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Perspective |
1 Department of Radiology, Rush North Shore Medical Center, 9600 Gross Point Rd., Skokie, IL 60076, and Rush Medical College, Chicago, IL.
Received October 31, 2000;
accepted after revision November 16, 2000.
Address correspondence to L. Berlin.
Introduction
 Top Introduction Trends in Breast Cancer...The "One-in-Eight" StatisticBreast Cancer and Mortality...Accuracy of Mammography: the...Efficacy of Mammography in...References |
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Has the frequency or severity of malpractice litigation related to delays in diagnoses of breast cancer changed in the months that have passed since publication of that AJR article? Have any of the public's perceptions or misperceptions regarding mammography changed? Does the public continue to believe that mammography is a perfect diagnostic test? Have there been any alterations in what the public perceives as the likelihood of women developing or dying from breast cancer? Has any new evidence been introduced that addresses the question of whether establishing an early diagnosis on screening mammography actually does reduce mortality from breast cancer?
In this article, I shall review considerable and, mostly, recently published data that will help answer not simply these questions but an even more important question—that is, is there a greater or lesser likelihood that a jury will rule that a defendant radiologist who is accused of missing a breast cancer on a mammogram, thereby delaying the diagnosis of breast cancer in a patient, is liable for malpractice?
Trends in Breast Cancer Litigation
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TopIntroductionTrends in Breast Cancer...The "One-in-Eight" StatisticBreast Cancer and Mortality...Accuracy of Mammography: the...Efficacy of Mammography in...References |
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TopIntroductionTrends in Breast Cancer...The "One-in-Eight" StatisticBreast Cancer and Mortality...Accuracy of Mammography: the...Efficacy of Mammography in...References |
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Writing in the New England Journal of Medicine, Phillips et al. [8] voiced concern about the frequent misuse of the one-in-eight statistic. "This is the only information on the risk of breast cancer that many women receive, and we believe that it is inadequate and potentially misleading," asserted these researchers. Nevertheless, the one-in-eight statistic seems to live on. An advertisement in the New York Times in October 2000 [9] publicizing a forthcoming special advertising section on breast cancer proclaimed in large print, "One of every eight American women will develop breast cancer" (Fig. 1). In another New York Times advertising supplement distributed in Chicago, the lead article stated, "The statistic scares every female but none can ignore it: one in every eight women in the United States will develop breast cancer" [10]. This same statistic has even found its way into the Journal of the American Medical Association. A recent "patient page" entitled "Know Your Options for Breast Cancer" included the statement that "11% of women will develop breast cancer in their lifetime" [11].
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Breast Cancer and Mortality Rates
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TopIntroductionTrends in Breast Cancer...The "One-in-Eight" StatisticBreast Cancer and Mortality...Accuracy of Mammography: the...Efficacy of Mammography in...References |
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Breast cancer is the disease women fear most.... Even though cardiovascular disease claims more lives than lung or breast cancer—one out of two American women dies of heart attacks and strokes—breast cancer inspires more fear.
In fact, 80% of women in whom breast cancer is diagnosed do not die of the disease [8], and the leading cause of death among women at any age is always something other than breast cancer. A chart published by the Mayo Clinic [13] (Fig. 2) realistically displays the various causes of death in women of any given age. The number of deaths caused by breast cancer in proportion to other causes is clearly shown and fails to provide a rational explanation as to why "breast cancer inspires more fear" than any other cause of death among women.
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Accuracy of Mammography: the Dot Game
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TopIntroductionTrends in Breast Cancer...The "One-in-Eight" StatisticBreast Cancer and Mortality...Accuracy of Mammography: the...Efficacy of Mammography in...References |
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Your critique of one of our public service announcements is well-taken.... In an effort to emphasize the benefits of mammography over physical examinations, some of our ads have oversold its potential to always find lesions when they are very, very small....Leading organizations have also been criticized for overselling the survival potential when cancers are found "early." We, and other organizations, are rethinking the spectrum of these messages....The particular public service message you enclosed [an ad showing a small dot, strongly implying that while the reader may have missed the dot, a mammographer would not] was pulled some time ago and will eventually be replaced by others that portray a more accurate and realistic message.... In the future you will see more accurate messages about both the benefits as well as limitations of mammography.
It is indeed true that the American Cancer Society no longer publishes "dot" ads; however, other organizations do. An advertisement published by the Illinois Foundation for Quality Health Care [14] (Fig. 3) shows two dots: one, 1 cm in diameter, is alleged to represent the "average size of tumors detected by regular breast-self examination." The second dot, 4 mm in diameter, is alleged to represent the "average size of tumors detected by screening mammograms." Another advertisement (Fig. 4), distributed by an insurance company in Michigan [15], shows a series of six circles or dots; the largest, 3.4 cm in diameter, is alleged to represent the size of lump that might be found "by a woman who rarely examines her own breasts." Progressively smaller dots are alleged to represent the size of a lump that might be found "by a woman who occasionally examines her own breasts," "by a woman who examines her own breasts every month," and "by a doctor or nurse giving a clinical breast exam." A dot 3 mm in diameter is alleged to represent the size of the lump that might be found "on a woman's first mammogram," and a dot 1.5 mm in diameter is alleged to represent the size of a lump that might be found "by getting a mammogram every 1-2 years."
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The radiology literature is replete with articles that document error rates among competent radiologists in the interpretation of mammograms. The literature also describes the large number of breast carcinomas seen retrospectively on mammograms originally interpreted as having normal findings once subsequent mammograms reveal a tumor. An article published in the ACR (American College of Radiology) Bulletin pointed out that 30-70% of breast cancers detected at followup mammography are visible in retrospect on initial mammograms that had been interpreted as showing normal findings [16]. Berg et al. [17] recently described research that found that experienced radiologists disagreed among themselves 32% of the time in recommending biopsy versus follow-up when interpreting screening mammograms and 45% of the time when interpreting diagnostic mammograms. Other articles published in 2000 confirmed high miss and disagreement rates in mammography and suggested that the accuracy rate can be improved by double interpretation by a second radiologist [18], by computer-assisted detection [19], or by establishing the number 2000 as the minimum number of mammograms interpreted annually by an individual radiologist [20]. It is much too soon to know whether any of these suggestions will improve the accuracy of mammographic interpretation. Even if these suggestions to prove effective in reducing error rates, it remains extremely doubtful that advertisements indicating that breast cancers the size of a small dot will be correctly diagnosed on mammograms, will ever be realistic. Nevertheless, the "dot game" seems to have a life of its own and continues to influence public perceptions.
Efficacy of Mammography in Lengthening Survival Times and Reducing
Death Rates of Patients with Breast Cancer
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TopIntroductionTrends in Breast Cancer...The "One-in-Eight" StatisticBreast Cancer and Mortality...Accuracy of Mammography: the...Efficacy of Mammography in...References |
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In his reflections, published in April 2000, on a 35-year-career as a mammographer, Edward Sickles [22] stated unequivocally that "mammography now is the most common imaging examination that directly results in the reduction of mortality from disease." Without doubt, Sickles' opinion is shared by almost all radiologists whose practices are dedicated to mammography, and also without doubt, these opinions are based on sound data. As emphasized by Feig [23], the American Cancer Society, the American College of Radiology, the American Medical Association, and the National Cancer Institute all now recommend annual screening for women beginning at 40 years old (the National Cancer Institute recommends screening mammography every 1-2 years). These guidelines are based on "statistically significant reductions in breast cancer deaths" [23] among women 35 years old and older who underwent screening mammography in randomized controlled trials. Feig reviewed European studies that found decreases in mortality rates from breast cancer of 18-40% as a result of mammography screening. In the United States, a 1989 study found a 30% decrease in the breast cancer mortality rate as a result of screening mammography [24]; in 2000, the American Cancer Society's director of cancer screening confirmed a 30% drop by extrapolating results of existing mammography trials [25]. The claim of a clear cause-and-effect relationship between screening mammography and decreased mortality rates from breast cancer has not gone unchallenged, however. Other researchers have voiced skepticism about the validity of the proposition that mammography lowers breast cancer mortality rates.
An article published in the New England Journal of Medicine in early 1993 warned that screening mammography may have the appearance of being highly effective but in reality may be ineffective [26]. In that article, Black and Welch suggested that the increase in breast carcinoma revealed by mammography was because of the finding of more ductal carcinoma in situ (DCIS) tumors, lesions that are often not malignant. As to evaluating the validity of mortality data, these researchers pointed out that such data are very much influenced by statistical phenomena known as lead-time bias and length bias. Lead-time bias pushes back the date of first diagnosis and thereby increases the interval between diagnosis and death, resulting in an apparent lengthening of survival. Length bias occurs because the more aggressive, fast-growing tumors are often found clinically and tend not to be diagnosed mammographically; primarily it is slower growing tumors that are diagnosed on mammography, a phenomenon that gives the appearance of longer survival. Black and Welch emphasized that they were not arguing that screening mammography was futile, but rather were pointing out that screening was being portrayed as highly effective when it was, in actuality, ineffective.
The controversy regarding the efficacy of mammography in decreasing mortality from breast cancer escalated in 1995 after an article by Canadian researchers was published in Lancet [27]. These researchers were extremely critical of previously published data that indicated that screening mammography decreased mortality rates from breast cancer, and concluded:
In the large majority of women whose breast cancer is diagnosed by screening, the outcome is unchanged. For most women the only "benefit" is extra time spent with the knowledge that they have the disease.... Public imagination has been captured by mammography, and all those involved in the screening industry have a major vested interest.... Public funding for breast cancer screening in any age group is not justifiable.
Fifteen months later, the Journal of the National Cancer Institute published an article by Chu et al. [28] that claimed that although a small portion of the decrease in breast cancer mortality rates could be attributed to the increased use of mammography, the increase in survival rates mainly reflected improvements in systemic adjuvant therapy, chiefly tamoxifen therapy. In the meantime, Sickles and Kopans [29] acknowledged in the Annals of Internal Medicine in 1995 that "those who require the highest degree of proof will deny that screening is beneficial for women...because published studies...do not show a statistically significant mortality reduction." Nonetheless, cautioned Sickles and Kopans:
We support the routine use of mammographic screening...because we interpret the evidence as indicating a high probability of benefit.... It seems much more prudent to endorse screening now and risk the unlikely subsequent determination that the effort was ineffective, than to withhold screening until it is determined whether "proof" will be obtained and risk the loss of so many women in the prime of life.... The decision to screen represents an opportunity for—not a guarantee of—early detection and diagnosis, but the decision not to screen represents the loss of this opportunity.
In 1997, the debate over efficacy of mammography screening developed into what one journalist called a "brawl," when the National Institute of Health held meetings to decide whether to recommend that women in their 40s undergo routine annual screening [30]. The director of the National Cancer Institute was quoted as saying he was "shocked to see firsthand the vitriol and animosity surrounding the issue" [30]. The editor of the Journal of the National Cancer Institute was reported to have described the meeting as "raucous" and "like no scientific meeting I'd ever seen before" [30]. Scientists seemed to line up in one of two groups. The experts who believed that screening should be officially recommended to women in their 40s were mainly radiologists, with a few surgeons and very few epidemiologists. The scientists who were skeptical about the benefit of screening mammography were mainly epidemiologists and public health physicians "versed in the science of evidence-based medicine" [30]. The chair of the National Cancer Advisory Board was quoted as pointing out that the animosity between the two groups of scientists was driven by beliefs that are "almost like a religion for some people" [30].
An article later in 1997 from the Journal of the American Medical Association discussed the debate at the National Cancer Institute over whether to recommend mammographic screening for women in their 40s. The chair of the Institute's advisory board said that there seemed to be confusion about the difference between finding cancer and saving lives [31]:
If I've heard one woman saying she had had her breast cancer diagnosed and was now cured, I've heard 100. But this misrepresents the truth. Not every one of these women will be cured. We have to keep in mind...the effectiveness of mammography [is] whether women lived or died, not just how many we found with breast cancer.
The debate over the efficacy of mammography screening resurfaced in 1999 with publication in a Swedish medical journal of a study that showed only a "very marginal and not significant" reduction in breast cancer mortality rate in women who had undergone mammography during a 10-year period [32]. The findings were quickly challenged by two Swedish epidemiologists who charged that the study was "defective," contained "many methodological limitations and fallacies," and "should not be considered seriously" [33].
In June 1999, Lancet published research from England and Scotland about breast cancer mortality rates during a 16-year period for women who were 45-67 years old and who had undergone mammography [34]. These researchers found a 27% decrease in mortality rates. Clinical examination in conjunction with screening mammography added little to the detection rates. Also in mid 1999, Michaelson et al. [35] used a computer simulation that showed that if mammographic screening were performed more frequently than annually, the mortality rate from breast cancer would be further reduced dramatically. That the public was convinced that mammography decreased mortality rates from breast cancer was evidenced by an article by science reporter Jane Brody in the New York Times in March 1999 that included the statement, "Early detection through mammography is one of the main reasons for the declining death rate from breast cancer" [36].
The argument as to whether screening mammography reduces mortality from breast cancer figuratively boiled over in January 2000, when Lancet published the work of Danish researchers who concluded that "screening for breast cancer with mammography is unjustified" because "there is no reliable evidence that screening decreases breast cancer mortality" [37]. An accompanying editorial written by a member of the National Evaluation Team for Breast Cancer Screening in the Netherlands [38] expressed amazement that "forty years after the start of the first breast-screening trial," researchers would challenge whether mortality reduction resulting from mammography screening actually exists. This editorial pointed out that data did in fact show decreasing mortality rates from breast cancer as a result of mammography screening in the United Kingdom, the Netherlands, and Finland, and concluded with a plea for further investigation.
Criticism of the Danish report from other sources was not as mild. An article in the Wall Street Journal quoted the chief medical officer of the American Cancer Society: "Wherever mammography has been applied in a systematic way, the death rates from breast cancer are dropping" [39]. In the same article, Daniel Kopans charged, "A lot of the Danish researchers' arguments are fallacious....It's unfortunate that The Lancet published this."
The controversy over efficacy of mammography continued to percolate briskly during 2000. In April, an article by Moody-Ayers et al. [40] published in the Archives of Internal Medicine concluded that "many of the breast cancers found by mammography screening have excellent prognosis not just because of early detection, but also because many of the cancers are relatively benign, requiring minimum therapy." These researchers explained that slow-growing lesions, DCIS in particular, are more likely to be found by mammography screening. The biologic behavior of DCIS is controversial, according to Moody-Ayers et al., and other researchers have suggested that these lesions should not even be regarded as cancer. Although Moody-Ayers et al. did not question the value of screening mammography, they did warn physicians and patients to be wary of overly enthusiastic interpretations of "therapeutic success," a misstep that has occurred in every era of medicine. "Since [mammography] screening detects early-stage and relatively benign tumors," concluded these researchers, "its survival advantages may become substantially overestimated."
DCIS is a controversial subject. To begin with, the benefit of surgical and medical intervention is not truly known [41]. One study found that the local recurrence rate of DCIS 8 years after excision ranges from 12% to 27%, and approximately one half of these recurrences are invasive and therefore a "threat to life" [42]. Before mammography, DCIS accounted for 2-3% of all diagnosed breast cancers; however, the percentage is now between 30% [22] and 40% [43]. Feig [43] believes DCIS to be a precursor of invasive ductal carcinoma; Sickles [22] believes DCIS to be cancer, although highly curable.
The argument that screening mammography reduces breast cancer mortality was strengthened further by a study published in Lancet in May 2000 that documented a decrease of 12-22% from 1987 to 1997 in the death rate of women 20-70 years old in the United Kingdom and of 9-19% in the United States, depending on specific age groupings [44]. These decreases were attributed to changes in the way breast cancer is diagnosed and treated, but the relative contributions to these decreases of drugs such as tamoxifen, and of screening mammography, were not quantified [45]. In July 2000, Tabar et al. [46] reported data that confirmed that after 20 years of follow-up in Sweden, "there was a significant 32% reduction in mortality from breast cancer associated with screening mammography.... Mammographic screening for breast cancer continues to save lives," concluded these researchers.
Uncertainty about whether mammography is efficacious in reducing breast cancer mortality was rekindled once again by Welch et al. [47] in June 2000. These researchers point out that 5-year survival rates frequently presented to the public and to policy makers as proof that we are making progress against cancer are extremely misleading. An increase in the 5-year survival rate may involve the finding of more patients early in their disease, and "any advance in the time of diagnosis will increase 5-year survival because of the spurious effect of lead-time." The only way to measure progress against cancer is using population-based mortality rates, claim Welch et al. Focusing attention on breast cancer specifically, these researchers report that the 5-year survival rate had increased from 60% for 1950-1954 to 86% for 1989-1995. However, the mortality rate had decreased only 8%, not a totally meaningless figure, but nonetheless, not a particularly impressive one either. Welch et al. suggest, but do not state with certainty, that the marked increased in 5-year survival rate, coupled with only a mild decrease in mortality rate, might be the result of the spurious effect of lead time and of more effective treatment rather than the result of successful early detection efforts.
In September 2000, another group of researchers [48] found that the mortality rate for breast cancer in England and Wales decreased 21% between 1990 and 1998; these researchers suggested that 15% of the decline was the result of better treatment and the remaining 6% the result of mammography screening. At the same time, a Canadian study published in the Journal of the National Cancer Institute drew attention from the national news media and also unleashed an immediate and angry response from the radiology community [49]. The Canadian study reported that in women 50-59 years old, the addition of annual mammography screening to physical examination detected considerably more small breast cancers with no spread to lymph nodes than screening with physical examination alone but had no impact on the breast cancer mortality rate. The American College of Radiology quickly issued a press release that called the Canadian study "badly flawed" [50]. "Breast cancer death rates have declined, in large part due to increased use of screening mammography....Other, well-conducted screening trials have documented that mammography does indeed save lives," said the American College of Radiology. The College pointed out a major reason it considered the Canadian report to be flawed: the Canadian study was based on "poor quality mammograms that were read by radiologists with no specific training in mammography." Perhaps anticipating that critics would level this allegation, the Canadian researchers included the fact that the mammograms subject to interpretation had "achieved high sensitivity and the expected cancer detection rates." The Canadian researchers claimed that criticism that the "films were unsatisfactory" and "other adverse comments" were "unjustified" [49].
A Harvard Medical School researcher [21] was more reflective, noting that although mammography in the Canadian study found breast cancers when they were smaller and apparently in an earlier stage than did the physical examinations, mammography did not ultimately decrease the breast cancer death rate. That's
...tough for people to understand.... But as we have come to understand that cancer is less an either/or phenomenon than an accumulation of abnormalities, it's a limitation that cancer screening studies (for many types of cancer) are bumping into more and more frequently.
Reactions to the Canadian study also appeared in the news media. The Chicago Tribune quoted the executive director of a breast cancer advocacy organization as saying [51]:
...mammograms have been over-promoted for years.... For 15 years, the message has been mammography is the answer for breast cancer detection for women—especially women over 50.... That's not the case...[Women] shouldn't rely on mammography to save their lives.
However, an article on breast cancer published in Parade magazine in October 2000 reaffirmed in bold print that "women aged 50-69 who have regular mammograms are 30% less likely to die from breast cancer than those who don't" [52].
That the public should trust mammography is constantly being reinforced not only by news reports but also in other ways. Medicare and other health insurers draw attention to mammography on an ongoing basis. Medicare informs recipients that the quality of a medical health plan is measured in two ways: the percentage of plan members who say that they received the best possible care from their health care plan, and the percentage of women between the ages of 52 and 69 who "got an x-ray to check for breast cancer (called a mammogram)" [53]. Other researchers also measure quality of medical care by determining how many women undergo mammography; one study found that health maintenance organization enrollees with breast cancer were diagnosed at earlier stages than were women in a fee-for-service setting because health maintenance organization enrollees are encouraged to obtain mammograms, thus implying that they receive better health care [54]. The message communicated to the public by equating quality of health care with the number of women who undergo screening mammography reinforces the notion that screening mammography is essential if breast cancer is to be conquered.
The fractious debate among experts as to whether screening mammography is efficacious in reducing breast cancer mortality rates has received extensive attention in medical journals and the press, but it may not have permeated the consciousness of the public. A survey of American women about how they interpret the mammography screening debate disclosed that 95% of the women responding said that they had paid "some attention" to the recent discussion regarding mammography screening; however, only 24% of respondents said that the discussion had improved their "understanding" of mammography [55]. Eighty-three percent of the women responding believed that mammography had proven benefits, but nearly half the women responding believed that the debate was more about money than about the question of benefits.
Frame [56] recently observed:
Screening for any cancer...is beneficial only if earlier detection of the disease leads to effective treatments that decrease mortality from the disease or provide longer survival and improved quality of life. Improved survival is only a benefit if it is not iatrogenic pseudosurvival, that is, because of overdiagnosis, lead-time, or length biases.
The debate as to whether screening mammography saves lives and lengthens survival rages on and will certainly not be resolved in the foreseeable future [21].
This article is not intended to be a comprehensive review of all available data on the subject of mammographic efficacy. Even if it were, no definitive answer to the question of whether mammography does indeed reduce mortality from breast cancer would be found. It seems intuitive and logical to believe that studies showing reduction in mortality rates from breast cancer in women who have undergone screening mammography do indeed have merit. However, quantifying a decrease in mortality rates caused specifically by mammography is extremely difficult. Although, as already mentioned, some data show a decrease in mortality rates from breast cancer of as much as 19% in the United States between 1987 and 1997 [44], other studies show decreases in mortality rates from breast cancer of 11.7% between 1980 and 1997 [57], 8% from 1950 to 1996 [47], 1.7% a year during the past decade [58], and 30% overall [24, 25]. Thus, limited agreement exists about actual percentages of decreases among the various sources that report breast cancer death rate statistics; even less agreement exists as to what has caused these decreases.
Let us return to the question asked at the beginning of this perspective: Will there be a greater or lesser likelihood in the coming months and years that a jury will rule that a defendant radiologist who is accused of missing a breast cancer on a mammogram, thereby delaying the diagnosis in a patient, is liable for malpractice? The public's perceptions regarding the incidence of and mortality rate from breast cancer and the accuracy and efficacy of mammography are inextricably linked to how jurors render decisions in malpractice cases that deal with delays in diagnosis. An English radiologist has suggested that many women falsely believe that screening prevents cancer rather than detects in earlier, that cancers arising after a screening examination with normal findings must have been missed, and that delays in diagnosis have adverse prognostic significance [59]. If this is at all true, the malpractice climate surrounding the missed mammographic diagnosis of breast cancer is not apt to improve until the controversies regarding dot size, lead time, fallibility, and impact on survival are clarified.
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TopIntroductionTrends in Breast Cancer...The "One-in-Eight" StatisticBreast Cancer and Mortality...Accuracy of Mammography: the...Efficacy of Mammography in...References |
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hle L.
Hälsokontroller med mammografi minskar inte
dödlighet i
bröstcancer.
Läkartidningen
1999;96:904
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