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Keywords:

  • hospitalization volume;
  • Crohn's disease;
  • inflammatory bowel disease;
  • mortality;
  • ulcerative colitis

Abstract

  1. Top of page
  2. Abstract
  3. Materials and methods
  4. Results
  5. Discussion
  6. REFERENCES

Background: We sought to determine patterns of hospitalizations for inflammatory bowel disease (IBD) to centers that regularly admit high volumes of IBD patients and whether they impacted health outcomes.

Methods: We queried US hospital discharges in the Nationwide Inpatient Sample to identify admissions with a primary diagnosis of Crohn's disease (CD) or ulcerative colitis (UC) between 1998 and 2004. We determined patterns and predictors of hospitalization at high IBD volume admission centers (HIVACs) (≥145 IBD admissions annually) and assessed their impact on mortality.

Results: Over 7 years the proportion of patients admitted to HIVACs increased from 2.3% to 14.8%. IBD patients were less likely to be admitted to an HIVAC if they were insured by Medicare (odds ratio [OR] 0.74; 95% confidence interval [CI]: 0.65–0.83) or Medicaid (OR 0.71; 95% CI: 0.60–0.84), or were uninsured (OR 0.42; 95% CI: 0.30–0.58) compared with those privately insured. Neighborhood income above the national median favored admission to an HIVAC (OR 1.99; 95% CI: 1.46–2.71). In-hospital mortality was lower among HIVACs compared to non-HIVACs (3.5/1000 versus 7.2/1000, P < 0.0001) and was persistent after adjustment for surgery status, age, comorbidity, and health insurance (OR 0.65; 95% CI: 0.49–0.87). When stratified by diagnosis, mortality was reduced at HIVACs among CD (OR 0.58; 95% CI: 0.37–0.90) but not UC admissions.

Conclusions: There is a rising trend in hospitalizations for IBD at HIVACs, which confers mortality benefit for those with CD. Prospective studies are warranted to further explore the impact of these high-volume centers on IBD health outcomes.

(Inflamm Bowel Dis 2008)

Inflammatory bowel disease (IBD), comprising Crohn's disease (CD) and ulcerative colitis (UC), is a chronically relapsing condition in which patients require hospitalization for surgery or medically refractory disease. More than 70% of CD patients and a third of UC patients may require IBD-related surgery over a lifetime. These hospitalizations account for at least half of direct costs attributable to IBD.1–3

With the advent of biological therapy and less invasive laparoscopic surgical procedures for IBD over the last decade, it is not known whether there has been an increase in referrals to medical centers that admit high volumes of IBD patients and consequently have expertise in the management of IBD. For the inpatient treatment of certain conditions such as acute stroke, trauma, or ST-elevation myocardial infarction, regionalization of admission to high-volume specialty centers has led to improved mortality and health outcomes.4–8 In IBD patients, Kaplan et al9 have shown that hospitals that perform high volumes of colectomies have lower postoperative mortality rates.

The primary aims of this study were to expand and generalize the findings of the Kaplan study and to determine whether hospitals with very high volumes of IBD admissions, both surgical and nonsurgical, exhibited lower mortality compared to lower-volume hospitals. Furthermore, we sought to assess temporal patterns of hospitalization to these high IBD volume admission centers (HIVACs) and predictors of admission to these centers.

Materials and methods

  1. Top of page
  2. Abstract
  3. Materials and methods
  4. Results
  5. Discussion
  6. REFERENCES

Data Source

All data were extracted from the Nationwide Inpatient Sample (NIS) between 1998 and 2004. The NIS is maintained as part of the Healthcare Cost and Utilization Project (HCUP) sponsored by the Agency for Healthcare Research and Quality (AHRQ). These databases reflect a 20% stratified sample of non-federal, acute-care hospitals in the United States. The sampling frame includes community and general hospitals and academic medical centers comprising ≈90% of all hospital discharges in the US. Each data entry includes a unique identifier, demographic variables (defined as age, gender, and race/ethnicity, median income for ZIP code), source of admission, discharge disposition, primary and secondary diagnoses (up to 15), primary and secondary procedures (up to 15), primary insurance payers, total hospital charges, and length of stay. NIS data concurs with the National Hospital Discharge Survey, supporting data reliability.10

Eligibility Criteria

Our analysis included all hospital discharges between the years 1998 and 2004 with the following criteria: 1) were at least 5 years of age; 2) had either a) a primary diagnosis of inflammatory bowel disease (UC or CD) identified by the Clinical Modification of the International Classification of Diseases, 9th Revision (ICD-9-CM) code of 555.0-556.9, or b) a primary diagnosis of a complication of UC or CD (anemia, dehydration, electrolyte imbalance, gastrointestinal bleeding, malnutrition, megacolon, obstruction, intraabdominal abscess) with a secondary or tertiary diagnosis of UC or CD. We excluded children under 5 years because of the uncertainty of diagnosis in this subpopulation. We also excluded IBD hospitalizations in which the length of stay was 24 hours or less.

