Summary
Background
Psoriasis is associated with cardiovascular disease, inflammatory bowel disease (IBD), metabolic syndrome, and psychiatric disease. Furthermore, psoriasis is associated with immune dysregulation and systemic inflammation.
Objective
To determine the association of psoriasis and psoriatic arthritis with IBD and the association of the combination of psoriasis or psoriatic arthritis with IBD and other gastrointestinal illnesses.
Methods
Discharge data from the 2000–2014 Nationwide Inpatient Sample, Healthcare Cost and Utilization Project (HCUP), which approximates a 20% stratified sample of all US hospitalizations, were analyzed. Multivariable logistic regression was used to examine the association between psoriasis and psoriatic arthritis with IBD and 23 gastrointestinal illnesses adjusting for sociodemographic characteristics.
Results
Psoriasis was associated with IBD (Crohn’s disease adjusted odds ratio (aOR)=2.13, 95% confidence interval (CI) [2.0–2.3], p<0.001). When adjusting for sociodemographics and IBD, psoriasis was associated with 21 of 23 gastrointestinal diseases examined, most notably celiac disease, autoimmune hepatitis, and non-alcoholic fatty liver disease. Psoriatic arthritis was also associated with IBD (Crohn’s disease, aOR=1.95, 95% CI [1.7–2.2], and ulcerative colitis, aOR= 2.66, 95% CI [2.4–2.9]).
Conclusion
Psoriasis and psoriatic arthritis inpatients have an associated increase in IBD and numerous other gastrointestinal illnesses.
Keywords: Crohn’s disease, Ulcerative colitis, Liver disease, Celiac disease, Cirrhosis
Introduction
Psoriasis is a chronic, recurrent, immune-mediated inflammatory disorder with an estimated prevalence of 2–4% in western countries [1–3]. First presentation of psoriasis follows a bimodal distribution, peaking at ages 15–20 years and ages 55–60 years [4]. Psoriasis most commonly presents as well-defined, symmetric, erythematous plaques with silvery scale. Clinically benign skin from psoriatic patients may demonstrate epidermal thickening, increased DNA synthesis, parakeratosis, and infiltration of macrophages and lymphocytes in the dermis [5]. Although dermatologic manifestations are mostly visible, psoriasis is a systemic inflammatory disease.
Inflammatory bowel disease (IBD) is a chronic, recurrent, immune-mediated inflammatory disorder affecting 7% of the United States population [6]. It presents as two main forms: Crohn’s disease (CD) and ulcerative colitis (UC), both resulting from a complex interaction of genetics, environment, and the gut microbiome. Population-based studies have shown an increasing incidence of IBD in the past century [7, 8].
Psoriasis and IBD have been shown to be closely connected diseases. Genome-wide association studies have revealed shared susceptibility loci between psoriasis and IBD, especially the 6p22, 16q, 1p31, and 5q33 loci, and interferon regulatory factor 5 [9, 10]. Furthermore, these conditions share pathogenetic mechanisms involving Th17 cells, regulatory T cells, and interleukins (IL) 17 and 23. Accordingly, methotrexate, TNF inhibitors, and IL-12/23 inhibitors can be used to treat psoriasis and IBD. Additional studies have shown common alterations in the gut microbiome [11, 12]. To date, risk associations between psoriasis and psoriatic arthritis with IBD have been reported [13–17], but not on a United States national scale. In this study, we quantify the prevalence and association of psoriasis and psoriatic arthritis with IBD and other gastrointestinal diseases in a nationwide inpatient sample.
Patients, material, methods
Data source
All data were extracted from the Nationwide Inpatient Sample (NIS), sponsored by the Healthcare Cost and Utilization Project (HCUP) [18], between 2000 and 2014. The dataset was intended for researchers to identify and analyze national trends in healthcare utilization, quality, and outcomes. The NIS contains an approximately 20% stratified, representative sample of all United States hospitalizations per year. Sample weights were created by NIS factoring sampling design of hospitals. These sample weights were needed to provide representative estimates of hospital discharges across the USA. All data were deidentified and no attempts were made to identify any of the individuals in the database. All parties with access to HCUP were compliant to the HCUP formal data use agreement. The NIS data concur with the National Hospital Discharge Survey, supporting data reliability [19].
Selection of psoriasis, psoriatic arthritis, and gastrointestinal illnesses
The databases were searched for a primary and/or secondary discharge diagnosis of psoriasis and psoriatic arthritis using the International Classification of Diseases, 9th revision, clinical modification (ICD-9-CM) code 696.1 and 696.0, respectively, both of which have been previously validated [20, 21]. The IBD was searched using ICD-9-CM codes previously validated in the NIS [22]. The primary diagnosis was defined in the NIS as the condition chiefly responsible for admission to hospital for care and per HCUP standards, is the first listed diagnosis. A maximum of 24 secondary diagnoses are allowed per discharge.
Gastrointestinal illnesses were selected based on those previously studied with psoriasis and other digestive diseases were selected a priori with unique ICD-9-CM codes for analysis [23]. A gastrointestinal disease was considered to be present with either a primary or secondary diagnosis. All comorbidities and their respective codes are presented in Supplemental Table 1.
Statistical analysis
Data were analyzed using SAS, Version 9.4 (SAS Institute, Cary, NC, USA). Independent variables were chosen to assess for sociodemographic disparities, as disparities in hospitalization rates have been observed in psoriasis and other dermatologic disorders, such as pemphigus and bullous pemphigoid [24–26]. Age, gender, race, and insurance status were included. Weighted frequencies of hospitalizations with either a primary or secondary ICD-9-CM code of psoriasis and psoriatic arthritis with and without IBD were determined for each independent variable. Summary statistics were generated for length of stay (LOS). Chi-square tests were employed to determine significant differences amongst all independent variables when comparing psoriasis with and without IBD and psoriatic arthritis with and without IBD. Significance was set to an alpha level of 0.05 a priori.
Multivariable logistic regression analyses were performed to identify the association of psoriasis and psoriatic arthritis with gastrointestinal illnesses. These analyses adjusted for age, gender, race, income, insurance status, obesity, smoking, and alcohol use when determining the association of psoriasis and psoriatic arthritis with and without IBD. All other gastrointestinal illnesses were adjusted for IBD. Odds ratios (ORs) and 95% CIs were plotted on forest plots through Open Meta Analyst, an open-source software supported by Brown University and the Agency for Healthcare Research and Quality [27]. The standard error of the mean for each variable is reported as ±.
Cochran-Armitage temporal trend tests were performed for psoriasis and psoriatic arthritis with IBD at an alpha level of 0.05 and point-wise error bars representing 95% confidence intervals. The incidence of hospital cases is expressed as cases per 1000 hospitalizations. All analyses used SAS/STAT survey analysis procedures to account for the complex NIS sampling scheme and produce unbiased standard errors. P-values were not adjusted for multiple tests and should be interpreted as exploratory only.
Results
Patient hospitalization characteristics
The total weighted population captured by the NIS included 554,266,249 hospitalizations (116,134,755 unweighted) between 2000 and 2014. Among this sample, 21,355 hospitalizations had a primary or secondary diagnosis of psoriasis and IBD versus1,233,331 psoriasis hospitalizations without IBD. Psoriasis inpatients with vs. without IBD were much more likely to be younger (51± 0.3 years vs. 60± 0.1 years, p<0.001). Psoriasis inpatients with IBD were more likely to be female (p<0.001) and privately insured (p<0.001), while psoriasis inpatients without IBD were more likely to have pay insurance through Medicare (p<0.001). Psoriasis inpatients with IBD had significantly longer stays for inpatient hospitalizations as opposed to those without IBD (5.4± 0.10 days vs. 5.2± 0.02 days, p=0.034).
