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Year 2019 / Volume 111 / Number 4
Original

Comparative study of overweight and obese patients with nonalcoholic fatty liver disease

256-263

DOI: 10.17235/reed.2019.5926/2018

Rocío Aller, Beatriz Burgueño Gomez, Rebeca Sigüenza, Conrado Fernández-Rodríguez, Natalia Fernández, Beatriz Antolín, Miguel Durà, María Pina, Sara Lorenzo, Concepción García, Daniel de Luis Román,

Abstract

Background and aims: non-alcoholic fatty liver disease (NAFLD) is the most common chronic liver disorder in the western world. Although NAFLD prevalence is higher in patients with a BMI > 25 kg /m2, it is unclear if there are differences between overweight and obese patients. The associated biochemical, dietary and genetic parameters were compared between overweight and obese patients with NAFLD. Methods: patients with biopsy-proven NAFLD (n = 203) were enrolled in a cross-sectional study. The MEDAS questionnaire was used to assess adherence to the Mediterranean diet. Biochemical, anthropometrical parameters and the I148M variant (rs738409) of the PNPLA3 gene and rs180069 of the TNF-α gene were evaluated. Results: overweight patients had higher serum adiponectin levels (22.5 ± 21.9 vs 11.2 ± 18.1 ng/ml; p < 0.05) and lower resistin (3.3 ± 1.7 vs 8.1 ± 8 ng/ml; p < 0.001) and leptin concentrations (22.9 ± 21.9 vs 55.8 ± 45 ng/ml; p < 0.001) than obese patients. Non-alcoholic steatohepatitis (NASH) was more frequent in the obese group (59.3% vs 41.3%; p = 0.02). The multivariate analysis showed adherence to the Mediterranean diet to be an independent protective factor for NASH and liver fibrosis in overweight patients (OR 0.7, 95% CI 0.5-0.8). Conclusions: NASH was more prevalent in obese patients than in overweight subjects. HOMA-IR and adherence to the Mediterranean diet provided protection against fibrosis in overweight patients. Adherence to the Mediterranean diet was the only independent factor associated with NASH in these patients.

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References

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DOI: 10.1002/hep.21327

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DOI: 10.1097/MD.0000000000007041

4. Matteoni CA, Younossi ZM, Gramlich T, Boparai N, Liu YC, McCullough AJ. Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity. Gastroenterology. 1999;116(6):1413-9.

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DOI: 10.1002/hep.20466

9. Kim D, Kim WR. Nonobese Fatty Liver Disease. Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association. 2017;15(4):474-85.

DOI: 10.1016/j.cgh.2016.08.028

10. Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, et al. The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Gastroenterological Association, American Association for the Study of Liver Diseases, and American College of Gastroenterology. Gastroenterology. 2012;142(7):1592-609.

DOI: 10.1053/j.gastro.2012.04.001

11. Ratziu V, Bellentani S, Cortez-Pinto H, Day C, Marchesini G. A position statement on NAFLD/NASH based on the EASL 2009 special conference. Journal of hepatology. 2010;53(2):372-84.

DOI: 10.1016/j.jhep.2010.04.008

12. Wildman RP, Muntner P, Reynolds K, McGinn AP, Rajpathak S, Wylie-Rosett J, et al. The obese without cardiometabolic risk factor clustering and the normal weight with cardiometabolic risk factor clustering: prevalence and correlates of 2 phenotypes among the US population (NHANES 1999-2004). Archives of internal medicine. 2008;168(15):1617-24.

DOI: 10.1001/archinte.168.15.1617

13. Dongiovanni P, Anstee QM, Valenti L. Genetic predisposition in NAFLD and NASH: impact on severity of liver disease and response to treatment. Current pharmaceutical design. 2013;19(29):5219-38.

DOI: 10.2174/13816128113199990381

14. Bedossa P. Pathology of non-alcoholic fatty liver disease. Liver international : official journal of the International Association for the Study of the Liver. 2017;37 Suppl 1:85-9.

DOI: 10.1111/liv.13301

15. Duart Duart MJ, Arroyo CO, Moreno Frigols JL. Validation of a kinetic model for the reactions in RIA. Clinical chemistry and laboratory medicine. 2002;40(11):1161-7.

16. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clinical chemistry. 1972;18(6):499-502.

17. Pfutzner A, Langenfeld M, Kunt T, Lobig M, Forst T. Evaluation of human resistin assays with serum from patients with type 2 diabetes and different degrees of insulin resistance. Clinical laboratory. 2003;49(11-12):571-6.

18. Meier U, Gressner AM. Endocrine regulation of energy metabolism: review of pathobiochemical and clinical chemical aspects of leptin, ghrelin, adiponectin, and resistin. Clinical chemistry. 2004;50(9):1511-25.

DOI: 10.1373/clinchem.2004.032482

19. Suominen P. Evaluation of an enzyme immunometric assay to measure serum adiponectin concentrations. Clinical chemistry. 2004;50(1):219-21.

DOI: 10.1373/clinchem.2003.025833

20. Executive Summary of The Third Report of The National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, And Treatment of High Blood Cholesterol In Adults (Adult Treatment Panel III). Jama. 2001;285(19):2486-97.

DOI: 10.1001/jama.285.19.2486

21. Leung JC, Loong TC, Wei JL, Wong GL, Chan AW, Choi PC, et al. Histological severity and clinical outcomes of nonalcoholic fatty liver disease in nonobese patients. Hepatology (Baltimore, Md). 2017;65(1):54-64.

DOI: 10.1002/hep.28697

22. Hadizadeh F, Faghihimani E, Adibi P. Nonalcoholic fatty liver disease: Diagnostic biomarkers. World journal of gastrointestinal pathophysiology. 2017;8(2):11-26.

DOI: 10.4291/wjgp.v8.i2.11

23. Gatselis NK, Ntaios G, Makaritsis K, Dalekos GN. Adiponectin: a key playmaker adipocytokine in non-alcoholic fatty liver disease. Clinical and experimental medicine. 2014;14(2):121-31.

DOI: 10.1007/s10238-012-0227-0

24. Chitturi S, Farrell G, Frost L, Kriketos A, Lin R, Fung C, et al. Serum leptin in NASH correlates with hepatic steatosis but not fibrosis: a manifestation of lipotoxicity? Hepatology (Baltimore, Md). 2002;36(2):403-9.

DOI: 10.1053/jhep.2002.34738

25. Stojsavljevic S, Gomercic Palcic M, Virovic Jukic L, Smircic Duvnjak L, Duvnjak M. Adipokines and proinflammatory cytokines, the key mediators in the pathogenesis of nonalcoholic fatty liver disease. World journal of gastroenterology. 2014;20(48):18070-91.

DOI: 10.3748/wjg.v20.i48.18070

DOI: 10.1371/journal.pone.0076161

27. Angulo P, Alba LM, Petrovic LM, Adams LA, Lindor KD, Jensen MD. Leptin, insulin resistance, and liver fibrosis in human nonalcoholic fatty liver disease. Journal of hepatology. 2004;41(6):943-9.

DOI: 10.1016/j.jhep.2004.08.020

28. Sofi F, Casini A. Mediterranean diet and non-alcoholic fatty liver disease: new therapeutic option around the corner? World journal of gastroenterology. 2014;20(23):7339-46.

DOI: 10.3748/wjg.v20.i23.7339

DOI: 10.1186/1743-7075-6-30

31. Kontogianni MD, Tileli N, Margariti A, Georgoulis M, Deutsch M, Tiniakos D, et al. Adherence to the Mediterranean diet is associated with the severity of non-alcoholic fatty liver disease. Clinical nutrition (Edinburgh, Scotland). 2014;33(4):678-83.

DOI: 10.1016/j.clnu.2013.08.014

32. Shin KC, Chung JH, Lee KH. Effects of TNF-alpha and leptin on weight loss in patients with stable chronic obstructive pulmonary disease. The Korean journal of internal medicine. 2007;22(4):249-55.

DOI: 10.3904/kjim.2007.22.4.249

33. Crespo J, Cayon A, Fernandez-Gil P, Hernandez-Guerra M, Mayorga M, Dominguez-Diez A, et al. Gene expression of tumor necrosis factor alpha and TNF-receptors, p55 and p75, in nonalcoholic steatohepatitis patients. Hepatology (Baltimore, Md). 2001;34(6):1158-63.

