening, nodal status at time of detection, survival 10 years postdiagnosis, and breast cancer mortality 10 years after entry. Consistently, two-modality screening achieved higher cancer detection rates and program sensitivity estimates than either modality alone; mammography alone achieved higher rates than clinical examination alone; interval cancer detection rates between screening examinations were higher following clinical examination alone than mammography alone; single-modality screening with mammography failed to detect breast cancers identified by clinical examination alone; the sensitivity of mammography was lower in younger than older women, while the reverse was true for clinical examination; and mammography identified a higher proportion of node-negative breast cancer than clinical examination. We conclude that combining clinical breast examination with mammography is desirable for women age 40-49 because mammography is less sensitive in younger than older women. Careful training and monitoring are, however, as essential with clinical examiners as with mammographers. In countries where breast cancer is not a major priority and where funding for and expertise in screening mammography are scarce, clinical examination of the breasts as a single screening modality unquestionably deserves consideration. However, in North America, where breast cancer is a priority and mammography is relatively accessible, the real issue is not “screening mammography versus clinical examination,” but rather “screening mammography with clinical examination versus screening mammography without clinical examination.” Unfortunately, this issue is rarely addressed, probably due to two major factors: pervasive confidence in technology as a solution for most problems facing society; and the population's generally inflated view of the risks of getting breast cancer, of dying from breast cancer and, in particular, of benefiting from mammographic screening (1,2). Furthermore, when clinical breast examination is considered for inclusion in a mammography screening program, it is often dismissed for economic reasons. In general, mammography gets much attention and clinical breast examination is usually given short shrift, just as chest x-rays and electrocardiograms have diminished reliance on percussion and auscultation of the chest. Several years ago, at a meeting on breast cancer, a speaker commented that “in an era when modern mammography is available, the use of clinical breast examination in screening is unethical and irrational.” He raised an important issue. What is the role of clinical breast examination in screening for breast cancer? Is it dispensable? Answering these questions is difficult because there are few opportunities allowing valid comparisons of two-modality screening (mammography and clinical breast examination) with single-modality screening (clinical breast examination alone). The question may be particularly important for women age 40 to 49, for whom there is widespread controversy about the efficacy of mammography screening. Data Sources Of eight randomized controlled trials (RCTs) of breast cancer screening reported to date (3), the four Swedish RCTs used only mammography, leaving four that incorporated clinical breast examination in their protocol, namely the New York Health Insurance Plan (HIP) Study (4), the Edinburgh RCT (5), and the Canadian National Breast Screening Studies (CNBSS) I (6) and II (7) (Table 11). The manner in which these RCTs differed from each other must be understood. Respective ages at entry were 40-64 years, 45-64 years, 40-49 years, and 50-59 years. The intervention group in the HIP study and both CNBSS trials received annual two-view mammography and clinical breast examination. In the Edinburgh trial, the intervention group received two-view mammography with clinical breast examination at the first screen visit, one-view mammography with clinical breast examination at the third, fifth, and seventh screens, and clinical breast examination alone at the second, fourth, and sixth screens. Control groups in the HIP and Edinburgh trials received no screening at all. In CNBSS-I, the control group received a single clinical breast examination and thereafter depended on “usual care” in the community. They were followed annually by mailed questionnaire. In CNBSS-II, the control group received annual clinical breast examinations. In addition to results from screening trials, clinical breast examination has