Affiliation of authors: D. Schrag, L. J. Hsieh, P. B. Bach, C. B. Begg (Department of Epidemiology and Biostatistics), F. Rabbani, H. Herr (Department of Urology), Memorial Sloan-Kettering Cancer Center, New York, NY.
Corresponding author: Deborah Schrag, M.D., M.P.H., Health Outcomes Research Group, Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021 (e-mail: schragd{at}mskcc.org).
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ABSTRACT |
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INTRODUCTION |
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Because of this high risk of recurrence, the recommendation for patients diagnosed with superficial bladder cancer has, since the 1970s, been bladder surveillance by frequent follow-up cystoscopic examinations. For example, current guidelines from the American Urologic Association (10) and the National Comprehensive Cancer Network (11), as well as reviews and case series in the urology literature (1216), recommend that patients with superficial bladder cancer (i.e., TNM stages TaN0M0, TisN0M0, or T1N0M0) receive cystoscopic surveillance at least every 36 months for the first 3 years after diagnosis and at least annually thereafter. Depending on the number and size of lesions, the depth of invasion, and the number of prior tumors, intravesical therapy may also be recommended but does not obviate the need for ongoing bladder surveillance (17,18).
We hypothesized that, because bladder surveillance is arduous, actual clinical practice with regard to surveillance would fall short of these guidelines. We therefore sought to identify patient and physician characteristics that are associated with low adherence to surveillance guidelines, to report practice patterns, and to encourage thoughtful evaluation of surveillance practice.
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METHODS |
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We identified a cohort of patients with superficial bladder cancer through linkage of the population-based Surveillance, Epidemiology, and End Results (SEER)1 Program cancer registries with the Medicare database of the Center for Medicare Service (CMS), which contains health care claims for Medicare enrollees. The SEER registries, which are sponsored by the National Cancer Institute, ascertain all incident cancer cases that are diagnosed in five states and six U.S. metropolitan areas, which contain approximately 14% of the U.S. population (19). SEER collects the following information on each incident cancer: primary site and histology as classified according to the International Classification of Disease for Oncology, 2nd edition (ICD-O-2) (20), tumor stage at diagnosis, and patient demographics. The Medicare program provides health insurance for 97% of the U.S. population aged 65 years or older. Medicare Provider Analysis and Review (MEDPAR) files provide details of all hospitalizations for persons eligible for Medicare Part A. For the 96% of Medicare beneficiaries who opt for Part B coverage, claims for care delivered in hospital outpatient departments and physicians offices are recorded in the outpatient and physician/supplier Medicare files. The SEER and Medicare data have been linked to facilitate population-based studies of cancer treatment. Ninety-four percent of patients in SEER aged 65 years or older have been successfully linked to their Medicare records (21).
Cohort Definition
All Medicare-enrolled patients aged 65 years or older who were diagnosed with primary superficial bladder cancer in one of the geographic areas covered by SEER from 1992 through 1996 were potentially eligible for inclusion in our study. All eligible patients were enrolled in both parts A and B of Medicare and had 36 months of follow-up data available. Patients enrolled in risk-contract health maintenance organizations (HMOs) were excluded from our study because claims that detail their care are not reported to CMS. During the study years, 16% of superficial bladder cancer patients were enrolled in an HMO at diagnosis.
Bladder cancers were defined using SEER codes 67.067.9 for cancer sites. We restricted our cohort to patients who were diagnosed with transitional cell tumors (SEER histology codes 8020, 8021, 8050, 8051, 8052, 8120, 8122, and 8130). Patients whose diagnoses were noted postmortem were excluded. We further selected patients who were diagnosed with superficial disease (stages Ta, Tis, or T1) by using information recorded in SEER on tumor size, lymph node involvement, and distant spread.
We searched Medicare inpatient, outpatient, and physician claims to identify patients who had at least one procedure for the diagnosis and/or treatment of superficial bladder cancer performed within 6 months of the diagnosis date recorded in SEER. These procedures were identified on the basis of International Classification of Diseases, 9th Revision (ICD-9) (22) codes and Current Procedural Terminology (CPT) systems for coding procedures on Medical claims (23). All codes for procedures that might conceivably have been accompanied by visualization of the bladder were included. The Appendix contains a complete list of the codes and procedure names.
