The burden of NAFLD in type 2 diabetic subjects from the general population: A Nationwide population-based follow-up study (NASHCO).

Forns index advanced fibrosis cardiovascular disease chronic kidney disease extrahepatic malignancy mortality fatty liver index obesity type 2 diabetes

Journal

Liver international : official journal of the International Association for the Study of the Liver
ISSN: 1478-3231
Titre abrégé: Liver Int
Pays: United States
ID NLM: 101160857

Informations de publication

Date de publication:
03 2022
Historique:
revised: 19 11 2021
received: 01 07 2021
accepted: 29 11 2021
pubmed: 24 1 2022
medline: 4 3 2022
entrez: 23 1 2022
Statut: ppublish

Résumé

The epidemiology and natural history of non-alcoholic fatty liver disease (NAFLD) in diabetes have been mainly investigated in the hospital setting. The goal of this study was to evaluate the characteristics of NAFLD and its impact on morbidity and mortality in type 2 diabetic subjects in a community setting. This study included 199 341 participants in the nationwide Constances cohort. After patients with excessive alcohol consumption, viral hepatitis or other causes of liver disease were excluded, 164 285 were analysed and 8386 (5.3%) were considered to have type 2 diabetes. The non-invasive diagnosis of NAFLD and advanced fibrosis was made using a combination of the fatty liver index and Forns index. Median follow-up was 2.5 years. Diabetes increased the risk of NAFLD by sixfold (adjusted OR 6.05, 95% CI 5.68-6.45) and the risk of advanced fibrosis by 3.76-fold (aOR 3.76, 95% CI 2.87-4.91) in NAFLD subjects. After controlling for confounders, the presence of NAFLD in diabetic subjects was associated with an increased risk of severe liver-related events (aHR 2.53, 95% CI 1.36-4.69), cardiovascular disease (CVD, aHR 2.71, 95% CI 1.72-4.26) and overall mortality (aHR 2.91, 95% CI 1.53-5.53). The risk of hepatic and extrahepatic complications in diabetic subjects with NAFLD significantly increased with the severity of fibrosis (P < .05). This prospective, longitudinal study in a large community-based cohort provides real-world evidence of the risk for NAFLD and advanced fibrosis in diabetes, and its impact on liver disease progression, diabetes-related complications such as CVD, and overall mortality. These data could be used to estimate real clinical and economic burden of NAFLD in diabetic subjects.

Sections du résumé

BACKGROUND
The epidemiology and natural history of non-alcoholic fatty liver disease (NAFLD) in diabetes have been mainly investigated in the hospital setting. The goal of this study was to evaluate the characteristics of NAFLD and its impact on morbidity and mortality in type 2 diabetic subjects in a community setting.
METHOD
This study included 199 341 participants in the nationwide Constances cohort. After patients with excessive alcohol consumption, viral hepatitis or other causes of liver disease were excluded, 164 285 were analysed and 8386 (5.3%) were considered to have type 2 diabetes. The non-invasive diagnosis of NAFLD and advanced fibrosis was made using a combination of the fatty liver index and Forns index. Median follow-up was 2.5 years.
RESULTS
Diabetes increased the risk of NAFLD by sixfold (adjusted OR 6.05, 95% CI 5.68-6.45) and the risk of advanced fibrosis by 3.76-fold (aOR 3.76, 95% CI 2.87-4.91) in NAFLD subjects. After controlling for confounders, the presence of NAFLD in diabetic subjects was associated with an increased risk of severe liver-related events (aHR 2.53, 95% CI 1.36-4.69), cardiovascular disease (CVD, aHR 2.71, 95% CI 1.72-4.26) and overall mortality (aHR 2.91, 95% CI 1.53-5.53). The risk of hepatic and extrahepatic complications in diabetic subjects with NAFLD significantly increased with the severity of fibrosis (P < .05).
CONCLUSION
This prospective, longitudinal study in a large community-based cohort provides real-world evidence of the risk for NAFLD and advanced fibrosis in diabetes, and its impact on liver disease progression, diabetes-related complications such as CVD, and overall mortality. These data could be used to estimate real clinical and economic burden of NAFLD in diabetic subjects.

Identifiants

pubmed: 35066992
doi: 10.1111/liv.15171
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

595-606

Informations de copyright

© 2022 John Wiley & Sons A/S . Published by John Wiley & Sons Ltd.

