ARTICLE

Trends in the Treatment of Ductal Carcinoma In Situ of the Breast

Nancy N. Baxter, Beth A. Virnig, Sara B. Durham, Todd M. Tuttle

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)


    ABSTRACT
 Top
 Notes
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
 References
 
Background: An increase in incidence of ductal carcinoma in situ (DCIS) of the breast has been documented, and concerns regarding overly aggressive treatment have been raised. This study was designed to evaluate the use of surgery and radiation therapy in treating DCIS. Methods: We used the National Cancer Institute’s Surveillance, Epidemiology, and End Results database to assess treatment of patients with DCIS with no evidence of microinvasion who were diagnosed from January 1, 1992, through December 31, 1999. We assessed the rates of mastectomy, breast reconstruction, radiation therapy after lumpectomy, and axillary dissection. Associations were analyzed by logistic regression. Results: During the study period, 25 206 patients met selection criteria. The incidence of DCIS dramatically increased with time; however, the incidence of comedo lesions did not change. The rate of mastectomy decreased from 43% in 1992 to 28% in 1999, after controlling for age, race, tumor size, comedo histology, and geographic location. However, because of the increase in the diagnosis of DCIS, the age-adjusted incidence of mastectomy for DCIS in the population did not change (7.8 per 100 000 women in 1992 and 1999). Almost half the patients undergoing lumpectomy did not undergo radiation therapy (55% in 1992 and 46% in 1999); in those with comedo histology, 33% did not undergo radiation therapy after lumpectomy, even in 1999. Overall, patients were less likely to have axillary dissection over time (34% in 1992 versus 15% in 1999), yet the rate of axillary dissection was still high (30%) in patients undergoing mastectomy in 1999. Large, statistically and clinically significant variation by geographic location was found in treatment. Conclusions: Treatment of DCIS changed in a clinically significant fashion between 1992 and 1999. Throughout this study, many patients were found to undergo aggressive surgical therapy, including mastectomy and axillary dissection, whereas others appeared to be undertreated, e.g., not receiving radiation therapy after lumpectomy, even in the presence of adverse histologic features. Variation in demographic and geographic factors indicates that at least some of these treatment differences reflect individual and institutional practice patterns that may be modifiable.



    INTRODUCTION
 Top
 Notes
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
 References
 
The incidence of ductal carcinoma in situ (DCIS) of the breast has risen dramatically in the United States. Before 1980, DCIS was rarely diagnosed (1), but currently more than 14% of breast cancers diagnosed in the United States are DCIS (2). About one in every 1300 screening mammographic examinations will lead to the diagnosis of DCIS (3).

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.


    PATIENTS AND METHODS
 Top
 Notes
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
 References
 
Data

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 Cochran–Armitage 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.


    RESULTS
 Top
 Notes
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
 References
 
From January 1, 1992, through December 31, 1999, a total of 25 206 patients meeting our study’s selection criteria were diagnosed with DCIS. The incidence of DCIS had a statistically significant 73% increase during this period with 2403 cases diagnosed in 1992 versus 4166 in 1999 (P<.001; Fig. 1). The incidence of DCIS with comedo histology did not change; thus, the proportion of cases of DCIS with comedo histology actually decreased during this period. Tumor grade was not reliably reported and therefore could not be evaluated. Less than 50% of lesions had a reported grade. We found no differences during this period in the age or race distribution of patients. Interestingly, median tumor size increased statistically significantly from 0.5 cm in 1992 to 1.0 cm in 1999 (P<.001). Of note, tumor size was not reported in one-third of the cases; the proportion of patients with reported tumor size did not change during this period. Because tumor size was missing for such a high number of patients, multivariable analyses were conducted with and without tumor size as a covariate. The relationships between other variables (age, race, comedo histology, and geographic location) and treatment did not differ between models, with or without tumor size as a covariate.



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Fig. 1. Age-adjusted incidence of ductal carcinoma in situ (DCIS) per 100 000 women over time, adjusted to age distribution of women 18 years old or older in the 2000 U.S. Census, excluding those with any prior cancers. Solid circles = those with DCIS with comedo histology; solid triangles = those with DCIS.

 
The overall rates of breast-conserving therapy, of radiation therapy after lumpectomy, of breast reconstruction after mastectomy, and of axillary dissection are presented in Table 1. Younger patients and those with comedo histology tended to undergo more aggressive care (mastectomy, radiation therapy, and axillary dissection). Statistically significant time trends were found in surgical therapy for DCIS. Overall, 97.5% of patients underwent a surgical procedure. The proportion of patients undergoing mastectomy declined markedly during this period from 43% in 1992 to 28% in 1999 (P<.001) (Fig. 2). Year of diagnosis remained an important predictor of mastectomy by use of logistic regression, after controlling for age, race, tumor size, comedo histology, and geographic location of the registry. Although 1763 more cases of DCIS were diagnosed in 1999 than in 1992, only 138 additional mastectomies were performed in 1999. From 1992 through 1999, the use of breast-conserving therapy was associated with older age (odds ratio [OR] = 1.6, 95% confidence interval [CI] = 1.3 to 1.8; Table 2). Younger patients, those with comedo histology, and those with tumors larger than 1 cm were statistically significantly more likely to undergo mastectomy (P<.001). We tested the model for statistically significant interactions. A statistically significant trend toward the increased use of breast-conserving therapy during the study period was found for tumors smaller than or equal to 1 cm and for tumors larger than 1 cm; however, the trend was stronger for tumors smaller than 1 cm (Ptrend<.001). Although the rate of mastectomy declined over the time period studied for women diagnosed with DCIS, because of the increase in diagnosis of DCIS, the actual incidence of mastectomy for DCIS in the population did not change. The incidence of mastectomy for DCIS per 100 000 women in the population (adjusted to the age distribution of women 18 years old or older in the 2000 U.S. Census) was 7.8 in 1992 and 7.8 in 1999.


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Table 1. Rates of breast-conserving therapy (BCT), radiation therapy after BCT, reconstruction after mastectomy, and axillary dissection for women with ductal carcinoma in situ from 1992 through 1999

 


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Fig. 2. Use of breast-conserving therapy over time for women with ductal carcinoma in situ. Open bars = no surgery; hatched bars = lumpectomy without radiation therapy; shaded bars = lumpectomy with radiation therapy; solid bars = mastectomy.

 

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Table 2. Association between receiving breast-conserving therapy (BCT) and receiving radiation therapy (multivariable model) for patients with ductal carcinoma in situ from 1992 through 1999*

 
Radiation therapy status was identified for 98.5% of the patients who underwent lumpectomy. In 1992, 45% of the patients who underwent lumpectomy received radiation therapy versus 54% in 1999 (Ptrend<.001). Multivariable modeling demonstrated that radiation therapy was more likely to be given to patients with larger tumors and to those with comedo histology than to those without such characteristics (Table 2); however, in 1999, 33% of those with comedo histology did not undergo radiation therapy after lumpectomy. African American patients were statistically significantly less likely to undergo radiation therapy (48%) after lumpectomy than non–African American patients (53%), after we controlled for age, comedo histology, tumor size, year of diagnosis, and geographic location (P = .02).

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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Fig. 3. Use of axillary dissection over time for patients with ductal carcinoma in situ. Solid circles = with mastectomy; solid squares = with breast-conserving therapy.

 
The proportion of patients who underwent breast reconstruction after mastectomy statistically significantly increased during the study period from 16% in 1992 to 32% in 1999 (P<.001). Breast reconstruction was statistically significantly more likely among younger patients than among older patients (P<.001), but it was less likely among African American patients than among non–African American patients (P = .03). SEER coding for breast reconstruction changed during the study period; however, the trend in favor of breast reconstruction was clearly present before the coding change.

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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Table 3. Treatment by geographic location of registry for patients with ductal carcinoma in situ from 1992 through 1999*

 

    DISCUSSION
 Top
 Notes
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
 References
 
The incidence of DCIS dramatically increased from January 1, 1992, through December 31, 1999. The potential for preventing invasive breast cancer is important, yet the risk of overtreatment is a clinically significant concern, particularly because the incidence of patients with DCIS with comedo histology did not change during our 8-year study period. The declining proportion of patients with comedo histology has not been previously reported. That finding is of interest, but its cause and importance are unclear. It may reflect an increasing sensitivity of mammography in the detection of DCIS with non–comedo histology over time, or it may echo changes in pathologic criteria for DCIS. In addition, there may be a trend toward reporting tumor grade rather than comedo status. Because the SEER registry has not reliably reported tumor grade in the past, we are unable to evaluate differences in tumor grade in our study. The proportion of DCIS patients with comedo histology reported over time needs to be evaluated in other population-based datasets, particularly in those with more detailed and consistent information regarding tumor grade. Similarly, the increase in tumor size found in this study period should not be overinterpreted. Tumor size is difficult to measure in DCIS, and data on the margin status are not available in SEER. For this reason, all analyses were conducted with and without tumor size as a covariate. Results of the analyses for other variables did not change.

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 factors—such as the underlying practice patterns of individual surgeons or institutions—likely 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 non–tumor-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.


    NOTES
 Top
 Notes
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
 References
 
1Editor’s note: SEER is a set of geographically defined, population-based, central cancer registries in the United States, operated by local nonprofit organizations under contract to the National Cancer Institute (NCI). Registry data are submitted electronically without personal identifiers to the NCI on a biannual basis, and the NCI makes the data available to the public for scientific research.

Supported in part by the University of Minnesota Cancer Center.

We thank Dr. Mary Knatterud for her helpful editorial comments.


    REFERENCES
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 Notes
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
 References
 

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Manuscript received August 13, 2003; revised January 7, 2004; accepted February 12, 2004.


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