Vol. 27 No. 4 (2023)
EXPERIMENTAL STUDIES

The impact of spinal cord stimulation on a chronic model of atrial fibrillation in a mini-pig experiment

pdf (Русский)
  • V.V. Shabanov,
  • A.G. Filippenko,
  • V.V. Beloborodov,
  • T.U. Khalkhoghaev,
  • V.I. Murtazin
V.V. Shabanov
Meshalkin National Medical Research Center, Ministry of Health of Russian Federation, Novosibirsk
A.G. Filippenko
Meshalkin National Medical Research Center, Ministry of Health of Russian Federation, Novosibirsk
Bio
V.V. Beloborodov
Meshalkin National Medical Research Center, Ministry of Health of Russian Federation, Novosibirsk
T.U. Khalkhoghaev
Meshalkin National Medical Research Center, Ministry of Health of Russian Federation, Novosibirsk
V.I. Murtazin
Meshalkin National Medical Research Center, Ministry of Health of Russian Federation, Novosibirsk
Study design
DOI: https://doi.org/10.21688/1681-3472-2023-4-43-51

Published 2023-12-26

Keywords

  • Animal Experimentation,
  • Arrhythmias, Cardiac,
  • Atrial Fibrillation,
  • Autonomic Nervous System,
  • Catheter Ablation,
  • Spinal Cord Stimulation,
  • Swine, Miniature
    • ...More
    Less

How to Cite

Shabanov, V., Filippenko, A., Beloborodov, V., Khalkhoghaev, T., & Murtazin, V. (2023). The impact of spinal cord stimulation on a chronic model of atrial fibrillation in a mini-pig experiment. Patologiya Krovoobrashcheniya I Kardiokhirurgiya, 27(4), 43–51. https://doi.org/10.21688/1681-3472-2023-4-43-51

Copyright (c) 2023 Shabanov V.V., Filippenko A.G., Beloborodov V.V., Khalkhoghaev T.U., Murtazin V.I.

Creative Commons License

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

Abstract

Introduction: Despite the advancement interventional methods for treating atrial fibrillation, the effectiveness of catheter ablation remains poor, especially in patients with persistent and long-persistent atrial fibrillation. Thus, experts continue to explore new treatments for this arrhythmia. The issue of experimental studies investigating the association between spinal cord stimulation and atrial fibrillation is mainly attributed to the lack of optimal algorithms for spinal cord stimulation in animal experiments. Therefore, it is important to develop adequate algorithms for spinal cord stimulation in the chronic model of atrial fibrillation.
Objective: To evaluate the impact of spinal cord stimulation on the model of atrial fibrillation in mini-pigs.
Methods: In a series of experiments, 6 (100%) successful implantations of electrodes and pacemakers, and spinal cord stimulation electrodes were performed. The electrodes were used to stimulate the atria, creating a model of atrial fibrillation, while the spinal cord stimulation was carried out using an electrode implanted into the spinal canal. During the experiment, an electrophysiological study was performed using an implanted pacemaker. The inducibility of atrial fibrillation was assessed before and after the experiment using various spinal cord stimulation algorithms.
Results: There were no complications associated with surgery or stimulation of the atria and spinal cord. Spinal stimulation had a modeling effect on the autonomic nervous system, significantly changing the average heart rate, Wenckebach point, and effective refractory period. When comparing spinal stimulation algorithms, algorithm 1 was found to significantly reduce the atrial fibrillation inducibility.
Conclusion: Spinal cord stimulation had a modeling effect on the autonomic nervous system, significantly changing the average heart rate, Wenckebach point, and effective refractory period. Inducibility of atrial fibrillation decreases with changes in the spinal pacing algorithm.

Received 15 September 2023. Revised 30 October 2023. Accepted 31 October 2023.

Funding: The study was supported by Russian Science Foundation (project No. 22-25-00672).

Conflict of interest: The authors declare no conflict of interest.

Contribution of the authors
Conception and study design: A.G. Filippenko, V.V. Shabanov, V.I. Murtazin
Data collection and analysis: A.G. Filippenko, T.U. Khalkhoghaev, V.V. Beloborodov
Statistical analysis: A.G. Filippenko, V.V. Shabanov
Drafting the article: A.G. Filippenko, V.V. Beloborodov
Critical revision of the article: V.V. Shabanov
Final approval of the version to be published: V.V. Shabanov, A.G. Filippenko, V.V. Beloborodov, T.U. Khalkhoghaev, V.I. Murtazin

pdf (Русский)

References

  1. Chugh S.S., Havmoeller R., Narayanan K., Singh D., Rienstra M., Benjamin E.J., Gillum R.F., Kim Y.-H., McAnulty J.H. Jr, Zheng Zh.-J., Forouzanfar M.H., Naghavi M., Mensah G.A., Ezzati M., Murray C.J.L. Worldwide epidemiology of atrial fibrillation: a Global Burden of Disease 2010 Study. Circulation. 2014;129(8):837-847. PMID: 24345399; PMCID: PMC4151302. https://doi.org/10.1161/CIRCULATIONAHA.113.005119
  2. Madhavan M., Hu T.Y., Gersh B.J., Roger V.L., Killian J., Weston S.A., Graff-Radford J., Asirvatham S.J., Chamberlain A.M. Efficacy of warfarin anticoagulation and incident dementia in a community-based cohort of atrial fibrillation. Mayo Clin Proc. 2018;93(2):145-154. PMID: 29329798; PMCID: PMC5814135. https://doi.org/10.1016/j.mayocp.2017.09.021
  3. Staerk L., Sherer J.A., Ko D., Benjamin E.J., Helm R.H. Atrial fibrillation: epidemiology, pathophysiology, and clinical outcomes. Circ Res. 2017;120(9):1501-1517. PMID: 28450367; PMCID: PMC5500874. https://doi.org/10.1161/CIRCRESAHA.117.309732
  4. Krijthe B.P., Kunst A., Benjamin E.J., Lip G.Y.H., Franco O.H., Hofman A., Witteman J.C.M., Stricker B.H., Heeringa J. Projections on the number of individuals with atrial fibrillation in the European Union, from 2000 to 2060. Eur Heart J. 2013;34(35):2746-2751. PMID: 23900699; PMCID: PMC3858024. https://doi.org/10.1093/eurheartj/eht280
  5. Patel N.J., Deshmukh A., Pant S., Singh V., Patel N., Arora Sh., Shah N., Chothani A., Savani G.T., Mehta K., Parikh V., Rathod A., Badheka A.O., Lafferty J., Kowalski M., Mehta J.L., Mitrani R.D., Viles-Gonzalez J.F., Paydak H. Contemporary trends of hospitalization for atrial fibrillation in the United States, 2000 through 2010: implications for healthcare planning. Circulation. 2014;129(23):2371-2379. PMID: 24842943. https://doi.org/10.1161/CIRCULATIONAHA.114.008201
  6. Serdechnaya E., Tatarsky B., Urieva S. Epidemiology. Atrial fibrillation in the Russian north. 25 years follow up. Europace Supplements. 2007;9(Suppl 3):iii22.
  7. Филатов А.Г., Тарашвили Э.Г. Эпидемиология и социальная значимость фибрилляции предсердий. Анналы аритмологии. 2012;9(2):5-13. Filatov A.G., Tarashvili E.G. Epidemiology and social significance of atrial fibrillation. Annaly arrhythmologii = Annals of Arrhythmology. 2012;9(2):5-13. (In Russ.)
  8. Olshansky B., Rosenfeld L.E., Warner A.L., Solomon A.J., O'Neill G., Sharma A., Platia E., Feld G.K., Akiyama T., Brodsky M.A., Greene H.L. The Atrial Fibrillation Follow-up Investigation of Rhythm Management (AFFIRM) study: approaches to control rate in atrial fibrillation. J Am Coll Cardiol. 2004;43(7):1201-1208. PMID: 15063430. https://doi.org/10.1016/j.jacc.2003.11.032
  9. Ganesan A.N., Shipp N.J., Brooks A.G., Kuklik P., Lau D.H., Lim H.S., Sullivan T., Roberts-Thomson K.C., Sanders P. Long‐term outcomes of catheter ablation of atrial fibrillation: a systematic review and meta‐analysis. J Am Heart Assoc. 2013;2(2):e004549. PMID: 23537812; PMCID: PMC3647286. https://doi.org/10.1161/JAHA.112.004549
  10. Packer D.L., Mark D.B., Robb R.A., Monahan K.H., Bahnson T.D., Moretz K., Poole J.E., Mascette A., Rosenberg Y., Jeffries N., Al-Khalidi H.R., Lee K.L.; CABANA Investigators. Catheter Ablation versus Antiarrhythmic Drug Therapy for Atrial Fibrillation (CABANA) trial: study rationale and design. Am Heart J. 2018;199:192-199. PMID: 29754661; PMCID: PMC6517320. https://doi.org/10.1016/j.ahj.2018.02.015
  11. Hindricks G., Potpara T., Dagres N., Arbelo E., Bax J.J., Blomström-Lundqvist C., Boriani G., Castella M., Dan G.-A., Dilaveris P.E., Fauchier L., Filippatos G., Kalman J.M., La Meir M., Lane D.A., Lebeau J.-P., Lettino M., Lip G.Y.H., Pinto F.J., Thomas G.N., Valgimigli M., Van Gelder I.C., Van Putte B.P., Watkins C.L., ESC Scientific Document Group. 2020 ESC Guidelines for the diagnosis and management of atrial fibrillation developed in collaboration with the European Association for Cardio-Thoracic Surgery (EACTS): The Task Force for the diagnosis and management of atrial fibrillation of the European Society of Cardiology (ESC) Developed with the special contribution of the European Heart Rhythm Association (EHRA) of the ESC. Eur Heart J. 2021;42(5):373-498. Erratum in: Eur Heart J. 2021;42(5):507; Eur Heart J. 2021;42(40):4194. PMID: 32860505. https://doi.org/10.1093/eurheartj/ehaa612
  12. Аракелян М.Г., Бокерия Л.А., Васильева Е.Ю., Голицын С.П., Голухова Е.З., Горев М.В., Давтян К.В., Драпкина О.М., Кропачева Е.С., Кучинская Е.А., Лайович Л.Ю., Миронов Н.Ю., Мишина И.Е., Панченко Е.П., Ревишвили А.Ш., Рзаев Ф.Г., Татарский Б.А., Уцумуева М.Д., Шахматова О.О., Шлевков Н.Б., Шпектор А.В., Андреев Д.А., Артюхина Е.А., Барбараш О.Л., Галявич А.С., Дупляков Д.В., Зенин С.А., Лебедев Д.С., Михайлов Е.Н., Новикова Н.А., Попов С.В., Филатов А.Г., Шляхто Е.В., Шубик Ю.В. Фибрилляция и трепетание предсердий. Клинические рекомендации 2020. Российский кардиологический журнал. 2021;26(7):4594. https://doi.org/10.15829/1560-4071-2021-4594 Arakelyan M.G., Bockeria L.A., Vasilyeva E.Yu., Golitsyn S.P., Golukhova E.Z., Gorev M.V., Davtyan K.V., Drapkina O.M., Kropacheva E.S., Kuchinskaya E.A., Layovich L.Yu., Miro­nov N.Yu., Mishina I.E., Panchenko E.P., Revishvili A.Sh., Rzaev F.G., Tatarsky B.A., Utsumueva M.D., Shakhmatova O.O., Shlevkov N.B., Shpektor A.V., Andreev D.A., Artyukhina E.A., Barbarash O.L., Galyavich A.S., Duplyakov D.V., Zenin S.A., Lebedev D.S., Mikhailov E.N., Novikova N.A., Popov S.V., Filatov A.G., Shlyakhto E.V., Shubik Yu.V. 2020 Clinical guidelines for Atrial fibrillation and atrial flutter. Rossiiskii kardiologicheskiyj jurnal = Russian Journal of Cardiology. 2021;26(7):4594. (In Russ.) https://doi.org/10.15829/1560-4071-2021-4594
  13. Hanna P., Buch E., Stavrakis S., Meyer C., Tompkins J.D., Ardell J.L., Shivkumar K. Neuroscientific therapies for atrial fibrillation. Cardiovasc Res. 2021;117(7):1732-1745. PMID: 33989382; PMCID: PMC8208752. https://doi.org/10.1093/cvr/cvab172
  14. Katritsis D.G., Pokushalov E., Romanov A., Giazitzoglou E., Siontis G.C.M., Po S.S., Camm A.J., Ioannidis J.P.A. Autonomic denervation added to pulmonary vein isolation for paroxysmal atrial fibrillation: a randomized clinical trial. J Am Coll Cardiol. 2013;62(24):2318-2325. PMID: 23973694. https://doi.org/10.1016/j.jacc.2013.06.053
  15. Driessen A.H.G., Berger W.R., Krul S.P.J., van den Berg N.W.E., Neefs J., Piersma F.R., Chan Pin Yin D.R.P.P., de Jong J.S.S.G., van Boven W.P., de Groot J.R. Ganglion Plexus Ablation in Advanced Atrial Fibrillation: The AFACT Study. J Am Coll Cardiol. 2016;68(11):1155-1165. PMID: 27609676. https://doi.org/10.1016/j.jacc.2016.06.036
  16. Yu L., Huang B., He W., Wang S., Liao K., Zhou X., He B., Lu Z., Jiang H. Spinal cord stimulation suppresses focal rapid firing-induced atrial fibrillation by inhibiting atrial ganglionated plexus activity. J Cardiovasc Pharmacol. 2014;64(6):554-559. PMID: 25165998. https://doi.org/10.1097/FJC.0000000000000154
