Background/Aims: The relationship between diet and non-alcoholic fatty liver disease (NAFLD) in patients with gallstone disease and in those who have a high risk for NAFLD has not been investigated. This study was conducted to investigate the association between the risk of NAFLD and dietary pattern in patients who underwent cholecystectomy. Additionally, we assessed the association between erythrocyte fatty acid composition, a marker for diet, and the risk of NAFLD. Methods: Patients (n = 139) underwent liver ultrasonography to determine the presence of NAFLD before laparoscopic cholecystectomy, reported dietary intake using food frequency questionnaire, and were assessed for blood fatty acid composition. Results: Fifty-eight patients were diagnosed with NAFLD. The risk of NAFLD was negatively associated with 2 dietary patterns: consuming whole grain and legumes and consuming fish, vegetables, and fruit. NAFLD was positively associated with the consumption of refined grain, meat, processed meat, and fried foods. Additionally, the risk of NAFLD was positively associated with erythrocyte levels of 16:0 and 18:2t, while it was negatively associated with 20:5n3, 22:5n3, and Omega-3 Index. Conclusion: The risk of NAFLD was negatively associated with a healthy dietary pattern of consuming whole grains, legumes, vegetables, fish, and fruit and with an erythrocyte level of n-3 polyunsaturated fatty acids rich in fish.

Keywords:
Dietary pattern, n-3 polyunsaturated fatty acid, Non-alcoholic fatty liver disease, Patient with cholecystectomy
1.
Smith BW, Adams LA: Non-alcoholic fatty liver disease. Crit Rev Clin Lab Sci 2011;48:97-113.
2.
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. Hepatology 2016;64:73-84.
3.
Jeong EH, Jun DW, Cho YK, Choe YG, Ryu S, Lee SM, Jang EC: Regional prevalence of non-alcoholic fatty liver disease in seoul and gyeonggi-do, Korea. Clin Mol Hepatol 2013;19:266-272.
4.
Adriano LS, Sampaio HA, Arruda SP, Portela CL, Melo ML, Carioca AA, Soares NT: Healthy dietary pattern is inversely associated with non-alcoholic fatty liver disease in elderly. Br J Nutr 2016;115:2189-2195.
5.
Aller R, Izaola O, de la Fuente B, De Luis Roman DA: Mediterranean diet Is associated with liver histology in patients with non alcoholic fatty liver disease. Nutr Hosp 2015;32:2518-2524.
6.
Kontogianni MD, Tileli N, Margariti A, Georgoulis M, Deutsch M, Tiniakos D, Fragopoulou E, Zafiropoulou R, Manios Y, Papatheodoridis G: Adherence to the Mediterranean diet is associated with the severity of non-alcoholic fatty liver disease. Clin Nutr 2014;33:678-683.
7.
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.
8.
Musso G, Gambino R, De Michieli F, Cassader M, Rizzetto M, Durazzo M, Faga E, Silli B, Pagano G: Dietary habits and their relations to insulin resistance and postprandial lipemia in nonalcoholic steatohepatitis. Hepatology 2003;37:909-916.
9.
Ouyang X, Cirillo P, Sautin Y, McCall S, Bruchette JL, Diehl AM, Johnson RJ, Abdelmalek MF: Fructose consumption as a risk factor for non-alcoholic fatty liver disease. J Hepatol 2008;48:993-999.
10.
Georgoulis M, Kontogianni MD, Margariti A, Tiniakos D, Fragopoulou E, Zafiropoulou R, Papatheodoridis G: Associations between dietary intake and the presence of the metabolic syndrome in patients with non-alcoholic fatty liver disease. J Hum Nutr Diet 2015;28:409-415.
11.
Han JM, Jo AN, Lee SM, Bae HS, Jun DW, Cho YK, Suk KT, Yoon JH, Ahn SB, Cho YJ, Kim SW, Jang EC: Associations between intakes of individual nutrients or whole food groups and non-alcoholic fatty liver disease among Korean adults. J Gastroenterol Hepatol 2014;29:1265-1272.
12.
Elizondo A, Araya J, Rodrigo R, Poniachik J, Csendes A, Maluenda F, Diaz JC, Signorini C, Sgherri C, Comporti M, Videla LA: Polyunsaturated fatty acid pattern in liver and erythrocyte phospholipids from obese patients. Obesity (Silver Spring) 2007;15:24-31.
13.
Chen LH, Wang YF, Xu QH, Chen SS: Omega-3 fatty acids as a treatment for non-alcoholic fatty liver disease in children: a systematic review and meta-analysis of randomized controlled trials. Clin Nutr 2016;pii:S0261-5614(16)31350-4.
14.
He XX, Wu XL, Chen RP, Chen C, Liu XG, Wu BJ, Huang ZM: Effectiveness of omega-3 polyunsaturated fatty acids in non-alcoholic fatty liver disease: a meta-analysis of randomized controlled trials. PLoS One 2016;11:e0162368.
15.
Lu W, Li S, Li J, Wang J, Zhang R, Zhou Y, Yin Q, Zheng Y, Wang F, Xia Y, Chen K, Liu T, Lu J, Zhou Y, Guo C: Effects of omega-3 fatty acid in nonalcoholic fatty liver disease: a meta-analysis. Gastroenterol Res Pract 2016;2016:1459790.
16.
Ahmed MH, Ali A: Nonalcoholic fatty liver disease and cholesterol gallstones: which comes first? Scand J Gastroenterol 2014;49:521-527.
17.
Ruhl CE, Everhart JE: Relationship of non-alcoholic fatty liver disease with cholecystectomy in the US population. Am J Gastroenterol 2013;108:952-958.
18.
Jessri M, Rashidkhani B: Dietary patterns and risk of gallbladder disease: a hospital-based case-control study in adult women. J Health Popul Nutr 2015;33:39-49.
19.
Misciagna G, Leoci C, Guerra V, Chiloiro M, Elba S, Petruzzi J, Mossa A, Noviello MR, Coviello A, Minutolo MC, Mangini V, Messa C, Cavallini A, De Michele G, Giorgio I: Epidemiology of cholelithiasis in southern Italy. Part II: risk factors. Eur J Gastroenterol Hepatol 1996;8:585-593.
20.
Kameda H, Ishihara F, Shibata K, Tsukie E: Clinical and nutritional study on gallstone disease in Japan. Jpn J Med 1984;23:109-113.
21.
Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, Charlton M, Sanyal AJ: 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;142:1592-1609.
22.
Harris W, von Schacky C, Park Y: Standardizing methods for assessing omega-3 fatty acid biostatus; in McNamara RK (ed): The Omega-3 Fatty Acid Deficiency Syndrome: Opportunities for Disease Prevention. Hauppauge, Nova Science Publishers, Inc., 2013, pp 385-398.
23.
Ministry of Health and Welfare. Korea National Health and Nutrition Examination Survey. 2011. http://knhanes.cdc.go.kr/.
24.
Yang CQ, Shu L, Wang S, Wang JJ, Zhou Y, Xuan YJ, Wang SF: Dietary patterns modulate the risk of non-alcoholic fatty liver disease in Chinese adults. Nutrients 2015;7:4778-4791.
25.
Chan R, Wong VW, Chu WC, Wong GL, Li LS, Leung J, Chim AM, Yeung DK, Sea MM, Woo J, Chan FK, Chan HL: Diet-quality scores and prevalence of nonalcoholic fatty liver disease: a population study using proton-magnetic resonance spectroscopy. PLoS One 2015;10:e0139310.
26.
Georgoulis M, Kontogianni MD, Tileli N, Margariti A, Fragopoulou E, Tiniakos D, Zafiropoulou R, Papatheodoridis G: The impact of cereal grain consumption on the development and severity of non-alcoholic fatty liver disease. Eur J Nutr 2014;53:1727-1735.
27.
Mohajeri D, Monadi A: Effects of tomato pulp on hepatic steatosis in the rats fed with high fat diet. Bratisl Lek Listy 2015;116:689-694.
28.
Ozturk F, Gul M, Ates B, Ozturk IC, Cetin A, Vardi N, Otlu A, Yilmaz I: Protective effect of apricot (Prunus armeniaca L.) on hepatic steatosis and damage induced by carbon tetrachloride in Wistar rats. Br J Nutr 2009;102:1767-1775.
29.
Peng CH, Chang HC, Yang MY, Huang CN, Wang SJ, Wang CJ: Oat attenuate non-alcoholic fatty liver and obesity via inhibiting lipogenesis in high fat-fed rat. J Funct Foods 2013;5:53-61.
30.
Baybutt RC, Molteni A: Dietary beta-carotene protects lung and liver parenchyma of rats treated with monocrotaline. Toxicology 1999;137:69-80.
31.
Jung JH, Kim HS: The inhibitory effect of black soybean on hepatic cholesterol accumulation in high cholesterol and high fat diet-induced non-alcoholic fatty liver disease. Food Chem Toxicol 2013;60:404-412.
32.
Papandreou D, Karabouta Z, Pantoleon A, Rousso I: Investigation of anthropometric, biochemical and dietary parameters of obese children with and without non-alcoholic fatty liver disease. Appetite 2012;59:939-944.
33.
Araya J, Rodrigo R, Videla LA, Thielemann L, Orellana M, Pettinelli P, Poniachik J: 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 (Lond) 2004;106:635-643.
34.
Kim S, Jin Y, Park Y: Estrogen and n-3 polyunsaturated fatty acid supplementation have a synergistic hypotriglyceridemic effect in ovariectomized rats. Genes Nutr 2015;10:475.
35.
Suzuki-Kemuriyama N, Matsuzaka T, Kuba M, Ohno H, Han SI, Takeuchi Y, Isaka M, Kobayashi K, Iwasaki H, Yatoh S, Suzuki H, Miyajima K, Nakae D, Yahagi N, Nakagawa Y, Sone H, Yamada N, Shimano H: Different effects of eicosapentaenoic and docosahexaenoic acids on atherogenic high-fat diet-induced non-alcoholic fatty Liver disease in mice. PLoS One 2016;11:e0157580.
36.
Oddy WH, Herbison CE, Jacoby P, Ambrosini GL, O'Sullivan TA, Ayonrinde OT, Olynyk JK, Black LJ, Beilin LJ, Mori TA, Hands BP, Adams LA: The western dietary pattern is prospectively associated with nonalcoholic fatty liver disease in adolescence. Am J Gastroenterol 2013;108:778-785.
37.
Singh SP, Singh A, Misra D, Misra B, Pati GK, Panigrahi MK, Kar SK, Bhuyan P, Pattnaik K, Meher C, Agrawal O, Rout N, Swain M, Aich P: Risk factors associated with non-alcoholic fatty liver disease in Indians: a case-control study. J Clin Exp Hepatol 2015;5:295-302.
38.
de Meijer VE, Le HD, Meisel JA, Akhavan Sharif MR, Pan A, Nose V, Puder M: Dietary fat intake promotes the development of hepatic steatosis independently from excess caloric consumption in a murine model. Metabolism 2010;59:1092-1105.
39.
Obara N, Fukushima K, Ueno Y, Wakui Y, Kimura O, Tamai K, Kakazu E, Inoue J, Kondo Y, Ogawa N, Sato K, Tsuduki T, Ishida K, Shimosegawa T: Possible involvement and the mechanisms of excess trans-fatty acid consumption in severe NAFLD in mice. J Hepatol 2010;53:326-334.
40.
Scribner KB, Pawlak DB, Ludwig DS: Hepatic steatosis and increased adiposity in mice consuming rapidly vs. slowly absorbed carbohydrate. Obesity (Silver Spring) 2007;15:2190-2199.
41.
Choi SH, Oh DJ, Kwon KH, Lee JK, Koh MS, Lee JH, Kang HW: A vegetarian diet does not protect against nonalcoholic fatty liver disease (NAFLD): a cross-sectional study between Buddhist priests and the general population. Turk J Gastroenterol 2015;26:336-343.
42.
Song SH, Kwon CI, Jin SM, Park HJ, Chung CW, Kwon SW, Ko KH, Hong SP: Clinical characteristics of acute cholecystitis with elevated liver enzymes not associated with choledocholithiasis. Eur J Gastroenterol Hepatol 2014;26:452-457.
43.
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.
© 2017 S. Karger AG, Basel
2017
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.