Background
With insufficient high-quality evidence to identify an optimal prostate cancer treatment modality,1 preferences of individual physicians can significantly affect management decisions of this disease. The NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines) for Prostate Cancer2 include radiation therapy as a treatment option for men with locoregional prostate cancer (to view the most recent version of these guidelines, visit NCCN.org). Many patients seek information and recommendations from urologists and radiation oncologists,3 the 2 most common specialists providing prostate cancer care.4 Urologists generally act as both diagnosticians (eg, diagnosing prostate cancer after performing diagnostic core needle biopsy) and proceduralists (eg, performing radical prostatectomy). In contrast, radiation oncologists usually act solely as proceduralists (eg, administering radiation therapy) during prostate cancer treatment. In the United States, urologists perform biopsies for patients with suspected prostate cancer and are generally the first physicians to discuss further diagnostic, treatment, and referral options.
A study comparing recommendations by urologists and radiation oncologists found that physicians overwhelmingly recommended therapy that they themselves deliver.5 Likewise, studies have reported a strong correlation between specialty seen and initial treatment received by patients with prostate cancer.3,4,6 Physicians play a major role in influencing patients’ treatment decisions.7,8 Multiple studies have indicated that physician characteristics are important determinants of referral patterns.9–13
This study examined urologists’ characteristics as determinants of radiation oncologist consultation for patients with locoregional prostate cancer.
Methods
Data Sources
Incident locoregional prostate cancer cases for 2004 through 2007 were selected from the SEER-Medicare database that links cancer registry information in selected US geographic areas with claims for covered health care services of Medicare beneficiaries (Figure 1). The SEER program represents 26% of the US population, whereas Medicare covers health services for 97% of people aged 65 years and older.14,15 Approximately 94% of SEER patients aged 65 years or older have been successfully linked with their Medicare claims.14,15 Geographic areas selected for inclusion in the SEER program are based on their ability to operate and maintain a high-quality, population-based cancer reporting system and for their
Definition of study cohort of 39,934 men with locoregional prostate cancer.
Abbreviations: AMAPM, American Medical Association Physician Masterfile; HMO, health maintenance organization.
aExact prostate-specific antigen levels at time of diagnosis were recorded in SEER from 2004, and up until 2007, Medicare files used Unique Physician Identification Numbers that are required to link with the AMAPM.
Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 13, 3; 10.6004/jnccn.2015.0042
Definition of study cohort of 39,934 men with locoregional prostate cancer.
Abbreviations: AMAPM, American Medical Association Physician Masterfile; HMO, health maintenance organization.
aExact prostate-specific antigen levels at time of diagnosis were recorded in SEER from 2004, and up until 2007, Medicare files used Unique Physician Identification Numbers that are required to link with the AMAPM.
Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 13, 3; 10.6004/jnccn.2015.0042
Definition of study cohort of 39,934 men with locoregional prostate cancer.
Abbreviations: AMAPM, American Medical Association Physician Masterfile; HMO, health maintenance organization.
aExact prostate-specific antigen levels at time of diagnosis were recorded in SEER from 2004, and up until 2007, Medicare files used Unique Physician Identification Numbers that are required to link with the AMAPM.
Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 13, 3; 10.6004/jnccn.2015.0042
Characteristics of physicians who treated SEER-Medicare patients were obtained from the AMAPM. This file contains physician information collected from multiple sources, including medical schools, state licensing boards, and the American Board of Medical Specialties (ABMS).17
Guidelines, published annually by NCCN since 1996 and throughout the study period, have consistently recommended radiation as a possible initial treatment option for locoregional prostate cancer (any T, any N, M0).18–24
An analytical cohort of patients with an index urologist was created using registry-claims linked data. Urologists perform core needle biopsies (Healthcare Common Procedure Coding System code 55700) to diagnose prostate cancer.25,26 The urologist who performed the biopsy on the day closest to the patients’ diagnosis date in SEER was assigned as the index urologist. Patients diagnosed with prostate cancer without undergoing biopsy, received their biopsy from a non-urologist, or had multiple biopsies performed by different urologists on the day closest to the patients’ diagnosis date were removed. These exclusions create a more homogenous population in terms of treatment selection.
Institutional Review Board approval was obtained from Emory University and Morehouse School of Medicine.