been evaluated in case series (8) and in screening projects (9,10), all disadvantaged by the lack of an appropriate comparison group. In contrast to the case series, two screening projects—the Breast Cancer Detection Demonstration Project (BCDDP) (9) in the United States and the DOM Project in Utrecht (10), both of which used two-modality screening—do provide useful data on clinical breast examination for comparison purposes with the RCTs. The quality of the breast examination is also an important issue. Clearly, high performance standards are as important for clinical examination as for mammography. The CNBSS has established what competent clinical breast examination alone can achieve in terms of cancer detection (11). Recent research on the efficacy of breast self-examination (BSE) also reinforces the importance of high standards: benefit from BSE seems to be restricted to competent practitioners (12,13). We are not aware of any published document describing training, monitoring, or routine evaluation of clinical examiners in the HIP study, the BCDDP, or the Edinburgh trial. In the Utrecht Project, the clinical examination was performed by the radiological technologist at the time of mammography, and she used a cupped hand to palpate four quadrants of each breast (personal communication). This is in marked contrast to the method applied in the CNBSS, where the examiners were trained to visually examine the breasts, to palpate the whole breast (not just the cone), to use a systematic search pattern, and to apply the pads of their fingers. Women were examined both sitting up and lying down (11). Overall, the standards achieved by CNBSS clinical breast examination were high. Approaches to Analysis The constraints on evaluation of clinical breast examination arising from the various study designs are apparent in Table 11. Even so, the four RCTs and the two screening projects that combined clinical breast examination with mammography allow several approaches to evaluating the role of the former: cancer detection rates, program sensitivities, mode of cancer detection, nodal status at time of cancer detection, survival 10 years postdiagnosis, and breast cancer mortality 10 years after entry. a) Cancer detection: Only the CNBSS allows detection rates to be compared for combined versus single-modality screening, since in the other two RCTs the comparison was screening versus no screening, and in the screening projects there were no control groups. In CNBSS-I, for women 40-49 years on entry, two-modality screening can be compared with clinical examination alone, but only for cancers detected at the first screening visit and up to 12 months thereafter. (Because intervention women received their second screening examination 12 months after the first, subsequent comparisons on the role of clinical breast examination are not possible; one can only compare program outcomes with respect to breast cancer incidence and breast cancer mortality.) In contrast, in CNBSS-II, for women 50-59 years on entry, two-modality screening can be compared with clinical examination alone for four or five successive annual screening examinations. Not only can breast cancer be detected as a direct consequence of a screening examination, it can also be detected in the interval between screening visits. Such “interval cancers” may only become detectable after the screening examination, or they may be missed by the screening process (in both cases, the screens are said to be “false negative”). Any evaluation of clinical breast examination must consider interval cancer rates. b) Program sensitivities (detection method): Only the CNBSS studies yield sensitivity estimates for a screening protocol that includes clinical examination alone. c) Mode of cancer detection: For women receiving two-modality screening, the proportions of breast cancer detected by mammography alone, by clinical examination alone, and by both simultaneously can be documented. This is possible within the intervention arm in the four RCTs and in the two screening projects. d) Nodal status at time of detection: This offers yet another way to evaluate clinical examination. With the data available, comparisons of nodal status are possible according to both mode of detection within the intervention arms in all four RCTs and intervention versus control status in the two CNBSS trials. The latter is of greater relevance in evaluating clinical breast examination. e) Survival postdiagnosis: For this