Education And Debate

Is clinical breast examination an acceptable alternative to mammographic screening?

BMJ 2000; 321 doi: https://doi.org/10.1136/bmj.321.7268.1071 (Published 28 October 2000) Cite this as: BMJ 2000;321:1071
  1. Indraneel Mittra, professor of surgerya,
  2. Michael Baum, professor emeritus of surgery (m.baum{at}ucl.ac.uk)b,
  3. Hazel Thornton, founder of Consumers Advisory Committee for Clinical Trialsc,
  4. Joan Houghton, director, CRC Unitd
  1. a Department of Surgical Oncology, Tata Memorial Hospital, Mumbai-400 012, India,
  2. b Department of Surgery, University College Medical School, London W1P 7LD,
  3. c Saionara, 31 Regent Street, Rowhedge, Colchester CO5 7EA,
  4. d CRC and UCL Cancer Trials Centre, Royal Free and University College London Medical School, London W1A 8AN
  1. Correspondence to: M Baum
  • Accepted 1 August 2000

Breast cancer screening and mammography have almost become synonymous in the public perception, yet this should not necessarily be the case. Ideally, a screening tool for breast cancer would reduce mortality from breast cancer while having a low false alarm rate and being relatively cheap. Screening should not be at the expense of the symptomatic services nor inappropriately divert scarce resources away from equally deserving areas of the NHS that are less politically sensitive.1

An ideal screening test would be simple, inexpensive, and effective. Of the three modalities of breast cancer screening—breast self examination, clinical breast examination, and mammography—breast self examination fulfils the first two criteria, but early results of two randomised trials conducted in Russia and China suggest that it would not be effective in reducing mortality from breast cancer. 2 3 Clinical breast examination is also relatively simple and inexpensive, but its effectiveness in reducing mortality from breast cancer has not been directly tested in a randomised trial. Mammography is complex, expensive, and only partially effective. We believe that there is sufficient circumstantial evidence to suggest that clinical breast examination is as effective as mammography in reducing mortality from breast cancer and that the time has come to compare these two screening methods directly in a randomised trial.

Summary points

The goal of breast screening is to prevent death and not simply to detect cancers by mammography

Mammography does detect some cancers “early,” but many of these are not potentially lethal and their detection causes needless anxiety

Clinical breast examination is more likely to detect cancers that are potentially lethal

Results of the second Canadian national breast screening study suggest that mammographic detection of cancers that are not palpable does not affect mortality

New GMC guidelines on informed consent state that women in the NHS breast screening programme should be informed of the drawbacks of mammography as well as its potential benefits

A national questionnaire survey is needed to determine if women would prefer clinical breast examination to mammography and whether a randomised trial comparing the two would be acceptable

Potential of clinical breast examination as a screening test

In comparing the effectiveness of mammography with that of clinical breast examination, it is worth considering the results of the NHS breast screening programme for women aged 50 to 64. In the first round of screening, over a million women were screened, and a little over 5000 cancers were detected.4 Of these, 60% were invasive cancers >1 cm in size. Such cancers would be expected to be detected also by clinical breast examination. In fact, in the US breast cancer detection demonstration project (BCDDP) 39% of cancers <1 cm in size were detected by clinical breast examination.5 In situ cancers, which accounted for 18% of the cancers detected by mammography in the NHS programme, would not be detected by clinical breast examination, thereby reducing the potential for overdiagnosis inflicted by mammography. Only the 22% of invasive cancers detected by mammography that were <1 cm in size would be missed by clinical breast examination. Consequently, any benefit of mammography over clinical breast examination must be derived from these 22% of invasive cancers that are <1 cm in size and from an uncertain number of cases of ductal carcinoma in situ that progress to invasive cancer if left undetected. We argue that these advantages are unlikely to be clinically important.

There are two reasons for this. Firstly, if you consider the exponential growth rate and doubling time of breast cancer you find that a single breast cancer cell has to undergo 30 doublings to reach a size of 1 cm, when it will contain 109 cells and be clinically palpable (see figure). Since the average size of a non-palpable, mammographically detected cancer can be assumed to be about 0.5 cm, the lead time gained by mammography over clinical breast examination would be of the order of only one doubling. Whether this lead time equivalent of one doubling in the natural course of 30 doublings would lead to a significantly greater reduction in mortality is questionable.6

Figure1

Exponential growth of breast cancer (reproduced from Mittra 19976 with permission of Landes Biosciences)

The second reason relates to a study reported by Klemi et al,7 which compared the biological properties of mammographically detected and clinically detected breast cancers that were matched for size. For each of eight properties studied (lymph node involvement, tumour differentiation, mitotic count, tumour necrosis, ductal type or otherwise, presence of oestrogen or progesterone receptor, and S phase fraction), the mammographically detected cancers showed better prognostic signs than the clinically detected cancers. In other words, screening is good for detecting cancers with low malignant potential, and this has been observed by other workers as well. 8 9

The only study that has addressed the question as to whether the detection of non-palpable cancers reduces mortality from breast cancer has been the second Canadian national breast screening study (CNBSS II).10 This study was designed in response to the recommendation in the early 1980s of the committee reviewing the results of the US breast cancer detection demonstration project,5 which had included both yearly mammography and clinical breast examination. Consequently, in the Canadian study women aged 50-59 were randomly allocated to either clinical breast examination plus mammography or clinical breast examination alone.10 Clinical examinations were performed by trained nurses, and their performance was shown to be as good as, if not better than, that of the study surgeons.11 After a mean follow up of 13 years, there is no sign of mortality being lower in the women subjected to mammography.10 Although longer follow up may reveal a benefit, currently there is no evidence to suggest that the detection of non-palpable cancers by mammography contributes to reducing mortality from breast cancer. What the Canadian study did do, however, was to highlight the harm caused by mammography: the rate of biopsy of benign lumps was three times higher with the combined screening compared with clinical breast examination alone.

