Root Causes and Modifiability of 30-Day Hospital Readmissions after Radical Cystectomy for Bladder Cancer Andrew C. James,* Jason P. Izard, Sarah K. Holt, Joshua K. Calvert, Jonathan L. Wright, Michael P. Porter and John L. Gore From the Department of Urology, University of Kentucky School of Medicine, Lexington, Kentucky (ACJ), Department of Urology, Queens University, Kingston, Ontario, Canada (JPI), Department of Urology, University of Washington School of Medicine (SKH, JKC, JLW, MPP, JLG) and Puget Sound Veterans Affairs Health Care System (MPP), Seattle, Washington

Abbreviations and Acronyms CCI ¼ Charlson comorbidity index LOS ¼ length of stay RC ¼ radical cystectomy SNF ¼ skilled nursing facility VTE ¼ venous thromboembolic event Accepted for publication October 23, 2015. No direct or indirect commercial incentive associated with publishing this article. The corresponding author certifies that, when applicable, a statement(s) has been included in the manuscript documenting institutional review board, ethics committee or ethical review board study approval; principles of Helsinki Declaration were followed in lieu of formal ethics committee approval; institutional animal care and use committee approval; all human subjects provided written informed consent with guarantees of confidentiality; IRB approved protocol number; animal approved project number. * Correspondence: Department of Urology, University of Kentucky School of Medicine, 800 Rose St., Room MS269, Lexington, Kentucky 40536-0298 (telephone: 859-323-6679; FAX: 859323-1944; e-mail: [email protected]).

See Editorial on page 821. Editor’s Note: This article is the second of 5 published in this issue for which category 1 CME credits can be earned. Instructions for obtaining credits are given with the questions on pages 1176 and 1177.

Purpose: Radical cystectomy is associated with high complication and rehospitalization rates. An understanding of the root causes of hospital readmissions and the modifiability of factors contributing to readmissions may decrease the morbidity associated with radical cystectomy. We characterize the indications for rehospitalization following radical cystectomy, and determine whether these indications represent immutable patient disease and procedure factors or whether they are modifiable. Materials and Methods: From MarketScanÒ databases we identified patients younger than 65 years with a diagnosis of bladder cancer who underwent radical cystectomy between 2008 and 2011 and were readmitted to the hospital within 30 days of radical cystectomy. All associated ICD-9 codes in the index admission, subsequent outpatient claims and readmission claims were independently reviewed by 3 surgeons to determine a root cause of rehospitalization. Causes were broadly categorized as medical, surgical or infectious, and reviewers determined whether the readmission was modifiable. Multivariate logistical regression models were used to identify factors associated with rehospitalization. Results: A total of 1,163 patients were included in the study and 242 (21%) were readmitted to the hospital within 30 days. Of these readmissions 26% were considered modifiable (kappa¼0.71). Of the nonmodifiable readmissions an infectious cause accounted for 52% and a medical cause accounted for 48%, whereas of the modifiable readmissions 62% were due to surgical causes, 30% to medical and 8% to infectious causes. On multivariate analysis only discharge to a skilled nursing facility was associated with modifiable (OR 6.12, 95% CI 2.32e16.14) or nonmodifiable (OR 3.27, 95% CI 1.63e6.53) hospital readmissions. Conclusions: The majority of rehospitalizations after radical cystectomy are attributable its inherent morbidity. However, optimization of aspects of pericystectomy care could minimize the morbidity of radical cystectomy. Key Words: patient readmission, urinary bladder neoplasms, cystectomy, complications, treatment outcomes

HOSPITAL readmissions are a major contributor to health care expenditures in the United States. Almost 20% of Medicare beneficiaries were



rehospitalized within 30 days of discharge at a cost of $17.4 billion in the years 2003 to 2004.1 Although estimates of the proportion of

0022-5347/16/1954-0894/0 THE JOURNAL OF UROLOGY® Ó 2016 by AMERICAN UROLOGICAL ASSOCIATION EDUCATION AND RESEARCH, INC. Vol. 195, 894-899, April 2016 Printed in U.S.A.


