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Journal of Clinical Oncology, Vol 23, No 4 (February 1), 2005: pp. 783-791 © 2005 American Society of Clinical Oncology. DOI: 10.1200/JCO.2005.04.175 Breast Cancer Treatment Guidelines in Older WomenFrom the Departments of Breast Medical Oncology and Epidemiology, The University of Texas M.D. Anderson Cancer Center, Houston, TX Address reprint requests to Sharon H. Giordano, MD, MPH, The University of Texas M.D. Anderson Cancer Center, 1515 Holcombe Blvd, Box 424, Houston, TX 77030; e-mail: sgiordan{at}mdanderson.org
PURPOSE: To determine patterns and predictors of concordance with institutional treatment guidelines among older women with breast cancer. METHODS: The study population included 1,568 patients aged 55 years and older who were treated at M.D. Anderson Cancer Center between July 1997 and January 2002 for stage I to IIIA invasive ductal and lobular breast cancer. Concordance with institutional guidelines was determined for definitive surgical therapy, radiotherapy after breast-conserving surgery, radiation therapy after mastectomy, adjuvant chemotherapy use, and adjuvant hormonal therapy use. The following variables were considered as possible modifiers of concordance: patient age, marital status, race, educational level, Eastern Cooperative Oncology Group performance status, comorbidity score, clinical stage, hormone receptor status, HER2-neu status, tumor grade, pathologic tumor size, lymphatic invasion, and number of lymph nodes involved. Logistic regression modeling was performed to determine the independent effect of each variable on guideline concordance.
RESULTS: Older women were less likely to receive treatment in concordance with guidelines for definitive surgical therapy (P < .001), postlumpectomy radiation (P = .03), adjuvant chemotherapy (P < .001), and adjuvant hormonal therapy (P < .001). In multivariate analysis, age CONCLUSION: After adjustment for comorbidity score, race, marital status, educational status, clinical stage, and tumor characteristics, increasing patient age was independently associated with decreased guideline concordance for definitive surgery, adjuvant chemotherapy, and adjuvant hormonal therapy. Future research should focus on delineating the possible reasons for guideline discordance.
The United States is undergoing a dramatic demographic shift with the aging of the population, which has resulted in an increasing number of cases of breast cancer diagnosed in older women. In 2004, approximately 215,990 women will be diagnosed with breast cancer, of whom 41% will be age 65 years or older.1,2 Although the number of older women with breast cancer is burgeoning, there has been limited research on this segment of the breast cancer population. Important questions remain regarding how these patients are medically treated compared with younger women and the determinants of treatment patterns. Multiple studies have demonstrated that treatment for women with breast cancer differs substantially by patient age, with older women more likely to receive substandard therapy.3–18 Older women are less likely to receive standard-of-care surgery, radiation therapy after breast-conserving surgery, and adjuvant chemotherapy.3–18 In contrast, the use of adjuvant hormonal therapy has been reported to be independent of patient age.8,13,15,19,20 The reasons for these differences in patterns of care of older patients are probably multifactorial and may include a higher rate of patient comorbidities, poorer performance status, less social support, difficulty with transportation, patient or family preference, concerns about quality of life, lower life expectancy, and age bias.3,4,21 In addition, because so few research studies have included older women, the lack of data may lead to less aggressive care. Studies that have examined the predictors of surgery and adjuvant radiation have found that chronologic age was associated with substandard therapy independently of performance status or comorbidities, suggesting that physicians may be undertreating healthy older women.3–5,9,15,22 Similarly, the few studies that have evaluated predictors of adjuvant chemotherapy use have found age to be inversely associated with chemotherapy use, after considering comorbidities.15,18 However, most of these studies have been limited to a single treatment modality and have lacked complete individual patient information on patient demographics, comorbidities, tumor characteristics, and details of treatment. At The University of Texas M.D. Anderson Cancer Center, we have prospectively collected a database containing complete and detailed information on all patients treated at the institution for breast cancer. This degree of comprehensive information has been unavailable in most studies published to date. In addition, M.D. Anderson has developed specific practice guidelines for breast cancer treatment, against which actual treatment patterns can be compared.23 This study was undertaken to determine patterns and predictors of concordance with institutional breast cancer practice guidelines among older women with breast cancer for surgical therapy, adjuvant postlumpectomy radiation therapy, adjuvant postmastectomy radiation therapy, adjuvant chemotherapy, and adjuvant hormonal therapy.