Powerful support for our contention has recently emerged from the Japanese national programme of clinical breast examination.12 In this study they describe a comparison of breast cancer mortality in municipalities with “high coverage” of clinical breast examination with that in suitable control municipalities. The percentage change in age adjusted mortality between 1986-90 and 1991-5 was over 40% in the area where “high coverage” was adopted compared with 3% in the control areas. It must be remembered that Japanese breasts lend themselves more to clinical breast examination than their European counterparts, being smaller and dome shaped rather than obese and pendulous, yet the Japanese experience could well translate to other populations.

Validity of results of second Canadian national breast screening study

The Canadian study is arguably the best conducted and most transparent of all randomised trials of screening for breast cancer, and every methodological aspect of the conduct of the trial has been published in detail.13 This is also the only randomised trial that has allowed external evaluation of the quality of its mammograms. Ironically, this transparency seems to have been its undoing, and the study has been mired in controversy and criticism from its inception. Its critics have claimed that over half of the mammograms were technically suboptimal in the first two years of the study and that even in the past two years only 70% of the films were of satisfactory quality.14 It was also reported that in several sites the mammography equipment was suboptimal and that radiologists and technicians had not received adequate training.15 The organisers of the Canadian study have refuted these charges, but the debate continues to fester.16

With regard to the quality of mammography in the Canadian study, the data published by Fletcher et al are of interest.17 They compared the performance parameters of the Canadian study with those of other reported randomised trials and showed that the various measures of screening quality in the Canadian study rivalled, if not exceeded, all other trials (see table). A comparison of indices of quality of the Canadian study with those of the US breast cancer detection demonstration project5 (both of which used yearly mammography plus clinical breast examination) showed that, although the cancer detection rates were similar in the two studies, the interval cancer rates were higher in the latter. 18 19

Indices of quality of screening in the major breast screening trials (adapted from Fletcher et al 199317 with permission from Oxford University Press)

View this table:

Even if the quality of mammograms was indeed a weakness of the study, the Canadian study also had certain strengths. Firstly, mammography was given annually rather than biennially, as has been usual in other modern breast cancer screening trials. Secondly, unlike other screening trials, the Canadian study tested the efficacy (rather than effectiveness) of screening: only those women who agreed to participate in the study were randomised. Consequently, any benefit of mammography should have been magnified as there was no dilution effect because of non-compliance in the intervention arm (usually around 30%).

Would clinical breast examination be an acceptable alternative to mammographic screening?

One of greatest benefits of the NHS breast screening programme in its 10 years of life has been the raising of people's awareness of breast cancer to the extent that many of the cancers in the screened population that are missed at mammography are found by the patients themselves.2022 Screening has therefore shifted the point of diagnosis backwards such that it has become less and less effective at reducing mortality. It has also been pointed out that the public believe the purpose of the NHS breast screening programme is to “find cancer early,” as stated by the leaflets inviting women for screening.

Ideally, we need to shift the diagnosis by screening to that point in the spectrum of presentation that will cost least both in human and financial terms and be most likely to be effective in reducing mortality: clinical breast examination would be able to fulfil this. Greater general awareness generated by the NHS breast screening programme has reduced the number of cancers remaining undetected until in a late stage. A change to clinical breast examination now would reduce the unnecessary detection of indolent, non-invasive cancers—thus restricting activity in outlying, expensive, non-productive areas of screening and focusing on the centre of the window of opportunity.

Finally it should be remembered that mammography is not appropriate technology for screening in the developing world. The misplaced desire to ape Western, “high tech” medicine in public health diverts scarce resources from simpler interventions that might have a far greater net benefit to society.23

Forming a partnership

The General Medical Council's new ethical guidelines for giving consent in screening emphasise that people considering screening should be advised about the drawbacks.24 The information currently provided to healthy women, exhorting them to attend screening because finding cancer early could save their life, is now less than honest and has not kept pace with the unexpected beneficial spin-offs and pitfalls of mammographic screening. Candidates for screening should be given honest, balanced information stating the numbers needed to screen to affect mortality and not frightened by irrelevant incidence figures or led to believe that earlier is better. Pressure from the media and women's advocacy groups tend to encourage an irrationally defensive attitude to mammographic screening. The adversarial mode is not conducive to achieving a review of the status quo: it tends to prevent a balanced assessment of the latest evidence or a proper analysis of cost effectiveness.

We must now move forward in partnership with the women themselves to plan future strategies. Proper information on which to base decisions, either about participating in a trial comparing clinical breast examination and mammography or for informing the development of a trial protocol, is essential for both the public and the profession. This could be achieved through a national questionnaire survey involving all eligible women.

Footnotes

  • Competing interests None declared.

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