readmissions that are modifiable vary considerably based on the patient population and methodology, a 2011 review of 34 studies found a median of 27% of readmissions were potentially modifiable.2 In an attempt to decrease the health and financial burden of the treatment of disease, hospital readmissions have been increasingly targeted by policy makers as demonstrated by recent penalties for readmissions for certain diagnoses and procedures.3 Despite improvements in mortality associated with radical cystectomy for bladder cancer, this operation is still associated with considerable morbidity. For patients with muscle invasive bladder cancer RC remains the gold standard of treatment, providing excellent local control and conferring long-term survival.4 Nevertheless, RC is associated with a 35% to 64% complication rate and a 26% to 35% rehospitalization rate.5e7 This may contribute to the finding that bladder cancer is the costliest cancer in terms of lifetime expenditures.8 We hypothesize that although many indications for rehospitalization after RC are inherent due to the extensive extirpative and reconstructive components of the surgery, a substantial proportion of these complications is modifiable. In this study we characterize reasons for rehospitalization after RC and determine whether these rehospitalizations could have been prevented. Understanding the mechanisms by which perioperative patient risk factors and treatment algorithms may be optimized could decrease the occurrence of these potentially modifiable complications.

METHODS Using MarketScan commercial databases we identified patients who underwent RC for a primary diagnosis of bladder cancer between 2008 and 2011. MarketScan comprises the inpatient and outpatient health insurance claims of more than 34 million enrollees annually from 150 employers and 13 commercial health plans across the United States. Patients older than 65 years may have dual coverage with Medicare with claims data not captured by MarketScan. Thus, we restricted our analysis to enrollees younger than 65. Procedure type and primary diagnosis were identified by CPT and ICD-9 procedure and diagnosis codes. Demographic information including age, gender, diversion type, CCI,9 length of index hospitalization, discharge disposition and receipt of neoadjuvant chemotherapy was collected. Rehospitalizations occurring within 30 days of RC were captured by MarketScan and the observed ICD-9 diagnosis and procedure codes for each readmission were analyzed to determine the primary reason for readmission. Readmission diagnoses were broadly categorized as medical, surgical or infectious. Medical causes included nonsurgical conditions such as failure to thrive, cardiac events, ileus and venous thromboembolic events. Surgical causes of readmission included any event incited by a


technical issue related to RC and/or the urinary diversion. Examples included readmissions with diagnosis and procedure codes suggesting anastomotic bowel leak, small bowel obstruction requiring re-exploration, ureteroenteric anastomotic stricture, fistulas associated with the bowel and/or urinary tract, and wound dehiscence requiring closure. The rehospitalization cause was categorized as infectious if the patient had a diagnosis code for any infection and did not have ICD-9 or procedure codes suggesting that a surgical factor contributed to the infection. Examples included patients with codes for urinary tract infection without the need for nephrostomy tubes, unspecified septicemia, intra-abdominal abscesses without a code for bowel leak, colitis and pneumonia. The identified inciting event and not the resulting sequelae served as the basis for categorization. For example, although a patient may have a code for pyelonephritis on hospital readmission, if a code for percutaneous nephrostomy tube placement was present, the root cause of rehospitalization was presumed to be surgical (ie ureteroenteric anastomotic stricture). In addition, readmission diagnoses were categorized by system type to better describe the root causes of these readmissions. Rehospitalizations associated with stoma complications were categorized as a genitourinary complication due to continuity with the urinary tract whereas anastomotic bowel leaks and bowel obstruction were categorized as gastrointestinal complications. To determine whether the primary diagnosis underlying each readmission was modifiable, 2 urologists independently reviewed the diagnosis and procedure codes for each rehospitalization. The reviewers then judged whether the rehospitalization could conceivably have been prevented from a provider perspective. Factors considered modifiable included readmissions attributable to surgical technique, or those that could have been avoided through optimal perioperative care such as judicious antibiotic administration, and VTEs which were presumed to be preventable through chemoprophylaxis. Modifiability was only considered from the perspective of the actions of providers. Factors potentially modifiable by the patient were not considered. A senior urologist reconciled cases in which the primary reviewers disagreed about modifiability. Multivariable logistical regression models were created to identify patient factors that were associated with modifiable or nonmodifiable readmission. We examined patient demographic and clinical characteristics. Patient demographic information included age, race/ethnicity and gender. Clinical covariates evaluated included LOS, burden of comorbid conditions, type of urinary diversion (ie continent orthotopic neobladder vs ileal conduit) and discharge disposition. Comorbidity indices were calculated using the Klabunde modification of the CCI.10 To ensure ascertainment of patient comorbidities we only included patients who were enrolled in MarketScan for 12 months before RC. We further excluded patients who underwent RC without a primary diagnosis of bladder cancer. A Cohen’s kappa score was calculated to determine the degree of inter-rater agreement between the 2 surgeons examining the modifiability of readmissions. This study qualified for a waiver of institutional review



board approval since the data are fully HIPAA (Health Insurance Portability and Accountability Act of 1996) compliant and completely de-identified.

