Association Between Serum Uric Acid and Non-Alcoholic Fatty Liver Disease: An Updated Systematic Review and Meta-Analysis

References

• 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):202–209. doi:10.1016/j.jhep.2020.03.039
   PubMed Web of Science ®Google Scholar
• Chalasani N, Younossi Z, Lavine JE, 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(1):328–357. doi:10.1002/hep.29367
   PubMed Web of Science ®Google Scholar
• 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(1):73–84. doi:10.1002/hep.28431
   PubMed Web of Science ®Google Scholar
• Powell EE, Wong VW, Rinella M. Non-alcoholic fatty liver disease. Lancet. 2021;397(10290):2212–2224. doi:10.1016/S0140-6736(20)32511-3
   PubMed Web of Science ®Google Scholar
• Fan JG, Farrell GC. Epidemiology of non-alcoholic fatty liver disease in China. J Hepatol. 2009;50(1):204–210. doi:10.1016/j.jhep.2008.10.010
   PubMed Web of Science ®Google Scholar
• Miyake T, Kumagi T, Furukawa S, et al. Non-alcoholic fatty liver disease: factors associated with its presence and onset. J Gastroenterol Hepatol. 2013;28(s4):71–78. doi:10.1111/jgh.12251
   PubMedGoogle Scholar
• Bai JX, Shu RM, Huang Y, Peng Z. 血尿酸与非酒精性脂肪性肝病发生风险相关性的随访队列研究 [Correlation between serum uric acid and risk of new-onset nonalcoholic fatty liver disease: a 5-year observational cohort study]. Zhonghua Gan Zang Bing Za Zhi. 2018;26(4):271–275. Chinese. doi:10.3760/cma.j.issn.1007-3418.2018.04.008
   PubMedGoogle Scholar
• Cai W, Wu X, Zhang B, et al. Serum uric acid levels and nonalcoholic fatty liver disease in Uyghur and Han ethnic groups in northwestern China. Arq Bras Endocrinol Metabol. 2013;57(8):617–622. doi:10.1590/S0004-27302013000800006
   PubMedGoogle Scholar
• Hu Y, Li Q, Min R, Deng Y, Xu Y, Gao L. The association between serum uric acid and diabetic complications in patients with type 2 diabetes mellitus by gender: a cross-sectional study. PeerJ. 2021;9:e10691. doi:10.7717/peerj.10691
   PubMed Web of Science ®Google Scholar
• Li Y, Xu C, Yu C, Xu L, Miao M. Association of serum uric acid level with non-alcoholic fatty liver disease: a cross-sectional study. J Hepatol. 2009;50(5):1029–1034. doi:10.1016/j.jhep.2008.11.021
   PubMed Web of Science ®Google Scholar
• Bao T, Ying ZY, Gong L, et al. Association between serum uric acid and nonalcoholic fatty liver disease in nonobese postmenopausal women: a cross-sectional study. Sci Rep. 2020;10(1). doi:10.1038/s41598-020-66931-9
   Web of Science ®Google Scholar
• Han L, Zhang Y, Yue C, Huang Y, Wu Y, Chen J. Preliminary study on risk factors for morbidity of nonalcoholic fatty liver disease in high-income male population. J Healthc Eng. 2022;2022:9331284. doi:10.1155/2022/9331284
   PubMed Web of Science ®Google Scholar
• Chen YL, Li H, Li S, et al. Prevalence of and risk factors for metabolic associated fatty liver disease in an urban population in China: a cross-sectional comparative study. BMC Gastroenterol. 2021;21(1):212. doi:10.1186/s12876-021-01782-w
   PubMed Web of Science ®Google Scholar
• Liu P, Ma F, Lou H, Zhu Y, Chen Y. 绝经后女性正常血尿酸水平与非酒精性脂肪性肝病的相关性 [Relationship between normal serum uric acid levels and nonalcoholic fatty liver disease in postmenopausal women]. Zhonghua Gan Zang Bing Za Zhi. 2014;22(1):53–57. Chinese. doi:10.3760/cma.j.issn.1007-3418.2014.01.012
   PubMedGoogle Scholar
• Liu PJ, Ma F, Lou HP, Zhu YN, Chen Y. Relationship between serum uric acid levels and hepatic steatosis in non-obese postmenopausal women. Climacteric. 2014;17(6):692–699. doi:10.3109/13697137.2014.926323
   PubMed Web of Science ®Google Scholar
• Fan NG, Zhang LJ, Xia ZH, Peng L, Wang YF, Peng YD. Sex-specific association between serum uric acid and nonalcoholic fatty liver disease in type 2 diabetic patients. J Diabetes Res. 2016;2016:1–6. doi:10.1155/2016/3805372
   Web of Science ®Google Scholar
• Wang ZL, Xu M, Hu ZG, Shrestha UK. Prevalence of nonalcoholic fatty liver disease and its metabolic risk factors in women of different ages and body mass index. Menopause. 2015;22(6):667–673. doi:10.1097/GME.0000000000000352
   PubMed Web of Science ®Google Scholar
• Darmawan G, Hamijoyo L, Hasan I. Association between serum uric acid and non-alcoholic fatty liver disease: a meta-analysis. Acta Med Indones. 2017;49(2):136–147.