Patient Characteristics
Sociodemographic and clinical characteristics of the analytic cohort were extracted from SEER data (see supplemental eTable 1, available with this article at JNCCN.org). For tumor grade, low corresponds to Gleason grade 2 through 4; intermediate to Gleason grade 5 through 6, and high to Gleason grade 7 through 10.27 Education and income levels were based on US Census tract data from 2000; the categories chosen were prespecified to ensure a reasonable distribution, with cutoffs approximately corresponding to quartiles. The prevalence of comorbid disease in the study cohort was calculated using a modified Charlson comorbidity index derived from Medicare Part A and Part B claims.28
Urologist Characteristics
Urologists were identified by using either the Health Care Financing Administration (HCFA) specialty codes in Medicare claims, the physician specialty information from the AMAPM, or the urology board certification identified through the ABMS information within the AMAPM. Other urologist characteristics extracted from the AMAPM can be found in supplemental eTable 1). Urologists’ patient volume was defined as the number of unique patients with prostate cancer that each urologist saw during the study period. Categories used for urologists’ patient volume, age, and years after medical school graduation were prespecified to ensure cutoffs approximating quartiles.
Physician Medical School Affiliation
Urologists’ medical school affiliation was derived from the SEER-Medicare Hospital (HOSP) file.29 Specifically, if the Medicare biopsy claim recorded in the institutional outpatient standard analytical file (OUTSAF) was submitted from a hospital with a major or without a medical school affiliation (as defined within the HOSP file), the associated index urologist was categorized as having a major or no medical school affiliation, respectively. Index urologists were categorized as having mixed medical school affiliations if the OUTSAF biopsy claims were from hospitals with limited or graduate medical school affiliations.30
Biopsy claims found within the National Claims History (NCH) file (consisting of mostly noninstitutional physician/supplier claims) did not have the associated provider (eg, hospital) identifier required to retrieve medical school affiliation (found within HOSP) for the index urologist. These NCH claims were assigned the provider identifier associated with the institutional inpatient Medicare Provider Analysis and Review (MEDPAR) claims if (1) the patient associated with both types of claims matched, (2) the NCH place of service was institutional,31 and (3) the NCH claims dates fell between the MEDPAR admission and discharge dates.
Subsequently, remaining NCH biopsy claims without assigned provider identifiers from MEDPAR claims were assigned provider identifiers from OUTSAF claims if (1) the patient and urologist associated with both claim types matched, (2) the NCH place of service was institutional,31 and (3) the NCH claims dates were between the OUTSAF claims dates. Urologists whose biopsy claims were only found in the NCH file and whose claims could not be assigned provider identifiers from OUTSAF or MEDPAR claims were categorized as having a noninstitutional affiliation.
Measurement of Outcomes
Whether the patient had a radiation oncologist consultation after being diagnosed with locoregional prostate cancer was the primary dichotomous outcome. Radiation oncologists were identified using either HCFA specialty codes, AMAPM’s physician specialty information, or ABMS radiation oncology board certification information. Patients were categorized as having radiation oncologist consultations if at least one radiation oncologist-associated Medicare claim was identified within 9 months after locoregional prostate cancer was diagnosed. A 9-month interval was selected to ensure sufficient time for multidisciplinary consultations with specialists before treatment selection4 and to minimize the possibility of significant cancer progression. A total of 568 patients who underwent prostatectomy before radiation oncologist consultation were excluded in the outcome measurement. As part of a sensitivity analysis to examine the impact of these consultations as potentially part of adjuvant radiation therapy, these patients were included in the outcome measurement but the results were not substantially changed (unpublished data, 2014).
Statistical Analyses
Differences in the proportion of patients consulting radiation oncologists across index urologists and patient characteristics were evaluated using chi-square tests. The effect of patient and urologist characteristics on the likelihood of a subsequent radiation oncologist consultation was assessed with logistic hierarchical generalized linear mixed models32 (GLMM) and estimated using restricted pseudo-likelihood methodology.32–34 The use of hierarchical GLMM accounted for possible clustering of subsequent radiation oncologist consultation among patients who had the same index urologist for diagnostic biopsy.29,35–37 The unit of analysis was the patient. The clustering variable was the index urologist associated with each patient. Univariate and adjusted multivariate odds ratios (ORs) and 95% CIs for the radiation oncologist consultation were calculated for each patient and urologist characteristic (supplemental eTable 2). Variables used in the adjusted model were selected a priori and based on previous studies that investigated the influence of patient and physician characteristics on clinical referral patterns.12,38
All statistical testing was 2-sided, performed at 5% significance level, and used SAS version 9.3 (SAS Institute, Cary, NC).
Results
The SEER-Medicare database contained 39,934 men diagnosed with incident locoregional prostate cancer from 2004 to 2007 who met study eligibility criteria. A total of 2405 urologists performed diagnostic biopsies on these patients, and were predominantly male (96.8%), board certified (93.4%), had patient volumes across the study period of fewer than 37 (60.5%), were trained in the United States (84.4%), and had an MD (97.6%) as opposed to a DO degree (supplemental eTable 3).
Overall, 24,549 (61.5%) patients consulted a radiation oncologist within 9 months after diagnosis (supplemental eTable 1). Radiation oncologist consultations were less common among patients who were aged 80 years or older; of Hispanic ethnicity; unmarried; residing in SEER areas covering Iowa, New Mexico, or Utah; and residing in census tracts with lower educational and median incomes levels. Consultations were also less common among patients with higher levels of comorbidities, tumor stages higher than T1, PSA levels greater than 20 ng/mL, low tumor grade, and/or positive regional lymph nodes. Index urologists treating patients who consulted radiation oncologists were more likely to be older than 57 years, have a patient volume of fewer than 37, be trained in the United States, and/or have a mixed medical school affiliation.
Using hierarchical GLMM, factors associated with patients’ subsequent radiation oncologist consultation after diagnosis were investigated, while controlling for multiple patients being diagnosed by the same urologist (supplemental eTable2). Unadjusted univariate ORs showed that lower propensities to consult radiation oncologists are associated with patients who were aged 80 years or older; of Hispanic ethnicity compared with white; were unmarried; residing in California, Detroit, Iowa, Kentucky, New Mexico, Seattle, or Utah as opposed to Georgia; and residing in census tracts with lower educational and/or median income levels. A significantly smaller association with radiation oncologist consultation was also observed for patients with higher levels of comorbidities (ie, comorbidity index ≥3 vs 0), clinical stage T2–T4 versus T1, regional lymph node metastasis stage N1 versus N0, low versus high tumor grade, and higher PSA levels. The index urologists for patients who subsequently consulted radiation oncologists were significantly more likely to have noninstitutional affiliations (OR, 1.21; 95% CI, 1.02–1.43; P=.03).
After the multivariate adjustment for patient and urologist characteristics, patients whose index urologists had noninstitutional affiliations (OR, 1.40; 95% CI, 1.17–1.67; P=.0002) as opposed to major medical school affiliations were significantly more likely to have a subsequent radiation oncologist consultation. In addition, patients who subsequently consulted radiation oncologists were also significantly more likely to be diagnosed by index urologists older than 57 years (OR, 1.21; 95% CI, 1.07–1.38; P=.003) and/or significantly less likely to be diagnosed by index urologists with patient volumes between 37 and 54 (OR, 0.88; 95% CI, 0.78–1.00; P=.049) as opposed to fewer than 37. Patient characteristics that remained significantly associated with lower odds of radiation oncologists consultation included age of 80 years or older; Hispanic ethnicity versus white; SEER region of residence in California, Iowa, or Utah as opposed to Georgia; residence in census tracts with lower educational levels; clinical stage T2–T4 versus T1; lower tumor grade; and PSA levels greater than 20.0 ng/mL compared with 0.1 to 9.9 ng/mL.
Discussion
To our knowledge, this is the first study to investigate the association of urologists’ characteristics on the likelihood of subsequent radiation oncologist consultation by men diagnosed with locoregional prostate cancer. The index urologists’ age, patient volume, and noninstitutional practice affiliation exerted a significant influence on patients’ subsequent radiation oncologist consultations. Similar radiation oncologist consultation patterns were found among patients diagnosed by institutional-affiliated urologists regardless of medical school affiliation level (major/mixed). Other significant associations found between patient-related sociodemographic and clinical factors and radiation oncologist consultations complement prior research.4
Significant associations with urologist age may be a result of younger urologists being keener to act as proceduralists and not actively referring their patients to radiation oncologists. In addition, older urologists may not feel the need to perform multiple procedures, and prefer the added value of a radiation oncologist consultation.
Physician practice settings are known to be associated with variation in primary treatment of prostate cancer39; inherent differences may exist between physicians practicing within major medical schools and those in noninstitutional settings that may explain observed variations. One possible reason major medical school–affiliated urologists refer less often may be related to the teaching nature of their institutions. Urologists affiliated with major medical schools may potentially want to reserve patients for their residents and fellows to perform surgery.
Given the rising prevalence of expectant management approaches during this study period,39 many of the patients who did not consult a radiation oncologist may have opted for active surveillance or watchful waiting. Current NCCN Guidelines2,40,41 recommend active surveillance for low-risk patients with an expected survival of less than 10 years and very-low-risk patients with an expected survival of less than 20 years (to view the most recent version of these guidelines, visit NCCN.org). However, during this study period, NCCN Guidelines18–24 allowed for expectant management or radiation therapy as possible treatment options for low-risk patients with an expected survival of less than 10 years. A significant proportion (27%–69%) of the study’s patients aged 75 years or older (with an expected survival ≈<10 years)42 had a radiation oncologist consultation. Based on current NCCN Guidelines,2 future research should investigate whether radiation oncologists should discuss treatment options with all of these patients. In addition, uncertainty surrounds the threshold for reclassifying prostate cancer from low risk to higher risk, which would trigger a physician recommendation for active treatment.40 Ongoing randomized clinical trials43 will further inform this important management decision and the need for multiple specialty consultations.
Physicians working for academic health providers are more commonly remunerated through a salary-only payment mechanism rather than a fee-for-service (FFS) model.44 Previous research has shown that different payment mechanisms influence clinical decision-making45 and physician behavior is significantly different under salaried versus FFS reimbursement models. A previous study concluded that, regarding inappropriate androgen deprivation therapy use, financial incentives might have played a lesser role for major medical school–affiliated urologists, because they were more likely to be salaried.36 In another recent study, urologists employed by NCCN Member Institutions (generally major medical school–affiliated institutions) were unlikely to derive financial benefits from recommending specific treatments such as intensity-modulated radiation therapy (IMRT).26
SEER-Medicare data limitations preclude direct ascertainment of individual physicians’ payment mechanisms (ie, salaried vs nonsalaried) and self-referral confirmation (ie, that the radiation oncologist and index urologist worked within the same practice; and that the urologist had a financial interest in the referral). Nonetheless, a 2012 report by the US Government Accountability Office (GAO) that investigated advanced imaging self-referral concerns noted that “financial incentive for providers to self-refer is most direct when the service is performed in a physician office.”46 In our study, as expected, greater than 90% of patients diagnosed by noninstitutional-affiliated urologists received biopsies in physician office settings. The GAO report also found that between 2004 and 2010, the greatest increase in CT self-referral rates occurred among urology and radiation oncology providers.46 Our findings may shed further light on the determinants of radiation oncologist consultations before IMRT self-referrals that were reported in another 2013 GAO report.47
We acknowledge other important study limitations when using the SEER-Medicare database.14,15,17 Multiple physician characteristics (eg, intrinsic motivation, professionalism, altruism) not measured in this study may influence practice patterns or response to financial incentives.48–52 Medicare claims–based categorization of medical school affiliation may be influenced by other patients seen (eg, younger patients, those with private insurance, and/or receiving care in health maintenance organizations). Therefore, our study observations may not be representative of the physicians’ entire practice. Nonetheless, 79% of men with incident prostate cancer are aged 65 years or older,53 and in 2010, 76% of Medicare beneficiaries were covered under traditional FFS.54 Medicare claims–based categorization of physicians’ medical school affiliation has also been used in previous literature.29,30,36,37
Whether a patient sees a radiation oncologist is likely influenced by many other factors. Individual patient selection biases not assessed may have led to variability in observations. Whether the present observations reflect urologists’ referral decisions or patients’ individual choices is unclear. Nonetheless, previous studies55,56 suggest that patient preference is unlikely to entirely explain the observed radiation oncologist consultation patterns. Further research is necessary to confirm whether subsequent radiation oncologist consultations reflect index urologist referral behavior, patient response, or urologist-patient interactions. Future studies should also examine subsequent urologist consultation after diagnosis and the association of physicians’ (both urologist and radiation oncologist) characteristics on the eventual treatment received by patients with prostate cancer.
Without a gold standard for prostate cancer treatment, urologists’ recommendations and referrals can be crucial in determining eventual treatment. Inherent differences in specialty-related treatment recommendations5,6 underscore the importance of obtaining second opinions from different types of specialists before selecting a specific treatment modality. Nevertheless, variation observed in this study should ideally be from the collective preferences and consents of well-informed patients and patient-centered clinical judgment of their physicians.
The authors have disclosed that they have no financial interests, arrangements, affiliations, or commercial interests with the manufacturers of any products discussed in this article or their competitors. This study was supported by the American Cancer Society, Intramural Research Department, Atlanta, Georgia.
The authors acknowledge the efforts of the Applied Research Program, Division of Cancer Control and Population Sciences, NCI; the Office of Research, Development and Information, Centers for Medicare & Medicaid Services; Information Management Services, Inc; and the SEER Program tumor registries in the creation of the SEER-Medicare database.
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