There were 5306 hospitalizations with a primary or secondary diagnosis of psoriatic arthritis and IBD versus 273,908 psoriatic arthritis hospitalizations without IBD. Psoriatic arthritis inpatients were mostly white, more often female, and between the ages of 40–79 years (p<0.001 each). Psoriatic arthritis hospitalizations with IBD were more likely to be female versus psoriatic arthritis hospitalizations without IBD (p=0.034). Psoriatic arthritis hospitalizations without IBD were disproportionately Hispanic (p=0.004). Like psoriasis hospitalizations with IBD, psoriatic arthritis hospitalizations with IBD had longer lengths of stay compared to those without IBD (5.4±0.2 days vs. 4.9±0.03 days, p=0.004). (Table 1).
Table 1.
Patient hospitalization characteristics
| Variable | Psoriasis | Psoriatic arthritis | ||||
|---|---|---|---|---|---|---|
| w/IBD | w/o IBD | P-value | w/IBD | w/o IBD | P-value | |
| Sex | – | – | <0.001* | – | – | 0.034* |
| Female | 11,750 (55.0) | 573,519 (47.0) | – | 3157 (60.0) | 152,160 (56.0) | – |
| Male | 9605 (45.0) | 638,167 (53.0) | – | 2149 (40.0) | 121,666 (44.0) | – |
| Age, years | – | – | <0.001* | – | – | <0.001* |
| 0–17 | 420 (2.0) | 8646 (0.7) | – | 47 (0.9) | 931 (0.3) | – |
| 18–39 | 5786 (27.0) | 133,749 (11.3) | – | 818 (15.0) | 24,026 (8.8) | – |
| 40–59 | 7889 (37.0) | 420,650 (35.4) | – | 2356 (44.0) | 107,055 (39.0) | – |
| 60–79 | 6015 (28.0) | 493,187 (41.5) | – | 1854 (35.0) | 118,003 (43.0) | – |
| >80 | 1244 (6.0) | 132,191 (11.1) | – | 231 (4.4) | 23,893 (8.7) | – |
| Race | – | – | <0.001* | – | – | 0.004* |
| White | 16,083 (88.0) | 823,323 (81.0) | – | 4308 (92.6) | 203,593 (88.4) | – |
| Black | 902 (4.9) | 67,990 (6.7) | – | 123 (2.6) | 7153 (3.1) | – |
| Hispanic | 634 (3.5) | 76,453 (7.5) | – | 96 (2.1) | 10,546 (4.6) | – |
| Asian | 211 (1.1) | 21,620 (2.1) | – | 24 (0.5) | 3290 (1.4) | – |
| Native American | 49 (0.2) | 5249 (0.5) | – | 24 (0.5) | 1017 (0.5) | – |
| Other | 420 (2.3) | 25,262 (2.5) | – | 78 (1.7) | 4677 (2.0) | – |
| Insurance | – | – | <0.001* | – | – | <0.001* |
| Medicare | 7742 (36.3) | 597,425 (49.4) | – | 2205 (41.6) | 131,768 (48.2) | – |
| Medicaid | 2174 (10.2) | 138,380 (11.4) | – | 355 (6.7) | 19,076 (7.0) | – |
| Private | 9782 (45.8) | 370,222 (30.6) | – | 2491 (46.9) | 108,819 (39.8) | – |
| Self-pay | 873 (4.1) | 57,977 (4.8) | – | 87 (1.6) | 6371 (2.3) | – |
| No charge | 97 (0.5) | 6363 (0.5) | – | a | 667 (0.2) | – |
| Other | 671 (3.1) | 39,311 (3.3) | – | 169 (3.2) | 6869 (2.5) | – |
| Length of stay, days (SE) | 5.4 (± 0.10) | 5.2 (± 0.02) | 0.034* | 5.4 (± 0.2) | 4.9 (± 0.03) | 0.004* |
Values are presented as n (%) unless specified. Percent applies to column.
IBD inflammatory bowel disease
Significant at level P = 0.05
Per the Nationwide Inpatient Sample data use agreement, cell sizes ≤10 should be avoided in publication. Missing values were encountered for age in 23,264, race in 194,845, and insurance in 2024 patients with psoriasis. Missing values were encountered for sex in 82, race in 44,203, and insurance in 256 patients with psoriatic arthritis. There were no significant differences between missing values among patients with or without IBD
Association of psoriasis with IBD and gastrointestinal illnesses
In multivariable regression models controlling for age, gender, race, income, insurance status, obesity, smoking, and alcohol use, psoriasis was significantly associated with IBD in both ulcerative colitis (adjusted odds ratio, aOR 2.13, 95% confidence interval, CI 2.0–2.3) and Crohn’s disease (aOR 2.48, 95% CI 2.4–2.6). When also controlling for IBD, psoriasis was significantly associated with other gastrointestinal diseases, including celiac disease (aOR 2.62, 95% CI 2.3–2.9), gastroesophageal reflux disease (GERD) (aOR 1.53, 95% CI 1.5–1.6), esophagitis (aOR 1.05, 95% CI 1.0–1.1), peptic ulcers (aOR 1.22, 95% CI 1.1–1.3), autoimmune hepatitis (aOR 3.13, 95% CI 2.6–3.7), cholelithiasis (aOR 1.04, 95% CI 1.0–1.1), non-alcoholic fatty liver disease (aOR 2.22, 95% CI 2.1–2.3), gastritis and duodenitis (aOR 1.04, 95% CI 1.0–1.1), cholangitis (aOR 1.21, 95% CI 1.1–1.4), irritable bowel syndrome (aOR 1.98, 95% CI 1.9–2.1), colon cancer (aOR 0.93, 95% CI 0.89–0.97), stomach cancer (aOR 0.73, 95% CI 0.65–0.82), esophageal cancer (aOR 0.87, 95% CI 0.77–0.99), pancreatic cancer (aOR 0.80, 95% CI 0.71–0.89), liver cancer (aOR 1.62, 95% CI 1.48–1.77), liver cirrhosis (aOR 2.95, 95% CI 2.85–3.06), noninfective gastroenteritis and colitis (aOR 1.07, 95% CI 1.03–1.12), intestinal infections (aOR 1.09, 95% CI 1.05–1.13), pernicious anemia (aOR 1.79, 95% CI 1.59–2.00), acute pancreatitis (aOR 1.09, 95% CI 1.05–1.13), and chronic pancreatitis (aOR 1.34, 95% CI 1.26–1.43) (Fig. 1).
Fig. 1.
Association between psoriasis and gastrointestinal comorbidities. Significant adjusted odds ratios, 95% confidence intervals, and p-values in bold. aOR adjusted odds ratio, GERD gastroesophageal reflux disease, NAFLD non-alcoholic fatty liver disease, IBS irritable bowel syndrome
Association of psoriatic arthritis with IBD and gastrointestinal illnesses
In multivariable regression models controlling for age, gender, race, income, insurance status, obesity, smoking, and alcohol use, psoriatic arthritis was significantly associated with IBD in both ulcerative colitis (aOR 1.95, 95% CI 1.7–2.2) and Crohn’s disease (aOR 2.66, 95% CI 2.4–2.9). When also controlling for IBD, psoriatic arthritis was significantly associated with other gastrointestinal diseases, including celiac disease (aOR 2.63, 95% CI 2.1–3.2), GERD (aOR 1.91, 95% CI 1.8–2.0), esophagitis (aOR 1.33, 95% CI 1.2–1.5), peptic ulcers (aOR 1.63, 95% CI 1.5–1.7), autoimmune hepatitis (aOR 3.54, 95% CI 2.6–4.8), NAFLD (aOR 3.02, 95% CI 2.8–3.3), gastritis and duodenitis (aOR 1.32, 95% CI 1.2–1.4), irritable bowel syndrome (aOR 2.42, 95% CI 2.3–2.6), colon cancer (aOR 0.66, 95% CI 0.59–0.74), stomach cancer (aOR 0.63, 95% CI 0.47–0.85), esophageal cancer (aOR 0.54–0.98, 95% CI), liver cirrhosis (aOR 2.87, 95% CI 2.66–3.09), noninfective gastroenteritis and colitis (aOR 1.37, 95% CI 1.26–1.48), intestinal infections (aOR 1.39, 95% CI 1.29–1.48), pernicious anemia (aOR 2.48, 95% CI 2.01–3.05), acute pancreatitis (aOR 1.28, 95% CI 1.17–1.39), and chronic pancreatitis (aOR 1.58, 95% CI 1.37–1.82) (Fig. 2).