Predictor and Outcome Variables

The primary objective of this study was to determine whether hospital admission volume was associated with in-hospital mortality. Thus, we conducted a threshold analysis to determine whether there was a threshold number of IBD admissions that would confer a maximal mortality benefit. This analysis was performed by calculating the adjusted odds ratio (OR) for in-hospital mortality comparing hospitals that had greater or equal to N IBD admissions compared those that had less than N admissions, while varying N from 5 to 200 (Fig. 1). The OR was adjusted for age, comorbidity, gender, surgical status, health insurance type, and geographical location using a multivariate logistic regression model. The threshold number of admissions (Nthreshold) was defined as the inflection point at which the mortality OR first plateaus and this was determined to be 145. We then defined an HIVAC as a hospital whose annual number of IBD admissions was equal or greater than 145 (Nthreshold).

thumbnail image

Figure 1. The relationship between in-hospital mortality and annual number of hospital admissions for inflammatory bowel disease. The odds ratio for mortality and the 95% upper and lower confidence bands are shown on the y-axis as the cutoff point for number of hospital admissions is varied on the x-axis. The maximal mortality benefit is achieved with greater than 145 IBD admissions per year and plateaus thereafter.

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Health insurance type was derived from the primary payer indicated in the hospital discharge abstract, and “self-pay” referred to individuals who had no health insurance coverage. Case-mix adjustment was performed using the validated Deyo modification of the Charlson Index.11, 12 The Charlson Index is a widely used instrument used to characterize and adjust for disease burden and case-mix in administrative data. This scale incorporates 17 comorbid conditions that are weighted to yield a summary index.13 Patients who underwent colectomy were identified by the ICD-9-CM code 45.8, and ileal pouch anal anastomosis (IPAA) was identified by the additional code for pouch formation (45.95). Bowel resection status was ascertained by ICD-9-CM procedure codes and included small and large bowel resections and anastomotic revisions (45.61–45.63, 45.71–45.79, 45.8, 46.93–46.94). The validity of these codes for major surgical procedures has been previously documented.14

Statistical Analysis

Data were analyzed using the Stata 9.0 SE software package (College Station, TX). Analyses took into account the stratified 2-stage cluster design using Stata's SVY (survey data) commands and incorporating individual discharge-level weights. Two-way χ2 analyses were performed to determine whether the proportion of IBD admissions hospitalized in HIVACs differed by calendar year. We used logistic regression with time as a dependent variable to identify time trends in hospitalization to HIVACs. Additional multiple logistic regression analysis was performed to identify other demographic and clinical factors in addition to calendar year that were associated with the admission to an HIVAC. These variables included age, gender, neighborhood income, primary health insurance carrier, Charlson Index, calendar year, and geographic region. Multiple logistic regression was also applied to determine the impact of admission to an HIVAC on in-hospital mortality while adjusting for age, gender, health insurance carrier, neighborhood income, whether the patient underwent resective bowel surgery or parenteral nutrition, calendar year, and hospital characteristics. Data for length of stay (LOS) and hospital charges were nonnormal and transformed into logarithmic scale. The unpaired t-test, using the distribution of the log-transformed LOS and total charges, was used to assess statistical significance of differences between groups. Multiple linear regression was similarly used to assess for associations between admission to an HIVAC and average LOS and hospital charges while adjusting for confounders.

Ethical Considerations

The analysis of the NIS uses completely unidentified data with no risk of loss of confidentiality and an initial expedited review by the Institutional Review Board of the Johns Hopkins Medical Institutions deemed it exempt from further ethical review.

Results

  1. Top of page
  2. Abstract
  3. Materials and methods
  4. Results
  5. Discussion
  6. REFERENCES

Patient Characteristics

Demographic and clinical characteristics of admissions for IBD are shown in Table 1. Patients who were discharged from HIVACs were younger on average than those from non-HIVACs (39 years versus 45 years, P < 0.001) and more likely to be privately insured (73% versus 58%, P < 0.0001) and reside in neighborhoods with income greater than the national median (76% versus 65%, P = 0.02). Active fistulizing disease was more prevalent among CD admissions to HIVACs than non-HIVACs (16% versus 9%, P < 0.001).