Patients who had died or who had a total cystectomy at any point during the study follow-up period were excluded from our analyses because surveillance is only warranted for patients as long as they have bladder mucosa at risk of recurring disease. Total cystectomies were identified on the basis of ICD-9 code 57.7 and CPT codes 51570, 51575, 51580, 51585, 51590, 51595, 51596, and 51597. We identified 6925 patients from our inception cohort (N = 9320) who had survived for at least 3 years after being diagnosed with superficial bladder cancer and had evidence of initial treatment for bladder cancer recorded in Medicare files. After excluding 208 patients who had a total cystectomy during the follow-up period, the 6717 patients that remained had superficial bladder cancer, an index diagnostic procedure for superficial bladder cancer, and bladder mucosa at risk for recurring disease for 36 months after diagnosis. Patients who had a partial cystectomy (ICD-9 code 57.6 and CPT codes 5155051565) in an attempt to preserve the bladder (N = 119) were included in our study because they still require ongoing surveillance of the residual bladder mucosa.
Identification of Surveillance
The primary outcome of our study was having low-intensity bladder surveillance, which was defined as having an examination of the bladder during fewer than two of the five contiguous 6-month intervals from month 7 through month 36 following a diagnosis. We chose this 30-month window because complete follow-up data for this interval were available from Medicare files. Because patients may undergo several diagnostic or therapeutic cystoscopic procedures as part of their initial evaluation and treatment, all bladder-related procedures recorded in the SEER database that were performed within 6 months of the date of diagnosis were ascribed to initial diagnosis and treatment and thus were not considered in our definition of low-intensity surveillance. We divided the period from month 7 through month 36 after diagnosis into five discrete 6-month follow-up intervals: months 712, months 1318, months 1924, months 2530, and months 3136. We reasoned that patients who were adherent to the recommended frequency of surveillance (at least once every 6 months) should have had at least one claim on record for a follow-up examination evident in each of the five follow-up intervals.
To estimate rates of adherence, we counted any procedure that conceivably could have involved evaluation of the bladder as one that was indicative of surveillance. For example, we assumed that a patient who had a claim for a transurethral prostate resection would have had a bladder inspection at the same time. Similarly, we assumed that intravesical installation of chemotherapy was accompanied by visualization of the bladder.
Patient Characteristics
We ascertained a patients race, sex, age at diagnosis, year of diagnosis, and reporting registry from SEER data. A patients socioeconomic status was approximated by using the median income in the census tract in which the patient resided; patients who lived in urban areas were ascertained on the basis of Metropolitan Statistical Areas defined by the U.S. Census Bureau. We used a modification by Romano et al. (24) of the comorbidity index developed by Charlson et al. (25) (i.e., the CharlsonRomano comorbidity index) to adjust for potential confounding that was based on the severity of non-cancer medical illness: all available inpatient Medicare claims for the 12-month interval preceding 1 month prior to diagnosis were examined and patients were assigned the maximal comorbidity observed. However, because this method does not capture comorbid illness that is treated in the outpatient setting, we also used a comorbidity index developed by Klabunde et al. (26) specifically for use with outpatient Medicare claims.
Physician Characteristics
To examine associations between physician characteristics and surveillance patterns, we identified the physician who performed the initial bladder cancer diagnostic procedure within 6 months of diagnosis for each cohort member. We accomplished this by using the Unique Physician Identifier Number (UPIN) that was included in the Medicare claims files. When a patient had more than two procedures, we assigned that patient to the physician who performed the greatest number of procedures on that patient. When a patient had two urologic procedures performed by two different physicians, we selected the physician who performed the second procedure, on the theory that the provider who had the most recent contact with the patient was likely to exert the greatest influence on that patients surveillance behavior.
