Epidemiology

Association between habitual yogurt consumption and newly diagnosed non-alcoholic fatty liver disease

Article metrics

Abstract

Background/Objectives

Many studies have suggested that probiotics may be applied as a therapeutic agent for non-alcoholic fatty liver disease (NAFLD). However, the effects of frequent yogurt consumption (as a natural probiotic source) on NAFLD remain poorly understood. This study was to examine the association of habitual yogurt consumption with newly diagnosed NAFLD in the general adult population.

Subject/Methods

Overall, 24,389 adults were included in this cross-sectional study. Yogurt consumption was estimated by using a validated self-administered food frequency questionnaire. NAFLD was diagnosed by abdominal ultrasonography. We used logistic regression models to assess the association between yogurt consumption categories and newly diagnosed NAFLD.

Results

The multivariable odds ratios with 95% confidence interval of newly diagnosed NAFLD were 1.00 (0.88, 1.14) for 1 time/week, 0.91 (0.81, 1.02) for 2–3 times/week, and 0.86 (0.76, 0.98) for ≥4 times/week (P for trend = 0.01), compared with those who consumed <1 time/week yogurt. The inverse association was observed in a sensitivity analysis.

Conclusion

Higher yogurt consumption was inversely associated with the prevalence of newly diagnosed NAFLD. These results are needed to be confirmed in randomized controlled trials or prospective studies.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1

References

  1. 1.

    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. https://doi.org/10.1002/hep.28431.

  2. 2.

    Li Z, Xue J, Chen P, Chen L, Yan S, Liu L. Prevalence of nonalcoholic fatty liver disease in mainland of China: a meta-analysis of published studies. J Gastroenterol Hepatol. 2014;29:42–51. https://doi.org/10.1111/jgh.12428.

  3. 3.

    Targher G, Byrne CD, Lonardo A, Zoppini G, Barbui C. Non-alcoholic fatty liver disease and risk of incident cardiovascular disease: a meta-analysis. J Hepatol. 2016;65:589–600. https://doi.org/10.1016/j.jhep.2016.05.013.

  4. 4.

    Francque SM, van der Graaff D, Kwanten WJ. Non-alcoholic fatty liver disease and cardiovascular risk: Pathophysiological mechanisms and implications. J Hepatol. 2016;65:425–43. https://doi.org/10.1016/j.jhep.2016.04.005.

  5. 5.

    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. https://doi.org/10.1002/hep.29367.

  6. 6.

    Wen L, Duffy A. Factors influencing the gut microbiota, inflammation, and type 2 diabetes. J Nutr. 2017;147:1468S–75S. https://doi.org/10.3945/jn.116.240754.

  7. 7.

    Ye H, Li Q, Zhang Z, Sun M, Zhao C, Zhang T. Effect of a novel potential probiotic Lactobacillus paracasei Jlus66 isolated from fermented milk on nonalcoholic fatty liver in rats. Food Funct. 2017;8:4539–46. https://doi.org/10.1039/c7fo01108c.

  8. 8.

    Xie N, Cui Y, Yin YN, Zhao X, Yang JW, Wang ZG, et al. Effects of two Lactobacillus strains on lipid metabolism and intestinal microflora in rats fed a high-cholesterol diet. BMC Complement Alter Med. 2011;11:53 https://doi.org/10.1186/1472-6882-11-53.

  9. 9.

    Esposito E, Iacono A, Bianco G, Autore G, Cuzzocrea S, Vajro P, et al. Probiotics reduce the inflammatory response induced by a high-fat diet in the liver of young rats. J Nutr. 2009;139:905–11. https://doi.org/10.3945/jn.108.101808.

  10. 10.

    Mouzaki M, Comelli EM, Arendt BM, Bonengel J, Fung SK, Fischer SE, et al. Intestinal microbiota in patients with nonalcoholic fatty liver disease. Hepatology. 2013;58:120–7. https://doi.org/10.1002/hep.26319.

  11. 11.

    Ma X, Hua J, Li Z. Probiotics improve high fat diet-induced hepatic steatosis and insulin resistance by increasing hepatic NKT cells. J Hepatol. 2008;49:821–30. https://doi.org/10.1016/j.jhep.2008.05.025.

  12. 12.

    Kim YA, Keogh JB, Clifton PM. Probiotics, prebiotics, synbiotics and insulin sensitivity. Nutr Res Rev. 2018;31:35–51. https://doi.org/10.1017/S095442241700018X.

  13. 13.

    Pereira DI, Gibson GR. Effects of consumption of probiotics and prebiotics on serum lipid levels in humans. Crit Rev Biochem Mol Biol. 2002;37:259–81. https://doi.org/10.1080/10409230290771519.

  14. 14.

    Bakhshimoghaddam F, Shateri K, Sina M, Hashemian M, Alizadeh M. Daily consumption of synbiotic yogurt decreases liver steatosis in patients with nonalcoholic fatty liver disease: a randomized controlled clinical trial. J Nutr. 2018;148:1276–84. https://doi.org/10.1093/jn/nxy088.

  15. 15.

    Nabavi S, Rafraf M, Somi MH, Homayouni-Rad A, Asghari-Jafarabadi M. Effects of probiotic yogurt consumption on metabolic factors in individuals with nonalcoholic fatty liver disease. J Dairy Sci. 2014;97:7386–93. https://doi.org/10.3168/jds.2014-8500.

  16. 16.

    Farrell GC, Chitturi S, Lau GK, Sollano JD. Asia-Pacific Working Party on NAFLD. Guidelines for the assessment and management of non-alcoholic fatty liver disease in the Asia-Pacific region: executive summary. J Gastroenterol Hepatol. 2007;22:775–7. https://doi.org/10.1111/j.1440-1746.2007.05002.x.

  17. 17.

    Zeng MD, Fan JG, Lu LG, Li YM, Chen CW, Wang BY, et al. Guidelines for the diagnosis and treatment of nonalcoholic fatty liver diseases. J Dig Dis. 2008;9:108–12. https://doi.org/10.1111/j.1751-2980.2008.00331.x.

  18. 18.

    Zhang S, Fu J, Zhang Q, Liu L, Meng G, Yao Z, et al. Association between nut consumption and non-alcoholic fatty liver disease in adults. Liver Int. 2019. https://doi.org/10.1111/liv.14164.

  19. 19.

    Yang YX, Wang GY, Pan XC. China food composition. 2nd ed. Beijing: Peking University Medical Press; 2009.

  20. 20.

    Yu B, Zhu Q, Meng G, Gu Y, Zhang Q, Liu L, et al. Habitual yoghurt consumption and depressive symptoms in a general population study of 19,596 adults. Eur J Nutr. 2018;57:2621–8. https://doi.org/10.1007/s00394-017-1532-x.

  21. 21.

    Craig CL, Marshall AL, Sjostrom M, Bauman AE, Booth ML, Ainsworth BE, et al. International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc. 2003;35:1381–95. https://doi.org/10.1249/01.MSS.0000078924.61453.FB.

  22. 22.

    Mancia G, De Backer G, Dominiczak A, Cifkova R, Fagard R, Germano G, et al. 2007 Guidelines for the Management of Arterial Hypertension: The Task Force for the Management of Arterial Hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC). J Hypertens. 2007;25:1105–87. https://doi.org/10.1097/HJH.0b013e3281fc975a.

  23. 23.

    Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL, Jr. et al. The Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure: the JNC 7 report. JAMA. 2003;289:2560–72. https://doi.org/10.1001/jama.289.19.2560.

  24. 24.

    Alberti KG, Zimmet PZ. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med. 1998;15:539–53.

  25. 25.

    Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009;120:1640–5. https://doi.org/10.1161/CIRCULATIONAHA.109.192644.

  26. 26.

    Gu Y, Hu K, Huang Y, Zhang Q, Liu L, Meng G, et al. White blood cells count as an indicator to identify whether obesity leads to increased risk of type 2 diabetes. Diabetes Res Clin Pract. 2018;141:140–7. https://doi.org/10.1016/j.diabres.2018.04.041.

  27. 27.

    Buendia JR, Li Y, Hu FB, Cabral HJ, Bradlee ML, Quatromoni PA, et al. Regular yogurt intake and risk of cardiovascular disease among hypertensive adults. Am J Hypertens. 2018;31:557–65. https://doi.org/10.1093/ajh/hpx220.

  28. 28.

    Chen M, Sun Q, Giovannucci E, Mozaffarian D, Manson JE, Willett WC, et al. Dairy consumption and risk of type 2 diabetes: 3 cohorts of US adults and an updated meta-analysis. BMC Med. 2014;12:215. https://doi.org/10.1186/s12916-014-0215-1.

  29. 29.

    Aller R, De Luis DA, Izaola O, Conde R, Gonzalez Sagrado M, Primo D, et al. Effect of a probiotic on liver aminotransferases in nonalcoholic fatty liver disease patients: a double blind randomized clinical trial. Eur Rev Med Pharm Sci. 2011;15:1090–5.

  30. 30.

    Wang H, Livingston KA, Fox CS, Meigs JB, Jacques PF. Yogurt consumption is associated with better diet quality and metabolic profile in American men and women. Nutr Res. 2013;33:18–26. https://doi.org/10.1016/j.nutres.2012.11.009.

  31. 31.

    Hobbs DA, Givens DI, Lovegrove JA. Yogurt consumption is associated with higher nutrient intake, diet quality and favourable metabolic profile in children: a cross-sectional analysis using data from years 1–4 of the National diet and Nutrition Survey, UK. Eur J Nutr. 2019;58:409–22. https://doi.org/10.1007/s00394-017-1605-x.

  32. 32.

    Xue L, He J, Gao N, Lu X, Li M, Wu X, et al. Probiotics may delay the progression of nonalcoholic fatty liver disease by restoring the gut microbiota structure and improving intestinal endotoxemia. Sci Rep. 2017;7:45176. https://doi.org/10.1038/srep45176.

  33. 33.

    Maddur H, Neuschwander-Tetri BA. More evidence that probiotics may have a role in treating fatty liver disease. Am J Clin Nutr. 2014;99:425–6. https://doi.org/10.3945/ajcn.113.082636.

  34. 34.

    Eslamparast T, Poustchi H, Zamani F, Sharafkhah M, Malekzadeh R, Hekmatdoost A. Synbiotic supplementation in nonalcoholic fatty liver disease: a randomized, double-blind, placebo-controlled pilot study. Am J Clin Nutr. 2014;99:535–42. https://doi.org/10.3945/ajcn.113.068890.

  35. 35.

    Melanson EL, Sharp TA, Schneider J, Donahoo WT, Grunwald GK, Hill JO. Relation between calcium intake and fat oxidation in adult humans. Int J Obes Relat Metab Disord. 2003;27:196–203. https://doi.org/10.1038/sj.ijo.802202.

  36. 36.

    Zemel MB. Proposed role of calcium and dairy food components in weight management and metabolic health. Phys Sportsmed. 2009;37:29–39. https://doi.org/10.3810/psm.2009.06.1707.

  37. 37.

    Shojaei Zarghani S, Soraya H, Alizadeh M. Calcium and vitamin D3 combinations improve fatty liver disease through AMPK-independent mechanisms. Eur J Nutr. 2018;57:731–40. https://doi.org/10.1007/s00394-016-1360-4.

  38. 38.

    Amarapurkar DN, Hashimoto E, Lesmana LA, Sollano JD, Chen PJ, Goh KL, et al. How common is non-alcoholic fatty liver disease in the Asia-Pacific region and are there local differences? J Gastroenterol Hepatol. 2007;22:788–93. https://doi.org/10.1111/j.1440-1746.2007.05042.x.

  39. 39.

    Agoritsas T, Merglen A, Shah ND, O'Donnell M, Guyatt GH. Adjusted analyses in studies addressing therapy and harm: users' guides to the medical literature. JAMA. 2017;317:748–59. https://doi.org/10.1001/jama.2016.20029.

Download references

Acknowledgements

We are grateful to all the people that have made this study. This study was supported by grants from the National Natural Science Foundation of China (Nos. 81673166, 81372118, 81372467, and 81302422), the key technologies R&D program of Tianjin (Key Project: Nos. 11ZCGYSY05700, 12ZCZDSY20400, 13ZCZDSY20200, and 15YFYZSY00020), the National Science and Technology Support Program (No. 2012BAI02B02), 2012 and 2016 Chinese Nutrition Society (CNS) Nutrition Research Foundation—DSM Research Fund (Nos. 2014–071, 2016–046 and 2016–023), the Technologies development program of Beichen District of Tianjin (Nos. bcws2013–21, bcws2014–05 and 2015-SHGY-02), the technologies project of Tianjin Binhai New Area (Nos. 2013–02–04 and 2013–02–06), the Science Foundation of Tianjin Medical University (Nos. 2010KY28 and 2013KYQ24), the Key Laboratory of Public Health Safety (Fudan University), Ministry of Education (No. GW2014–5), and the National Training Programs of Innovation and Entrepreneurship for Undergraduates (No. 201510062013), China.

Author information

SZ drafted the manuscript. JF, QZ, LL, ML, GM and ZY interpreted the results and contributed to the discussions. HW, YX, XB, YG, SS, XW, MZ, QJ, KS, YW, and HX contributed to collect the data. KN designed the study, analyzed the data, reviewed, and edited the manuscript. KN had full access to all the data and took responsibility for the integrity of the data. All authors approved the final version.

Correspondence to Kaijun Niu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark