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Hepatology International

, Volume 13, Issue 6, pp 757–765 | Cite as

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

  • Bin Liu
  • Yingrui Li
  • Yu Li
  • Yajie Liu
  • Yuling Yan
  • Aoran Luo
  • Hong Ren
  • Qiang SheEmail author
Original Article

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.

Keywords

Non-alcoholic fatty liver disease Non-alcoholic steatohepatitis Epicardial adipose tissue Epicardial fat 

Notes

Author 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.

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).

Compliance with ethical standards

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.

Supplementary material

12072_2019_9972_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 16 kb)
12072_2019_9972_MOESM2_ESM.doc (66 kb)
Supplementary material 2 (DOC 65 kb)

References

  1. 1.
    Tomic D, Kemp WW, Roberts SK. Nonalcoholic fatty liver disease: current concepts, epidemiology and management strategies. Eur J Gastroenterol Hepatol 2018;30(10):1103–1115CrossRefGoogle Scholar
  2. 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:e11293CrossRefGoogle Scholar
  3. 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;44:1072–1079CrossRefGoogle Scholar
  4. 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;2018:2784537PubMedPubMedCentralGoogle Scholar
  5. 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:e0214CrossRefGoogle Scholar
  6. 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;41:1235–1243CrossRefGoogle Scholar
  7. 7.
    Sengul C, Ozveren O. Epicardial adipose tissue: a review of physiology, pathophysiology, and clinical applications. Anatolian J Cardiol 2013;13:261–265Google Scholar
  8. 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;19:490–497CrossRefGoogle Scholar
  9. 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;4:1–6CrossRefGoogle Scholar
  10. 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:e0162473CrossRefGoogle Scholar
  11. 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;22:332–336CrossRefGoogle Scholar
  12. 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;62:928–933CrossRefGoogle Scholar
  13. 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;28:1345–1355CrossRefGoogle Scholar
  14. 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.e1CrossRefGoogle Scholar
  15. 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;15:226–232CrossRefGoogle Scholar
  16. 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;16:974–979PubMedPubMedCentralGoogle Scholar
  17. 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;67:41–48CrossRefGoogle Scholar
  18. 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;163:608–611CrossRefGoogle Scholar
  19. 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;8:6330–6340PubMedGoogle Scholar
  20. 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;112:481–487CrossRefGoogle Scholar
  21. 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;5:13CrossRefGoogle Scholar
  22. 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;237:490–493CrossRefGoogle Scholar
  23. 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;217:125–129CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. 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–e51PubMedGoogle Scholar
  26. 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;24:613–618CrossRefGoogle Scholar
  27. 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;41:1295–1302CrossRefGoogle Scholar
  28. 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;17:115–130CrossRefGoogle Scholar
  29. 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 CrossRefPubMedGoogle Scholar

Copyright information

© Asian Pacific Association for the Study of the Liver 2019

Authors and Affiliations

  • Bin Liu
    • 1
  • Yingrui Li
    • 1
  • Yu Li
    • 1
  • Yajie Liu
    • 1
  • Yuling Yan
    • 1
  • Aoran Luo
    • 2
  • Hong Ren
    • 2
  • Qiang She
    • 1
    Email author
  1. 1.Department of CardiologyThe Second Affiliated Hospital of Chongqing Medical UniversityChongqingChina
  2. 2.Institute for Hepatitis, Key Laboratory of Molecular Biology for Infectious Diseases, Ministry of EducationThe Second Affiliated Hospital of Chongqing Medical UniversityChongqingChina

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