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Increases in Ductal Carcinoma In Situ (DCIS) of the Breast in Relation to Mammography: A Dilemma

Increases in Ductal Carcinoma In Situ (DCIS) of the Breast in Relation to Mammography: A Dilemma Abstract The increased use of screening mammography has resulted in a marked increase in detected cases of ductal carcinoma in situ (DCIS) of the breast since the early 1980s. In 1993, there were an estimated 23,275 newly diagnosed cases of DCIS in the United States, of which 4,676 were in women aged 40-49. DCIS accounted for 14.7% of all newly diagnosed breast cancers in women aged 40-49 in 1993, and perhaps 40% of all mammographically detected breast cancers in this age group are DCIS. Among women aged 40-49, an estimated 1,890 mastectomies and 2,707 lumpectomies (with or without radiation) were performed for DCIS in 1993. There is an urgent need to better understand the relationship of mammographically detected DCIS to invasive and potentially life-threatening breast cancer. Better information about the appropriate treatment of DCIS is also needed to reduce the confusion and uncertainty many women and their physicians currently experience in the face of a DCIS diagnosis. For the present, women considering screening mammography should be told the likelihood of being diagnosed with DCIS and that only some DCIS cases may be clinically significant but almost all will be treated surgically. The widespread adoption of screening mammography has led to a marked increase in detected cases of ductal carcinoma in situ (DCIS) of the breast (1). DCIS is usually referred to as “preinvasive” or “noninvasive” cancer because it is confined to the milk ducts of the breast and has not spread to the surrounding breast tissue. Although DCIS lesions are usually not clinically palpable, they are visible on mammograms. Before the advent of mammography, they were often only detected incidental to a biopsy for a palpable lesion that was diagnosed as benign. Extrapolating data from the National Cancer Institute's Surveillance, Epidemiology, and End Results (SEER) program (2), we estimate that there were 23,275 newly diagnosed cases of DCIS in the United States in 1993, of which 4,676 were in women aged 40-49. The increase in detected DCIS cases among women aged 40-49 is beneficial if those cases would have progressed to a life-threatening stage in the absence of screening at age 40-49. It is much less desirable if those cases rarely progress to invasive breast cancer (resulting in unnecessary treatment and anxiety) or if waiting until age 50 to be screened and to detect those cancers has no or only a minimal effect on the chance of breast cancer death. In short, we face the question of whether detecting DCIS through screening mammography, especially at ages 40-49, does more harm than good. Based on follow-up of small numbers of untreated cases and of larger series of cases treated only by wide excision or lumpectomy, it appears that only a minority of DCIS cases will progress to or recur as invasive cancer (29). However, current knowledge of factors associated with recurrence is limited and, in the absence of good prognostic markers, treatment for DCIS is not radically different than that for Stage I invasive breast cancer. Thus, while screening mammography may benefit some women age 40-49 through early detection of potentially fatal breast cancers, it is potentially harming other women through detection of DCIS lesions that may be clinically insignificant but, for lack of better prognostic information, are almost always treated surgically. There is a critical need for better understanding of the epidemiologic, clinical, histopathologic, and genetic characteristics that distinguish those cases of DCIS that will go on to progress or recur from those that will not. The fact that most abnormal mammography results are false positives has been discussed elsewhere (3,4; see also papers by Anderson, Lee, Sickles, Kerlikowske, Linver, Rimer, and Harris in this monograph). The focus here is on detection of what is technically a true positive (DCIS) but which, in some cases at least, may be clinically insignificant. For each woman who is contemplating screening, the willingness to risk a false positive or a positive result that may be clinically insignificant will differ, and it is therefore important that women know the probabilities of such outcomes in order to make their own informed decisions. Trends in DCIS Incidence Rates According to SEER data, between 1983 and 1993, age-adjusted incidence rates for DCIS in the United States increased 314%. (For comparison, the increase in incidence rates for invasive breast cancer over the same period was 15.7% percent.) Increases in DCIS incidence rates in the United States were dramatic for women 40 and older but much more modest for women under 40 (Fig. 11), who are much less likely to undergo screening mammography. In particular, among women 40-49 years of age, incidence rates increased 339% between 1983 and 1993 (compared to 10.8% for invasive breast cancer). For all age groups combined, DCIS accounted for 2.8% of newly diagnosed breast cancers in the United States in 1973, 3.8% in 1983, and 12.5% in 1993. Among women ages 40-49, DCIS accounted for 3.7% of all breast cancers in 1973, 4.2% in 1983, and 14.7% in 1993 (2). Relation of the DCIS Epidemic to Mammography Screening There were 134 mammography machines in the United States in 1982 and an estimated 10,000 by 1990 (5). Meanwhile, use of mammography increased markedly; the proportion of U.S. women reporting recent mammography doubled between 1987 and 1992 (6). Most but not all of the increase in invasive breast cancer incidence during the 1980s has been attributed to increased detection through screening (7), and probably most of the excess of DCIS cases today compared to earlier years can be too. Mammography screening programs, which focus on asymptomatic women, typically report much higher proportions of DCIS among all breast cancers detected than is observed in data from general tumor registries, which include cases in symptomatic women as well. For example, of breast cancers detected among women aged 40 and older undergoing first screening mammography at the Mobile Mammography Screening Program of the University of California, San Francisco (UCSF) during 1985-1996 who had no report of a palpable mass, 29.9% were DCIS. Among breast cancer cases detected among women aged 40-49 having their first mammograms in that program, 42.6% were DCIS, with substantial but lower proportions being DCIS in the older age groups (Table 11). The higher proportion of DCIS among younger compared to older women with mammographically detected breast cancers is sometimes misinterpreted to mean that DCIS is more