Table 1. Baseline Characteristics of Patients Discharged from High IBD Volume Admission Centers (HIVACs) and non-HIVACs
Demographic VariablesNon-HIVAC (N = 95,500)HIVAC (N = 11,171)
  • HIVAC = High IBD volume admission center

  • *

    P < 0.01

  • **

    P < 0.05

Age (SE)44.6 (0.2)38.8 (0.7)**
Female Gender57%53%**
Race  
 White81%81%
 Non-white19%19%
Health Insurance  
 Private58%73%**
 Medicare24%14%**
 Medicaid10%9%**
 Self-Pay5%2%**
 Other3%2%**
Income Above Median65%76%*
Charlson Index0.30.2**
IBD Diagnosis  
 Crohn's disease62%62%
  Obstructing11%15%
  Fistulizing9%16%**
 Ulcerative colitis38%38%
Geographic Region  
 Northeast23%39%
 Midwest24%22%
 South36%35%
 West17%4%

Hospital Characteristics

HIVACs were concentrated in the Northeast and uncommon in the West, while non-HIVACs were more evenly distributed geographically (Table 2). These high-volume centers were exclusively located in urban settings. Compared to non-HIVACs, HIVACs were considerably more likely to be in the top tertile within their state for hospital bed size (88% versus 37%, P < 0.0001). The vast majority of HIVACs were teaching hospitals (91%), while one-fifth of non-HIVACs were teaching centers.

Table 2. Characteristics of High IBD Volume Admission Centers (HIVACs) and non-HIVACs
Demographic VariablesNon-HIVAC (N = 2803)HIVAC (N = 62)
  • HIVAC = High IBD volume admission center

  • *

    P < 0.05

  • **

    P < 0.001

Geographic Region  
 Northeast17%34%*
 Midwest29%22%*
 South35%40%*
 West19%4%*
Hospital size - top tertile37%88%**
Hospital Location  
 Rural38%0%**
 Urban62%100%**
Teaching hospital20%91%**

Patterns of Hospitalizations to HIVACs

Approximately 10.5% (n = 11,171) of all IBD admissions were hospitalized in HIVACs, and these proportions were similar for both CD (10.6%, n = 6,946) and UC (10.5%, n = 4,225). Over the 7-year study period the proportion of IBD admissions to HIVACs rose nearly 6-fold, from 2.3% to 14.8% (P = 0.007), reflecting an average annual 24% relative increase. This temporal trend was similar for both UC and CD (Fig. 2).

thumbnail image

Figure 2. Time trends in admission to high IBD volume admission centers (HIVACs). There is a rising trend in the proportion of IBD admissions admitted to HIVACs (P < 0.0001). When stratified by disease diagnosis (CD versus UC), time trends are nearly identical in both groups.

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Predictors of Admission to an HIVAC

Figure 3 shows the independent association of demographic and clinical predictors to likelihood of admission to an HIVAC. UC patients had slightly greater odds than CD patients of being admitted to an HIVAC (OR 1.12; 95% confidence interval [CI]: 1.03–1.23) but this association was eliminated when patients who had undergone IPAA were excluded. Increasing age and comorbidity were associated with increased likelihood of admission to a non-HIVAC. Compared to those privately insured, there were lower rates of HIVAC admissions among those with Medicare (OR 0.72; 95% CI: 0.63–0.83), Medicaid (OR 0.67; 95% CI: 0.57–0.79), and those who were uninsured (OR 0.35; 95% CI: 0.24–0.51). Neighborhood income that was greater than the national median was associated with increased odds of admission to an HIVAC (OR 1.79; 95% CI: 1.20–2.69). There were no statistically significant geographic variations in the likelihood of being admitted to an HIVAC. After multivariate adjustment, there was an annual average 28% rise in the odds of admission to an HIVAC over the 7-year period.

thumbnail image

Figure 3. Sociodemographic and clinical predictors for admission to a high IBD volume admission center (HIVAC). The adjusted odds ratios for the association between sociodemographic and clinical variables and the likelihood of admission to an HIVAC are graphically depicted (solid boxes) with corresponding 95% confidence intervals. Reference categories are shown as solid circles. These values are numerically shown to the right. Each odds ratio is simultaneously adjusted for all other variables.