We also used the UPIN to characterize physicians according to the total number of Medicare patients with superficial bladder cancer they evaluated. (This measure of case volume does not reflect the absolute number of patients seen by a physician because it excludes patients younger than 65 years and those enrolled in managed care plans.) To more fully characterize the physicians who rendered care to cohort members, we used data from the 1998 American Medical Association (AMA) Physician Masterfile, in which characteristics of licensed U.S. physicians are described. Linkage between the AMA Masterfile and the Medicare claims was accomplished using UPINs, which are recorded in both files. Patients for whom no UPIN was recorded for the index procedure (1.5%) or whose doctors UPIN was missing from the Masterfile (1.0%) were excluded (n = 171) from the analysis of physician characteristics in relation to surveillance. We could not examine the association between hospital characteristics and patients surveillance behavior because superficial bladder cancer does not usually require hospitalization.
Statistical Analysis
To assess the associations between surveillance for superficial bladder cancer and patient and physician characteristics, we first evaluated each variable in a univariate analysis. Tumor stage and histologic grade, as well as patient age, sex, race, median income, inpatient and outpatient comorbidity scores, and residential status were included in a logistic regression analysis to identify the adjusted odds ratios (ORs) for each characteristic with respect to surveillance. We examined data from the reporting SEER registry to evaluate geographic variations in surveillance but excluded the registry from our multivariable model because registry included 11 categories and overlapped with the assessment of residences within urban ZIP codes. For analyses of association between physician characteristics and surveillance for bladder cancer, physician variables that were associated with low-intensity surveillance in univariate analyses (P<.10) were retained in the multivariable models. To assess the overall association between surveillance and patient age, tumor histologic grade, inpatient and outpatient comorbidity, income level, year of diagnosis, physician case volume, and the physicians year of medical school graduation, we tested for trend by using maximum likelihood estimates (27). SAS software (version 8.0; SAS Institute, Cary, NC) was used for all statistical analyses. PROC SQL and PROC LOGISTIC procedures in SAS were used for claims analyses and OR estimates, respectively. All statistical tests were two-sided.
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RESULTS |
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Table 1 displays the characteristics of cohort members who survived for at least 3 years after being diagnosed with superficial bladder cancer. Patients who had a total cystectomy were more likely to have stage T1 disease or lesions with an unspecified depth of mucosal penetration than patients who did not have a total cystectomy. Cystectomy recipients were slightly younger (median age = 72 years, standard deviation [SD] = 5.3 years) than nonrecipients (median age = 74 years, SD = 6.5 years) and more likely to have poorly differentiated tumors than nonrecipients.
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Table 2 displays the relative odds for receiving low-intensity surveillance (i.e., examinations in fewer than two follow-up intervals) according to patient characteristics. Patients whose tumors had better prognosis on the basis of well-differentiated histology were more likely to have low-intensity surveillance than those with poorly differentiated tumors, and this association persisted after adjustment for other characteristics (adjusted OR = 0.59, 95% confidence interval [CI] = 0.48 to 0.72, poorly versus well-differentiated tumor histology). Older age at diagnosis was inversely associated with adherence to surveillance. The adjusted odds ratio of low-intensity surveillance was 1.54, 95% CI = 1.35 to 1.74, for patients 75 years and older compared with those 6574 years old (data not shown). Fig. 1
illustrates the percentage of cohort members who had at least one, at least two, at least three, at least four, or five surveillance procedures over the 30-month follow-up interval according to their age at diagnosis. The association between age and the number of surveillance examinations remained statistically significant after simultaneous adjustment for all variables in a multivariable logistic regression model (Ptrend<.001, Table 2
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A patients race was an important predictor of adherence to surveillance: compared with the 17.2% of white patients who had low-intensity surveillance, 29.2% of black patients and 29.7% of patients of other races did so. The adjusted OR of low-intensity surveillance for nonwhites was 1.94 (95% CI = 1.57 to 2.40) (data not shown). Although fewer women (17.0%) than men (18.5%) had low-intensity surveillance, this difference was statistically significant only in the adjusted multivariable analysis (adjusted OR = 0.80, 95% CI = 0.69 to 0.92; P = .002). Surveillance was more frequent among patients residing in census tracts with higher median incomes; low-intensity surveillance rate was 16.0% in the highest income quartile and 20.1% in the lowest income quartile (Ptrend<.001). As illustrated in Table 2, other patient characteristics, including tumor stage, were not associated with low-intensity surveillance.
