Autonomic responses during acute myocardial infarction in the rat model: implications for arrhythmogenesis
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Theofilos M. Kolettis
, Marianthi Kontonika
Abstract
Background
Autonomic responses participate in the pathophysiology of acute myocardial infarction, but their precise time course remains unclear. Here, we investigated the autonomic activity and ventricular tachyarrhythmias in conscious, unrestrained rats post-infarction.
Methods
The left coronary artery was ligated in 12 Wistar rats, and six rats were sham operated, followed by 24-h electrocardiographic recording via implanted telemetry transmitters. Sympathetic activity was assessed by detrended fluctuation analysis and vagal activity by time- and frequency-domain analysis of heart rate variability. The duration of the ventricular tachyarrhythmias was measured, and voluntary motion served as a marker of heart failure.
Results
In sham-operated rats, heart rate and sympathetic activity remained low, whereas vagal activity rose progressively after the fourth hour. Post-ligation, medium-sized antero-septal necrosis was observed, reaching ~20% of the left ventricular volume; tachyarrhythmias were frequent, displaying a bimodal curve, and motion counts were low. Vagal activity decreased early post-ligation, coinciding with a high incidence of tachyarrhythmias, but tended to rise subsequently in rats with higher motion counts. Sympathetic activity increased after the third hour, along with a second tachyarrhythmia peak, and remained elevated throughout the 24-h period.
Conclusions
Vagal withdrawal, followed by gradual sympathetic activation, may participate in arrhythmogenesis during acute myocardial infarction.
Acknowledgment
We thank Ms. Eleni Goga, BA, for coordinating this project.
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: This work was supported by the Cardiovascular Research Institute, Ioannina, Greece.
Employment or leadership: None declared.
Honorarium: None declared.
Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.
References
1. Kolettis TM. Coronary artery disease and ventricular tachyarrhythmia: pathophysiology and treatment. Curr Opin Pharmacol 2013;13:210–7.10.1016/j.coph.2013.01.001Search in Google Scholar
2. Kolettis TM. Ventricular tachyarrhythmias during acute myocardial infarction: the role of endothelin-1. Life Sci 2014;118:136–40.10.1016/j.lfs.2014.01.060Search in Google Scholar
3. Thoren PN. Activation of left ventricular receptors with nonmedullated vagal afferent fibers during occlusion of a coronary artery in the cat. Am J Cardiol 1976;37:1046–51.10.1016/0002-9149(76)90422-7Search in Google Scholar
4. Shen MJ, Zipes DP. Role of the autonomic nervous system in modulating cardiac arrhythmias. Circ Res 2014;114:1004–21.10.1161/CIRCRESAHA.113.302549Search in Google Scholar PubMed
5. Reyes del Paso GA, Langewitz W, Mulder LJ, van Roon A, Duschek S. The utility of low frequency heart rate variability as an index of sympathetic cardiac tone: a review with emphasis on a reanalysis of previous studies. Psychophysiology 2013;50:477–87.10.1111/psyp.12027Search in Google Scholar PubMed
6. Billman GE. The LF/HF ratio does not accurately measure cardiac sympatho-vagal balance. Front Physiol 2013;4:26.10.3389/fphys.2013.00026Search in Google Scholar PubMed PubMed Central
7. Franciosi S, Perry FK, Roston TM, Armstrong KR, Claydon VE, Sanatani S. The role of the autonomic nervous system in arrhythmias and sudden cardiac death. Auton Neurosci 2017;205:1–11.10.1016/j.autneu.2017.03.005Search in Google Scholar PubMed
8. Huikuri HV, Makikallio TH, Peng CK, Goldberger AL, Hintze U, Moller M. Fractal correlation properties of R-R interval dynamics and mortality in patients with depressed left ventricular function after an acute myocardial infarction. Circulation 2000;101:47–53.10.1161/01.CIR.101.1.47Search in Google Scholar PubMed
9. Laborde S, Mosley E, Thayer JF. Heart rate variability and cardiac vagal tone in psychophysiological research – recommendations for experiment planning, data analysis, and data reporting. Front Psychol 2017;8:213.10.3389/fpsyg.2017.00213Search in Google Scholar PubMed PubMed Central
10. Ytrehus K, Liu Y, Tsuchida A, Miura T, Liu GS, Yang XM, et al. Rat and rabbit heart infarction: effects of anesthesia, perfusate, risk zone, and method of infarct sizing. Am J Physiol 1994;267:H2383–90.10.1152/ajpheart.1994.267.6.H2383Search in Google Scholar PubMed
11. Minicucci MF, Azevedo PS, Duarte DR, Matsubara BB, Matsubara LS, Campana AO, et al. Comparison of different methods to measure experimental chronic infarction size in the rat model. Arq Bras Cardiol 2007;89:83–7.10.1590/S0066-782X2007001400004Search in Google Scholar
12. Howarth FC, Jacobson M, Shafiullah M, Adeghate E. Effects of insulin treatment on heart rhythm, body temperature and physical activity in streptozotocin-induced diabetic rat. Clin Exp Pharmacol Physiol 2006;33:327–31.10.1111/j.1440-1681.2006.04370.xSearch in Google Scholar PubMed
13. Jardine DL, Charles CJ, Ashton RK, Bennett SI, Whitehead M, Frampton CM, et al. Increased cardiac sympathetic nerve activity following acute myocardial infarction in a sheep model. J Physiol 2005;565:325–33.10.1113/jphysiol.2004.082198Search in Google Scholar PubMed PubMed Central
14. Kolettis TM, Kontonika M, Barka E, Daskalopoulos EP, Baltogiannis GG, Tourmousoglou C, et al. Central sympathetic activation and arrhythmogenesis during acute myocardial infarction: modulating effects of endothelin-B receptors. Front Cardiovasc Med 2015;2:6.10.3389/fcvm.2015.00006Search in Google Scholar PubMed PubMed Central
15. Yu L, Wang M, Hu D, Huang B, Zhou L, Zhou X, et al. Blocking the Nav1.8 channel in the left stellate ganglion suppresses ventricular arrhythmia induced by acute ischemia in a canine model. Sci Rep 2017;7:534.10.1038/s41598-017-00642-6Search in Google Scholar PubMed PubMed Central
16. Kolettis TM. Ventricular arrhythmias during acute ischemia/infarction: mechanisms and management. In: Kibos AS, Knight BP, Essebag V, Fishberger SB, Slevin M, Tintoiu IC, editors. Cardiac arrhythmias: from basic mechanism to state-of-the-art management. London: Springer-Verlag, 2014:237–51.10.1007/978-1-4471-5316-0_18Search in Google Scholar
17. Zhou S, Jung BC, Tan AY, Trang VQ, Gholmieh G, Han SW, et al. Spontaneous stellate ganglion nerve activity and ventricular arrhythmia in a canine model of sudden death. Heart Rhythm 2008;5:131–9.10.1016/j.hrthm.2007.09.007Search in Google Scholar PubMed
18. Opthof T, Coronel R, Vermeulen JT, Verberne HJ, van Capelle FJ, Janse MJ. Dispersion of refractoriness in normal and ischaemic canine ventricle: effects of sympathetic stimulation. Cardiovasc Res 1993;27:1954–60.10.1093/cvr/27.11.1954Search in Google Scholar PubMed
19. Kolettis TM, Kontonika M, La Rocca V, Vlahos AP, Baltogiannis GG, Kyriakides ZS. Local conduction during acute myocardial infarction in rats: interplay between central sympathetic activation and endothelin. J Arrhythm 2017;33:144–6.10.1016/j.joa.2016.07.010Search in Google Scholar PubMed PubMed Central
20. Kolettis TM, Kontonika M, Valenti MC, Vilaeti AD, Baltogiannis GG, Papalois A, et al. Arrhythmogenesis after acute myocardial necrosis with and without preceding ischemia in rats. J Basic Clin Physiol Pharmacol 2014;25:143–53.10.1515/jbcpp-2013-0117Search in Google Scholar PubMed
21. McAreavey D, Neilson JM, Ewing DJ, Russell DC. Cardiac parasympathetic activity during the early hours of acute myocardial infarction. Br Heart J 1989;62:165–70.10.1136/hrt.62.3.165Search in Google Scholar PubMed PubMed Central
22. Chrousos GP. Stress and disorders of the stress system. Nat Rev Endocrinol 2009;5:374–81.10.1038/nrendo.2009.106Search in Google Scholar PubMed
23. Taggart P, Critchley H, Lambiase PD. Heart-brain interactions in cardiac arrhythmia. Heart 2011;97:698–708.10.1136/hrt.2010.209304Search in Google Scholar PubMed
24. Kochiadakis GE, Marketou ME, Igoumenidis NE, Simantirakis EN, Parthenakis FI, Manios EG, et al. Autonomic nervous system activity before and during episodes of myocardial ischemia in patients with stable coronary artery disease during daily life. Pacing Clin Electrophysiol 2000;23:2030–9.10.1111/j.1540-8159.2000.tb00772.xSearch in Google Scholar PubMed
25. Buchholz B, Donato M, Perez V, Ivalde FC, Hocht C, Buitrago E, et al. Preischemic efferent vagal stimulation increases the size of myocardial infarction in rabbits. Role of the sympathetic nervous system. Int J Cardiol 2012;155:490–1.10.1016/j.ijcard.2011.12.082Search in Google Scholar PubMed
26. Raya TE, Gay RG, Lancaster L, Aguirre M, Moffett C, Goldman S. Serial changes in left ventricular relaxation and chamber stiffness after large myocardial infarction in rats. Circulation 1988;77:1424–31.10.1161/01.CIR.77.6.1424Search in Google Scholar PubMed
