Vol. 25 No. 3 (2021)
REVIEWS

The role of epicardial adipose tissue and autonomic nervous system in pathophysiology of cardiac arrhythmias

PDF (Русский)
  • D.V. Losik,
  • N.A. Nikitin,
  • S.M. Minin,
  • E.V. Fisher,
  • I.L. Mikheenko,
  • A.M. Chernyavskiy,
  • A.B. Romanov
D.V. Losik
Meshalkin National Medical Research Center, Novosibirsk
Bio
N.A. Nikitin
Avicenna Medical Center, Novosibirsk
S.M. Minin
Meshalkin National Medical Research Center, Novosibirsk
E.V. Fisher
Meshalkin National Medical Research Center, Novosibirsk
I.L. Mikheenko
Meshalkin National Medical Research Center, Novosibirsk
A.M. Chernyavskiy
Meshalkin National Medical Research Center, Novosibirsk
A.B. Romanov
Meshalkin National Medical Research Center, Novosibirsk
DOI: https://doi.org/10.21688/1681-3472-2021-3-27-33

Published 2021-09-28

Keywords

  • atrial fibrillation,
  • autonomic nervous system,
  • epicardial adipose tissue,
  • heart failure,
  • ventricular tachycardia

How to Cite

Losik, D., Nikitin, N., Minin, S., Fisher, E., Mikheenko, I., Chernyavskiy, A., & Romanov, A. (2021). The role of epicardial adipose tissue and autonomic nervous system in pathophysiology of cardiac arrhythmias. Patologiya Krovoobrashcheniya I Kardiokhirurgiya, 25(3), 27–33. https://doi.org/10.21688/1681-3472-2021-3-27-33

Copyright (c) 2021 Losik D.V., Nikitin N.A., Minin S.M., Fisher E.V., Mikheenko I.L., Chernyavskiy A.M., Romanov A.B.

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Abstract

The role of epicardial adipose tissue (EAT) in the pathogenesis and prognosis of cardiovascular diseases has been actively discussed. This review provides information regarding the main mechanisms by which EAT influences the pathophysiology of rhythm disturbances, such as atrial fibrillation and ventricular arrhythmias, as well as their relationship with chronic heart failure. The pathogenesis of cardiac arrhythmias is exceedingly complex. As such, the mechanism by which EAT influences arrhythmias and heart failure can vary according to the anatomy and type of arrhythmia, one of which involves the autonomic nervous system (ANS). Some studies have shown a good treatment effects by targeting EAT in atrial fibrillation, whereas others have found that EAT volume can be used to predict the efficacy of radiofrequency ablation, a method for treating atrial fibrillation and ventricular arrhythmias. However, no standards have yet been established for the use of EAT visualisation. Fundamental, translational and clinical research are needed to study the role of EAT and ANS in the pathogenesis of cardiovascular diseases.

Received 15 March 2021. Revised 25 April 2021. Accepted 26 April 2021.

Funding: The work is supported by a grant of the Russian Science Foundation (project No. 17-75-20118).

Conflict of interest: The authors declare no conflicts of interests.

Contribution of the authors
Conception and study design: D.V. Losik, N.A. Nikitin, S.M. Minin, A.B. Romanov, A.M. Chernyavskiy
Drafting the article: D.V. Losik, I.L. Mikheenko, E.V. Fisher, N.A. Nikitin
Critical revision of the article: D.V. Losik, I.L. Mikheenko, E.V. Fisher, N.A. Nikitin
Final approval of the version to be published: D.V. Losik, N.A. Nikitin, S.M. Minin, E.V. Fisher, I.L. Mikheenko, A.M. Chernyavskiy, A.B. Romanov

PDF (Русский)

