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Hepatobiliary and Pancreatic Manifestations in Inflammatory Bowel Diseases: a Referral Center Study Fotios S

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Hepatobiliary and Pancreatic Manifestations in Inflammatory Bowel Diseases: a Referral Center Study Fotios S Fousekis et al. BMC Gastroenterology (2019) 19:48 https://doi.org/10.1186/s12876-019-0967-3 RESEARCH ARTICLE Open Access Hepatobiliary and pancreatic manifestations in inflammatory bowel diseases: a referral center study Fotios S. Fousekis1, Konstantinos H. Katsanos1, Vasileios I. Theopistos1, Gerasimos Baltayiannis1, Maria Kosmidou2, Georgios Glantzounis3, Leonidas Christou2, Epameinondas V. Tsianos2 and Dimitrios K. Christodoulou1* Abstract Background: Hepatobiliary and pancreatic manifestations have been reported in patients with Crohn’s disease or ulcerative colitis. Our aim was to describe the prevalence of hepatobiliary and pancreatic manifestations in inflammatory bowel disease and their association with the disease itself and the medications used. Methods: Data were retrospectively extracted from the clinical records of patients followed up at our tertiary IBD referral Center. Results: Our study included 602 IBD patients, with liver function tests at regular intervals. The mean follow-up was 5.8 years (Std. Dev.: 6.72). Abdominal imaging examinations were present in 220 patients and revealed findings from the liver, biliary tract and pancreas in 55% of examined patients (120/220). The most frequent findings or manifestations from the liver, biliary tract and pancreas were fatty liver (20%, 44/220), cholelithiasis (14.5%, 32/220) and acute pancreatitis (0.6%, 4/602), respectively. There were 7 patients with primary sclerosing cholangitis. Regarding hepatitis viruses, one-third of the patients had been tested for hepatitis B and C. 5% (12/225) of them had positive hepatitis B surface antigen and 13.4% had past infection with hepatitis B virus (positive anti-HBcore). In addition, most of the patients were not immune against hepatitis B (negative anti-HBs), while 3% of patients were anti-HCV positive and only one patient had active hepatitis C. Furthermore, 24 patients had drug-related side effects from the liver and pancreas. The side effects included 21 cases of hepatotoxicity and 3 cases of acute pancreatitis. Moreover, there were two cases of HBV reactivation and one case of chronic hepatitis C, which were successfully treated. Conclusion: In our study, approximately one out of four patients had some kind by a hepatobiliary or pancreatic manifestation. Therefore, it is essential to monitor liver function at regular intervals and differential diagnosis should range from benign diseases and various drug related side effects to severe disorders, such as primary sclerosing cholangitis. Keywords: Inflammatory bowel disease, Hepatotoxicity, Acute pancreatitis, Hepatobiliary manifestations, Pancreatic manifestations, Fatty liver, Immunomodulators * Correspondence: [email protected] 1Department of Gastroenterology and Hepatology, Medical school and University of Ioannina, Ioannina, Greece Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Fousekis et al. BMC Gastroenterology (2019) 19:48 Page 2 of 8 Background 100 person-months [10]. On the other hand, thiopurine Ulcerative colitis and Crohn’s disease are inflammatory induced liver damage is not dose dependent and the diseases which affect the gastrointestinal tract. However, abnormalities in liver tests occur more frequently in the both disorders can also involve other organ systems as first months of therapy [11]. The incidence of well. It is not unusual for patients with IBD to have thiopurine-induced liver injury is approximately 4% [12]. manifestations from the liver, pancreas, gallbladder and Anti–tumor necrosis factor (anti-TNF) biological agents biliary tree. The strongest associated disease with IBD is rarely cause liver damage. Anti-TNF-induced liver dam- primary sclerosing cholangitis (PSC). PSC is an idio- age may occur irrespectively of the number of infusions pathic chronic progressive disease of the biliary tree and or injections, time and dose [13]. Additionally, patients can cause stenosis and destruction of extra- and intrahe- with IBD have reduced immunogenicity due to the pres- patic bile ducts. It is estimated that 5% of patients with ence of IBD (malabsorption and malnutrition) and UC develop PSC and up to 80–90% of patients with PSC immunosuppressive treatment (immunomodulators and have UC [1]. Other manifestations from the biliary tree biological agents). Hence, IBD patients have an increased in IBD patients include cholangitis and cholangiocarci- risk of hepatitis B reactivation or loss of immunity noma, mainly as complications of PSC [2]. The gallbladder against hepatitis B and exacerbation of hepatitis C [14]. is an organ that may be affected by IBD. Cholelithiasis is Acute pancreatitis and, more infrequently, chronic more common in patients with CD than in general popu- pancreatitis and autoimmune pancreatitis may occur in lation and patients with CD have a two-fold increased risk patients with IBD due to the disease itself or side effects of gallstones. On the other hand, patients with UC do not of medication used in the treatment. The increased inci- have any additional risk [3]. The main independent risk dence of acute pancreatitis in Crohn’s disease can be factors for the development of gallstones are ileo-colonic attributed to anatomic abnormalities of the duodenum CD location, the extent of ileal resection (> 30 cm), disease and more frequent development of cholelithiasis in duration (> 15 years) and multiple or prolonged total par- Crohn’s disease as a result of ileal disease [15]. Also, enteral nutrition treatments [4]. Hepatic manifestations in acute pancreatitis is a fairly frequent side effect of IBD vary and range from benign disorders, such as fatty azathioprine and 6-mercaptopourine use (4%) [12] and a liver to end-stage hepatic failure as a complication of PSC less common side effect of 5-aminosalicylate (5-ASA) or primary biliary cirrhosis. Non-alcoholic fatty liver and corticosteroid treatment [16]. disease (NAFLD) refers to the accumulation of fat in The aim of this retrospective study was to document hepatocytes without alcohol use. Hepatic steatosis can be the manifestations of the liver, pancreas and biliary tree diagnosed either by imaging or by histology (biopsy). in patients with Inflammatory Bowel Disease and Prevalence of NAFLD in IBD patients varies, ranging from describe their association with the disease itself and the 8.2 to 40% [5]. Furthermore, it seems that IBD patients medications used. develop NAFLD with fewer metabolic risk factors than general population [6]. Other hepatic manifestations in Methods patients with IBD include liver abscess [7], granulomatous In our retrospective study, we included 602 patients with hepatitis, hepatic amyloidosis and primary biliary cirrhosis IBD, who were monitored at our tertiary University Hos- (PBC). The first three disorders are more frequent in CD, pital from 1977 to 2016. The diagnosis of the disease was while PBC is more common in patients with UC [8]. based on histopathological findings after ileocolonoscopy In addition, drug-induced hepatotoxicity is common with biopsies. Inclusion criteria for the study were diagno- side effect of IBD treatment. More analytically, in the sis of IBD and regular follow-up from time of diagnosis United Kingdom from 1991 to 1998, the incidence of with frequent laboratory tests. Consequently, every patient hepatitis was 3.2 and 6 cases per million prescriptions who participated in this study had baseline liver function for mesalazine and sulfasalazine, respectively. What is tests measured at diagnosis of IBD and at regular intervals, more, it seems that there is a stronger association be- at least every 6 months. All patients were followed up from tween 5-ASA induced hepatotoxicity and rheumatoid the time of diagnosis of IBD in our referral center. Further- arthritis than IBD [9]. Also, methotrexate has been asso- more, 220 patients underwent imaging evaluation, such as ciated with liver damage and it was proposed that the ultrasound and computed tomography, and were tested for mechanism is dose dependent. A meta-analysis of clin- hepatitis viruses B and C. A complete registry of all clinical, ical trials showed that the rate of abnormal aminotrans- laboratory, imaging and histologic abnormalities related to ferase serum levels [defined as up to a 2 fold elevate liver, biliary tree and pancreas was made. over the upper limit of the normal (ULN)] in patients treated with methotrexate for IBD was 1.4 per 100 Statistical analysis person-months, while the incidence of hepatotoxicity Data were analyzed using SPSS software version 22. All (defined as greater than a 2 fold over ULN) was 0.9 per clinical and pathological features were categorized as Fousekis et al. BMC Gastroenterology (2019) 19:48 Page 3 of 8 either continuous or categorical variables. Continuous variables were summarized as means and standard deviation. Results The average age of patients was 39 years (Std. Dev. 17.4) at diagnosis. 57.5% of IBD patients
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