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© 2001 American Society for Clinical Oncology Factors Predicting the Use of Breast-Conserving Therapy in Stage I and II Breast CarcinomaFrom the American College of Surgeons Commission on Cancer, Chicago, IL; and American College of Radiology, Philadelphia, PA. Address reprint requests to Monica Morrow, MD, Department of Surgery, Northwestern Memorial Hospital, 251 East Huron St, Galter 13-174, Chicago, IL 60611.
PURPOSE: To define patterns of care for the local therapy of stage I and II breast cancer and to identify factors used to select patients for breast-conserving therapy (BCT). PATIENTS AND METHODS: A convenience sample of 16,643 patients with stage I and II breast cancer treated in 1994 was obtained from hospital-based tumor registries. Histologic variables were determined from original pathology reports. RESULTS: BCT was performed in 42.6% of patients. Multivariate analysis demonstrated that living in the Northeast United States (odds ratio [OR], 2.48; 95% confidence interval [CI], 2.16 to 2.84), having a clinical T1 tumor (OR, 2.51; 95% CI, 2.27 to 2.78), and having a tumor without an extensive intraductal component (OR, 2.07; 95% CI, 1.81 to 2.37) were the strongest predictors of breast-conserving surgery. Radiation therapy was given to 86% of patients who had breast-conserving surgery. Age less than 70 years was the most significant predictor of receiving radiation (OR, 2.11; 95% CI, 1.77 to 2.25). Tumor variables did not correlate with the use of radiation, but favorable tumor characteristics were associated with the use of breast-conserving surgery. CONCLUSION: Despite strong evidence supporting the use of BCT, the majority of women continue to be treated with mastectomy. Predictors of the use of BCT do not correspond to those suggested in guidelines.
IN ITS 1999 REPORT "Ensuring Quality Cancer Care," the National Cancer Policy Board recommended the use of systematically developed guidelines for cancer treatment based on the best available evidence and that studies of factors influencing patterns of care be conducted to improve our knowledge about the quality of cancer care.1 A large body of evidence supports the appropriateness of breast-conserving therapy (BCT), consisting of tumor excision, axillary dissection, and breast irradiation, in the management of stage I and II breast carcinoma. Six prospective randomized trials have demonstrated that survival after BCT is equal to survival after mastectomy.2-7 These results were widely disseminated in a 1990 National Institutes of Health consensus panel which concluded that "breast conservation treatment is an appropriate method of primary therapy for the majority of women with stage I and II breast cancer."8 In 1992, a multidisciplinary group, which included representatives from the American College of Surgeons (ACOS), American College of Radiology (ACR), the College of American Pathologists, and the Society of Surgical Oncology, developed and disseminated guidelines for patient selection for BCT.9 These guidelines listed only four absolute contraindications to BCT, including the following: (1) first or second trimester of pregnancy, (2) a history of prior therapeutic irradiation to the breast region, (3) multiple primary tumors in separate quadrants of the breast, and (4) extensive indeterminate or malignant-appearing calcifications throughout the breast. Since that time, a variety of population-based studies have reported that fewer than 50% of patients with stage I and II breast cancer undergo BCT,10-12 and factors such as age, geographic location, and payer status have been observed to influence the use of BCT. In recent years, the more widespread implementation of screening mammography programs and a greater public awareness of breast cancer have resulted in a larger proportion of breast cancers being detected at a localized stage. In the National Cancer Data Base’s 1994 report on breast carcinoma, 75% of newly diagnosed breast cancers were stage I or II,13 making the pool of potential candidates for BCT quite large. The objectives of this joint study of the ACOS Commission on Cancer and the ACR were to define current patterns of care for the local therapy of stage I and II breast cancer and to identify factors used to select patients for BCT and determine their relationship to the 1992 guidelines for BCT.
