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Characteristics of Urologists Predict the Use of Androgen Deprivation Therapy for Prostate Cancer

Vahakn B. Shahinian, Yong-fang Kuo, Jean L. Freeman, Eduardo Orihuela, James S. Goodwin

From the Department of Internal Medicine, University of Michigan, Ann Arbor, MI; and the Department of Internal Medicine, the Department of Preventive Medicine and Community Health, the Department of Surgery Division of Urology, and the Sealy Center on Aging, University of Texas Medical Branch, Galveston, TX

Address reprint requests to Vahakn B. Shahinian, MD, University of Michigan, 102 Observatory Rd, Simpson Memorial Institute Room 301, Ann Arbor, MI 48109-0725; e-mail: vahakn{at}umich.edu

	ABSTRACT

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Purpose We previously have reported wide variations among urologists in the use of androgen deprivation for prostate cancer. Using the Surveillance, Epidemiology, and End Results–Medicare linked database, we examined how individual urologist characteristics influenced the use of androgen deprivation therapy.

Methods Participants included 82,375 men with prostate cancer who were diagnosed from January 1, 1992, through December 31, 2002, and the 2,080 urologists who provided care to them. Multilevel analyses were used to estimate the likelihood of androgen deprivation use within 6 months of diagnosis in the overall cohort, in a subgroup in which use would be of uncertain benefit (primary therapy for localized prostate cancer), and in a subgroup in which use would be evidence-based (adjuvant therapy with radiation for locally advanced disease).

Results In the overall cohort of patients, a multilevel model adjusted for patient characteristics, tumor characteristics, and urologist characteristics (eg, board certification, academic affiliation, patient panel size, years since medical school graduation) showed that the likelihood of androgen deprivation use was significantly greater for patients who saw urologists without an academic affiliation. This pattern also was noted when the analysis was limited to settings in which androgen deprivation would have been of uncertain benefit. Odds ratios for use in that context were 1.66 (95% CI, 1.27 to 2.16) for urologists with no academic affiliation and 1.45 (95% CI, 1.13 to 1.85) for urologists with minor versus major academic affiliations.

Conclusion Use of androgen deprivation for prostate cancer varies by the characteristics of the urologist. Patients of non–academically affiliated urologists were significantly more likely to receive primary androgen deprivation therapy for localized prostate cancer, a setting in which the benefits are uncertain.

	INTRODUCTION

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Androgen deprivation therapy has become common for prostate cancer.^1,2 Although historically limited to palliation of metastatic prostate cancer, the 1990s witnessed a dramatic growth in the use of androgen deprivation across all stages and grades.¹

Part of the rise in use appeared to be evidence based. Androgen deprivation as adjuvant treatment with radiation for locally advanced or high-risk tumors was known to be beneficial for slowing the progression of prostate cancer as early as 1992.³ By 1996, clinical trial evidence of overall survival benefit was available⁴ and was reflected in the National Comprehensive Cancer Network (NCCN) guidelines of the time.⁵ In contrast, the use of androgen deprivation as primary therapy in localized disease was, and is, of uncertain benefit, because no clinical trials have demonstrated its efficacy in that context.⁶ Neither the NCCN nor the American Urological Association guidelines recommended androgen deprivation for localized prostate cancer,^5,7 yet its use for that indication more than tripled during the 1990s.^1,8

Considering the potential harms of androgen deprivation (eg, fractures, sexual dysfunction, reduced quality of life),⁹ its uncertain benefits in some settings, and its substantial financial costs,¹⁰ the wide geographic variations noted in its use are a cause for concern.^11,12 When examining the possible contribution of physician practice style to the variation in androgen deprivation use,¹³ we showed that which urologist a patient with prostate cancer sees is a more important predictor of receipt of androgen deprivation therapy than either tumor or patient characteristics.¹⁴

To further explore the role of the urologist, we examined the effect of individual urologist characteristics on the likelihood of androgen deprivation use in a large cohort of men with prostate cancer. We also performed subgroup analyses to test our hypothesis that a relationship would exist between urologist characteristics and the strength of the evidence for the indication of androgen deprivation therapy on the likelihood of its use. Specifically, we hypothesized that urologists with board certification and an academic affiliation would be more likely to prescribe androgen deprivation for patients when its use would be evidence-based and less likely to prescribe it for patients when its use would be of uncertain benefit.