References

  1. Kirchhof P., Benussi S., Kotecha D., Ahlsson A., Atar D., Casadei B., Castella M., Diener H.-C., Heidbuchel H., Hendriks J., Hindricks G., Manolis A.S., Oldgren J., Popescu B.A., Schotten U., Van Putte B., Vardas P., ESC Scientific Document Group. 2016 ESC Guidelines for the management of atrial fibrillation developed in collaboration with EACTS. Eur Heart J. 2016;37(38):2893-2962. PMID: 27567408. https://doi.org/10.1093/eurheartj/ehw210
  2. Лосик Д.В., Романов А.Б., Шабанов В.В., Байрамова С.А., Якубов А.А., Стенин И.Г., Покушалов Е.А. Прогрессирование фибрилляции предсердий после неэффективной первичной процедуры радиочастотной изоляции легочных вен: рандомизированное сравнение повторной катетерной аблации и медикаментозного метода лечения. Патология кровообращения и кардиохирургия. 2015;19(2):84-92. [Losik D.V., Romanov A.B., Shabanov V.V., Bairamova S.A., Yakubov A.A., Stenin I.G., Pokushalov Ye.A. Progression of atrial fibrillation after a failed initial ablation procedure in patients with paroxysmal atrial fibrillation: a randomized comparison of antiarrhythmic drug therapy vs re-ablation. Patologiya krovoobrashcheniya i kardiokhirurgiya = Circulation Pathology and Cardiac Surgery. 2015;19(2):84-92. (In Russ.)] http://doi.org/10.21688/1681-3472-2015-2-84-92
  3. Sacks H.S., Fain J.N. Human epicardial adipose tissue: a review. Am Heart J. 2007;153(6):907-917. PMID: 17540190. https://doi.org/10.1016/j.ahj.2007.03.019
  4. Iacobellis G. Local and systemic effects of the multifaceted epicardial adipose tissue depot. Nat Rev Endocrinol. 2015;11(6):363-371. PMID: 25850659. https://doi.org/10.1038/nrendo.2015.58
  5. Hatem S.N., Sanders P. Epicardial adipose tissue and atrial fibrillation. Cardiovasc Res. 2014;102(2):205-213. PMID: 24648445. https://doi.org/10.1093/cvr/cvu045
  6. Batal O., Schoenhagen P., Shao M., Ayyad A.E., Van Wagoner D.R., Halliburton S.S., Tchou P.J., Chung M.K. Left atrial epicardial adiposity and atrial fibrillation. Circ Arrhythm Electrophysiol. 2010;3(3):230-236. PMID: 20504944; PMCID: PMC2974566. https://doi.org/10.1161/CIRCEP.110.957241
  7. Thanassoulis G., Massaro J.M., O'Donnell C.J., Hoffmann U., Levy D., Ellinor P.T., Wang T.J., Schnabel R.B., Vasan R.S., Fox C.S., Benjamin E.J. Pericardial fat is associated with prevalent atrial fibrillation: the Framingham Heart Study. Circ Arrhythm Electrophysiol. 2010;3(4):345-350. PMID: 20558845; PMCID: PMC2953855. https://doi.org/10.1161/CIRCEP.109.912055
  8. Wong C.X., Abed H.S., Molaee P., Nelson A.J., Brooks A.G., Sharma G., Leong D.P., Lau D.H., Middeldorp M.E., Roberts-Thomson K.C., Wittert G.A., Abhayaratna W.P., Worthley S.G., Sanders P. Pericardial fat is associated with atrial fibrillation severity and ablation outcome. J Am Coll Cardiol. 2011; 57(17):1745-1751. PMID: 21511110. https://doi.org/10.1016/j.jacc.2010.11.045
  9. Venteclef N., Guglielmi V., Balse E., Gaborit B., Cotillard A., Atassi F., Amour J., Leprince P., Dutour A., Clément K., Hatem S.N. Human epicardial adipose tissue induces fibrosis of the atrial myocardium through the secretion of adipo-fibrokines. Eur Heart J. 2015;36(13):795-805a. PMID: 23525094. https://doi.org/10.1093/eurheartj/eht099
  10. Mahajan R., Nelson A., Pathak R.K., Middeldorp M.E., Wong C.X., Twomey D.J., Carbone A., Teo K., Agbaedeng T., Linz D., de Groot J.R., Kalman J.M., Lau D.H., Sanders P. Electroanatomical remodeling of the atria in obesity: impact of adjacent epicardial fat. JACC Clin Electrophysiol. 2018;4(12):1529-1540. PMID: 30573116. https://doi.org/10.1016/j.jacep.2018.08.014
  11. Iwasaki Y.-K., Kato T., Xiong F., Shi Y.-F., Naud P., Maguy A., Mizuno K., Tardif J.-C., Comtois P., Nattel S. Atrial fibrillation promotion with long-term repetitive obstructive sleep apnea in a rat model. J Am Coll Cardiol. 2014;64(19):2013-2023. PMID: 25440097. https://doi.org/10.1016/j.jacc.2014.05.077
  12. Shen M.J., Choi E.-K., Tan A.Y., Lin S.-F., Fishbein M.C., Chen L.S., Chen P.-S. Neural mechanisms of atrial arrhythmias. Nat Rev Cardiol. 2011;9(1):30-39. PMID: 21946776. https://doi.org/10.1038/nrcardio.2011.139
  13. Kimura K., Ieda M., Fukuda K. Development, maturation, and transdifferentiation of cardiac sympathetic nerves. Circ Res. 2012;110(2):325-336. PMID: 22267838. https://doi.org/10.1161/CIRCRESAHA.111.257253
