Diet, weight loss, and liver health in nonalcoholic fatty liver disease: Pathophysiology, evidence, and practice

Hepatology

Volumn 63, Issue 6, 2016, Pages 2032-2043

  Marchesini, Giulio ^a   Petta, Salvatore ^b   Dalle Grave, Riccardo ^c  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF PALERMO   (Italy)

^c Villa Garda Hospital   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

TRIACYLGLYCEROL;

CALORIC INTAKE; CLINICAL EFFECTIVENESS; COGNITIVE BEHAVIORAL THERAPY; DIET; GENE INTERACTION; GENETIC BACKGROUND; HUMAN; LIFESTYLE MODIFICATION; LIPID METABOLISM; LIPID STORAGE; LIPOGENESIS; LIVER METABOLISM; MEDITERRANEAN DIET; NONALCOHOLIC FATTY LIVER; PATHOPHYSIOLOGY; PATIENT SAFETY; PHYSICAL ACTIVITY; PRIORITY JOURNAL; REVIEW; RISK FACTOR; WEIGHT REDUCTION;

EID: 84978245141     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.28392     Document Type: Review

References (79)

1. Wong RJ, Aguilar M, Cheung R, Perumpail RB, Harrison SA, Younossi ZM, Ahmed A. Nonalcoholic steatohepatitis is the second leading etiology of liver disease among adults awaiting liver transplantation in the United States. Gastroenterology 2015;148:547-555.
2. Bergqvist CJ, Skoien R, Horsfall L, Clouston AD, Jonsson JR, Powell EE. Awareness and opinions of non-alcoholic fatty liver disease by hospital specialists. Intern Med J 2013;43:247-253.
3. Ratziu V, Cadranel JF, Serfaty L, Denis J, Renou C, Delassalle P, et al. A survey of patterns of practice and perception of NAFLD in a large sample of practicing gastroenterologists in France. J Hepatol 2012;57:376-383.
4. Donnelly KL, Smith CI, Schwarzenberg SJ, Jessurun J, Boldt MD, Parks EJ. Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J Clin Invest 2005;115:1343-1351.
5. Ducheix S, Montagner A, Theodorou V, Ferrier L, Guillou H. The liver X receptor: a master regulator of the gut-liver axis and a target for non alcoholic fatty liver disease. Biochem Pharmacol 2013;86:96-105.
6. Fabbrini E, Mohammed BS, Magkos F, Korenblat KM, Patterson BW, Klein S. Alterations in adipose tissue and hepatic lipid kinetics in obese men and women with nonalcoholic fatty liver disease. Gastroenterology 2008;134:424-431.
7. Browning JD, Horton JD. Molecular mediators of hepatic steatosis and liver injury. J Clin Invest 2004;114:147-152.
8. Loomba R, Schork N, Chen CH, Bettencourt R, Bhatt A, Ang B, et al.; Genetics of NAFLD in Twins Consortium. Heritability of hepatic fibrosis and steatosis based on a prospective twin study. Gastroenterology 2015;149:1784-1793.
9. Zarrinpar A, Gupta S, Maurya MR, Subramaniam S, Loomba R. Serum microRNAs explain discordance of non-alcoholic fatty liver disease in monozygotic and dizygotic twins: a prospective study. Gut 2015 May 22. pii: gutjnl-2015-309456. doi: 10.1136/gutjnl-2015-309456. [Epub ahead of print]
10. Browning JD, Szczepaniak LS, Dobbins R, Nuremberg P, Horton JD, Cohen JC, et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 2004;40:1387-1395.
11. Petersen KF, Dufour S, Feng J, Befroy D, Dziura J, Dalla Man C, et al. Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men. Proc Natl Acad Sci U S A 2006;103:18273-18277.
12. Speliotes EK, Yerges-Armstrong LM, Wu J, Hernaez R, Kim LJ, Palmer CD, et al. Genome-wide association analysis identifies variants associated with nonalcoholic fatty liver disease that have distinct effects on metabolic traits. PLoS Genet 2011;7:e1001324.
13. Kozlitina J, Smagris E, Stender S, Nordestgaard BG, Zhou HH, Tybjaerg-Hansen A, et al. Exome-wide association study identifies a TM6SF2 variant that confers susceptibility to nonalcoholic fatty liver disease. Nat Genet 2014;46:352-356.