approach, data from the three North American studies—CNBSS, HIP, BCDDP—relate survival to mode of detection for two-modality screening. Additionally, in the CNBSS, survival associated with single-modality screening can be reported. f) Mortality from breast cancer 10 years after entry: CNBSS-I breast cancer mortality in cases with year-one screen and interval detections will be described because it offers the only opportunity to compare mortality following a single episode of two-modality screening to mortality following a single episode of single-modality nonmammographic screening in women age 40-49. What Can Screening With Clinical Breast Examination Achieve? a) Cancer detection: Unfortunately, there are only three trials in which clinical breast examination was conducted in the absence of mammography: the Edinburgh trial (5) and CNBSS I and II (6,7). It is clear from Table 22 that two-modality screening will detect more breast cancer than clinical examination alone. Edinburgh detection rates for clinical examination at screening rounds 2, 4, and 6 were lower than the rates observed in the CNBSS for women age 50-59 (7). However, the Edinburgh women received mammography in rounds 1, 3, 5, and 7, and this may have depleted the breast cancers available for diagnosis by clinical examination in the following years. The rates might also be lower because the quality of the clinical examination did not match that in the CNBSS. A straightforward comparison of the Edinburgh and Canadian trials is clearly impossible. The CNBSS-I detection rate for women age 40-49 screened with clinical examination alone at the first screening round was 2.46/1,000 (6), a rate exceeding the rates reported for the Swedish two-county and Stockholm mammography-alone trials, which were 2.09/1,000 and 2.06/1,000, respectively, in women age 40-49 at entry (3). Interval cancer rates can be expected to be higher following screening with clinical breast examination alone compared to screening with mammography. At the first screen, for those age 40-49 at entry, CNBSS interval cancer rates were higher in women allocated to receive clinical breast examination only (1.11/1,000 women) than in those receiving two-modality screening (0.75/1,000 women). Given that CNBSS mammography achieves detection rates and sensitivity estimates that match other trials (3), it cannot be suggested that the comparison of CNBSS interval rates is unduly favorable to clinical examination. For women age 40-49, this raises the question, How important is the difference between interval rates in the two groups being compared? b) Program sensitivity (detection method): Sensitivity estimates are higher for two-modality screening than for single-modality with mammography. For women age 40-49 on entry, the sensitivity of two-modality screening with two-view mammography was much higher in the CNBSS (81%) compared to single-modality with single-view mammography in the two-county study (62%) and in the first screen of the Stockholm study (53%) (3). Only the CNBSS trials can compare the sensitivity of mammographic screening with screening by clinical breast examination alone (11). Comparing CNBSS sensitivity rates for two-modality screening to single modality with clinical breast examination in the two age groups, 40-49 at entry and 50-59 at entry, four observations can be made. First, two-modality screening achieved a higher sensitivity in older (88%) than younger (81%) women. Secondly, sensitivity estimates for clinical examination alone were slightly higher in younger women (68% vs. 63%). Thirdly, two-modality screening achieved a higher sensitivity in both older and younger women than single-modality screening with clinical breast examination. Fourth, in the CNBSS, the observed sensitivity for clinical examination alone in women age 40-49 is of the same order of magnitude (68%) as that observed in the two-county and Stockholm mammography-alone trials (62% and 53%, respectively) (3). However, the fact remains that mammography achieves higher detection rates than clinical examination alone (Table 33). It may be advisable to use 1) two-modality screening for women age 40-49, based on lower mammography and higher clinical examination sensitivity estimates for this age group compared to older women and 2) single-modality, two-view mammographic screening for women 50 years and over, based on higher mammography sensitivity estimates and lower estimates for clinical examination for older women relative to