Omega-3 supplementation and non-alcoholic fatty liver disease: A systematic review and meta-analysis

Journal of Hepatology

Volumn 56, Issue 4, 2012, Pages 944-951

  Parker, Helen M ^a   Johnson, Nathan A ^a   Burdon, Catriona A ^a   Cohn, Jeffrey S ^b   O'Connor, Helen T ^a   George, Jacob ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b HEART RESEARCH INSTITUTE   (Australia)

Author keywords

Diet; Fatty liver; Fish oil; Obesity; Polyunsaturated fatty acid

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; FISH OIL; OMEGA 3 FATTY ACID; PLACEBO;

DIET SUPPLEMENTATION; DRUG EFFECT; HUMAN; INSULIN RESISTANCE; LIVER FUNCTION TEST; META ANALYSIS; NONALCOHOLIC FATTY LIVER; OBESITY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SYSTEMATIC REVIEW; TREATMENT OUTCOME;

ADULT; ALANINE TRANSAMINASE; ASPARTATE AMINOTRANSFERASES; DIETARY SUPPLEMENTS; FATTY ACIDS, OMEGA-3; FATTY LIVER; FEMALE; HUMANS; LIPID METABOLISM; LIVER; MALE; TREATMENT OUTCOME;

EID: 84858703583     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2011.08.018     Document Type: Review

References (69)

1. P. Pettinelli, T. del Pozo, J. Araya, R. Rodrigo, A.V. Araya, and G. Smok Enhancement in liver SREBP-1c/PPAR-alpha ratio and steatosis in obese patients: correlations with insulin resistance and n-3 long-chain polyunsaturated fatty acid depletion Biochim Biophys Acta-Mol Basis Dis 1792 2009 1080 1086
2. A.J. Sanyal, N. Chalasani, K.V. Kowdley, A. McCullough, A.M. Diehl, and N.M. Bass Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis N Engl J Med 362 2010 1675 1685
3. S.M. Mazhar, M. Shiehmorteza, and C.B. Sirlin Noninvasive assessment of hepatic steatosis Clin Gastroenterol Hepatol 7 2009 135 140
4. A. Wieckowska, A.J. McCullough, and A.E. Feldstein Noninvasive diagnosis and monitoring of nonalcoholic steatohepatitis: present and future Hepatology 46 2007 582 589 (Pubitemid 47344794)
5. S.A. Harrison, S. Torgerson, and P.H. Hayashi The natural history of nonalcoholic fatty liver disease: a clinical histopathological study Am J Gastroenterol 98 2003 2042 2047 (Pubitemid 37185803)
6. L.A. Adams, J.F. Lymp, J. St Sauver, S.O. Sanderson, K.D. Lindor, and A. Feldstein The natural history of nonalcoholic fatty liver disease: a population-based cohort study Gastroenterology 129 2005 113 121 (Pubitemid 41002048)
7. M. Ekstedt, L.E. Franzen, U.L. Mathiesen, L. Thorelius, M. Holmqvist, and G. Bodemar Long-term follow-up of patients with NAFLD and elevated liver enzymes Hepatology 44 2006 865 873 (Pubitemid 46489550)
8. G. Targher, and G. Arcaro Non-alcoholic fatty liver disease and increased risk of cardiovascular disease Atherosclerosis 191 2007 235 240 (Pubitemid 46400718)
9. G. Marchesini, M. Brizi, A.M. Morselli-Labate, G. Bianchi, E. Bugianesi, and A.J. McCullough Association of nonalcoholic fatty liver disease with insulin resistance Am J Med 107 1999 450 455 (Pubitemid 29528333)
10. S. Chitturi, S. Abeygunasekera, G.C. Farrell, J. Holmes-Walker, J.M. Hui, and C. Fung NASH and insulin resistance: Insulin hypersecretion and specific association with the insulin resistance syndrome Hepatology 35 2002 373 379 (Pubitemid 34106377)
11. D. Yunianingtias, and D. Volker Nutritional aspects of non-alcoholic steatohepatitis treatment Nutr Diet 63 2006 79 90
12. J.D. Browning, L.S. Szczepaniak, R. Dobbins, P. Nuremberg, J.D. Horton, and J.C. Cohen Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity Hepatology 40 2004 1387 1395 (Pubitemid 39657013)
13. P. Angulo Obesity and nonalcoholic fatty liver disease Nutr Rev 65 2007 S57 S63
14. F. Angelico, M. Del Ben, R. Conti, S. Francioso, K. Feole, and D. Maccioni Non-alcoholic fatty liver syndrome: a hepatic consequence of common metabolic diseases J Gastroenterol Hepatol 18 2003 588 594 (Pubitemid 36645294)
15. G. Pagano, G. Pacini, G. Musso, R. Gambino, F. Mecca, and N. Depetris Nonalcoholic steatohepatitis, insulin resistance, and metabolic syndrome: further evidence for an etiologic association Hepatology 35 2002 367 372 (Pubitemid 34106376)
16. J.E. Shaw, R.A. Sicree, and P.Z. Zimmet Global estimates of the prevalence of diabetes for 2010 and 2030 Diabetes Res Clin Pract 87 2010 4 14
17. Y. Ostchega, C.F. Dillon, J.P. Hughes, M. Carroll, and S. Yoon Trends in hypertension prevalence, awareness, treatment, and control in older US adults: data from the National Health and Nutrition Examination Survey 1988 to 2004 J Am Geriatr Soc 55 2007 1056 1065 (Pubitemid 47024610)
18. J.A. Cutler, P.D. Sorlie, M. Wolz, T. Thom, L.E. Fields, and E.J. Roccella Trends in hypertension prevalence, awareness, treatment, and control rates in United States adults between 1988-1994 and 1999-2004 Hypertension 52 2008 818 827
19. Y.S. Khader, A. Batieha, M. El-Khateeb, M. Al Omari, and K. Ajlouni Prevalence of dyslipidemia and its associated factors among Jordanian adults J Clin Lipidol 4 2010 53 58
20. T. Lobstein, L. Baur, and R. Uauy Obesity in children and young people: a crisis in public health Obes Rev 5 2004 4 85
21. B. Rokholm, J.L. Baker, and T.I.A. Sørensen The leveling off of the obesity epidemic since the year 1999 - a review of evidence and perspectives Obes Rev 11 2010 835 846
22. J. Dixon, P. Bhathal, and P. O'Brien Weight loss and non-alcoholic fatty liver disease: falls in gamma-glutamyl transferase concentrations are associated with histologic improvement Obes Surg 16 2006 1278 1286 (Pubitemid 44671797)
23. J.B. Dixon, P.S. Bhathal, N.R. Hughes, and P.E. O'Brien Nonalcoholic fatty liver disease: improvement in liver histological analysis with weight loss Hepatology 39 2004 1647 1654 (Pubitemid 38702666)
24. A.S. George, A. Bauman, A. Johnston, G. Farrell, T. Chey, and J. George Effect of a lifestyle intervention in patients with abnormal liver enzymes and metabolic risk factors J Gastroenterol Hepatol 24 2009 399 407