Physician Characteristics and Patient Adherence to Surveillance
The 6546 cohort members for whom the physician rendering primary treatment for bladder cancer could be identified received care from 1136 different physicians. The physicians characteristics are shown in Table 3. The numbers represent patients receiving care from physicians with particular characteristics. For each of the characteristics listed in Table 3
, the percentage of physicians with a particular characteristic was similar to the percentage of patients who received care from physicians with the same characteristic. For example, 5960 patients (91.1%) received care from board-certified urologists, and 994 physicians (87.5%) were board-certified urologists (data not shown). The majority of patients received care from physicians who were white, were male, had graduated from U.S. allopathic medical schools, and whose primary professional activity was patient care.
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Bladder cancer is a disease of smokers, and smokers are at risk for other malignancies such as lung cancers which may pose more immediate health risks and thereby obviate the need for bladder surveillance. Therefore, we examined the association between being diagnosed with a second malignancy and adherence to bladder surveillance. Among the 369 patients (5.5%) who received a diagnosis of a second non-urothelial malignancy within 3 years of their bladder cancer diagnosis, the low-intensity surveillance rate was 16%, whereas the low-intensity surveillance rate among those without a second diagnosis of a non-urothelial primary malignancy was 18% (data not shown). Thus, second non-urothelial malignancies did not explain the observed low rates of adherence to bladder surveillance.
Effect of Other Serious Medical Conditions on Adherence to Surveillance
To examine whether the development of other medical conditions after a bladder cancer diagnosis was associated with low rates of surveillance, we calculated an inpatient comorbidity score for each patient by using the CharlsonRomano comorbidity index for patients who were observed during the 30-month period subsequent to bladder cancer diagnosis. For the 1216 patients (18.1%) who had low-intensity surveillance, the CharlsonRomano inpatient comorbidity index observed during the follow-up period was 0 for 641 patients (52.7%), 1 for 250 patients (20.6%), and 2 or more for 325 patients (26.7%) (data not shown). For the 5501 cohort members (81.9%) who had at least two surveillance exams, the CharlsonRomano comorbidity index was 0 for 3356 patients (61.0%), 1 for 1188 patients (21.6%), and 2 for 957 patients (17.4%) (data not shown). We also determined how many times each patient had been hospitalized for any cause. For patients who had low-intensity surveillance, 27% had no hospitalizations, 29% had one hospitalization, 18% had two hospitalizations, and 27% had three or more hospitalizations over the 30-month period following bladder cancer diagnosis (data not shown). By contrast, for patients who had at least two follow-up surveillance examinations, 28% had no hospitalizations, 31% had one hospitalization, 17% had two hospitalizations, and 24% had three or more hospitalizations (data not shown). Both the CharlsonRomano comorbidity index and the number of hospitalizations during the follow-up period suggest that patients who had low-intensity surveillance were sicker than other cohort members. However, the magnitude of these differences is small and indicates that alternative explanations must also account for the observed low rates of adherence to bladder surveillance.
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DISCUSSION |
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Older age was strongly associated with low-intensity surveillance. Neither comorbidity prior to diagnosis nor comorbid events experienced during the follow-up period appear to explain the association between age and low adherence to surveillance. However, our dataset lacks critically important information about patient performance and functional status, both of which may influence both patient and provider thresholds for performing regular bladder surveillance. Low-intensity surveillance does not necessarily indicate that a patient received inappropriate medical care. Our analysis does not elucidate whether low patient adherence to surveillance with increasing age is a result of physicians nihilistic views about the value of bladder surveillance or, alternatively, because patients are unaware that surveillance is indicated, are reluctant to undergo an unpleasant invasive test, or are unable to avail themselves of it due to barriers such as lack of transportation or social support. Our finding of a strong association between age and treatment underscores what has by now emerged as a common theme based on the availability of the SEERMedicare data for population-based cancer research (28,29).
Our finding that nonwhite patients and patients residing in census tracts with the lowest median incomes were more likely to have low-intensity surveillance than white patients and patients residing in census tracts with the highest median incomes, respectively, even after adjustment for other characteristics, provides unequivocal evidence of the persistent inequities in the U.S. health care system (3032). Interventions to enhance adherence to surveillance must be developed and should focus on reaching nonwhite and poor Americans.
