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    Investig Clin Urol. 2023 Nov;64(6):561-571. English.
    Published online Oct 17, 2023.
    https://doi.org/10.4111/icu.20230125
    © The Korean Urological Association
    Original Article

    Impact of rural residence on the presentation, management and survival of patients with non-metastatic muscle-invasive bladder carcinoma

    Furkan Dursun,1 Ahmed Elshabrawy,1 Hanzhang Wang,1 Dharam Kaushik,1,2 Michael A. Liss,1,2 Robert S. Svatek,1,2 John L. Gore,3 and Ahmed M. Mansour1,2,4
      • 1Department of Urology, University of Texas Health San Antonio, San Antonio, TX, USA.
      • 2UT Health San Antonio MD Anderson Cancer Center, San Antonio, TX, USA.
      • 3Department of Urology, University of Washington, Seattle, WA, USA.
      • 4Urology and Nephrology Center, Mansoura University, Mansoura, Egypt.
    • Corresponding Author: Furkan Dursun. Department of Urology, University of Texas Health San Antonio, 7703 Floyd Curl Drive, San Antonio, TX 78229, USA. TEL: +1-210-567-5643, FAX: +1-210-567-6868, Email: furkandursun@gmail.com
    Received April 10, 2023; Revised June 15, 2023; Accepted July 16, 2023.

    This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

    Abstract

    Purpose

    To assess the impact of rural and remote residence on the receipt of guidelines-recommended treatment, quality of treatment and overall survival (OS) in patients with non-metastatic muscle-invasive bladder cancer (MIBC).

    Materials and Methods

    Patients with MIBC were identified using National Cancer Database. Patients were classified into three residential areas. Logistic regression models were used to assess associations between geographic residence and receipt of radical cystectomy (RC) or chemoradiation therapy (CRT). Models were fitted to assess quality benchmarks of RC and CRT.

    Results

    We identified 71,395 patients. Of those 58,874 (82.5%) were living in Metro areas, 8,534 (11.9%) in urban-rural adjacent (URA), and 3,987 (5.6%) in urban-rural remote to metro area (URR). URR residence was significantly associated with poor OS compared to URA and Metro residence (HR 0.87, 95% CI 0.81–0.94 and HR 0.90, 95% CI 0.87–0.93, p<0.001). There was no difference in the likelihood of receiving RC and CRT among different residential areas. Among patients who underwent RC; individuals living in URR were less likely to receive neoadjuvant chemotherapy and adequate lymph node dissection, and had a higher probability of positive surgical margin than those living in metro areas. For those who received CRT; individuals living in Metro areas were more likely to receive concomitant systemic therapy compared to URR.

    Conclusions

    Rural residence is associated with lower OS for MIBC patients and less likelihood of meeting quality benchmarks for RC and CRT. This data should be used to guide further health policy and allocation of resources for rural population.

    Keywords
    Chemoradiotherapy; Cystectomy; Rural population; Urban population; Urinary bladder neoplasms

    INTRODUCTION

    Bladder cancer is the 6th most common cancer in the United States with estimated 83,700 new cases and 17,200 related deaths for 2021 [1]. Approximately 25% of the newly diagnosed patients present with muscle-invasive bladder cancer (MIBC), and nearly half of these patients will develop metastases during the course of their diseases [2, 3]. The recommended treatment for non-metastatic MIBC is neoadjuvant chemotherapy (NAC) followed by radical cystectomy (RC) and adequate lymph node dissection (LND) or bladder preservation with maximal transurethral resection followed by concurrent chemoradiation therapy (CRT) [2, 4].

    In addition to tumor characteristics, non-cancer related factors such as race, ethnicity, and socioeconomic status have been reported to contribute to disparities in the presentation, treatment, and mortality of several cancers [5, 6, 7, 8]. Furthermore, area of geographic residence has been recently associated with cancer outcomes. Specifically, reports has shown that patients living in rural areas have increased risk of mortality from different cancers [9, 10, 11]. Regionalization of bladder cancer treatment to high volume centers has been associated with care disparities particularly for disadvantaged populations [12, 13]. As cancer care becomes more centralized, patients residing outside of metro areas have unique challenges to access resources.