27. Hohnloser SH, Kuck KH, Dorian P, Roberts RS, Hampton JR, Hatala R, et al. Prophylactic use of an implantable cardioverter-defibrillator after acute myocardial infarction. N Engl J Med 2004;351:2481–8.10.1056/NEJMoa041489Search in Google Scholar PubMed
28. Li M, Zheng C, Sato T, Kawada T, Sugimachi M, Sunagawa K. Vagal nerve stimulation markedly improves long-term survival after chronic heart failure in rats. Circulation 2004;109:120–4.10.1161/01.CIR.0000105721.71640.DASearch in Google Scholar PubMed
29. Opitz CF, Mitchell GF, Pfeffer MA, Pfeffer JM. Arrhythmias and death after coronary artery occlusion in the rat. Continuous telemetric ECG monitoring in conscious, untethered rats. Circulation 1995;92:253–61.10.1161/01.CIR.92.2.253Search in Google Scholar PubMed
30. Tulppo MP, Kiviniemi AM, Hautala AJ, Kallio M, Seppanen T, Makikallio TH, et al. Physiological background of the loss of fractal heart rate dynamics. Circulation 2005;112:314–9.10.1161/CIRCULATIONAHA.104.523712Search in Google Scholar PubMed
©2018 Walter de Gruyter GmbH, Berlin/Boston
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- Comparative hypoglycemic potentials and phytochemical profiles of 12 common leafy culinary vegetables consumed in Nsukka, Southeastern Nigeria
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- The effects of oral pregabalin on post-Lichtenstein herniorrhaphic pain: a randomized clinical trial
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- Influence of age and gender on blood pressure variability and baroreflex sensitivity in a healthy population in the Indian sub-continent
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- Phytotherapy
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- Hematology and erythrocyte osmotic fragility of the Franquet’s fruit bat (Epomops franqueti)
- Behavior and Neuroprotection
- Haloperidol-induced parkinsonism is attenuated by varenicline in mice
- Antioxidant-mediated neuroprotection by Allium schoenoprasum L. leaf extract against ischemia reperfusion-induced cerebral injury in mice
- Effects of acetone extract of Cola nitida on brain sodium-potassium adenosine triphosphatase activity and spatial memory in healthy and streptozotocin-induced diabetic female Wistar rats
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Articles in the same Issue
- Frontmatter
- Letter to the Editor
- Blister-packed levothyroxine sodium or bottle-packed levothyroxine sodium
- Metabolism
- Comparative hypoglycemic potentials and phytochemical profiles of 12 common leafy culinary vegetables consumed in Nsukka, Southeastern Nigeria
- Infection
- The effects of oral pregabalin on post-Lichtenstein herniorrhaphic pain: a randomized clinical trial
- Cardiovascular Function
- Influence of age and gender on blood pressure variability and baroreflex sensitivity in a healthy population in the Indian sub-continent
- Autonomic responses during acute myocardial infarction in the rat model: implications for arrhythmogenesis
- Phytotherapy
- Role of reactive oxygen species–total antioxidant capacity status in Telfairia occidentalis leaves–associated spermatoprotective effect: a pointer to fatty acids benefit
- Antidiabetic and renoprotective effect of Anogeissus acuminata leaf extract on experimentally induced diabetic nephropathy
- Oxidative Stress
- Aged coconut oil with a high peroxide value induces oxidative stress and tissue damage in mercury-treated rats
- Anti-ulcerogenic effect of the methanol extract of Chasmanthera dependens (Hochst) stem on male Wistar rats
- Hematological Profile
- Evaluation of hematological alterations after therapeutic use of dipyrone in healthy adults: a prospective study
- Hematology and erythrocyte osmotic fragility of the Franquet’s fruit bat (Epomops franqueti)
- Behavior and Neuroprotection
- Haloperidol-induced parkinsonism is attenuated by varenicline in mice
- Antioxidant-mediated neuroprotection by Allium schoenoprasum L. leaf extract against ischemia reperfusion-induced cerebral injury in mice
- Effects of acetone extract of Cola nitida on brain sodium-potassium adenosine triphosphatase activity and spatial memory in healthy and streptozotocin-induced diabetic female Wistar rats
- Case Report
- Conservative treatment of postoperative chylothorax: a case report
- Short Communication
- Improved serotonergic neurotransmission by genistein pretreatment regulates symptoms of obsessive-compulsive disorder in streptozotocin-induced diabetic mice