We expected to identify clear differences between physicians whose patients received low-intensity surveillance and physicians whose patients adhered more closely to surveillance guidelines. However, we found that the physicians who treat superficial bladder cancer are remarkably similar in terms of training and specialization and that there is little to distinguish those providers with patients adhering to guidelines from those whose patients received low-intensity follow-up.
Should we be perturbed that superficial bladder surveillance is underutilized, given that there is no established survival benefit evident from randomized trials of surveillance and that this strategy has a very high cost-effectiveness ratio, even under favorable assumptions of effectiveness (33)? Our results should not be construed to mean that efforts to increase adherence to surveillance are necessarily warranted. Rather, our findings are a challenge to the urologic oncology community to support studies to determine the reasons underlying existing patterns of care. If adherence to surveillance recommendations is low because clinicians doubt that Herculean efforts are warranted to detect recurrences or believe that particular subgroups of patients (e.g., those with grade 1 unifocal tumors) can be evaluated less frequently than every 36 months, the guidelines should be re-evaluated and modified to incorporate such factors. If there are particular areas of controversy among clinicians, randomized trials of several alternate follow-up schedules should be conducted. However, if there is indeed consensus that intensive surveillance is indicated, we should be concerned that actual care deviates from guidelines, particularly because nonmedical factors, such as race and socioeconomic status, influence patient care.
Several limitations of our analysis must be noted. First, within any claims-based analysis such as ours, the potential exists for inaccurate coding, especially because clinical information available from billing records is not as detailed as that available from chart review (3437). However, because Medicare reimbursement for surveillance cystoscopy is substantial, it is unlikely that patients actually had procedures that were simply not submitted to CMS for payment. Although we used a clinically relevant method to assess comorbidity, we may have failed to identify patients who would be considered to be poor candidates for surveillance on the basis of rare illnesses poorly captured by comorbidity indices or poor functional status. However, this possibility seems unlikely, because all of the patients in our cohort were deemed sufficiently fit to undergo baseline diagnostic procedures and survived for at least 3 years after diagnosis.
The second and most important limitation of our analysis is that it does not reveal whether patients, physicians, patientphysician communication, or other aspects of the health care system account for the apparent underutilization of bladder surveillance. Analyses that use SEERMedicare data to measure adherence to guidelines or quality of care shed relatively little light on why a particular medical intervention, such as surveillance cystoscopy, appears to be inappropriately utilized. Nevertheless, they do provide important benchmarks that depict real-world practice patterns and suggest areas of priority for further research. Over the past decade, clinical guidelines specifying the strategies for prevention, treatment, and surveillance deemed most appropriate on the basis of evidence-based reviews and consensus panels have proliferated. In only a few instances have clinical guidelines included specific blueprints for evaluating their dissemination and implementation or for measuring adherence to specific recommendations. Recent efforts to evaluate the impact of practice guidelines on real-world practice have gathered momentum (38). These efforts will need to involve both reviews of claims and patient records and interviews with patients and providers.
On the basis of evidence that U.S. cancer care is deficient in many important respects, the National Cancer Institute and the U.S. Congress have made improving the quality of cancer care a priority (39,40). Quality improvement will require the assembly of a "toolbox" of quality measures that can be used to track changes in response to interventions. Presently, quality measures for most malignancies, including bladder cancer, are lacking. Measuring the extent to which patients adhere to clinical guidelines is an important first step. However, such measurements must lead to further scrutiny of the reasons for non-adherence and thereby help to define good measures of high-quality cancer care.
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APPENDIX |
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NOTES |
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We acknowledge the efforts of the Applied Research Program, NCI, and Dr. Joan Warren, coordinator of the SEERMedicare program; the Office of Information Services and the Office of Strategic Planning, Center for Medicare Service; Information Management Services, Inc.; and the SEER Program tumor registries in the creation of the SEERMedicare database. We also thank Ramsey Tate for her editorial assistance.
1 Editors note: SEER is a set of geographically defined, population-based central cancer registries in the United States, operated by local nonprofit organizations under contract to the National Cancer Institute (NCI). Registry data are submitted electronically without personal identifiers to the NCI on a biannual basis, and the NCI makes the data available to the public for scientific research.
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Manuscript received May 28, 2002; revised January 28, 2003; accepted February 7, 2003.
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