    To date, there is limited data on the impact of geographic residence on bladder cancer diagnosis, treatment and survival [14]. The primary objective of this study was to assess the impact of geographic residence at the time of diagnosis on overall survival (OS) in MIBC. Secondary objectives included evaluation of the impact of geographic residence on the receipt of guidelines-recommended treatment for MIBC and evaluation of the quality of offered treatment according to consensus benchmarks. We hypothesized that patients residing in rural and remote areas would have less access to care and would less likely receive optimal treatment and subsequently have less favorable OS.

    MATERIALS AND METHODS

    1. Data source

    The National Cancer Database (NCDB) was established in 1989 as a joint effort of the Commission on Cancer (CoC) of the American Cancer Society and American College of Surgeons. It is a nationwide, hospital-based, oncology data set that currently captures 70% of all newly diagnosed malignancies in the US annually, from more than 1,500 participating CoC accredited hospitals [15]. The NCDB data have been de-identified and thus the study was exempt from Institutional Review Board approval.

    2. Study population

    The NCDB was queried for patients with histologically confirmed urothelial carcinoma of the bladder between 2004 to 2015 according to International Classification of Diseases for Oncology, Third Edition (ICD-O-3) topography codes (C67.0-C67.99). Patients with clinical stage cT2-4, N0-3, M0 were further identified according to the American Joint Committee on Cancer (AJCC) Staging Manual, 7th edition. Patients without information on treatment modality for the primary site and those with missing pathological stage and histology were excluded from the analysis.

    3. Urban/rural classification

    The NCDB assigns each patient into one of the categories based on the information recorded at the time of diagnosis using the typology published by the US Department of Agriculture (USDA) Economic Research Service. USDA defines a non-metro county as adjacent if it physically adjoins one or more metro areas, and has at least 2% of its employed labor force commuting to central metro counties [16]. For the purpose of analysis, patients were divided into three groups: metro, urban-rural adjacent to a metro area (URA), and urban-rural remote to a metro area (URR) (Supplementary Table 1).

    4. Covariates

    Patient specific variables include age at diagnosis, sex, race/ethnicity, baseline Charlson-Deyo comorbidity index (CCI), and clinical tumor stage. Sociodemographic variables included education level, insurance status, and ZIP code level median income quartile. Treatment-related variables included receipt of RC or CRT and facility type. In the RC cohort, receipt of NAC, time to surgery, surgical margin status and number of examined lymph nodes (LNs) were evaluated. In the CRT cohort, the total regional dose as well as receipt of concomitant radiosensitizing therapy (defined as receipt systemic therapy within 60 days from the start of radiotherapy) were reported.

    5. Outcomes

    The primary end point was OS from initial diagnosis to the date of death or censor at last follow-up as recorded in the cancer registry. Specifically, we compared OS of patients living in Metro, URA and URR areas. To evaluate the impact of treatment in local facilities versus travel to distant facilities to seek treatment, we compared the OS in the subgroup of patients who commuted less or more than 50 miles to reach the health care facility [17]. Secondary endpoints included receipt of guidelines-recommended treatment (RC or CRT) as well as quality of treatment benchmarks. For RC cohort, quality benchmarks included receipt of NAC, adequate LND (>16 LNs), RC within 12 weeks from the date of diagnosis (for patients who didn’t receive NAC) and rates of positive surgical margins (PSMs) [18, 19]. For the CRT cohort, quality benchmarks included the receipt of a regional dose of at least 60 Gy and administration of concurrent radiosensitizing chemotherapy [20].

    6. Statistical analysis

    Medians and interquartile ranges were reported for continuous variables, while frequencies and proportions were reported for categorical variables. We used chi-square test for categorical variables and Kruskal–Wallis test for continuous variables to evaluate univariate relationship between patient sociodemographic, clinical, and treatment variables across different residential areas. Kaplan–Meier survival curves were constructed to evaluate survival in each residential category. Log-rank tests evaluated statistical differences in survival probabilities for Kaplan–Meier curves. Multivariable Cox proportional hazard models were fitted to determine independent predictors of OS after adjusting for confounding variables. Subgroup analysis also compared the OS in the subgroup of patients who need to commute less or more than 50 miles to reach the health care facility within each residential category. To evaluate our secondary endpoints, multivariable logistic regression models were fitted to evaluate factors that are independently associated with receipt of RC or CRT as well as factors associated with meeting selected quality benchmarks. All statistical analysis was preformed using Stata statistical software (Version 15; College Station), with a 2-sided p-value of 0.05 determined as being statically significant.

    RESULTS

    1. Cohort characteristics

    A total of 71,395 non-metastatic MIBC patients were identified. Of these 3,987 (5.6%) resided in URR areas, 8,534 (11.9%) resided in URA areas, and 58,874 (82.5%) resided in Metro areas (Table 1). Most included patients were male and aged >70 years. According to the residential area at diagnosis, the percentage of White patients versus other races was higher in URR areas compared with URA and Metro areas. Conversely, more Black and Hispanic patients were identified in Metro areas.

    Table 1
    Demographic and clinical characteristics of non-metastatic muscle invasive bladder cancer patients stratified according to the residency status, diagnosed within the NCDB from 2004 to 2015

    Patients living in Metro areas tended to have higher ZIP code-level income and education and were more likely to have private insurance compared with patients living in URR and URA areas.

    Nearly 58% of patients living in URR areas and 32% of patients living in URA areas had to travel more than 50 miles to receive healthcare compared with only 8% of patients living in Metro areas.

    2. Diagnosis and treatment patterns

    No significant differences were noted in clinical stage at presentation across different residential areas. However, the median time between the diagnosis and most definitive treatment was significantly longer for patients living in URR compared to Metro areas (23 vs. 14 d, p<0.001), but there was no significant difference between patients living in URR and URA (23 vs. 21 d, p=0.07).

    CRT utilization in URR, URA and metro areas were 17.1% vs. 18.4% vs. 18.9% respectively. While the rates of RC utilization were 41.9% vs. 40.0% vs. 35.6%. Among patients who received RC, no statistical difference was noted among the groups with respect to PSM rates, 30-day readmission rates as well as 30- and 90-day mortality rates (Table 1).

    3. Survival

    The 5-year OS rates for patients residing in URR, URA and Metro areas were 28.4% (95% confidence interval [CI] 26.7%–30.0%), 29.7% (95% CI 28.6%–30.8%), and 30.1% (95% CI 30.6%–31.5%), respectively. 10-year OS rates were 16.8% (95% CI 14.9%–18.9%), 16.7% (95% CI 15.3%–18.2%), and 22.2% (95% CI 21.7%–22.7%), respectively. Kaplan–Meier survival curves stratified by area of residence showed that patients resided in Metro areas had statistically significant higher OS probability compared to URR residents (p=0.01). No OS difference between URA vs. Metro and URA vs. URR residents (p=0.072 and p=0.99, respectively, Fig. 1) were appreciated.

    Fig. 1
    Kaplan–Meier overall survival curve for non-metastatic MIBC based on area of residency. URA, urban-rural adjacent; URR, urban-rural remote; MIBC, muscle-invasive bladder cancer.

    Multivariable Cox regression analysis revealed that the hazard of death over time was significantly lower for those living in URA and Metro areas compared with URR residents (hazard ratio [HR] 0.87, 95% CI 0.81–0.94, p<0.001 and HR 0.90, 95% CI 0.87–0.93, p<0.001, respectively; Table 2). Additionally, commuting more than 50 miles to receive healthcare was a significant predictor of better OS for patients residing in URR areas (HR 0.88, CI 0.80–0.96, p=0.007). Such survival benefit with commuting was not observed in Metro and URA areas.