Data Collection An invitation to participate in the study was sent to 2,000 hospitals in the United States, including 1,400 with cancer programs accredited by the ACOS Commission on Cancer. Each tumor registrar was asked to submit the first 25 consecutive cases of stage I or II breast cancer treated in 1994. Patients were eligible if they received their breast cancer diagnosis and initial course of treatment at the participating institution. A representative of the institution’s radiation oncology department completed the radiation oncology worksheet portion of the questionnaire. A total of 842 hospitals submitted data. Ninety-three percent had cancer programs approved by the Commission of Cancer of the ACOS. Characteristics of the responding hospitals and the total group of hospitals invited to participate were very similar. Of the invited hospitals, 41% had community cancer programs, 33% had community comprehensive programs, 24% were National Cancer Institute (NCI) cancer centers or teaching programs, and 2% belonged to other categories. Corresponding figures for the responding hospitals were 43% community hospitals, 36% comprehensive community, 16% teaching or NCI, and 5% unknown. There was also a similar geographic distribution for those invited and those responding. Twenty-six percent of invited hospitals and 30% of respondents were from the Midwest. Figures for the Northeast were 22% and 21%, for the South Atlantic 17% and 16%, for the South 15% and 14%, for the Mountain region 4% and 4%, and for the Pacific region 15% and 14%. Detailed definitions for geographic regions and hospital types are provided below. Study Subjects and Definition of Variables Data were submitted for 17,931 breast cancer patients diagnosed in 1994. A total of 16,643 patients with pathologic stage I-II breast cancer were analyzed for this report. All disease stages and the classification of tumor size and nodal status are according to the fifth edition of the American Joint Committee on Cancer staging manual.14 A total of 1,288 patients were excluded from the analysis for the following reasons: for 984 patients, staging was not performed or was incomplete; 266 had pathologic T3 tumors and would not be considered standard candidates for breast-conserving surgery (BCS); and 38 had surgery other than BCS or mastectomy. The definition of BCS included any surgery coded as partial mastectomy with or without axillary lymph node dissection. Mastectomy by our definition included mastectomy with or without axillary lymph node dissection, radical mastectomy, extended radical mastectomy, or subcutaneous mastectomy with or without axillary lymph node dissection. Race was categorized as white, black, Hispanic, and other. The other group included Asian, Pacific Islander, and American Indian/Eskimo. For the multivariate and univariate analysis, black and Hispanic races were combined into one group, black + Hispanic. Insurance carriers were categorized as private insurance, health maintenance organization (HMO), preferred provider organization (PPO), federally funded, or state-funded programs. The federally funded programs included Medicare + supplement, VA Comprehensive Health Care Administration Medical Plan United States, and military and Indian health services. State-funded insurance included Medicaid, welfare, and a small number of uninsured patients. For the univariate and multivariate analyses, the insurance carriers were broken into two large groups: private, which included HMO, PPO, and private insurance; and government, which included the federally and state-funded programs. For the purpose of this study, the following regional definitions were used: Northeast: Maine, Vermont, New Hampshire, Massachusetts, Rhode Island, Connecticut, New York, Pennsylvania, and New Jersey; South Atlantic: Delaware, District of Columbia, Maryland, West Virginia, Virginia, North Carolina, South Carolina, Georgia, and Florida; Midwest: Wisconsin, Michigan, Illinois, Indiana, Ohio, Minnesota, North Dakota, South Dakota, Iowa, Nebraska, Kansas, and Missouri; South: Kentucky, Tennessee, Mississippi, Alabama, Oklahoma, Arkansas, Texas, and Louisiana; Mountain: Montana, Idaho, Wyoming, Nevada, Utah, Colorado, Arizona, and New Mexico; and Pacific: Washington, Oregon, California, Alaska, and Hawaii. Hospitals also were grouped according to the type of cancer programs as defined by the Commission on Cancer of the ACOS. The groups included community hospitals with a comprehensive cancer program, which provides a full range of diagnostic and treatment services on site or by referral. A community hospital cancer program also has a full range of diagnostic and treatment services but generally has to refer a portion of cancer treatment to another institution. A hospital-associated cancer program has a limited range of diagnostic and cancer treatment services available on site and refers for such services, and cancer conferences are held monthly. An integrated cancer program hospital offers one treatment modality and forms partnerships with another hospital facility to provide other services. Teaching hospital cancer programs are based in institutions with at least four full residency programs and have a full range of board-certified specialty services in oncology. An NCI-designated comprehensive cancer program has both basic and clinical research along with a full range of diagnostic and treatment services on site, board-certified physicians in the oncology specialties, and residency programs. For purposes of analysis, the teaching hospital cancer programs and NCI-designated comprehensive cancer program are grouped together as a single variable, teaching programs; community hospital cancer programs, hospital-associated cancer programs, and integrated cancer program institutions are grouped as community programs; and comprehensive cancer programs are comprehensive community. The various breast cancer histologies were classified as favorable or unfavorable. Tubular, papillary, apocrine, and mucinous histologies were considered favorable, and the rest were considered unfavorable. All histologic variables were determined from the original pathology report. Central pathology review was not conducted. Statistical Analysis The univariate analysis for the likelihood of BCS versus mastectomy and the subsequent use of radiotherapy (RT) after BCS is reported as odds ratios (ORs) with 95% confidence intervals (CIs). P values less than .05 indicate statistical significance. For the multivariate analysis with logistic regression, the use of BCS and the use of RT were the independent variables, respectively. For each, backwards selection was used to fit the models where variables were removed if not significant at the level of P = .05.
Patient characteristics are listed in Table 1. The mean patient age was 60.8 years, with a median of 62 years. Women younger than age 40 made up 6.2% of the group, whereas those 70 and older accounted for 30.1% of cases. The majority of patients, 70.9%, were postmenopausal. This age distribution was reflected in the insurance status of the patients, with 42.1% having Medicare or other federally funded insurance. A total of 78.6% of the cases were treated in community hospitals, with only 16.3% treated in NCI-designated cancer centers or teaching hospital programs. The Midwest was the most heavily represented geographic region (30.2% of cases), followed by the Northeast (21.4%). The majority of patients were white (85.9%), with blacks accounting for 7.8% of the study population, and Hispanics 2.9%.
Tumor characteristics are listed in Table 2. Favorable histologic tumor types made up 4.2% of cases in the series, with infiltrating ductal, lobular, or infiltrating tumors not otherwise specified comprising 92.6% of the group. A histologic grade was assigned to 78.6% of cases, and 13.3% were well-differentiated. Stage I carcinomas were somewhat more common than stage II tumors, accounting for 57.2% of all cases. BCS was performed in 7,097 patients (42.6%), with the remainder undergoing some form of mastectomy. A series of both patient and tumor factors was examined in both univariate and multivariate analysis to determine whether they influenced the rates of BCT. The results of the univariate analysis for the entire data set of 16,643 patients are listed in Table 3. Patients having BCS had a median age of 59 years compared with 64 years (P < .0001) for those undergoing mastectomy. The use of BCS also varied by geographic region, with the highest rates noted in the Northeast (54%) and Pacific regions (47%), and the lowest rates in the South (32%) and Midwest (37%). Payer status also correlated with the type of surgical procedure. The use of BCS did not differ between privately insured patients and those in HMOs. However, patients with private insurance were 1.6 times more likely to undergo BCS than those with governmental insurance. The use of BCS increased as hospital size increased, being 14% more frequent in community hospitals treating larger numbers of cancer cases compared with their smaller counterparts and 59% more frequent in teaching hospitals and NCI-designated cancer centers. Patients with favorable prognostic characteristics, such as T1 tumors, clinically negative axillary nodes, and low histologic grade tumors, were significantly more likely than those with unfavorable prognostic features to undergo BCS.
A stepwise logistic regression model incorporating the variables examined in the univariate analysis was constructed for the 11,644 patients with complete data. The results are listed in Table 4. Both patient and tumor characteristics remained predictive of the likelihood of undergoing BCS. The strongest predictors of BCS were living in the Northeast region, having a clinical T1 tumor, and having a tumor without an extensive intraductal component. In this model, favorable histologic subtype was not a significant predictive factor. Because a significant number of patients were missing data on tumor grade, the multivariate analyses were rerun with grade excluded as a variable. This allowed the inclusion of 3,009 additional patients in the model (data not shown). Northeast region, clinical T1 tumor, and the absence of an extensive intraductal component remained the strongest predictors of BCS.
Radiation therapy was given to 86% of patients who had BCS. A univariate analysis of factors predicting the use of RT is listed in Table 5. Women over age 70 were significantly less likely than their younger counterparts to receive RT, as were those with government rather than private insurance. A multivariate analysis of factors predicting the use of RT was carried out for the 5,044 patients with complete data ( Table 6). Age remained the most significant predictor of the use of RT, with patients under age 70 more than twice as likely to receive RT as patients age 70 and older. White patients were 45% more likely than patients of other races to receive RT. After adjustment for other variables, type of insurance was no longer a significant predictor of use of RT. No consistent pattern was observed between tumor variables and the use of RT. Patients with T1 tumors received treatment more often than patients with T2 tumors, but patients with unfavorable histology were more likely to be irradiated than those with favorable histology. Nodal status, tumor grade, tumor location, and the presence of an extensive intraductal component (EIC) were not predictors of the use of RT.
