Nutrición Hospitalaria 03969 / http://dx.doi.org/10.20960/nh.03969

Trabajo Original

Prevalence of non-alcoholic fatty liver disease (NAFLD) in a cohort of patients with type 2 diabetes: the PHIGNA-DM2 study

Antonio Jesús Martínez-Ortega, Ana Piñar Gutiérrez, Carmen Lara-Romero, Pablo Jesús Remón Ruiz, Javier Ampuero-Herrojo, Irene de Lara-Rodríguez, Manuel Romero-Gómez, Pedro P. García Luna, Alfonso Soto-Moreno

Prepublicado: 2022-09-19

Publicado: 2022-10-13

VOLUMEN 39, NÚM. 5, septiembre-octubre (2022), PAG. 1012-1018

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Compártelo:

Background: type 2 diabetes (T2D) is a risk factor for nonalcoholic fatty liver disease (NAFLD). Objective: to evaluate the prevalence of NAFLD in a cohort of patients with T2D. Methods: an observational, descriptive study performed between May 2018 and December 2019 at the Endocrinology and Nutrition Unit. The χ² test was performed for qualitative variables and a non-parametric test for the comparison of medians of quantitative variables. Steatosis degree was defined by the coefficient attenuated parameter (CAP): (S0: < 248 dB/m; S1: 248-268 dB/m; S2: 268-288 dB/m; S3: > 288 dB/m) or stiffness: F0-F1: < 8 kPa; F2: 8-10 kPa; F3: 10-15 kPa; F4: > 15 kPa, using transient elastography (TE) (FibroScan®). A univariate analysis was performed and subsequently a multivariate analysis with statistically significant variables used to study the predictive factors of intense steatosis and advanced fibrosis. Results: n = 104 patients with T2D; 84 (80.7 %) were obese. TE demonstrated advanced fibrosis in 20 % and intense steatosis (S3) in more than 50 %. Lower total bilirubin (OR: 0.028; 95 % CI: (0.002-0.337); p = 0.005) was found to be an independent factor for S3 steatosis in the multivariate analysis. BMI ((OR: 1.497; 95 % CI: (1.102-2.034); p = 0.01)) was a predictive factor for advanced fibrosis in a multivariate analysis. Conclusions: NAFLD-associated intense steatosis and NAFLD-associated fibrosis were commonly found in patients with T2DM and obesity. Diabetic patients should be screened for liver disease as one more target organ.

Palabras Clave: Type 2 diabetes. Diabetes mellitus. Nonalcoholic fatty liver disease. Liver fibrosis. Liver steatosis. Elastography.

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Bibliografía
Artículos Relacionados

Byrne C, Targher G. NAFLD: A multisystem disease. Journal of Hepatology. 2015;62:S47-S64.
DOI: 10.1016/j.jhep.2014.12.012

Wong RJ, Cheung R, Ahmed A. Nonalcoholic steatohepatitis is the most rapidly growing indication for liver transplantation in patients with hepatocellular carcinoma in the US. Hepatology. 2014;59:2188-95.
DOI: 10.1002/hep.26986

Browning JD, Szczepaniak LS, Dobbins R, Nuremberg P, Horton JD, Cohen JC. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 2004;40:1387–1395.
DOI: 10.1002/hep.20466

Tsuneto A, Hida A, Sera N, Imaizumi M, Ichimaru S, Nakashima E, et al. Fatty liver incidence and predictive variables. Hypertens Res 2010;33:638–643. [4]
DOI: 10.1038/hr.2010.45

Romeo S, Kozlitina J, Xing C, Pertsemlidis A, Cox D, Pennacchio LA, et al. Genetic variation in PNPLA3 confers susceptibility to nonalcoholic fatty liver disease. Nat Genet 2008;40:1461–1465.
DOI: 10.1038/ng.257

Anstee QM, Targher G, Day CP. Progression of NAFLD to diabetes mellitus, cardiovascular disease or cirrhosis. Nat Rev Gastroenterol Hepatol 2013;10:330–344.
DOI: 10.1038/nrgastro.2013.41

Hyysalo J, Mannisto VT, Zhou Y, Arola J, Karja V, Leivonen M, et al. A population-based study on the prevalence of NASH using scores validated against liver histology. J Hepatol 2013;60:839–846.
DOI: 10.1016/j.jhep.2013.12.009

Musso G, Cassader M, Olivetti C, Rosina F, Carbone G, Gambino R. Association of obstructive sleep apnoea with the presence and severity of non-alcoholic fatty liver disease. A systematic review and meta-analysis. Obes Rev 2013;14:417–431.
DOI: 10.1111/obr.12020