  17. Лосик Д.В., Белобородов В.В., Фишер Е.В., Муртазин В.И., Филиппенко А.Г., Михеенко И.Л., Шабанов В.В., Романов А.Б. Новая эндокардиальная би-электродная стимуляция правого предсердия у мини-свиней для создания модели фибрилляции предсердий. Патология кровообращения и кардиохирургия. 2023;27(1):47-53. https://dx.doi.org/10.21688/1681-3472-2023-1-47-53 Losik D.V., Beloborodov V.V., Fisher E.V., Murtazin V.I., Filippenko A.G., Mikheenko I.L., Shabanov V.V., Romanov A.B. New atrial fibrillation model with endocardial approach by CRT bi-electrode atrial pacing in mini-pigs. Patologiya krovo­obrashcheniya i kardiokhirurgiya = Circulation Pathology and Cardiac Surgery. 2023;27(1):47-53. (In Russ.) https://dx.doi.org/10.21688/1681-3472-2023-1-47-53
  18. Chen J., Wasmund S.L., Hamdan M.H. Back to the future: the role of the autonomic nervous system in atrial fibrillation. Pacing Clin Electrophysiol. 2006;29(4):413-421. PMID: 16650271. https://doi.org/10.1111/j.1540-8159.2006.00362.x
  19. Augustinsson L.E., Carlsson C.A., Holm J., Jivegård L. Epidural electrical stimulation in severe limb ischemia. Pain relief, increased blood flow, and a possible limb-saving effect. Ann Surg. 1985;202(1):104-110. PMID: 3874610; PMCID: PMC1250845. https://doi.org/10.1097/00000658-198507000-00017
  20. Jacobs M.J., Jörning P.J., Beckers R.C., Ubbink D.T., van Kleef M., Slaaf D.W., Reneman R.S. Foot salvage and improvement of microvascular blood flow as a result of epidural spinal cord electrical stimulation. J Vasc Surg. 1990;12(3):354-360. PMID: 2398593.
  21. DeJongste M.J. Spinal cord stimulation for ischemic heart disease. Neurol Res. 2000;22(3):293-298. PMID: 10769823. https://doi.org/10.1080/01616412.2000.11740673
  22. Fanciullo G.J., Robb J.F., Rose R.J., Sanders J.H. Jr. Spinal cord stimulation for intractable angina pectoris. Anesth Analg. 1999;89(2):305-306. PMID: 10439736. https://doi.org/10.1097/00000539-199908000-00009
  23. Jessurun G.A., DeJongste M.J., Hautvast R.W., Tio R.A., Brouwer J., van Lelieveld S., Crijns H.J. Clinical follow-up after cessation of chronic electrical neuromodulation in patients with severe coronary artery disease: a prospective randomized controlled study on putative involvement of sympathetic activity. Pacing Clin Electrophysiol. 1999;22(10):1432-1439. PMID: 10588144. https://doi.org/10.1111/j.1540-8159.1999.tb00346.x
  24. Bernstein S.A., Wong B., Vasquez C., Rosenberg S.P., Rooke R., Kuznekoff L.M., Lader J.M., Mahoney V.M., Budylin T., Älvstrand M., Rakowski-Anderson T., Bharmi R., Shah R., Fow­ler S., Holmes D., Farazi T.G., Chinitz L.A., Morley G.E. Spinal cord stimulation protects against atrial fibrillation induced by tachypacing. Heart Rhythm. 2012;9(9):1426-1433.e3. PMID: 22554859; PMCID: PMC3634125. https://doi.org/10.1016/j.hrthm.2012.04.038
  25. Olgin J.E., Takahashi T., Wilson E., Vereckei A., Steinberg H., Zipes D.P. Effects of thoracic spinal cord stimulation on cardiac autonomic regulation of the sinus and atrioventricular nodes. J Cardiovasc Electrophysiol. 2002;13(5):475-481. PMID: 12030530. https://doi.org/10.1046/j.1540-8167.2002.00475.x
  26. Cardinal R., Pagé P., Vermeulen M., Bouchard C., Ardell J.L., Foreman R.D., Armour J.A. Spinal cord stimulation suppresses bradycardias and atrial tachyarrhythmias induced by mediastinal nerve stimulation in dogs. Am J Physiol Regul Integr Comp Physiol. 2006;291(5):R1369-R1375. PMID: 16778070. https://doi.org/10.1152/ajpregu.00056.2006