Surgeon Characteristics and Receipt of Adjuvant Radiotherapy in Women With Breast Cancer

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1 ARTICLE Surgeon Characteristics and Receipt of Adjuvant Radiotherapy in Women With Breast Cancer Dawn L. Hershman, Donna Buono, Russell B. McBride, Wei Yann Tsai, Kathy Ann Joseph, Victor R. Grann, Judith S. Jacobson Background Methods Results Conclusions Adjuvant radiotherapy following breast conservation surgery (BCS) is considered to be an indicator of quality of care for the majority of women with breast cancer, but many women do not receive adjuvant radiotherapy. We investigated the association of surgeon-related factors with receipt of adjuvant radiotherapy after BCS. We used the linked Surveillance, Epidemiology and End Results (SEER) Medicare database to identify women aged 65 years or older with stage I/II breast cancer who were diagnosed between 1991 and 2002 and underwent BCS. We collected demographic and clinical data from SEER and treatment information from Medicare claims data. The American Medical Association Masterfile was used to obtain information on surgeons characteristics, including sex, medical school location (United States or elsewhere), and type of degree (MD or Doctorate in Osteopathic Medicine [DO]). The associations of patient (age, race, rural vs urban residence, comorbidities, marital status), tumor (hormone receptor status, grade, stage), and surgeon-related factors with receipt of adjuvant radiotherapy were analyzed using Generalized Estimating Equations to control for clustering. All statistical tests were two-sided. Of women in our sample, (75%) received radiotherapy. Patients who received adjuvant radiotherapy were younger, had fewer comorbidities, and were more likely to be white, married, from an urban area, and diagnosed in a later year compared with those who did not. They were also more likely to have a surgeon who was female (79% vs 73%), had an MD degree (75% vs 68%), or was US trained (75% vs 70%). The multivariable analysis confirmed the association of radiotherapy with having a surgeon who was female (odds ratio [OR] = 1.13; 95% confidence interval [CI] = 1.06 to 1.27), had an MD degree (OR = 1.55; 95% CI = 1.24 to 1.91), was US trained (OR = 1.12; 95% CI = 1.01 to 1.25), or had more than 15 patients (OR = 1.18; 95% CI = 1.10 to 1.28). Surgeon characteristics were associated with patients receipt of adjuvant radiotherapy after BCS after controlling for patient and tumor characteristics, although the individual effect sizes were small for surgeon sex, location of training, and type of medical degree. More research is warranted to confirm the associations to determine whether they reflect surgeon behavior, patient response, or physician patient interactions. J Natl Cancer Inst 2008;100: Research on quality of care in oncology has focused on how patient factors, such as race/ethnicity, age, and socioeconomic status (SES), result in suboptimal care. However, little research has addressed how physician characteristics such as sex, training, practice volume, and type of practice may influence the quality of care patients receive. In the 1980s, adjuvant radiation therapy after breast conservation surgery (BCS) ( 1 ) was found to reduce the risk of local recurrence for patients with breast cancer ( 2 4 ). Recent meta-analyses showed that, among 7300 patients treated with BCS, those who received adjuvant radiotherapy had a 5-year local recurrence risk of 7% and a 15-year breast cancer mortality risk of 30.5%. By comparison, those who received surgery alone had a 5-year local recurrence risk of 26% and 35.9% breast cancer mortality after 15 years ( P <.001) ( 5, 6 ). In response to these findings, a report published by the Agency for Healthcare Research and Quality recognized post-bcs radiotherapy as both an indicator and a measure of quality care ( 7 ). Affiliations of authors: Departments of Medicine (DLH, VRG) and Surgery (KAJ) and the Herbert Irving Comprehensive Cancer Center (DLH, WYT, KAJ, VRG, JSJ), College of Physicians and Surgeons, and the Departments of Epidemiology (DLH, DB, RBM, VRG, JSJ) and Biostatistics (WYT), Mailman School of Public Health, Columbia University; New York Presbyterian Hospital, New York. Correspondence to: Dawn L. Hershman, MD, MS, Herbert Irving Comprehensive Cancer Center, Rm 1068, 161 Fort Washington, New York ( dlh23@columbia.edu ). See Funding and Notes following References. DOI: /jnci/djm320 The Author Published by Oxford University Press. All rights reserved. For Permissions, please journals.permissions@oxfordjournals.org. jnci.oxfordjournals.org JNCI Articles 199