Musso G, Gambino R, Cassader M, Pagano G. Meta-analysis: natural history of non-alcoholic fatty liver disease (NAFLD) and diagnostic accuracy of noninvasive tests for liver disease severity. Ann Med 2011;43:617–649.
DOI: 10.3109/07853890.2010.518623

Ekstedt M, Franzen LE, Mathiesen UL, Thorelius L, Holmqvist M, Bodemar G, et al. Long-term follow-up of patients with NAFLD and elevated liver enzymes. Hepatology 2006;44:865–873.
DOI: 10.1002/hep.21327

Ekstedt M, Hagstrom H, Nasr P, Fredrikson M, Stal P, Kechagias S, et al. Fibrosis stage is the strongest predictor for disease-specific mortality in NAFLD after up to 33 years of follow-up. Hepatology 2014. http:// dx.doi.org/10.1002/hep.27368.
DOI: 10.1002/hep.27368

Boursier J, Vergniol J, Guillet A, et al. Diagnostic accuracy and prognostic significance of blood fibrosis tests and liver stiffness measurement by FibroScan® in non-alcoholic fatty liver disease. J Hepatol. 2016;65:570-78.
DOI: 10.1016/j.jhep.2016.04.023

Blachier M, Leleu H, Peck-Radosavljevic M, Valla DC, Roudot-Thoraval F. The burden of liver disease in Europe: a review of available epidemiological data. J Hepatol 2013;58:593–608.
DOI: 10.1016/j.jhep.2012.12.005

Zoppini G, Fedeli U, Gennaro N, Saugo M, Targher G, Bonora E. Mortality from chronic liver diseases in diabetes. Am J Gastroenterol 2014;109:1020–1025.
DOI: 10.1038/ajg.2014.132

de Marco R, Locatelli F, Zoppini G, Verlato G, Bonora E, Muggeo M. Causespecific mortality in type 2 diabetes. The Verona Diabetes Study. Diabetes Care 1999;22:756–761.
DOI: 10.2337/diacare.22.5.756

Brunt EM. Nonalcoholic steatohepatitis. Semin Liver Dis 2004;24:3–20.
DOI: 10.1055/s-2004-823098

Ertle J, Dechene A, Sowa JP, Penndorf V, Herzer K, Kaiser G, et al. Nonalcoholic fatty liver disease progresses to hepatocellular carcinoma in the absence of apparent cirrhosis. Int J Cancer 2011;128:2436–2443.
DOI: 10.1002/ijc.25797

Stickel F, Hellerbrand C. Non-alcoholic fatty liver disease as a risk factor for hepatocellular carcinoma: mechanisms and implications. Gut 2010;59:1303–1307.
DOI: 10.1136/gut.2009.199661

Starley BQ, Calcagno CJ, Harrison SA. Nonalcoholic fatty liver disease and hepatocellular carcinoma: a weighty connection. Hepatology 2010;51:1820–1832.
DOI: 10.1002/hep.23594

Kwok, R.; Choi, K.; Wong, G.; Zhang, Y. Screening diabetic patients for non-alcoholic fatty liver disease with controlled attenuation parameter and liver stiffness measurements: A prospective cohort study. Gut 2015, 65, 1359–1368.

Lai, L.; Yusoff, W.; Vethakkan, S.; Mustapha, N. Screening for non-alcoholic fatty liver disease in patients with type 2 diabetes mellitus using transient elastography. J. Hepatol. 2019, 34, 1396–1403

Tuong T, Tran D, Phu P, Hong T, Dinh T, Chu D. Non-Alcoholic Fatty Liver Disease in Patients with Type 2 Diabetes: Evaluation of Hepatic Fibrosis and Steatosis Using FibroScan®. Diagnostics 2020, 10, 159;
DOI: 10.3390/diagnostics10030159

Singh A, Le P, Peerzada MM, Lopez R, Alkhouri N. The Utility of Noninvasive Scores in Assessing the Prevalence of Nonalcoholic Fatty Liver Disease and Advanced Fibrosis in Type 2 Diabetic Patients. J Clin Gastroenterol. 2018 Mar;52(3):268-272.
DOI: 10.1097/MCG.0000000000000905

Guiu B, Girod-Crevisy E, Binquet C, Duvillard L, Masson D, Lepage C, et al. Prediction for steatosis in type-2 diabetes: clinic-biological markers versus H-MR spectroscopy. Eur Radiol. 2012;22:855-63.
DOI: 10.1007/s00330-011-2326-9

Vilar-Gomez, Chalasani N. Non-invasive assessment of non-alcoholic fatty liver disease: clinical prediction rules and blood-based biomarkers. Journal of Hepatology. 2018;68:305-315.
DOI: 10.1016/j.jhep.2017.11.013