younger women. c) Mode of cancer detection: Table 33 displays the mode of cancer detection (for screen-detected tumors) in the intervention arms of the four RCTs and the two screening projects. The proportions detected by clinical breast examination alone vary from 3.3% in Edinburgh (5) to 44.7% in the HIP study (15). If one looks at the proportion of all clinically positive screening examinations, it varies from 44% for Utrecht to 74% for Edinburgh. The usefulness of clinical breast examination is demonstrated by the fact that there is no trial in which mammography identified all breast cancers. Although Edinburgh comes close at 96%, its provision of mammography every second year precludes results that can truly evaluate the role of clinical breast examination. The data in Table 33 reinforce the advisability of adding clinical breast examination to mammography screening in younger women. In the CNBSS, for women age 40-49 allocated to mammography, clinical examination alone was the mode of cancer detection in 23.5%, compared to only 12% for women age 50-59 allocated to mammography. d) Nodal status: Mammographically detected cancers are more likely to be node negative than those detected by clinical examination. Table 44 reveals not only that single-modality screening in CNBSS-I detected fewer cancers (55) at the first screening round than two-modality (86), but also that the latter is associated with a higher proportion of node-negative invasive tumors and a marginally higher proportion of node-positive tumors. Since equal numbers of women were assigned to the intervention and control arms, 25,214 and 25,216, respectively, it is appropriate to show frequencies rather than rates. e) Survival postdiagnosis: Table 55 compares survival at 10 years postdiagnosis according to mode of detection for women with screen-detected breast cancer. Lead-time bias is not an issue here because what is being described are the survival rates associated with the three modes of detection possible in two-modality screening. The comparisons across these North American screening studies are impeded by unmatched age groupings for the cohorts, with younger women having a lower risk of breast cancer than older. CNBSS-I has the youngest cohort (age 40-49) (6) compared with the HIP Study (age 40-64) (14) and the BCDDP (age 34-74) (9). The highest survival rates are observed in the CNBSS for every mode of detection in women who received combined mammography and clinical examination. Because the CNBSS is the most recently conducted study of the three displayed, one contributing element may be better mammographic technology in the CNBSS compared to the two older trials. CNBSS 10-year survival postdiagnosis for women assigned to receive a single clinical examination matched that observed for women in the mammography arm who were detected by clinical examination only. Although the survival rates associated with detection by mammography alone in all three studies exceed those for the other two modes of detection, this is insufficient to prove that mortality from breast cancer has been reduced. The major conclusion of the Boston case series (8), implausibly endorsed in the journal Science (15), was that five-year survival postdiagnosis was excellent at 95% for women whose breast cancers were detected by mammography alone, while that for women whose breast cancer was physically palpable was much lower at 74%. The usefulness of such case series, however, is limited by the lack of an appropriate comparison group, lead-time bias, and selection bias. Indeed, in CNBSS-1, seven-year survival for breast cancer patients age 40-49 detected by mammography alone was 95%, while that for women who did not receive mammography was 91% (6). f) Deaths 10 years after entry: Much concern has been expressed about the asymmetric distribution of advanced breast cancer in CNBSS-I at the first screening round in women age 40-49 on entry (16,17), namely an excess of advanced breast cancer detected in the two-modality arm of the trial compared to the control arm. Table 66 displays the distribution of deaths that have occurred approximately 10 years after entry, in CNBSS-I women who had breast cancer detected either at the first screening round or in the first 12 months thereafter. For two-modality and single-modality groups, the distribution of breast cancer deaths in cases detected in the first year is now 21 versus 19, respectively, compared to 16 versus 10 at the seven-year follow-up (6). Including deaths in women with breast cancer due to other causes [all causes of death in breast cancer patients are verified by external panel review (18)], the totals are 22 and 21 for the two groups, respectively. This near equalization in distribution should lessen the persuasiveness of criticism directed at the CNBSS (16,17), especially in light of similar patterns of mortality observed in other trials (18). The CNBSS mortality results are compatible with conclusions reached from meta-analyses, namely that benefit from screening women age 40-49 is slow to appear. The recently published external review of CNBSS randomization (19) by forensic experts found no evidence of subversion in CNBSS randomization procedures. An accompanying editorial (20) includes factual inaccuracies that have recently been corrected (21). This is not the first time that factual inaccuracies have been published (18). Conclusions Proponents of mammography screening in women age 40-49 have rightly said it is inappropriate to recommend clinical breast examination for screening in the absence of evidence. Certainly evidence from an RCT in North America comparing screening with clinical breast examination to no screening will never be available. Therefore, evidence on clinical breast examination from existing trials and projects must be examined. In fact, only the CNBSS allows comparative evaluation of clinical breast examination, and the comparison is with two-modality screening, not “no screening.” Because proponents of mammography have repeatedly called the CNBSS mammography “flawed” (16,17), the question arises, Are the achievements of clinical breast examination in the CNBSS enhanced because of “flawed mammography”? As has been reported before (18), there is much evidence to answer “no.” The CNBSS has achieved results equal to or better than other RCTs with respect to successful randomization (which cannot be similarly documented for any other trial), cancer detection rates, prevalence/incidence ratio, and survival. In short, there is no persuasive evidence that “flawed” mammography enhanced the achievements of clinical breast examination observed in the CNBSS. Unquestionably, by any of the parameters examined, screening with mammography, alone or in combination with clinical exam, performs better than clinical breast examination alone. The differences described may be smaller and possibly less important than many would predict, with one major exception: cancer detection rates. These are always considerably higher when mammography is used. Nevertheless, this may not be an unqualified benefit given the likelihood of overdiagnosis (22,23). Because two-modality screening out-performs mammography alone, there is a role for clinical breast examination in breast screening if women are to gain the most benefit from screening. It has long been known that biopsy of a palpable mass should not be deferred because of negative mammograms (24). With mammography alone, lumps will be overlooked, especially in younger women. As with mammography, breast examination technique must be excellent in order to be useful. And excellence can be achieved. It has been demonstrated that medical school curricula could be revised to enhance clinical breast examination competence among medical students (25) and that educational programs can effectively improve examination competence among health professionals (26). The need to achieve excellence should not be a deterrent to clinical breast examination any more than it has been to mammography. If clinical breast examination is to be employed in screening, examiners will need to be carefully trained and monitored. If the costs of a screening program must be limited, one could recommend that clinical breast examination should, at the very least, be part of the screening protocol for women under age 50 because, at that age, the sensitivity of mammography is lower than in later years. Table 1. Available data sources for evaluating clinical breast examination* Source (start date)   Design   Age at entry (year)   Study intervention   Frequency   Control intervention   HIP (1963) (4)  RCT  40-64  MA + CBE  q l y  No screening  Edinburgh (1979) (5)  RCT  45-64  MA + CBE  q 2 y  No screening        (Rounds 1, 3, 5, 7)        CBE  q 2 y  No screening        (Rounds 2, 4, 6)  CNBSS-I (1980) (6)  RCT  40-49  MA + CBE  q 1 y  Single CBE  CNBSS-II (1980) (7)  RCT  50-59  MA + CBE  q l y  Annual CBE  BCDDP (1972) (9)  Project  37-74  MA + CBE  q 1 y  NA  Utrecht (1975) (10)  Project  50-64  MA + CBE  Variable  NA  Source (start date)   Design   Age at entry (year)   Study intervention   Frequency   Control intervention   HIP (1963) (4)  RCT  40-64  MA + CBE  q l y  No screening  Edinburgh (1979) (5)  RCT  45-64  MA + CBE  q 2 y  No screening        (Rounds 1, 3, 5, 7)        CBE  q 2 y  No screening        (Rounds 2, 4, 6)  CNBSS-I (1980) (6)  RCT  40-49  MA + CBE  q 1 y  Single CBE  CNBSS-II (1980) (7)  RCT  50-59  MA + CBE  q l y  Annual CBE  BCDDP (1972) (9)  Project  37-74  MA + CBE  q 1 y  NA  Utrecht (1975) (10)  Project  50-64  MA + CBE  Variable  NA  * MA = mammography; CBE = clinical breast examination; q 1 y = annually; q 2 y = every two years. View Large Table 2. Screen detection rates/1000: two- versus single-modality screening*   CNBSS   Edinburgh (5)   Trial age intervention rounds   40-49 (6)   50-59 (7)   45-64   MA + CBE   CBE   MA + CBE   CBE   MA + CBE   CBE   1  3.89  2.46  7.20  3.45  6.15  —  2  1.74  —  3.74  1.95  —  1.75  3  1.99  —  2.48  1.28  3.15  —  4  2.38  —  3.14  0.89  —  0.85  5  1.84  —  2.84  1.64  3.33  —  6  —  —  —  —  —  1.03  7  —  —  —  —  3.08  —    CNBSS   Edinburgh (5)   Trial age intervention rounds   40-49 (6)   50-59 (7)   45-64   MA + CBE   CBE   MA + CBE   CBE   MA + CBE   CBE   1  3.89  2.46  7.20  3.45  6.15  —  2  1.74  —  3.74  1.95  —  1.75  3  1.99  —  2.48  1.28  3.15  —  4  2.38  —  3.14  0.89  —  0.85  5  1.84  —  2.84  1.64  3.33  —  6  —  —  —  —  —  1.03  7  —  —  —  —  3.08  —  * MA = mammography; CBE = clinical breast examination. View Large Table 3. Mode of cancer detection with two-modality screening* Study   Age (year)   n   Percent detected at screening   MA only   CBE only   MA + CBE   HIP (1988) (14)  40-64  132  33.3  44.7  22.0  BCDDP (1987)† (9)  37-74  3548  35.5  7.9  53.3  Edinburgh (1990)‡ (5)  45-64  88  22.7  3.4  73.9  CNBSS† (6)  40-49  255  40.4  23.5  36.1  CNBS† (7)  50-59  325  53.2  12.0  34.8  Utrecht (1984)‡ (10)  50-69  196  55.6  9.7  34.6  Study   Age (year)   n   Percent detected at screening   MA only   CBE only   MA + CBE   HIP (1988) (14)  40-64  132  33.3  44.7  22.0  BCDDP (1987)† (9)  37-74  3548  35.5  7.9  53.3  Edinburgh (1990)‡ (5)  45-64  88  22.7  3.4  73.9  CNBSS† (6)  40-49  255  40.4  23.5  36.1  CNBS† (7)  50-59  325  53.2  12.0  34.8  Utrecht (1984)‡ (10)  50-69  196  55.6  9.7  34.6  * MA = mammography; CBE = clinical breast examination. † All cancers. ‡ Invasive cancers. View Large Table 4. Screen-1 nodal status of invasive cancers in patients age 40-49 from CNBSS* Allocation nodal status   Annual MA + CBE   Single CBE   n   (%)   n   (%)   Node-negative  52  (60)  30  (54)  Node-positive  33  (38)  20  (36)  Status unknown  1  (2)  5  (10)    Total  86  (100)  55  (100)  Allocation nodal status   Annual MA + CBE   Single CBE   n   (%)   n   (%)   Node-negative  52  (60)  30  (54)  Node-positive  33  (38)  20  (36)  Status unknown  1  (2)  5  (10)    Total  86  (100)  55  (100)  * MA = mammography; CBE = clinical breast examination. View Large Table 5. Survival at 10 years by mode of detection—screen cancers only (%)*   Study (age, year)   Mode of detection   HIP (40-64) (4)   BCDDP (34-74) (9)   CNBSS (40-49) (6)   MA + CBE   MA + CBE   MA + CBE   Single CBE   MA only  77  85  93  NA  CBE only  59  76  84  86  MA + CBE  55  77  81  NA    Study (age, year)   Mode of detection   HIP (40-64) (4)   BCDDP (34-74) (9)   CNBSS (40-49) (6)   MA + CBE   MA + CBE   MA + CBE   Single CBE   MA only  77  85  93  NA  CBE only  59  76  84  86  MA + CBE  55  77  81  NA  * MA = mammography; CBE = clinical breast examination. View Large Table 6. Deaths due to invasive breast cancer 10 years* after entry among CNBSS subjects aged 40-49† Allocation   MA + CBE   CBE only   Screen-1  15  9  Interval-1  6  10  Deaths due to other causes  1  2    Total  22  21  Allocation   MA + CBE   CBE only   Screen-1  15  9  Interval-1  6  10  Deaths due to other causes  1  2    Total  22  21  * One CBE screen death occurred at 10 y 3 m and one at 10 y 16 d. † MA = mammography; CBE = clinical breast examination. View Large References (1) Black WC, Nease RF Jr, Tosteson AN. Perceptions of breast cancer risk and screening effectiveness in women younger than 50 years of age. J Natl Cancer Inst  1995; 87: 720-31. Google Scholar (2) Baines CJ. Women and breast cancer: is it really possible for the public to be well informed? [editorial]. Can Med Assoc J  1992; 146: 2147-8. Google Scholar (3) Fletcher SW, Black W, Harris R, Rimer BK, Shapiro S. Report of the International Workshop on Screening for Breast Cancer. J Natl Cancer Inst  1993; 85: 1644-56. Google Scholar (4) Shapiro S, Venet W, Strax P, Venet L, Roescer R. Ten- to fourteen-year effect of screening on breast cancer mortality. J Natl Cancer Inst  1982; 69: 349-55. Google Scholar (5) Roberts MM, Alexander FE, Anderson I, Chetly U, Donnan PT, Forrest P, et al. Edinburgh trial of screening for breast cancer: mortality at seven years. Lancet  1990; 335: 241-6. Google Scholar (6) Miller AB, Baines CJ, To T, Wall C. Canadian National Breast Screening Study: 1. Breast cancer detection and death rates among women aged 40 to 49 years [published erratum appears in Can Med Assoc J 1993;148:718]. Can Med Assoc J  1992; 147: 1459-76. Google Scholar (7) Miller AB, Baines CJ, To T, Wall C. Canadian National Breast Screening Study: II. Breast cancer detection and death rates among women aged 50-59 years [published erratum appears in Can Med Assoc J 1993;148:718]. Can Med Assoc J  1992; 147: 1477-88. Google Scholar (8) Stacey-Clear A, McCarthy KA, Hall DA, Pile-Spellman E, White G, Hulka C, et al. Breast cancer survival among women under age 50: is mammography detrimental? Lancet  1992; 340: 991-4. Google Scholar (9) Seidman H, Gelb SK, Silverberg E, LaVerda N, Lubera JA. Survival experience in the Breast Cancer Detection Demonstration Project. CA  1987; 37: 258-90. Google Scholar (10) DeWaard EF, Collette HJA, Rombach JJ, Banders-van Halewijn EA, Honing C. The DOM project for the early detection of breast cancer, Utrecht, The Netherlands. J Chron Dis  1984; 37: 1-44. Google Scholar (11) Baines CJ, Miller AB, Bassett AA. Physical examination. Its role as a single screening modality in the Canadian National Breast Screening Study. Cancer  1989; 63: 1816-22. Google Scholar (12) Newcomb PA, Weiss NS, Storer BE, Scholes D, Young BE, Voigt LF. Breast self examination in relation to the occurrence of advanced breast cancer. J Natl Cancer Inst  1 991; 83: 2605. Google Scholar (13) Harvey BJ, Miller AB, Baines CJ, Corey PN. A nested case-control study of breast self examination practice. Can Med Assoc J . In press. Google Scholar (14) Shapiro S, Venet W, Strax P, Venet L. Current results of the breast cancer screening randomized trial: the Health Insurance Plan (HIP) of Greater New York Study. In: Day NE, Miller AB, editors. Screening for Breast Cancer. Toronto: Hans Huber, 1988:3-15. Google Scholar (15) Good news on mammograms. Science  1992 ; 258: 739. Google Scholar (16) Tarone E. The excess of patients with advanced breast cancer in young women screened with mammography in the Canadian National Breast Screening Study. Cancer  1995; 75: 997-1003. Google Scholar (17) Kopans DB, Feig SA. The Canadian National Breast Screening Study: a critical review. AJR Am J Roentgenol  1993; 161: 755-60. Google Scholar (18) Baines CJ. The Canadian National Breast Screening Study: a perspective on criticisms. Ann Int Med  1994; 120: 326-34. Google Scholar (19) Bailar JC III, MacMahon B. Randomization in the CNBSS: a review for evidence of subversion. Can Med Assoc J  1997; 156: 193-9. Google Scholar (20) Boyd NF. The review of randomization in the Canadian National Breast Screening Study. Is the debate over? Can Med Assoc J  1997; 156: 207-9. Google Scholar (21) Cohen M, Kaufert P, MacWilliam L, Tate R. Checking random assignment with claims data. Can Med Assoc J  1997; 156: 1269-70. Google Scholar (22) Fletcher SW. Breast cancer screening among women in their forties: an overview of the issues. Monogr Natl Cancer Inst  1997; 22: 5-9. Google Scholar (23) Andersson I, Janzon L. Reduced breast cancer mortality in women under age 50: Updated results from the Malmö Mammographic Screening Program. Monogr Natl Cancer Inst  1997; 22: 63-7. Google Scholar (24) Winchester DP. Physical examination of the breast. Cancer  1992; 69: 1947-9. Google Scholar (25) Campbell HS, McBean M, Mandin H, Bryant H. Teaching medical students how to perform a clinical breast examination. Acad Med  1994; 69: 993-5. Google Scholar (26) Campbell HS, Pilgrin CA, Fletcher SE, Morgan TM, Lin S. Improving physicians' and nurses' clinical breast examination. A randomized controlled trial. Am J Prev Med  1991; 7: 1-8. Google Scholar Oxford University Press

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JNCI MonographsOxford University Press

Published: Jan 1, 1997

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