2 CONTEXT AND CAVEATS Prior knowledge The extent to which such surgeon characteristics as sex, location of medical education, and type of degree are associated with their patients receipt of adjuvant radiotherapy following breast conservation surgery was unknown. Study design Generalized Estimating Equations were used to analyze the association of patient and surgeon characteristics based on information from the American Medical Association Masterfile and the linked Surveillance, Epidemiology and End Results Medicare database. Contribution After controlling for patient characteristics, this study found associations between surgeon characteristics and an indicator of the quality of breast cancer care, receipt of adjuvant therapy after breast conservation surgery. Implications More research is warranted to confirm the observed associations and to determine whether they are reflective of surgeon behavior, patient response, or physician patient interaction. Limitations The database did not provide information on a number of potentially important surgeon- and patient-related variables and did not allow investigators to differentiate between lack of referral or patient refusal as the reason for not receiving radiotherapy. Since the early 1990s, the use of radiotherapy following lumpectomy has increased, but it remains far from universal ( 8, 9 ) only 62% 94% of patients, depending on the population sampled, receive this treatment ( ). BCS itself is more common among younger patients, those in urban areas, and those diagnosed in academic medical centers than among older patients, those in rural areas, and those diagnosed in community hospitals, respectively ( 15 ). Compared with white non-hispanic women, Hispanic women were 38% less likely to receive radiotherapy following breast cancer surgery, and, for patients as a whole, the probability of receiving radiotherapy decreased by 3% for every 5 additional miles between the patient s residence and an radiotherapy facility ( 9 ). Thus, patient characteristics have been associated with the receipt of post- BCS radiotherapy and, therefore, with quality of care. Little is known about the influence of physician characteristics on breast cancer care. In this study, we used a large populationbased registry to investigate the association of physician-related factors with receipt of adjuvant radiotherapy following BCS. Patients and Methods Study Database This study utilized the Surveillance, Epidemiology and End Results (SEER) Medicare linked database, which was codeveloped by the US National Cancer Institute (NCI) and the Center for Medicare and Medicaid Services. The SEER Program represented roughly 14% of the United States population in 1991 and, since 2000, it represents approximately 26%. Medicare covers hospital services, physician services, some drug therapy, and other medical services for more than 97% of persons aged 65 or older. The linked SEER Medicare database contains clinical, demographic, and medical claims data on patients aged 65 years or older and is a unique population-based resource for longitudinal epidemiologic and health outcomes studies. Its characteristics and validation have been described comprehensively elsewhere ( 16, 17 ). To obtain information on the characteristics of the SEER Medicare patients physicians, we used the Unique Physician Identification Number (UPIN) to link the Medicare claims with the American Medical Association (AMA) Masterfile as described elsewhere ( 18 ). This file contains data collected from physician members of the AMA, including sex, age, medical degree (MD or Doctorate in Osteopathic Medicine [DO]), location of medical school (United States vs foreign), year of graduation, employment setting, and specialty ( 18 ). Patient Selection We initially identified all female Medicare participants aged 65 years or older who were diagnosed with stage I/II breast cancer from January 1, 1991, through December 31, 2002, who underwent BCS within 3 months (n = ) after their date of diagnosis and did not have a claim for