	METHODS

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Data Sources
Surveillance, Epidemiology, and End Results-Medicare. The Surveillance, Epidemiology, and End Results (SEER) program consists of a group of population-based tumor registries in selected geographic areas of the United States.¹⁵ Medicare is a federal program that covers health services for 97% of people aged 65 years and older. The information in the two programs have been linked.¹⁶ The SEER-Medicare database also contains a hospital file that includes information on hospital characteristics, such as academic affiliation, and is derived from the Provider of Service survey submitted by hospitals to Medicare.¹⁷ The SEER-Medicare database version used for this study contains Medicare claims through 2004 and cancer cases from the SEER-11 registries through 2002.

American Medical Association (AMA) Physician Masterfile. The AMA Physician Masterfile contains information on all physicians in the United States regardless of membership in the AMA.¹⁸ The information is collected from primary sources, such as medical schools, residency training programs, state licensing agencies, and the American Board of Medical Specialties. Physicians are also surveyed every 3 years regarding their current practice.

Study Subjects
The study included men with incident prostate cancer from 1992 through 2002 who were at least 66 years old at diagnosis (163,613 patients). To ensure complete information, the following patients were excluded: those not enrolled in both Medicare Part A and Part B for 12 months before and 6 months after their cancer diagnosis (15,117 patients); those who died within 6 months of diagnosis (3,232 patients); those who were members of a health maintenance organization (36,640 patients); or those who were diagnosed by autopsy or on a death certificate (2,004 patients); 106,620 patients remained eligible.

Physicians providing care to patients within a year of diagnosis were initially identified through encrypted Unique Physician Identifier Numbers (UPIN) on Medicare physician claims. The UPINs were linked to the AMA Physician Masterfile, and only physicians with urology as their primary specialty code were selected. Patients who did not see at least one urologist in the year after diagnosis on at least 2 different days (14,635 patients) were excluded. If a patient saw two or more urologists, they were assigned to the urologist who saw them for at least 75% of urologist visits in the year after diagnosis. If no single urologist accounted for at least 75% of the visits, the patient was excluded (9,610 patients).

The primary analysis included all eligible patients, regardless of cancer stage or grade at diagnosis. To test whether the effect of urologist characteristics on the use of androgen deprivation was influenced by the strength of the indication for its use, we also performed analyses in two subgroups of patients: those for whom use of androgen deprivation therapy would have been evidence-based and those for whom its use would have been of uncertain benefit. Androgen deprivation together with radiation therapy was known to have salutary effects on disease progression since the early 1990s, although clinical trial evidence of overall survival benefit did not come until 1996 and later.^3-5,19,20 The evidence-based group of patients included those receiving radiation who had T3 or T4 tumors without regional or distant metastases (locally advanced) or who had T2 tumors with high-grade histology (localized but high risk) tumors (n = 6,300 patients; n = 1,112 urologists). The uncertain-benefit group included patients with T1 or T2 tumors who had either low- (Gleason score 2 to 4) or moderate- (Gleason score 5 to 7) grade histology and who did not receive radiation or radical prostatectomy (n = 18,211 patients; n = 1,393 urologists). This group was chosen because no clinical trial evidence of efficacy for primary androgen deprivation exists in this setting⁶ and because, even under theoretical considerations, it is difficult to show survival benefit from any intervention in such patients because of the slow natural progression and the competing risk of death from causes other than prostate cancer.²¹ In additional analyses, patients were stratified by era of diagnosis into a 1992-to-1995 period and a 1996-to-2002 period to examine changes in the effect of urologist characteristics over the study period.

Measures
Patient demographics and tumor characteristics were derived from the SEER records in the linked database and were used to categorize patients by age, ethnicity, SEER region of residence at the time of diagnosis, year of diagnosis, clinical stage (T1 through T4), and grade (well differentiated, Gleason 2 to 4; moderately differentiated, Gleason 5 to 7; un- or poorly differentiated or unknown, Gleason 8 to 10).²² The stage was assigned by using the SEER Extent-of-Disease classification system.²³ The socioeconomic characteristics of each patient were based on the percent of adults with less than 12 years of education and on the median income of the zip code of residence from the 2000 United States Census data. Comorbidity was measured using an adaptation of the Charlson Comorbidity Index for use with Medicare physician claims data.^24,25

Urologist board certification was available from the AMA, which was based on information from the American Board of Medical Specialties.¹⁸ Patient panel size was defined as the number of patients with prostate cancer assigned to each urologist over the study period and was categorized as less than 15, 15 to 59, 60 to 119, and 120 or more patients. These categories were prespecified and were chosen to ensure a reasonable distribution for the number of patients per panel, with cutoffs roughly corresponding to the second quartile, third quartile, and 90th percentile. Hospital affiliation with a medical school was available from the SEER-Medicare Hospital file and was categorized as none, minor affiliation, or major affiliation. Hospitals with a major affiliation play an important part in the teaching program of the medical school by hosting a clinical clerkship program, whereas those with a minor affiliation have only residency programs or occasional student rotations.²⁶ Urologists were categorized as having a major or no academic affiliation if all their inpatient Medicare claims submitted were from a hospital with a major or with no academic affiliation, respectively. All other urologists were categorized as having a minor academic affiliation. Some urologists could not be assigned an affiliation, because no inpatient claims were available for them (378 urologists; 594 patients), and were excluded from the main analyses. We performed a multiple imputation procedure²⁷ to examine the impact of the missing data and found that the results were not substantially changed (data not presented).

The outcome was receipt of androgen deprivation. Androgen deprivation was defined as the receipt of at least one dose of a gonadotropin-releasing hormone (GnRH) agonist (identified through Medicare claims codes used to designate each dose given of injectable medications^1,28) or of orchiectomy (defined by the presence of the Current Procedural Terminology codes or International Classification of Diseases [ninth revision] procedure codes in the Medicare claims) in the first 6 months following the diagnosis of cancer. As such, the study was limited to examining early use of androgen deprivation without consideration for whether patients received androgen deprivation later in their course.

Statistical Analyses
Differences across strata of urologist characteristics in the proportion of patients receiving androgen deprivation were evaluated with ² statistics. The effect of urologist characteristics on the outcome of androgen deprivation use was evaluated using hierarchical, generalized linear models.^29,30 These models accounted for the clustering of patients within urologists. Models entering the urologist, patient, and tumor characteristics listed above as independent variables were estimated. Odds ratios (ORs), along with 95% CIs, for the use of androgen deprivation for each urologist characteristic were calculated. The median urologist rates of androgen deprivation use for various indications were estimated from the models and were plotted by the calendar year of diagnosis to show a change in use over time.

Analyses were performed with SAS version 9.1 (SAS Institute, Cary, NC). All tests of statistical significance were two-sided, and P < .05 was considered significant. The study protocol was approved by the local institutional review board at the University of Texas Medical Branch at Galveston (Galveston, TX).

	RESULTS

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A total of 2,080 urologists were identified as providing care to 82,375 patients with incident prostate cancer from 1992 through 2002. A majority of urologists were board certified (93.5%), did not have a major academic affiliation (81.5%), and were male (97.8%). Table 1 presents the proportion of patients receiving androgen deprivation within 6 months of diagnosis by strata of urologist characteristics. Overall, 34.4% of patients received androgen deprivation, 5.2% received orchiectomy, and 29.2% received GnRH agonists. A total of 25.7% of urologists provided care to 60 or more patients with incident prostate cancer during the study period. In the overall cohort, a greater proportion of the patients of younger, female, non–board-certified, and non–major academically affiliated urologists received androgen deprivation.

View larger version (14K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 1. Urologist-specific rates of androgen deprivation use in the evidence-based group of patients, adjusted for patient characteristics, were estimated from hierarchical, generalized linear models for each era of diagnosis (1992 to 1993, 1994 to 1995, 1996 to 1997, 1998 to 1999, and 2000 to 2002). The median urologist-specific rates for urologists with a major versus no academic affiliation were plotted for each era of diagnosis. ADT, androgen-deprivation therapy.

View larger version (13K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 2. Urologist-specific rates of androgen deprivation use in the uncertain-benefit group of patients, adjusted for patient characteristics, were estimated from hierarchical, generalized linear models for each era of diagnosis (1992 to 1993, 1994 to 1995, 1996 to 1997, 1998 to 1999, and 2000 to 2002). The median urologist-specific rates for urologists with a major versus no academic affiliation were plotted for each era of diagnosis. ADT, androgen-deprivation therapy.

	DISCUSSION

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How did our findings compare with our initial hypotheses? Patients of non–board-certified urologists were significantly more likely to receive androgen deprivation in the uncertain-benefit group in unadjusted analyses (Table 1), though this finding did not achieve statistical significance in the multivariable analyses (Table 4). The increased use of androgen deprivation by non–board-certified urologists in the evidence-based group from 1992 to 1995 is difficult to explain, although this effect was abolished in the period from 1996 to 2002. The effect of the urologist academic affiliation on evidence-based use showed an interesting pattern (Fig 1). The greater use of androgen deprivation in this context by academic urologists from 1992 to 1995 is consistent with what is known about early adopters, who tend to be providers who are involved in the testing of new therapies.³¹ Following publication of the clinical trials, use in this setting increased dramatically for all groups of urologists but at a significantly higher rate for urologists without academic affiliation. This may result from more cautious or selective use of androgen deprivation by academic urologists in response to the evidence.³² In addition, factors other than evidence of benefit may have influenced the use of androgen deprivation by urologists without an academic affiliation. Financial incentive might play a greater role for non–academically affiliated urologists, who more likely may be paid on a fee-for-service, rather than a salaried basis. Through the 1990s, androgen deprivation use in the form of GnRH agonists allowed a substantial profit for every dose administered and formed a substantial portion of private-practice urologist income.^33,34 Physicians in academic settings may have more time for a discussion of risks and benefits, which could lead to lower use of androgen deprivation in settings where its benefits are uncertain.³² Finally, academic physicians may be less influenced by the pharmaceutical industry marketing of GnRH agonists.³⁵