    Table 2
    Multivariable Cox proportional hazards regression model evaluating overall survival in the non-metastatic MIBC patient population

    Other factors that were independently associated with better OS included the receipt of RC (HR 0.89, 95% CI 0.86–0.92, p<0.001) and removal of more than 16 LNs during RC (HR 0.87, 95% CI 0.84–0.90, p<0.001). PSM after RC was identified as a predictor of poorer OS (HR 1.90, 95% CI 1.84–1.97, p<0.001). Additionally, female sex, older age, African American race, having Medicaid or Medicare insurance, higher CCI were associated with poor OS for non-metastatic MIBC patients (Table 2).

    4. Quality of treatment benchmarks

    In the RC subgroup, compared with patients living in URR, patients in Metro areas were more likely to receive NAC (odds ratio [OR] 1.11, 95% CI 1.04–1.18, p=0.002), adequate LND (OR 1.10, 95% CI 1.05–1.15, p<0.001) and less likely to have PSM (OR 0.94, 95% CI 0.89–1.00, p=0.040), consequently, better OS was noted in this group (HR 0.92, 95% CI 0.88–0.95, p<0.001) (Table 3).

    Table 3
    Association of area of residence with mortality and quality benchmarks of radical cystectomy in patients with MIBC who underwent radical cystectomy, in NCDB from 2004 to 2015

    In the CRT subgroup, patients residing in Metro areas were more likely to receive concomitant radiosensitizing systemic therapy (compared with URR, OR 1.07, 95% CI 1.03–1.12, p=0.001) Similar OS benefit was noted in the CRT subgroup who reside in Metro areas (compared with URR, HR 0.90, 95% CI 0.83–0.98, p=0.015) (Table 4). Notably, there was no difference among residence areas in terms of the likelihood of receiving RC nor CRT (Tables 3, 4).

    Table 4
    Association of area of residence with mortality and quality benchmarks of combined modality treatment in patients with MIBC who received combined modality treatment, in NCDB from 2004 to 2015

    DISCUSSION

    Our results indicate that patients with MIBC living in URR areas are less likely to meet important quality of treatment benchmarks and have higher hazards of all-cause mortality compared to patients residing in Metro areas. Moreover, traveling more than 50 miles was associated with improved survival odds in patients living in URR.

    Defining a residential area is usually based on the population size and density, location, sectoral employment, provision of infrastructure and services. Rural-urban grouping in literature was commonly based on the population size. We utilized a more granular classification based on the location of urban and rural areas in relation to Metro areas (adjacent vs. remote).

    Lower OS has been reported for patients living in rural areas for several cancers [8, 11, 21, 22]. Increased stage at diagnosis, reduced access to subspecialities, and decreased utilization of systemic and radiation therapies have been reported in colorectal, pancreatic, and breast cancers [22, 23, 24]. Similarly, health care avoidance and lower rates of insurance among rural residents have been reported as reasons of delay in diagnosis [25, 26, 27]. After diagnosis; limited provider availability and the need to travel for treatment may cause delays in treatment. Additionally, rural residents may have barriers to access the contemporary treatments modalities or clinical trials which are mostly available in tertiary healthcare facilities [28, 29].

    Deuker et al. [14] studied the effect of residency status on bladder cancer stage at presentation, cancer-specific mortality, and other cause mortality, using the Surveillance, Epidemiology, and End Results (SEER) database. Their definition for residential area was based on the population size only (rural areas <2,500, urban clusters ≥2,500, and urbanized areas ≥50,000 inhabitants). They reported no significant differences in access to treatment or stage distribution, but rurality was associated with higher all-cause mortality and interestingly higher cancer-specific mortality for non-muscle invasive disease [14]. We observed a similar pattern in terms of OS, furthermore, there was a significant difference with regards to the quality benchmarks of treatment in favor of patients living in metro areas.