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Procedural and Resource Utilization

The unadjusted rate of colectomy among UC patients admitted to HIVACs was higher than the rate among those admitted to non-HIVACs (22.1% versus 10.4%, P < 0.0001). After multivariate adjustment for demographic factors, comorbidity, health insurance, geographic region, hospital characteristics, and elective admission status, we found that hospital colectomy volume was itself a predictor of whether a UC patient underwent colectomy, with every incremental volume increase of 10 procedures being associated more than a 2-fold rise in the odds of colectomy (OR 2.08; 95% CI: 1.79–2.41). When colectomy volume and other confounders were accounted for, admission to an HIVAC was actually associated with a lower likelihood of undergoing colectomy (OR 0.35; 95% CI: 0.24–0.51). Among CD admissions, bowel resections were also more likely at HIVACs compared to non-HIVACs (32.1% versus 18.3%, P < 0.0001). However, after multivariate adjustment the association between admission to an HIVAC and bowel resection status was not statistically significant (OR 0.98; 95% CI: 0.81–1.18). The association between hospital bowel resection volume and likelihood of bowel resection, although statistically significant, was very clinically modest (OR 1.09; 95% CI: 1.05–1.13 for every additional 10 procedures). There were no differences in the utilization of colonoscopy (4.0% versus 4.4%, P = 0.41) or parenteral nutrition (9.2% versus 6.1%, P = 0.08) between the HIVAC and non-HIVAC groups, respectively.

The average length of stay was higher in the HIVAC compared to the non-HIVACs (7.5 versus 6.6 days, P < 0.001). The difference was due primarily to higher surgical rates among HIVACs and there was no difference in LOS after multivariate adjustment (2% difference in LOS, P = 0.45). Hospital charges were also increased at HIVACs compared to non-HIVACs ($30,010 versus $22,738, P = 0.0005). The differences in economic expenditure were largely attributable to higher crude surgical rates at HIVACs, but there was a persistent 14% higher average hospital charge among HIVACs compared to non-HIVACs (P = 0.01) even after multivariate adjustment.

In-hospital Mortality

Figure 1 demonstrates the relationship between hospital IBD admission volume and in-hospital mortality. A statistically significant reduction in odds of mortality is first observed in hospitals with 140 or more IBD admissions per year compared with those with less than 140 admissions (OR 0.68; 95% CI: 0.51–0.91). The mortality benefit plateaus with 145 IBD hospital admissions, and this cutoff was used to define HIVAC. Unadjusted mortality was lower in the HIVAC group compared to the non-HIVAC group for all IBD admissions (3.5/1000 versus 7.2/1000, P < 0.0001), CD admissions (2.3/1000 versus 4.8/1000, P = 0.002), and UC admissions (5.5/1000 versus 11.1/1000, P = 0.004). After multivariate adjustment for surgical status, age, gender, comorbidity, health insurance, geographic region, and use of parenteral nutrition, IBD admissions to HIVACs exhibited 35% lower odds of in-hospital mortality compared to non-HIVACs (OR 0.65; 95% CI: 0.49–0.87). The presence of surgery did not modify the effect of being admitted to an HIVAC on mortality (i.e., no statistical interaction). We conducted a sensitivity analysis restricting analyses to a subgroup of patients younger than 60 years who were less likely to have a diagnosis of ischemic colitis miscoded as IBD. In this subgroup the adjusted OR of in-hospital mortality among HIVACs compared to non-HIVACs was 0.29 (95% CI: 0.10–0.79). When stratified by IBD diagnosis, CD admissions to HIVACs also had a similar mortality benefit after multivariate adjustment for surgery and other mortality predictors (OR 0.58; 95% CI: 0.37–0.90). However, there was no statistically significant difference in in-hospital mortality between HIVACs and non-HIVACs among UC admissions following adjustment for surgery and other confounders (OR 0.68; 95% CI: 0.43–1.11).

Discussion

  1. Top of page
  2. Abstract
  3. Materials and methods
  4. Results
  5. Discussion
  6. REFERENCES

We have shown that CD patients admitted to hospitals with very high volumes of IBD admissions experienced 30% lower odds of in-hospital death than those admitted to lower-volume hospitals irrespective of surgical status. These findings expand previous findings of lower mortality among UC patients who had undergone colectomy and were admitted to centers with high colectomy volumes.15

Higher surgical volume has been shown consistently to be a predictor of perioperative health outcomes for a wide gamut of procedures.16–18 Additionally, surgical volume is not even necessarily specific to a particular procedure in order to confer benefit.19 These findings may suggest that there are other resources at high-volume hospitals aside from surgical expertise such as skilled nursing, ancillary specialty services, and intensive care units that contribute to reduced mortality. Our findings of correlation between mortality and IBD admissions independent of surgical status also implies that other nonsurgical factors play in a role in lower adverse outcomes. We hypothesize that HIVACs may have relatively greater access to resources including IBD medical specialists, multidisciplinary support by radiology, and nutritional services. Further prospective studies are necessary to elaborate on the specific mechanisms of reduced mortality within these high-volume centers.

Interestingly, we found that patients admitted to HIVACs were more likely to undergo IBD-related bowel resection. It may be that patients with greater disease severity are being admitted to these HIVACs. However, we also found that a hospital's colectomy volume was also a strong predictor of the likelihood of an individual admitted to that hospital receiving colectomy. We have previously shown considerable regional variation in colectomy rates suggesting that the indications for the procedure are ill-defined and subjective.20 In this context, colectomy volume may be an indicator of access to both colorectal surgeons and surgical resources and possibly institutional preference for surgical intervention. We found that after adjusting for these above factors the adjusted odds of undergoing colectomy was actually lower at HIVACs compared to non-HIVACs. One possible explanation may be that HIVACs may concurrently offer more effective medical alternatives to surgery. Unfortunately, the NIS database does not contain medication utilization data to address this hypothesis. Procedural volume had less of an impact on likelihood of CD-related bowel resections. Because surgery for CD is not curative, as for UC, and only performed when absolutely necessary for disease complications, these procedures may be less subject to physician preferences and institutional resources. This speculation is supported by our previous finding that regional variations in rates of bowel resection among hospitalized CD patients is considerably less than that observed for UC.21

Also noteworthy, are the rising trends in admissions to HIVACs that may reflect increasing regionalization of IBD care. As the armamentarium of IBD biological agents continues to grow and as more minimally invasive approaches to IBD surgery develop, we would expect that IBD inpatient care would become more specialized.22–24 This trend is supported by our data. It is disconcerting, however, that access to HIVACs is influenced by sociodemographic factors such as type of health insurance and income. These disparities are likely driven by geographic access. Those living in rural areas, which tend to be areas with lower income levels, have virtually no access to HIVACs.25 Even within urban areas, lower-income neighborhoods may be resource-poor, whereby residents may not have access to a nearby HIVAC. These local geographic barriers may be compounded by income-based barriers to transportation.26 The considerably lower rate of admission to HIVACs among those Medicaid recipients and the uninsured may additionally reflect lesser access to IBD subspecialists who regularly admit to HIVACs.

The main limitation of this study inherent to administrative data is potential misclassification of diagnosis based on diagnosis codes from a single hospitalization. Because the NIS data cannot be linked to medical records, we cannot validate ICD-9 coding for IBD diagnosis in the NIS dataset, though this has been accomplished elsewhere.27, 28 It is conceivable that ischemic colitis may have been miscoded as IBD more frequently at non-HIVACs than HIVACs, and that this may have led to a biased lower mortality at HIVACs. However, our sensitivity analyses restricted to a subgroup younger than 60 years who are unlikely to have ischemic colitis showed an even stronger mortality benefit for those hospitalized at HIVACs. Another substantial limitation of the NIS data is that there are no IBD-specific severity measures, and thus disease severity cannot be compared between HIVACs and non-HIVACs. Although it is possible that sicker IBD patients are admitted more frequently to non-HIVACs than HIVACs, this scenario is counterintuitive and unlikely.

Despite the limitations of this NIS dataset, it allows a comprehensive and national perspective on trends in the delivery of IBD inpatient care and its potential impact on health outcomes. The nature of these data is exploratory and certainly not sufficient to advocate regionalization of IBD healthcare, as has been done for other acute conditions. However, these findings should prompt further investigation using primary and prospective data to determine the specific mechanisms of mortality differences between HIVACs and non-HIVACs. These findings also underscore the need to develop practice guidelines and measures of quality of care for the inpatient management of IBD in order to reduce differences in outcomes between high and low IBD volume centers. Finally, we must take measures to understand and alleviate sociodemographic disparities in access to centers that implement more effective IBD healthcare delivery.

REFERENCES

  1. Top of page
  2. Abstract
  3. Materials and methods
  4. Results
  5. Discussion
  6. REFERENCES
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