RESULTS We identified 1,163 patients who underwent RC for bladder cancer between 2008 and 2011, of whom 242 (21%) were readmitted to the hospital within 30 days after RC (table 1). The majority of patients were male, and between 55 and 64 years old. Ileal conduit was the most common urinary diversion but 37% of patients underwent continent urinary reconstruction. Most patients had a CCI of 0 and 19% received neoadjuvant chemotherapy. There was agreement in the categorization of 211 (87%) rehospitalizations (kappa¼0.71). After reconciliation 178 readmissions (74%) were deemed nonmodifiable. Factors associated with hospital readmissions are shown in table 2. Discharge to a SNF was significantly associated with modifiable (OR 3.97, 95% CI 1.66e9.50) and nonmodifiable (OR 2.91, 95% CI 1.52e5.57) readmissions. Continent urinary diversion was significantly associated with nonmodifiable readmission (OR 1.46, 95% CI 1.04e2.04). On multivariable analysis discharge to a SNF remained significantly associated with modifiable and nonmodifiable readmissions.

Table 1. Characteristics of study sample

No. pts Age: Less than 50 50e54 55e59 60e64 Gender: M F Diversion type: Ileal conduit Neobladder Unknown CCI: 0 1 2 or Greater LOS (days): Less than 7 8e11 12+ Discharge status: SNF Home Unknown Neoadjuvant chemotherapy:* No Yes

No. No Readmission (%)

No. Nonmodifiable Readmission (%)

No. Modifiable Readmission (%)

921 (100)

178 (100)

64 (100)

96 151 243 431

(10.4) (16.4) (26.4) (46.8)

17 22 61 78

(9.6) (12.4) (34.3) (43.8)

7 (10.9) 15 (23.4) 16 (25) 26 (40.6)

705 (76.5) 216 (23.5)

141 (79.2) 37 (20.8)

52 (81.3) 12 (18.8)

505 (54.8) 330 (35.8) 86 (9.3)

83 (46.6) 79 (44.4) 16 (9)

37 (57.8) 21 (32.8) 6 (9.4)

616 (66.9) 192 (20.8) 113 (12.3)

133 (74.7) 28 (15.7) 17 (9.6)

44 (68.8) 15 (23.4) 5 (7.8)

438 (47.6) 305 (33.1) 178 (19.3)

76 (42.7) 68 (38.2) 34 (19.1)

29 (45.3) 26 (40.6) 9 (14.1)

28 (3) 841 (91.3) 52 (5.6)

15 (8.4) 155 (87.1) 8 (4.5)

7 (10.9) 53 (82.8) 4 (6.3)

758 (82.3) 163 (17.7)

138 (77.5) 40 (22.5)

51 (79.7) 13 (20.3)

* Defined as receipt of doxorubicin, methotrexate, vinblastine, cisplatin, carboplatin or gemcitabine within 6 months of RC.

The root cause of the rehospitalization was medical in 104 (43%) patients, surgical in 41 (17%) and infectious in 97 (40%). Among patients whose readmissions were categorized as nonmodifiable an infectious cause accounted for 52% of the readmissions and a medical cause accounted for 48% of the readmissions. By definition, all surgical readmissions were considered modifiable. Of the modifiable readmissions 63% were categorized as having a surgical cause, 29% a medical cause and 8% an infectious cause. The largest proportion of all cause rehospitalizations was due to genitourinary diagnoses (38%) while gastrointestinal diagnoses were the second most common (31%) (see figure). These diagnoses were also the most common contributors to unpreventable rehospitalizations (34% and 27%, respectively). VTEs were a common cause of preventable rehospitalizations (28%). Among patients with an infectious cause of hospital readmission, most involved the urinary tract (63%), whereas 20% of infectious readmissions were for gastrointestinal or other intraabdominal infections. Among patients with a surgical cause of readmission most also involved the urinary system (54%), with 29% of surgical readmissions for gastrointestinal complications and 15% for wound complications. We stratified modifiable causes of readmission by urinary diversion type, and found that gastrointestinal complications and VTEs were the most common indication for rehospitalization after continent urinary diversion (gastrointestinal complications and VTEs 38%, genitourinary diagnoses 19%). Among patients undergoing ileal conduit diversion, urinary complications were the most common indication for rehospitalization (43% vs 21% for VTEs and 19% for gastrointestinal diagnoses).

