Non-alcoholic Fatty Liver Disease among patients with Inflammatory Bowel Disease in Qatar: Prevalence and Risk Factors

Non-alcoholic Fatty Liver Disease among patients with Inflammatory Bowel Disease in Qatar: Prevalence and Risk Factors

Dr. Muneera Al-Mohannadi1, Dr. Prem Chandra2, Dr. Betsy Varughese1, Dr. Abdulwahab Hamid1, Dr. Ahmed Badi1, Dr. Saad Al Kaabi1, Dr. Rafie Yakoob1, Dr. Khalid Al-Ejji1, Dr. Khaleel Sultan1, Dr. Adham A. H. Darweesh3, Nevin Abunahia1 and Dr. Moutaz Derbala4

1Gastroenterology & Hepatology, Hamad Medical Corporation, 2Research Affairs, Hamad Medical Corporation, 3Radiology, Hamad Medical Corporation, 4Prof., Hamad Medical Corporation, Doha. Qatar.

Background: Non-alcoholic fatty liver disease (NAFLD) has been increasingly identified in patients with inflammatory bowel disease (IBD), though metabolic risk factors for NAFLD are less frequent in IBD patients. Qatar is among countries characterized by the high prevalence of fatty liver. We aimed to characterize NAFLD in IBD patients and to determine factors associated with its severity.

Methods: A retrospective observational study was conducted to estimate the prevalence of NAFLD in all IBD patients followed at Hamad hospital, Doha, Qatar between January 2008 to December 2017. The associations between two or more qualitative variables were assessed using χ2-test and quantitative data between two independent groups were analyzed using the unpaired t-test. Multivariate logistic regression analysis was applied to determine the predictive values of each predictor for NAFLD among IBD patients.

Results: Among 913 IBD patients with a mean age of 36.9±13.2 years and BMI 26.9±6.1; 550 were males (60.2%), 383(41.9%) with Crohn’s disease and 530 (58.1%) with Ulcerative colitis. 24 (22.2%) patients had severe steatosis. The overall prevalence of NAFLD was 11.8% (95% CI 9.9, 14.1) and does not differ significantly between CD and UC patients (11.7% vs 11.9%; P=0.949).Patients who developed NAFLD were older at baseline (42.6±12.5 vs 36.2±13.1 years; P<0.001), had higher BMI (29.3±5.7 vs 26.6±6.1; P<0.001) and higher prevalence of diabetes (26% vs 10.3%; P<0.001) and hypertension (19% vs 10.3%; P=0.011).Multivariate analysis showed age >40 to 50 years (adjusted OR 2.98; 95% CI 1.62, 5.48; P=0.001), age >50 years (adjusted OR 2.03; 95% CI 1.03, 4.0; P=0.04), BMI > 30 kg/m2 (adjusted OR 2.24; 95% CI 1.28, 3.91; P=0.01) and diabetes mellitus (adjusted OR 1.98; 95% CI 1.15, 3.4; P=0.02) significantly associated with an increased risk of NAFLD. Females were less likely having the risk of NAFLD (adjusted OR 0.58; 95% CI 0.36, 0.93; P = 0.02) in comparison to males. The treatment with biologic does not increase the risk of steatosis. The predicted cutoff NAFLD score ≥ -1.67 had good predictive ability for significant steatosis in IBD cases.

Conclusion: The prevalence of NAFLD is not uncommon among IBD patients in Qatar. Older age, high BMI and diabetes mellitus increase the risk of NAFLD in IBD patients. Patients with risk factors need to be monitored closely and considered for early interventions which can limit the use of more hepatotoxic drugs and can achieve early remission of the disease. Non-invasive screening of NAFLD using NAFLD Score in IBD patients with risk factors could help early diagnosis and treatment of the disease and can easily be implemented in any setting of IBD clinics.

Keywords: Non-alcoholic Fatty Liver Disease, Inflammatory Bowel Disease, Qatar, Prevalence, Risk Factors

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Muneera Al- Mohannadi, Prem Chandra, Betsy Varughese, Abdulwahab Hamid, Ahmed Badi, Saad Al Kaabi, Rafie Yakoob, Khalid Al- Ejji, K-haleel Sultan, Adham AH Darweesh, Nevin Abunahia and Moutaz Derbala. Non- alcoholic Fatty Liver Disease among patients with Inflammatory Bowel Disease in Qatar: Prevalence and Risk Factors. Open Journal of Gastroenterology and Hepatology, 2020; 3:40. DOI: 10.28933/ojgh-2020-08-2805


1. Benedict M, Zhang X. Non-alcoholic fatty liver disease: An expanded review. WJH. 2017;9(16): 715 -732.
2. Sayiner M, Koenig A, Henry L, Younossi ZM. Epidemiology of Nonalcoholic Fatty Liver Disease and Nonalcoholic Steatohepatitis in the United States and the Rest of the World. Clinics in Liver Disease. 2016;20(2):205 -214.
3. Sartini A, Gitto S, Bianchini M, Verga MC, Di Girolamo M, Bertani A, et al. Non-alcoholic fatty liver disease phenotypes in patients with inflammatory bowel disease. Cell Death Dis. 2018;9(2):87.
4. Bargiggia S, Maconi G, Elli M, Molteni P, Ardizzone S, Parente F, et al. Sonographic prevalence of liver steatosis and biliary tract stones in patients with inflammatory bowel disease: study of 511 subjects at a single center. Journal of Clinical Gastroenterology.2003;36(5): 417 – 420.
5. Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M. Global epidemiology of nonalcoholic fatty liver disease-Meta-analytic assessment of prevalence, incidence, and outcomes: Hepatology. 2016;64(1):73 – 84.
6. Chalasani N, Younossi Z, Lavine JE, Charlton M, Cusi K, Rinella M, et al. The diagnosis and management of nonalcoholic fatty liver disease: Practice guidance from the American Association for the Study of Liver Diseases:Hepatology. 2018;67(1):328 – 357.
7. Younossi Z, Anstee QM, Marietti M, Hardy T, Henry L, Eslam M, et al. Global burden of NAFLD and NASH: trends, predictions, risk factors and prevention. Nat Rev Gastroenterol Hepatol. 2018;15(1):11 – 20.
8. Arab JP, Karpen SJ, Dawson PA, Arrese M, Trauner M. Bile acids and nonalcoholic fatty liver disease: Molecular insights and therapeutic perspectives. Hepatology. 2017;65(1):350 – 362.
9. Bringiotti R. Intestinal microbiota: The explosive mixture at the origin of inflammatory bowel disease? WJGP. 2014;5(4):550-559.
10. Miele L, Valenza V, La Torre G, Montalto M, Cammarota G, Ricci R, et al. Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease. Hepatology. 2009;49(6):1877-1887.
11. Anderson EL, Howe LD, Jones HE, Higgins JPT, Lawlor DA, Fraser A. The Prevalence of Non-Alcoholic Fatty Liver Disease in Children and Adolescents: A Systematic Review and Meta-Analysis. PLoS ONE. 2015;10(10):e0140908.
12. Chao CY, Battat R, Al Khoury A, Restellini S, Sebastiani G, Bessissow T. Co-existence of non-alcoholic fatty liver disease and inflammatory bowel disease: A review article. WJG. 2016;22 (34):7727-7734.
13. Angulo P, Hui JM, Marchesini G, Bugianesi E, George J, Farrell GC, et al. The NAFLD fibrosis score: A noninvasive system that identifies liver fibrosis in patients with NAFLD. Hepatology. 2007;45(4):846 – 854.
14. Khan N, Abbas AM, Whang N, Balart LA, Bazzano LA, Kelly TN. Incidence of Liver Toxicity in Inflammatory Bowel Disease Patients Treated with Methotrexate: A Meta-Analysis of Clinical Trials: Inflammatory Bowel Diseases. 2012;18(2): 359 – 367.
15. Gisbert JP, Luna M, González-Lama Y, Pousa ID, Velasco M, Moreno-Otero R, et al. Liver injury in inflammatory bowel disease: Long-term follow-up study of 786 patients: Inflammatory Bowel Diseases. 2007;13(9):1106 -1114.
16. Sourianarayanane A, Garg G, Smith TH, Butt MI, McCullough AJ, Shen B. Risk factors of non-alcoholic fatty liver disease in patients with inflammatory bowel disease. Journal of Crohn’s and Colitis. 2013;7(8):e279 – e285.
17. Zou ZY, Shen B, Fan J G. Systematic Review with Meta-analysis: Epidemiology of Nonalcoholic Fatty Liver Disease in Patients with Inflammatory Bowel Disease. Inflammatory Bowel Diseases. 2019;25(11):1764 -1772.
18. Glassner K, Malaty HM, Abraham BP. Epidemiology and Risk Factors of Nonalcoholic Fatty Liver Disease Among Patients with Inflammatory Bowel Disease: Inflammatory Bowel Diseases. 2017;23(6):998 -1003.
19. DeNicola E, Aburizaiza OS, Siddique A, Khwaja H, Carpenter DO. Obesity and public health in the Kingdom of Saudi Arabia. Reviews on Environmental Health. 2015;30(3):191-205.
20. Abuyassin B, Laher I. Diabetes epidemic sweeping the Arab world. WJD. 2016;7(8):165-174.
21. Alswat K, Aljumah A, Sanai F, Abaalkhail F, Alghamdi M, Al Hamoudi W, et al. Nonalcoholic fatty liver disease burden-Saudi Arabia and United Arab Emirates, 2017–2030. Saudi J Gastroenterol. 2018;24(4):211 – 219.
22. Henao-Mejia J, Elinav E, Thaiss CA, Licona-Limon P, Flavell RA. Role of the intestinal microbiome in liver disease. Journal of Autoimmunity. 2013; 46:66 -73.
23. Park SH, Kim PN, Kim KW, Lee SW, Yoon SE, Park SW, et al. Macrovesicular Hepatic Steatosis in Living Liver Donors: Use of CT for Quantitative and Qualitative Assessment. Radiology. 2006;239 (1):105-112.
24. Saroli Palumbo C, Restellini S, Chao C-Y, Aruljothy A, Lemieux C, Wild G, et al. Screening for Nonalcoholic Fatty Liver Disease in Inflammatory Bowel Diseases: A Cohort Study Using Transient Elastography. Inflammatory Bowel Diseases. 2019;25(1):124 -133.
25. Arieira C, Monteiro S, Xavier S, Dias de Castro F, Magalhães J, Moreira MJ, et al. Hepatic steatosis and patients with inflammatory bowel disease: when transient elastography makes the difference. European Journal of Gastroenterology & Hepatology. 2019;31(8):998 -1003.
26. Adams LC, Lübbe F, Bressem K, Wagner M, Hamm B, Makowski MR. Non-alcoholic fatty liver disease in underweight patients with inflammatory bowel disease: A case-control study. PLoS ONE. 2018;13(11):e0206450.
27. Betrapally NS, Gillevet PM, Bajaj JS. Gut microbiome and liver disease. Translational Research. 2017; 179:49 – 59.
28. Carr RM, Patel A, Bownik H, Oranu A, Kerner C, Praestgaard A, et al. Intestinal Inflammation Does Not Predict Nonalcoholic Fatty Liver Disease Severity in Inflammatory Bowel Disease Patients. Dig Dis Sci. 2017;62(5):1354 -1361.
29. Paolella G. Gut-liver axis and probiotics: Their role in non-alcoholic fatty liver disease. WJG. 2014;20(42):15518 – 15531.
30. Kwong EK, Zhou H. Sphingosine-1-phosphate signaling and the gut-liver axis in liver diseases. Liver Research. 2019;3(1):19 -24.
31. Karbalaei R, Piran M, Rezaei-Tavirani M, Asadzadeh-Aghdaei H, Heidari MH. A systems biology analysis protein-protein interaction of NASH and IBD based on comprehensive gene information. Gastroenterol Hepatol Bed Bench. 2017;10(3):194 -201.
32. Yalcin M, Akarsu M, Celik A, Sagol O, Tunali S, Ertener O, et al. A comparison of the effects of infliximab, adalimumab, and pentoxifylline on rats with non-alcoholic steatohepatitis. Turk J Gastroenterol. 2015;25(1):167-175.
33. Lapumnuaypol K, Kanjanahattakij N, Pisarcik D, Thongprayoon C, Wijarnpreecha K, Cheungpasitporn W. Effects of inflammatory bowel disease treatment on the risk of nonalcoholic fatty liver disease: a meta-analysis. European Journal of Gastroenterology & Hepatology. 2018;30(8):854 -860.
34. Girardin M, Manz M, Manser C, Biedermann L, Wanner R, Frei P, et al. First-Line Therapies in Inflammatory Bowel Disease. Digestion. 2012;86(s1):6-10.
35. Schröder T, Schmidt KJ, Olsen V, Möller S, Mackenroth T, Sina C, et al. Liver steatosis is a risk factor for hepatotoxicity in patients with inflammatory bowel disease under immunosuppressive treatment: European Journal of Gastroenterology & Hepatology. 2015;27(6): 698 -704.
36. Candelli M, Nista EC, Pignataro G, Zannoni G, de Pascalis B, Gasbarrini G, et al. Steatohepatitis during methylprednisolone therapy for ulcerative colitis exacerbation. J Intern Med. 2003;253(3): 391-392.
37. Gisbert JP, González-Lama Y, Maté J. Thiopurine-Induced Liver Injury in Patients With Inflammatory Bowel Disease: A Systematic Review. Am J Gastroenterology. 2007;102(7): 1518 -1527.
38. Sumida Y. Limitations of liver biopsy and non-invasive diagnostic tests for the diagnosis of nonalcoholic fatty liver disease/nonalcoholic steatohepatitis. WJG. 2014;20(2):475 – 485.
39. Das C, Baruah M, Singh D. Imaging of nonalcoholic fatty liver disease: A road less travelled. Indian J Endocr Metab. 2013;17(6):990 – 995.
40. Lee DH. Imaging evaluation of non-alcoholic fatty liver disease: focused on quantification. Clin Mol Hepatol. 2017;23(4):290 – 301.
41. Peleg N, Issachar A, Sneh-Arbib O, Shlomai A. AST to Platelet Ratio Index and fibrosis 4 calculator scores for non-invasive assessment of hepatic fibrosis in patients with non-alcoholic fatty liver disease. Digestive and Liver Disease. 2017;49(10):113

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