Affiliation of authors: Division of Surgical Oncology and School of Public Health, University of Minnesota, Minneapolis
Correspondence to: Nancy Baxter, MD, PhD, MMC 450, Department of Surgery, University of Minnesota, 420 Delaware St. SE, Minneapolis, MN 55455 (e-mail: baxte025{at}umn.edu)
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ABSTRACT |
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INTRODUCTION |
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The biologic behavior of DCIS detected by mammography is unclear. Few patients with DCIS ultimately die of breast cancer; in a population-based study (2), only 1.9% of patients with DCIS had died of breast cancer within 10 years of their diagnosis. Despite the relatively benign nature of DCIS, patients commonly have undergone aggressive care, similar to that recommended for invasive breast cancer (4). The risks of overdiagnosis and overtreatment have been recognized (2,5). Nonetheless, some cases of DCIS have a less benign course than other cases; some histologic features, particularly the presence of comedo histology, are associated with more aggressive behavior (6).
Variations in the treatment of patients with DCIS have been previously described (710). A more standard approach to treatment has been recommended (1117). In an evaluation of the incidence and treatment of DCIS using Surveillance, Epidemiology, and End Results (SEER)1 cancer registry data from 1973 through 1992, Ernster et al. (7) found that the proportion of patients with DCIS who were treated with mastectomy decreased from 71% in 1983 to 44% in 1992. They also noted that 44% of the patients in 1992 who underwent lumpectomy received radiation therapy. Winchester et al. (9,10) evaluated the treatment of DCIS by use of the National Cancer Database (managed by the American College of Surgeons) between 1985 and 1993, and they also found a statistically significant increase in the use of breast-conserving therapy. They noted that the rate of radiation therapy after lumpectomy increased from 38% to 54% over the study period.
Given the increased use of breast-conserving therapy in patients with invasive breast cancer (18,19), along with better knowledge of the effectiveness of breast-conserving therapy in patients with DCIS (2022), a more current evaluation of patterns of care is needed. Evaluation of trends in other aspects of care may also provide important insights. For example, in the past, up to half of the patients with DCIS reportedly underwent axillary lymph node dissection (10), a potentially morbid procedure with questionable long-term benefit and a limited role in routine treatment of this disease (10,2325). We set out to evaluate the management of DCIS from 1992 through 1999. Specifically, we looked at factors that influenced management, including race, age, tumor size, comedo histology, and geographic location.
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PATIENTS AND METHODS |
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We obtained data from the SEER cancer registry, a population-based registry for collecting information on cancer incidence and survival data from 11 population-based cancer registries and from three supplemental registries (covering about 14% of the U.S. population) (26). Three of those registries were added to SEER in January 1992; therefore, data from those sites were available only after that date. SEER reports data by registry and, thus, our study period includes data from the corresponding 11 distinct geographic sites. Collected data included patient characteristics, primary tumor site, morphologic features, stage at diagnosis, first course of treatment, and follow-up for vital status. First course of treatment extends to the completion of the treatment plan, if one exists. If no such plan is known, first course of treatment is then coded for treatments received within the first year after diagnosis or until there is evidence of disease progression or treatment failure, if this occurs within 1 year. If a patient has multiple cancer-directed therapies, the most invasive is recorded. For example, if a patient underwent a complete mastectomy after a lumpectomy with positive margins, the patient would be coded as having a mastectomy for the first course of surgical therapy (26).
Patients
Patients included in our study were aged 18 years or older and were diagnosed with any histologic type of in situ carcinoma of the breast (other than lobular carcinoma in situ alone) from January 1, 1992, through December 31, 1999; the diagnosis was confirmed microscopically. Patients who had a previous malignant diagnosis in the SEER registry were excluded. Patients with any evidence of microinvasive disease would be considered by SEER to have invasive breast cancer and thus were excluded from the study (26).
Statistical Analysis
We calculated annual age-adjusted incidence standardized to the 2000 U.S. population. For each of the 8 years, we calculated the rates of mastectomy, axillary dissection, breast reconstruction, and radiation therapy as a proportion of the total number of DCIS cases. The SEER registry routinely collects data on the number of lymph nodes examined, so we used those data to determine the rate of axillary dissection. For patients undergoing mastectomy, those with five or more lymph nodes examined were considered to have had an axillary dissection. (We selected the number five to avoid considering lymph nodes that were inadvertently harvested in the axillary tail of a simple mastectomy specimen as indicative of an axillary dissection.) For patients undergoing lumpectomy, those with any lymph nodes examined were considered to have undergone an axillary dissection. We calculated the rate of breast reconstruction as a proportion of the total number of mastectomies performed. Likewise, we calculated the rate of radiation therapy use as a proportion of the total number of lumpectomies performed. Using the CochranArmitage trend test on one degree of freedom, we determined whether rates had changed over time in a fashion similar to that used in other recent publications (27,28). Using logistic regression, we evaluated any association of the use of mastectomy, radiation therapy, reconstruction, or axillary dissection with tumor size [SEER records the pathologic size of the tumor when a resected specimen is available (26)], comedo histology, race, age, year of diagnosis, and geographic location by registry. All statistical tests were two-sided.
Because our study used preexisting data with no personal identifiers, the Human Subjects Committee of the University of Minnesota Institutional Review Board determined that it was exempt from review.
