Patients with Celiac Disease Have High Prevalence of Fatty Liver and Metabolic Syndrome.

Abdominal obesity Gluten free diet Gluten sensitive enteropathy Non-alcoholic fatty liver disease Nontropical sprue

Journal

Digestive diseases and sciences
ISSN: 1573-2568
Titre abrégé: Dig Dis Sci
Pays: United States
ID NLM: 7902782

Informations de publication

Date de publication:
25 Apr 2024
Historique:
received: 28 02 2023
accepted: 14 07 2023
medline: 25 4 2024
pubmed: 25 4 2024
entrez: 25 4 2024
Statut: aheadofprint

Résumé

In recent years, patients with celiac disease (CeD) have been reported to have a high prevalence of fatty liver and metabolic syndrome. We conducted a systematic review and meta-analysis to assess the prevalence of fatty liver and metabolic syndrome in patients with CeD and effect of gluten-free diet in them. The PubMed, Embase and the Cochrane Library databases were searched for original studies upto November 18, 2022. We included full-text articles published in the English language after 1990 that used well-defined criteria for CeD, fatty liver and metabolic syndrome. A random effects model was used to calculate pooled prevalence. Of 350 studies identified, 11 studies (n = 2578) were included in the analysis. On analysis of both cross-sectional and longitudinal studies, pooled prevalence of fatty liver and metabolic syndrome in treatment-naïve patients with CeD were 18.2% (95% CI 8.3-30.8%, n = 1237) and 4.3% (95% CI 2.4-6.7, n = 1239) and in those on GFD of varying duration was 28.2% (95% CI 20.7-36.4%, n = 1368) and 21.3% (95% CI 11.7-32.9%, n = 2193), respectively. There was no difference in the prevalence of fatty liver and metabolic syndrome between low- or high-income group countries. Patients with CeD have a high prevalence of fatty liver and metabolic syndrome which increases further with the initiation of GFD. Patients with CeD should thus be screened and monitored for development of fatty liver and metabolic syndrome. They should be counselled appropriately regarding their diet and inclusion of physical activity in their lifestyle.

Identifiants

pubmed: 38662156
doi: 10.1007/s10620-024-08426-5
pii: 10.1007/s10620-024-08426-5
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Makharia GK, Singh P, Catassi C et al. The global burden of coeliac disease: opportunities and challenges. Nat Rev Gastroenterol Hepatol 2022;19:313–327.
doi: 10.1038/s41575-021-00552-z pubmed: 34980921
Cheng J, Brar PS, Lee AR et al. Body mass index in celiac disease: beneficial effect of a gluten-free diet. J Clin Gastroenterol 2010;44:267–271.
doi: 10.1097/MCG.0b013e3181b7ed58 pubmed: 19779362
Kabbani TA, Goldberg A, Kelly CP et al. Body mass index and the risk of obesity in coeliac disease treated with the gluten-free diet. Aliment Pharmacol Ther 2012;35:723–729.
doi: 10.1111/j.1365-2036.2012.05001.x pubmed: 22316503
Singh I, Agnihotri A, Sharma A et al. Patients with celiac disease may have normal weight or may even be overweight. Indian J Gastroenterol 2016;35:20–24.
doi: 10.1007/s12664-016-0620-9 pubmed: 26892766
Barone M, Iannone A, Cristofori F, et al. Risk of obesity during a gluten-free diet in pediatric and adult patients with celiac disease: a systematic review with meta-analysis. Nutr Rev August 2022:nuac052.
Younossi ZM, Koenig AB, Abdelatif D et al. Global epidemiology of nonalcoholic fatty liver disease-Meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology 2016;64:73–84.
doi: 10.1002/hep.28431 pubmed: 26707365
Noubiap JJ, Nansseu JR, Lontchi-Yimagou E et al. Geographic distribution of metabolic syndrome and its components in the general adult population: A meta-analysis of global data from 28 million individuals. Diabetes Res Clin Pract 2022;188:109924.
doi: 10.1016/j.diabres.2022.109924 pubmed: 35584716
Singh S, Allen AM, Wang Z, et al. Fibrosis progression in nonalcoholic fatty liver vs nonalcoholic steatohepatitis: a systematic review and meta-analysis of paired-biopsy studies. Clin Gastroenterol Hepatol 2015;13:643–654.e1–9; quiz e39–40.
Kasper P, Martin A, Lang S et al. NAFLD and cardiovascular diseases: a clinical review. Clin Res Cardiol 2021;110:921–937.
doi: 10.1007/s00392-020-01709-7 pubmed: 32696080
Mottillo S, Filion KB, Genest J et al. The metabolic syndrome and cardiovascular risk a systematic review and meta-analysis. J Am Coll Cardiol 2010;56:1113–1132.
doi: 10.1016/j.jacc.2010.05.034 pubmed: 20863953
Raiteri A, Granito A, Faggiano C et al. Hepatic Steatosis in Patients with Celiac Disease: The Role of Packaged Gluten-Free Foods. Nutrients 2022;14:2942.
doi: 10.3390/nu14142942 pubmed: 35889899 pmcid: 9316041
Manka P, Sydor S, Schänzer-Ocklenburg JM et al. A Potential Role for Bile Acid Signaling in Celiac Disease-Associated Fatty Liver. Metabolites 2022;12:130.
doi: 10.3390/metabo12020130 pubmed: 35208205 pmcid: 8879761
Agarwal A, Singh A, Mehtab W et al. Patients with celiac disease are at high risk of developing metabolic syndrome and fatty liver. Intest Res 2021;19:106–114.
doi: 10.5217/ir.2019.00136 pubmed: 32312034
Rispo A, Imperatore N, Guarino M et al. Metabolic-associated fatty liver disease (MAFLD) in coeliac disease. Liver Int 2021;41:788–798.
doi: 10.1111/liv.14767 pubmed: 33319459
Remes-Troche JM, Cobos-Quevedo ODJ, Rivera-Gutiérrez X et al. Metabolic effects in patients with celiac disease, patients with nonceliac gluten sensitivity, and asymptomatic controls, after six months of a gluten-free diet. Revista de Gastroenterología de México 2020;85:109–117.
doi: 10.1016/j.rgmx.2019.02.002 pubmed: 31000461
Ciccone A, Gabrieli D, Cardinale R et al. Metabolic Alterations in Celiac Disease Occurring after Following a Gluten-Free Diet. Digestion 2019;100:262–268.
doi: 10.1159/000495749 pubmed: 30554200
Tovoli F, Negrini G, Farì R et al. Increased risk of nonalcoholic fatty liver disease in patients with coeliac disease on a gluten-free diet: beyond traditional metabolic factors. Aliment Pharmacol Ther 2018;48:538–546.
doi: 10.1111/apt.14910 pubmed: 29984415
Tortora R, Rispo A, Alisi A et al. PNPLA3 rs738409 Polymorphism Predicts Development and Severity of Hepatic Steatosis but Not Metabolic Syndrome in Celiac Disease. Nutrients 2018;10:E1239.
