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Association of epicardial adipose tissue with non-alcoholic fatty liver disease: a meta-analysis

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Abstract

Background

Increased epicardial adipose tissue (EAT) has been proposed as a risk factor for non-alcoholic fatty liver disease (NAFLD). The aim of this study was to investigate the association of EAT with NAFLD.

Methods

The PubMed, EMBASE, and Cochrane databases were systematically reviewed by two independent investigators to identify relevant studies assessing the association of EAT thickness (EAT-t) and volume (EAT-v) with NAFLD. Comparisons between NAFLD subjects and controls were performed with meta-analysis and trial sequential analysis (TSA).

Results

A total of thirteen case–control studies (n = 2260 patients) were included in the final analysis. The EAT was significantly increased in NAFLD patients compared with the controls (EAT, SMD: 0.73, 95% CI 0.51–0.94, p < 0.001; TSA-adjusted 95% CI 0.07–0.18; p < 0.001). When comparing the subgroups of NAFLD, the EAT-t in the severe-hepatic steatosis subgroup was thicker than that in the moderate subgroup (SMD: 1.43, 95% CI 0.15–2.71, p = 0.029). This study indicated that the EAT-t in the F3–4 fibrosis subgroup was thicker than that in the F0–2 fibrosis subgroup (SMD: 0.72, 95% CI 0.30–1.14, p = 0.001). The proportion of hypertension (OR = 1.64, 95% CI = 1.24–2.18, p = 0.001) and atherosclerotic cardiovascular disease (ASCVD) (OR = 1.66, 95% CI = 1.21–2.28, p = 0.002) was higher in the high-EAT-t group compared with the low-EAT-t group in NAFLD patients.

Conclusions

The EAT was increased in the NAFLD subjects compared to the controls. The increase in the EAT was associated with the severity of steatosis, fibrosis and cardiovascular disease in patients with NAFLD. These findings provide new information regarding the development and progression of NAFLD.

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References

  1. Tomic D, Kemp WW, Roberts SK. Nonalcoholic fatty liver disease: current concepts, epidemiology and management strategies. Eur J Gastroenterol Hepatol 2018;30(10):1103–1115

    Article  Google Scholar 

  2. Weng S, Zhou J, Chen X, Sun Y, Mao Z, Chai K. Prevalence and factors associated with nonalcoholic fatty pancreas disease and its severity in China. Medicine 2018;97:e11293

    Article  Google Scholar 

  3. Altin C, Yilmaz M, Ozsoy HM, Gezmis E, Balci S, Tekindal MA, et al. Assessment of epicardial fat and carotid intima media thickness in gestational hypertension. J Obst Gynaecol Res 2018;44:1072–1079

    Article  CAS  Google Scholar 

  4. Li B, Zhang C, Zhan YT. Nonalcoholic fatty liver disease cirrhosis: a review of its epidemiology, risk factors, clinical presentation, diagnosis, management, and prognosis. Can J Gastroenterol Hepatol 2018;2018:2784537

    PubMed  PubMed Central  Google Scholar 

  5. Golabi P, Otgonsuren M, de Avila L, Sayiner M, Rafiq N, Younossi ZM. Components of metabolic syndrome increase the risk of mortality in nonalcoholic fatty liver disease (NAFLD). Medicine 2018;97:e0214

    Article  Google Scholar 

  6. Apostolopoulou M, Gordillo R, Koliaki C, Gancheva S, Jelenik T, De Filippo E, et al. Specific hepatic sphingolipids relate to insulin resistance, oxidative stress, and inflammation in nonalcoholic steatohepatitis. Diabetes Care 2018;41:1235–1243

    Article  CAS  Google Scholar 

  7. Sengul C, Ozveren O. Epicardial adipose tissue: a review of physiology, pathophysiology, and clinical applications. Anatolian J Cardiol 2013;13:261–265

    Google Scholar 

  8. Mancio J, Azevedo D, Saraiva F, Azevedo AI, Pires-Morais G, Leite-Moreira A, et al. Epicardial adipose tissue volume assessed by computed tomography and coronary artery disease: a systematic review and meta-analysis. Eur Heart J Cardiovasc Imag 2018;19:490–497