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RESULTS |
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The use of axillary dissection declined statistically significantly over the study period from 34% in 1992 to 15% in 1999 (P<.001). Among patients who underwent axillary dissection, a median number of 11 lymph nodes were examined. Axillary dissection was more common in those with comedo histology, but even in such patients, the rate decreased with time from 40% in 1992 to 20% in 1999. There was a strong negative association between breast-conserving therapy and axillary dissection. Axillary dissection was much more likely among patients who underwent mastectomy (42% of patients overall) than among patients who had breast-conserving therapy (8.5% of patients overall) (P<.001) (Fig. 3). In 1999 the rate of axillary dissection was still high (30%) in those undergoing mastectomy.
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Geographic location of treatment as recorded by registry was a statistically significant predictor of the use of breast-conserving therapy, radiation therapy after breast-conserving therapy, and axillary dissection (Table 3). Large, statistically and clinically significant differences were found between geographic locations in univariate and multivariable analyses (all P<.001). Among registries, the overall rate of breast-conserving therapy ranged from 55% to 74%, the rate of radiation therapy after lumpectomy ranged from 39% to 74%, and the rate of axillary dissection after mastectomy ranged from 34% to 54%.
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DISCUSSION |
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From 1992 through 1999, treatment of DCIS changed in a clinically significant manner. Overall changes included a decrease in mastectomy rates and, for patients who underwent mastectomy, an increase in breast reconstruction. However, a larger number of patients actually underwent mastectomy for treatment of DCIS in 1999 than in 1992 because of the dramatic increase in the incidence of DCIS. The overall rate of mastectomy for the 8-year study period was 34%, indicating that a large number of patients underwent aggressive treatment for DCIS. In many such cases, mastectomy may have been medically appropriate or based on patient preference. However, the changing incidence of mastectomy over time and the variation in treatment by location seem to indicate that other modifiable factorssuch as the underlying practice patterns of individual surgeons or institutionslikely played an important role.
The overall rate of axillary dissection in patients who underwent mastectomy was surprisingly high (42%), particularly because current treatment guidelines for DCIS now recommend against routine axillary dissection (12,16,17,29) and because the procedure was not routinely recommended during the study period (23). The very low risk of lymph nodal metastasis in DCIS does not justify the morbidity of axillary dissection. Even sentinel node biopsy, a clinically significantly less morbid procedure, is highly controversial in DCIS and generally not recommended (3032). In our study, the median number of lymph nodes (11 lymph nodes) retrieved in patients who underwent axillary dissection was high enough to indicate that these cases represented true axillary dissection and not inadvertent axillary lymph node removal with simple mastectomy. Our findings of an association between axillary dissection and mastectomy may, in part, reflect the more aggressive nature of tumors treated in this fashion (i.e., of larger comedo tumors), so such an approach may have been medically justified at times. However, given the marked reduction that we found in the rate of axillary dissection over the short period of our study and the statistically significant variation found by geographic location, axillary dissection may very likely have reflected nontumor-related factors, such as underlying practice patterns of individual surgeons or institutions.
According to our study, many patients apparently underwent aggressive surgical treatment for DCIS. Yet other patients appear to have been undertreated, with no radiation therapy after lumpectomy for almost half of them, even in many patients with adverse risk factors. For example, of the patients whose tumors have comedo histology, more than one-third did not undergo radiation therapy after lumpectomy. Since at least 1993, radiation therapy after lumpectomy has been recommended for most patients with DCIS; the preponderance of evidence indicates a statistically significant reduction in ipsilateral in situ and invasive breast cancer recurrence with lumpectomy and radiation therapy versus radiation therapy alone (20,22,33,34), particularly for patients whose tumors had comedo histology (35,36). Overall, the current rate of radiation therapy after lumpectomy does not appear to have substantially increased, compared with that in previous studies in the 1990s (7,10), despite the publication of a major randomized trial in 1993 (20) that demonstrated a benefit of radiation therapy for such patients. Granted, some patients with a favorable prognosis might not benefit from radiation therapy; this possibility may explain its omission in some cases (37). However, in our study, we saw a statistically significant variation in the rate of radiation therapy by race, age, and geographic location. Thus, selection of patients for breast-conserving therapy without radiation therapy cannot be explained solely on the basis of unmeasured tumor characteristics.
Our study has several limitations. First, it used population-based data with only limited information on patient and tumor characteristics and with no information on any use of hormonal therapy. In addition, there was no information on mode of detection, the presence of multifocal disease, or margin status. Such variables, of course, may affect treatment decisions. However, the statistically significant changes in DCIS treatment that our study uncovered were largely independent of patient and tumor characteristics. These variations in patterns of care for this disease likely reflected individual provider practice patterns, particularly given differences seen between registries. We believe that heightened awareness and establishment of standard treatment recommendations could improve DCIS treatment. Continued study of treatment trends and factors influencing treatment are needed. With additional years of follow-up of patients with DCIS, it will be possible to examine the impact of treatment changes on longer-term outcomes, such as the development of invasive breast cancer and mortality.
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NOTES |
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Supported in part by the University of Minnesota Cancer Center.
We thank Dr. Mary Knatterud for her helpful editorial comments.
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Manuscript received August 13, 2003; revised January 7, 2004; accepted February 12, 2004.
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