Références

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. Hepatololgy. 2016;64:73-84.
Rinella ME. Nonalcoholic fatty liver disease: a systematic review. JAMA. 2015;313:2263-2273.
Serfaty L, Lemoine M. Definition and natural history of metabolic steatosis: clinical aspects of NAFLD, NASH and cirrhosis. Diabetes Metab. 2008;34:634-637.
Francque SM, van der Graaff D, Kwanten WJ. Non-alcoholic fatty liver disease and cardiovascular risk: pathophysiological mechanisms and implications. J Hepatol. 2016;65:425-443.
Sanna C, Rosso C, Marietti M, Bugianesi E. Non-alcoholic fatty liver disease and extra-hepatic cancers. Int J Mol Sci. 2016;17:717.
Musso G, Gambino R, Tabibian JH, et al. Association of non-alcoholic fatty liver disease with chronic kidney disease: a systematic review and meta-analysis. PLoS Med. 2014;11:e1001680.
Younossi ZM, Golabi P, de Avila L, et al. The global epidemiology of NAFLD and NASH in patients with type 2 diabetes: a systematic review and meta-analysis. J Hepatol. 2019;71:793-801.
Targher G, Bertolini L, Padovani R, et al. Prevalence of nonalcoholic fatty liver disease and its association with cardiovascular disease among type 2 diabetic patients. Diabetes Care. 2007;30:1212-1218.
Targher G, Bertolini L, Rodella S, et al. Nonalcoholic fatty liver disease is independently associated with an increased incidence of cardiovascular events in type 2 diabetic patients. Diabetes Care. 2007;30:2119-2121.
Targher G, Bertolini L, Rodella S, et al. Non-alcoholic fatty liver disease is independently associated with an increased prevalence of chronic kidney disease and proliferative/laser-treated retinopathy in type 2 diabetic patients. Diabetologia. 2008;51:444-450.
Kwok R, Choi KC, Wong GL, et al. Screening diabetic patients for non-alcoholic fatty liver disease with controlled attenuation parameter and liver stiffness measurements: a prospective cohort study. Gut. 2016;65:1359-1368.
Casey SP, Kemp WW, McLean CA, Topliss DJ, Adams LA, Roberts SK. A prospective evaluation of the role of transient elastography for the detection of hepatic fibrosis in type 2 diabetes without overt liver disease. Scand J Gastroenterol. 2012;47:836-841.
Dunn MA, Behari J, Rogal SS, et al. Hepatic steatosis in diabetic patients does not predict adverse liver-related or cardiovascular outcomes. Liver Int. 2013;33:1575-1582.
Adams LA, Harmsen S, St Sauver JL, et al. Nonalcoholic fatty liver disease increases risk of death among patients with diabetes: a community-based cohort study. Am J Gastroenterol. 2010;105:1567-1573.
Younossi ZM, Gramlich T, Matteoni CA, Boparai N, McCullough A. Nonalcoholic fatty liver disease in patients with type 2 diabetes. Clin Gastroenterol Hepatol. 2004;2:262-265.
Zins M, Goldberg M, CONSTANCES team. The French CONSTANCES population-based cohort: design, inclusion and follow-up. Eur J Epidemiol. 2015;30:1317-1328.
Nabi O, Lacombe K, Boursier J, Mathurin P, Zins M, Serfaty L. Risk factors of nonalcoholic fatty liver disease and advanced fibrosis in general population: the French nationwide NASH-CO study. Gastroenterology. 2020;159:791-793.
Ruiz F, Goldberg M, Lemonnier S, et al. High quality standards for a large-scale prospective population-based observational cohort: Constances. BMC Public Health. 2016;16(1):877.
Gache P, Michaud P, Landry U, et al. The alcohol use disorders identification test (AUDIT) as a screening tool for excessive drinking in primary care: reliability and validity of a French version. Alcohol Clin Exp Res. 2005;29:2001-2007.
Clark JM, Brancati FL, Diehl AM. The prevalence and etiology of elevated aminotransferase levels in the United States. Am J Gastroeneterol. 2003;98:960-967.
Alberti KGMM, Zimmet P, Shaw J. Metabolic syndrome-a new world-wide definition. A consensus statement from the international diabetes federation. Diabetes Med. 2006;23:469-480.
Bedogni G, Bellentani S, Miglioli L, et al. The fatty liver index: a simple and accurate predictor of hepatic steatosis in the general population. BMC Gastroenterol. 2006;6:33.
Zelber-Sagi S, Webb M, Assy N, et al. Comparison of fatty liver index with noninvasive methods for steatosis detection and quantification. World J Gastroenterol. 2013;19:57-64.
Koehler EM, Schouten JNL, Hansen BE, Hofman A, Stricker BH, Janssen HLA. External validation of the fatty liver index for identifying nonalcoholic fatty liver disease in a population-based study. Clin Gastroenterol Hepatol. 2013;11:1201-1204.
Forns X, Ampurdanès S, Llovet JM, et al. Identification of chronic hepatitis C patients without hepatic fibrosis by a simple predictive model. Hepatology. 2002;36:986-992.
SNDS: Système National des Données de Santé | CNIL. https://www.cnil.fr/fr/snds-systeme-national-des-donnees-de-sante
Hagström H, Adams LA, Allen AM, et al. Administrative coding in electronic health care record-based research of NAFLD: an expert panel consensus statement. Hepatology. 2021;74:474-482.
Nones RB, Ivantes CP, Pedroso MLA. Can FIB4 and NAFLD fibrosis scores help endocrinologists refer patients with non-alcoholic fat liver disease to a hepatologist? Arch Endocrinol Metab. 2017;61:276-281.
Yang M, Jiang L, Wang Y, et al. Step layered combination of noninvasive fibrosis models improves diagnostic accuracy of advanced fibrosis in nonalcoholic fatty liver disease. J Gastrointestin Liver Dis. 2019;28:289-296.
Hagström H, Talbäck M, Andreasson A, et al. Ability of noninvasive scoring systems to identify individuals in the population at risk for severe liver disease. Gastroenterology. 2020;158:200-214.
Roulot D, Roudot-Thoraval FN, Kontchou G, et al. Concomitant screening for liver fibrosis and steatosis in French type 2 diabetic patients using Fibroscan. Liver Int. 2017;37:1897-1906.
Doycheva J, Cui J, Nguyen P, et al. Non-invasive screening of diabetics in primary care for NAFLD and advanced fibrosis by MRI and MRE. Aliment Pharmacol Ther. 2016;43:83-95.
Meex RCR, Watt MJ. Hepatokines: linking nonalcoholic fatty liver disease and insulin resistance. Nat Rev Endocrinol. 2017;13:509-520.
Koehler EM, Plompen EPC, Schouten JNL, et al. Presence of diabetes mellitus and steatosis is associated with liver stiffness in a general population: the Rotterdam study. Hepatology. 2016;63:138-147.
Mantovani A, Byrne CD, Bonora E, Targher G, Mantovani A, et al. Nonalcoholic fatty liver disease and risk of incident type 2 diabetes: a meta-analysis. Diabetes Care. 2018;41:372-382.
De Marco R, Locatelli F, Zoppini G, Verlato G, Bonora E, Muggeo M. Cause-specific mortality in type 2 diabetes. The Verona Diabetes Study. Diabetes Care. 1999;22:756-761.
El-Serag HB, Tran T, Everhart JE. Diabetes increases the risk of chronic liver disease and hepatocellular carcinoma. Gastroenterology. 2004;126:460-468.
Pang Y, Kartsonaki C, Turnbull I, et al. Diabetes, plasma glucose, and incidence of fatty liver, cirrhosis, and liver cancer: a prospective study of 0.5 million people. Hepatology. 2018;68:1308-1318.
Stepanova M, Clement S, Wong R, Saab S, Ahmed A, Younossi ZM. Patients with diabetes and chronic liver disease are at increased risk for overall mortality: a population study from the United States. Clin Diabet. 2017;35:79-83.
Shlomai G, Neel B, LeRoith D, Gallagher EJ, Shlomai G, et al. Type 2 diabetes mellitus and cancer: the role of pharmacotherapy. J Clin Oncol. 2016;34:4261-4269.
Dulai PS, Singh S, Patel J, et al. Increased risk of mortality by fibrosis stage in nonalcoholic fatty liver disease: systematic review and meta-analysis. Hepatology. 2017;65:1557-1565.

Auteurs

Oumarou Nabi (O)

Sorbonne Université, INSERM, Institut Pierre Louis d'Epidémiologie et de Santé Publique IPLESP, AP-HP, Public Health Department, Saint-Antoine Hospital, Paris, France.
UMS 11 Inserm, Université Paris Saclay, Université de Paris, Versailles-Saint Quentin University, Versailles, France.

Jerome Boursier (J)

HepatoGastroenterology Department, Anger University Hospital, Angers, France.
HIFIH Laboratory, UPRES EA3859, SFR 4208, Angers University, Angers, France.

Nathanaël Lapidus (N)

Sorbonne Université, INSERM, Institut Pierre Louis d'Epidémiologie et de Santé Publique IPLESP, AP-HP, Public Health Department, Saint-Antoine Hospital, Paris, France.

Philippe Mathurin (P)

Liver Unit, CHU, Lille, France.

Victor de Ledinghen (V)

Bordeaux University Hospital Branch, Bordeaux, France.

Jean-Michel Petit (JM)

Department of Endocrinology-Diabetology, CHU Dijon, Dijon, France.

Marcel Goldberg (M)

UMS 11 Inserm, Université Paris Saclay, Université de Paris, Versailles-Saint Quentin University, Versailles, France.
Université de Paris, Paris, France.

Marie Zins (M)

UMS 11 Inserm, Université Paris Saclay, Université de Paris, Versailles-Saint Quentin University, Versailles, France.
Université de Paris, Paris, France.

Karine Lacombe (K)

Sorbonne Université, INSERM, Institut Pierre Louis d'Epidémiologie et de Santé Publique IPLESP, AP-HP, Public Health Department, Saint-Antoine Hospital, Paris, France.
Infectious Diseases Department, Hôpital Saint-Antoine, APHP, Paris, France.

Lawrence Serfaty (L)

Hepatogastroenterology Service, Hôpital Hautepierre, Hôpitaux Universitaires de Strasbourg, Strasbourg, France.
INSERM UMR_S938, Université Paris-Sorbonne, Paris, France.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH