- Email: [email protected]
Regionalization of radical cystectomy in the United States
Urologic Oncology: Seminars and Original Investigations ] (2017) ∎∎∎–∎∎∎
Original article
Regionalization of radical cystectomy in the United States Christopher B. Anderson, M.D., M.P.H.a,*, Renee Gennarelli, M.S.b, Harry W. Herr, M.D.c, Elena B. Elkin, Ph.D.b a
b
Department of Urology, Columbia University Medical Center, New York, NY Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY c Urology Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY Received 10 October 2016; received in revised form 19 January 2017; accepted 22 March 2017
Abstract Purpose: Radical cystectomy (RC) has become increasingly regionalized to high-volume hospitals. Our objective was to describe changes in regional market concentration and the distribution of RCs among hospitals, and examine how these changes affect patient travel distance to surgery. Materials and methods: We used the surveillance, epidemiology, and end results-Medicare database to identify patients who had RC for bladder cancer from 2001 to 2011. We defined RC market concentration within each Hospital Referral Regions (HRR) in surveillance, epidemiology, and end results using the Hirschman-Herfindhal Index. We measured straight-line patient travel distance to the nearest cystectomy provider hospital and used linear regression to evaluate the effect of market concentration on travel distance for surgery. We performed a similar analysis on patients who had laparoscopic cholecystectomy as a comparator. Results: We identified 10,802 patients with bladder cancer who had RC. From 2001 to 2011, 40% of HRRs had a statistically significant increase in Hirschman-Herfindhal Index, 53% had no significant change and 7% had a statically significant decrease. The median patient travel distance increased significantly from 10.4 miles (interquartile range: 2.6–30.2) to 16 miles (interquartile range: 6.3–40.4, P o 0.0001). Patients who lived in a highly concentrated HRR had to travel significantly further than patients who lived in an unconcentrated HRR (β ¼ 37.5, P o 0.001). These trends were not seen for laparoscopic cholecystectomy. Conclusions: Between 2001 and 2011, RC became increasingly regionalized to a small group of hospitals with a resultant increase in regional RC market concentration and patient travel distance. The clinical consequences on these changes to patients who require RC are uncertain. r 2017 Elsevier Inc. All rights reserved.
Keywords: Cystectomy; Health care quality, access, and evaluation; Travel; Urinary bladder neoplasms; Healthcare market
1. Introduction An inverse association between hospital volume and perioperative mortality for complex surgical procedures was demonstrated more than a decade ago, prompting proposals to regionalize these operations to high-volume hospitals [1,2]. Subsequently, there has been a regionalization of several complex operations, such as pancreatectomy and esophagectomy, to high-volume hospitals [3–5]. Although regionalization has been mandated in some countries, trends in the United States appear to be market driven, secondary Funding: Regional. * Corresponding author. Tel.: þ1-212-305-0114; fax: þ1-212-342-6870. E-mail address: [email protected] (C.B. Anderson). http://dx.doi.org/10.1016/j.urolonc.2017.03.026 1078-1439/r 2017 Elsevier Inc. All rights reserved.
to patient demand, physician referral patterns, and availability of providers [6]. Although regionalizing complex cancer surgery to highvolume hospitals is associated with improved outcomes, it may also have implications for access to care. Regionalization of radical surgery for pancreatic, esophageal, colon, and rectal cancers was associated with increased patient travel distance over time, in proportion to the degree of regionalization [4]. Over 7,000 radical cystectomies (RCs) are performed in the United States each year, and the procedure is considered the gold-standard treatment for high-risk bladder cancer [7]. Despite this, RC continues to carry significant perioperative morbidity and mortality [8]. Similar to other complex cancer operations, patients who have cystectomy at high-
2
C.B. Anderson et al. / Urologic Oncology: Seminars and Original Investigations ] (2017) ∎∎∎–∎∎∎
volume hospitals generally have better surgical outcomes, including lower mortality rate, shorter hospital length of stay, fewer complications, and are more likely to get a continent urinary diversion [1,9,10]. Although RCs have become increasingly concentrated at high-volume hospitals, the effect of this trend on patient access to the procedure is unclear [11,12]. Prior studies have described regionalization of RC, and other procedures, by defining hospital volume thresholds and observing shifts from low- to high-volume hospitals over time [4,12]. This approach requires the assignment of arbitrary volume thresholds and omits information about changes in the number of providers. It also ignores changes in the geographic distribution of hospitals that provide RC, which may have an important influence on patient travel distance and therefore access to care. Our objective was to identify changes in the distribution of hospitals that provide RC, in the competitiveness of regional markets, and in patient travel distances. We hypothesized that there has been increasing regionalization of RC over time, reflected by a smaller number of hospitals performing the procedure, increasing inequality in the distribution of procedures across hospitals, and a greater concentration of RCs within regional tertiary care markets. We also hypothesized that as a result of increasing regionalization, patients are required to travel greater distances to reach a hospital that provides RC. 2. Methods 2.1. Data We used the population-based surveillance, epidemiology, and end results (SEER)-Medicare database. The SEER registry collects all incident cancer cases in 18 geographic regions, encompassing nearly 30% of the population of the United States, and includes patient-level data on cancer characteristics and treatment type [13]. All patients residing in SEER aged 65 and older have linked Medicare billing claims that provide supplemental data on patient characteristics and health resource usage. The study was deemed exempt research by the Institutional Review Board of Memorial Sloan Kettering Cancer Center, and it was conducted in adherence with a Data Use Agreement from the National Cancer Institute. 2.2. Cohort To evaluate regional health care markets, we identified Hospital Referral Regions (HRRs) within SEER. HRRs are regional health care markets where Medicare beneficiaries receive tertiary surgical care [14]. Of the 306 HRRs, 94 overlap with SEER regions. To maximize data completeness, we only included HRRs in which at least 75% of the resident population was within the boundaries of a SEER
region. The geographic distribution of the population within each HRR was defined by 2000 census counts in ZIP Code Tabulation Areas (ZCTAs). Of the 94 HRRs with SEER overlap, 72 had at least 75% of their population within SEER boundaries and were included in the study (Supplemental Fig. 1). We varied this threshold between 70% and 90% and a similar number of HRRs met inclusion criteria. In the SEER-Medicare dataset, we identified all patients aged 65 or older with a diagnosis of bladder cancer (ICD-9 diagnosis codes 188.0–188.0, 233.7, 236.7, and 239.4) who had RC at a hospital within an included HRR between 2001 and 2011 (N ¼ 9,769). This cohort included patients who had RC for any indication. 2.3. Distribution of RCs The distribution of RCs among all hospitals in the included HRRs was characterized using Lorenz curves, which have been used to describe the distribution of health care resources [15,16]. We used Lorenz curves to depict the cumulative percentage of radical cystecomies performed by X percentage of hospitals each year. The further the curve deviates from the 451 line from the origin, the less equal the distribution of procedures among hospitals. A Gini coefficient quantifies the distribution of a Lorenz curve, and varies from 0 to 1 with higher values reflecting greater inequality. For our purposes, higher values of the Gini coefficient reflect greater regionalization of the procedure. We plotted Lorenz curves and estimated Gini coefficients to describe the distribution of cystectomies for each year of analysis. 2.4. Market concentration of RCs We used the Hirschman-Herfindhal Index (HHI) to assess changes in regional cystectomy markets over time. The HHI is an econometric measure that estimates the amount of concentration (and presumed lack of competition) within a market [17]. We estimated the HHI for each HRR in each year based on all patients who had RC within the HRR, using a hospital's procedure volume to represent its share of the regional RC market. The HHI is calculated by summing the squared market shares of each participant in the market and varies from 0 to 1 with 0 representing perfect competition and 1 complete monopoly. For example, a HRR with 5 hospitals that each performed 20% of procedures has a HHI of (0.22 þ 0.22 þ 0.22 þ 0.22 þ 0.22 þ 0.22) ¼ 0.2. Alternatively, a HRR with 4 hospitals that each performed 5% of procedures and 1 that performed 80% has an HHI of (0.052 þ 0.052 þ 0.052 2 2 þ 0.05 þ 0.8 ) ¼ 0.74. Federal agencies have defined a HHI o 0.15 as an unconcentrated market, 0.15 r HHI r 0.25 as a moderately concentrated market, and HHI 4 0.25 as a highly concentrated market [18].
C.B. Anderson et al. / Urologic Oncology: Seminars and Original Investigations ] (2017) ∎∎∎–∎∎∎
2.5. Travel distance to cystectomy We estimated patient travel distance in miles to the nearest hospital that performed cystectomy using straightline travel distance from the patient0 s ZIP code centroid to the hospital0 s ZIP code centroid. This is a proxy for travel time [19]. This analysis included all patients who lived within the 72 HRRs and had RC, regardless of the HRR in which they had surgery (N ¼ 10,802). To account for changes in ZIP code boundaries that occurred during the study period, ZIP code centroid coordinates were obtained from the year-specific ZIP code datasets provided by SAS, and patient travel distance was calculated using the ZIP code coordinates from the patient0 s year of surgery. Unencrypted ZIP codes were used with special permission from the SEER-Medicare program and each SEER registry. 2.6. Analysis Patient characteristics were described using frequencies and percentages. Lorenz curves were constructed to plot the distribution of RCs among all provider hospitals within the 72 included HRRs for each year of analysis. All hospitals were included in each Lorenz curve unless the hospital did not exist during the specific time period. In addition to single-year Lorenz curves, we created curves for 2001 to 2006 and 2007 to 2011. Year-specific Gini coefficients were estimated based on the single-year Lorenz curves, and unadjusted linear regression was used to assess trends over time. Year-specific HHIs for each HRR were calculated and compared over time. Each HRR was categorized as unconcentrated, moderately concentrated, highly concentrated or missing. If an HRR did not perform any RCs during a given year, it was not possible to calculate an HHI and HHI was considered missing. We considered a meaningful rise in market concentration to be a significant increase in the slope of the HRR-specific HHI over time, which we used to describe increased RC regionalization. We described patient travel distance using continuous and categorical terms. In addition, we estimated the percentage of patients who had RC within their HRR of residence and the percentage who traveled outside of their HRR of residence for surgery. Finally, we used linear regression to estimate the effect of HRR- and year-specific HHI on travel distance for surgery. To include all HRRs in the regression model, HHI was classified in 6 levels: 0 r HHI o 0.2, 0.2 r HHI o 0.4, 0.4 r HHI o 0.6, 0.6 r HHI o 0.8, 0.8 r HHI o 1.0, and no procedures performed. To evaluate whether observed trends in RC markets were specific to this procedure and not a reflection of systematic health care changes over time, we examined changes in regional market concentration and patient travel distance for cholecystectomy. We hypothesized that markets for cholecystectomy and geographic access to cholecystectomy would not exhibit notable changes during the study period.
3
From a 5% random sample of Medicare beneficiaries with no history of cancer who lived in a SEER area, we identified those who resided in one of the 72 included HRRs and had an inpatient claim for cholecystectomy (ICD-9 51.20, 51.21, 51.22, 51.23, and 51.24) between 2001 and 2011 (N ¼ 9,980), and analyses were performed as described for RC in bladder cancer patients. All statistical analysis was performed using SAS version 9.4 (Cary, NC).
3. Results We identified 10,802 bladder cancer patients who lived in an included HRR and had RC between 2001 and 2011. Most patients were white, male, and lived in a metropolitan area (Table 1). In the earlier part of the study period, 2001 to 2006, approximately 50% of hospitals performed 10% of procedures. In the later part of the study period, 2007 to 2011, 70% of hospitals performed 10% of procedures (Fig. 1). Single-year Lorenz curves exhibited a shift toward increasing inequality in the distribution of procedures across hospitals (data not shown). The annual Gini coefficients increased significantly over time, from 0.69 in 2001 to 0.82 in 2011 (P o 0.001, Supplementary Table). Regional market concentration generally increased over time in the 72 HRRs. In 2001, 8 HRRs (11%) did not perform any RCs and 68% were highly concentrated (Supplementary Fig. 2A). In 2011, 11 HRRs (15%) did not perform any RCs and 74% were highly concentrated (Supplementary Fig. 2B). From 2001 to 2011, 40% of HRRs had a statistically significant increase in their HHI, 53% had no significant change and 7% had a statistically significant decrease in HHI. The median patient travel distance increased significantly over time from 10.4 miles (interquartile range: 2.6–30.2) to 16 miles (interquartile range: 6.3–40.4, P o 0.0001). The percentage of patients who traveled less than 15 miles for their surgery fell from 58% to 48%, whereas percentage traveling 15 to 50 miles increased from 26% to 31% (Fig. 2). Patients who lived in a highly concentrated HRR or in an HRR that did not perform any RCs had to travel significantly further than patients who lived in an unconcentrated HRR (Table 2). We did not observe an increase in nonmetropolitan location of residence over time for patients diagnosed with bladder cancer (P ¼ 0.11). Approximately 36% of patients traveled outside of their HRR of residence for RC (Table 3). Significantly more patients left their HRR of residence for the procedure over time (P o 0.001). Most patients (87%) had RC at a hospital within 1 of the 72 included HRRs. Of the 1,351 patients who had cystectomy outside of these HRRs, most (79%) had surgery in 1 of 6 cities not located in SEER that were home to high-volume tertiary referral centers: Manhattan, Philadelphia, Ann Arbor, Nashville, Rochester (Minnesota), and Houston.