14. Sookoian S, Pirola CJ. Meta-analysis of the influence of I148M variant of patatin-like phospholipase domain containing 3 gene (PNPLA3) on the susceptibility and histological severity of nonalcoholic fatty liver disease. Hepatology 2011;53:1883-1894.
15. Dongiovanni P, Petta S, Maglio C, Fracanzani AL, Pipitone R, Mozzi E, et al. Transmembrane 6 superfamily member 2 gene variant disentangles nonalcoholic steatohepatitis from cardiovascular disease. Hepatology 2015;61:506-514.
16. Lazo M, Hernaez R, Eberhardt MS, Bonekamp S, Kamel I, Guallar E, et al. Prevalence of nonalcoholic fatty liver disease in the United States: the Third National Health and Nutrition Examination Survey, 1988-1994. Am J Epidemiol 2013;178:38-45.
17. Lonardo A, Ballestri S, Marchesini G, Angulo P, Loria P. Nonalcoholic fatty liver disease: a precursor of the metabolic syndrome. Dig Liver Dis 2015;47:181-190.
18. Cui Z, Truesdale KP, Bradshaw PT, Cai J, Stevens J. Three-year weight change and cardiometabolic risk factors in obese and normal weight adults who are metabolically healthy: the atherosclerosis risk in communities study. Int J Obes (Lond) 2015;39:1203-1208.
19. Marchesini G, Mazzotti A. NAFLD incidence and remission: only a matter of weight gain and weight loss? J Hepatol 2015;62:15-17.
20. De la Cruz AC, Bugianesi E, George J, Day CP, Liaquat H, Charatcharoenwitthaya P, et al. Characteristics and long-term prognosis of lean patients with nonalcoholic fatty liver disease [Abstract]. Gastroenterology 2014;146:S-909.
21. Green CJ, Hodson L. The influence of dietary fat on liver fat accumulation. Nutrients 2014;6:5018-5033.
22. Utzschneider KM, Bayer-Carter JL, Arbuckle MD, Tidwell JM, Richards TL, Craft S. Beneficial effect of a weight-stable, low-fat/low-saturated fat/low-glycaemic index diet to reduce liver fat in older subjects. Br J Nutr 2013;109:1096-1104.
23. Rosqvist F, Iggman D, Kullberg J, Cedernaes J, Johansson HE, Larsson A, et al. Overfeeding polyunsaturated and saturated fat causes distinct effects on liver and visceral fat accumulation in humans. Diabetes 2014;63:2356-2368.
24. Sobrecases H, Lê KA, Bortolotti M, Schneiter P, Ith M, Kreis R, Boesch C, et al. Effects of short-term overfeeding with fructose, fat and fructose plus fat on plasma and hepatic lipids in healthy men. Diabetes Metab 2010;36:244-246.
25. Vors C, Pineau G, Drai J, Meugnier E, Pesenti S, Laville M, et al. Postprandial endotoxemia linked with chylomicrons and LPS handling in obese vs lean men: a lipid dose-effect trial. J Clin Endocrinol Metab 2015;100:3427-3435.
26. Zelber-Sagi S, Nitzan-Kaluski D, Goldsmith R, Webb M, Blendis L, Halpern Z, Oren R. Long term nutritional intake and the risk for non-alcoholic fatty liver disease (NAFLD): a population based study. J Hepatol 2007;47:711-717.
27. Maersk M, Belza A, Stodkilde-Jorgensen H, Ringgaard S, Chabanova E, Thomsen H, et al. Sucrose-sweetened beverages increase fat storage in the liver, muscle, and visceral fat depot: a 6-mo randomized intervention study. Am J Clin Nutr 2012;95:283-289.
28. Abdelmalek MF, Suzuki A, Guy C, Unalp-Arida A, Colvin R, Johnson RJ, Diehl AM. Increased fructose consumption is associated with fibrosis severity in patients with nonalcoholic fatty liver disease. Hepatology 2010;51:1961-1971.
29. Chiu S, Sievenpiper JL, de Souza RJ, Cozma AI, Mirrahimi A, Carleton AJ, Effect of fructose on markers of non-alcoholic fatty liver disease (NAFLD): a systematic review and meta-analysis of controlled feeding trials. Eur J Clin Nutr 2014;68:416-423.
30. Petta S, Marchesini G, Caracausi L, Macaluso FS, Camma C, Ciminnisi S, et al. Industrial, not fruit fructose intake is associated with the severity of liver fibrosis in genotype 1 chronic hepatitis C patients. J Hepatol 2013;59:1169-1176.
31. Madero M, Arriaga JC, Jalal D, Rivard C, McFann K, Perez-Mendez O, et al. The effect of two energy-restricted diets, a low-fructose diet versus a moderate natural fructose diet, on weight loss and metabolic syndrome parameters: a randomized controlled trial. Metabolism 2011;60:1551-1559.
32. Hannukainen JC, Nuutila P, Borra R, Kaprio J, Kujala UM, Janatuinen T, et al. Increased physical activity decreases hepatic free fatty acid uptake: a study in human monozygotic twins. J Physiol 2007;578:347-358.
33. Lee S, Bacha F, Hannon T, Kuk JL, Boesch C, Arslanian S. Effects of aerobic versus resistance exercise without caloric restriction on abdominal fat, intrahepatic lipid, and insulin sensitivity in obese adolescent boys: a randomized, controlled trial. Diabetes 2012;61:2787-2795.
34. 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 Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology 2012;55:2005-2023.
35. Ratziu V, Bellentani S, Cortez-Pinto H, Day C, Marchesini G. A position statement on NAFLD/NASH based on the EASL 2009 special conference. J Hepatol 2010;53:372-384.
36. Patel NS, Doycheva I, Peterson MR, Hooker J, Kisselva T, Schnabl B, et al. Effect of weight loss on magnetic resonance imaging estimation of liver fat and volume in patients with nonalcoholic steatohepatitis. Clin Gastroenterol Hepatol 2015;13:561-568.e1.
37. Dalle Grave R, Calugi S, Gavasso I, El Ghoch M, Marchesini G. A randomized trial of energy-restricted high-protein versus high-carbohydrate, low-fat diet in morbid obesity. Obesity (Silver Spring) 2013;21:1774-1781.
38. Haufe S, Engeli S, Kast P, Bohnke J, Utz W, Haas V, et al. Randomized comparison of reduced fat and reduced carbohydrate hypocaloric diets on intrahepatic fat in overweight and obese human subjects. Hepatology 2011;53:1504-1514.
39. Estruch R, Ros E, Salas-Salvado J, Covas MI, Corella D, Aros F, et al. Primary prevention of cardiovascular disease with a Mediterranean diet. N Engl J Med 2013;368:1279-1290.
40. Villanova N, Pasqui F, Burzacchini S, Forlani G, Manini R, Suppini A, et al. A physical activity program to reinforce weight maintenance following a behavior program in overweight/obese subjects. Int J Obes (Lond) 2006;30:697-703.
41. Keating SE, Hackett DA, George J, Johnson NA. Exercise and non-alcoholic fatty liver disease: a systematic review and meta-analysis. J Hepatol 2012;57:157-166.
42. Montesi L, Caselli C, Centis E, Nuccitelli C, Moscatiello S, Suppini A, Marchesini G. Physical activity support or weight loss counseling for nonalcoholic fatty liver disease? World J Gastroenterol 2014;20:10128-10136.
43. Fabricatore AN. Behavior therapy and cognitive-behavioral therapy of obesity: is there a difference? J Am Diet Assoc 2007;107:92-99.
44. Jensen MD, Ryan DH, Apovian CM, Ard JD, Comuzzie AG, Donato KA, et al. 2013 AHA/ACC/TOS guideline for the management of overweight and obesity in adults: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines and The Obesity Society. Circulation 2014;129:S102-S138.
45. Bellentani S, Dalle Grave R, Suppini A, Marchesini G. Behavior therapy in nonalcoholic fatty liver disease: The need for a multidisciplinary approach. Hepatology 2008;47:746-754.