    Previous studies evaluated the relationship between distance from reporting hospital and survival in cancer patients. Ryan et al. [30] evaluated the relation between distance and overall mortality in patients with MIBC using the NCDB. They reported lower overall mortality for patients who travel more compared to patients traveling less. When they analyzed a subgroup of patients who underwent RC, the difference was not significant, however, they found longer distance was associated with surgery at a high-volume institution and receipt of NAC [30]. Distance to travel may also be considered as an indicator for rurality, however, patients traveled further were more likely to have RC at high volume centers and more likely to receive NAC. Similarly, we found that travelling more than 50 miles to seek care was associated with better OS in URR but not in URA and Metro areas.

    Despite the presence of well-established guideline-based recommendations for treatment of patients with nonmetastatic MIBC [2, 3, 4], there is growing evidence that differences exist in guideline compliance and treatment delivery [13]. Leow et al. [19] proposed measurable quality indicators including preoperative, intraoperative, and postoperative phases of treatment for patients with MIBC. These quality benchmarks were suggested to allow physicians, administrators, and payers to track, report, and improve outcomes of MIBC. Our results showed the treatment quality indicators were less likely met in URR compared to Metro areas, with subsequent impact on the survival outcomes.

    Mitigating residence-based health disparities requires implementation of different strategies to achieve equitable rural health care. This includes diffusion of evidence-based practices in rural communities and integration of quality improvement initiatives (e.g., the Quality Improvement Networks/Organizations Program), improving access to care, advancing telehealth and telemedicine, empowering patients’ decision-making tools and leveraging partnerships with tertiary care centers.

    Our results should be interpreted within the inherent limitations relative to the observational retrospective nature of the database. The NCDB does not capture detailed information on performance status, comorbid conditions and treatment-related complications, which may affect the treatment utilization and survival outcomes. Moreover, cancer-specific survival couldn’t be estimated as such data is not captured in the database. We also used zip code-level measures of socioeconomic data which may not reflect patient-specific status. Finally, our findings can only be generalized to facilities participating in the NCDB and may represent a biased sample of facilities.

    CONCLUSIONS

    URR residency was associated with increased time to treatment and lower OS among patients with MIBC. This survival disparity was consistent across patients who underwent RC and those who received CRT. Although there were no differences in the likelihood of receiving RC or CRT based on residence area, metro populations were more likely to meet quality treatment benchmarks. Additional investigations are required to assess the underlying mechanisms and develop strategies to address and minimize these disparities.

    SUPPLEMENTARY MATERIAL

    Supplementary material can be found via https://doi.org/10.4111/icu.20230125.

    Supplementary Table 1

    Classification of rurality using US Department of Agriculture 2013 Rural-Urban Continuum codes

    Click here to view.(18K, pdf)

    Notes

    CONFLICTS OF INTEREST:The authors have nothing to disclose.

    FUNDING:None.

    AUTHORS’ CONTRIBUTIONS:

    • Research conception and design: Furkan Dursun, Ahmed Elshabrawy, and Ahmed M. Mansour.

    • Data acquisition: Ahmed Elshabrawy and Hanzhang Wang.

    • Statistical analysis: Hanzhang Wang and Ahmed M. Mansour.

    • Data analysis and interpretation: John L. Gore and Ahmed M. Mansour.

    • Drafting of the manuscript: Furkan Dursun and Ahmed Elshabrawy.

    • Critical revision of the manuscript: Dharam Kaushik, Michael A. Liss, Robert S. Svatek, John L. Gore, and Ahmed M. Mansour.

    • Administrative, technical, or material support: Ahmed M. Mansour.

    • Supervision: Ahmed M. Mansour.

    • Approval of the final manuscript: all authors.

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    MeSH Terms
    Benchmarking
    Chemoradiotherapy
    Cystectomy
    Health Policy
    Humans
    Logistic Models
    Lymph Node Excision
    Margins of Excision
    Neoadjuvant Therapy
    Resource Allocation
    Rural Population
    Urban Population
    Urinary Bladder Neoplasms
    Urinary Bladder*
    Metrics
    Share
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