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Open Access 01-12-2022 | Obesity | Research

Healthy dietary patterns and metabolic dysfunction-associated fatty liver disease in less-developed ethnic minority regions: a large cross-sectional study

Authors: Xiaofen Xie, Bing Guo, Xiong Xiao, Jianzhong Yin, Ziyun Wang, Xiaoman Jiang, Jingzhong Li, Lu Long, Junmin Zhou, Ning Zhang, Yuan Zhang, Ting Chen, Baima Kangzhuo, Xing Zhao

Published in: BMC Public Health | Issue 1/2022

Abstract

Background

Little is known about the associations between healthy dietary patterns and metabolic dysfunction-associated fatty liver disease (MAFLD) in less-developed ethnic minority regions (LEMRs), where the prevalence of MAFLD is increasing rapidly and dietary habits are quite different from those in developed countries. Moreover, a significant subset of MAFLD individuals in LEMRs are nonobese, but the efficacy of dietary patterns on MAFLD individuals with different obese statuses is also unclear. We aimed to test the associations of two wildly recommended a priori dietary patterns—Alternate Mediterranean diet (AMED) and Dietary Approaches to Stop Hypertension (DASH)—with the risk of MAFLD in the total population, and further in nonobese and obese individuals.

Methods

We recruited 99,556 participants in the China Multi-Ethnic Cohort Study, an ongoing cohort study in less-developed southwest China. Using validated food frequency questionnaire, each participant was assigned an AMED score and a DASH score. MAFLD was ascertained as hepatic steatosis on ultrasound together with diabetes, overweight/obesity, or two other metabolic risk factors. We performed logistic regression with inverse probability of exposure weighting (IPEW) to examine associations between two dietary patterns and MAFLD, adjusting for potential confounders under the guidance of directed acyclic graphs. Further, analyses were stratified by body mass index.

Results

We included 66,526 participants (age 49.5±11.0; 62.6% women), and the prevalence of MAFLD was 16.1%. Participants in the highest quintile of DASH score showed strong inverse associations with risks of MAFLD (OR = 0.85; 95% CI, 0.80-0.91; P_trend < 0.001) compared with participants in the lowest quintile. The association between DASH and nonobese MAFLD (OR = 0.69; 95% CI, 0.61-0.78; P_trend < 0.001) was stronger (I² = 78.5 % ; P_{heterogeneity} = 0.001) than that with obese MAFLD (OR = 0.90; 95% CI, 0.83-0.98; P_trend = 0.002). There was a null association between AMED and MAFLD risk.

Conclusions

In LEMRs, a DASH diet but not AMED was associated with MAFLD. The relationship appeared to be more pronounced in nonobese MAFLD individuals than in obese MAFLD individuals.

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Younossi ZM, Koenig AB, Abdelatif D, et al. Global epidemiology of nonalcoholic fatty liver disease-Meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology. 2016;64(1):73–84. https://doi.org/10.1002/hep.28431 [published Online First: 29 Dec 2015].CrossRefPubMed

Anstee QM, Targher G, Day CP. Progression of NAFLD to diabetes mellitus, cardiovascular disease or cirrhosis. Nat Rev Gastroenterol Hepatol. 2013;10(6):330–44. https://doi.org/10.1038/nrgastro.2013.41 [published Online First: 20 Mar 2013].CrossRefPubMed

Eslam M, Sanyal AJ, George J, et al. MAFLD: a consensus-driven proposed nomenclature for metabolic associated fatty liver disease. Gastroenterology. 2020;158(7):1999–2014.e1. https://doi.org/10.1053/j.gastro.2019.11.312 [published Online First: 12 Feb 2020].CrossRef

Eslam M, Newsome PN, Sarin SK, et al. A new definition for metabolic dysfunction-associated fatty liver disease: An international expert consensus statement. J Hepatol. 2020;73(1):202–9. https://doi.org/10.1016/j.jhep.2020.03.039 [published Online First: 12 Mar 2020].CrossRefPubMed

