Methods
In this nationwide, retrospective cohort study, we queried the Nationwide Readmissions Database (NRD) between 2016 and 2018 using International Classification of Diseases 10th Revision (ICD-10) to identify patients hospitalized for the following GI disorders: diverticular disease, irritable bowel syndrome (IBS), inflammatory bowel disease (IBD), chronic pancreatitis, esophageal disorders, gallbladder disease, gastroparesis, celiac disease, acute pancreatitis, functional GI disease, infectious gastroenteritis, noninfectious colitis, colorectal cancer, cholangitis,
Clostridioides difficile infection, gallbladder/biliary cancer, GI bleed, upper GI cancer, and pancreatic cancer (
Table A1). GI disorders were selected based on general classifications of commonly hospitalized discrete GI diagnoses. As this study focused on GI conditions, primary liver pathologies were not included. The NRD is a national database developed for the Healthcare Cost and Utilization Project that contains data from approximately 35 million discharges annually, while incorporating a complex sampling design that permits nationally representative estimates.
4- Nguyen N.H.
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Annual burden and costs of hospitalization for high-need, high-cost patients with chronic gastrointestinal and liver diseases.
The NRD uniquely allows for patient linkage to identify all hospitalizations for an individual patient across a given calendar year, but not across multiple calendar years. To provide adequate time for evaluation of 30-day readmission, discharge dates for index hospitalizations had to occur before December to be included in the study.
To ensure hospitalized individuals were admitted for a GI-specific diagnosis, only admissions with ICD-10 codes for GI diagnoses listed in the first 3 diagnosis positions were included. The comparison group of non-GI hospitalizations was composed of all individuals without a GI indication in the first 3 diagnosis positions. Hospitalizations with multiple GI conditions were counted separately for each condition. For each subject, the following patient-specific characteristics were also collected: age (grouped into 4 cohorts: age 0–20, 21–40, 41–60, and greater than 60 years), sex, Charlson-Deyo comorbidity index, primary payer (Medicare, Medicaid, private insurance, self-pay, no charge, other), and zip code income quartile. The Charlson-Deyo comorbidity index is a composite score of predefined comorbidities used as a representation of overall disease burden, which may influence outcomes.
5HCUP nationwide readmissions database (NRD).
Hospital-specific characteristics included hospital bed size (small, medium, large) and hospital location/teaching status (urban teaching, urban nonteaching, rural). These variables were incorporated into regression models as covariates.
Outcomes included LOS, hospital charges, 30-day all-cause readmission after index hospitalization, and inhospital death during index hospitalization. Hospital charges were estimated for the index hospitalization. Readmission excluded inhospital death or transfers. The annual number of patients hospitalized for each GI indication was estimated using weighted frequencies that provided nationally representative values. Multivariable linear regression was used to evaluate the outcomes of LOS and total hospital charges for each patient hospitalized for GI vs non-GI indications, while adjusting for age, sex, Charlson comorbidity index, payer source, zip code income quartile, hospital bed size, and hospital location/teaching status. Multivariable logistic regression was used to evaluate the outcomes of 30-day readmission and death for individual GI indications, as compared to non-GI indications collectively, adjusting for the same covariates. Statistical significance was defined with a threshold of 0.05. All analyses were performed using SAS version 9.4 (SAS Institute, Cary, North Carolina).
The University of California at Los Angeles Institutional Review Board deemed the study exempt due to de-identified population-level data obtained from the NRD (IRB #19-001212).
Discussion
In this nationwide analysis, we compared healthcare utilization metrics between patients hospitalized for specific GI indications and those collectively hospitalized for non-GI indications. We found that GI bleed, gallbladder disease, and diverticular disease were the most common indications for hospitalization, while celiac disease, cholangitis, and gallbladder/biliary cancer were the least common. Conditions associated with increased relative adjusted LOS were upper GI cancer, C difficile infection, functional GI disorders, gallbladder/biliary cancer, colorectal cancer, pancreatic cancer, IBD, cholangitis, and gastroparesis. Upper GI, colorectal, and gallbladder/biliary cancer along with functional GI disorders, gallbladder disease, and cholangitis were associated with increased adjusted hospital charges. All GI indications were associated with increased adjusted odds of 30-day readmission, and the GI indications associated with the highest adjusted odds for readmission were gastroparesis, gallbladder/biliary cancer, IBD, and cholangitis. Increased odds of adjusted inhospital mortality were found in upper GI cancer and pancreatic cancer.
Our findings have important implications for researchers, policy makers, and healthcare providers. Our finding that all GI indications were associated with increased odds of 30-day readmission when compared to non-GI indications collectively is novel and may guide future systems-based research. While prior research has identified risk factors for readmissions for individual diseases, it is unclear what is driving this readmission trend common to all GI disorders. Previously identified risk factors for individual disorders include lack of endoscopy on hospitalization and depression for ulcerative colitis, as well as polysubstance use, pancreatic neoplasms, or coexisting mental health disorders in acute and chronic pancreatitis.