There are limitations to this study. Only men 66 years and older were included, and use of androgen deprivation in health maintenance organizations could not be examined. Some study exclusions may have limited the generalizability of the results. For instance, some patients receiving care from multiple urologists were excluded (nearly 10% of our initial study sample). The unadjusted rate of androgen deprivation use among those patients was 37% v 34% in the final study sample. Despite the population-based nature of the study, statistical power was limited for some of the stratified analyses, which rendered CIs too wide for meaningful interpretation of some results. Assignment of the urologist academic affiliation based on Medicare claims may have been imperfect. However, misclassification would tend to bias the results to the null so that significant associations should still be valid. Finally, some potentially relevant variables, such as prostate-specific antigen levels, were not available. However, after adjustment for other important tumor variables such as stage and grade, it is unlikely that there would be substantial differences in prostate-specific antigen levels across urologist characteristics. Furthermore, it might be expected that patients with higher-risk disease would tend to see academically affiliated urologists. This should have led to more, rather than the less, use of androgen deprivation noted among academically affiliated urologists in this study.

What implications do our study findings have for optimizing the use of androgen deprivation therapy? First, the use of androgen deprivation in settings of uncertain benefit was common even among urologists with a major academic affiliation (Table 1). If all patients with prostate cancer saw academic urologists, there would be only an estimated 10.5% reduction in the number of patients who would be prescribed androgen deprivation in settings of uncertain benefit. Nevertheless, the significant associations noted in this study between urologist characteristics and the use of androgen deprivation provide insight into what efforts may be successful for improving the use of this therapy. The effects of academic affiliation suggest that provider education should be a priority. Current practice guidelines for the management of prostate cancer may not be sufficient. For example, the NCCN guidelines on the management of prostate cancer are primarily composed of algorithms that describe current standards of care.⁵ Use of boundary guidelines, which specifically define appropriate and inappropriate use of therapy, may be more helpful.³⁶ Ongoing clinical trials should eventually help clarify the optimal role of androgen deprivation therapy, possibly reducing variations in its use.^37,38 In addition, the reductions in reimbursement for GnRH agonists brought about by the Medicare Modernization Act in 2003 should help reduce discretionary use of androgen deprivation. Some discretion in the use of androgen deprivation in settings where its benefits are uncertain is expected, and use in that context may not necessarily be inappropriate. Nevertheless, the significant differences in androgen deprivation use as a function of urologist characteristics are cause for concern. Efforts directed at reducing variations in the use of androgen deprivation therapy among urologists are needed.

	AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

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The authors indicated no potential conflicts of interest.

	AUTHOR CONTRIBUTIONS

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Conception and design: Vahakn B. Shahinian, Yong-fang Kuo, Jean L. Freeman, Eduardo Orihuela, James S. Goodwin

Financial support: Vahakn B. Shahinian, Jean L. Freeman, James S. Goodwin

Collection and assembly of data: Yong-fang Kuo

Data analysis and interpretation: Vahakn B. Shahinian, Yong-fang Kuo, Jean L. Freeman, Eduardo Orihuela, James S. Goodwin

Manuscript writing: Vahakn B. Shahinian, James S. Goodwin

Final approval of manuscript: Vahakn B. Shahinian, Yong-fang Kuo, Jean L. Freeman, Eduardo Orihuela, James S. Goodwin

	ACKNOWLEDGMENTS

 
We thank the Applied Research Program, National Cancer Institute; the Office of Research, Development and Information, Centers for Medicare & Medicaid Services; Information Management Services Inc; and the Surveillance, Epidemiology, and End Results (SEER) Program tumor registries in the creation of the SEER-Medicare database.

	NOTES

 
Supported in part by Public Health Service Grants No. RO1CA116758, P50CA105631, and R24HS011618. The funding bodies had no role in data extraction and analyses, in the writing of the manuscript, or in the decision to submit the manuscript for publication.

This study used the linked Surveillance, Epidemiology, and End Results (SEER)–Medicare database. The interpretation and reporting of these data are the sole responsibility of the authors.

Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.

	REFERENCES

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Submitted November 14, 2006; accepted July 27, 2007.

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