mastectomy within 90 days after BCS (n = ). We used Medicare claims to identify patients who had received radiotherapy within 1 year of the date of diagnosis. Women who did not participate in Medicare Parts A and B during the 12 months before their diagnosis and women who had a prior breast cancer or other cancer, end-stage renal disease, or a breast cancer diagnosis without histologic confirmation were excluded. Also excluded were women whose physician did not have a UPIN number or a primary or secondary specialty listed in the AMA Masterfile (n = 1144). If a patient had two physicians, the physician who billed for the surgery was counted as her surgeon; if neither was listed as the operating physician, then the first physician listed was used. Among women with three or more physicians (n = 149), only those who had a surgical oncologist (n = 19) were included in the study. Surgeon Characteristics Surgeon characteristics that were analyzed based on the variables in the AMA Masterfile included sex, year of graduation, primary employment setting (private vs other), location of training (United States vs other), and type of degree (MD or DO). Physician age was characterized by decade of birth. Physicians patient volumes (ie, total number of claims for BCS in the database ) were dichotomized as 1 15 vs 15 procedures. We defined high surgeon volume as a surgeon who performed more than 15 of the surgeries in the sample. They represented the most active 15% of the surgeons who performed over 80% of the surgeries. Measurement of Treatments and Outcomes We identified and categorized patients with respect to the surgery, radiotherapy, and chemotherapy they received using the SEER Medicare linked databases and International Classification of Diseases, Ninth Revision, Clinical Modification ( ICD-9-CM ) procedure, Current Procedural Terminology, Fourth Edition ( CPT-4 ), Healthcare Common Procedure Coding System ( HCPCS ), and ICD-9-CM V codes. These codes have been found to capture virtually all breast cancer cases ( 19 ). 200 Articles JNCI Vol. 100, Issue 3 February 6, 2008

3 We categorized patients as having had BCS if they had any of the following procedures: segmental mastectomy, lumpectomy, quadrantectomy, tylectomy, wedge resection, excisional biopsy, nipple resection, and partial mastectomy unspecified. We categorized patients as having had adjuvant radiotherapy if they had received beam radiation, radioactive implants, radioisotopes, or other radiation ( 20 ). We ascertained chemotherapy exposure in the Medicare files using codes for ICD-9-CM diagnosis, ICD-9-CM procedural, CPT, HCPCS, and revenue center codes ( 16, 17 ). Socioeconomic Status of Patients An aggregate SES score was generated from a hierarchy of income data from the 2000 census according to the method adapted from Krieger et al. ( 21 ). Patients were ranked on a 1 5 scale, where 1 was the lowest value, based on a formula incorporating as many of the following as were available: median income in the census tract of residence, median income in the zip code of residence, census tract per capita income, and zip code per capita income. Patients for whom values for all variables were missing were assigned to the lowest SES category. Comorbid Disease To assess the prevalence of comorbid disease in our cohort, we used the Klabunde adaptation of the Charlson comorbidity index ( ). Medicare inpatient and outpatient claims were searched for ICD-9- CM diagnostic codes indicating a history of myocardial infarction, congestive heart failure, peripheral vascular disease, cerebrovascular disease, chronic pulmonary disease, connective tissue disease, ulcer, liver disease, diabetes, hemiplegia, renal disease, or AIDS from 12 months before to 1 month after the diagnosis of cancer. Each condition was weighted, and patients were assigned a score based on the Klabunde Charlson index ( 24 ). Statistical Analysis The chi-square test was used to compare surgeon-related, demographic, and clinical characteristics between patients who received radiotherapy and those who did not and between patients who were operated on by a female surgeon and those who were operated on by a male surgeon. Univariate odds ratios (ORs) were calculated individually for each variable. All hypothesis tests were two-sided. The Generalized Estimating Equation (GEE) methodology was