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Predictive factors for and incidence of hospital readmissions of patients with acute and chronic pancreatitis.
The presence of any neoplasm is a risk factor for readmission for all hospitalized internal medicine patients.
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Predictors of hospital readmissions for ulcerative colitis in the United States: a national database study.
For gastroparesis, a condition associated with multiple metrics of increased healthcare utilization in our study, prior research has demonstrated that post-discharge care fragmentation is a key driver of readmissions, LOS, and hospitalization costs for gastroparesis, an issue that may be driving utilization for other GI disorders as well.
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Predictors of hospital readmissions in internal medicine patients: application of Andersen's model.
Patients with GI disorders may also struggle with follow-up care due to limited availability of GI subspecialty care. Causes common to all GI disorders, including systemic causes such as poor post-discharge follow-up require further investigation.
Another consideration is the chronic nature of GI conditions that may lead to increased risk of readmission. Between 2005 and 2018, the most common discharge diagnoses were septicemia, heart failure, osteoarthritis, childbirth complications, and pneumonia.
10Frequency of hospital readmission and care fragmentation in gastroparesis: a nationwide analysis.
Apart from osteoarthritis, these conditions have acute or acute-on-chronic presentations that may have lower risk of admission than the GI conditions in our study, many of which are chronic, recurrent diseases that may have increased likelihood of readmission. As noted previously, the chronic, recurrent nature of GI disorders may explain why post-discharge care fragmentation may affect utilization among GI conditions more than non-GI conditions. This highlights the need for future research into various patient-specific, GI-specific, and systems-level factors that predict hospital admission for all GI conditions.
Our study highlights several individual conditions associated with high healthcare utilization for which research should be done to identify interventions that may decrease utilization burden. For gastric cancer (part of upper GI cancer), 5-year survival remains below 30% for all cases and below 5% for those diagnosed with metastatic disease.
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Causes of hospitalization in the USA between 2005 and 2018.
Our study demonstrates that patients with gastric cancer still have increased LOS, hospitalization costs, and readmission risk relative to patients with non-GI indications. There are no US screening guidelines for gastric cancer, and current American Gastroenterological Association guidelines for surveillance of premalignant gastric cancer are reported to be based on very low quality of evidence.
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Burden of gastric cancer.
Future research is warranted into screening and surveillance programs despite the low incidence of gastric cancer given the ongoing resource burden demonstrated.
Cholangitis was also associated with increased healthcare utilization across multiple metrics, specifically LOS, total charges, and readmissions, though was infrequently an indication for hospitalization. The ICD-10 coding in our study (
Table A1) defines cholangitis as bacterial or primary sclerosing cholangitis (PSC). For patients with PSC, the lack of effective medical therapies and long-term complications of cirrhosis, biliary strictures, and cholangiocarcinoma likely contribute to the significant healthcare burden seen in our study.
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To our knowledge, there are no studies addressing utilization patterns of bacterial cholangitis or PSC. Our findings demonstrate that cholangitis, although an uncommon indication for hospitalization, remains a significant contributor to healthcare utilization, the drivers of which warrant future research.
Using our study, policy makers may be able to concentrate their efforts on changes to reduce the resource burden among the conditions with the highest utilization metrics. Intraluminal GI malignancies (upper GI and colorectal cancer) were associated with increased utilization burden across multiple metrics. Despite existing American Gastroenterological Association screening guidelines
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Primary sclerosing cholangitis.
for esophageal pre-malignant lesions, 37% of patients are diagnosed with metastatic esophageal cancer (part of upper GI cancer) at initial diagnosis.
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Adherence to existing guidelines for Barrett’s esophagus is improving, but remains relatively low overall, especially in community practice settings.
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Prior studies have shown an association with lower socioeconomic status and decreased adherence to screening guidelines, suggesting limitations in access to care.
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Policy changes addressing potential access to endoscopy as well as increased incentives, potentially through changes in payment structure, for providers who adhere to existing Barrett’s screening guidelines may reduce the late-stage presentation of esophageal cancer and associated costs.
With improvement in colon cancer screening, US incidence has been decreasing over the past 3 decades with diagnosis at earlier stages of disease.
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Despite this, there exist significant racial disparities in costs for colon cancer, with Black colorectal cancer patients having higher costs during every phase of care compared to White patients.
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This may be a result of persistently low rates of colorectal cancer screening among Black populations due to patient, provider, and systems-level barriers.
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Racial/ethnic disparities in colorectal cancer treatment utilization and phase-specific costs, 2000-2014.
While we were unable to stratify by race or ethnicity due to limitations in the NRD, policy changes addressing these barriers may help mitigate ongoing hospital-related healthcare costs demonstrated in this study.