DISCUSSION We show that more than 75% of rehospitalizations after RC in this relatively younger, healthy cohort are likely nonmodifiable. In addition, given that rehospitalization within 30 days of RC was not associated with comorbidity, age, gender, receipt of neoadjuvant chemotherapy or diversion type, our study indicates that the majority of rehospitalizations are due to the inherent morbidity associated with this operation, and are largely independent of patient and treatment variables. Importantly, our findings reflect a substantial readmission burden in a younger, privately insured population compared to typical RC series as most of our patients had minimal comorbidities. Furthermore, we were able to categorize the root causes of readmissions, and found that medical and surgical



Table 2. Multivariate logistical regression analysis of factors associated with hospital readmission after RC Modifiable Readmissions

Age: Less than 50 50e54 55e59 60e64 Gender: M F CCI: 0 1þ LOS (days): 7 or Less 8e11 12þ Discharge status: Home SNF Diversion type: Ileal conduit Neobladder Neoadjuvant chemotherapy: No Yes

Nonmodifiable Readmissions

Unadjusted OR (95% CI)

Adjusted OR (95% CI)*

Unadjusted OR (95% CI)

Adjusted OR (95% CI)*

Ref 1.36 (0.54e3.46) 0.90 (0.36e2.26) 0.83 (0.35e1.96)

Ref 1.30 (0.50e3.39) 0.91 (0.36e2.31) 0.67 (0.27e1.65)

Ref 0.82 (0.42e1.62) 1.42 (0.79e2.55) 1.02 (0.58e1.81)

Ref 0.87 (0.44e1.74) 1.37 (0.75e2.50) 1.00 (0.56e1.80)

Ref 0.75 (0.39e1.44)

Ref 0.76 (0.39e1.48)

Ref 0.86 (0.58e1.27)

Ref 0.87 (0.57e1.31)

Ref 0.94 (0.70e1.28)

Ref 0.94 (0.68e1.29)

Ref 0.87 (0.72e1.07)

Ref 0.87 (0.70e1.08)

Ref 1.29 (0.74e2.23) 0.76 (0.35e1.96)

Ref 1.20 (0.67e2.14) 0.49 (0.20e1.19)

Ref 1.28 (0.90e1.84) 1.10 (0.71e1.71)

Ref 1.35 (0.93e1.96) 0.96 (0.59e1.54)

Ref 3.97 (1.66e9.50)

Ref 6.12 (2.32e6.14)

Ref 2.91 (1.52e5.57)

Ref 3.27 (1.63e6.53)

Ref 0.87 (0.50e1.51)

Ref 0.77 (0.42e1.40)

Ref 1.46 (1.04e2.04)

Ref 1.30 (0.90e1.86)

Ref 1.19 (0.63e2.23)

Ref 1.29 (0.67e2.48)

Ref 1.35 (0.91e1.99)

Ref 1.41 (0.94e2.12)

* Model included all variables.

Frequency of readmission contribuƟon (%)

causes contributed to the majority of all cause readmissions, and that surgical causes, not postoperative practice variations, contributed to the majority of potentially modifiable readmissions. By characterizing the root causes of readmission and determining the modifiability of readmissions, we can identify targets for quality improvement that may decrease the burden associated with RC. Several previous studies have examined complication and rehospitalization rates after RC. The 30-day mortality in contemporary series has decreased to 1% to 3.9%7,11e13 from 2.4% to 15% in series before 1990, but minor and major complications occur in up to 50% of patients treated with RC.6,14 Because the patient population undergoing RC is generally older, with comorbid conditions common among the elderly, patients treated with RC 45 40 35 30 25 20 15







Contribution of root causes of rehospitalization by system

are subject to medical complications such as respiratory and cardiovascular events in addition to surgical/technical complications related to cystectomy and urinary diversion. Readmissions resulting from these complications are likewise common. Stimson et al reviewed patients undergoing RC with a 90-day rehospitalization rate of 26%, and determined that gender and age adjusted CCI were independent predictors of rehospitalization.6 Hu et al studied the diagnoses associated with hospital readmission after radical cystectomy, and the timing of and factors associated with rehospitalizations.15 In their population of 1,782 patients 26% were readmitted to the hospital within 30 days of discharge after RC, with 67% of rehospitalizations occurring within 2 weeks of discharge. In addition, readmitted patients were more likely to have experienced a complication during the index admission. Although these studies thoroughly characterized types and rates of complications as well as causes of rehospitalization, they did not specifically examine the root causes of rehospitalizations and the modifiability of the diagnoses that contributed to the readmission. Our study indicates that the majority of rehospitalizations following RC are provider independent, and the high complication and rehospitalization rates associated with RC are inherent to the morbidity of the procedure. The majority of all cause readmissions were due to an underlying medical cause, and an infectious cause was the inciting event in a large proportion of cases. Surgical causes



