Skip to main content
Log in

Epicardial adipose tissue in patients with chronic kidney disease: a meta-analysis study and trial sequential analysis

  • Nephrology - Original Paper
  • Published:
International Urology and Nephrology Aims and scope Submit manuscript

Abstract

Background

Cardiovascular disease is the most common cause of death in patients with chronic kidney disease (CKD). Epicardial adipose tissue (EAT) is an independent predictor of cardiovascular disease in the general population, and usually increases in the patients with cardiovascular disease risk. The change of EAT in patients with CKD was still controversial. For further understanding, we conducted a meta-analysis of the relevant literature.

Methods

Eligible studies were searched in PubMed, EMBASE, Web of Science, and Scopus on March 13, 2020. The summarized standard mean difference (SMD) with 95% confidence intervals (CIs) were used to assess the association between EAT (thickness and volume) and CKD. Trial sequential analysis was conducted to estimate whether the evidence of the results is sufficient.

Results

In total, 17 studies with 1961 participants (1205 patients in the CKD group and 756 participants in the control group) were involved. The EAT thickness was significantly increased in the CKD group compared to the control group (SMD = 1.31, 95% CI 0.89–1.73, P < 0.001) in eleven studies. The EAT volume was significantly increased in the CKD group compared to the control group (SMD = 0.77, 95% CI 0.63–0.91, P < 0.001) in six studies. Trial sequential analysis indicated that the available samples were sufficient and confirmed that firm evidence was reached.

Conclusions

Patients with CKD have higher EAT thickness and volume compared to control subjects without CKD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Availability of data and material

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

References

  1. Chen TK, Knicely DH, Grams ME (2019) Chronic kidney disease diagnosis and management: a review. JAMA 322(13):1294–1304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Romagnani P, Remuzzi G, Glassock R, Levin A, Jager KJ, Tonelli M, Massy Z, Wanner C, Anders HJ (2017) Chronic kidney disease. Nat Rev Dis Primers 3:17088

    Article  PubMed  Google Scholar 

  3. Jha V, Garcia-Garcia G, Iseki K, Li Z, Naicker S, Plattner B, Saran R, Wang AY, Yang CW (2013) Chronic kidney disease: global dimension and perspectives. Lancet 382(9888):260–272

    Article  PubMed  Google Scholar 

  4. Chiu DY, Green D, Abidin N, Sinha S, Kalra PA (2015) Cardiac imaging in patients with chronic kidney disease. Nat Rev Nephrol 11(4):207–220

    Article  PubMed  Google Scholar 

  5. Sarnak MJ, Amann K, Bangalore S, Cavalcante JL, Charytan DM, Craig JC, Gill JS, Hlatky MA, Jardine AG, Landmesser U, Newby LK, Herzog CA, Cheung M, Wheeler DC, Winkelmayer WC, Marwick TH, Conference P (2019) Chronic kidney disease and coronary artery disease: JACC state-of-the-art review. J Am Coll Cardiol 74(14):1823–1838

    Article  CAS  PubMed  Google Scholar 

  6. Iacobellis G (2015) Local and systemic effects of the multifaceted epicardial adipose tissue depot. Nat Rev Endocrinol 11(6):363–371

    Article  CAS  PubMed  Google Scholar 

  7. Xu Y, Cheng X, Hong K, Huang C, Wan L (2012) How to interpret epicardial adipose tissue as a cause of coronary artery disease: a meta-analysis. Coron Artery Dis 23(4):227–233

    Article  PubMed  Google Scholar 

  8. Li Y, Liu B, Li Y, Jing X, Deng S, Yan Y, She Q (2019) Epicardial fat tissue in patients with diabetes mellitus: a systematic review and meta-analysis. Cardiovasc Diabetol 18(1):3

    Article  PubMed  PubMed Central  Google Scholar 

  9. Erkan AF, Tanindi A, Kocaman SA, Ugurlu M, Tore HF (2016) Epicardial adipose tissue thickness is an independent predictor of critical and complex coronary artery disease by Gensini and Syntax Scores. Tex Heart Inst J 43(1):29–37

    Article  PubMed  PubMed Central  Google Scholar 

  10. Versteylen MO, Takx RA, Joosen IA, Nelemans PJ, Das M, Crijns HJ, Hofstra L, Leiner T (2012) Epicardial adipose tissue volume as a predictor for coronary artery disease in diabetic, impaired fasting glucose, and non-diabetic patients presenting with chest pain. Eur Heart J Cardiovasc Imaging 13(6):517–523