  14. Romanov A., Pokushalov E., Ponomarev D., Bayramova S., Shabanov V., Losik D., Stenin I., Elesin D., Mikheenko I., Strelnikov A., Sergeevichev D., Kozlov B., Po S.S., Steinberg J.S. Long-term suppression of atrial fibrillation by botulinum toxin injection into epicardial fat pads in patients undergoing cardiac surgery: Three-year follow-up of a randomized study. Heart Rhythm. 2019;16(2):172-177. PMID: 30414841. https://doi.org/10.1016/j.hrthm.2018.08.019
  15. Minin S.M., Nikitin N.A., Shabanov V.V., Losik D.V., Mikheenko I.L., Ponomarev D.N., Pokushalov E.A., Romanov A.B. Evaluation of CZT SPECT imaging for cardiac sympathetic innervation in healthy individuals and patients with atrial fibrillation. Russian Open Medical Journal. 2018;7(3):e0308. https://doi.org/10.15275/rusomj.2018.0308
  16. Nikitin N., Minin S., Romanov A., Shabanov V., Losik D., Elesin D., Stenin I., Mikheenko I., Baavour R., Pokushalov E. Hybrid 123I-mIBG SPECT/CT cardiac imaging for identification of left atrial ganglionated plexi in healthy individuals and patients with atrial fibrillation. Eur Heart J Cardiovasc Imaging. 2019;20(Suppl_3):jez15. https://doi.org/10.1093/ehjci/jez150
  17. Maan A., Mansour M., Ruskin J.N., Heist E.K. Role of epicardial fat in atrial fibrillation pathophysiology and clinical implications. J Innov Card Rhythm Manag. 2013;4:1077-1082. Available from: https://www.innovationsincrm.com/cardiac-rhythm-management/2013/january/387-epicardial-fat-atrial-fibrillation-pathophysiology
  18. Dukkipati S.R., Koruth J.S., Choudry S., Miller M.A., Whang W., Reddy V.Y. Catheter ablation of ventricular tachycardia in structural heart disease: indications, strategies, and outcomes — Part II. J Am Coll Cardiol. 2017;70(23):2924-2941. PMID: 29216988. https://doi.org/10.1016/j.jacc.2017.10.030
  19. Chistiakov D.A., Grechko A.V., Myasoedova V.A., Melnichenko A.A., Orekhov A.N. Impact of the cardiovascular system-associated adipose tissue on atherosclerotic pathology. Atherosclerosis. 2017;263:361-368. PMID: 28629772. https://doi.org/10.1016/j.atherosclerosis.2017.06.017
  20. Sepehri Shamloo A., Schoene K., Stauber A., Darma A., Dagres N., Dinov B., Bertagnolli L., Hilbert S., Müssigbrodt A., Husser D., Bollmann A., Hindricks G., Arya A. Epicardial adipose tissue thickness as an independent predictor of ventricular tachycardia recurrence following ablation. Heart Rhythm. 2019;16(10):1492-1498. PMID: 31202898. https://doi.org/10.1016/j.hrthm.2019.06.009
  21. Kanat S., Duran Karaduman B., Tütüncü A., Tenekecioğlu E., Mutluer F.O., Akar Bayram N. Effect of echocardiographic epicardial adipose tissue thickness on success rates of premature ventricular contraction ablation. Balkan Med J. 2019;36(6):324-330. PMID: 31347351; PMCID: PMC6835166. https://doi.org/10.4274/balkanmedj.galenos.2019.2019.4.88
  22. Rajendran P.S., Nakamura K., Ajijola O.A., Vaseghi M., Armour J.A., Ardell J.L., Shivkumar K. Myocardial infarction induces structural and functional remodelling of the intrinsic cardiac nervous system. J Physiol. 2016;594(2):321-341. PMID: 26572244; PMCID: PMC4713729. https://doi.org/10.1113/JP271165
  23. Ajijola O.A., Lux R.L., Khahera A., Kwon O., Aliotta E., Ennis D.B., Fishbein M.C., Ardell J.L., Shivkumar K. Sympathetic modulation of electrical activation in normal and infarcted myocardium: implications for arrhythmogenesis. Am J Physiol Heart Circ Physiol. 2017;312(3):H608-H621. PMID: 28087519; PMCID: PMC5402014. https://doi.org/10.1152/ajpheart.00575.2016
  24. Wu Ch.-K., Tsai H.-Y., Su M.-Y.M., Wu Y.-F., Hwang J.-J., Tseng W.-Y., Lin J.-L., Lin L.-Y. Pericardial fat is associated with ventricular tachyarrhythmia and mortality in patients with systolic heart failure. Atherosclerosis. 2015;241(2):607-614. PMID: 26116961. https://doi.org/10.1016/j.atherosclerosis.2015.05.025
  25. Doesch C., Haghi D., Flüchter S., Suselbeck T., Schoenberg S.O., Michaely H., Borggrefe M., Papavassiliu T. Epicardial adipose tissue in patients with heart failure. J Cardiovasc Magn Reson. 2010;12(1):40. PMID: 20624277; PMCID: PMC2914772. https://doi.org/10.1186/1532-429X-12-40
  26. van Woerden G., Gorter T.M., Westenbrink B.D., Willems T.P., van Veldhuisen D.J., Rienstra M. Epicardial fat in heart failure patients with mid-range and preserved ejection fraction. Eur J Heart Fail. 2018;20(11):1559-1566. PMID: 30070041; PMCID: PMC6607508. https://doi.org/10.1002/ejhf.1283
  27. Marrouche N.F., Brachmann J., Andresen D., Siebels J., Boersma L., Jordaens L., Merkely B., Pokushalov E., Sanders P., Proff J., Schunkert H., Christ H., Vogt J., Bänsch D., CASTLE-AF Investigators. Catheter ablation for atrial fibrillation with heart failure. N Engl J Med. 2018;378(5):417-427. PMID: 29385358. https://doi.org/10.1056/NEJMoa1707855