introduced by Zeger and Liang ( 25 ) to deal with clustering in data that otherwise would be analyzed by means of a generalized linear model, and GEEs (PROC GENMOD in SAS) have become an important strategy in the analysis of correlated data ( 25, 26 ). We used GEEs to account for the correlations of outcome measures among patients who had the same physician. The unit of analysis was the patient. For each patient, the physician s unique UPIN number was used as the clustering variable. The model assumptions were as follows: the data had a binomial distribution, the link function was logit, and the type of variance was exchangeable. We evaluated the odds of radiotherapy for all the categories of each variable, controlling for all the other variables in the model. The model included 1) operating physician characteristics (sex, type of degree, country of training, practice type, surgical volume); 2) patient demographic variables (age, race, place of residence, marital status, SES); and 3) clinical variables (tumor grade, American Joint Committee on Cancer stage, hormone receptor status, comorbidity score). We also performed the same analysis for the odds of consultation with a radiation oncologist. To take into account the increases in both radiotherapy and in female physicians over time, we stratified the patients by year of diagnosis in two time frames: and , representing an even distribution of the female physicians. All statistical analyses were conducted using the SAS system for Windows, Version Results We identified women in the SEER Medicare database who were diagnosed with stage I or II breast cancer during the study period and who met the eligibility criteria. A total of 4455 surgeons operated on these patients; patients (82%) saw a radiation oncologist, and (75%) underwent radiotherapy. In each year from 1991 through 1999, the proportions of newly diagnosed patients who saw a radiation oncologist and who received radiotherapy increased, and since then the proportions have stabilized ( Fig. 1 ). The physicians who performed BCS on these patients were predominantly male (88%), in private practice (79%), trained in the United States (81%), and holders of MD (95%) as opposed to DO degrees. Table 1 compares the distributions of patients who did and did not receive radiotherapy according to the demographic and clinical characteristics of the patient and the surgeon. As the unadjusted odds ratios show, radiotherapy use was associated with all of the clinical, demographic, and physician variables assessed in Table 1, except for the surgeon s type of practice (private or not). Patients who received radiotherapy were statistically significantly more likely than those who did not to have a surgeon who was female Radiation Therapy Radiation Oncology Consulation Fig. 1. Percentage of patients (n = ) diagnosed with stage I/II breast cancer in the Surveillance, Epidemiology, and End Results Medicare database who were billed for a consultation with a radiation oncologist and underwent radiation therapy after breast conservation surgery, by year of breast cancer diagnosis between January 1, 1991, and December 31, jnci.oxfordjournals.org JNCI Articles 201

4 Table 1. Unadjusted associations between receipt of radiotherapy among elderly patients who had breast conservation surgery for early-stage breast cancer and the characteristics of their surgeons and their own demographic and clinical characteristics * Characteristics No. (%) OR (95% CI) Surgeon characteristics Degree DO 485 (68) 1.00 (Referent) MD (75) 1.65 (1.42 to 1.92 ) US trained No 3018 (70) 1.00 (Referent) Yes (75) 1.28 (1.19 to 1.38) Decade of graduation Before (70) 1.00 (Referent) (73) 1.20 (1.09 to 1.32) (75) 1.31 (1.20 to 1.44) (77) 1.43 (1.30 to 1.57) After (76) 1.36 (1.18 to 1.57) Type of practice Nonprivate 3515 (74) 1.00 (Referent) Private (75) 1.05 (0.98 to 1.12) No. of BCS procedures (72) 1.00 (Referent) > (77) 1.23 (1.16 to 1.29) Sex Male (74) 1.00 (Referent) Female 3806 (79) 1.34 (1.24 to 1.44) Patient demographic characteristics Age at diagnosis (89) 1.00 (Referent) (87) 0.80 (0.72 to 0.89) (80) 0.49 (0.45 to 0.54) (47) 0.11 (0.10 to 0.12) Race White (75) 1.00 (Referent) Black 921 (64) 0.61 (0.54 to 0.68) Hispanic 226 (75) 0.97 (0.75 to 1.26) Other 750 (76) 1.03 (0.89 to 1.20) Residence Nonmetropolitan 1163 (64) 1.00 (Referent) Metropolitan (75) 1.71 (1.55 to 1.89) Marital status Unmarried (67) 1.00 (Referent) Married (84) 2.53 (2.39 to 2.68) Unknown 711 (66) 0.94 (0.83 to 1.08) SES Lowest quintile 3244 (67) 1.00 (Referent) 2nd quintile 3957 (74) 1.36 (1.24 to 1.46) 3rd quintile 4501 (75) 1.47 (1.35 to 1.59) 4th quintile 4879 (77) 1.60 (1.47 to 1.74) Highest quintile 5292 (78) 1.72 (1.59 to 1.87) Patient clinical characteristics Stage I (75) 1.00 (Referent) II 6085 (73) 0.88 (0.83 to 0.93) Hormone receptor status ER and PR 2197 (78) 1.00 (Referent) ER+ and/or PR (76) 0.89 (0.81 to 0.98) Unknown 3179 (65) 0.50 (0.45 to 0.56) Grade Poorly differentiated (76) 1.00 (Referent) Well/moderately differentiated 4961 (75) 0.94 (0.88 to 1.00) Unknown 2798 (67) 0.64 (0.60 to 0.69) Received chemotherapy No (73) 1.00 (Referent) Yes 2937 (89) 2.98 (2.66 to 3.33) Comorbidity score (79) 1.00 (Referent) (72) 0.67 (0.63 to 0.71) > (61) 0.42 (0.39 to 0.45) * A total of patients (75% of patients in the sample) received radiotherapy. OR = odds ratio; CI = confidence interval; DO = Doctor of Osteopathic Medicine; MD = Medical Degree; BCS = breast conservation surgery; SES = socioeconomic status; ER = estrogen receptor; PR = progesterone receptor. (79% vs 73%), had an MD degree (75% vs 68%), or was US trained (75% vs 70%). Female surgeons were more likely than male surgeons to have patients who resided in a metropolitan location, were married, received chemotherapy, and had no comorbid conditions (data not shown). Female surgeons were slightly more likely than male surgeons to have DO degrees and to be US trained; they also performed more BCS procedures and were less likely to practice in a private setting ( Table 2 ). The proportion of female surgeons performing breast cancer surgery increased from 7% in 1991 to 24% in 2002 ( Fig. 2 ). Controlling for known potential demographic and clinical confounders, patients who received radiotherapy were more likely than patients who did not to have their BCS performed by a surgeon who had an MD rather than a DO degree (OR = 1.55; 95% CI = 1.24 to 1.91, P <.001), was US trained (OR = 1.12, 95% CI = 1.01 to 1.25, P =.03), had performed procedures on more than 15 patients in this cohort (OR = 1.18, 95% CI = 1.10 to 1.28, P <.001), and was female (OR = 1.13, 95% CI = 1.06 to 1.27, P =.04) ( Table 3 ). In addition, patients who received radiotherapy were more likely than those who did not to be young, to be married, to have stage I rather than stage II disease, to have no comorbid conditions, to reside in a metropolitan area, to be above the lowest category of SES, and to receive adjuvant chemotherapy and were less likely to be of black race/ethnicity. To control for the interaction between year of diagnosis and surgeon sex, we conducted separate GEE analyses of the association between surgeon sex and receipt of radiotherapy among patients stratified into two groups by year of diagnosis ( and ) ( Table 4 ). Surgeon sex was not associated with receipt of radiotherapy among patients diagnosed during ( P =.44). However, patients diagnosed between 1999 and 2002 were more likely to receive adjuvant radiotherapy if they had a female surgeon than if they had a male surgeon (OR = 1.17, 95% CI = 1.01 to 1.36, P =.04). Discussion In our sample population of women older than 65 in the linked SEER Medicare database, in , 25% of women did not receive radiotherapy following BCS, although the proportions of patients who received radiotherapy increased among patients diagnosed in each succeeding year during the 1990s ( Fig. 1 ). Patients characterized by increased age, black race, residence in a nonmetropolitan location, or unmarried status were less likely than others to receive adjuvant radiotherapy after BCS. After adjustment for patient and tumor characteristics, receipt of post-bcs radiotherapy was also associated with surgeon characteristics including sex, location of training (United States vs foreign), type of degree, and number of patients operated on in the cohort. Surgeon characteristics have been found to play an important role in the receipt of other types of postsurgical care besides radiotherapy. Cyran et al. ( 27 ) found that patients with early-stage breast cancer who were seen by female surgeons were more likely to receive BCS, as opposed to mastectomy, than patients seen by male surgeons. Using SEER Medicare data, other investigators observed associations between physician characteristics and receipt of androgen deprivation therapy for prostate cancer ( 28 ) as well as 202 Articles JNCI Vol. 100, Issue 3 February 6, 2008