   PubMed Web of Science ®Google Scholar
• Gong SL, Song JQ, Wang L, Zhang SQ, Wang YG. Hyperuricemia and risk of nonalcoholic fatty liver disease: a systematic review and meta-analysis. Eur J Gastroenterol Hepatol. 2016;28(2):132–138. doi:10.1097/MEG.0000000000000507
   PubMed Web of Science ®Google Scholar
• Huang F, Liu AD, Fang HS, Geng XP. Serum uric acid levels in non-alcoholic steatosis patients: a meta-analysis. Asia Pac J Clin Nutr. 2017;26(2):334–342. doi:10.6133/apjcn.092016.04
   PubMed Web of Science ®Google Scholar
• Liu ZT, Que SP, Zhou L, Zheng SS. Dose-response relationship of serum uric acid with metabolic syndrome and non-alcoholic fatty liver disease incidence: a meta-analysis of prospective studies. Sci Rep. 2015;5:14325.
   PubMed Web of Science ®Google Scholar
• Wijarnpreecha K, Panjawatanan P, Lekuthai N, Thongprayoon C, Cheungpasitporn W, Ungprasert P. Hyperuricaemia and risk of nonalcoholic fatty liver disease: a meta-analysis. Liver Int. 2017;37(6):906–918. doi:10.1111/liv.13329
   PubMed Web of Science ®Google Scholar
• Zhou YJ, Wei FF, Fan Y. High serum uric acid and risk of nonalcoholic fatty liver disease: a systematic review and meta-analysis. Clin Biochem. 2016;49(7–8):636–642. doi:10.1016/j.clinbiochem.2015.12.010
   PubMed Web of Science ®Google Scholar
• Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Syst Rev. 2021;10(1):1–11. doi:10.1186/s13643-021-01626-4
   PubMed Web of Science ®Google Scholar
• Hu J, Dong Y, Chen X, et al. Prevalence of suicide attempts among Chinese adolescents: a meta-analysis of cross-sectional studies. Compr Psychiatry. 2015;61:78–89. doi:10.1016/j.comppsych.2015.05.001
   PubMed Web of Science ®Google Scholar
• Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25(9):603–605. doi:10.1007/s10654-010-9491-z
   PubMed Web of Science ®Google Scholar
• Cai W, Song JM, Zhang B, Sun YP, Yao H, Zhang YX. The prevalence of nonalcoholic fatty liver disease and relationship with serum uric acid level in Uyghur population. TheScientificWorldJournal. 2014;2014:393628. doi:10.1155/2014/393628
   PubMedGoogle Scholar
• Catanzaro R, Calabrese F, Palermo F, et al. The relationship between serum uric acid and non alcoholic fatty liver disease: a cross-sectional retrospective study. Dig Liver Dis. 2014;46:S114.
   Google Scholar
• Chao G, Chen L. Study on the independent effect of thyroid hormone based on uric acid level on NAFLD. J Health Popul Nutr. 2021;40(1):21. doi:10.1186/s41043-021-00247-w
   PubMed Web of Science ®Google Scholar
• Chen Y, Huang Q, Ai P, et al. Association between serum uric acid and non-alcoholic fatty liver disease according to different menstrual status groups. Can J Gastroenterol Hepatol. 2019;2019:2763093. doi:10.1155/2019/2763093
   PubMed Web of Science ®Google Scholar
• Cho HC. Prevalence and factors associated with nonalcoholic fatty liver disease in a nonobese Korean population. Gut Liver. 2016;10(1):117–125. doi:10.5009/gnl14444
   PubMed Web of Science ®Google Scholar
• Cui L, Meng L, Wang G, et al. Prevalence and risk factors of hyperuricemia: results of the Kailuan cohort study. Mod Rheumatol. 2017;27(6):1066–1071. doi:10.1080/14397595.2017.1300117
   PubMed Web of Science ®Google Scholar
• Cui YL, Liu J, Shi HY, Hu WM, Song L, Zhao Q. Serum uric acid is positively associated with the prevalence of nonalcoholic fatty liver in non-obese type 2 diabetes patients in a Chinese population. J Diabetes Complications. 2021;35(5):107874. doi:10.1016/j.jdiacomp.2021.107874
   PubMed Web of Science ®Google Scholar
• Golmohammadi S, Tavasoli M, Asadi N. Prevalence and risk factors of hyperuricemia in patients with chronic kidney disease and non-alcoholic fatty liver. Clin Exp Gastroenterol. 2020;13:299–304. doi:10.2147/CEG.S253619
   PubMed Web of Science ®Google Scholar
• Hu MY, Liu JB, Zhou CH, Li XL. Analysis of the interaction effects among the risk factors for hyperuricaemia in adults: a cross-sectional survey in Guilin, China. Int J Clin Exp Med. 2017;10(6):9376–9386.
   Web of Science ®Google Scholar
• Hu XY, Li Y, Li LQ, et al. Risk factors and biomarkers of non-alcoholic fatty liver disease: an observational cross-sectional population survey. BMJ Open. 2018;8(4):e019974. doi:10.1136/bmjopen-2017-019974
   PubMed Web of Science ®Google Scholar
• Hwang IC, Suh SY, Suh AR, Ahn HY. The relationship between normal serum uric acid and nonalcoholic fatty liver disease. J Korean Med Sci. 2011;26(3):386–391. doi:10.3346/jkms.2011.26.3.386
   PubMed Web of Science ®Google Scholar
• Kuo CF, Yu KH, Luo SF, et al. Gout and risk of non-alcoholic fatty liver disease. Scand J Rheumatol. 2010;39(6):466–471. doi:10.3109/03009741003742797
   PubMed Web of Science ®Google Scholar
• Lee JW, Cho YK, Ryan MC, et al. Serum uric acid as a predictor for the development of nonalcoholic fatty liver disease in apparently healthy subjects: a 5-year retrospective cohort study. Gut Liver. 2010;4(3):378–383. doi:10.5009/gnl.2010.4.3.378
   PubMed Web of Science ®Google Scholar
• Lee K. Relationship between uric acid and hepatic steatosis among Koreans. Diabetes Metab. 2009;35(6):447–451. doi:10.1016/j.diabet.2009.04.011
   PubMed Web of Science ®Google Scholar
• Lee YJ, Lee HR, Lee JH, Shin YH, Shim JY. Association between serum uric acid and non-alcoholic fatty liver disease in Korean adults. Clin Chem Lab Med. 2010;48(2):175–180. doi:10.1515/CCLM.2010.037
   PubMed Web of Science ®Google Scholar
• Li Y, Song CL, Yang HH, et al. 苏州60岁及以上老年人群非酒精性肝脏脂肪变性状况及影响因素分析 [Study about the risk factors of non-alcoholic fatty liver disease among people aged over 60 years old in Suzhou]. Zhonghua yu fang yi xue za zhi. 2017;51(5):444–446. Chinese. doi:10.3760/cma.j.issn.0253-9624.2017.05.014
   PubMedGoogle Scholar
• Liu C, Liu W, Zhang G, et al. Conjunctional relationship between serum uric acid and serum nickel with non-alcoholic fatty liver disease in men: a cross-sectional study. Int J Environ Res Public Health. 2022;19(11):6424.
   PubMed Web of Science ®Google Scholar
• Liu CQ, He CM, Chen N, et al. Serum uric acid is independently and linearly associated with risk of nonalcoholic fatty liver disease in obese Chinese adults. Sci Rep. 2016;6:38605.