Fig. 2.
Association between psoriatic arthritis and gastrointestinal comorbidities. Significant adjusted odds ratios, 95% confidence intervals, and p-values in bold. aOR adjusted odds ratio, GERD gastroesophageal reflux disease, NAFLD non-alcoholic fatty liver disease, IBS irritable bowel syndrome
Trends of psoriasis and psoriatic arthritis with IBD
Among hospitalizations with psoriasis and psoriatic arthritis, rates of a concomitant diagnosis of IBD increased from 2000 to 2014 (p<0.001) (Fig. 3). In 2000, 11.7 psoriasis with IBD diagnoses per 1000 hospitalizations were made and in 2014, the number increased to 22.5 diagnoses per 1000 hospitalizations, representing a 92.3% increase. Likewise, in 2000, 12.2 psoriatic arthritis with IBD diagnoses per 1000 hospitalizations were made and in 2014, the number increased to 23 diagnoses per 1000 hospitalizations showing an 88.5% rise across a 15-year period.
Fig. 3.
Incidence of hospitalization for psoriasis and psoriatic arthritis with IBD. Incidence of hospitalization for both psoriasis and psoriatic arthritis with IBD (blue and red, respectively) per 1000 hospitalizations are rising. Estimates and 95% confidence intervals are presented
Discussion
In this study, we show that weighted frequencies of sex, age, race, and insurance status were significantly different amongst psoriasis inpatients with vs. without IBD and psoriatic arthritis inpatients with vs. without IBD. Psoriasis inpatients with vs. without IBD were much more likely to be younger, female, and privately insured. Psoriasis inpatients without IBD were more likely to be insured with Medicare. Psoriatic arthritis inpatients with vs. without IBD were much more likely to be white, female, and between the ages of 40–79 years. Both psoriasis and psoriatic arthritis with vs. without IBD had longer lengths of inpatient hospitalization, likely due to increased complexity of comorbid health disorders.
The present study highlights the association of psoriasis and psoriatic arthritis with gastrointestinal diseases, particularly IBD, even after controlling for demographic variables. The strongest associations in psoriasis inpatients were IBD, celiac disease, autoimmune hepatitis, NAFLD, and liver cirrhosis. Esophageal, stomach, colon, and pancreatic cancer all had lower odds, while liver cancer had higher odds in psoriasis inpatients. Psoriatic arthritis inpatients shared the associations with liver diseases, as well as a particularly strong association with IBS and pernicious anemia.
Although psoriasis patients have been shown to smoke and drink alcohol more than other dermatology patients, both lifestyle factors were controlled for in multivariable regression models [28, 29]. Nonetheless, psoriasis and psoriatic arthritis showed increased odds of developing liver diseases, including liver cancer, autoimmune hepatitis, NAFLD, and liver cirrhosis. The effects of psoriasis and psoriatic arthritis on the liver remain unclear. In the current study, past use of methotrexate, a hepatotoxic drug used in psoriasis, could not be obtained. Previous studies have shown increased risk of liver disease in psoriasis and psoriatic arthritis patients [30–32]. It has been documented that autoimmune hepatitis is a complication of psoriatic anti-tumor necrosis factor α treatment due to the production of autoantibodies. This study stresses the importance of careful monitoring of liver enzymes in psoriasis and psoriatic arthritis patients, especially when treated with hepatotoxic drugs. Further studies are needed to investigate why there is a negative association with psoriasis and psoriatic arthritis with other gastrointestinal cancers as previous reports suggest increased risk [31, 33–35].