doi: 10.3390/nu10091239
Imperatore N, Tortora R, Testa A et al. Proton pump inhibitors as risk factor for metabolic syndrome and hepatic steatosis in coeliac disease patients on gluten-free diet. J Gastroenterol 2018;53:507–516.
doi: 10.1007/s00535-017-1381-7 pubmed: 28823009
Tortora R, Capone P, De Stefano G et al. Metabolic syndrome in patients with coeliac disease on a gluten-free diet. Alimentary Pharmacology & Therapeutics 2015;41:352–359.
doi: 10.1111/apt.13062
Kabbani TA, Kelly CP, Betensky RA et al. Patients With Celiac Disease Have a Lower Prevalence of Non–Insulin-Dependent Diabetes Mellitus and Metabolic Syndrome. Gastroenterology 2013;144:912-917.e1.
doi: 10.1053/j.gastro.2013.01.033 pubmed: 23354016
Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 2000;283:2008–2012.
Revised criteria for diagnosis of coeliac disease. Report of Working Group of European Society of Paediatric Gastroenterology and Nutrition. Arch Dis Child 1990;65:909–911.
doi: 10.1136/adc.65.8.909
Ludvigsson JF, Leffler DA, Bai JC et al. The Oslo definitions for coeliac disease and related terms. Gut 2013;62:43–52.
doi: 10.1136/gutjnl-2011-301346 pubmed: 22345659
Hill ID, Dirks MH, Liptak GS et al. Guideline for the diagnosis and treatment of celiac disease in children: recommendations of the North American Society for Pediatric Gastroenterology, Hepatology and Nutrition. J Pediatr Gastroenterol Nutr 2005;40:1–19.
doi: 10.1002/j.1536-4801.2005.tb00917.x pubmed: 15625418
Felber J, Aust D, Baas S, et al. [Results of a S2k-Consensus Conference of the German Society of Gastroenterolgy, Digestive- and Metabolic Diseases (DGVS) in conjunction with the German Coeliac Society (DZG) regarding coeliac disease, wheat allergy and wheat sensitivity]. Z Gastroenterol 2014;52:711–743.
Husby S, Koletzko S, Korponay-Szabó I et al. European Society Paediatric Gastroenterology, Hepatology and Nutrition Guidelines for Diagnosing Coeliac Disease 2020. J Pediatr Gastroenterol Nutr 2020;70:141–156.
doi: 10.1097/MPG.0000000000002497 pubmed: 31568151
Hamaguchi M, Kojima T, Itoh Y et al. The severity of ultrasonographic findings in nonalcoholic fatty liver disease reflects the metabolic syndrome and visceral fat accumulation. Am J Gastroenterol 2007;102:2708–2715.
doi: 10.1111/j.1572-0241.2007.01526.x pubmed: 17894848
Sabir N, Sermez Y, Kazil S et al. Correlation of abdominal fat accumulation and liver steatosis: importance of ultrasonographic and anthropometric measurements. Eur J Ultrasound 2001;14:121–128.
doi: 10.1016/S0929-8266(01)00153-7 pubmed: 11704429
Ferraioli G, Wong VW-S, Castera L, et al. Liver Ultrasound Elastography: An Update to the World Federation for Ultrasound in Medicine and Biology Guidelines and Recommendations. Ultrasound Med Biol 2018;44:2419–2440.
Rout G, Kedia S, Nayak B et al. Controlled Attenuation Parameter for Assessment of Hepatic Steatosis in Indian Patients. J Clin Exp Hepatol 2019;9:13–21.
doi: 10.1016/j.jceh.2018.02.010 pubmed: 30765934
Authors/Task Force Members, Rydén L, Grant PJ, et al. ESC Guidelines on diabetes, pre-diabetes, and cardiovascular diseases developed in collaboration with the EASD: the Task Force on diabetes, pre-diabetes, and cardiovascular diseases of the European Society of Cardiology (ESC) and developed in collaboration with the European Association for the Study of Diabetes (EASD). Eur Heart J 2013;34:3035–3087.
Alberti KGMM, Zimmet P, Shaw J. Metabolic syndrome--a new world-wide definition. A Consensus Statement from the International Diabetes Federation. Diabet Med 2006;23:469–480.
Misra A, Chowbey P, Makkar BM et al. Consensus statement for diagnosis of obesity, abdominal obesity and the metabolic syndrome for Asian Indians and recommendations for physical activity, medical and surgical management. J Assoc Physicians India 2009;57:163–170.
pubmed: 19582986
Sinay I, Costa, de Loreto. Consenso Latinoamericano de la Asociación Latinoamericana de Diabetes (ALAD): Epidemiología, Diagnóstico, Control, Prevención y Tratamiento del Síndrome Metabólico en Adultos. https://www.scienceopen.com/document?vid=e533b22a-02e7-4eeb-834a-165d8f5121c2 . Accessed June 27, 2022.
Study Quality Assessment Tools | NHLBI, NIH. https://www.nhlbi.nih.gov/health-topics/study-quality-assessment-tools . Accessed July 4, 2022.
Altman DG, Bland JM. How to obtain the P value from a confidence interval. BMJ 2011;343:d2304.
doi: 10.1136/bmj.d2304 pubmed: 22803193
Rosenblad A. Introduction to Meta-Analysis by Michael Borenstein, Larry V. Hedges, Julian P.T. Higgins, Hannah R. Rothstein. International Statistical Review 2009;77:478–479.
Egger M, Davey Smith G, Schneider M et al. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997;315:629–634.
doi: 10.1136/bmj.315.7109.629 pubmed: 9310563 pmcid: 2127453
Valvano M, Longo S, Stefanelli G et al. Celiac Disease, Gluten-Free Diet, and Metabolic and Liver Disorders. Nutrients 2020;12:940.
doi: 10.3390/nu12040940 pubmed: 32231050 pmcid: 7230624
Taetzsch A, Das SK, Brown C et al. Are Gluten-Free Diets More Nutritious? An Evaluation of Self-Selected and Recommended Gluten-Free and Gluten-Containing Dietary Patterns. Nutrients 2018;10:E1881.
doi: 10.3390/nu10121881
Barone M, Della Valle N, Rosania R et al. A comparison of the nutritional status between adult celiac patients on a long-term, strictly gluten-free diet and healthy subjects. Eur J Clin Nutr 2016;70:23–27.
doi: 10.1038/ejcn.2015.114 pubmed: 26173865
Miranda J, Lasa A, Bustamante MA et al. Nutritional differences between a gluten-free diet and a diet containing equivalent products with gluten. Plant Foods Hum Nutr 2014;69:182–187.
doi: 10.1007/s11130-014-0410-4 pubmed: 24578088
Sainsbury K, Halmos EP, Knowles S et al. Maintenance of a gluten free diet in coeliac disease: The roles of self-regulation, habit, psychological resources, motivation, support, and goal priority. Appetite 2018;125:356–366.
doi: 10.1016/j.appet.2018.02.023 pubmed: 29481913
Vereczkei Z, Farkas N, Hegyi P et al. It Is High Time for Personalized Dietary Counseling in Celiac Disease: A Systematic Review and Meta-Analysis on Body Composition. Nutrients 2021;13:2947.
doi: 10.3390/nu13092947 pubmed: 34578835 pmcid: 8466091
Gami AS, Witt BJ, Howard DE et al. Metabolic syndrome and risk of incident cardiovascular events and death: a systematic review and meta-analysis of longitudinal studies. J Am Coll Cardiol 2007;49:403–414.
doi: 10.1016/j.jacc.2006.09.032 pubmed: 17258085
Chen J, Muntner P, Hamm LL, et al. The metabolic syndrome and chronic kidney disease in U.S. adults. Ann Intern Med 2004;140:167–174.
Emilsson L, Lebwohl B, Sundström J et al. Cardiovascular disease in patients with coeliac disease: A systematic review and meta-analysis. Dig Liver Dis 2015;47:847–852.
doi: 10.1016/j.dld.2015.06.004 pubmed: 26160499
Ng CH, Lim WH, Hui Lim GE, et al. Mortality Outcomes by Fibrosis Stage in Nonalcoholic Fatty Liver Disease: A Systematic Review and Meta-analysis. Clin Gastroenterol Hepatol May 2022:S1542–3565(22)00439–6.
Younossi Z, Anstee QM, Marietti M et al. Global burden of NAFLD and NASH: trends, predictions, risk factors and prevention. Nat Rev Gastroenterol Hepatol 2018;15:11–20.
doi: 10.1038/nrgastro.2017.109 pubmed: 28930295
Saklayen MG. The Global Epidemic of the Metabolic Syndrome. Curr Hypertens Rep 2018;20:12.
doi: 10.1007/s11906-018-0812-z pubmed: 29480368 pmcid: 5866840

Auteurs

Nishant Aggarwal (N)

William Beaumont University Hospital, Royal Oak, MI, USA.

Ashish Agarwal (A)

All India Institute of Medical Sciences, Jodhpur, India.

Hasan Alarouri (H)

Mayo Clinic, Rochester, MN, USA.

Vignesh Dwarakanathan (V)

Employee's State Insurance Corporation Hospital, Chennai, India.

Sana Dang (S)

Vardhman Mahavir Medical College & Safdarjung Hospital, New Delhi, India.

Vineet Ahuja (V)

All India Institute of Medical Sciences, New Delhi, India.

Govind K Makharia (GK)

All India Institute of Medical Sciences, New Delhi, India. govindmakharia@gmail.com.

Classifications MeSH