This study is a retrospective cohort study of women age 55 years and older diagnosed with breast cancer and treated at M.D. Anderson between July 1997 and January 2002. The records of all newly diagnosed breast cancer patients treated at M.D. Anderson Multidisciplinary Breast Center since July 1997 have been abstracted and entered into a prospective electronic database, the Breast Cancer Management Systems Database, by trained data managers. This study included women with stage I to IIIA invasive ductal and lobular breast cancer. Women who were still undergoing adjuvant chemotherapy were excluded, as were all men. The study was approved by the institutional review boards at The University of Texas M.D. Anderson Cancer Center and at The University of Texas School of Public Health.
Data were extracted on the following variables: patient age, marital status, race, educational level, Eastern Cooperative Oncology Group performance status, comorbidities, clinical and pathologic stage (TNM system), method of presentation, estrogen receptor status, progesterone receptor status, HER2-neu status, tumor grade, pathologic tumor size, intramammary lymphatic invasion, number of lymph nodes involved, and details of treatment with surgery, chemotherapy, radiation, and hormonal therapy. Data were incomplete regarding marital status, educational level, and medical comorbidities, and patients' charts were reviewed to complete these variables. A comorbidity score was calculated using the method of Charlson et al, 24 which has been validated in both inpatient and outpatient populations with breast cancer. Descriptive analyses were performed with patient age stratified into three categories: 55 to 64 years, 65 to 74 years, and
The M.D. Anderson guidelines for the treatment of invasive breast cancer were used to determine concordance with guidelines (Table 1). Initial guidelines were published on September 24, 1996. New and updated versions of the guidelines were activated on September 8, 1998, November 17, 1998, and October 25, 2000. Therefore, treatment dates were used to determine which guideline was applicable at the time a patient was being treated if there were any changes in treatment recommendations. Concordance with guidelines was determined for the following: definitive surgical therapy, adjuvant radiation therapy after breast-conserving surgery, postmastectomy radiation, adjuvant chemotherapy, and adjuvant hormonal therapy. Definitive surgical therapy was defined as lumpectomy, partial mastectomy, segmental mastectomy, modified radical mastectomy, subcutaneous mastectomy, skin-sparing mastectomy, or radical mastectomy. Definitive surgical therapy had to include axillary lymph node dissection or sentinel node biopsy, with completion axillary dissection if the sentinel node was involved. Guideline concordance was determined for the entire cohort of patients and for each of the three following age strata: 55 to 64 years, 65 to 74 years, and
For each of the five guidelines, patient and tumor characteristics were considered as possible modifiers of concordance. Age, level of education, race, marital status, and comorbidity score were included in all final models, as these variables have been previously demonstrated to significantly impact treatment patterns.3,5,10,18,25,26 Different categorization schemes were explored to ensure adequate cell size. Age was explored as both a continuous and categoric variable. Univariate measures of association were calculated to determine the association between each dependent variable and guideline concordance. Multiple logistic regression analyses were performed to determine the association between age and guideline concordance, adjusting for the effects of potential confounders. Results are presented as odds ratios (ORs) with 95% CIs. Statistical analyses were performed with STATA 7.0 software (Stata Corp, College Station, TX).
A total of 1,568 women were included in this retrospective cohort study. Patient characteristics are listed in Table 2. Women aged 65 years and older were significantly more likely to be white, unmarried, and have less than a college education. As expected, each older cohort had a higher percentage of women with significant comorbidities, consistent with the aging process.10,27 No statistically significant difference in stage at diagnosis by patient age was seen. Significant differences were detected in estrogen receptor status, nuclear grade, and presence of intramammary lymphatic invasion, with older women less likely to have estrogen receptor-negative tumors, high-grade tumors, or tumors with intramammary lymphatic invasion.
Figure 1 shows concordance rates for the five treatment guidelines of interest by patient age. Overall concordance with treatment guidelines was high for use of definitive surgical therapy (90.4%), adjuvant radiation after breast-conserving surgery (94.2%), and adjuvant hormonal therapy (93.7%). However, overall concordance was lower for adjuvant chemotherapy (70.7%) and for adjuvant postmastectomy radiation (54.1%). Guideline concordance for use of definitive surgical therapy, adjuvant radiation after breast conservation, adjuvant chemotherapy, and adjuvant hormonal therapy was lower for older women.
Univariate and multivariate predictors of guideline concordance for definitive surgical therapy are listed in Table 3. In univariate analysis, low tumor stage, high comorbidity score, and patient age of 75 years or older were associated with lack of definitive surgical treatment. In multivariate analysis, age of 75 years or older and stage I disease remained significant predictors of receiving less than definitive surgery. Women with stage II or III disease at diagnosis had 4.33 times the odds of having definitive surgery compared with women with stage I disease (95% CI, 2.16 to 8.72). Women who were age 75 years or older were also significantly less likely to receive definitive surgical therapy (OR, 0.27; 95% CI, 0.13 to 0.54).