Previous studies have explored the association of psoriasis and psoriatic arthritis with IBD. Possible theories explaining this association include genetic abnormalities, immune dysfunction, and alteration of gut microbiota [23]. Chromosomal locus 6p21 is the most studied genetic region, encoding major histocompatibility complex-related genes [36]. Both psoriasis and IBD share susceptibility loci on chromosome 6p21, with psoriasis linked to PSORS1 and IBD to IBD3 [9]. Moreover, immune dysfunction affecting interleukin 23, 17, and 12 have been found in the pathogenesis of psoriasis and IBD [37–40]. Psoriasis patients have been shown to have decreased gut microbiome diversity, similar to IBD patients [11, 41].
To our knowledge, prior studies have not examined the trend of psoriasis and psoriatic arthritis with IBD in hospitalized patients. This nationwide analysis of hospital discharges demonstrates that psoriasis inpatients with IBD and psoriatic arthritis inpatients with IBD have experienced a considerable absolute rise in concomitant diagnoses. In part, this may be due to rising prevalence of psoriasis and IBD overall [42, 43]. Given that psoriasis and IBD are more prevalent in older age groups, it is likely that the absolute rise in psoriasis with IBD will continue to increase as the average US lifespan is forecasted to increase.
Strengths of the study include the size and diversity of the patient population in sex, age, race, and insurance status in a nationally representative sample. Moreover, the study used previously validated ICD-9-CM codes known to have high positive predictive value for psoriasis, psoriatic arthritis, and IBD.
Limitations of the study include exclusively reviewing an inpatient population, suggesting that Berkson’s bias may be present, overestimating severe disease phenotypes since these cases are more prone to hospitalization. This warrants further studies examining the observed trends in an outpatient setting. Furthermore, medication use was not accessible for review. Consequently, the effect of psoriatic therapeutics, particularly methotrexate and biologics, may confound the results. Also, since the data set is based on discharge diagnoses, an individual patient with multiple admissions could have been counted multiple times, introducing bias. Lastly, outside the analysis of psoriasis and psoriatic arthritis with IBD, this was a cross-sectional study that did not explore trends of psoriasis and psoriatic arthritis with other gastrointestinal diseases. Therefore, it remains unknown if these associations have been rising or decreasing over the 15-year period studied.
In conclusion, psoriasis and psoriatic arthritis are associated with IBD and a number of gastrointestinal diseases. Significant gender, age, racial, and healthcare disparities exist in hospitalized psoriasis and psoriatic arthritis inpatients with vs. without IBD. The incidence of hospitalizations for psoriasis and psoriatic arthritis with IBD significantly increased between 2000 and 2014. Further studies are needed to confirm these findings and uncover the mechanisms tying psoriasis and psoriatic arthritis to gastrointestinal diseases.
Supplementary Material
Footnotes
Conflict of interest A. Yousaf, R. Raiker, S.M. Davis, S. Gayam and Z. Zinn declare that they have no competing interests.
Compliance with ethical guidelines
Ethical standards Ethics approval: approved by the West Virginia University institutional review board, protocol # 2002899647.
Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00508-020-01740-8) contains supplementary material, which is available to authorized users.
Contributor Information
Ahmed Yousaf, Department of Dermatology, West Virginia University, 64 Medical Center Drive, Morgantown, WV 26506, USA.
Rahul Raiker, Department of Dermatology, West Virginia University, 64 Medical Center Drive, Morgantown, WV 26506, USA.
Stephen M. Davis, Department of Health Policy, Management & Leadership, West Virginia University, Morgantown, WV, USA Department of Emergency Medicine, West Virginia University, Morgantown, WV, USA.
Swapna Gayam, Department of Medicine, Section of Gastroenterology and Hepatology, West Virginia University, Morgantown, WV, USA.
Zachary Zinn, Department of Dermatology, West Virginia University, 64 Medical Center Drive, Morgantown, WV 26506, USA.
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