    Article  PubMed  Google Scholar 

  11. Sheng YN, Zhao DM, Ma QL, Gao Y (2017) Association between epicardial fat volume and coronary artery calcification in patients with chronic kidney disease. Chin J Cardiol 45(2):121–125

    CAS  Google Scholar 

  12. Karatas A, Canakci E, Bektas O, Bayrak T, Bayrak A, Altinbas A, Turkmen E (2018) Relationship of epicardial fat tissue thickness with oxidant biomarkers in chronic kidney disease. Bratisl Lek Listy 119(9):566–571

    CAS  PubMed  Google Scholar 

  13. Ozkurt S, Karavelioǧlu Y, Musmul A (2013) Echocardiographic evaluation of epicardial adipose tissue in non-diabetic, non-hypertensive hemodialysis patients. Ren Fail 35(6):891–895

    Article  PubMed  Google Scholar 

  14. Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339:b2535

    Article  Google Scholar 

  15. Iacobellis G, Willens HJ (2009) Echocardiographic epicardial fat: a review of research and clinical applications. J Am Soc Echocardiogr 22(12):1311–1319 (quiz 1417-1318)

    Article  PubMed  Google Scholar 

  16. Ueno K, Anzai T, Jinzaki M, Yamada M, Jo Y, Maekawa Y, Kawamura A, Yoshikawa T, Tanami Y, Sato K, Kuribayashi S, Ogawa S (2009) Increased epicardial fat volume quantified by 64-multidetector computed tomography is associated with coronary atherosclerosis and totally occlusive lesions. Circ J 73(10):1927–1933

    Article  PubMed  Google Scholar 

  17. National Kidney F (2015) KDOQI clinical practice guideline for hemodialysis adequacy: 2015 update. Am J Kidney Dis 66(5):884–930

    Article  Google Scholar 

  18. Wetterslev J, Jakobsen JC, Gluud C (2017) Trial sequential analysis in systematic reviews with meta-analysis. BMC Med Res Methodol 17(1):39

    Article  PubMed  PubMed Central  Google Scholar 

  19. Tonbul HZ, Turkmen K, Kayikcioglu H, Ozbek O, Kayrak M, Biyik Z (2011) Epicardial adipose tissue and coronary artery calcification in diabetic and nondiabetic end-stage renal disease patients. Ren Fail 33(8):770–775

    Article  PubMed  Google Scholar 

  20. Turkmen K, Kayikcioglu H, Ozbek O, Solak Y, Kayrak M, Samur C, Anil M, Zeki Tonbul H (2011) The relationship between epicardial adipose tissue and malnutrition, inflammation, atherosclerosis/calcification syndrome in ESRD patients. Clin J Am Soc Nephrol CJASN 6(8):1920–1925

    Article  PubMed  Google Scholar 

  21. Turkmen K, Ozbek O, Kayikcioglu H, Kayrak M, Solak Y, Nayman A, Anil M, Babur H, Tonbul HZ (2012) The relationship between epicardial adipose tissue and coronary artery calcification in peritoneal dialysis patients. Cardiorenal Med 2(1):43–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Erdur MF, Tonbul HZ, Ozbiner H, Ozcicek A, Ozcicek F, Akbas EM, Ozbek O, Hamur H, Turkmen K (2013) The relationship between atherogenic index of plasma and epicardial adipose tissue in hemodialysis and peritoneal dialysis patients. Ren Fail 35(9):1193–1198

    Article  CAS  PubMed  Google Scholar 

  23. Altun B, Tasolar H, Eren N, Binnetoʇlu E, Altun M, Temiz A, Gazi E, Barutcu A, Altunoren O, Colkesen Y, Uysal F (2014) Epicardial adipose tissue thickness in hemodialysis patients. Echocardiography (Mount Kisco, NY) 31(8):941–946

    Article  Google Scholar 

  24. Atakan A, Macunluoglu B, Kaya Y, Ari E, Demir H, Asicioglu E, Kaspar C (2014) Epicardial fat thickness is associated with impaired coronary flow reserve in hemodialysis patients. Hemodial Int 18(1):62–69

    Article  PubMed  Google Scholar 

  25. Colak H, Kilicarslan B, Tekce H, Tanrisev M, Tugmen C, Aktas G, Kursat S (2015) Relationship between epicardial adipose tissue, inflammation and volume markers in hemodialysis and transplant patients. Ther Apher Dial 19(1):56–62

    Article  CAS  PubMed  Google Scholar 

  26. Nakanishi K, Fukuda S, Tanaka A, Otsuka K, Taguchi H, Yoshikawa J, Shimada K (2016) Epicardial adipose tissue accumulation is associated with renal dysfunction and coronary plaque morphology on multidetector computed tomography. Circ J 80(1):196–201

    Article  CAS  PubMed  Google Scholar 

  27. Abdallah E, El-Shishtawy S, Sherif N, Ali A, El-Bendary O (2017) Assessment of the relationship between serum paraoxonase activity and epicardial adipose tissue in hemodialysis patients. Int Urol Nephrol 49(2):329–335

    Article  CAS  PubMed  Google Scholar 

  28. Aydin E, Altin C, Sakallioglu O, Yilmaz M, Gezmis E, Elif Sade L, Muderrisoglu H (2017) Epicardial adipose tissue thickness and carotid intima-media thickness in hemodialysis patients. Acta Cardiol Sinica 33(3):266–272

    Google Scholar 

  29. Gok Oguz E, Akoglu H, Ulusal Okyay G, Karaveli Gursoy G, Yildirim T, Merhametsiz O, Cimen T, Canbakan B, Yeter E, Ayli MD (2017) Increased serum renalase in peritoneal dialysis patients: Is it related to cardiovascular disease risk? Nefrologia 37(2):189–194

    Article  PubMed  Google Scholar 

  30. Ozcicek A, Ozcicek F, Yildiz G, Timuroglu A, Demirtas L, Buyuklu M, Kuyrukluyildiz U, Akbas EM, Topal E, Turkmen K (2017) Neutrophil-to-lymphocyte ratio as a possible indicator of epicardial adipose tissue in patients undergoing hemodialysis. Arch Med Sci AMS 13(1):118–123

    Article  PubMed  Google Scholar 

  31. Ayan H, Akilli R, Kaya B, Paydas S, Kara E, Cureoglu A (2019) Relationship between SCUBE1 levels and echocardiography and electrocardiography findings and epicardial adipose tissue/carotid intima-media thickness in patients receiving renal replacement therapy. Exp Clin Transplant 17:181–187

    Article  PubMed  Google Scholar 

  32. Yilmaz Z, İnce H, Aydin E, Yildirim Y, Yilmaz Aydin F, Yüksel E, Karabulut A, Dursun L, Kadiroğlu AK, Yilmaz ME (2020) Relationship between epicardial adipose tissue and body composition as determined by multi-frequency bioelectrical impedance analysis in patients with stage 5 chronic kidney disease. Med Sci Monit 26:e920233

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Silberberg JS, Barre PE, Prichard SS, Sniderman AD (1989) Impact of left ventricular hypertrophy on survival in end-stage renal disease. Kidney Int 36(2):286–290

    Article  CAS  PubMed  Google Scholar 

  34. Tonelli M, Karumanchi SA, Thadhani R (2016) Epidemiology and mechanisms of uremia-related cardiovascular disease. Circulation 133(5):518–536

    Article  CAS  PubMed  Google Scholar 

  35. Gansevoort RT, Correa-Rotter R, Hemmelgarn BR, Jafar TH, Heerspink HJ, Mann JF, Matsushita K, Wen CP (2013) Chronic kidney disease and cardiovascular risk: epidemiology, mechanisms, and prevention. Lancet 382(9889):339–352

    Article  PubMed  Google Scholar 

  36. Aoqui C, Cuppari L, Kamimura MA, Canziani ME (2013) Increased visceral adiposity is associated with coronary artery calcification in male patients with chronic kidney disease. Eur J Clin Nutr 67(6):610–614

    Article  CAS  PubMed  Google Scholar 

  37. Kamimura MA, Carrero JJ, Canziani ME, Watanabe R, Lemos MM, Cuppari L (2013) Visceral obesity assessed by computed tomography predicts cardiovascular events in chronic kidney disease patients. Nutr Metab Cardiovasc Dis NMCD 23(9):891–897

    Article  CAS  PubMed  Google Scholar 

  38. Cordeiro AC, Qureshi AR, Lindholm B, Amparo FC, Tito-Paladino-Filho A, Perini M, Lourenco FS, Pinto IM, Amodeo C, Carrero JJ (2013) Visceral fat and coronary artery calcification in patients with chronic kidney disease. Nephrol Dial Transplant 28(Suppl 4):iv152–159

    Article  CAS  PubMed  Google Scholar 

  39. Oikawa M, Owada T, Yamauchi H, Misaka T, Machii H, Yamaki T, Sugimoto K, Kunii H, Nakazato K, Suzuki H, Saitoh S, Takeishi Y (2015) Epicardial adipose tissue reflects the presence of coronary artery disease: comparison with abdominal visceral adipose tissue. Biomed Res Int 2015:483982

    Article  PubMed  PubMed Central  Google Scholar 

  40. Lin HH, Lee JK, Yang CY, Lien YC, Huang JW, Wu CK (2013) Accumulation of epicardial fat rather than visceral fat is an independent risk factor for left ventricular diastolic dysfunction in patients undergoing peritoneal dialysis. Cardiovasc Diabetol 12:127

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Karastergiou K, Evans I, Ogston N, Miheisi N, Nair D, Kaski JC, Jahangiri M, Mohamed-Ali V (2010) Epicardial adipokines in obesity and coronary artery disease induce atherogenic changes in monocytes and endothelial cells. Arterioscler Thromb Vasc Biol 30(7):1340–1346

    Article  CAS  PubMed  Google Scholar 

  42. Gaborit B, Sengenes C, Ancel P, Jacquier A, Dutour A (2017) Role of epicardial adipose tissue in health and disease: a matter of fat? Compr Physiol 7(3):1051–1082

    Article  PubMed  Google Scholar 

  43. Turan MN, Gungor O, Asci G, Kircelli F, Acar T, Yaprak M, Ceylan N, Demirci MS, Bayraktaroglu S, Toz H, Ozkahya M, Ok E (2013) Epicardial adipose tissue volume and cardiovascular disease in hemodialysis patients. Atherosclerosis 226(1):129–133

    Article  CAS  PubMed  Google Scholar 

  44. D'Marco LG, Bellasi A, Kim S, Chen Z, Block GA, Raggi P (2013) Epicardial adipose tissue predicts mortality in incident hemodialysis patients: a substudy of the Renagel in New Dialysis trial. Nephrol Dial Transplant 28(10):2586–2595

    Article  CAS  PubMed  Google Scholar 

  45. Cordeiro AC, Amparo FC, Oliveira MA, Amodeo C, Smanio P, Pinto IM, Lindholm B, Stenvinkel P, Carrero JJ (2015) Epicardial fat accumulation, cardiometabolic profile and cardiovascular events in patients with stages 3–5 chronic kidney disease. J Intern Med 278(1):77–87

    Article  CAS  PubMed  Google Scholar 

  46. Shlipak MG, Fried LF, Cushman M, Manolio TA, Peterson D, Stehman-Breen C, Bleyer A, Newman A, Siscovick D, Psaty B (2005) Cardiovascular mortality risk in chronic kidney disease: comparison of traditional and novel risk factors. JAMA 293(14):1737–1745

    Article  CAS  PubMed  Google Scholar 

  47. Salazar J, Luzardo E, Mejias JC, Rojas J, Ferreira A, Rivas-Rios JR, Bermudez V (2016) Epicardial fat: physiological, pathological, and therapeutic implications. Cardiol Res Pract 2016:1291537

    Article  PubMed  PubMed Central  Google Scholar 

  48. Kurella M, Lo JC, Chertow GM (2005) Metabolic syndrome and the risk for chronic kidney disease among nondiabetic adults. J Am Soc Nephrol JASN 16(7):2134–2140

    Article  PubMed  Google Scholar 

  49. Banerjee D, Recio-Mayoral A, Chitalia N, Kaski JC (2011) Insulin resistance, inflammation, and vascular disease in nondiabetic predialysis chronic kidney disease patients. Clin Cardiol 34(6):360–365

    Article  PubMed  PubMed Central  Google Scholar 

  50. Rhee CM, Ahmadi SF, Kalantar-Zadeh K (2016) The dual roles of obesity in chronic kidney disease: a review of the current literature. Curr Opin Nephrol Hypertens 25(3):208–216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Ulusal Okyay G, Okyay K, Polattas Solak E, Sahinarslan A, Pasaoglu O, Ayerden Ebinc F, Pasaoglu H, Boztepe Derici U, Sindel S, Arinsoy T (2015) Echocardiographic epicardial adipose tissue measurements provide information about cardiovascular risk in hemodialysis patients. Hemodial Int 19(3):452–462

    Article  PubMed  Google Scholar 

Download references

Funding

None.

Author information

Authors and Affiliations

Authors

Contributions

GS designed the study, collected the data and drafted the manuscript. WQ collected the data and analyzed the data. KL collected the data and analyzed the data. XY analyzed the data and drafted the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Xiaona Yu.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Ethical statement

The authors have no ethical conflicts to disclose.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 100 kb)

Supplementary file2 (PDF 356 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Song, G., Qiao, W., Liu, K. et al. Epicardial adipose tissue in patients with chronic kidney disease: a meta-analysis study and trial sequential analysis. Int Urol Nephrol 52, 2345–2355 (2020). https://doi.org/10.1007/s11255-020-02575-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11255-020-02575-y

Keywords

Navigation