Younossi Z, Tacke F, Arrese M, et al. Global perspectives on nonalcoholic fatty liver disease and nonalcoholic steatohepatitis. Hepatology. 2019;69(6):2672–82. https://doi.org/10.1002/hep.30251 [published Online First: 05 Sep 2018].CrossRefPubMed

Agbim U, Carr RM, Pickett-Blakely O, et al. Ethnic disparities in adiposity: focus on non-alcoholic fatty liver disease, visceral, and generalized obesity. Curr Obes Rep. 2019;8(3):243–54. https://doi.org/10.1007/s13679-019-00349-x.CrossRefPubMedPubMedCentral

Dong B, Arnold LW, Peng Y, et al. Ethnic differences in cardiometabolic risk among adolescents across the waist–height ratio spectrum: National Health and Nutrition Examination Surveys (NHANES). Int J Cardiol. 2016;222:622–8. https://doi.org/10.1016/j.ijcard.2016.07.169.CrossRefPubMed

Zhou F, Zhou J, Wang W, et al. Unexpected rapid increase in the burden of NAFLD in China from 2008 to 2018: a systematic review and meta-analysis. Hepatology. 2019;70(4):1119–33. https://doi.org/10.1002/hep.30702 [published Online First: 10 May 2019].CrossRefPubMed

Wang XJ, Malhi H. Nonalcoholic fatty liver disease. Ann Intern Med. 2018;169(9):ITC65–80. https://doi.org/10.7326/AITC201811060 [published Online First: 07 Nov 2018].CrossRefPubMed

10.

Alferink LJ, Kiefte-de Jong JC, Erler NS, et al. Association of dietary macronutrient composition and non-alcoholic fatty liver disease in an ageing population: the Rotterdam Study. Gut. 2019;68(6):1088–98. https://doi.org/10.1136/gutjnl-2017-315940 [published Online First: 02 Aug 2018].CrossRefPubMed

11.

Zelber-Sagi S, Ivancovsky-Wajcman D, Fliss Isakov N, et al. High red and processed meat consumption is associated with non-alcoholic fatty liver disease and insulin resistance. J Hepatol. 2018;68(6):1239–46. https://doi.org/10.1016/j.jhep.2018.01.015 [published Online First: 25 Mar 2018].CrossRefPubMed

12.

Cespedes EM, Hu FB. Dietary patterns: from nutritional epidemiologic analysis to national guidelines. The Am J Clin Nutr. 2015;101(5):899–900. https://doi.org/10.3945/ajcn.115.110213.CrossRefPubMed

13.

European Association for the Study of the L, European Association for the Study of D, European Association for the Study of O. EASL-EASD-EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease. J Hepatol. 2016;64(6):1388–402. https://doi.org/10.1016/j.jhep.2015.11.004 [published Online First: 12 Apr 2016].CrossRef

14.

Hydes TJ, Ravi S, Loomba R, et al. Evidence-based clinical advice for nutrition and dietary weight loss strategies for the management of NAFLD and NASH. Clin Mol Hepatol. 2020;26(4):383–400. https://doi.org/10.3350/cmh.2020.0067 [published Online First: 18 July 2020].CrossRefPubMedPubMedCentral

15.

Kim D, Kim WR. Nonobese fatty liver disease. Clin Gastroenterol Hepatol. 2017;15(4):474–85. https://doi.org/10.1016/j.cgh.2016.08.028 [published Online First: 02 Sep 2016].CrossRefPubMed

16.

Younossi ZM, Stepanova M, Negro F, et al. Nonalcoholic fatty liver disease in lean individuals in the United States. Medicine. 2012;91(6):319–27. https://doi.org/10.1097/MD.0b013e3182779d49 [published Online First: 03 Nov 2012].CrossRefPubMed

17.

Hagstrom H, Nasr P, Ekstedt M, et al. Risk for development of severe liver disease in lean patients with nonalcoholic fatty liver disease: A long-term follow-up study. Hepatol Commun. 2018;2(1):48–57. https://doi.org/10.1002/hep4.1124 [published Online First: 07 Feb 2018].CrossRefPubMed

18.

Cruz ACD, Bugianesi E, George J, et al. 379 Characteristics and long-term prognosis of lean patients with nonalcoholic fatty liver disease. Gastroenterology. 2014;146(5):S-909. https://doi.org/10.1016/s0016-5085(14)63307-2.

19.

Zhao X, Hong F, Yin J, et al. Cohort profile: the China Multi-Ethnic cohort (CMEC) study. Int J Epidemiol. 2020. https://doi.org/10.1093/ije/dyaa185 [published Online First: 25 Nov 2020].

20.

National Institute for Nurtition and Health. China food composition tables. 6th ed. Beijing: Peking University Medical Press; 2018.

21.

National Health Commission of the People’s Republic of China. Dietary guide for adult diabetes patients (WS/T 429-2013), 2013.

22.

Xiao X, Qin Z, Lv X, et al. Dietary patterns and cardiometabolic risks in diverse less-developed ethnic minority regions: results from the China Multi-Ethnic Cohort (CMEC) Study. Lancet Reg Health West Pac. 2021;15:100252. https://doi.org/10.1016/j.lanwpc.2021.100252.CrossRefPubMedPubMedCentral

23.

Trichopoulou A, Costacou T, Bamia C, et al. Adherence to a Mediterranean diet and survival in a Greek population. N Engl J Med. 2003;348(26):2599–608.CrossRef

24.

Fung TT, McCullough ML, Newby PK, et al. Diet-quality scores and plasma concentrations of markers of inflammation and endothelial dysfunction. Am J Clinical nutrition. 2005;82(1):163–73.CrossRef

25.

Shan Z, Li Y, Baden MY, et al. Association between healthy eating patterns and risk of cardiovascular disease. JAMA Intern Med. 2020;180(8):1090–100. https://doi.org/10.1001/jamainternmed.2020.2176 [published Online First: 17 Jun 2020].CrossRefPubMed

26.

Chiu S, Bergeron N, Williams PT, et al. Comparison of the DASH (Dietary Approaches to Stop Hypertension) diet and a higher-fat DASH diet on blood pressure and lipids and lipoproteins: a randomized controlled trial. Am J Clin Nutr. 2016;103(2):341–7. https://doi.org/10.3945/ajcn.115.123281 [published Online First: 01 Jan 2016].CrossRefPubMed

27.

Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. The Lancet 2004;363(9403):157-163. doi: https://doi.org/10.1016/s0140-6736(03)15268-3

28.

Ferguson KD, McCann M, Katikireddi SV, et al. Evidence synthesis for constructing directed acyclic graphs (ESC-DAGs): a novel and systematic method for building directed acyclic graphs. Int J Epidemiol. 2020;49(1):322–9. https://doi.org/10.1093/ije/dyz150 [published Online First: 22 July 2019].CrossRefPubMed

29.

Trichopoulou A, Bamia C, Trichopoulos D. Anatomy of health effects of Mediterranean diet: Greek EPIC prospective cohort study. BMJ. 2009;338:b2337. https://doi.org/10.1136/bmj.b2337 [published Online First: 25 Jun 2009].CrossRefPubMedPubMedCentral

30.

van Buuren S, Groothuis-Oudshoorn K. mice: Multivariate Imputation by chained equations in R. J Stat Softw. 2011;45(3):1–67. https://doi.org/10.18637/jss.v045.i03 [published Online First: 12 Dec 2011].CrossRef

31.

Chen C, Lu FC. The guidelines for prevention and control of overweight and obesity in Chinese adults. Biomed Environ Sci. 2004;17(Suppl):1–36.

32.

Eslam M, Alkhouri N, Vajro P, et al. Defining paediatric metabolic (dysfunction)-associated fatty liver disease: an international expert consensus statement. Lancet Gastroenterol Hepatol. 2021;6(10):864–73. https://doi.org/10.1016/S2468-1253(21)00183-7.CrossRefPubMed

33.

Nan Y, An J, Bao J, et al. The Chinese Society of Hepatology position statement on the redefinition of fatty liver disease. J Hepatol. 2021;75(2):454–61. https://doi.org/10.1016/j.jhep.2021.05.003.CrossRefPubMed

34.

Mendez-Sanchez N, Arrese M, Gadano A, et al. The Latin American Association for the Study of the Liver (ALEH) position statement on the redefinition of fatty liver disease. Lancet Gastroenterol Hepatol. 2021;6(1):65–72. https://doi.org/10.1016/S2468-1253(20)30340-X.CrossRefPubMed

35.

Shiha G, Alswat K, Al Khatry M, et al. Nomenclature and definition of metabolic-associated fatty liver disease: a consensus from the Middle East and north Africa. Lancet Gastroenterol Hepatol. 2020. https://doi.org/10.1016/s2468-1253(20)30213-2.

36.

van Kleef L, Ayada I, Alferink L, et al. Metabolic dysfunction associated fatty liver disease improves detection of high liver stiffness: The rotterdam study. Hepatology (Baltimore, Md). 2021. https://doi.org/10.1002/hep.32131.

37.

Yamamura S, Eslam M, Kawaguchi T, et al. MAFLD identifies patients with significant hepatic fibrosis better than NAFLD. Liver Int. 2020;40(12):3018–30. https://doi.org/10.1111/liv.14675.CrossRefPubMed

38.

Lin S, Huang J, Wang M, et al. Comparison of MAFLD and NAFLD diagnostic criteria in real world. Liver Int. 2020;40(9):2082–9. https://doi.org/10.1111/liv.14548.CrossRefPubMed

39.

Zhang S, Gu Y, Bian S, et al. Dietary patterns and risk of non-alcoholic fatty liver disease in adults: a prospective cohort study. Clin Nutr. 2021;40(10):5373–82. https://doi.org/10.1016/j.clnu.2021.08.021 [published Online First: 25 Sep 2021].CrossRefPubMed

40.

Xia Y, Zhang Q, Liu L, et al. Intermediary effect of inflammation on the association between dietary patterns and non-alcoholic fatty liver disease. Nutrition. 2020;71:110562. https://doi.org/10.1016/j.nut.2019.110562 [published Online First: 2019 07 Dec].CrossRefPubMed

41.

Yang CQ, Shu L, Wang S, et al. Dietary patterns modulate the risk of non-alcoholic fatty liver disease in Chinese adults. Nutrients. 2015;7(6):4778–91. https://doi.org/10.3390/nu7064778 [published Online First: 2015 18 Jun].CrossRefPubMedPubMedCentral

42.

Liu X, Peng Y, Chen S, et al. An observational study on the association between major dietary patterns and non-alcoholic fatty liver disease in Chinese adolescents. Medicine (Baltimore). 2018;97(17):e0576. https://doi.org/10.1097/MD.0000000000010576 [published Online First: 2018 29 Apr].CrossRef

43.

Chan R, Wong VW, Chu WC, et al. Diet-quality scores and prevalence of nonalcoholic fatty liver disease: a population study using proton-magnetic resonance spectroscopy. PLoS One. 2015;10(9):e0139310. https://doi.org/10.1371/journal.pone.0139310 [published Online First: 30 Sep 2015].CrossRefPubMedPubMedCentral

44.

Razavi Zade M, Telkabadi MH, Bahmani F, et al. The effects of DASH diet on weight loss and metabolic status in adults with non-alcoholic fatty liver disease: a randomized clinical trial. Liver Int. 2016;36(4):563–71. https://doi.org/10.1111/liv.12990 [published Online First: 28 Oct 2015].CrossRefPubMed

45.

Xiao ML, Lin JS, Li YH, et al. Adherence to the Dietary Approaches to Stop Hypertension (DASH) diet is associated with lower presence of non-alcoholic fatty liver disease in middle-aged and elderly adults. Public Health Nutr. 2020;23(4):674–82. https://doi.org/10.1017/S1368980019002568 [published Online First: 01 Oct 2019].CrossRefPubMed

46.

Dehghan M, Mente A, Rangarajan S, et al. Association of dairy intake with cardiovascular disease and mortality in 21 countries from five continents (PURE): a prospective cohort study. The Lancet. 2018;392(10161):2288–97. https://doi.org/10.1016/S0140-6736(18)31812-9.CrossRef

47.

Zong G, Sun Q, Yu D, et al. Dairy consumption, type 2 diabetes, and changes in cardiometabolic traits: a prospective cohort study of middle-aged and older Chinese in Beijing and Shanghai. Diabetes Care. 2014;37(1):56–63. https://doi.org/10.2337/dc13-0975.CrossRefPubMed

48.

Rice BH, Cifelli CJ, Pikosky MA, et al. Dairy components and risk factors for cardiometabolic syndrome: recent evidence and opportunities for future research. Adv Nutr. 2011;2(5):396–407. https://doi.org/10.3945/an.111.000646 [published Online First: 15 Feb 2012].CrossRefPubMedPubMedCentral

49.

Mena-Sanchez G, Becerra-Tomas N, Babio N, et al. Dairy product consumption in the prevention of metabolic syndrome: a systematic review and meta-analysis of prospective cohort studies. Adv Nutr. 2019;10(suppl_2):S144–S53. https://doi.org/10.1093/advances/nmy083 [published Online First: 16 May 2019].CrossRefPubMedPubMedCentral

50.

Lorenzen JK, Nielsen S, Holst JJ, et al. Effect of dairy calcium or supplementary calcium intake on postprandial fat metabolism, appetite, and subsequent energy intake. Am J Clin Nutr. 2007;85(3):678–87.CrossRef

51.

Shen X, Jin C, Wu Y, et al. Prospective study of perceived dietary salt intake and the risk of non-alcoholic fatty liver disease. J Hum Nutr Diet. 2019;32(6):802–9. https://doi.org/10.1111/jhn.12674 [published Online First: 19 Jun 2019].CrossRefPubMed

52.

Aktary ML, Eller LK, Nicolucci AC, et al. Cross-sectional analysis of the health profile and dietary intake of a sample of Canadian adults diagnosed with non-alcoholic fatty liver disease. Food Nutr Res. 2020;64:4548. https://doi.org/10.29219/fnr.v64.4548 [published Online First: 17 Oct 2020].

53.

Soltani S, Kolahdouz Mohammadi R, Shab-Bidar S, et al. Sodium status and the metabolic syndrome: a systematic review and meta-analysis of observational studies. Crit Rev Food Sci Nutr. 2019;59(2):196–206. https://doi.org/10.1080/10408398.2017.1363710 [published Online First: 29 Aug 2017].CrossRefPubMed

54.

Brey CW, Akbari-Alavijeh S, Ling J, et al. Salts and energy balance: a special role for dietary salts in metabolic syndrome. Clin Nutr. 2019;38(5):1971–85. https://doi.org/10.1016/j.clnu.2018.10.021 [published Online First: 18 Nov 2018].CrossRefPubMed

55.

He Y, Li Y, Yang X, et al. The dietary transition and its association with cardiometabolic mortality among Chinese adults, 1982–2012: a cross-sectional population-based study. The Lancet Diabetes & Endocrinology. 2019;7(7):540–8. https://doi.org/10.1016/S2213-8587(19)30152-4.CrossRef

56.

Khalatbari-Soltani S, Imamura F, Brage S, et al. The association between adherence to the Mediterranean diet and hepatic steatosis: cross-sectional analysis of two independent studies, the UK Fenland Study and the Swiss CoLaus Study. BMC Med. 2019;17(1):19. https://doi.org/10.1186/s12916-019-1251-7 [published Online First: 25 Jan 2019].CrossRefPubMedPubMedCentral

57.

Baratta F, Pastori D, Polimeni L, et al. Adherence to Mediterranean diet and non-alcoholic fatty liver disease: effect on insulin resistance. Am J Gastroenterol. 2017;112(12):1832–9. https://doi.org/10.1038/ajg.2017.371 [published Online First: 25 Oct 2017].CrossRefPubMed

58.

Liyanage T, Ninomiya T, Wang A, et al. Effects of the Mediterranean diet on cardiovascular outcomes-a systematic review and meta-analysis. PLoS One. 2016;11(8):e0159252. https://doi.org/10.1371/journal.pone.0159252 [published Online First: 11 Aug 2016].CrossRefPubMedPubMedCentral

59.

Rees K, Takeda A, Martin N, et al. Mediterranean-style diet for the primary and secondary prevention of cardiovascular disease. The Cochrane Database of Systematic Reviews. 2019;3(3):Cd009825. https://doi.org/10.1002/14651858.CD009825.pub3 [published Online First: 14 Mar 2019].CrossRefPubMed

60.

Kwak JH, Jun DW, Lee SM, et al. Lifestyle predictors of obese and non-obese patients with nonalcoholic fatty liver disease: a cross-sectional study. Clin Nutr. 2018;37(5):1550–7. https://doi.org/10.1016/j.clnu.2017.08.018 [published Online First: 18 Sep 2017].CrossRefPubMed

61.

Romeo S, Kozlitina J, Xing C, et al. Genetic variation in PNPLA3 confers susceptibility to nonalcoholic fatty liver disease. Nat Genet. 2008;40(12):1461–5. https://doi.org/10.1038/ng.257.CrossRefPubMedPubMedCentral

62.

Shen J, Wong GL, Chan HL, et al. PNPLA3 gene polymorphism and response to lifestyle modification in patients with nonalcoholic fatty liver disease. J Gastroenterol Hepatol. 2015;30(1):139–46. https://doi.org/10.1111/jgh.12656 [published Online First: 22 July 2014].CrossRefPubMed

63.

Wei JL, Leung JC, Loong TC, et al. Prevalence and severity of nonalcoholic fatty liver disease in non-obese patients: a population study using proton-magnetic resonance spectroscopy. Am J Gastroenterol. 2015;110(9):1306–14. https://doi.org/10.1038/ajg.2015.235 quiz 15 [published Online First: 29 July 2015].CrossRefPubMed

64.

Bennett DA, Landry D, Little J, et al. Systematic review of statistical approaches to quantify, or correct for, measurement error in a continuous exposure in nutritional epidemiology. BMC Med Res Methodol. 2017;17(1):146. https://doi.org/10.1186/s12874-017-0421-6 [published Online First: 21 Sep 2017].CrossRefPubMedPubMedCentral

65.

Looman M, Boshuizen HC, Feskens EJ, et al. Using enhanced regression calibration to combine dietary intake estimates from 24 h recall and FFQ reduces bias in diet-disease associations. Public Health Nutr. 2019;22(15):2738–46. https://doi.org/10.1017/s1368980019001563 [published Online First: 03 July 2019].CrossRefPubMed

Title: Healthy dietary patterns and metabolic dysfunction-associated fatty liver disease in less-developed ethnic minority regions: a large cross-sectional study
Authors: Xiaofen Xie
Bing Guo
Xiong Xiao
Jianzhong Yin
Ziyun Wang
Xiaoman Jiang
Jingzhong Li
Lu Long
Junmin Zhou
Ning Zhang
Yuan Zhang
Ting Chen
Baima Kangzhuo
Xing Zhao
Publication date: 01-12-2022
Publisher: BioMed Central
Keywords: Obesity
Obesity
Fatty Liver
Published in: BMC Public Health / Issue 1/2022
Electronic ISSN: 1471-2458
DOI: https://doi.org/10.1186/s12889-021-12486-x

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Healthy dietary patterns and metabolic dysfunction-associated fatty liver disease in less-developed ethnic minority regions: a large cross-sectional study

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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