Analysis of concordance with guidelines showed that adjuvant radiation therapy after breast conservation was more likely to be administered to women in the younger age categories (Table 4). In the unadjusted analysis, a comorbidity score of 3 or higher, high tumor grade, and age 75 years or older were associated with decreased likelihood of being treated with post-breast-conserving radiation therapy. In the multivariate analysis, age was associated with lower odds of receiving radiation therapy, but this association was not statistically significant (OR, 0.36; 95% CI, 0.10 to 1.30). A comorbidity score of 1 to 2 was also associated with a decreased likelihood of being treated with radiation (OR, 0.31; 95% CI, 0.11 to 0.90). Similarly, a comorbidity score of 3 or higher was associated with decreased odds of receiving radiation, but this was not statistically significant (OR, 0.25; 95% CI, 0.02 to 2.87). Of note, nonwhite race was strongly associated with decreased likelihood of being treated with radiation after breast-conserving surgery. The odds of a nonwhite woman receiving radiation therapy after a lumpectomy was 0.29 times that for a white woman receiving postlumpectomy radiation (95% CI, 0.09 to 0.91). For postmastectomy radiation, no variables were significantly associated with the use of this adjuvant treatment in univariate and multivariate analyses. Patients who were older than 75 years were less likely to receive postmastectomy radiation, but the 95% CIs were wide (OR, 0.1; 95% CI, 0.01 to 2.1).
In the unadjusted analysis of concordance with chemotherapy guidelines, higher clinical stage, lower comorbidity scores, estrogen receptor-negative tumors, high nuclear grade, and younger age were all significantly associated with guideline concordance (Table 5). In the multivariate analysis, high clinical stage, estrogen receptor-negative status, and younger age were all significantly associated with guideline concordance for adjuvant chemotherapy. Women with clinical stage II and III disease were 6.16 times more likely to be given chemotherapy in concordance with guidelines than women with stage I breast cancer (95% CI, 3.51 to 10.82). Women who had tumors that expressed the estrogen receptor were significantly less likely to be given chemotherapy than women with estrogen receptor-negative tumors (OR, 0.20; 95% CI, 0.09 to 0.47). After adjusting for all other factors noted above, patient age was a predictor of receipt of chemotherapy per guidelines. Women aged 65 to 74 years and older than 75 years were 76% less likely (OR, 0.24; 95% CI, 0.14 to 0.43) and 97% (OR, 0.03; 95% CI, 0.01 to 0.95) less likely, respectively, to receive chemotherapy according to M.D. Anderson guidelines than women aged 55 to 64 years.
Predictors of concordance with hormonal therapy guidelines are shown in Table 5. Univariate analysis showed that being unmarried, having stage I breast cancer, and being older than 75 years were associated with not receiving hormonal therapy according to the guidelines. After adjusting for other known predictive factors, low tumor stage and advanced age were still significant predictors of discordance with hormone therapy guidelines, although marital status was not. Women with stage II/III cancer were 2.76 times more likely to have hormonal therapy consistent with guidelines than women with stage I disease (95% CI, 1.14 to 6.69). Women aged 56 to 74 years were 56% less likely to receive hormonal therapy concordant with guidelines, although this association was not statistically significant (OR, 0.44; 95% CI, 0.17 to 1.15). Women aged 75 years or older were 90% less likely to be treated with hormonal therapy when indicated by guidelines (OR, 0.10; 95% CI, 0.03 to 0.27) than women aged 55 to 64 years.
In this study of 1,568 women with stage I to IIIA infiltrating ductal or lobular breast cancer aged 55 years and older, we have shown that clinical factors, comorbidities, patient race, and patient age are all independent predictors of concordance with institutional practice guidelines for the treatment of early-stage breast cancer. As would be expected, clinical factors were among the most important factors in predicting therapy concordant with guidelines. More advanced clinical disease stage, in particular, was highly predictive of therapy concordant with guidelines for treatment with definitive surgical therapy, adjuvant chemotherapy, and adjuvant hormonal therapy. Similarly, having an estrogen receptor-negative tumor was strongly associated with increased concordance with adjuvant chemotherapy guidelines. These findings are consistent with patients who have a higher risk of disease recurrence being treated more aggressively. The role of clinical judgment was also apparent in that patients who had a high burden of coexisting illnesses were less likely to receive therapy concordant with guidelines. Higher comorbidity scores were associated with poorer guideline adherence for adjuvant systemic therapies and postlumpectomy radiation, although the association only reached statistical significance for postlumpectomy radiation therapy. Interestingly, the comorbidity burden of the M.D. Anderson patients was higher than that reported in the general population, despite a younger age distribution than in comparable population-based studies.22,28,29 For instance, in the M.D. Anderson patient population aged 65 years and older, 63% had a comorbidity score of 0, 20% had a score of 1, and 17% had a score of 2 or higher. This is in contrast with data from the population-based Virginia Cancer Registry, which found only 76% of patients had a Charlson comorbidity score of 0, 15% had a score of 1, and 9% had a score of 2 or higher, or a study on breast cancer patients aged 65 years and older using Surveillance, Epidemiology, and End Results–Medicare database, which reported 79% of patients with a score of 0, 8% with a score of 1, and 13% with a score of 3 or higher.22,28 A possible explanation could be better ascertainment of comorbidities in the present study than in previous trials, because our comorbidity index was ascertained by chart abstraction rather than International Classification of Diseases 09 codes; however, a population-based study of chart abstraction to ascertain Charlson comorbidity scores still reported lower comorbidity scores than were seen in our patient population.29 Despite higher than expected comorbidity scores, the patients' functional status was very good, with all but three patients having an Eastern Cooperative Oncology Group performance status of 0 or 1. The high functional status of our patients may reflect our current referral patterns, because only one third to one half of our patients are from the local area. Thus a substantial proportion of our patients travel for their care, which may bias our patients toward those with a good performance status. A striking finding in this study was that nonwhite women were significantly less likely to receive radiotherapy after breast-conserving surgery (OR, 0.29; 95% CI, 0.09 to 0.91). Unfortunately, sample size was too limited to allow further stratification into African American, Hispanic, and other ethnic minorities. Mandelblatt et al15 have reported that older black women are twice as likely as older white women to have radiotherapy omitted. Because no studies, including the present study, have distinguished the reasons for omission of radiotherapy, it remains unclear what factors account for this apparent racial disparity. This does not seem to represent a systematic undertreatment of nonwhite patients because race was not a predictive factor for any other modality of therapy. Race could be confounded by patient socioeconomic status, insurance status, availability of transportation, or patient choice. It is also possible that cultural beliefs may impact whether women choose to have radiotherapy. Our finding clearly requires further investigation into the differences in the use of adjuvant radiotherapy between white and minority populations. After adjustment for clinical factors, patient demographics, and comorbidity scores, patient age still emerged as a significant predictor of guideline concordance for definitive surgical therapy, adjuvant chemotherapy, and adjuvant hormonal therapy. Advancing patient age was associated with poorer concordance with guidelines. For concordance with chemotherapy guidelines, women aged 65 to 74 years and those older than 75 years had 0.24 times and 0.03 times lower odds of being treated in concordance with chemotherapy guidelines. These findings are consistent with a study by DeMichele et al18 on adherence to chemotherapy guidelines, which reported that the odds of receiving a recommendation for chemotherapy decreased by 22% for each year of increasing patient age. It is noteworthy that so few of our older patients who were candidates for chemotherapy per guidelines were actually treated with chemotherapy. Existing medical illnesses do not explain this finding, as 87% of our patients had comorbidity scores of 0 to 1 and only 30% of the women aged 65 to 74 years and 4% of women older than 75 years who were candidates for chemotherapy actually received it. Similarly, virtually all of the patients in this study had excellent functional status. Our study did not examine the role of patient or physician preference in chemotherapy use. However, the study by DeMichele et al found no difference in patient acceptance of chemotherapy by patient's age.18 This suggests that physicians are not offering chemotherapy to healthy older women. The medical controversy surrounding the optimal adjuvant treatment of older women likely contributes to poorer adherence to guidelines among older women. Although the M.D. Anderson guidelines do not specify an age limit for the use of chemotherapy, there is clearly a lack of clinical trials-based evidence regarding chemotherapy use in older women. The St. Gallen Consensus guidelines and the National Institutes of Health guidelines provide clear recommendations for chemotherapy use in high-risk women age 70 years or younger.30–32 However, for women over the age of 70 years, there is sparse information from randomized controlled trials, and many oncologists are reluctant to expose older women to the toxic effects of chemotherapy in the absence of definitive data showing efficacy. In addition, the magnitude of risk reduction from chemotherapy declines with age and the risk of death from competing causes increases, leading to additional decline in the benefit of chemotherapy for older patients.10,33 The decision analysis of Extermann et al34 demonstrated that the percentage risk of relapse needed to justify the use of chemotherapy is higher in older than younger women. Thus the threshold for chemotherapy set in our institutional guidelines may not be appropriate for older women with baseline low risks of recurrence. We also found that patient age was associated with concordance with guidelines for hormonal therapy. Previous studies had indicated that age was not a significant factor in the use of hormonal therapy or that hormonal therapy use increased with increasing patient age.20,35,36 Our findings were in contrast to these studies, because we found a decreased use of hormonal therapies in women older than 75 years. However, even in our oldest age group, 83% of patients were treated in concordance with guidelines (as compared with 95% of women aged 55 to 74 years). For all age groups, concordance is higher than reported previously. For instance, Silliman36 reported that only 53% of women age 65 to 69 years and 74% of women age 70 to 79 years were offered adjuvant tamoxifen. The less frequent use of hormonal therapy in the oldest group of women may be due to physician beliefs, patient's preference, financial considerations, lack of insurance, or increasing prevalence of specific comorbidities that may preclude the use of tamoxifen, such as thromboembolic disease. In our cohort of patients, age was not a significant predictor of receipt of adjuvant radiotherapy after breast conservation. This is in contrast to the findings from larger population-based studies that have found that older women have a lower likelihood of receiving radiation therapy after lumpectomy.14,15,17,22,37 At tertiary referral centers, physicians may be more aggressive in treating older women than physicians in community practice; or, conversely, women who are more motivated and who are more likely to accept therapy are those who travel to referral centers for treatment. There also is existing controversy on the benefit of postlumpectomy radiation in older women with early-stage estrogen receptor-positive tumors.38,39 Among women 50 years and older with small hormone receptor-positive breast tumors, radiation plus tamoxifen significantly reduced the risk of recurrence after lumpectomy.39 In a similar study of women age 70 years and older with stage I estrogen receptor-positive tumors, radiation also lowered the risk of local recurrence from 4% to 1%; however, given the baseline low risk, the authors conclude that omission of radiation in this group of patients can be a reasonable choice.38 The ability to generalize the findings of our study may be limited because the cohort of patients is from a single tertiary care institution and may not be representative of all patients in the general population. Our patients seemed to have a higher burden of comorbid illnesses, but possibly better functional status than has been seen in other population-based studies. Similarly, the treatment patterns, physicians, and interest in research at M.D. Anderson may systematically differ from community practices. However, strengths of this study include a large cohort of patients with comprehensive information on patient demographics, comorbidities, functional status, tumor pathology, and details of multimodality treatment, including surgery, radiation, and adjuvant systemic therapies. In addition, although our overall guideline adherence rates (eg, for adjuvant tamoxifen) were higher than has been previously reported, the factors that predict guideline deviation may be more similar across institutions. We have evaluated patterns and predictors of the treatment of older women across several breast cancer treatment modalities, yet it remains unclear why some women were not treated according to institutional practice guidelines. Many reasons exist, including those that are clinically valid, which could include medical contraindications or early disease recurrence. In addition, we have not examined the role of patient preferences in treatment decisions. It is possible that older women are more likely to refuse chemotherapy or hormonal therapy or that nonwhite women are more likely to decline adjuvant radiation. Further research is needed to distinguish the medically valid and appropriate reasons from those that represent a failure of the system to provide standard care. Discerning the reasons for guideline discordance is a research priority so that appropriate interventions can be developed when guideline discordance results in inappropriate care.
The authors indicated no potential conflicts of interest.
Supported in part by the Nellie B. Connally Breast Cancer Research Fund. S.H.G. is supported by National Institutes of Health grant No. 1K07CA109064-01. Authors' disclosures of potential conflicts of interest are found at the end of this article.
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39. Fyles AW, McCready DR, Manchul LA, et al: Tamoxifen with or without breast irradiation in women 50 years of age or older with early breast cancer. N Engl J Med 351:963–970, 2004 Submitted April 30, 2004; accepted October 27, 2004. This article has been cited by other articles:
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Copyright © 2005 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
75 years predicted a deviation from guidelines for definitive surgical therapy, adjuvant chemotherapy, and adjuvant hormonal therapy. Nonwhite race was associated with decreased likelihood of adjuvant radiation therapy after breast conservation. 
2 test, or Fisher's exact test when appropriate, was used to determine the association between dichotomized age and patient characteristics. All P values presented are two-sided. 