Ciardullo S, Muraca E, Perra S, Bianconi E, Zerbini F, Oltolini A, Cannistraci R, Parmeggiani P, Manzoni G, Gastaldelli A, Lattuada G, Perseghin G. Screening for non-alcoholic fatty liver disease in type 2 diabetes using non-invasive scores and association with diabetic complications. BMJ Open Diabetes Res Care. 2020 Feb;8(1):e000904.
DOI: 10.1136/bmjdrc-2019-000904

Kunustor SK, Bakker SK, Gansevoort RT, Chowdhury R, Dulaart RP. Circulating total bilirubin and risk of incident cardiovascular disease in the general population. Arterioscler Thromb Vasc Biol. 2015;35(3):716-24.
DOI: 10.1161/ATVBAHA.114.304929

Kunustor SK, Kieneker LM, Burgess S, Bakker SJL, Dullaart RPF. Circulating total bilirubin and future risk of hypertension in the general population: the prevention of renal and vascular end-stage disease (PREVEND) prospective study and a mendelian randomization approach. J Am Heart Assoc. 2017. https://doi.org/10.1161/JAHA.117.006503.
DOI: 10.1161/JAHA.117.006503

Nano J, Muka T, Cepeda M, et al. Association of circulating total bilirubin with the metabolic syndrome and type 2 diabetes: a systematic review and meta-analysis of observational evidence. Diabetes Metab. 2016;42(6):389-97.
DOI: 10.1016/j.diabet.2016.06.002

Kunutsor S, Frysz M, Verweij N, Kieneker L, Bakker SJL, Dullaart RPF. Circulating total bilirubin and risk of non-alcoholic fatty liver disease in the PREVEND study; observational findings and a Mendelian randomization study. European Journal of Epidemiology. 2020;35:123-137.
DOI: 10.1007/s10654-019-00589-0

Hinds TD Jr, Adeosun SO, Alamodi AA, Stec DE. Does bilirubin prevent hepatic steatosis through activation of the PPARα nuclear receptor? Med Hypotheses. 2016 Oct;95:54-57.
DOI: 10.1016/j.mehy.2016.08.013

Stec DE, Hinds TD Jr. Natural Product Heme Oxygenase Inducers as Treatment for Nonalcoholic Fatty Liver Disease. Int J Mol Sci. 2020 Dec 14;21(24):9493.
DOI: 10.3390/ijms21249493

Tirosh O. Hypocix signaling and cholesterol lipotoxicity in fatty liver disease progression. Oxidative Medicina and Cellular Longevity. 2018. https://doi.org/10.1155/2018/25481.54

Wong VW, Wong GL, Tsang SW, Hui AY, Chan AW, Choi PC, Chim AM, et al. Metabolic and histological features of non-alcoholic fatty liver disease patients with different serum alanine aminotransferase levels. Aliment Pharmacol Ther. 2009;29:387-396.
DOI: 10.1111/j.1365-2036.2008.03896.x

Loo SY, Chan WK. Emerging new standard for non-invasive assessment of liver disease mortality in non-alcoholic fatty liver disease. Hepatobiliary Surg Nutr. 2017;6:135-137.
DOI: 10.21037/hbsn.2017.03.06

Chan WK, Treeprasertsuk S, Imajo K, Nakajima A, Seki Y, Kasama K,Kakizaki S, et al. Clinical features and treatment of nonalcoholic fatty liver diseaseacross the Asia Pacific region-the GO ASIA initiative. Aliment Pharmacol Ther. 2018;47:816-825.
DOI: 10.1111/apt.14506

Armstrong MJ, Houlihan DD, Bentham L, et al. Presence of severity of non-alcoholic fatty liver disease in a large prospective primary care cohort. J Hepatol. 2012;56:234-40.
DOI: 10.1016/j.jhep.2011.03.020

Mathur S, Mehta DK, Kapoor S, Yadav S. Liver function in type 2 diabetes mellitus patients. Int J Sci Stud. 2016;3:43-47.

Witters, P.; Freson, K.; Verslype, C.; Peerlinck, K. Review article: Blood platelet number and function in chronic liver disease and cirrhosis. Aliment. Pharm. Ther. 2008, 27, 1017–1029.

Eddowes P, Sasso M, Allison M, Tsochatzis E, Anstee Q, Sheridan D, et al. Accuracy of FibroScan Controlled Attenuation Parameter and Liver Stiffness Measurement in Assessing Steatosis and Fibrosis in Patients With Nonalcoholic Fatty Liver Disease. Gastroenterology. 2019;156:1717-30.
DOI: 10.1053/j.gastro.2019.01.042

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