common in younger women and that screening is therefore particularly important for younger women. However, population-based cancer incidence data for the United States show that DCIS incidence rates do not decrease with age (except at the very oldest ages, when screening is less frequent), while rates for invasive breast cancer increase dramatically with age (2). Thus, DCIS comprises a higher proportion of mammographically detected cases in younger women not because they have more DCIS than older women, but because they have much less invasive breast cancer. Even in mammography screening programs, the number of DCIS cases detected per 10,000 first screening mammograms does not appear to be lower among women 50 and older than among women 40-49, as shown in Table 11 for the UCSF screening program. In sum, a larger proportion of the breast cancers detected among younger women are DCIS, which makes the issue of possible overdiagnosis of DCIS through screening especially important for this age group, but DCIS is not more common in women aged 40-49 than in older women. Is DCIS a Precursor of Invasive Breast Cancer? Is DCIS a precursor of invasive breast cancer and, if so, what proportion of DCIS progresses to invasive disease? To have actual proof that DCIS is a precursor of invasive breast cancer, we would have to diagnose but not treat a group of women with DCIS and follow them over time to determine whether invasive breast cancer occurs. Short of that, based on the more circumstantial evidence that we do have, it is probably safe to say that some fraction of DCIS progresses to clinically detectable invasive cancer, but DCIS is not an obligate precursor lesion. Several lines of evidence support a precursor role. For example, the few epidemiologic studies that have examined risk factors for DCIS show similarities with invasive breast cancer, including a family history of breast cancer and nulliparity or older age at first childbirth (8,9,10,11). Although the role of menopausal hormone use in invasive breast cancer remains somewhat controversial, several (11,12,13) but not all (14) studies have shown it to be a risk factor for DCIS. Secondly, many laboratory studies have compared genetic markers in DCIS and invasive breast tumors and found similarities, much more commonly with high-grade or comedo DCIS than low-grade or non-comedo DCIS (15,16,17), although whether these markers actually predict DCIS progression to invasive disease is unclear. Finally, the distribution of DCIS lesions in the breast is almost identical to the distribution of invasive breast cancers (18). On the other hand, there is evidence to suggest that perhaps the majority of DCIS cases do not progress to clinically significant invasive breast cancer and therefore might not be considered precursor lesions. For example, the prevalence of DCIS in seven autopsy series of women who died of causes unrelated to breast cancer ranges from as low as 0.2% to as high as 18.2%, with four of the studies finding a prevalence of greater than 10% (19,20,21,22,23,24,25). There are also several series of women who had breast biopsies 30 to 40 years ago that were interpreted at the time to be benign breast disease and who were therefore untreated beyond biopsy. When their pathology slides were re-reviewed some years later, it was determined that the women actually had had DCIS, and they were then followed to determine what proportion subsequently developed invasive breast cancer. Although these studies are often cited in support of a precursor role for DCIS, even they suggest that following biopsy alone, the majority of DCIS does not progress to invasive breast cancer. Perhaps the two most informative series are those of Page et al. and of Eusebi et al., as other studies generally had smaller numbers or large losses to follow-up. Page et al. identified 28 women who were biopsied between 1952 and 1968 in Nashville, Tennessee, and who had an average of 30 years of follow-up, during which time nine women (32%) developed ipsilateral invasive breast cancer (26,27). Eusebi et al., identified 80 patients who were biopsied between 1964 and 1976 in northern Italy, with an average of 17.5 years of follow-up; nine of these women (11.3%) developed ipsilateral invasive breast cancer (28). Even these are small clinical series; also, it is difficult to know the extent to which we can extrapolate from the experience of these historic cases of DCIS, which occurred in women with breast symptoms, to the experience of women diagnosed with DCIS today, most of which is occult disease detected mammographically. There are also a number of series of women treated by wide excision alone who have been followed for breast cancer recurrence (either as DCIS or invasive disease). Most of these studies show that about 4% to 5% of such cases recur as invasive cancer after 3 to 10 years of follow-up (29). The best known randomized trial of DCIS treatment (lumpectomy versus lumpectomy plus radiation) reported a 10.5% five-year cumulative incidence of ipsilateral invasive cancer in women treated by lumpectomy alone (30). The lower recurrence rates in the earlier case series may reflect greater selection for smaller tumors in those studies compared to randomized trials. It is generally thought that patients with specific histologic types of DCIS, namely those with high nuclear grade or comedo-type DCIS, are at greatest risk of recurrence, although whether this holds up after long-term follow-up or whether nuclear grade or comedo-type DCIS affects actual survival per se is unclear (31). The Eastern Cooperative Oncology Group (ECOG) has proposed a large observational study of minimal treatment (local excision) for DCIS of small size and low nuclear grade, which would provide useful information on recurrence for women with what is currently considered to be low-risk DCIS. We do know that the vast majority of women with DCIS do quite well in terms of subsequent breast cancer mortality. Among women in the population-based SEER cancer database who were diagnosed with DCIS between 1978 and 1993, 0.5% died of breast cancer within five years and 2.6% within 10 years (32). Whether these low proportions reflect the effectiveness of treatment (almost all cases were treated surgically) or the fact that DCIS is a relatively benign disease to begin with—or both—is unclear. One caveat is that the experience of women classified in the SEER database as having DCIS may overestimate the likelihood of breast cancer death associated with DCIS, since reexamination of original pathology reports for those women suggests that up to 15% of cases coded as DCIS in SEER actually had early invasive cancer (Ann Coleman, Ph.D., personal communication). Moreover, the women with the longest follow-up are those diagnosed in the era preceding the widespread adoption of screening mammography, and it may be inappropriate to extrapolate from their experience to that of women diagnosed more recently by mammography. Although we still know relatively little about the natural history of DCIS, it is probably fair to conclude that some DCIS cases will progress to clinically significant invasive breast cancer but many will not. DCIS Treatment Trends: Mastectomy versus Lumpectomy Most all DCIS is treated surgically, either by mastectomy or by lumpectomy with or without radiation; according to SEER data for 1993, only 1.7% of DCIS cases did not have surgery. As shown in Table 22 for women of all ages combined, the proportion of DCIS cases treated by mastectomy has declined substantially over time, from 71% in 1983 to 39.7% in 1993; among women aged 40-49 years, the decline over that time period was from 75.8% to 40.4%. The proportion of DCIS cases treated by breast conserving therapy has increased over time; among women aged 40-49 in 1993, 32.9% of cases were treated by lumpectomy plus radiation and 25% by lumpectomy alone (2). Extrapolating from SEER incidence rates and treatment patterns to the general U.S. population, an estimated 9,245 mastectomies were performed for DCIS in the United States in 1993, of which 1,890 were in women 40-49; an additional 2,707 women aged 40-49 are estimated to have had lumpectomy with or without radiation in 1993. Over the period 1983-1993, an estimated 89,845 breasts were removed for DCIS in U.S. women, including 17,456 among women aged 40-49, and presumably most of those cases were mammographically detected. Although over half of DCIS cases in the United States were treated by mastectomy until 1991, it is of interest that there are no randomized clinical trials of mastectomy versus other treatment options for DCIS, nor are there ever likely to be, given that lumpectomy plus radiation already has been shown to be equal in effectiveness to mastectomy for treatment of early-stage invasive breast cancer. The largest randomized clinical trial of DCIS treatment published to date is the National Surgical Adjuvant Breast Project study (NSABP-B-17); it randomized approximately 800 women with DCIS to receive either lumpectomy alone or lumpectomy plus radiation. Results published in 1993, based on a mean follow-up of 43 months, showed statistically significantly lower rates of breast cancer recurrence in the group that received lumpectomy plus radiation (30). Recently presented data based on eight years of follow-up continue to confirm the difference: invasive breast cancer had occurred in 13.4% of the women treated by wide excision alone compared to 3.9% of those treated by lumpectomy plus radiation (Norman Wolmark, M.D., “The NSABP Experience in DCIS,” 19th Annual San Antonio Breast Cancer Symposium, San Antonio, Texas, Dec. 11, 1996). However, although numbers of deaths were small (only about 20 deaths from all causes combined in each group), survival per se did not differ between the two groups. Other randomized clinical trials of DCIS treatment by lumpectomy with or without radiation or tamoxifen are underway (33). Current Dilemmas Posed by Detection of DCIS Our increased ability to detect DCIS through mammography and the resultant “epidemic” of reported DCIS cases present women and their physicians with a dilemma: probably only a minority of DCIS cases will actually go on to invasive breast cancer and become clinically important. However, since current medical knowledge does not permit us to identify which women with DCIS will progress to invasive cancer and which will not, at present most women with a DCIS diagnosis are treated surgically. The hope is that by detecting malignant changes as early as possible, we are saving lives. The concern is that we may be detecting changes which for many women would never become life threatening or even clinically apparent and that, in the process, we are overtreating women. Thus, it behooves us to learn whether there is a survival benefit associated with early detection and treatment of DCIS and, if so, whether it obtains only for specific subtypes of DCIS. We need to know the appropriate clinical strategies for different subtypes of DCIS. These strategies could range from biopsy followed by watchful waiting, on the one hand, to mastectomy on the other. The situation is similar to the current dilemma posed by prostate specific antigen (PSA) screening for prostate cancer; while debate continues as to whether that test reduces risk of prostate cancer death, it is known that PSA screening picks up many occult cancers that are clinically unimportant but for which thousands of men have had their prostates removed, in some cases resulting in impotence and incontinence (34). On the basis of breast cancer incidence rates and actual treatment patterns in the SEER data (2), we have estimated the numbers of surgeries for breast cancer among U.S. women aged 40-49 in 1983 and 1993 by stage of disease, assuming that the total number of women in the population was the same in both years (i.e., we used the 1993 population data). The total number of breast surgeries for breast cancer among women 40-49 increased from 24,343 to 30,535 between 1983 and 1993 (Table 33). Among women 40-49, there were increases in breast surgeries of 333% for DCIS and 32% for localized invasive cancer, and decreases of 8% for regional disease and 4% for distant disease. Because the proportion of cases treated by mastectomy declined over time for all stages of breast cancer, there were fewer mastectomies performed overall in 1993 than in 1983; however, as we have seen earlier, this was not true for DCIS because the dramatic increase in DCIS incidence rates resulted in an increase in the number of DCIS-related mastectomies, despite the declining proportion of DCIS cases being treated by mastectomy over time. Thus, we have a fairly good idea of the likelihood of a DCIS diagnosis for women undergoing mammography screening and of the likelihood of various types of breast surgery. What we still don't know is whether detection of breast cancer at the DCIS stage ultimately saves lives. Directions for Future Research It is agreed that most of the increase in reported cases of DCIS results from better detection of the disease through mammography rather than a true excess of new cases. Especially given the numbers of women diagnosed with DCIS in recent years, there is urgent need to better understand the relationship of mammographically detected DCIS to invasive and potentially life-threatening breast cancer. DCIS shares at least some risk factors and genetic changes in common with invasive breast cancer, which suggests etiologic similarities and supports the position that at least some DCIS cases are precursors