    Article  Google Scholar 

  9. Wojcik-Cichy K, Koslinska-Berkan E, Piekarska A. The influence of NAFLD on the risk of atherosclerosis and cardiovascular diseases. Clin Exp Hepatol 2018;4:1–6

    Article  Google Scholar 

  10. Fracanzani AL, Pisano G, Consonni D, Tiraboschi S, Baragetti A, Bertelli C, et al. Epicardial adipose tissue (EAT) thickness is associated with cardiovascular and liver damage in nonalcoholic fatty liver disease. PLoS ONE 2016;11:e0162473

    Article  Google Scholar 

  11. Iacobellis G, Barbarini G, Letizia C, Barbaro G. Epicardial fat thickness and nonalcoholic fatty liver disease in obese subjects. Obesity (Silver Spring, Md) 2014;22:332–336

    Article  Google Scholar 

  12. Petta S, Argano C, Colomba D, Cammà C, Di Marco V, Cabibi D, et al. Epicardial fat, cardiac geometry and cardiac function in patients with non-alcoholic fatty liver disease: association with the severity of liver disease. J Hepatol 2015;62:928–933

    Article  Google Scholar 

  13. Brouha SS, Nguyen P, Bettencourt R, Sirlin CB, Loomba R. Increased severity of liver fat content and liver fibrosis in non-alcoholic fatty liver disease correlate with epicardial fat volume in type 2 diabetes: a prospective study. Eur Radiol 2018;28:1345–1355

    Article  Google Scholar 

  14. Kim BJ, Cheong ES, Kang JG, Kim BS, Kang JH. Relationship of epicardial fat thickness and nonalcoholic fatty liver disease to coronary artery calcification: from the CAESAR study. J Clin Lipidol 2016;10: 619–626.e1

    Article  Google Scholar 

  15. Cho KI, Jo EA, Cho SH, Kim BH. The influence of epicardial fat and nonalcoholic fatty liver disease on heart rate recovery in metabolic syndrome. Metab Syndr Relat Disord 2017;15:226–232

    Article  CAS  Google Scholar 

  16. Oğuz D, Ünal HÜ, Eroğlu H, Gülmez Ö, Çevik H, Altun A. Aortic flow propagation velocity, epicardial fat thickness, and osteoprotegerin level to predict subclinical atherosclerosis in patients with nonalcoholic fatty liver disease. Anatol J Cardiol 2016;16:974–979

    PubMed  PubMed Central  Google Scholar 

  17. Psychari SN, Rekleiti N, Papaioannou N, Varhalama E, Drakoulis C, Apostolou TS, et al. Epicardial fat in nonalcoholic fatty liver disease: properties and relationships with metabolic factors, cardiac structure, and cardiac function. Angiology 2016;67:41–48

    Article  CAS  Google Scholar 

  18. Gruzdeva OV, Akbasheva OE, Dyleva YA, Antonova LV, Matveeva VG, Uchasova EG, et al. Adipokine and cytokine profiles of epicardial and subcutaneous adipose tissue in patients with coronary heart disease. Bull Exp Biol Med 2017;163:608–611

    Article  CAS  Google Scholar 

  19. Gao Y, Zhang K, Xi H, Cai A, Wu X, Cui J, et al. Diagnostic and prognostic value of circulating tumor DNA in gastric cancer: a meta-analysis. Oncotarget 2017;8:6330–6340

    PubMed  Google Scholar 

  20. Tiu J, Waddell JN, Al-Amleh B, Jansen van Vuuren WA, Swain MV. Coordinate geometry method for capturing and evaluating crown preparation geometry. J Prosth Dent 2014;112:481–487

    Article  Google Scholar 

  21. Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 2005;5:13

    Article  Google Scholar 

  22. Sunbul M, Agirbasli M, Durmus E, Kivrak T, Akin H, Aydin Y, et al. Arterial stiffness in patients with non-alcoholic fatty liver disease is related to fibrosis stage and epicardial adipose tissue thickness. Atherosclerosis 2014;237:490–493