4
C.B. Anderson et al. / Urologic Oncology: Seminars and Original Investigations ] (2017) ∎∎∎–∎∎∎
Table 1 Characteristics of the cohort Characteristic Sex Male Female Race White Black Other/unknown Age 65–69 70–74 75–79 80–84 85þ Region West Midwest South Northeast Marital status Married Not married Unknown Tumor stage T0/Ta/Tis T1 T2 T3 T4 or metastatic Unknown Median household income Quartile 1 Quartile 2 Quartile 3 Quartile 4 Unknown Setting of residence Metropolitan Nonmetropolitan
Number
Percentage
8,048 2,754
75 26
9,669 533 600
90 5 6
2,393 2,849 2,828 1,996 736
22 26 26 18 7
5,290 1,155 2,084 2,273
49 11 19 21
7,141 3,265 396
66 30 4
1,614 2,232 2,951 2,443 1,388 174
15 21 27 23 13 2
2,629 2,631 2,630 2,629 283
24 24 24 24 3
9,398 1,404
87 13
In contrast to the observed trends for RC, there was no significant increase in HRR-specific HHI over time for cholecystectomy. In 2001, 60% of HRRs had highly concentrated cholecystectomy markets, which declined to 54% in 2011. Approximately 83% of HRRs had no significant change in HHI over time. Very few patients traveled more than 50 miles to have cholecystectomy and there was no significant change in the percentage of patients who had surgery outside their HRR of residence. There was no significant increase in mean travel distance for cholecystectomy over time and no significant association between market concentration or year and patient travel distance (data not shown).
4. Discussion Between 2001 and 2011, we observed evidence of increasing regionalization of RC among hospitals within
Fig. 1. Lorenz curves for the distribution of radical cystectomies among all hospitals in 2001–2006 and 2007–2011. (Color version of figure is available online.)
the 18 SEER regions. A rightward shift of the Lorenz curve and an increase in the Gini coefficient suggest that a greater percentage of procedures are now being performed by a smaller percentage of hospitals. The relatively high Gini coefficient in 2001 suggests that the distribution of cystectomies among hospitals was already significant skewed, however it became more so over time. We also observed a large number of highly concentrated regional markets in 2001 that became even more concentrated, and a significant increase in the HRR-specific HHI over time, signifying increasing regionalization of RC. The changes we observed in the distribution of RCs among hospitals are consistent with a recent report based on hospital discharge data from 3 states, which found a shift in RCs from low- to high-volume hospitals between 1996 and 2009 [12]. By 2009, most procedures were performed at high- and very high–volume hospitals, and several hospitals stopped performing RC altogether. Another study used inpatient discharge data from 1988 through 2000 and found that most cystectomies were performed at urban hospitals, and the percentage of procedures performed at high-volume hospitals and teaching hospitals increased significantly over time [11]. In the absence of a mandate to regionalize RCs to high-volume hospitals in the United States, the cause of increased regionalization is likely a function of patient demand, physician referral patterns, and the availability of surgeons and hospitals that offer the procedure. Increased regionalization of complex cancer surgery has been described for several procedures. Using discharge data from 3 states between 1996 and 2006, one study found a redistribution of esophagectomy, pancreatectomy, and colectomy from low- to high-volume hospitals [4]. Another study using Nationwide Inpatient Sample discharge data
C.B. Anderson et al. / Urologic Oncology: Seminars and Original Investigations ] (2017) ∎∎∎–∎∎∎
5
Fig. 2. Miles traveled to hospital for patients having radical cystectomy.
examined trends in pancreatectomy, esophagectomy, gastrectomy and major lung resection from 1997 to 2006 [5]. Many hospitals stopped performing these complex operations, and there was a significant shift from low- to high-volume hospitals. A study that used Medicare data to examine trends in market concentration and mortality for several complex operations, including RC, found an increase in the proportion of patients treated at highvolume hospitals and a reduction in postoperative mortality between 1999 and 2008 [3]. Although the absolute mortality reduction for cystectomy was modest (4.3%–3.7%), the relative reduction in mortality was 14%, much of which was attributed to increases in hospital volume. Although there is an unquestionable trend toward regionalization of several complex operations and a benefit to having surgery at high-volume center, the increasing concentration of specialty surgical care also has implications for patient access. We found an increase in mean patient travel distance over time, which was significantly associated with the increasing market concentration of RC. The fraction of patients who traveled more than 100 miles was Table 2 Association between Hirschman-Herfindahl Index and patient travel distance to radical cystectomy HHI
β Coefficient
Standard error
P value
0 r HHI o 0.2 0.2 r HHI o 0.4 0.4 r HHI o 0.6 0.6 r HHI o 0.8 0.8 r HHI o 1.0 No procedures
Ref 10.7 16.7 21.8 37.5 84.9
Ref 3.6 4.3 6.0 5.2 7.3
0.003 o0.001 o0.001 o0.001 o0.001
Higher value indicates greater market concentration. HHIs were estimated for each hospital referral region (N ¼ 72) and year (2001–2011).
fairly constant over time at approximately 10%, however there was an increase in those who traveled 15 to 50 miles and a decrease in the percentage of patients who traveled o15 miles. Others have found similar associations between the concentration of specialty care and patient access. A cross-sectional study examining geographic access to medical oncologists found increasing travel times to more specialized oncology treatment centers [20]. Although this study did not examine variations in utilization, processes of care or cancer outcomes as a function of travel burden, it did find an inverse relationship between specialization of care and access. Following a Medicare requirement that bariatric surgery patients seek treatment at highvolume Centers of Excellence, patients presenting for bariatric surgery experienced significantly longer travel distances [21]. Finally, travel distance for esophagectomy,
Table 3 Location of radical cystectomy in comparison to patient residence by year of procedure Year
Different HRR N (%)
Same HRR N (%)
Total
2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011
186 243 280 252 302 392 414 438 431 454 459
490 562 560 556 598 653 694 763 681 697 697
676 805 840 808 900 1,045 1,108 1,201 1,112 1,151 1,156
(28%) (30%) (33%) (31%) (34%) ((38%) (37%) (36%) (39%) (39%) (40%)
(72%) (70%) (67%) (69%) (66%) (63%) (63%) (64%) (61%) (61%) (60%)
6
C.B. Anderson et al. / Urologic Oncology: Seminars and Original Investigations ] (2017) ∎∎∎–∎∎∎
pancreatectomy and colectomy all increased over time in proportion to the degree each became centralized [4]. We also observed an increase in the proportion of patients who traveled outside their tertiary health care regions for RC over time, further evidence of regionalization. A recent study used discharge data from Washington State between 2003 and 2007 to examine travel requirements for patients having RC, radical prostatectomy, radical nephrectomy, partial nephrectomy and transurethral resection of the prostate [22]. Significantly more patients had to travel outside of their HRR of residence for RC than for any other procedure. Although HRR boundaries were not created based on RC specifically, they are intended to define geographic areas in which patients receive tertiary care for complex surgical procedures. Therefore, these findings may have implications for access to tertiary surgical care. Our study has several limitations. Our results may only be generalizable to the Medicare population, who make up at least 60% of RC patients [7]. Because the cohort only included patients diagnosed within SEER, our estimates of the degree of regionalization and market concentration may not reflect trends in the entire country. We used methods designed for econometric analysis to quantify changes in regional health care markets. Although this is not a novel application of these methods, HHI for HRRs with low procedure counts is very sensitive to small changes over time. Most importantly, this study alone does not describe the clinical effect of shifts in RC markets and changes in travel distance on patients with bladder cancer. Although regionalization of complex cancer operations has several benefits, it may also have unintended consequences. In addition to increases in patient travel distance, regionalization of surgical care has been associated with increased fragmentation of care, delays in treatment, delays in diagnosis and decreased utilization of indicated treatments [23–28]. Because most regional markets for RC were already concentrated in 2001, and travel distance increased modestly on average, it is unclear whether further regionalization has had meaningful consequences for bladder cancer patients. However, it is known that longer travel distance is associated with decreased utilization of RC, and there are already gender, racial and age disparities in access to tertiary hospitals for urologic oncology procedures [11,29,30]. Thus, the possibility of growing disparities in access to RC as a result of regionalization requires further study.
5. Conclusion Between 2001 and 2011, RC became increasingly regionalized to a small group of hospitals. As a result, there was an increase in regional RC market concentration and an increase in patient travel distance over time. The consequences of these changes for bladder cancer patients who require RC are uncertain.
Appendix A. Supporting information Supplementary data associated with this article can be found in the online version at http://dx.doi.org/10.1016/ j.urolonc.2017.03.026.
References [1] Birkmeyer JD, Siewers AE, Finlayson EV, et al. Hospital volume and surgical mortality in the United States. N Engl J Med 2002;346:1128– 37. [2] Dudley RA, Johansen KL, Brand R, et al. Selective referral to highvolume hospitals: estimating potentially avoidable deaths. J Am Med Assoc 2000;283:1159–66. [3] Finks JF, Osborne NH, Birkmeyer JD. Trends in hospital volume and operative mortality for high-risk surgery. N Engl J Med 2011;364: 2128–37. [4] Stitzenberg KB, Sigurdson ER, Egleston BL, et al. Centralization of cancer surgery: implications for patient access to optimal care. J Clin Oncol 2009;27:4671–8. [5] Learn PA, Bach PB. A decade of mortality reductions in major oncologic surgery: the impact of centralization and quality improvement. Med Care 2010;48:1041–9. [6] National Institute for Health and Care Excellence. Improving outcomes in urological cancers. Available at: http://www.nice.org.uk/ guidance/csguc/uptake [accessed 15.09.15]. [7] Faiena I, Dombrovskiy V, Koprowski C, et al. Performance of partial cystectomy in the United States from 2001 to 2010: trends and comparative outcomes. Can J Urol 2014;21:7520–7. [8] Shabsigh A, Korets R, Vora KC, et al. Defining early morbidity of radical cystectomy for patients with bladder cancer using a standardized reporting methodology. Eur Urol 2009;55:164–74. [9] Goossens-Laan CA, Gooiker GA, van Gijn W, et al. A systematic review and meta-analysis of the relationship between hospital/surgeon volume and outcome for radical cystectomy: an update for the ongoing debate. Eur Urol 2011;59:775–83. [10] Hollenbeck BK, Wei Y, Birkmeyer JD. Volume, process of care, and operative mortality for cystectomy for bladder cancer. Urology 2007;69:871–5. [11] Hollenbeck BK, Taub DA, Miller DC, et al. The regionalization of radical cystectomy to specific medical centers. J Urol 2005;174:1385– 9:[discussion 1389]. [12] Smaldone MC, Simhan J, Kutikov A, et al. Trends in regionalization of radical cystectomy in three large northeastern states from 1996 to 2009. Urol Oncol 2012. [13] Warren JL, Klabunde CN, Schrag D, et al. Overview of the SEERMedicare data: content, research applications, and generalizability to the United States elderly population. Med Care 2002;40:IV-3–18. [14] The Dartmouth Atlas. Data by Region. Available at: http://www. dartmouthatlas.org/data/region/. [accessed 15.09.15]. [15] Matsumoto M, Ogawa T, Kashima S, et al. The impact of rural hospital closures on equity of commuting time for haemodialysis patients: simulation analysis using the capacity-distance model. Int J Health Geogr 2012;11:28. [16] Tsutsui A, Ohno Y, Hara J, et al. Trends of centralization of childhood cancer treatment between 1975 and 2002 in Osaka, Japan. Jpn J Clin Oncol 2009;39:127–31. [17] The United States Department of Justice. Herfindahl-Hirschman Index. Available at: https://www.justice.gov/atr/herfindahl-hirschma n-index. [accessed 01.06.16]. [18] The United States Department of Justice and the Federal Trade Commission. Horzontal Merger Guidelines. Available at: http://www. justice.gov/atr/horizontal-merger-guidelines-08192010; 2010. [accessed 05.09.15].
C.B. Anderson et al. / Urologic Oncology: Seminars and Original Investigations ] (2017) ∎∎∎–∎∎∎ [19] Phibbs CS, Luft HS. Correlation of travel time on roads versus straight line distance. Med Care Res Rev 1995;52:532–42. [20] Onega T, Duell EJ, Shi X, et al. Geographic access to cancer care in the U.S. Cancer 2008;112:909–18. [21] Livingston EH, Burchell I. Reduced access to care resulting from centers of excellence initiatives in bariatric surgery. Arch Surg 2010;145:993–7. [22] Mossanen M, Izard J, Wright JL, et al. Identification of underserved areas for urologic cancer care. Cancer 2014;120:1565–71. [23] Goldberg DS, French B, Forde KA, et al. Association of distance from a transplant center with access to waitlist placement, receipt of liver transplantation, and survival among US veterans. J Am Med Assoc 2014;311:1234–43. [24] Massarweh NN, Chiang YJ, Xing Y, et al. Association between travel distance and metastatic disease at diagnosis among patients with colon cancer. J Clin Oncol 2014;32: 942–8.
7
[25] Stitzenberg KB, Chang Y, Smith AB, et al. Exploring the burden of inpatient readmissions after major cancer surgery. J Clin Oncol 2015;33:455–64. [26] Tomaszewski JJ, Handorf E, Corcoran AT, et al. Care transitions between hospitals are associated with treatment delay for patients with muscle invasive bladder cancer. J Urol 2014;192:1349–54. [27] Tsai TC, Orav EJ, Jha AK. Care fragmentation in the postdischarge period: surgical readmissions, distance of travel, and postoperative mortality. JAMA Surg 2015;150:59–64. [28] Petersen LA, Normand SL, Leape LL, et al. Regionalization and the underuse of angiography in the Veterans Affairs Health Care System as compared with a fee-for-service system. N Engl J Med 2003;348:2209–17. [29] Gore JL, Litwin MS, Lai J, et al. Use of radical cystectomy for patients with invasive bladder cancer. J Natl Cancer Inst 2010;102:802–11. [30] Trinh QD, Sun M, Sammon J, et al. Disparities in access to care at high-volume institutions for uro-oncologic procedures. Cancer 2012;118:4421–6.
Original article
Regionalization of radical cystectomy in the United States Christopher B. Anderson, M.D., M.P.H.a,*, Renee Gennarelli, M.S.b, Harry W. Herr, M.D.c, Elena B. Elkin, Ph.D.b a
b
Department of Urology, Columbia University Medical Center, New York, NY Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY c Urology Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY Received 10 October 2016; received in revised form 19 January 2017; accepted 22 March 2017
Abstract Purpose: Radical cystectomy (RC) has become increasingly regionalized to high-volume hospitals. Our objective was to describe changes in regional market concentration and the distribution of RCs among hospitals, and examine how these changes affect patient travel distance to surgery. Materials and methods: We used the surveillance, epidemiology, and end results-Medicare database to identify patients who had RC for bladder cancer from 2001 to 2011. We defined RC market concentration within each Hospital Referral Regions (HRR) in surveillance, epidemiology, and end results using the Hirschman-Herfindhal Index. We measured straight-line patient travel distance to the nearest cystectomy provider hospital and used linear regression to evaluate the effect of market concentration on travel distance for surgery. We performed a similar analysis on patients who had laparoscopic cholecystectomy as a comparator. Results: We identified 10,802 patients with bladder cancer who had RC. From 2001 to 2011, 40% of HRRs had a statistically significant increase in Hirschman-Herfindhal Index, 53% had no significant change and 7% had a statically significant decrease. The median patient travel distance increased significantly from 10.4 miles (interquartile range: 2.6–30.2) to 16 miles (interquartile range: 6.3–40.4, P o 0.0001). Patients who lived in a highly concentrated HRR had to travel significantly further than patients who lived in an unconcentrated HRR (β ¼ 37.5, P o 0.001). These trends were not seen for laparoscopic cholecystectomy. Conclusions: Between 2001 and 2011, RC became increasingly regionalized to a small group of hospitals with a resultant increase in regional RC market concentration and patient travel distance. The clinical consequences on these changes to patients who require RC are uncertain. r 2017 Elsevier Inc. All rights reserved.
Keywords: Cystectomy; Health care quality, access, and evaluation; Travel; Urinary bladder neoplasms; Healthcare market
1. Introduction An inverse association between hospital volume and perioperative mortality for complex surgical procedures was demonstrated more than a decade ago, prompting proposals to regionalize these operations to high-volume hospitals [1,2]. Subsequently, there has been a regionalization of several complex operations, such as pancreatectomy and esophagectomy, to high-volume hospitals [3–5]. Although regionalization has been mandated in some countries, trends in the United States appear to be market driven, secondary Funding: Regional. * Corresponding author. Tel.: þ1-212-305-0114; fax: þ1-212-342-6870. E-mail address: [email protected] (C.B. Anderson). http://dx.doi.org/10.1016/j.urolonc.2017.03.026 1078-1439/r 2017 Elsevier Inc. All rights reserved.
to patient demand, physician referral patterns, and availability of providers [6]. Although regionalizing complex cancer surgery to highvolume hospitals is associated with improved outcomes, it may also have implications for access to care. Regionalization of radical surgery for pancreatic, esophageal, colon, and rectal cancers was associated with increased patient travel distance over time, in proportion to the degree of regionalization [4]. Over 7,000 radical cystectomies (RCs) are performed in the United States each year, and the procedure is considered the gold-standard treatment for high-risk bladder cancer [7]. Despite this, RC continues to carry significant perioperative morbidity and mortality [8]. Similar to other complex cancer operations, patients who have cystectomy at high-
2
C.B. Anderson et al. / Urologic Oncology: Seminars and Original Investigations ] (2017) ∎∎∎–∎∎∎
volume hospitals generally have better surgical outcomes, including lower mortality rate, shorter hospital length of stay, fewer complications, and are more likely to get a continent urinary diversion [1,9,10]. Although RCs have become increasingly concentrated at high-volume hospitals, the effect of this trend on patient access to the procedure is unclear [11,12]. Prior studies have described regionalization of RC, and other procedures, by defining hospital volume thresholds and observing shifts from low- to high-volume hospitals over time [4,12]. This approach requires the assignment of arbitrary volume thresholds and omits information about changes in the number of providers. It also ignores changes in the geographic distribution of hospitals that provide RC, which may have an important influence on patient travel distance and therefore access to care. Our objective was to identify changes in the distribution of hospitals that provide RC, in the competitiveness of regional markets, and in patient travel distances. We hypothesized that there has been increasing regionalization of RC over time, reflected by a smaller number of hospitals performing the procedure, increasing inequality in the distribution of procedures across hospitals, and a greater concentration of RCs within regional tertiary care markets. We also hypothesized that as a result of increasing regionalization, patients are required to travel greater distances to reach a hospital that provides RC. 2. Methods 2.1. Data We used the population-based surveillance, epidemiology, and end results (SEER)-Medicare database. The SEER registry collects all incident cancer cases in 18 geographic regions, encompassing nearly 30% of the population of the United States, and includes patient-level data on cancer characteristics and treatment type [13]. All patients residing in SEER aged 65 and older have linked Medicare billing claims that provide supplemental data on patient characteristics and health resource usage. The study was deemed exempt research by the Institutional Review Board of Memorial Sloan Kettering Cancer Center, and it was conducted in adherence with a Data Use Agreement from the National Cancer Institute. 2.2. Cohort To evaluate regional health care markets, we identified Hospital Referral Regions (HRRs) within SEER. HRRs are regional health care markets where Medicare beneficiaries receive tertiary surgical care [14]. Of the 306 HRRs, 94 overlap with SEER regions. To maximize data completeness, we only included HRRs in which at least 75% of the resident population was within the boundaries of a SEER
region. The geographic distribution of the population within each HRR was defined by 2000 census counts in ZIP Code Tabulation Areas (ZCTAs). Of the 94 HRRs with SEER overlap, 72 had at least 75% of their population within SEER boundaries and were included in the study (Supplemental Fig. 1). We varied this threshold between 70% and 90% and a similar number of HRRs met inclusion criteria. In the SEER-Medicare dataset, we identified all patients aged 65 or older with a diagnosis of bladder cancer (ICD-9 diagnosis codes 188.0–188.0, 233.7, 236.7, and 239.4) who had RC at a hospital within an included HRR between 2001 and 2011 (N ¼ 9,769). This cohort included patients who had RC for any indication. 2.3. Distribution of RCs The distribution of RCs among all hospitals in the included HRRs was characterized using Lorenz curves, which have been used to describe the distribution of health care resources [15,16]. We used Lorenz curves to depict the cumulative percentage of radical cystecomies performed by X percentage of hospitals each year. The further the curve deviates from the 451 line from the origin, the less equal the distribution of procedures among hospitals. A Gini coefficient quantifies the distribution of a Lorenz curve, and varies from 0 to 1 with higher values reflecting greater inequality. For our purposes, higher values of the Gini coefficient reflect greater regionalization of the procedure. We plotted Lorenz curves and estimated Gini coefficients to describe the distribution of cystectomies for each year of analysis. 2.4. Market concentration of RCs We used the Hirschman-Herfindhal Index (HHI) to assess changes in regional cystectomy markets over time. The HHI is an econometric measure that estimates the amount of concentration (and presumed lack of competition) within a market [17]. We estimated the HHI for each HRR in each year based on all patients who had RC within the HRR, using a hospital's procedure volume to represent its share of the regional RC market. The HHI is calculated by summing the squared market shares of each participant in the market and varies from 0 to 1 with 0 representing perfect competition and 1 complete monopoly. For example, a HRR with 5 hospitals that each performed 20% of procedures has a HHI of (0.22 þ 0.22 þ 0.22 þ 0.22 þ 0.22 þ 0.22) ¼ 0.2. Alternatively, a HRR with 4 hospitals that each performed 5% of procedures and 1 that performed 80% has an HHI of (0.052 þ 0.052 þ 0.052 2 2 þ 0.05 þ 0.8 ) ¼ 0.74. Federal agencies have defined a HHI o 0.15 as an unconcentrated market, 0.15 r HHI r 0.25 as a moderately concentrated market, and HHI 4 0.25 as a highly concentrated market [18].
C.B. Anderson et al. / Urologic Oncology: Seminars and Original Investigations ] (2017) ∎∎∎–∎∎∎
2.5. Travel distance to cystectomy We estimated patient travel distance in miles to the nearest hospital that performed cystectomy using straightline travel distance from the patient0 s ZIP code centroid to the hospital0 s ZIP code centroid. This is a proxy for travel time [19]. This analysis included all patients who lived within the 72 HRRs and had RC, regardless of the HRR in which they had surgery (N ¼ 10,802). To account for changes in ZIP code boundaries that occurred during the study period, ZIP code centroid coordinates were obtained from the year-specific ZIP code datasets provided by SAS, and patient travel distance was calculated using the ZIP code coordinates from the patient0 s year of surgery. Unencrypted ZIP codes were used with special permission from the SEER-Medicare program and each SEER registry. 2.6. Analysis Patient characteristics were described using frequencies and percentages. Lorenz curves were constructed to plot the distribution of RCs among all provider hospitals within the 72 included HRRs for each year of analysis. All hospitals were included in each Lorenz curve unless the hospital did not exist during the specific time period. In addition to single-year Lorenz curves, we created curves for 2001 to 2006 and 2007 to 2011. Year-specific Gini coefficients were estimated based on the single-year Lorenz curves, and unadjusted linear regression was used to assess trends over time. Year-specific HHIs for each HRR were calculated and compared over time. Each HRR was categorized as unconcentrated, moderately concentrated, highly concentrated or missing. If an HRR did not perform any RCs during a given year, it was not possible to calculate an HHI and HHI was considered missing. We considered a meaningful rise in market concentration to be a significant increase in the slope of the HRR-specific HHI over time, which we used to describe increased RC regionalization. We described patient travel distance using continuous and categorical terms. In addition, we estimated the percentage of patients who had RC within their HRR of residence and the percentage who traveled outside of their HRR of residence for surgery. Finally, we used linear regression to estimate the effect of HRR- and year-specific HHI on travel distance for surgery. To include all HRRs in the regression model, HHI was classified in 6 levels: 0 r HHI o 0.2, 0.2 r HHI o 0.4, 0.4 r HHI o 0.6, 0.6 r HHI o 0.8, 0.8 r HHI o 1.0, and no procedures performed. To evaluate whether observed trends in RC markets were specific to this procedure and not a reflection of systematic health care changes over time, we examined changes in regional market concentration and patient travel distance for cholecystectomy. We hypothesized that markets for cholecystectomy and geographic access to cholecystectomy would not exhibit notable changes during the study period.
3
From a 5% random sample of Medicare beneficiaries with no history of cancer who lived in a SEER area, we identified those who resided in one of the 72 included HRRs and had an inpatient claim for cholecystectomy (ICD-9 51.20, 51.21, 51.22, 51.23, and 51.24) between 2001 and 2011 (N ¼ 9,980), and analyses were performed as described for RC in bladder cancer patients. All statistical analysis was performed using SAS version 9.4 (Cary, NC).
3. Results We identified 10,802 bladder cancer patients who lived in an included HRR and had RC between 2001 and 2011. Most patients were white, male, and lived in a metropolitan area (Table 1). In the earlier part of the study period, 2001 to 2006, approximately 50% of hospitals performed 10% of procedures. In the later part of the study period, 2007 to 2011, 70% of hospitals performed 10% of procedures (Fig. 1). Single-year Lorenz curves exhibited a shift toward increasing inequality in the distribution of procedures across hospitals (data not shown). The annual Gini coefficients increased significantly over time, from 0.69 in 2001 to 0.82 in 2011 (P o 0.001, Supplementary Table). Regional market concentration generally increased over time in the 72 HRRs. In 2001, 8 HRRs (11%) did not perform any RCs and 68% were highly concentrated (Supplementary Fig. 2A). In 2011, 11 HRRs (15%) did not perform any RCs and 74% were highly concentrated (Supplementary Fig. 2B). From 2001 to 2011, 40% of HRRs had a statistically significant increase in their HHI, 53% had no significant change and 7% had a statistically significant decrease in HHI. The median patient travel distance increased significantly over time from 10.4 miles (interquartile range: 2.6–30.2) to 16 miles (interquartile range: 6.3–40.4, P o 0.0001). The percentage of patients who traveled less than 15 miles for their surgery fell from 58% to 48%, whereas percentage traveling 15 to 50 miles increased from 26% to 31% (Fig. 2). Patients who lived in a highly concentrated HRR or in an HRR that did not perform any RCs had to travel significantly further than patients who lived in an unconcentrated HRR (Table 2). We did not observe an increase in nonmetropolitan location of residence over time for patients diagnosed with bladder cancer (P ¼ 0.11). Approximately 36% of patients traveled outside of their HRR of residence for RC (Table 3). Significantly more patients left their HRR of residence for the procedure over time (P o 0.001). Most patients (87%) had RC at a hospital within 1 of the 72 included HRRs. Of the 1,351 patients who had cystectomy outside of these HRRs, most (79%) had surgery in 1 of 6 cities not located in SEER that were home to high-volume tertiary referral centers: Manhattan, Philadelphia, Ann Arbor, Nashville, Rochester (Minnesota), and Houston.
4
C.B. Anderson et al. / Urologic Oncology: Seminars and Original Investigations ] (2017) ∎∎∎–∎∎∎
Table 1 Characteristics of the cohort Characteristic Sex Male Female Race White Black Other/unknown Age 65–69 70–74 75–79 80–84 85þ Region West Midwest South Northeast Marital status Married Not married Unknown Tumor stage T0/Ta/Tis T1 T2 T3 T4 or metastatic Unknown Median household income Quartile 1 Quartile 2 Quartile 3 Quartile 4 Unknown Setting of residence Metropolitan Nonmetropolitan
Number
Percentage
8,048 2,754
75 26
9,669 533 600
90 5 6
2,393 2,849 2,828 1,996 736
22 26 26 18 7
5,290 1,155 2,084 2,273
49 11 19 21
7,141 3,265 396
66 30 4
1,614 2,232 2,951 2,443 1,388 174
15 21 27 23 13 2
2,629 2,631 2,630 2,629 283
24 24 24 24 3
9,398 1,404
87 13
In contrast to the observed trends for RC, there was no significant increase in HRR-specific HHI over time for cholecystectomy. In 2001, 60% of HRRs had highly concentrated cholecystectomy markets, which declined to 54% in 2011. Approximately 83% of HRRs had no significant change in HHI over time. Very few patients traveled more than 50 miles to have cholecystectomy and there was no significant change in the percentage of patients who had surgery outside their HRR of residence. There was no significant increase in mean travel distance for cholecystectomy over time and no significant association between market concentration or year and patient travel distance (data not shown).
4. Discussion Between 2001 and 2011, we observed evidence of increasing regionalization of RC among hospitals within
Fig. 1. Lorenz curves for the distribution of radical cystectomies among all hospitals in 2001–2006 and 2007–2011. (Color version of figure is available online.)
the 18 SEER regions. A rightward shift of the Lorenz curve and an increase in the Gini coefficient suggest that a greater percentage of procedures are now being performed by a smaller percentage of hospitals. The relatively high Gini coefficient in 2001 suggests that the distribution of cystectomies among hospitals was already significant skewed, however it became more so over time. We also observed a large number of highly concentrated regional markets in 2001 that became even more concentrated, and a significant increase in the HRR-specific HHI over time, signifying increasing regionalization of RC. The changes we observed in the distribution of RCs among hospitals are consistent with a recent report based on hospital discharge data from 3 states, which found a shift in RCs from low- to high-volume hospitals between 1996 and 2009 [12]. By 2009, most procedures were performed at high- and very high–volume hospitals, and several hospitals stopped performing RC altogether. Another study used inpatient discharge data from 1988 through 2000 and found that most cystectomies were performed at urban hospitals, and the percentage of procedures performed at high-volume hospitals and teaching hospitals increased significantly over time [11]. In the absence of a mandate to regionalize RCs to high-volume hospitals in the United States, the cause of increased regionalization is likely a function of patient demand, physician referral patterns, and the availability of surgeons and hospitals that offer the procedure. Increased regionalization of complex cancer surgery has been described for several procedures. Using discharge data from 3 states between 1996 and 2006, one study found a redistribution of esophagectomy, pancreatectomy, and colectomy from low- to high-volume hospitals [4]. Another study using Nationwide Inpatient Sample discharge data
C.B. Anderson et al. / Urologic Oncology: Seminars and Original Investigations ] (2017) ∎∎∎–∎∎∎
5
Fig. 2. Miles traveled to hospital for patients having radical cystectomy.
examined trends in pancreatectomy, esophagectomy, gastrectomy and major lung resection from 1997 to 2006 [5]. Many hospitals stopped performing these complex operations, and there was a significant shift from low- to high-volume hospitals. A study that used Medicare data to examine trends in market concentration and mortality for several complex operations, including RC, found an increase in the proportion of patients treated at highvolume hospitals and a reduction in postoperative mortality between 1999 and 2008 [3]. Although the absolute mortality reduction for cystectomy was modest (4.3%–3.7%), the relative reduction in mortality was 14%, much of which was attributed to increases in hospital volume. Although there is an unquestionable trend toward regionalization of several complex operations and a benefit to having surgery at high-volume center, the increasing concentration of specialty surgical care also has implications for patient access. We found an increase in mean patient travel distance over time, which was significantly associated with the increasing market concentration of RC. The fraction of patients who traveled more than 100 miles was Table 2 Association between Hirschman-Herfindahl Index and patient travel distance to radical cystectomy HHI
β Coefficient
Standard error
P value
0 r HHI o 0.2 0.2 r HHI o 0.4 0.4 r HHI o 0.6 0.6 r HHI o 0.8 0.8 r HHI o 1.0 No procedures
Ref 10.7 16.7 21.8 37.5 84.9
Ref 3.6 4.3 6.0 5.2 7.3
0.003 o0.001 o0.001 o0.001 o0.001
Higher value indicates greater market concentration. HHIs were estimated for each hospital referral region (N ¼ 72) and year (2001–2011).
fairly constant over time at approximately 10%, however there was an increase in those who traveled 15 to 50 miles and a decrease in the percentage of patients who traveled o15 miles. Others have found similar associations between the concentration of specialty care and patient access. A cross-sectional study examining geographic access to medical oncologists found increasing travel times to more specialized oncology treatment centers [20]. Although this study did not examine variations in utilization, processes of care or cancer outcomes as a function of travel burden, it did find an inverse relationship between specialization of care and access. Following a Medicare requirement that bariatric surgery patients seek treatment at highvolume Centers of Excellence, patients presenting for bariatric surgery experienced significantly longer travel distances [21]. Finally, travel distance for esophagectomy,
Table 3 Location of radical cystectomy in comparison to patient residence by year of procedure Year
Different HRR N (%)
Same HRR N (%)
Total
2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011
186 243 280 252 302 392 414 438 431 454 459
490 562 560 556 598 653 694 763 681 697 697
676 805 840 808 900 1,045 1,108 1,201 1,112 1,151 1,156
(28%) (30%) (33%) (31%) (34%) ((38%) (37%) (36%) (39%) (39%) (40%)
(72%) (70%) (67%) (69%) (66%) (63%) (63%) (64%) (61%) (61%) (60%)
6
C.B. Anderson et al. / Urologic Oncology: Seminars and Original Investigations ] (2017) ∎∎∎–∎∎∎
pancreatectomy and colectomy all increased over time in proportion to the degree each became centralized [4]. We also observed an increase in the proportion of patients who traveled outside their tertiary health care regions for RC over time, further evidence of regionalization. A recent study used discharge data from Washington State between 2003 and 2007 to examine travel requirements for patients having RC, radical prostatectomy, radical nephrectomy, partial nephrectomy and transurethral resection of the prostate [22]. Significantly more patients had to travel outside of their HRR of residence for RC than for any other procedure. Although HRR boundaries were not created based on RC specifically, they are intended to define geographic areas in which patients receive tertiary care for complex surgical procedures. Therefore, these findings may have implications for access to tertiary surgical care. Our study has several limitations. Our results may only be generalizable to the Medicare population, who make up at least 60% of RC patients [7]. Because the cohort only included patients diagnosed within SEER, our estimates of the degree of regionalization and market concentration may not reflect trends in the entire country. We used methods designed for econometric analysis to quantify changes in regional health care markets. Although this is not a novel application of these methods, HHI for HRRs with low procedure counts is very sensitive to small changes over time. Most importantly, this study alone does not describe the clinical effect of shifts in RC markets and changes in travel distance on patients with bladder cancer. Although regionalization of complex cancer operations has several benefits, it may also have unintended consequences. In addition to increases in patient travel distance, regionalization of surgical care has been associated with increased fragmentation of care, delays in treatment, delays in diagnosis and decreased utilization of indicated treatments [23–28]. Because most regional markets for RC were already concentrated in 2001, and travel distance increased modestly on average, it is unclear whether further regionalization has had meaningful consequences for bladder cancer patients. However, it is known that longer travel distance is associated with decreased utilization of RC, and there are already gender, racial and age disparities in access to tertiary hospitals for urologic oncology procedures [11,29,30]. Thus, the possibility of growing disparities in access to RC as a result of regionalization requires further study.
5. Conclusion Between 2001 and 2011, RC became increasingly regionalized to a small group of hospitals. As a result, there was an increase in regional RC market concentration and an increase in patient travel distance over time. The consequences of these changes for bladder cancer patients who require RC are uncertain.
Appendix A. Supporting information Supplementary data associated with this article can be found in the online version at http://dx.doi.org/10.1016/ j.urolonc.2017.03.026.
References [1] Birkmeyer JD, Siewers AE, Finlayson EV, et al. Hospital volume and surgical mortality in the United States. N Engl J Med 2002;346:1128– 37. [2] Dudley RA, Johansen KL, Brand R, et al. Selective referral to highvolume hospitals: estimating potentially avoidable deaths. J Am Med Assoc 2000;283:1159–66. [3] Finks JF, Osborne NH, Birkmeyer JD. Trends in hospital volume and operative mortality for high-risk surgery. N Engl J Med 2011;364: 2128–37. [4] Stitzenberg KB, Sigurdson ER, Egleston BL, et al. Centralization of cancer surgery: implications for patient access to optimal care. J Clin Oncol 2009;27:4671–8. [5] Learn PA, Bach PB. A decade of mortality reductions in major oncologic surgery: the impact of centralization and quality improvement. Med Care 2010;48:1041–9. [6] National Institute for Health and Care Excellence. Improving outcomes in urological cancers. Available at: http://www.nice.org.uk/ guidance/csguc/uptake [accessed 15.09.15]. [7] Faiena I, Dombrovskiy V, Koprowski C, et al. Performance of partial cystectomy in the United States from 2001 to 2010: trends and comparative outcomes. Can J Urol 2014;21:7520–7. [8] Shabsigh A, Korets R, Vora KC, et al. Defining early morbidity of radical cystectomy for patients with bladder cancer using a standardized reporting methodology. Eur Urol 2009;55:164–74. [9] Goossens-Laan CA, Gooiker GA, van Gijn W, et al. A systematic review and meta-analysis of the relationship between hospital/surgeon volume and outcome for radical cystectomy: an update for the ongoing debate. Eur Urol 2011;59:775–83. [10] Hollenbeck BK, Wei Y, Birkmeyer JD. Volume, process of care, and operative mortality for cystectomy for bladder cancer. Urology 2007;69:871–5. [11] Hollenbeck BK, Taub DA, Miller DC, et al. The regionalization of radical cystectomy to specific medical centers. J Urol 2005;174:1385– 9:[discussion 1389]. [12] Smaldone MC, Simhan J, Kutikov A, et al. Trends in regionalization of radical cystectomy in three large northeastern states from 1996 to 2009. Urol Oncol 2012. [13] Warren JL, Klabunde CN, Schrag D, et al. Overview of the SEERMedicare data: content, research applications, and generalizability to the United States elderly population. Med Care 2002;40:IV-3–18. [14] The Dartmouth Atlas. Data by Region. Available at: http://www. dartmouthatlas.org/data/region/. [accessed 15.09.15]. [15] Matsumoto M, Ogawa T, Kashima S, et al. The impact of rural hospital closures on equity of commuting time for haemodialysis patients: simulation analysis using the capacity-distance model. Int J Health Geogr 2012;11:28. [16] Tsutsui A, Ohno Y, Hara J, et al. Trends of centralization of childhood cancer treatment between 1975 and 2002 in Osaka, Japan. Jpn J Clin Oncol 2009;39:127–31. [17] The United States Department of Justice. Herfindahl-Hirschman Index. Available at: https://www.justice.gov/atr/herfindahl-hirschma n-index. [accessed 01.06.16]. [18] The United States Department of Justice and the Federal Trade Commission. Horzontal Merger Guidelines. Available at: http://www. justice.gov/atr/horizontal-merger-guidelines-08192010; 2010. [accessed 05.09.15].
C.B. Anderson et al. / Urologic Oncology: Seminars and Original Investigations ] (2017) ∎∎∎–∎∎∎ [19] Phibbs CS, Luft HS. Correlation of travel time on roads versus straight line distance. Med Care Res Rev 1995;52:532–42. [20] Onega T, Duell EJ, Shi X, et al. Geographic access to cancer care in the U.S. Cancer 2008;112:909–18. [21] Livingston EH, Burchell I. Reduced access to care resulting from centers of excellence initiatives in bariatric surgery. Arch Surg 2010;145:993–7. [22] Mossanen M, Izard J, Wright JL, et al. Identification of underserved areas for urologic cancer care. Cancer 2014;120:1565–71. [23] Goldberg DS, French B, Forde KA, et al. Association of distance from a transplant center with access to waitlist placement, receipt of liver transplantation, and survival among US veterans. J Am Med Assoc 2014;311:1234–43. [24] Massarweh NN, Chiang YJ, Xing Y, et al. Association between travel distance and metastatic disease at diagnosis among patients with colon cancer. J Clin Oncol 2014;32: 942–8.
7
[25] Stitzenberg KB, Chang Y, Smith AB, et al. Exploring the burden of inpatient readmissions after major cancer surgery. J Clin Oncol 2015;33:455–64. [26] Tomaszewski JJ, Handorf E, Corcoran AT, et al. Care transitions between hospitals are associated with treatment delay for patients with muscle invasive bladder cancer. J Urol 2014;192:1349–54. [27] Tsai TC, Orav EJ, Jha AK. Care fragmentation in the postdischarge period: surgical readmissions, distance of travel, and postoperative mortality. JAMA Surg 2015;150:59–64. [28] Petersen LA, Normand SL, Leape LL, et al. Regionalization and the underuse of angiography in the Veterans Affairs Health Care System as compared with a fee-for-service system. N Engl J Med 2003;348:2209–17. [29] Gore JL, Litwin MS, Lai J, et al. Use of radical cystectomy for patients with invasive bladder cancer. J Natl Cancer Inst 2010;102:802–11. [30] Trinh QD, Sun M, Sammon J, et al. Disparities in access to care at high-volume institutions for uro-oncologic procedures. Cancer 2012;118:4421–6.