   PubMed Web of Science ®Google Scholar
• Liu J, Xu CF, Ying LM, et al. Relationship of serum uric acid level with non-alcoholic fatty liver disease and its inflammation progression in non-obese adults. Hepatol Res. 2017;47(3):E104–E112. doi:10.1111/hepr.12734
   PubMed Web of Science ®Google Scholar
• Ma ZM, Zhang JB, Kang XP, et al. Hyperuricemia precedes non-alcoholic fatty liver disease with abdominal obesity moderating this unidirectional relationship: three longitudinal analyses. Atherosclerosis. 2020;311:44–51. doi:10.1016/j.atherosclerosis.2020.08.006
   PubMed Web of Science ®Google Scholar
• Pan XT, Xie XX, Peng HW, et al. Risk prediction for non-alcoholic fatty liver disease based on biochemical and dietary variables in a Chinese Han Population. Front Public Health. 2020;8. doi:10.3389/fpubh.2020.00220
   Web of Science ®Google Scholar
• Ryu S, Chang Y, Kim SG, Cho J, Guallar E. Serum uric acid levels predict incident nonalcoholic fatty liver disease in healthy Korean men. Metabolism. 2011;60(6):860–866. doi:10.1016/j.metabol.2010.08.005
   PubMed Web of Science ®Google Scholar
• Shen Y, Wang Y, Chang C, Li S, Li W, Ni B. Prevalence and risk factors associated with hyperuricemia among working population at high altitudes: a cross-sectional study in Western China. Clin Rheumatol. 2019;38(5):1375–1384. doi:10.1007/s10067-018-4391-9
   PubMed Web of Science ®Google Scholar
• Shih MH, Lazo M, Liu SH, Bonekamp S, Hernaez R, Clark JM. Association between serum uric acid and nonalcoholic fatty liver disease in the US population. J Formos Med Assoc. 2015;114(4):314–320. doi:10.1016/j.jfma.2012.11.014
   PubMed Web of Science ®Google Scholar
• Sirota JC, McFann K, Targher G, Johnson RJ, Chonchol M, Jalal DI. Elevated serum uric acid levels are associated with non-alcoholic fatty liver disease independently of metabolic syndrome features in the United States: liver ultrasound data from the national health and nutrition examination survey. Metabolism. 2013;62(3):392–399. doi:10.1016/j.metabol.2012.08.013
   PubMed Web of Science ®Google Scholar
• Tang Y, Xu Y, Liu P, et al. No evidence for a causal link between serum uric acid and nonalcoholic fatty liver disease from the dongfeng-tongji cohort study. Oxid Med Cell Longev. 2022;2022:6687626. doi:10.1155/2022/6687626
   PubMedGoogle Scholar
• Tung TH, Chang TH, Chiu WH, et al. Clinical correlation of nonalcoholic fatty liver disease in a Chinese taxi drivers population in Taiwan: experience at a teaching hospital. BMC Res Notes. 2011;4:315. doi:10.1186/1756-0500-4-315
   PubMedGoogle Scholar
• Wang M, Wang M, Zhang R, et al. A combined association of serum uric acid, alanine aminotransferase and waist circumference with non-alcoholic fatty liver disease: a community-based study. PeerJ. 2022;10:e13022. doi:10.7717/peerj.13022
   PubMed Web of Science ®Google Scholar
• Wang Z, Xu M, Peng J, et al. Prevalence and associated metabolic factors of fatty liver disease in the elderly. Exp Gerontol. 2013;48(8):705–709. doi:10.1016/j.exger.2013.05.059
   PubMed Web of Science ®Google Scholar
• Wei F, Li J, Chen C, et al. Higher serum uric acid level predicts non-alcoholic fatty liver disease: a 4-year prospective cohort study. Front Endocrinol. 2020;11:179. doi:10.3389/fendo.2020.00179
   PubMed Web of Science ®Google Scholar
• Wu SJ, Zhu GQ, Ye BZ, et al. Association between sex-specific serum uric acid and non-alcoholic fatty liver disease in Chinese adults: a large population-based study. Medicine. 2015;94(17):e802. doi:10.1097/MD.0000000000000802
   PubMed Web of Science ®Google Scholar
• Xie Y, Wang M, Zhang Y, et al. Serum uric acid and non-alcoholic fatty liver disease in non-diabetic Chinese men. PLoS One. 2013;8(7):e67152. doi:10.1371/journal.pone.0067152
   PubMed Web of Science ®Google Scholar
• Xu C, Yu C, Xu L, Miao M, Li Y, Ng IOL. High serum uric acid increases the risk for nonalcoholic fatty liver disease: a prospective observational study. PLoS One. 2010;5(7):e11578. doi:10.1371/journal.pone.0011578
   PubMed Web of Science ®Google Scholar
• Yamada T, Suzuki S, Fukatsu M, Wada T, Yoshida T, Joh T. Elevated serum uric acid is an independent risk factor for nonalcoholic fatty liver disease in Japanese undergoing a health checkup. Acta Gastroenterol Belg. 2010;73(1):12–17.