This study demonstrates that, in 1994, fewer than one half of the patients with stage I and II breast cancer in this large convenience sample were treated with BCT. The 42.6% rate of breast conservation noted in this study represents an increase in the percentage of cases treated in this fashion compared with earlier reports from the National Cancer Data Base13 and other sources.10-12 In a National Cancer Data Base study including data from 1985, 1988, and 1990 for stage 0 and I cancers, breast conservation rates increased from 25.8% to 29.8% to 38.1%.13 The relatively slow rate of increase in the use of the procedure over time is consistent with the observations from the 1980s15,16 and is somewhat surprising in view of the large body of mature scientific data that supports the efficacy of BCT.2-7 In comparison, the switch from the use of radical mastectomy to modified radical mastectomy, which occurred without the benefit of large-scale prospective randomized trials, was essentially complete within 10 years.17 Potential reasons for high mastectomy rates include large numbers of patients with contraindications to BCT, patient preference for mastectomy, or physician use of inappropriate selection criteria for BCT. The findings of this study support the use of inappropriate selection criteria as a major cause of high mastectomy rates. We observed a decrease in the likelihood of breast preservation for each decade of increase in age, which ranged from 11% to 19% depending on the model used. Increasing patient age has been associated with high mastectomy rates in a number of studies.10,11,15 Because the incidence of complications caused by breast irradiation does not increase with increasing age,18 and lumpectomy and axillary dissection is not a higher-morbidity operative procedure than mastectomy, medical contraindications to breast conservation do not seem to explain the higher mastectomy rates observed in older patients. Single-institution studies have demonstrated that when offered the option of breast preservation, women over age 70 choose this therapy with the same frequency as their younger counterparts.19,20 These data suggest that physician assumptions about the lack of importance of breast preservation in elderly women, rather than medical factors, may be responsible for the higher mastectomy rates seen in older women. The geographic variation in the use of breast preservation has also been noted in previous reports.11,13,21 Studies from the National Cancer Data Base13 and a study of national Medicare claims data demonstrate patterns similar to those in our study,21 with the highest rates of breast conservation in New England and the lowest rates in the Southern states. Comparison with the Surveillance, Epidemiology, and End-Results (SEER) data is more difficult because of the selected geographic sites in the SEER sample, but a similar pattern of higher rates of breast conservation in New England and the Pacific region than in the South was noted.11 However, the data from our study also suggest that geographic variations in the surgical therapy of breast cancer are slowly decreasing. In a 1990 study from the National Cancer Data Base of the American College of Surgeons, which used similar methods and the same geographic definitions, 52.6% of patients treated in New England for stage O and stage I carcinoma had breast conservation compared with 24% of cases treated in the South, a 28.6% difference.13 In the 1994 data sample presented here, this discrepancy in the use of breast conservation decreased to 22%. These differences in the use of BCT remain significant after controlling for other factors such as age, tumor characteristics, and insurance status. As such, they seem to reflect attitudinal differences, which although decreasing, are persistent and reproducible. A striking finding in our study is the direct correlation between factors predictive of an increased risk of systemic relapse of breast cancer as determined by the initial hospital pathology report and the use of mastectomy. The preferential use of mastectomy for large tumors, those with palpable adenopathy, and those with high-grade histology strongly suggest that BCS is not accepted as an equal treatment to mastectomy, but rather is viewed as a less aggressive procedure that is appropriate for patients with good-prognosis lesions. The higher mastectomy rates observed for T2 tumors could partially be explained by appropriate medical practice. The removal of a T2 tumor with a margin of normal breast tissue is less likely to result in a good cosmetic outcome than the removal of a smaller T1 lesion, and some patients with T2 tumors may have been selected appropriately for mastectomy. However, Morrow et al19 found that medical contraindications to breast conservation were present in only 28% of 169 patients with stage II tumors. Similarly, Foster et al20 reported that 72% of 102 patients with T2 tumors successfully underwent BCT. A medically appropriate rationale for higher mastectomy rates for patients with palpable adenopathy does not exist. The presence of axillary nodal metastases is an indication for systemic therapy, but Morrow et al19 observed that axillary node metastases were not predictive of the ability to undergo BCT after controlling for tumor size. The finding that fewer than one third of patients with T2 lesions or palpable adenopathy undergo breast preservation, coupled with the progressive increase in mastectomy rates with increasing histologic grade of the primary tumor, indicates a need for further physician education regarding selection criteria for breast preservation. The absolute contraindications to breast preservation described by the ACOS, American College of Radiology, College of American Pathologists, and Society of Surgical Oncology make no reference to prognostic variables in the selection of local