5 Table 2. Characteristics of surgeons performing breast conservation surgery on cohort members , by sex * Surgeon characteristics referral to an oncologist after a diagnosis of stage III colon cancer ( 29 ) or lung cancer ( 30 ). The probability of a patient s being referred to subspecialists has also been associated with the primary care physician s sex, number of years in practice, practice patient volume, and patient population characteristics ( ). Patients with breast cancer are more likely to have BCS if their surgeon is female or has a large case volume than if their surgeon is male or performs relatively few procedures ( 27, 34 ). Thus, patients who are similar in demographic and clinical characteristics may get different treatments depending on their surgeons. We found that the number of female breast cancer patients registered in the SEER Medicare database whose BCS was performed by a female surgeon has increased steadily since Patients who received radiotherapy were more likely to have had a female surgeon than those who did not. Furthermore, patients who received radiotherapy were more likely to have a surgeon who performed BCS on more than 15 other patients in the SEER Medicare database than those who did not. We also found that patients of physicians with more patients with claims for BCS in the dataset were more likely than other patients to receive adjuvant radiotherapy. Others have also found that surgical volume influences quality of care and outcomes ( 35, 36 ). Considering that medical graduates who were not trained in the United States represent approximately 25% of the US physician supply ( 37 ), surprisingly few studies have compared the performance of these medical graduates with that of US-trained graduates. Elderly women patients of medical school graduates trained outside the United States appear to have lower mammography referral rates than comparable patients of US-trained physicians, but this may reflect a difference in clinical decision making rather than patient preference ( 38 ). A study in Canada based on a large database found that the survival of patients with acute myocardial Male Female Total No. % No. % No. % P value Total Degree.02 MD DO US trained <.001 No Yes Decade of graduation <.001 Before After Type of practice <.001 Private Other No. of BCS procedures on patients in the cohort < > * A total of 4455 surgeons operated on the patients in the sample. MD = Medical Degree; DO = Doctor of Osteopathy; BCS = breast conservation surgery. P value based on chi-square test. infarction treated by graduates of medical schools outside of Canada was similar to that of patients treated by Canadian-trained physicians ( 39 ). We found no studies that investigated the quality of care of surgeons who were medical graduates of institutions outside the United States. Nonetheless, Moore and Rhodenbaugh ( 40 ) found that surgical residency programs discriminated against international medical graduates in their admissions. Virtually no research has compared allopathic and osteopathic physicians, although one Percent * 2001* 2002* % Female Surgeons Fig. 2. Percentage of female surgeons who performed breast cancer surgery by year of their patients breast cancer diagnoses recorded in the Surveillance, Epidemiology, and End Results (SEER) Medicare database between January 1, 1991, and December 31, 2002 (526 female surgeons, total surgeons). Asterisks denote the period ( ) in which the percentage of the population in SEER increased from 14% of the US population to 26% of the US population. jnci.oxfordjournals.org JNCI Articles 203

6 Table 3. Multivariable analysis of associations between receipt of radiotherapy and demographic, tumor, and surgeon characteristics among elderly patients who had breast conservation surgery for early-stage breast cancer * Characteristics OR (95% CI) P value Surgeon characteristics Degree DO 1.00 (Referent) MD 1.55 (1.25 to 1.93) <.001 US trained No 1.00 (Referent) Yes 1.12 (1.01 to 1.25).03 Type of practice Nonprivate 1.00 (Referent) Private 0.96 (0.88 to 1.05).38 No. of BCS procedures (Referent) > (1.08 to 1.28) <.001 Sex Male 1.00 (Referent) Female 1.13 (1.01 to 1.27).04 Patient demographic characteristics Age at diagnosis (Referent) (0.76 to 0.94) (0.49 to 0.60) < (0.12 to 0.15) <.001 Race White 1.00 (Referent) Black 0.74 (0.64 to 0.87) <.001 Hispanic 0.87 (0.66 to 1.16).34 Other 0.85 (0.71 to 1.01).06 Residence Metropolitan 1.00 (Referent) Nonmetropolitan 0.58 (0.51 to 0.67) <.001 Marital status Unmarried 1.00 (Referent) Married 1.48 (1.38 to 1.57) <.001 SES Lowest quintile 1.00 (Referent) 2nd quintile 1.17 (1.06 to 1.29) <.001 3rd quintile 1.20 (1.08 to 1.33) <.001 4th quintile 1.25 (1.13 to 1.40) <.001 Highest quintile 1.17 (1.05 to 1.29) <.001 Patient clinical characteristics Stage I 1.00 (Referent) II 0.87 (0.81 to 0.93) <.001 Hormone receptor status ER and PR 1.00 (Referent) Er+ and/or PR (0.86 to 1.07).46 Unknown 0.58 (0.51 to 0.66) <.001 Grade Poorly differentiated 1.00 (Referent) Well/moderately 0.98 (0.91 to 1.06).69 differentiated Unknown 0.85 (0.77 to 0.92) <.001 Received chemotherapy No 1.00 (Referent) Yes 1.47 (1.29 to 1.66) <.001 Comorbidity score (Referent) (0.71 to 0.81) <.001 > (0.48 to 0.57) <.001 * Each variable was corrected for the other listed characteristics and year of diagnosis. OR = odds ratio; CI = confidence interval; DO = Doctor of Osteopathic Medicine; MD = Medical Degree; BCS = breast conservation surgery; SES = socioeconomic status; ER = estrogen receptor; PR = progesterone receptor. P values from a Generalized Estimating Equations model. Table 4. Relative odds that a patients with stage I/II breast cancer would undergo radiation after breast conservation surgery given that the physician performing surgery was female (vs male), stratified by year of diagnosis * Year of diagnosis OR (95% CI) P value (0.90 to 1.27) (1.01 to 1.36).04 * Each model controls for age, year of diagnosis, race, hormone receptor status, socioeconomic status, breast cancer grade, marital status, comorbidity, physician characteristics, and physician volume. OR = odds ratio; CI = confidence interval. P values from a Generalized Estimating Equations model. small study found that osteopathic physicians were less likely to recommend cancer screening for their patients ( 41 ). In our study, controlling for patient, tumor, and surgeon characteristics, black women were still less likely than white women to receive post-bcs radiotherapy ( Table 3 ). Differences according to race have also been observed in the frequency of breast cancer screening practices ( 42, 43 ), the length of intervals between onset of symptoms and treatment for breast cancer ( 44, 45 ), and the stage at diagnosis ( 46, 47 ). In addition, the use of BCS vs mastectomy has been found to vary by geographic region, SES, and race/ethnicity in the United States ( ). In a recent analysis of SEER data, Joslyn et al. ( 51 ) reported that black women with early-stage breast cancer were less likely than white women to receive adjuvant radiotherapy. Another factor that may contribute to medical decision making is the gender and racial concordance between the physician and patient. Patients who are seen by a physician of their own race have reported more participatory decision making and more satisfaction than patients seen by a physician of a different race ( 52, 53 ). Women seen by a female physician have been observed to be more likely to undergo screening with Pap smears and mammograms than those seen by a male physician, particularly if the physician is an internist or family practitioner ( 54 ). Similarly, cancer-screening activity was higher among patients seen by medical doctors than those seen by doctors of osteopathic medicine ( 41 ). Female physicians were more likely than male physicians to ask new patients about components of prevention, to believe in the effectiveness of mammography, to feel personal responsibility for ensuring that their patients received screening, and to report comfort in performing Pap smears and breast examinations ( 55 ). Thus, it is clear that decision making involves a complex interaction between the physician and patient and their individual characteristics. Our study had a number of limitations. The SEER Medicare dataset that we used is population based, but it does not include data on variables that might also have been associated with receipt of radiotherapy, such as physical condition or performance status, psychological outlook, communication by the patient with her physician, or health behaviors. It also did not enable us to differentiate between lack of referral and patient refusal. In addition, the AMA Masterfile that we used did not provide information on the race/ ethnicity or board certification status of the surgeons. In addition, our study was limited to patients over the age of 65 and may not be generalizable to younger populations. Recent data 204 Articles JNCI Vol. 100, Issue 3 February 6, 2008

7 suggest that while the local recurrence rates are reduced, the survival benefits of adjuvant radiation may be attenuated in patients over the age of 70 with hormone receptor positive cancer treated with tamoxifen ( 56,57). These data were not known during the time period of our analysis, although some investigators may have anticipated that these were going to be the findings and acted accordingly. Because post-bcs radiation has been shown to reduce local recurrence as well as to improve both disease-free and overall survival in women with localized breast cancer ( 5, 58 ), it is recognized as an indicator of quality of care ( 7 ). Our finding of associations between this procedure and referring physician characteristics may therefore support other evidence that certain subgroups of breast surgeons have deficiencies in training or continued education and practice ( 59, 60 ). Moreover, breast cancer is not unique in this regard. In a survey of 30 health conditions ranging from osteoarthritis to breast cancer, McGlynn et al. ( 61 ) estimated that, on average, Americans received about half (54.9%) of the recommended medical care processes for basic care. Another limitation of our study was the use of odds ratios to characterize the relationship between surgeon characteristics and receipt of radiotherapy, controlling for other factors and correcting for clustering. The odds ratio is a good approximation of the relative risk when the outcome is rare but can be an overestimate when the outcome is common. Methods of calculating multivariable relative risks have been developed for studies of common outcomes ( 62, 63 ). No such method has been developed for use in hierarchical logistic models, where clustering has a substantial effect on the estimate. Bias occurs because these formulas proposed in other contexts fail to take into consideration the complex relationship between the outcome and exposure for each covariate pattern ( 64 ). In addition, the calculation does not consider the covariance between the estimated incidence and estimated odds ratio, and, therefore, the precision of the confidence intervals can be affected ( 64 ). It should be noted that it is likely that the true relative risks are slightly lower than the odds ratio we have reported, but they are unlikely to be dramatically different given the small overall effect sizes that we found ( Table 3 ). Our study is one of the first to demonstrate associations between certain surgeon characteristics and quality of breast cancer care, although the individual effect sizes were small for surgeon sex, location of training, and type of medical degree. Further research is essential to confirm these associations. 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JAMA ; 280 ( 19 ): McNutt LA, Wu C, Xue X, Hafner JP. Estimating the relative risk in cohort studies and clinical trials of common outcomes. Am J Epidemiol ; 157 ( 10 ): Funding American Society of Clinical Oncology Advanced Clinical Research Award (to D. L. H.); American Cancer Society (RSGT CPHPS to D. L. H., RSGHP PBP to V. R. G.); Department of Defense Breast Cancer Center of Excellence Award (BC043120). Notes This study used the linked SEER Medicare database. The analysis, interpretation and reporting of the data, writing of the manuscript, and decision to publish were the sole responsibility of the authors. The authors acknowledge the efforts of the Applied Research Branch, Division of Cancer Prevention and Population Science, NCI; the Office of Information Services, and the Office of Strategic Planning, HCFA; Information Management Services, Inc; and the SEER Program tumor registries in the creation of the SEER Medicare database. Manuscript received June 18, 2007 ; revised December 7, 2007 ; accepted December 17, Articles JNCI Vol. 100, Issue 3 February 6, 2008