25. S.G. Mattar, L.M. Velcu, M. Rabinovitz, A.J. Demetris, A.M. Krasinskas, and E. Barinas-Mitchell Surgically-induced weight loss significantly improves nonalcoholic fatty liver disease and the metabolic syndrome Ann Surg 242 2005 610 620 (Pubitemid 41428657)
26. K. Promrat, D.E. Kleiner, H.M. Niemeier, E. Jackvony, M. Kearns, and J.R. Wands Randomized controlled trial testing the effects of weight loss on nonalcoholic steatohepatitis Hepatology 51 2010 121 129
27. S.A. Harrison, W. Fecht, E.M. Brunt, and B.A. Neuschwander-Tetri Orlistat for overweight subjects with nonalcoholic steatohepatitis: a randomized, prospective trial Hepatology 49 2009 80 86
28. AIHW. Australian hospital statistics 2009-10. Canberra: AIHW; 2011.
29. A.C.F. De Moraes, R.P. Fadoni, L.M. Ricardi, T.C. Souza, C.F. Rosaneli, and A.T.A. Nakashima Prevalence of abdominal obesity in adolescents: a systematic review Obes Rev 12 2010 69 77
30. AIHW. Australian hospital statistics 2006-07. Canberra: AIHW; 2008.
31. E.H. Livingston, and C.Y. Ko Socioeconomic characteristics of the population eligible for obesity surgery Surgery 135 2004 288 296 (Pubitemid 38297379)
32. G. Musso, R. Gambino, M. Cassader, and G. Pagano A meta-analysis of randomized trials for the treatment of nonalcoholic fatty liver disease Hepatology 52 2010 79 104
33. M.R. DiMatteo Variations in patients' adherence to medical recommendations: a quantitative review of 50 years of research Medical Care 42 2004 200 209
34. L. Osterberg, and T. Blaschke Adherence to medication N Engl J Med 353 2005 487 497 (Pubitemid 41127293)
35. S.E. Mahady, A.C. Webster, S. Walker, A. Sanyal, and J. George The role of thiazolidinediones in non-alcoholic steatohepatitis - a systematic review and meta analysis J Hepatol 2011 10.1016/j.jhep.2011.03.01
36. H. Cortez-Pinto, L. Jesus, H. Barros, C. Lopes, M.C. Moura, and M.E. Camilo How different is the dietary pattern in non-alcoholic steatohepatitis patients? Clin Nutr 25 2006 816 823 (Pubitemid 44426431)
37. L. Vilar, C.P.M.S. Oliveira, J. Faintuch, E.S. Mello, M.A. Nogueira, and T.E. Santos High-fat diet: a trigger of non-alcoholic steatohepatitis? Preliminary findings in obese subjects Nutrition 24 2008 1097 1102
38. G. Musso, R. Gambino, F. De Michieli, M. Cassader, M. Rizzetto, and M. Durazzo Dietary habits and their relations to insulin resistance and postprandial lipemia in nonalcoholic steatohepatitis Hepatology 37 2003 909 916 (Pubitemid 36397404)
39. L.C. Hudgins, M. Hellerstein, C. Seidman, R. Neese, J. Diakun, and J. Hirsch Human fatty acid synthesis is stimulated by a eucaloric low fat, high carbohydrate diet J Clin Invest 97 1996 2081 2091 (Pubitemid 26143963)
40. S. Solga, A.R. Alkhuraishe, J.M. Clark, M. Torbenson, A. Greenwald, and A.M. Diehl Dietary composition and nonalcoholic fatty liver disease Dig Dis Sci 49 2004 1578 1583 (Pubitemid 39335538)
41. S. Zelber-Sagi, D. Nitzan-Kaluski, R. Goldsmith, M. Webb, L. Blendis, and Z. Halpern Long term nutritional intake and the risk for non-alcoholic fatty liver disease (NAFLD): a population based study J Hepatol 47 2007 711 717 (Pubitemid 47503432)
42. J. Araya, R. Rodrigo, L.A. Videla, L. Thielemann, M. Orellana, and P. Pettinelli Increase in long-chain polyunsaturated fatty acid n-6/n-3 ratio in relation to hepatic steatosis in patients with non-alcoholic fatty liver disease Clin Sci 106 2004 635 643 (Pubitemid 38797577)
43. A. Elizondo, J. Araya, R. Rodrigo, J. Poniachik, A. Csendes, and F. Maluenda Polyunsaturated fatty acid pattern in liver and erythrocyte phospholipids from obese patients Obesity 15 2007 24 31 (Pubitemid 46219780)
44. M. Sekiya, N. Yahagi, T. Matsuzaka, Y. Najima, M. Nakakuki, and R. Nagai Polyunsaturated fatty acids ameliorate hepatic steatosis in obese mice by SREBP-1 suppression Hepatology 38 2003 1529 1539 (Pubitemid 37466979)
45. M. Capanni, F. Calella, M.R. Biagini, S. Genise, L. Raimondi, and G. Bedogni Prolonged n-3 polyunsaturated fatty acid supplementation ameliorates hepatic steatosis in patients with non-alcoholic fatty liver disease: a pilot study Aliment Pharmacol Ther 23 2006 1143 1151 (Pubitemid 43779354)
46. A. Hatzitolios, C. Savopoulos, G. Lazaraki, I. Sidiropoulos, P. Haritanti, and A. Lefkopoulos Efficacy of omega-3 fatty acids, atorvastatin and orlistat in non-alcoholic fatty liver disease with dyslipidemia Indian J Gastroenterol 23 2004 131 134 (Pubitemid 39145721)
47. N. Tanaka, K. Sano, A. Horiuchi, E. Tanaka, K. Kiyosawa, and T. Aoyama Highly purified eicosapentaenoic acid treatment improves nonalcoholic steatohepatitis J Clin Gastroenterol 42 2008 413 418 (Pubitemid 351450629)
48. F.S. Zhu, S. Liu, X.M. Chen, Z.G. Huang, and D.W. Zhang Effects of n-3 polyunsaturated fatty acids from seal oils on nonalcoholic fatty liver disease associated with hyperlipidemia World J Gastroenterol: WJG 14 2008 6395 6400
49. J. Xu, H. Cho, S. O'Malley, J.H.Y. Park, and S.D. Clarke Dietary polyunsaturated fats regulate rat liver sterol regulatory element binding proteins-1 and -2 in three distinct stages and by different mechanisms J Nutr 132 2002 3333 3339 (Pubitemid 35304240)
50. Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 2005;5. article number 13.
51. S.H. Downs, and N. Black The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions J Epidemiol Community Health 52 1998 377 384 (Pubitemid 28438523)
52. J.E. Nelson, B.D. Maliken, C. Saunders, J. Stevenson, T. Richards, and K.V. Kowdley A randomized, masked, controlled study of omega-3 polyunsaturated fatty acid vs. monounsaturated fatty acid diet supplementation for the treatment of nonalcoholic fatty liver disease Gastroenterology 136 2009 A847 A848
53. F. Sofi, I. Giangrandi, F. Cesari, I. Corsani, R. Abbate, and G.F. Gensini Effects of a 1-year dietary intervention with n-3 polyunsaturated fatty acid-enriched olive oil on non-alcoholic fatty liver disease patients: a preliminary study Int J Food Sci Nutr 61 2010 792 802
54. L. Spadaro, O. Magliocco, D. Spampinato, S. Piro, C. Oliveri, and C. Alagona Effects of n-3 polyunsaturated fatty acids in subjects with nonalcoholic fatty liver disease Digest Liver Dis 40 2008 194 199 (Pubitemid 351181793)
55. R. Chen, Q. Guo, W.J. Zhu, Q. Xie, H. Wang, and W. Cai Therapeutic efficacy of (omega)-3 polyunsaturated fatty acid capsule in treatment of patients with non-alcoholic fatty liver disease World Chin J Digestol 16 2008 2002 2006
56. A.J. Cussons, G.F. Watts, T.A. Mori, and B.G.A. Stuckey Omega-3 fatty acid supplementation decreases liver fat content in polycystic ovary syndrome: a randomized controlled trial employing proton magnetic resonance spectroscopy J Clin Endocrinol Metab 94 2009 3842 3848
57. G.L. Vega, M. Chandalia, L.S. Szczepaniak, and S.M. Grundy Effects of N-3 fatty acids on hepatic triglyceride content in humans J Investig Med 56 2008 780 785
58. J. Hartweg, A.J. Farmer, R.R. Holman, and A. Neil Potential impact of omega-3 treatment on cardiovascular disease in type 2 diabetes Curr Opin Lipidol 20 2009 30 38
59. C.E. Friedberg, M. Janssen, R.J. Heine, and D.E. Grobbee Fish oil and glycemic control in diabetes - a meta-analysis Diabetes Care 21 1998 494 500 (Pubitemid 28172922)
60. E.M. Balk, A.H. Lichtenstein, M. Chung, B. Kupelnick, P. Chew, and J. Lau Effects of omega-3 fatty acids on serum markers of cardiovascular disease risk: a systematic review Atherosclerosis 189 2006 19 30 (Pubitemid 44468073)
61. M.C. Morris, F. Sacks, and B. Rosner Does fish oil lower blood pressure? A meta-analysis of controlled trials Circulation 88 1993 523 533 (Pubitemid 23228051)
62. N.A. Johnson, T. Sachinwalla, D.W. Walton, K. Smith, A. Armstrong, and M.W. Thompson Aerobic exercise training reduces hepatic and visceral lipids in obese individuals without weight loss Hepatology 50 2009 1105 1112
63. K. Toshimitsu, B. Matsuura, I. Ohkubo, T. Niiya, S. Furukawa, and Y. Hiasa Dietary habits and nutrient intake in non-alcoholic steatohepatitis Nutrition 23 2007 46 52 (Pubitemid 44959764)
64. Leclercq IA, Molendi-Coste O, Legry V. Why and how meet n-3 PUFA dietary recommendations? Gastroenterol Res Pract 2011. article number 364040.
65. N. Kalogeropoulos, D.B. Panagiotakos, C. Pitsavos, C. Chrysohoou, G. Rousinou, and M. Toutouza Unsaturated fatty acids are inversely associated and n-6/n-3 ratios are positively related to inflammation and coagulation markers in plasma of apparently healthy adults Clin Chim Acta 411 2010 584 591
66. R. Wall, R.P. Ross, G.F. Fitzgerald, and C. Stanton Fatty acids from fish: the anti-inflammatory potential of long-chain omega-3 fatty acids Nutr Rev 68 2010 280 289
67. A.M. Zivkovic, J.B. German, and A.J. Sanyal Comparative review of diets for the metabolic syndrome: implications for nonalcoholic fatty liver disease Am J Clin Nutr 86 2007 285 300 (Pubitemid 47256910)
68. G. D'Assignies, C. Kauffmann, Y. Boulanger, M. Bilodeau, V. Vilgrain, and G. Soulez Simultaneous assessment of liver volume and whole liver fat content: a step towards one-stop shop preoperative MRI protocol Eur Radiol 21 2011 301 309
69. S. Meisamy, C.D.G. Hines, G. Hamilton, C.B. Sirlin, C.A. McKenzie, and H. Yu Quantification of hepatic steatosis with T1-independent, T2-corrected MR imaging with spectral modeling of fat: blinded comparison with MR spectroscopy Radiology 258 2011 767 775