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Mammography Screening for Breast Cancer


									          Mammography Screening for Breast Cancer
                                                      Robert A. Smith, PhD

Introduction                                                        studies was determining the efficacy of breast imaging with
    In 2005, breast cancer is the most common cancer diag-          mammography in the reduction of deaths from breast cancer.
nosed in women, and the second leading cause of death from          Among these eight trials, the Health Insurance Plan of Greater
cancer. In the U.S. in 2005, nearly 270,000 women will be           New York (HIP) study of breast cancer screening was the first
diagnosed with either invasive or in situ breast cancer, and        of these studies to be initiated (1963), and nearly twenty years
40,410 women will die from this disease.1 Because incidence         later the last of these studies, the Gothenberg trial, was initiated
rates are continuing to increase at a small rate each year, and     in 1982. The latest follow-up for these trials was in the late
because the post-war birth cohort is aging and swelling the size    1990s, with the exception of the Swedish Two County study
of the population of women in the age groups at risk for breast     which still maintains active follow-up after 20 years.6 The most
cancer, each year a larger number of women will need screening,     recent meta-analysis of all the trials combined shows a statis-
and a larger number of women will need treatment for breast         tically significant mortality reduction of 20% among women
cancer.2 However, while the age-adjusted incidence rate and         aged 40-69 associated with an invitation to screening (see Table
number of new cases of breast cancer is increasing each year, the   1 next page). 16 Breast cancer mortality reductions observed in
age adjusted mortality rate and number of deaths is declining       the individual trials range from 32% (the Swedish Two County
at an average annual rate of -2.3% per year since 1990.1 ,2 What    Trial) to no difference in the death rate between the invited and
these statistical trends mean to clinicians and to women, and       control group (National Breast Screening Study [NBSS] I &
indeed, to the entire community that is touched by breast           II). 16
cancer, cannot be understated. At a time when the population           The RCTs were initiated over a long period of time. Al-
of women at risk is growing by more than a million women            though they differed in important ways, i.e., study method-
each year, in 2005 there will be thousands fewer breast cancer      ology, screening protocol, adherence to the randomization
deaths than would otherwise have occurred if the long-term          assignment (compliance and contamination), and the number
pre-1990 trend in stable age-adjusted mortality rates had           of screening rounds before the end of the trial (or before an
continued.                                                          invitation was extended to the control group), it is not entirely
   This article is devoted to summarizing the current status of     possible to identify the specific factors or combination of
breast cancer screening and the pivotal role screening plays in     factors that account for the range of differences in the end
saving lives from breast cancer. The main evidence for screening    results. However, there is remarkable consistency in the relative
derives from the randomized clinical trials of screening and        risk of being diagnosed with an advanced breast cancer and the
more recently from the evaluations of service screening (i.e.,      relative risk of dying from breast cancer (see Table 1 next page).
screening outside of experimental settings) in the community.       In this respect, one can speculate about possible ways in which
Although numerous aspects of mammography have been a                a particular RCT was conducted, both in terms of known and
source for on-going debate, the evidence and underlying logic       obvious differences, as well as those factors that are less
supporting early breast cancer detection is sound and sup-          apparent that also could influence end results (the quality of the
ported by leading guidelines groups. At this time, the greatest     screening process, thresholds for diagnosis, follow-up mecha-
potential to reduce deaths from breast cancer is through            nisms, etc.) Yet, the most simple and straightforward data
reducing the incidence rate of advanced disease.                    explain very clearly why some RCTs showed significant mor-
                                                                    tality reductions, and some did not - specifically those trials that
Mammography                                                         succeeded in reducing the risk of being diagnosed with a node
The Randomized Trials of Breast Cancer Screening                    positive tumor, which is the fundamental goal of screening,
    Mammography is a low-dose x-ray examination of the              also observed a parallel reduction in the death rate from breast
breast using dedicated equipment. Eight prospective random-         cancer.16 ,17 Michaelson and colleagues have detailed the cumu-
ized clinical trials (RCT) of breast cancer screening with mam-     lative distribution of tumor sizes between the invited and
mography have been completed,3-14 and one recently initiated        control group in the Swedish Two County trial and the NBSS
trial in the United Kingdom (UK) focused on younger women           1 & 2. This difference also is very apparent, which explains why
still is underway.15 Some of the RCTs also included clinical        the Two County Trial observed a statistically significant mor-
breast examinations (CBE), but the primary focus of these           tality reduction and the NBSS did not.18
Address Correspondence to: Dr. Robert A. Smith, Director            Age Specific Benefits of Mammography
of Cancer Screening, Cancer Control Sciences Department,                 Perhaps only those who have been sleeping on a hill in
American Cancer Society, 1599 Clifton Rd, NE, Atlanta,              the Catskill Mountains for the past 20 years are unaware that
GA 300345 Email:                           there has been an unrelenting debate over the value of screening

www . DCMS online . org                                                                     Northeast Florida Medicine    Fall 2005   7
          Table 1                 The Randomized Trials of Breast Cancer Screening

in women under age 50.19 What has been most remarkable               deaths in the years after diagnosis.24 In women 50+, the wider
about this debate for the past decade or more is that it has         screening interval was effective in grade three tumors due to
persisted despite persuasive evidence showing that screening         longer sojourn times. For grade 1 and 2 tumors, a similar effect
is effective in women ages 40-49. This debate arose out of an        was seen in women under age 50 and over age 50 at random-
interest in exploring age-specific benefits from the early RCTs.     ization. The results are consistent with other large series that
Although three trials showed a statistically significant mortal-     have showed little difference in 5 and 10 year survival by age
ity reduction for women aged 50+, before 1997 mortality              when survival is calculated based on tumor characteristics. 25 In
reductions for women randomized in their forties did not             that same year, results from two second generation trials that
achieve statistical significance. Further, there was concern about   screened women under age 50 (at randomization) at 12-18
radiation exposure in younger women, which was reasonable,           month intervals showed statistically significant mortality re-
but poorly quantified and influenced by bias in benefit to risk      ductions of 36% and 44% associated with an invitation to
calculations.20                                                      screening 7 ,11, and with longer follow-up, meta-analysis also
                                                                     has show mortality reductions among women aged 40-49 and
   Although none of the early RCTs were designed with
                                                                     50+ at randomization, with no statistically significant differ-
sufficient statistical power to measure age-specific benefits in
                                                                     ence between the relative risks. 16
10 year subgroups, a lack of confidence in the value of mam-
mography in younger women took hold.21 Those who sup-                   Despite these data, some persist in looking backwards and
ported screening beginning in the forties cited the limitations      clinging to the older data to argue that screening women in their
of study design, the lack of evidence to suggest why mammog-         forties remains controversial. 26 However, based on current
raphy shouldn’t be effective in this group, and compelling           evidence, there is no basis for continuing to question the
evidence that the reason mammography appeared to be less             benefit of screening in this age group.
effective was due to the fact that premenopausal women in the
                                                                     The Evaluation of Service Screening
RCTs were screened at too long an interval.22 In 1985 Tabar,
                                                                         Service screening is a common European description for
et al showed that the interval cancer rate was twice as high in
                                                                     organized screening in the community. In the U.S. there are
women under age 50 compared with women 50 plus. If the
                                                                     very few service screening programs—most screening is what
screening interval is too long, then faster growing tumors have
                                                                     is referred to as opportunistic, i.e., screening that occurs as a
the opportunity to progress undetected from small curable
                                                                     result of individual initiative, or coincidently, as in the case
cancers to those that have spread and have worse prognosis.23
                                                                     when a physician reminds his or her patient that they are due
In 1997, data from three Swedish RCTs confirmed this hy-
                                                                     for a mammogram. The available data suggest that a majority
pothesis. Tabar et al showed that what appeared to be a delay
                                                                     of women in the U.S. cannot depend on a reminder system to
in benefit was simply the lack of 2 yearly screening on mortality
                                                                     help them get regular mammograms at an interval
from grade three tumors, which account for most of the early