    Article  CAS  Google Scholar 

  23. Yilmaz Y, Kurt R, Gurdal A, Alahdab YO, Yonal O, Senates E, et al. Circulating vaspin levels and epicardial adipose tissue thickness are associated with impaired coronary flow reserve in patients with nonalcoholic fatty liver disease. Atherosclerosis 2011;217:125–129

    Article  CAS  Google Scholar 

  24. Granér M, Nyman K, Siren R, Pentikäinen MO, Lundbom J, Hakkarainen A, et al. Ectopic fat depots and left ventricular function in nondiabetic men with nonalcoholic fatty liver disease. Circulation Cardiovasc Imag 2015. https://doi.org/10.1161/CIRCIMAGING.114.001979

    Article  Google Scholar 

  25. Topuz M, Dogan A, Celik A, Can C, Ozdogru I, Kemal Eryol N. Investigation of the relationship between non-alcoholic fatty liver disease and coronary artery disease. La Clinica Terapeutica 2014;165:e46–e51

    CAS  PubMed  Google Scholar 

  26. Colak Y, Karabay CY, Tuncer I, Kocabay G, Kalayci A, Senates E, et al. Relation of epicardial adipose tissue and carotid intima-media thickness in patients with nonalcoholic fatty liver disease. Eur J Gastroenterol Hepatol 2012;24:613–618

    Article  Google Scholar 

  27. Lana JP, Martins LB, Oliveira MC, Menezes-Garcia Z, Yamada LT, Vieira LQ, et al. TNF and IL-18 cytokines may regulate liver fat storage under homeostasis conditions. Appl Physiol Nutr Metab 2016;41:1295–1302

    Article  CAS  Google Scholar 

  28. Spiroglou SG, Kostopoulos CG, Varakis JN, Papadaki HH. Adipokines in periaortic and epicardial adipose tissue: differential expression and relation to atherosclerosis. J Atherosc Thromb 2010;17:115–130

    Article  CAS  Google Scholar 

  29. Turan Y. The nonalcoholic fatty liver disease fibrosis score is related to epicardial fat thickness and complexity of coronary artery disease. Angiology 2019. https://doi.org/10.1177/0003319719844933

    Article  PubMed  Google Scholar 

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Funding

This study was funded by the National Natural Science Foundation of China (81770251) and the National Natural Science Foundation of China Youth Science Fund Project (81800254).

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Authors and Affiliations

  1. Department of Cardiology, The Second Affiliated Hospital of Chongqing Medical University, 74 Linjiang Road, Chongqing, 400010, China

    Bin Liu, Yingrui Li, Yu Li, Yajie Liu, Yuling Yan & Qiang She

  2. Institute for Hepatitis, Key Laboratory of Molecular Biology for Infectious Diseases, Ministry of Education, The Second Affiliated Hospital of Chongqing Medical University, Chongqing, 400010, China

    Aoran Luo & Hong Ren

Authors
  1. Bin Liu
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  2. Yingrui Li
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  3. Yu Li
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  4. Yajie Liu
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  5. Yuling Yan
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  7. Hong Ren
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  8. Qiang She
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Contributions

Conceived and designed the experiments: QS and BL. Collected the data: BL, Yingrui L, and Yu L. Analyzed the data: BL, Yuling Y, and Yajie L. Wrote the paper: BL. Revised the paper: BL, Yingrui L, Yuling Y, Aoran L, HR and QS.

Corresponding author

Correspondence to Qiang She.

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Conflict of interest

Bin Liu, Yingrui Li, Yu Li, Yajie Liu, Yuling Yan, Aoran Luo, Hong Ren and Qiang She declare that they have no competing interests.

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Liu, B., Li, Y., Li, Y. et al. Association of epicardial adipose tissue with non-alcoholic fatty liver disease: a meta-analysis. Hepatol Int 13, 757–765 (2019). https://doi.org/10.1007/s12072-019-09972-1

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  • DOI: https://doi.org/10.1007/s12072-019-09972-1

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