DOI: 10.1053/jhep.2001.29628

34. Morin CL, Schlaepfer IR, Eckel RH. Tumor necrosis factor-alpha eliminates binding of NF-Y and an octamer-binding protein to the lipoprotein lipase promoter in 3T3-L1 adipocytes. The Journal of clinical investigation. 1995;95(4):1684-9.

DOI: 10.1172/JCI117844

35. Valenti L, Fracanzani AL, Dongiovanni P, Santorelli G, Branchi A, Taioli E, et al. Tumor necrosis factor alpha promoter polymorphisms and insulin resistance in nonalcoholic fatty liver disease. Gastroenterology. 2002;122(2):274-80.

DOI: 10.1053/gast.2002.31065

1. Fazel Y, Koenig AB, Sayiner M, et al. Epidemiology and natural history of non-alcoholic fatty liver disease. Metabolism: clinical and experimental. 2016;65(8):1017-25.

DOI: 10.1016/j.metabol.2016.01.012

2. Ekstedt M, Franzen LE, Mathiesen UL, et al. Long-term follow-up of patients with NAFLD and elevated liver enzymes. Hepatology (Baltimore, Md). 2006;44(4):865-73.

DOI: 10.1002/hep.21327

3. Zhang S, Du T, Li M, et al. Triglyceride glucose-body mass index is effective in identifying nonalcoholic fatty liver disease in nonobese subjects. Medicine. 2017;96(22):e7041.

DOI: 10.1097/MD.0000000000007041

4. Matteoni CA, Younossi ZM, Gramlich T, et al. Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity. Gastroenterology. 1999;116(6):1413-9.

DOI: 10.1016/S0016-5085(99)70506-8

5. Grundy SM, Cleeman JI, Daniels SR, et al. Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation. 2005;112(17):2735-52.

DOI: 10.1161/CIRCULATIONAHA.105.169404

6. Gomez de la Cuesta S, Aller de la Fuente R, Tafur Sanchez C, et al. Analytical, anthropometric and dietary factors associated with the development of fibrosis in patients with nonalcoholic fatty liver disease. Revista espanola de enfermedades digestivas : organo oficial de la Sociedad Espanola de Patologia Digestiva. 2018;110(5):292-8.

DOI: 10.17235/reed.2018.5118/2017

8. Browning JD, Szczepaniak LS, Dobbins R, et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology (Baltimore, Md). 2004;40(6):1387-95.

DOI: 10.1002/hep.20466

9. Kim D, Kim WR. Nonobese Fatty Liver Disease. Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association. 2017;15(4):474-85.

DOI: 10.1016/j.cgh.2016.08.028

10. Chalasani N, Younossi Z, Lavine JE, et al. The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Gastroenterological Association, American Association for the Study of Liver Diseases, and American College of Gastroenterology. Gastroenterology. 2012;142(7):1592-609.

DOI: 10.1053/j.gastro.2012.04.001

11. Ratziu V, Bellentani S, Cortez-Pinto H, et al. A position statement on NAFLD/NASH based on the EASL 2009 special conference. Journal of hepatology. 2010;53(2):372-84.

DOI: 10.1016/j.jhep.2010.04.008

12. Wildman RP, Muntner P, Reynolds K, et al. The obese without cardiometabolic risk factor clustering and the normal weight with cardiometabolic risk factor clustering: prevalence and correlates of 2 phenotypes among the US population (NHANES 1999-2004). Archives of internal medicine. 2008;168(15):1617-24.

DOI: 10.1001/archinte.168.15.1617

13. Dongiovanni P, Anstee QM, Valenti L. Genetic predisposition in NAFLD and NASH: impact on severity of liver disease and response to treatment. Current pharmaceutical design. 2013;19(29):5219-38.

DOI: 10.2174/13816128113199990381

14. Bedossa P. Pathology of non-alcoholic fatty liver disease. Liver international : official journal of the International Association for the Study of the Liver. 2017;37 Suppl 1:85-9.

DOI: 10.1111/liv.13301

15. Duart Duart MJ, Arroyo CO, Moreno Frigols JL. Validation of a kinetic model for the reactions in RIA. Clinical chemistry and laboratory medicine. 2002;40(11):1161-7.

DOI: 10.1515/cclm.2002.203

17. Pfutzner A, Langenfeld M, Kunt T,et al. Evaluation of human resistin assays with serum from patients with type 2 diabetes and different degrees of insulin resistance. Clinical laboratory. 2003;49(11-12):571-6.

DOI: 10.1373/clinchem.2004.032482

19. Suominen P. Evaluation of an enzyme immunometric assay to measure serum adiponectin concentrations. Clinical chemistry. 2004;50(1):219-21.

DOI: 10.1373/clinchem.2003.025833

DOI: 10.1001/jama.285.19.2486

21. Leung JC, Loong TC, Wei JL, et al. Histological severity and clinical outcomes of nonalcoholic fatty liver disease in nonobese patients. Hepatology (Baltimore, Md). 2017;65(1):54-64.

DOI: 10.1002/hep.28697

22. Hadizadeh F, Faghihimani E, Adibi P. Nonalcoholic fatty liver disease: Diagnostic biomarkers. World journal of gastrointestinal pathophysiology. 2017;8(2):11-26.

DOI: 10.4291/wjgp.v8.i2.11

23. Gatselis NK, Ntaios G, Makaritsis K, et al . Adiponectin: a key playmaker adipocytokine in non-alcoholic fatty liver disease. Clinical and experimental medicine. 2014;14(2):121-31.

DOI: 10.1007/s10238-012-0227-0

24. Chitturi S, Farrell G, Frost L, et al. Serum leptin in NASH correlates with hepatic steatosis but not fibrosis: a manifestation of lipotoxicity? Hepatology (Baltimore, Md). 2002;36(2):403-9.

DOI: 10.1053/jhep.2002.34738

25. Stojsavljevic S, Gomercic Palcic M, Virovic Jukic L, et al. Adipokines and proinflammatory cytokines, the key mediators in the pathogenesis of nonalcoholic fatty liver disease. World journal of gastroenterology. 2014;20(48):18070-91.

DOI: 10.3748/wjg.v20.i48.18070

26. Hashiba M, Ono M, Hyogo H, et al. Glycemic variability is an independent predictive factor for development of hepatic fibrosis in nonalcoholic fatty liver disease. PloS one. 2013;8(11):e76161.

DOI: 10.1371/journal.pone.0076161

27. Angulo P, Alba LM, Petrovic LM, et al. Leptin, insulin resistance, and liver fibrosis in human nonalcoholic fatty liver disease. Journal of hepatology. 2004;41(6):943-9.

DOI: 10.1016/j.jhep.2004.08.020

28. Garcia-Monzon C, Vargas-Castrillon J, Porrero JL, et al. Prevalence and risk factors for biopsy-proven non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in a prospective cohort of adult patients with gallstones. Liver international : official journal of the International Association for the Study of the Liver. 2015;35(8):1983-91.

DOI: 10.1111/liv.12813

29. Sofi F, Casini A. Mediterranean diet and non-alcoholic fatty liver disease: new therapeutic option around the corner? World journal of gastroenterology. 2014;20(23):7339-46.

DOI: 10.3748/wjg.v20.i23.7339

30. Aller R, Izaola O, de la Fuente B, et al. Mediterranean diet is associated with liver histology in patients with non alcoholic fatty liver disease. Nutricion hospitalaria. 2015;32(6):2518-24.

31. Tzima N, Pitsavos C, Panagiotakos DB, et al. Adherence to the Mediterranean diet moderates the association of aminotransferases with the prevalence of the metabolic syndrome; the ATTICA study. Nutrition & metabolism. 2009;6:30.

DOI: 10.1186/1743-7075-6-30

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Aller R, Burgueño Gomez B, Sigüenza R, Fernández-Rodríguez C, Fernández N, Antolín B, et all. Comparative study of overweight and obese patients with nonalcoholic fatty liver disease . 5926/2018

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Publication history

Received: 17/09/2018

Accepted: 29/11/2018

Online First: 11/02/2019

Published: 04/04/2019

Article revision time: 60 days

Article Online First time: 147 days

Article editing time: 199 days

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