   PubMed Web of Science ®Google Scholar
• Yang C, He Q, Chen Z, et al. A bidirectional relationship between hyperuricemia and metabolic dysfunction-associated fatty liver disease. Front Endocrinol. 2022;13:821689. doi:10.3389/fendo.2022.821689
   PubMed Web of Science ®Google Scholar
• Yang C, Yang SJ, Xu WW, Zhang JH, Fu WG, Feng CH. Association between the hyperuricemia and nonalcoholic fatty liver disease risk in a Chinese population: a retrospective cohort study. PLoS One. 2017;12(5):e0177249.
   PubMed Web of Science ®Google Scholar
• Yang HH, Li DM, Song XC, et al. Joint associations of serum uric acid and ALT with NAFLD in elderly men and women: a Chinese cross-sectional study. J Transl Med. 2018;16. doi:10.1186/s12967-018-1657-6
   Web of Science ®Google Scholar
• Yu HF, Zhao L, Liu LJ, Li YF, Sun J, Liu YD. Relationship between serum uric acid level and nonalcoholic fatty liver disease in type 2 diabetes patients. Medicine. 2021;100(33):e26946. doi:10.1097/MD.0000000000026946
   PubMed Web of Science ®Google Scholar
• Yu XL, Shu L, Shen XM, Zheng XY, Zheng PF. Gender difference on the relationship between hyperuricemia and nonalcoholic fatty liver disease among Chinese an observational study. Medicine. 2017;96(39):e8164. doi:10.1097/MD.0000000000008164
   PubMed Web of Science ®Google Scholar
• Zhang S, Du T, Li M, Lu H, Lin X, Yu X. Combined effect of obesity and uric acid on nonalcoholic fatty liver disease and hypertriglyceridemia. Medicine. 2017;96(12):e6381. doi:10.1097/MD.0000000000006381
   PubMed Web of Science ®Google Scholar
• Zheng XY, Gong LL, Luo R, et al. Serum uric acid and non-alcoholic fatty liver disease in non-obesity Chinese adults. Lipids Health Dis. 2017;16(1). doi:10.1186/s12944-017-0531-5
   Google Scholar
• Li C, Hsieh MC, Chang SJ. Metabolic syndrome, diabetes, and hyperuricemia. Curr Opin Rheumatol. 2013;25(2):210–216. doi:10.1097/BOR.0b013e32835d951e
   PubMed Web of Science ®Google Scholar
• Zhu Y, Hu Y, Huang T, et al. High uric acid directly inhibits insulin signalling and induces insulin resistance. Biochem Biophys Res Commun. 2014;447(4):707–714. doi:10.1016/j.bbrc.2014.04.080
   PubMed Web of Science ®Google Scholar
• Vacca M, Allison M, Griffin JL, Vidal-Puig A. Fatty acid and glucose sensors in hepatic lipid metabolism: implications in NAFLD. Semin Liver Dis. 2015;35(3):250–261. doi:10.1055/s-0035-1562945
   PubMed Web of Science ®Google Scholar
• Xu C. Hyperuricemia and nonalcoholic fatty liver disease: from bedside to bench and back. Hepatol Int. 2016;10(2):286–293. doi:10.1007/s12072-015-9682-5
   PubMed Web of Science ®Google Scholar
• Wan X, Xu C, Lin Y, et al. Uric acid regulates hepatic steatosis and insulin resistance through the NLRP3 inflammasome-dependent mechanism. J Hepatol. 2016;64(4):925–932. doi:10.1016/j.jhep.2015.11.022
   PubMed Web of Science ®Google Scholar
• Xu C, Wan X, Xu L, et al. Xanthine oxidase in non-alcoholic fatty liver disease and hyperuricemia: one stone hits two birds. J Hepatol. 2015;62(6):1412–1419. doi:10.1016/j.jhep.2015.01.019
   PubMed Web of Science ®Google Scholar