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Nutrition in acute and chronic diseases

Mediators of dietary diversity score (DDS) on NAFLD in Iranian adults: a structural equation modeling study

European Journal of Clinical Nutrition volume 77, pages 370–379 (2023)Cite this article

Subjects

Abstract

Background

The current study examines the association between the Dietary Diversity Score (DDS) and nonalcoholic fatty liver disease (NAFLD) in Iranian adults using structural equation modeling (SEM).

Methods

A sample of 3220 adults from the Amol Cohort Study was recruited for this cross-sectional study. Dietary acid load (DAL) and DDS were calculated using the data obtained from a validated food frequency questionnaire. Anthropometric parameters, blood pressure, biochemical measurements, and liver ultrasonography were evaluated according to standard protocols.

Results

DDS was neither directly nor indirectly associated with a greater prevalence of NAFLD. In the second model (DDS sub-scores model), the association of DAL with NAFLD was fully mediated through waist circumference (WC) (of DAL to WC: β = 0.14, P < 0.0001, and of WC to NAFLD: β = 0.50, P < 0.001). Vegetable and fruit diversity scores had a significant negative indirect relationship with NAFLD prevalence through DAL (β = −0.06, P = 0.001, β = −0.10, P < 0.001, respectively). Meat diversity score was positively associated with NAFLD prevalence in a full mediational process through DAL (β = 0.12, P < 0.001). The SEM fit indices suggested a reasonably adequate fit of the data to the DDS model (Χ2/df = 4.76, GFI = 0.98, AGFI = 0.97, IFI = 0.97, CFI = 0.97, RMSEA = 0.03, and SRMR = 0.02) and its sub-scores model (Χ2/df = 4.72, GFI = 0.98, AGFI = 0.97, IFI = 0.95, CFI = 0.95, RMSEA = 0.03, and SRMR = 0.02).

Conclusion

Meat diversity and lack of vegetable and fruit diversity were indirectly associated with NAFLD prevalence through DAL and WC mediators. Interventions for NAFLD may be more successful if they target a lower intake of animal protein sources and dietary diversity, particularly vegetable and fruit diversity.

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Fig. 1: Study flowchart.
Fig. 2: Hypothesized model in which DAL and WC as mediating variables relate socio-demographic variables and DDS to NAFLD.
Fig. 3: Final structural model of relationship between DDS and NAFLD.
Fig. 4: Final structural model of relationship between DDS sub groups and NAFLD.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Chalasani N, Younossi Z, Lavine JE, Charlton M, Cusi K, Rinella M, et al. The diagnosis and management of nonalcoholic fatty liver disease: practice guidance from the American Association for the Study of Liver Diseases. Hepatology. 2018;67:328–57.

    Article  PubMed  Google Scholar 

  2. Farrell GC, Larter CZ. Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology. 2006;43:S99–112.

    Article  CAS  PubMed  Google Scholar 

  3. Estes C, Chan HL, Chien RN, Chuang WL, Fung J, Goh GB-B, et al. Modelling NAFLD disease burden in four Asian regions—2019–2030. Alimentary Pharmacol Therapeutics. 2020;51:801–11.

    Article  CAS  Google Scholar 

  4. Moghaddasifar I, Lankarani K, Moosazadeh M, Afshari M, Ghaemi A, Aliramezany M, et al. Prevalence of non-alcoholic fatty liver disease and its related factors in Iran. Int J Organ Transplant Med. 2016;7:149.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Romero-Gómez M, Zelber-Sagi S, Trenell M. Treatment of NAFLD with diet, physical activity and exercise. J Hepatol. 2017;67:829–46.

    Article  PubMed  Google Scholar 

  6. Hu FB. Dietary pattern analysis: a new direction in nutritional epidemiology. Curr Opin Lipidol. 2002;13:3–9.

    Article  CAS  PubMed  Google Scholar 

  7. Habte TY, Krawinkel M. Dietary diversity score: a measure of nutritional adequacy or an indicator of healthy diet. J Nutr Health Sci. 2016;3:303.

    Google Scholar 

  8. Conklin AI, Monsivais P, Khaw K-T, Wareham NJ, Forouhi NG. Dietary diversity, diet cost, and incidence of type 2 diabetes in the United Kingdom: a prospective cohort study. PLoS Med. 2016;13:e1002085.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Azadbakht L, Mirmiran P, Esmaillzadeh A, Azizi F. Dietary diversity score and cardiovascular risk factors in Tehranian adults. Public Health Nutr. 2006;9:728–36.

    Article  PubMed  Google Scholar 

  10. Golpour-Hamedani S, Rafie N, Pourmasoumi M, Saneei P, Safavi SM. The association between dietary diversity score and general and abdominal obesity in Iranian children and adolescents. BMC Endocr Disord. 2020;20:1–8.

    Article  Google Scholar 

  11. Doustmohammadian A, Saeidlou SN, Esfandyari S, Gholizadeh E, Maadi M, Motamed N, et al. Dietary Acid Load (DAL), Glycated Hemoglobin A1c (HbA1c), and Metabolic Syndrome (MeS) Mediate the Association of the Adherence to the Dietary Approaches to Stopping Hypertension (DASH) and Mediterranean Diet (MeD) With Nonalcoholic Fatty Liver Disease. Front Nutr. 2022;9:921415. https://doi.org/10.3389/fnut.2022.921415.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Chan R, Wong VW-S, Chu WC-W, Wong GL-H, Li LS, Leung J, et al. Higher estimated net endogenous Acid production may be associated with increased prevalence of nonalcoholic Fatty liver disease in chinese adults in Hong Kong. PLoS One. 2015;10:e0122406.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Doustmohammadian A, Pishgar E, Clark CC, Sobhrakhshankhah E, Nikkhah M, Faraji AH, et al. Empirically-derived dietary patterns in relation to non-alcoholic fatty liver diseases among adult participants in Amol, Northern Iran: A Structural Equation Modeling Approach. Front Nutr. 2022;9:821544. https://doi.org/10.3389/fnut.2022.821544.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Akter S, Eguchi M, Kuwahara K, Kochi T, Ito R, Kurotani K, et al. High dietary acid load is associated with insulin resistance: The Furukawa Nutrition and Health Study. Clin Nutr. 2016;35:453–9.

    Article  CAS  PubMed  Google Scholar 

  15. Lim S, Kim J-W, Targher G. Links between metabolic syndrome and metabolic dysfunction-associated fatty liver disease. Trends Endocrinol Metab. 2021;32:500–14.

    Article  CAS  PubMed  Google Scholar 

  16. Asrih M, Jornayvaz FR. Metabolic syndrome and nonalcoholic fatty liver disease: Is insulin resistance the link? Mol Cell Endocrinol. 2015;418:55–65.

    Article  CAS  PubMed  Google Scholar 

  17. Abbasalizad Farhangi M, Nikniaz L, Nikniaz Z. Higher dietary acid load potentially increases serum triglyceride and obesity prevalence in adults: an updated systematic review and meta-analysis. PloS One. 2019;14:e0216547.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Ghaemi A, Hosseini N, Osati S, Ehrampoush E, Honarvar B, Homayounfar R. Waist circumference is a mediator of dietary pattern in Non-alcoholic fatty liver disease. Sci Rep. 2018;8:1–9.

    Article  CAS  Google Scholar 

  19. Alavian SM, Esmaillzadeh A, Adibi P, Azadbakht L. Dietary quality indices and biochemical parameters among patients with non alcoholic fatty liver disease (NAFLD). Hepatitis monthly. 2013;13:e10943. https://doi.org/10.5812/hepatmon.10943.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Pasdar Y, Moradi S, Moludi J, Darbandi M, Niazi P, Nachvak SM, et al. Risk of metabolic syndrome in non-alcoholic fatty liver disease patients. Mediterranean J Nutr Metab. 2019;12:353–63.

    Article  Google Scholar 

  21. Sberna A, Bouillet B, Rouland A, Brindisi M, Nguyen A, Mouillot T, et al. European Association for the Study of the Liver (EASL), European Association for the Study of Diabetes (EASD) and European Association for the Study of Obesity (EASO) clinical practice recommendations for the management of non‐alcoholic fatty liver disease: evaluation of their application in people with Type 2 diabetes. Diabet Med. 2018;35:368–75.

    Article  CAS  PubMed  Google Scholar 

  22. Mirmiran P, Esfahani FH, Mehrabi Y, Hedayati M, Azizi F. Reliability and relative validity of an FFQ for nutrients in the Tehran lipid and glucose study. Public health Nutr. 2010;13:654–62.

    Article  PubMed  Google Scholar 

  23. Ghaffarpour M, Houshiar-Rad A & Kianfar H (1999) The Manual for Household Measures, Cooking Yields Factors and Edible Portion of Foods. Tehran: Keshaverzi Press (In persian).

  24. Azar M, Sarkisian E. Food composition table of Iran. Tehran: National Nutrition and Food Research Institute, Shahid Beheshti University. 1980;65.

  25. Table FC Food and nutrition information center, UnitedStates Department of Agriculture (USDA) (2019). https://fdc.nal.usda.gov (Accessed August 2021).

  26. Kant AK, Schatzkin A, Harris TB, Ziegler RG, Block G. Dietary diversity and subsequent mortality in the first national health and nutrition examination survey epidemiologic follow-up study. Am J Clin Nutr. 1993;57:434–40.

    Article  CAS  PubMed  Google Scholar 

  27. Kant AK, Block G, Schatzkin A, Ziegler RG, Nestle M. Dietary diversity in the US population, NHANES II, 1976–1980. J Am Dietetic Assoc. 1991;91:1526–31.

    Article  CAS  Google Scholar 

  28. Remer T, Dimitriou T, Manz F. Dietary potential renal acid load and renal net acid excretion in healthy, free-living children and adolescents. Am J Clin Nutr. 2003;77:1255–60.

    Article  CAS  PubMed  Google Scholar 

  29. Frassetto LA, Todd KM, Morris RC Jr, Sebastian A. Estimation of net endogenous noncarbonic acid production in humans from diet potassium and protein contents. Am J Clin Nutr. 1998;68:576–83.

    Article  CAS  PubMed  Google Scholar 

  30. Remer T, Manz F. Potential renal acid load of foods and its influence on urine pH. J Am Dietetic Assoc. 1995;95:791–7.

    Article  CAS  Google Scholar 

  31. Du Bois D. A formula to estimate the approximate surface area if height and weight be known. Nutrition. 1989;5:303–13.

    PubMed  Google Scholar 

  32. Verbraecken J, Van de Heyning P, De Backer W, Van Gaal L. Body surface area in normal-weight, overweight, and obese adults. A comparison study. Metabolism. 2006;55:515–24.

    Article  CAS  PubMed  Google Scholar 

  33. Kant AK, Graubard BI. Energy density of diets reported by American adults: association with food group intake, nutrient intake, and body weight. Int J Obes. 2005;29:950–6.

    Article  CAS  Google Scholar 

  34. Ledikwe JH, Blanck HM, Khan LK, Serdula MK, Seymour JD, Tohill BC, et al. Dietary energy density determined by eight calculation methods in a nationally representative United States population. J Nutr. 2005;135:273–8.

    Article  CAS  PubMed  Google Scholar 

  35. Hagströmer M, Oja P, Sjöström M. The International Physical Activity Questionnaire (IPAQ): a study of concurrent and construct validity. Public Health Nutr. 2006;9:755–62.

    Article  PubMed  Google Scholar 

  36. Willett W. Nutritional Epidemiology. 3rd ed New York, NY: Oxford University Press; (2013).

  37. Azadbakht L, Esmaillzadeh A. Dietary diversity score is related to obesity and abdominal adiposity among Iranian female youth. Public Health Nutr. 2011;14:62–9.

    Article  PubMed  Google Scholar 

  38. Osuna-Padilla I, Leal-Escobar G, Garza-García C, Rodríguez-Castellanos F. Dietary acid load: mechanisms and evidence of its health repercussions. Nefrolía (Engl Ed). 2019;39:343–54.

    Article  CAS  Google Scholar 

  39. Abris GP, Provido SMP, Hong S, Yu SH, Lee CB, Lee JE. Association between dietary diversity and obesity in the Filipino Women’s Diet and Health Study (FiLWHEL): a cross-sectional study. PLoS One. 2018;13:e0206490.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Fatahi S, Qorbani M, Surkan PJ, Azadbakht L. Associations between dietary acid load and obesity among Iranian women. J Cardiovasc Thorac Res. 2021;13:3.

    Article  Google Scholar 

  41. Sookoian S, Pirola CJ. Systematic review with meta‐analysis: risk factors for non‐alcoholic fatty liver disease suggest a shared altered metabolic and cardiovascular profile between lean and obese patients. Alimentary Pharmacol Therapeutics. 2017;46:85–95.

    Article  CAS  Google Scholar 

  42. Karimbeiki R, Pourmasoumi M, Feizi A, Abbasi B, Hadi A, Rafie N, et al. Higher dietary diversity score is associated with obesity: a case–control study. Public Health. 2018;157:127–34.

    Article  CAS  PubMed  Google Scholar 

  43. Kant AK, Schatzkin A, Ziegler RG. Dietary diversity and subsequent cause-specific mortality in the NHANES I epidemiologic follow-up study. J Am Coll Nutr. 1995;14:233–8.

    Article  CAS  PubMed  Google Scholar 

  44. Hooper D, Coughlan J, Mullen M. Structural equation modelling: guidelines for determining model fit. Electron J Bus Res Methods. 2008;6:53–60.

    Google Scholar 

  45. Noureddin M, Zelber‐Sagi S, Wilkens LR, Porcel J, Boushey CJ, Le Marchand L, et al. Diet associations with nonalcoholic fatty liver disease in an ethnically diverse population: the Multiethnic Cohort. Hepatology. 2020;71:1940–52.

    Article  CAS  PubMed  Google Scholar 

  46. Lei S, Liu ZW, Yun L, Cai G, Zhang H, Song LJ, et al. The prevalence of nonalcoholic fatty liver disease and its association with lifestyle/dietary habits among university faculty and staff in Chengdu. Biomed Environ Sci. 2012;25:383–91.

    Google Scholar 

  47. Li Y, He Y, Wang D, Gao X. Association between dietary acid‐based load and obesity in Chinese adults. Wiley Online Library. 2012.

  48. Almeida NS, Rocha R, Cotrim HP, Daltro C. Anthropometric indicators of visceral adiposity as predictors of non-alcoholic fatty liver disease: a review. World J Hepatol. 2018;10:695.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Pang Q, Zhang J-Y, Song S-D, Qu K, Xu X-S, Liu S-S, et al. Central obesity and nonalcoholic fatty liver disease risk after adjusting for body mass index. World J Gastroenterology: WJG. 2015;21:1650.

    Article  PubMed Central  Google Scholar 

  50. Pilgrim A, Robinson S, Sayer AA, Roberts H. An overview of appetite decline in older people. Nurs Older People. 2015;27:29.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Hays NP, Roberts SB. The anorexia of aging in humans. Physiol Behav. 2006;88:257–66.

    Article  CAS  PubMed  Google Scholar 

  52. Hoshiar-Rad A, Kianfar H, Bani-Eghbal B, Dadkhah M, Ghafar-Pour M, editors. Determining of dietary variety in rural and urban families of Tehran. Proceedings of the Fourth Iranian Congress of Nutrition, Tehran, Iran, Tehran University; 1997.

  53. Mirmiran P, Azadbakht L, Azizi F. Dietary diversity within food groups: an indicator of specific nutrient adequacy in Tehranian women. J Am Coll Nutr. 2006;25:354–61.

    Article  PubMed  Google Scholar 

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Acknowledgements

We greatly appreciate the participants, healthcare executives in public health centers in Amol, and the GILDRC staff (www.gildrc.ac.ir), without whom the study would not have been possible.

Funding

This research was conducted by a grant from the research council of Iran University of Medical Sciences of Iran (IUMS) (grant NO: 99–2–30–19054).

Author information

Authors and Affiliations

  1. Gastrointestinal and Liver Diseases Research Center, Iran University of Medical Sciences, Tehran, Iran

    Azam Doustmohammadian, Bahareh Amirkalali, Esmaeel Gholizadeh, Mahmoodreza Khoonsari, Amir Hossein Faraji, Mehdi Nikkhah, Mansooreh Maadi, Mohsen Reza Mansourian, Fahimeh Safarnezhad Tameshkel, Arian Afzali & Farhad Zamani

  2. Department of Social Medicine, Zanjan University of Medical Sciences, Zanjan, Iran

    Nima Motamed

  3. Student Research Committee (National Nutrition and Food Technology Research Institute, Department of Community Nutrition, School of Nutrition Sciences and Food Technology), Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Melika Hajjar

  4. Centre for Intelligent Healthcare, Coventry University, Coventry, CV1 5FB, UK

    Cain C. T. Clark

  5. Eye Reasearch Center, The Five Senses Health Institute, Rassoul Akram Hospital, Iran University of Medical Sciences, Tehran, Iran

    Samira Chaibakhsh

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  1. Azam Doustmohammadian
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Contributions

FZ, MK, AHF, MN, MRM, and AD were responsible for the study concept and design. AD and NM had full access to all data and took responsibility for the integrity of the data and the accuracy of the data analysis. MM, FST, and AA were involved in data collection. AD, NM, CC, and SC analyzed and interpreted the data. MH and AD wrote the initial draft of the manuscript. All authors revised the manuscript critically for important intellectual content and approved the final manuscript. FZ is the guarantor and takes responsibility for the paper as a whole.

Corresponding author

Correspondence to Farhad Zamani.

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The authors declare no competing interests.

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The current study was conducted according to the guidelines laid down in the Declaration of Helsinki, and procedures involving human subjects/patients were approved by the Iran University of Medical Sciences (IUMS) ethical committee (No. IR.IUMS.REC.1399.1393). Written informed consent was obtained from all participants prior to the study.

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Doustmohammadian, A., Amirkalali, B., Gholizadeh, E. et al. Mediators of dietary diversity score (DDS) on NAFLD in Iranian adults: a structural equation modeling study. Eur J Clin Nutr 77, 370–379 (2023). https://doi.org/10.1038/s41430-022-01240-0

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