precipitated readmission in the fewest cases. When further substratifying readmissions on the basis of modifiability, an underlying infectious diagnosis was the leading contributor to nonmodifiable readmissions while a medical cause contributed to the remainder. No nonmodifiable readmissions were considered the result of a surgical cause by virtue of the definition used for a nonmodifiable readmission. Of those readmissions classified as modifiable, the majority were attributable to a surgical cause while an infectious cause contributed the smallest number of rehospitalizations in this group. Although most hospital readmissions were considered nonmodifiable, we identified several potential opportunities to optimize peri-cystectomy care and minimize morbidity after RC. These include VTE chemoprophylaxis administration, appropriate perioperative antibiotic administration and surgical technique. Of the 21% of patients who were readmitted within 30 days of RC, 2% were readmitted with Clostridium difficile colitis, 7.4% due to VTEs, 9% due to surgical factors involving urinary diversion or ureteroenteric anastomosis and 2% with wound dehiscence. Our findings regarding the contributions of VTEs and C. difficile colitis as potentially modifiable factors are consistent with those of a recent study by Revels et al, showing that hospitals performing major oncologic resections that were identified as low mortality hospitals had significantly higher use of postoperative VTE chemoprophylaxis compared with high mortality hospitals.16 In addition, Revels et al found that high mortality hospitals were more likely to continue perioperative antibiotics for longer than 24 hours postoperatively. Extended prophylaxis can increase the risk of antibiotic associated infectious colitis,17 and this association may be more important for procedures like RC with a long postoperative LOS.18 While the majority of readmissions in our study were deemed nonmodifiable, we were able to quantify the contribution of potential modifiable causes of rehospitalization, facilitating an understanding of the degree of improvement in rehospitalization that may be observed with the optimization of care. Initiatives that promote appropriate antibiotic and VTE prophylaxis administration as well as improvement in aspects of surgical technique may have a substantial impact on the hospital readmission burden. While patient comorbidities such as diabetes, obesity, nutritional factors and smoking may contribute to readmissions deemed modifiable, we highlight areas in which a particular emphasis on technique and management may decrease rehospitalizations. There are several important limitations that should be noted when interpreting our findings. Our data are based on an administrative claims database and, thus, are dependent on appropriate

coding for diagnoses and procedures to determine the causes of each rehospitalization. Using billing codes and administrative data as a substitute for clinical data may lead to misclassification of the cause or modifiability of the readmissions. In addition, data on antibiotic duration and VTE prophylaxis were not available for this study. Prior studies estimated that administrative claims data overestimated the modifiability of postoperative readmissions compared with clinical data.2 Thus, the magnitude of potential improvement in rehospitalization rates with attention to surgical and perioperative care practice quality may be lower than we anticipated. Next, our population was restricted to patients younger than 65 years and their status as employed beneficiaries affirms their likely good functional status. Given that most diagnoses of bladder cancer occur during the eighth decade of life and that previous reports have demonstrated an increased risk of early complications and 30-day rehospitalization rates in elderly populations, our findings may not be entirely applicable to a considerable proportion of patients who undergo RC.19e21 Additionally, the readmission burden after RC may be lessened in ways not examined in our study, such as decreasing the intensity of readmission through earlier diagnosis of complications as well as optimizing post-discharge protocols with improved followup timing and earlier intervention.22 Lastly, our classification of readmission modifiability relied on subjective interpretation. We attempted to minimize this limitation by having 2 surgeons independently review each readmission. Interobserver agreement between the 2 surgeons was high with a kappa score of 0.71. Despite these limitations we found that RC is associated with considerable morbidity in a relatively young and healthy patient population. Although the majority of hospital readmissions after RC are not modifiable, emphasis on appropriate VTE prophylaxis, judicious perioperative antibiotic administration and rigorous surgical technique may alleviate some of the burden associated with rehospitalization after RC.

CONCLUSIONS The majority of rehospitalization after RC is attributable to the inherent morbidity of the procedure. Even in a young, healthy population the complications and resulting rehospitalizations associated with RC are substantial. However, optimization of aspects of peri-cystectomy care, particularly regarding VTE chemoprophylaxis administration, appropriate perioperative antibiotic administration and improvements in surgical technique, could minimize the morbidity associated with RC.



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Root Causes and Modifiability of 30-Day Hospital Readmissions after Radical Cystectomy for Bladder Cancer.

Radical cystectomy is associated with high complication and rehospitalization rates. An understanding of the root causes of hospital readmissions and ...
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