46. Arena R, Lavie CJ, Hivert MF, Williams MA, Briggs PD, Guazzi M. Who will deliver comprehensive healthy lifestyle interventions to combat non-communicable disease? Introducing the healthy lifestyle practitioner discipline. Exp Rev Cardiovasc Ther 2016;14:15-22.
47. Dalle Grave R, Calugi S, Centis E, El Ghoch M, Marchesini G. Cognitive-behavioral strategies to increase the adherence to exercise in the management of obesity. J Obes 2011;2011:348293.
48. Wadden TA, Webb VL, Moran CH, Bailer BA. Lifestyle modification for obesity: new developments in diet, physical activity, and behavior therapy. Circulation 2012;125:1157-1170.
49. Wilson GT, Schlam TR. The transtheoretical model and motivational interviewing in the treatment of eating and weight disorders. Clin Psychol Rev 2004;24:361-378.
50. Miller WR, Rollnick S. Motivational Interviewing, 2nd ed. New York: The Guilford Press; 2002.
51. Centis E, Moscatiello S, Bugianesi E, Bellentani S, Fracanzani AL, Calugi S, et al. Stage of change and motivation to healthier lifestyle in non-alcoholic fatty liver disease. J Hepatol 2013;58:771-777.
52. Wesche-Thobaben JA. The development and description of the comparison group in the Look AHEAD trial. Clin Trials 2011;8:320-329.
53. Wing RR, Jeffery RW, Burton LR, Thorson C, Nissinoff KS, Baxter JE. Food provision vs structured meal plans in the behavioral treatment of obesity. Int J Obes Relat Metab Disord 1996;20:56-62.
54. Perri MG, Martin AD, Leermakers EA, Sears SF, Notelovitz M. Effects of group- versus home-based exercise in the treatment of obesity. J Consult Clin Psychol 1997;65:278-285.
55. Andersen RE, Wadden TA, Bartlett SJ, Zemel B, Verde TJ, Franckowiak SC. Effects of lifestyle activity vs structured aerobic exercise in obese women: a randomized trial. JAMA 1999;281:335-340.
56. Jakicic JM, Wing RR, Butler BA, Robertson RJ. Prescribing exercise in multiple short bouts versus one continuous bout: effects on adherence, cardiorespiratory fitness, and weight loss in overweight women. Int J Obes Relat Metab Disord 1995;19:893-901.
57. Mangeri F, Montesi L, Forlani G, Dalle Grave R, Marchesini G. A standard ballroom and Latin dance program to improve fitness and adherence to physical activity in individuals with type 2 diabetes and in obesity. Diabetol Metab Syndr 2014;6:74.
58. Ueno T, Sugawara H, Sujaku K, Hashimoto O, Tsuji R, Tamaki S, et al. Therapeutic effects of restricted diet and exercise in obese patients with fatty liver. J Hepatol 1997;27:103-107.
59. Hickman IE, Jonsson JR, Prins JB, Ash S, Purdie DM, Clouston AD, Powell EE. Modest weight loss and physical activity in overweight patients with chronic liver disease results in sustained improvements in alanine aminotransferase, fasting insulin, and quality of life. Gut 2004;53:413-419.
60. Kantartzis K, Thamer C, Peter A, Machann J, Schick F, Schraml C, et al. High cardiorespiratory fitness is an independent predictor of the reduction in liver fat during a lifestyle intervention in non-alcoholic fatty liver disease. Gut 2009;58:1281-1288.
61. Oza N, Eguchi Y, Mizuta T, Ishibashi E, Kitajima Y, Horie H, et al. A pilot trial of body weight reduction for nonalcoholic fatty liver disease with a home-based lifestyle modification intervention delivered in collaboration with interdisciplinary medical staff. J Gastroenterol 2009;44:1203-1208.
62. St George A, Bauman A, Johnston A, Farrell G, Chey T, George J. Effect of a lifestyle intervention in patients with abnormal liver enzymes and metabolic risk factors. J Gastroenterol Hepatol 2009;24:399-407.
63. Albu JB, Heilbronn LK, Kelley DE, Smith SR, Azuma K, Berk ES, et al. Metabolic changes following a 1-year diet and exercise intervention in patients with type 2 diabetes. Diabetes 2010;59:627-633.
64. Lazo M, Solga SF, Horska A, Bonekamp S, Diehl AM, Brancati FL, et al. Effect of a 12-month intensive lifestyle intervention on hepatic steatosis in adults with type 2 diabetes. Diabetes Care 2010;33:2156-2163.
65. Promrat K, Kleiner DE, Niemeier HM, Jackvony E, Kearns M, Wands JR, et al. Randomized controlled trial testing the effects of weight loss on nonalcoholic steatohepatitis. Hepatology 2010;51:121-129.
66. Moscatiello S, Di Luzio R, Bugianesi E, Suppini A, Hickman I, Di Domizio S, et al. Cognitive-behavioral treatment of non-alcoholic fatty liver disease: a propensity score-adjusted observational study. Obesity (Silver Spring) 2011;19:763-770.
67. Sun WH, Song MQ, Jiang CQ, Xin YN, Ma JL, Liu YX, et al. Lifestyle intervention in non-alcoholic fatty liver disease in Chengyang District, Qingdao, China. World J Hepatol 2012;4:224-230.
68. Eckard C, Cole R, Lockwood J, Torres DM, Williams CD, Shaw JC, Harrison SA. Prospective histopathologic evaluation of lifestyle modification in nonalcoholic fatty liver disease: a randomized trial. Therap Adv Gastroenterol 2013;6:249-259.
69. Scaglioni F, Marino M, Ciccia S, Procaccini A, Busacchi M, Loria P, et al. Short-term multidisciplinary non-pharmacological intervention is effective in reducing liver fat content assessed non-invasively in patients with nonalcoholic fatty liver disease (NAFLD). Clin Res Hepatol Gastroenterol 2013;37:353-358.
70. Hickman IJ, Byrne NM, Croci I, Chachay VS, Clouston AD, Hills AP, et al. A pilot randomised study of the metabolic and histological effects of exercise in non-alcoholic steatohepatitis. J Diabetes Metab 2013;4:300.
71. Yoshimura E, Kumahara H, Tobina T, Matsuda T, Ayabe M, Kiyonaga A, et al. Lifestyle intervention involving calorie restriction with or without aerobic exercise training improves liver fat in adults with visceral adiposity. J Obes 2014;2014:197216.
72. Wong VW, Chan RS, Wong GL, Cheung BH, Chu WC, Yeung DK, et al. Community-based lifestyle modification programme for non-alcoholic fatty liver disease: a randomized controlled trial. J Hepatol 2013;59:536-542.
73. Vilar-Gomez E, Martinez-Perez Y, Calzadilla-Bertot L, Torres-Gonzalez A, Gra-Oramas B, Gonzalez-Fabian L, et al. Weight loss through lifestyle modification significantly reduces features of nonalcoholic steatohepatitis. Gastroenterology 2015;149:367-378.e5; quiz, e14-15.
74. Ekstedt M, Hagstrom H, Nasr P, Fredrikson M, Stal P, Kechagias S, Hultcrantz R. Fibrosis stage is the strongest predictor for disease-specific mortality in NAFLD after up to 33 years of follow-up. Hepatology 2015;61:1547-1554.
75. Lassailly G, Caiazzo R, Buob D, Pigeyre M, Verkindt H, Labreuche J, et al. Bariatric surgery reduces features of nonalcoholic steatohepatitis in morbidly obese patients. Gastroenterology 2015;149:379-388.
76. Burza MA, Romeo S, Kotronen A, Svensson PA, Sjoholm K, Torgerson JS, et al. Long-term effect of bariatric surgery on liver enzymes in the Swedish Obese Subjects (SOS) study. PLoS One 2013;8:e60495.
77. Sjostrom L. Review of the key results from the Swedish Obese Subjects (SOS) trial—a prospective controlled intervention study of bariatric surgery. J Intern Med 2013;273:219-234.
78. Pi-Sunyer X. The Look AHEAD Trial: a review and discussion of its outcomes. Curr Nutr Rep 2014;3:387-391.
79. Marchesini G, Mazzella N, Forlani G. Weight loss for a healthy liver. Gastroenterology 2015;149:274-278.