to invasive disease. Other evidence suggests that many cases of DCIS are not clinically significant; in most autopsy series examined, occult DCIS is not uncommon in women who died of causes other than breast cancer, and small historical series of women with DCIS who received no treatment beyond diagnostic biopsy show that most did not subsequently develop clinically apparent invasive breast cancer. Thus, biologic and epidemiologic studies are needed to identify prognostic markers and risk factors associated with progression; these studies should focus on specific histologic types of DCIS and perhaps correlate them with breast imaging studies. Better information about the appropriate treatment of DCIS is also needed to reduce the confusion and uncertainty many women and their physicians currently experience in the face of a DCIS diagnosis. For the present, informed decision making about screening mammography should include the likelihood of being diagnosed with DCIS, with an explanation that only some DCIS cases may be clinically significant, as well as the likelihood of having breast surgery as a result of DCIS detection. Table 1. Percent of breast cancer that is DCIS among cancers detected during first screening mammography, and cases of DCIS and invasive cancer detected per 10,000 first screenings*, by age, UCSF Mobile Mammography Screening Program, 1985-1996** Age   Total cancers   % DCIS   Cases per 10,000 screens   DCIS   Invasive cancer   30-39  11  90.9%  11  1  40-49  47  42.6%  14  19  50-59  56  28.6%  20  51  60-69  58  19.0%  22  94  70+  39  28.2%  42  106  Age   Total cancers   % DCIS   Cases per 10,000 screens   DCIS   Invasive cancer   30-39  11  90.9%  11  1  40-49  47  42.6%  14  19  50-59  56  28.6%  20  51  60-69  58  19.0%  22  94  70+  39  28.2%  42  106  * Women who present for screening with no report of a palpable mass. ** Based on the authors' analysis of the database of E. A. Sickles, M.D., Department of Radiology, University of California, San Francisco. View Large Table 2. Estimated numbers of DCIS cases, percent treated by mastectomy, and estimated numbers of mastectomies for DCIS in all U.S. women and in women aged 40-49, 1983-1993 Year   Estimated number of DCIS cases   % Cases treated by mastectomy   Estimated number of mastectomies   All women   Ages 40-49   All women   Ages 40-49   All women   Ages 40-49   1983  4,901  742  71.0  75.8  3,479  563  1984  7,069  1,433  66.6  67.7  4,706  971  1985  9,897  1,991  59.5  57.5  5,887  1,144  1986  12,279  2,283  56.1  57.0  6,890  1,300  1987  16,034  3,000  59.3  62.8  9,515  1,884  1988  17,196  3,345  57.8  56.3  9,934  1,882  1989  16,584  3,086  56.3  53.0  9,334  1,635  1990  19,890  3,970  53.7  51.0  10,682  2,025  1991  20,735  4,325  47.8  44.2  9,908  1,912  1992  23,438  4,973  43.8  45.3  10,265  2,250  1993  23,275  4,676  39.7  40.4  9,245  1,890    Total  171,298  33,824      89,845  17,456  Year   Estimated number of DCIS cases   % Cases treated by mastectomy   Estimated number of mastectomies   All women   Ages 40-49   All women   Ages 40-49   All women   Ages 40-49   1983  4,901  742  71.0  75.8  3,479  563  1984  7,069  1,433  66.6  67.7  4,706  971  1985  9,897  1,991  59.5  57.5  5,887  1,144  1986  12,279  2,283  56.1  57.0  6,890  1,300  1987  16,034  3,000  59.3  62.8  9,515  1,884  1988  17,196  3,345  57.8  56.3  9,934  1,882  1989  16,584  3,086  56.3  53.0  9,334  1,635  1990  19,890  3,970  53.7  51.0  10,682  2,025  1991  20,735  4,325  47.8  44.2  9,908  1,912  1992  23,438  4,973  43.8  45.3  10,265  2,250  1993  23,275  4,676  39.7  40.4  9,245  1,890    Total  171,298  33,824      89,845  17,456  * Based on extrapolations from NCI's SEER program data on cancer incidence rates and treatment patterns (2). View Large Table 3. Estimated numbers* of breast surgeries for DCIS and other stages of breast cancer among white and black U.S. women aged 40-49, 1983 and 1993** Stage and type of surgery   1983   1993   Estimated number   Percent of all cases   Estimated number   Percent of all cases   DCIS   Breast conserving  258  24  2,704  58   Mastectomy  804  76  1,890  40    Total  1,062  100  4,594  98  Localized   Breast conserving  2,442  20  8,622  55   Mastectomy  9,373  78  6,996  44    Total  11,815  98  15,618  99  Regional   Breast conserving  1,289  13  2,980  32   Mastectomy  8,690  85  6,238  67    Total  9,979  98  9,218  99  Distant   Breast conserving  167  13  222  18   Mastectomy  698  56  609  40    Total  865  69  831  67  All stages combined   Breast conserving  4,338  17  14,619  46   Mastectomy  20,005  78  15,916  50    Total  24,343  95  30,535  96  Stage and type of surgery   1983   1993   Estimated number   Percent of all cases   Estimated number   Percent of all cases   DCIS   Breast conserving  258  24  2,704  58   Mastectomy  804  76  1,890  40    Total  1,062  100  4,594  98  Localized   Breast conserving  2,442  20  8,622  55   Mastectomy  9,373  78  6,996  44    Total  11,815  98  15,618  99  Regional   Breast conserving  1,289  13  2,980  32   Mastectomy  8,690  85  6,238  67    Total  9,979  98  9,218  99  Distant   Breast conserving  167  13  222  18   Mastectomy  698  56  609  40    Total  865  69  831  67  All stages combined   Breast conserving  4,338  17  14,619  46   Mastectomy  20,005  78  15,916  50    Total  24,343  95  30,535  96  * Based on extrapolations from NCI's SEER program data on cancer incidence rates and treatment patterns (2). ** Assumes the same number of women in the population in both years, namely the population distribution of U.S. women in 1993. Estimates based on rates for in situ cancer not including cases of lobular carcinoma in situ. Estimated numbers within each stage category do not include cases with no surgery or those with breast cancer-related surgery outside of the breast. However, the percentages shown reflect the proportions of all cases in each stage category (including those with no surgery or those with breast cancer-related surgery outside of the breast) that were treated by breast-conserving surgery or mastectomy, and those proportions usually do not add up to 100% of all cases in the category. The “All stages combined” category includes breast cancers of unknown stage. If cases with no surgery and those with breast cancer-related surgery outside of the breast had been included, numbers would be slightly higher (e.g., totals would be 25,511 and 31,618 for 1983 and 1993, respectively). View Large Fig. 1. View largeDownload slide Trends in DCIS incidence rates among U.S. women, by age, 1973-1993. 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An examination of the evidence. N Engl J Med  1995; 333: 1401-5. Google Scholar Oxford University Press http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png JNCI Monographs Oxford University Press

Increases in Ductal Carcinoma In Situ (DCIS) of the Breast in Relation to Mammography: A Dilemma

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

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Oxford University Press
Copyright
Oxford University Press
ISSN
1052-6773
eISSN
1745-6614
DOI
10.1093/jncimono/1997.22.151
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Abstract

Abstract The increased use of screening mammography has resulted in a marked increase in detected cases of ductal carcinoma in situ (DCIS) of the breast since the early 1980s. In 1993, there were an estimated 23,275 newly diagnosed cases of DCIS in the United States, of which 4,676 were in women aged 40-49. DCIS accounted for 14.7% of all newly diagnosed breast cancers in women aged 40-49 in 1993, and perhaps 40% of all mammographically detected breast cancers in this age group are DCIS. Among women aged 40-49, an estimated 1,890 mastectomies and 2,707 lumpectomies (with or without radiation) were performed for DCIS in 1993. There is an urgent need to better understand the relationship of mammographically detected DCIS to invasive and potentially life-threatening breast cancer. Better information about the appropriate treatment of DCIS is also needed to reduce the confusion and uncertainty many women and their physicians currently experience in the face of a DCIS diagnosis. For the present, women considering screening mammography should be told the likelihood of being diagnosed with DCIS and that only some DCIS cases may be clinically significant but almost all will be treated surgically. The widespread adoption of screening mammography has led to a marked increase in detected cases of ductal carcinoma in situ (DCIS) of the breast (1). DCIS is usually referred to as “preinvasive” or “noninvasive” cancer because it is confined to the milk ducts of the breast and has not spread to the surrounding breast tissue. Although DCIS lesions are usually not clinically palpable, they are visible on mammograms. Before the advent of mammography, they were often only detected incidental to a biopsy for a palpable lesion that was diagnosed as benign. Extrapolating data from the National Cancer Institute's Surveillance, Epidemiology, and End Results (SEER) program (2), we estimate that there were 23,275 newly diagnosed cases of DCIS in the United States in 1993, of which 4,676 were in women aged 40-49. The increase in detected DCIS cases among women aged 40-49 is beneficial if those cases would have progressed to a life-threatening stage in the absence of screening at age 40-49. It is much less desirable if those cases rarely progress to invasive breast cancer (resulting in unnecessary treatment and anxiety) or if waiting until age 50 to be screened and to detect those cancers has no or only a minimal effect on the chance of breast cancer death. In short, we face the question of whether detecting DCIS through screening mammography, especially at ages 40-49, does more harm than good. Based on follow-up of small numbers of untreated cases and of larger series of cases treated only by wide excision or lumpectomy, it appears that only a minority of DCIS cases will progress to or recur as invasive cancer (29). However, current knowledge of factors associated with recurrence is limited and, in the absence of good prognostic markers, treatment for DCIS is not radically different than that for Stage I invasive breast cancer. Thus, while screening mammography may benefit some women age 40-49 through early detection of potentially fatal breast cancers, it is potentially harming other women through detection of DCIS lesions that may be clinically insignificant but, for lack of better prognostic information, are almost always treated surgically. There is a critical need for better understanding of the epidemiologic, clinical, histopathologic, and genetic characteristics that distinguish those cases of DCIS that will go on to progress or recur from those that will not. The fact that most abnormal mammography results are false positives has been discussed elsewhere (3,4; see also papers by Anderson, Lee, Sickles, Kerlikowske, Linver, Rimer, and Harris in this monograph). The focus here is on detection of what is technically a true positive (DCIS) but which, in some cases at least, may be clinically insignificant. For each woman who is contemplating screening, the willingness to risk a false positive or a positive result that may be clinically insignificant will differ, and it is therefore important that women know the probabilities of such outcomes in order to make their own informed decisions. Trends in DCIS Incidence Rates According to SEER data, between 1983 and 1993, age-adjusted incidence rates for DCIS in the United States increased 314%. (For comparison, the increase in incidence rates for invasive breast cancer over the same period was 15.7% percent.) Increases in DCIS incidence rates in the United States were dramatic for women 40 and older but much more modest for women under 40 (Fig. 11), who are much less likely to undergo screening mammography. In particular, among women 40-49 years of age, incidence rates increased 339% between 1983 and 1993 (compared to 10.8% for invasive breast cancer). For all age groups combined, DCIS accounted for 2.8% of newly diagnosed breast cancers in the United States in 1973, 3.8% in 1983, and 12.5% in 1993. Among women ages 40-49, DCIS accounted for 3.7% of all breast cancers in 1973, 4.2% in 1983, and 14.7% in 1993 (2). Relation of the DCIS Epidemic to Mammography Screening There were 134 mammography machines in the United States in 1982 and an estimated 10,000 by 1990 (5). Meanwhile, use of mammography increased markedly; the proportion of U.S. women reporting recent mammography doubled between 1987 and 1992 (6). Most but not all of the increase in invasive breast cancer incidence during the 1980s has been attributed to increased detection through screening (7), and probably most of the excess of DCIS cases today compared to earlier years can be too. Mammography screening programs, which focus on asymptomatic women, typically report much higher proportions of DCIS among all breast cancers detected than is observed in data from general tumor registries, which include cases in symptomatic women as well. For example, of breast cancers detected among women aged 40 and older undergoing first screening mammography at the Mobile Mammography Screening Program of the University of California, San Francisco (UCSF) during 1985-1996 who had no report of a palpable mass, 29.9% were DCIS. Among breast cancer cases detected among women aged 40-49 having their first mammograms in that program, 42.6% were DCIS, with substantial but lower proportions being DCIS in the older age groups (Table 11). The higher proportion of DCIS among younger compared to older women with mammographically detected breast cancers is sometimes misinterpreted to mean that DCIS is more common in younger women and that screening is therefore particularly important for younger women. However, population-based cancer incidence data for the United States show that DCIS incidence rates do not decrease with age (except at the very oldest ages, when screening is less frequent), while rates for invasive breast cancer increase dramatically with age (2). Thus, DCIS comprises a higher proportion of mammographically detected cases in younger women not because they have more DCIS than older women, but because they have much less invasive breast cancer. Even in mammography screening programs, the number of DCIS cases detected per 10,000 first screening mammograms does not appear to be lower among women 50 and older than among women 40-49, as shown in Table 11 for the UCSF screening program. In sum, a larger proportion of the breast cancers detected among younger women are DCIS, which makes the issue of possible overdiagnosis of DCIS through screening especially important for this age group, but DCIS is not more common in women aged 40-49 than in older women. Is DCIS a Precursor of Invasive Breast Cancer? Is DCIS a precursor of invasive breast cancer and, if so, what proportion of DCIS progresses to invasive disease? To have actual proof that DCIS is a precursor of invasive breast cancer, we would have to diagnose but not treat a group of women with DCIS and follow them over time to determine whether invasive breast cancer occurs. Short of that, based on the more circumstantial evidence that we do have, it is probably safe to say that some fraction of DCIS progresses to clinically detectable invasive cancer, but DCIS is not an obligate precursor lesion. Several lines of evidence support a precursor role. For example, the few epidemiologic studies that have examined risk factors for DCIS show similarities with invasive breast cancer, including a family history of breast cancer and nulliparity or older age at first childbirth (8,9,10,11). Although the role of menopausal hormone use in invasive breast cancer remains somewhat controversial, several (11,12,13) but not all (14) studies have shown it to be a risk factor for DCIS. Secondly, many laboratory studies have compared genetic markers in DCIS and invasive breast tumors and found similarities, much more commonly with high-grade or comedo DCIS than low-grade or non-comedo DCIS (15,16,17), although whether these markers actually predict DCIS progression to invasive disease is unclear. Finally, the distribution of DCIS lesions in the breast is almost identical to the distribution of invasive breast cancers (18). On the other hand, there is evidence to suggest that perhaps the majority of DCIS cases do not progress to clinically significant invasive breast cancer and therefore might not be considered precursor lesions. For example, the prevalence of DCIS in seven autopsy series of women who died of causes unrelated to breast cancer ranges from as low as 0.2% to as high as 18.2%, with four of the studies finding a prevalence of greater than 10% (19,20,21,22,23,24,25). There are also several series of women who had breast biopsies 30 to 40 years ago that were interpreted at the time to be benign breast disease and who were therefore untreated beyond biopsy. When their pathology slides were re-reviewed some years later, it was determined that the women actually had had DCIS, and they were then followed to determine what proportion subsequently developed invasive breast cancer. Although these studies are often cited in support of a precursor role for DCIS, even they suggest that following biopsy alone, the majority of DCIS does not progress to invasive breast cancer. Perhaps the two most informative series are those of Page et al. and of Eusebi et al., as other studies generally had smaller numbers or large losses to follow-up. Page et al. identified 28 women who were biopsied between 1952 and 1968 in Nashville, Tennessee, and who had an average of 30 years of follow-up, during which time nine women (32%) developed ipsilateral invasive breast cancer (26,27). Eusebi et al., identified 80 patients who were biopsied between 1964 and 1976 in northern Italy, with an average of 17.5 years of follow-up; nine of these women (11.3%) developed ipsilateral invasive breast cancer (28). Even these are small clinical series; also, it is difficult to know the extent to which we can extrapolate from the experience of these historic cases of DCIS, which occurred in women with breast symptoms, to the experience of women diagnosed with DCIS today, most of which is occult disease detected mammographically. There are also a number of series of women treated by wide excision alone who have been followed for breast cancer recurrence (either as DCIS or invasive disease). Most of these studies show that about 4% to 5% of such cases recur as invasive cancer after 3 to 10 years of follow-up (29). The best known randomized trial of DCIS treatment (lumpectomy versus lumpectomy plus radiation) reported a 10.5% five-year cumulative incidence of ipsilateral invasive cancer in women treated by lumpectomy alone (30). The lower recurrence rates in the earlier case series may reflect greater selection for smaller tumors in those studies compared to randomized trials. It is generally thought that patients with specific histologic types of DCIS, namely those with high nuclear grade or comedo-type DCIS, are at greatest risk of recurrence, although whether this holds up after long-term follow-up or whether nuclear grade or comedo-type DCIS affects actual survival per se is unclear (31). The Eastern Cooperative Oncology Group (ECOG) has proposed a large observational study of minimal treatment (local excision) for DCIS of small size and low nuclear grade, which would provide useful information on recurrence for women with what is currently considered to be low-risk DCIS. We do know that the vast majority of women with DCIS do quite well in terms of subsequent breast cancer mortality. Among women in the population-based SEER cancer database who were diagnosed with DCIS between 1978 and 1993, 0.5% died of breast cancer within five years and 2.6% within 10 years (32). Whether these low proportions reflect the effectiveness of treatment (almost all cases were treated surgically) or the fact that DCIS is a relatively benign disease to begin with—or both—is unclear. One caveat is that the experience of women classified in the SEER database as having DCIS may overestimate the likelihood of breast cancer death associated with DCIS, since reexamination of original pathology reports for those women suggests that up to 15% of cases coded as DCIS in SEER actually had early invasive cancer (Ann Coleman, Ph.D., personal communication). Moreover, the women with the longest follow-up are those diagnosed in the era preceding the widespread adoption of screening mammography, and it may be inappropriate to extrapolate from their experience to that of women diagnosed more recently by mammography. Although we still know relatively little about the natural history of DCIS, it is probably fair to conclude that some DCIS cases will progress to clinically significant invasive breast cancer but many will not. DCIS Treatment Trends: Mastectomy versus Lumpectomy Most all DCIS is treated surgically, either by mastectomy or by lumpectomy with or without radiation; according to SEER data for 1993, only 1.7% of DCIS cases did not have surgery. As shown in Table 22 for women of all ages combined, the proportion of DCIS cases treated by mastectomy has declined substantially over time, from 71% in 1983 to 39.7% in 1993; among women aged 40-49 years, the decline over that time period was from 75.8% to 40.4%. The proportion of DCIS cases treated by breast conserving therapy has increased over time; among women aged 40-49 in 1993, 32.9% of cases were treated by lumpectomy plus radiation and 25% by lumpectomy alone (2). Extrapolating from SEER incidence rates and treatment patterns to the general U.S. population, an estimated 9,245 mastectomies were performed for DCIS in the United States in 1993, of which 1,890 were in women 40-49; an additional 2,707 women aged 40-49 are estimated to have had lumpectomy with or without radiation in 1993. Over the period 1983-1993, an estimated 89,845 breasts were removed for DCIS in U.S. women, including 17,456 among women aged 40-49, and presumably most of those cases were mammographically detected. Although over half of DCIS cases in the United States were treated by mastectomy until 1991, it is of interest that there are no randomized clinical trials of mastectomy versus other treatment options for DCIS, nor are there ever likely to be, given that lumpectomy plus radiation already has been shown to be equal in effectiveness to mastectomy for treatment of early-stage invasive breast cancer. The largest randomized clinical trial of DCIS treatment published to date is the National Surgical Adjuvant Breast Project study (NSABP-B-17); it randomized approximately 800 women with DCIS to receive either lumpectomy alone or lumpectomy plus radiation. Results published in 1993, based on a mean follow-up of 43 months, showed statistically significantly lower rates of breast cancer recurrence in the group that received lumpectomy plus radiation (30). Recently presented data based on eight years of follow-up continue to confirm the difference: invasive breast cancer had occurred in 13.4% of the women treated by wide excision alone compared to 3.9% of those treated by lumpectomy plus radiation (Norman Wolmark, M.D., “The NSABP Experience in DCIS,” 19th Annual San Antonio Breast Cancer Symposium, San Antonio, Texas, Dec. 11, 1996). However, although numbers of deaths were small (only about 20 deaths from all causes combined in each group), survival per se did not differ between the two groups. Other randomized clinical trials of DCIS treatment by lumpectomy with or without radiation or tamoxifen are underway (33). Current Dilemmas Posed by Detection of DCIS Our increased ability to detect DCIS through mammography and the resultant “epidemic” of reported DCIS cases present women and their physicians with a dilemma: probably only a minority of DCIS cases will actually go on to invasive breast cancer and become clinically important. However, since current medical knowledge does not permit us to identify which women with DCIS will progress to invasive cancer and which will not, at present most women with a DCIS diagnosis are treated surgically. The hope is that by detecting malignant changes as early as possible, we are saving lives. The concern is that we may be detecting changes which for many women would never become life threatening or even clinically apparent and that, in the process, we are overtreating women. Thus, it behooves us to learn whether there is a survival benefit associated with early detection and treatment of DCIS and, if so, whether it obtains only for specific subtypes of DCIS. We need to know the appropriate clinical strategies for different subtypes of DCIS. These strategies could range from biopsy followed by watchful waiting, on the one hand, to mastectomy on the other. The situation is similar to the current dilemma posed by prostate specific antigen (PSA) screening for prostate cancer; while debate continues as to whether that test reduces risk of prostate cancer death, it is known that PSA screening picks up many occult cancers that are clinically unimportant but for which thousands of men have had their prostates removed, in some cases resulting in impotence and incontinence (34). On the basis of breast cancer incidence rates and actual treatment patterns in the SEER data (2), we have estimated the numbers of surgeries for breast cancer among U.S. women aged 40-49 in 1983 and 1993 by stage of disease, assuming that the total number of women in the population was the same in both years (i.e., we used the 1993 population data). The total number of breast surgeries for breast cancer among women 40-49 increased from 24,343 to 30,535 between 1983 and 1993 (Table 33). Among women 40-49, there were increases in breast surgeries of 333% for DCIS and 32% for localized invasive cancer, and decreases of 8% for regional disease and 4% for distant disease. Because the proportion of cases treated by mastectomy declined over time for all stages of breast cancer, there were fewer mastectomies performed overall in 1993 than in 1983; however, as we have seen earlier, this was not true for DCIS because the dramatic increase in DCIS incidence rates resulted in an increase in the number of DCIS-related mastectomies, despite the declining proportion of DCIS cases being treated by mastectomy over time. Thus, we have a fairly good idea of the likelihood of a DCIS diagnosis for women undergoing mammography screening and of the likelihood of various types of breast surgery. What we still don't know is whether detection of breast cancer at the DCIS stage ultimately saves lives. Directions for Future Research It is agreed that most of the increase in reported cases of DCIS results from better detection of the disease through mammography rather than a true excess of new cases. Especially given the numbers of women diagnosed with DCIS in recent years, there is urgent need to better understand the relationship of mammographically detected DCIS to invasive and potentially life-threatening breast cancer. DCIS shares at least some risk