therapy.9 The contraindications address the three essential elements of BCT, which include: (1) the ability to reduce the tumor burden to a microscopic level, (2) the ability to safely irradiate the breast, and (3) the ability to detect tumor recurrence within the preserved breast. None of the factors in this study that were found to correlate with a greater likelihood of mastectomy, with the possible exception of increasing tumor size, qualify as selection criteria for breast conservation when these essential elements are considered. The presence of EIC in association with an invasive tumor also was found to be a strong predictor of mastectomy. Older studies in which patients were treated by gross excision without margin evaluation suggested that an EIC was an indicator of an increased risk of local failure after BCT.22 However, subsequent studies demonstrated that if negative margins were obtained, patients with an EIC were not at increased risk of local recurrence.23 The addition of RT to BCS remains a standard of care. Six randomized clinical trials have compared conservative surgery alone with conservative surgery plus RT and have shown an average crude rate of reduction in the risk of local recurrence of 75% with the addition of RT.2,24-28 A subset of patients who failed to benefit from RT was not identified in these studies. Overall, 86% of women undergoing BCS in this study received postoperative RT. This represents improved utilization compared with the 57% to 81% use of RT reported from nine SEER areas during 1985 to 198611 but is similar to the 84% to 88% utilization of RT after BCS in Western Washington State between 1983 and 1989.15 Age was the major factor predicting the use of postoperative RT in this study, with 88% of women under age 70 receiving RT compared with 79% age 70 and older. The decline in the use of RT with increasing age has been documented in several other studies11,15,29,30 and cannot be explained on the basis of toxicity.18 However, rates of local recurrence after wide excision alone in older women are reported to be low in some studies,24 and may account for some of the failure to use RT in this group. An increasing number of comorbid conditions has also been correlated with a decrease in the use of RT30 and may represent appropriate medical practice. The presence of comorbid conditions was not assessed in this study. This study provides information about the surgical therapy of a large group of patients with stage I and II breast cancer. However, the large sample size means that small absolute differences between groups, which may be of questionable clinical importance, achieve statistical significance. Caution should be used in drawing conclusions based on extremely small differences between groups or small subsets of the study population. This is particularly true of the racial differences observed in the study because only 14% of the patients studied were nonwhite. Because the data set was not population based, its generalizability could be questioned. However, the trends that we have observed regarding the impact of age, disease stage, geographic variation, and insurance status also have been reported in population-based studies.10,11,15,16,21,31 The obvious question which arises from this study is what percentage of women with stage I and II breast cancer should be treated with BCT? The incidence and type of contraindications to breast conservation vary with tumor stage and the populations studied. Two prospective analyses found that the incidence of contraindications to BCT ranged from approximately 10% in stage I patients to 30% in stage II patients.19,32 In an analysis of 1,514 patients from 18 hospitals in Massachusetts and 1,061 patients from 30 hospitals in Minnesota, 16% and 20%, respectively, were found to be ineligible for BCT on the basis of a review of the medical record.33 In addition, some women who are candidates for breast conservation chose to undergo mastectomy. Psychologic studies comparing patients undergoing mastectomy and breast conservation have failed to demonstrate major differences in psychologic well-being on the basis of operative procedure,34-38 although patients having breast preservation tend to have more concern about body image.39 This information suggests that the percentage of women choosing BCS will vary with the population being studied. A reasonable goal for any patient population is that all women should be adequately informed regarding the option of breast conservation and what the procedure entails. However, if the proportion of the patients in our study who were ineligible for BCT was similar to that reported in the literature, only about half of the eligible patients would have elected BCS, a figure substantially lower than that observed in other studies.19,32 Data from this study indicate that eligibility criteria for the procedure are not well understood in the physician community or are not being clearly communicated to patients. Continuing physician education is the first step in addressing this problem. However, to be effective, education regarding selection criteria for breast conservation must include not only surgeons, but the entire spectrum of physicians who now advise patients on the local therapy of breast cancer, including radiation oncologists, medical oncologists, radiologists, gynecologists, and primary care providers. The results of this study also indicate that widely publicized results of multiple randomized trials comparing BCT to mastectomy in combination with treatment guidelines developed by a multidisciplinary group are resulting in very gradual changes in the local therapy of stage I and II breast cancer.
Supported in part by Patterns of Care Study Grant no. NCI CA-65435.
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Copyright © 2001 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