For individual gastroenterology providers, our study has important implications for clinical practice. In particular, focusing on non-luminal GI cancers (pancreatic, gallbladder/biliary) our study demonstrated increased healthcare utilization across most utilization metrics. Five-year survival rates for gallbladder, biliary, and pancreatic cancer are poor, at 19%, 9%, and 9% respectively, with over 40% of cases presenting with distant disease at diagnosis.
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Gallbladder cancer incidence and mortality, United States 1999-2011.
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Cancer statistics, 2022.
There are limited data assessing the burden of gallbladder and biliary cancer, but recent studies have demonstrated that medical costs associated with pancreatic cancer have been rising, driven primarily by treatment of advanced cancer along with inpatient costs, which have nearly tripled over the last decade.
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Burden of pancreatic cancer: from epidemiology to practice.
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Inpatient burden of pancreatic cancer in the United States: an analysis of national trends in the United States from 1997 to 2012.
For gallbladder, biliary, and pancreatic cancer, the lack of effective screening measures, presence of advanced stage at diagnosis, and poor prognostic outcomes of these diseases highlight the importance of palliative care interventions to reduce healthcare utilization burden. It is well-established that palliative care leads to higher quality of life and lower costs for patients with poor-prognosis cancer.
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Healthcare costs, treatment patterns, and resource utilization among pancreatic cancer patients in a managed care population.
Among pancreatic, gallbladder, and extrahepatic cholangiocarcinoma, there are low rates of palliative care consults (<15%), but there are significant reductions in cost of care in those who do engage with palliative care.
27- Brumley R.
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Palliative care and end-of-life health care utilization in elderly patients with pancreatic cancer.
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Inpatient palliative care utilisation among patients with gallbladder cancer in the United States: a 10-year perspective.
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Inpatient palliative care is less utilized in rare, fatal extrahepatic cholangiocarcinoma: a ten-year national perspective.
These data suggest timely referral and use of palliative care in the appropriate clinical setting may serve as a way to both improve patient-centered outcomes such as quality of life while also reducing healthcare utilization.
Our study has several strengths. The NRD allowed for weighted estimates of all hospitalizations throughout the United States, which allows for generalizability of our findings to a variety of different practice settings, geographic locations, ages, and socioeconomic backgrounds. Another strength of our study was its novelty as the first to compare relative inhospital utilization metrics between GI indications and non-GI indications. By controlling for various characteristics, including hospital, patient, and socioeconomic characteristics, we were able to make more generalizable conclusions that may be important in guiding future policy and research.
Limitations of this study included its retrospective and observational nature, with the inability to determine causation. Another limitation included the inability to track patients over multiple calendar years, which may lead to multiple hospitalizations counted for an individual patient over multiple years. However, given that the measure of utilization in our study is patients hospitalized per year, this would not be expected to significantly alter our conclusions. There is a possibility that despite a GI indication listed as one of the first 3 diagnosis positions, a patient may have been hospitalized for a primarily non-GI related concern depending on the coding leading to overrepresentation of certain indications. Given the large number of possible GI conditions, we had to group related conditions into categories (eg, esophageal disorders). This action invariably led to some loss of granularity and introduced the risk of combining 2 or more GI conditions with differing impact on healthcare utilization. Another limitation of our study is that it did not include outpatient measures of healthcare utilization—however, given that hospitalizations comprise a significant portion of healthcare costs, our results still provide important data to guide policy, funding, and resource management. Prior research has additionally demonstrated disparities in utilization between malignancies, however, the NRD did not allow for analysis of race or ethnicity data, and future research should address these disparities. Given the use of a nationwide database, our study was limited by the lack of certain granular data such as disease severity, cancer subtypes, and presence of metastatic disease, which would be helpful in targeting future efforts.
Article info
Publication history
Published online: January 09, 2023
Accepted:
January 5,
2023
Received:
December 6,
2022
Footnotes
Conflicts of Interest: The authors disclose no conflicts.
Funding: We gratefully acknowledge funding by the National Institute on Alcohol Abuse and Alcoholism of the National Institutes of Health under award number K23AA028297 (Chen) and Gilead Sciences Research Scholars Program in Liver Disease—The Americas (Chen). The content is solely the authors’ responsibility and does not necessarily represent the official views of the National Institutes of Health or other sponsors.
Ethical Statement: The corresponding author, on behalf of all authors, jointly and severally, certifies that their institution has approved the protocol for any investigation involving humans or animals and that all experimentation was conducted in conformity with ethical and humane principles of research.
Data Transparency Statement: Data, analytic methods, and study materials will not be made available to other researchers.
Reporting Guidelines: SAGER, STROBE.
Copyright
© 2023 Published by Elsevier, Inc on behalf of the AGA Institute