8   Fall 2005   Northeast Florida Medicine                                                                     www . DCMS online . org
recommended by the American Cancer Society (ACS) or the                in overall breast cancer mortality after adjustment for selection
United States Preventive Task Force (USPTF).27                         bias, associated with the policy of offering screening to the
                                                                       population. The similarity of these two estimates is due to the
    As noted, while the breast cancer screening RCTs demon-
                                                                       extraordinarily high screening attendance rate (> 90%). Greater
strated the efficacy of screening, they provide a less clear measure
                                                                       breast cancer mortality reductions were observed in those
of the effectiveness of modern mammography for several
                                                                       counties that had offered screening longer than 10 years (-32%)
reasons. First, RCT methodology is based on “intention to
                                                                       compared with counties that had offered screening less than
treat,” meaning the final analysis is based on the randomiza-
                                                                       10 years (-18%), adding to the evidence that long term follow-
tion assignment and not strictly exposure to screening. In the
                                                                       up is necessary to measure the benefit of a screening program
experimental group there will be deaths among women who
                                                                       on reducing breast cancer deaths.
never got a mammogram, and likewise, in the control group
there will be deaths averted because women sought mammog-                 Finally, in a separate analysis, the investigators examined the
raphy outside of the trial. Humans cannot be treated like              effectiveness of mammography based on age at diagnosis. The
laboratory animals, and thus non-adherence to the random-              importance of this analysis becomes evident when one consid-
ization assignment results in diminished statistical power and         ers that controversies around screening younger women were
bias in the estimate of benefit.                                       complicated by the fact that age at randomization in the RCTs
                                                                       was regarded as a proxy for age at diagnosis, when in fact a
   There is a trade off, of course, because the RCT intention to
                                                                       significant proportion of women randomized in their forties
treat analysis with a death endpoint holds other more worri-
                                                                       passed their fiftieth birthday during the trial. One hypothesis
some biases (lead time bias, length bias, overdiagnosis bias,
                                                                       that was advanced to explain the small benefit that was
and selection bias) constant between the two groups. How-
                                                                       observed in women in their forties was that it was mostly due
ever, for the practicing physician advising a patient to be
                                                                       to those women randomized in their forties who were diag-
screened, the true benefit of screening is more closely approxi-
                                                                       nosed with breast cancer after their fiftieth birthday. 31 They
mated by the mortality reduction among women who actually
                                                                       observed a 48% mortality reduction in women ages 40-49 at
participate in screening. Second, as noted above, the RCTs
                                                                       diagnosis based on the 18-onth screening interval offered to
represent a continuum of technological advancement and
                                                                       women aged 40-54 in Sweden, and a 44% mortality reduction
clinical experience, as well as design decisions that contributed
                                                                       in women aged 50-69 at diagnosis based on a 24-month
to failing to measure the ultimate advantage of the value of early
                                                                       screening interval. These data demonstrate that organized
detection. Mammography has come a long way since the most
                                                                       screening with high rates of attendance in a setting that achieves
recent RCTs were initiated, and it is not only reasonable but
                                                                       a high degree of programmatic quality assurance can achieve
important to measure the effectiveness of mammography in
                                                                       breast cancer mortality reductions equal to or greater than
the community.
                                                                       observed in the randomized trials.
   The evaluation of screening in the community is more
                                                                       Physical Examination of the Breast—Clinical Breast Exam and
challenging than in a controlled study. The effect of screening
                                                                       Breast Self Exam
on population-based mortality rates depends on knowing (1)
when screening is introduced, (2) the duration of time required           Breast self examination (BSE) has been endorsed for many
to invite the eligible population to screening, (3) the rate of        years as a simple way for women to identify beast cancer earlier
screening uptake in a population, and (4) the ability to distin-       than they otherwise would if a cancer progressed to the point
guishing between screened and unscreened cohorts in mortal-            of being symptomatic. While this concept is inherently logical,
ity analysis. This last point is especially important because          the evidence for a benefit from BSE is quite limited and
deaths resulting from cases diagnosed before the introduction          contradictory. The early studies of BSE were not prospective
of screening will predominate in mortality statistics for ten or       randomized trials, and although many were suggestive of a
more years after the introduction of screening.28                      benefit, others were not. 32 One completed RCT that was
                                                                       conducted in Shanghai concluded that teaching BSE was not
   The Swedish Organised Service Screening Evaluation Group            associated with a mortality reduction, and questioned the
has been able to classify breast cancer cases before and after the     wisdom to devoting resources to instruction in self examina-
introduction to screening on the basis of exposure to screening        tion. 33 ,34 Although not noted by the authors, the group
in order to measure the benefit of screening among those               randomized to BSE instruction had a lower cumulative inci-
women who actually attended screening, and also to measure             dence of advanced disease, and thus with longer follow-up, a
the effect over time of changes in awareness and therapy that          mortality benefit could be anticipated. Still, it appeared that the
also may have contributed to mortality reductions independent          advantages of BSE instruction were modest.
of screening. 28-30 A recent report, which expanded an earlier
analysis of two Swedish counties to seven counties in the                  The logic for BSE is so straightforward that at first glance
Uppsala region, Duffy and colleagues compared breast cancer            these results seem counterintuitive. However, the findings
mortality in the pre-screening and post-screening periods              have clear implications for any setting in which there is a
among women aged 40-69 in six counties, and 50-69 in one               heightened awareness of breast symptoms. In the Shanghai
county. 28 Overall, they observed a 44% mortality reduction in         study, the results showed a relatively high rate of self-detection
women who actually underwent screening, and a 39% reduction            of localized breast cancer in the control group, suggesting that
                                                                       a significant proportion of the women in the Shanghai already

www . DCMS online . org                                                                        Northeast Florida Medicine    Fall 2005   9
were highly responsive to new breast symptoms without                    lower rate of breast cancer detection attributable to CBE alone.
formal instruction in BSE. Thus, there may be a limit to the             Oestreicher, et al. measured the sensitivity of CBE in 468
potential of BSE to measurably improve on what is achieved               women diagnosed with breast cancer within a year of screening.
through incidental self-detection in a highly aware population.          Overall, the sensitivity of CBE was 35%, but the majority of
While there are some data that suggest that highly regular and           these CBE detected cases (83.6%) also were visible on mam-
competent BSE is associated with more favorable tumor                    mography at the time of screening. Among women with false
characteristics among women with self-detected tumors, 35 it             negative mammograms, 37% were detected by CBE, but
also appears to be the case that the majority of women will not          overall, similar to the findings of Bobo et al, only 5.7% (n=27)
practice BSE in that manner. It also is possible that the                of breast cancers were diagnosed by CBE only. 44 ,45
contribution of BSE is lessened as a population gains increas-
                                                                            At this time, in women screened with regular high quality
ing awareness about breast cancer and symptoms of breast
                                                                         mammography, the cancer detection rate for CBE appears to
cancer, and has increasing access to mammography. Based on
                                                                         be low, and it also is low among women under the age of 40
these data, the ACS no longer recommends routine BSE, but
                                                                         due to the lower annual incidence in that age group. At a time
rather recommends that women have a discussion with their
                                                                         when a growing proportion of women are receiving regular
doctor about BSE and then decide for themselves whether to
                                                                         mammograms, the relative contribution of CBE to early
do monthly BSE or not. According to the ACS, it is acceptable
                                                                         breast cancer detection, and its cost-effectiveness, is worthy of
to do routine BSE, to not do routine BSE, or do BSE
                                                                         renewed attention. While some women may benefit from
irregularly. What is important is that women and their doctor
                                                                         regular CBE, it likely also is the case that in other groups of
discuss self examination, symptoms of breast cancer, and the
                                                                         women the exam adds little to the benefit currently derived
importance of prompt reporting of any new changes in their
                                                                         from women’s increased awareness and responsiveness to
                                                                         breast symptoms. An additional consideration is that the
   The logic for clinical breast examination is more straightfor-        average performance of CBE has low quality, further limiting
ward. Today, mammography and clinical breast examination                 the value of the routine use of this exam.46 At this time, the
are recommended to women 40 and older because (1) there are              ACS recommends CBE at the time of a preventive health
randomized controlled trial (RCT) data showing the combi-                examinations for women ages 20-39 at least every three years,
nation of mammography and CBE was associated with lower                  and annually beginning at age 40. ACS recommends that
breast cancer mortality 36-38;; (2) evidence from these RCTs and         clinicians use this time to talk with patients about breast cancer
demonstration projects showed that some cancers detected by              issues, the importance of awareness of symptoms, and prompt
CBE were not detected by mammography, and (3) clinical                   reporting of new symptoms if they should arise. 47 With careful
experience today also has shown that some palpable cancers               attention to the details prior to the mammography, CBE may
maynot be visualized on a mammogram, or cancers may arise                identify an area of suspicion that will not be visible on
with symptoms between screening exams. 39 However, it is                 mammography, and/or provide information that guides
important to understand the limits of CBE.                               subsequent imaging exams.
    On all aspects (sensitivity, specificity, predictive value, etc.),   Summary
the performance characteristics of CBE are poorer than those                   The evidence supporting the value of regular
of mammography. Sensitivity of CBE in particular was esti-               mammography screening in women aged 40 and older is
mated in a recent meta-analysis to be only 54%. 40 Although              sound, and among the factors that contribute to the cure of
it commonly cited that two trials demonstrated breast cancer             breast cancer, the diagnosis of a tumor early in its natural history
mortality reductions associated with the combination of                  has greater value than advances in therapy can offer to a women
mammography and CBE 5 ,41, these trials took place many years            diagnosed with advanced disease. 23 ,48 These advantages,
ago at a time when mammography quality was lower and the                 however, are only consistently achieved when women attend
proportion of breast cancers not visible with modern, high-              regular, high quality screening. As Michaelson and colleagues
quality mammography is considerably lower today than in the              have shown, failure to return for regular mammography can
past. 42-44 For example, Bobo and colleagues examined the                result in diagnosis of tumors when they are larger, more
experience from 752,081 CBEs in the Centers for Disease                  advanced, and have poorer prognosis. 49 It cannot be stressed
Control’s Breast and Cervical Cancer Early Detection Program             too strongly that, apart from insurance coverage, the key factor
and found that 6.9% of all CBEs were coded as abnormal.                  that explains whether or not a woman has had a recent
While the rate of breast cancer detection in the combined                mammogram is a recommendation from her doctor. 50 Even
mammography and CBE program was five cancers per 1,000                   after more than two decades of growing participation in
examinations, only 5.1% of the malignancies (193/3753), or               mammography, women still rely in large part on their doctor
2.56 per 10,000 CBE exams, were detected in women with an                as the critical gatekeeper, and office systems can measurably
abnormal CBE and benign findings on the mammogram. 42                    enhance the facilitation of that critical role. 51 This year,
Because women with self-detected breast symptoms were 7.2                thousands fewer women will die from breast cancer due to
times as likely to have an abnormal exam, it also is likely that         advances in screening, awareness, and therapy. These gains are
some proportion of these CBE-positive cases were first de-               also attributable in large part to the key role clinicians have
tected by women themselves, which would mean an even                     played in providing the trusted advice that women get regular

10   Fall 2005   Northeast Florida Medicine                                                                          www . DCMS online . org
mammograms. The blueprint for continued progress and                      14. Miller AB, To T, Baines CJ, Wall C. The Canadian National
greater mortality reductions is well defined, and with greater                Breast Screening Study-1: breast cancer mortality after 11 to
attention to the totality of small but critical details that contribute       16 years of follow-up. A randomized screening trial of
to the detection of early stage breast cancer, further gains in               mammography in women age 40 to 49 years. Ann Intern Med
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                      WE ONLY DO
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                                                                                            examination (CBE). Breast Cancer Res Treat 2002;76(1):73-81.

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                                                                                        45. Bobo JK, Lee NC, Thames SF. Findings from 752,081 clinical
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                                                                                            from 1995 through 1998. J Natl Cancer Inst 2000;92(12):971-
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                                                                                            et al. Clinical breast examination: practical recommendations
                                  Counsel to:                                               for optimizing performance and reporting. CA Cancer J Clin
                 Duval County Medical Society                                           47. Smith RA, Saslow D, Sawyer KA, Burke W, Costanza ME,
                    Florida Chapter, American                                               Evans WP, 3rd, et al. American Cancer Society guidelines for
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                       College of Surgeons                                                  2003;53(3):141-169.
                    Florida Chapter, American                                           48. Etzioni R, Urban N, Ramsey S, McIntosh M, Schwartz S, Reid
                                                                                            B, et al. The case for early detection. Nat Rev Cancer
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                                                                                            screening in women. Surg Oncol Clin N Am 1997;6(2):203-211.
                                                                                        51. Meissner HI, Smith RA, Rimer BK, Wilson KM, Rakowski W,
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12    Fall 2005      Northeast Florida Medicine                                                                                     www . DCMS online . org

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