factors and genetic changes in common with invasive breast cancer, which suggests etiologic similarities and supports the position that at least some DCIS cases are precursors to invasive disease. Other evidence suggests that many cases of DCIS are not clinically significant; in most autopsy series examined, occult DCIS is not uncommon in women who died of causes other than breast cancer, and small historical series of women with DCIS who received no treatment beyond diagnostic biopsy show that most did not subsequently develop clinically apparent invasive breast cancer. Thus, biologic and epidemiologic studies are needed to identify prognostic markers and risk factors associated with progression; these studies should focus on specific histologic types of DCIS and perhaps correlate them with breast imaging studies. Better information about the appropriate treatment of DCIS is also needed to reduce the confusion and uncertainty many women and their physicians currently experience in the face of a DCIS diagnosis. For the present, informed decision making about screening mammography should include the likelihood of being diagnosed with DCIS, with an explanation that only some DCIS cases may be clinically significant, as well as the likelihood of having breast surgery as a result of DCIS detection. Table 1. Percent of breast cancer that is DCIS among cancers detected during first screening mammography, and cases of DCIS and invasive cancer detected per 10,000 first screenings*, by age, UCSF Mobile Mammography Screening Program, 1985-1996** Age   Total cancers   % DCIS   Cases per 10,000 screens   DCIS   Invasive cancer   30-39  11  90.9%  11  1  40-49  47  42.6%  14  19  50-59  56  28.6%  20  51  60-69  58  19.0%  22  94  70+  39  28.2%  42  106  Age   Total cancers   % DCIS   Cases per 10,000 screens   DCIS   Invasive cancer   30-39  11  90.9%  11  1  40-49  47  42.6%  14  19  50-59  56  28.6%  20  51  60-69  58  19.0%  22  94  70+  39  28.2%  42  106  * Women who present for screening with no report of a palpable mass. ** Based on the authors' analysis of the database of E. A. Sickles, M.D., Department of Radiology, University of California, San Francisco. View Large Table 2. Estimated numbers of DCIS cases, percent treated by mastectomy, and estimated numbers of mastectomies for DCIS in all U.S. women and in women aged 40-49, 1983-1993 Year   Estimated number of DCIS cases   % Cases treated by mastectomy   Estimated number of mastectomies   All women   Ages 40-49   All women   Ages 40-49   All women   Ages 40-49   1983  4,901  742  71.0  75.8  3,479  563  1984  7,069  1,433  66.6  67.7  4,706  971  1985  9,897  1,991  59.5  57.5  5,887  1,144  1986  12,279  2,283  56.1  57.0  6,890  1,300  1987  16,034  3,000  59.3  62.8  9,515  1,884  1988  17,196  3,345  57.8  56.3  9,934  1,882  1989  16,584  3,086  56.3  53.0  9,334  1,635  1990  19,890  3,970  53.7  51.0  10,682  2,025  1991  20,735  4,325  47.8  44.2  9,908  1,912  1992  23,438  4,973  43.8  45.3  10,265  2,250  1993  23,275  4,676  39.7  40.4  9,245  1,890    Total  171,298  33,824      89,845  17,456  Year   Estimated number of DCIS cases   % Cases treated by mastectomy   Estimated number of mastectomies   All women   Ages 40-49   All women   Ages 40-49   All women   Ages 40-49   1983  4,901  742  71.0  75.8  3,479  563  1984  7,069  1,433  66.6  67.7  4,706  971  1985  9,897  1,991  59.5  57.5  5,887  1,144  1986  12,279  2,283  56.1  57.0  6,890  1,300  1987  16,034  3,000  59.3  62.8  9,515  1,884  1988  17,196  3,345  57.8  56.3  9,934  1,882  1989  16,584  3,086  56.3  53.0  9,334  1,635  1990  19,890  3,970  53.7  51.0  10,682  2,025  1991  20,735  4,325  47.8  44.2  9,908  1,912  1992  23,438  4,973  43.8  45.3  10,265  2,250  1993  23,275  4,676  39.7  40.4  9,245  1,890    Total  171,298  33,824      89,845  17,456  * Based on extrapolations from NCI's SEER program data on cancer incidence rates and treatment patterns (2). View Large Table 3. Estimated numbers* of breast surgeries for DCIS and other stages of breast cancer among white and black U.S. women aged 40-49, 1983 and 1993** Stage and type of surgery   1983   1993   Estimated number   Percent of all cases   Estimated number   Percent of all cases   DCIS   Breast conserving  258  24  2,704  58   Mastectomy  804  76  1,890  40    Total  1,062  100  4,594  98  Localized   Breast conserving  2,442  20  8,622  55   Mastectomy  9,373  78  6,996  44    Total  11,815  98  15,618  99  Regional   Breast conserving  1,289  13  2,980  32   Mastectomy  8,690  85  6,238  67    Total  9,979  98  9,218  99  Distant   Breast conserving  167  13  222  18   Mastectomy  698  56  609  40    Total  865  69  831  67  All stages combined   Breast conserving  4,338  17  14,619  46   Mastectomy  20,005  78  15,916  50    Total  24,343  95  30,535  96  Stage and type of surgery   1983   1993   Estimated number   Percent of all cases   Estimated number   Percent of all cases   DCIS   Breast conserving  258  24  2,704  58   Mastectomy  804  76  1,890  40    Total  1,062  100  4,594  98  Localized   Breast conserving  2,442  20  8,622  55   Mastectomy  9,373  78  6,996  44    Total  11,815  98  15,618  99  Regional   Breast conserving  1,289  13  2,980  32   Mastectomy  8,690  85  6,238  67    Total  9,979  98  9,218  99  Distant   Breast conserving  167  13  222  18   Mastectomy  698  56  609  40    Total  865  69  831  67  All stages combined   Breast conserving  4,338  17  14,619  46   Mastectomy  20,005  78  15,916  50    Total  24,343  95  30,535  96  * Based on extrapolations from NCI's SEER program data on cancer incidence rates and treatment patterns (2). ** Assumes the same number of women in the population in both years, namely the population distribution of U.S. women in 1993. Estimates based on rates for in situ cancer not including cases of lobular carcinoma in situ. Estimated numbers within each stage category do not include cases with no surgery or those with breast cancer-related surgery outside of the breast. However, the percentages shown reflect the proportions of all cases in each stage category (including those with no surgery or those with breast cancer-related surgery outside of the breast) that were treated by breast-conserving surgery or mastectomy, and those proportions usually do not add up to 100% of all cases in the category. The “All stages combined” category includes breast cancers of unknown stage. If cases with no surgery and those with breast cancer-related surgery outside of the breast had been included, numbers would be slightly higher (e.g., totals would be 25,511 and 31,618 for 1983 and 1993, respectively). View Large Fig. 1. View largeDownload slide Trends in DCIS incidence rates among U.S. women, by age, 1973-1993. 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