The role of low-level vagus nerve stimulation in cardiac therapy

References

• Lanska DJ.  J.L. Corning and vagal nerve stimulation for seizures in the 1880s. Neurology. 2002;58(3):452–459.
   PubMed Web of Science ®Google Scholar
• Morris GL 3rd, Gloss D, Buchhalter J, et al. Evidence-based guideline update: vagus nerve stimulation for the treatment of epilepsy: report of the Guideline Development Subcommittee of the American Academy of Neurology. Neurology. 2013;81(16):1453–1459.
   PubMed Web of Science ®Google Scholar
• Howland RH. Vagus nerve stimulation. Curr Behav Neurosci Rep. 2014;1(2):64–73.
   PubMedGoogle Scholar
• Goldberger AL, Pavelec RS. Vagally-mediated atrial fibrillation in dogs: conversion with bretylium tosylate. Int J Cardiol. 1986;13(1):47–55.
   PubMed Web of Science ®Google Scholar
• Wang Z, Page P, Nattel S. Mechanism of flecainide’s antiarrhythmic action in experimental atrial fibrillation. Circ Res. 1992;71(2):271–287.
   PubMed Web of Science ®Google Scholar
• Li S, Scherlag BJ, Yu L, et al. Low-level vagosympathetic stimulation: a paradox and potential new modality for the treatment of focal atrial fibrillation. Circ Arrhythm Electrophysiol. 2009;2(6):645–651.
   PubMed Web of Science ®Google Scholar
• Murray AR, Atkinson L, Mahadi MK, et al. The strange case of the ear and the heart: the auricular vagus nerve and its influence on cardiac control. Auton Neurosci. 2016;199:48–53.
   PubMed Web of Science ®Google Scholar
• Li YF, Jackson KL, Stern JE, et al. Interaction between glutamate and GABA systems in the integration of sympathetic outflow by the paraventricular nucleus of the hypothalamus. Am J Physiol Heart Circ Physiol. 2006;291(6):H2847–2856.
   PubMed Web of Science ®Google Scholar
• Zheng H, Liu X, Li Y, et al. Gene transfer of neuronal nitric oxide synthase to the paraventricular nucleus reduces the enhanced glutamatergic tone in rats with chronic heart failure. Hypertension. 2011;58(5):966–973.
   PubMed Web of Science ®Google Scholar
• Ardell JL. The cardiac neuronal hierarchy and susceptibility to arrhythmias. Heart Rhythm. 2011;8(4):590–591.
   PubMed Web of Science ®Google Scholar
• Armour JA. Cardiac neuronal hierarchy in health and disease. Am J Physiol Regul Integr Comp Physiol. 2004;287(2):R262–271.
   PubMed Web of Science ®Google Scholar
• Armour JA, Murphy DA, Yuan BX, et al. Gross and microscopic anatomy of the human intrinsic cardiac nervous system. Anat Rec. 1997;247(2):289–298.
   PubMedGoogle Scholar
• Janes RD, Brandys JC, Hopkins DA, et al. Anatomy of human extrinsic cardiac nerves and ganglia. Am J Cardiol. 1986;57(4):299–309.
   PubMed Web of Science ®Google Scholar
• Kawashima T. The autonomic nervous system of the human heart with special reference to its origin, course, and peripheral distribution. Anat Embryol (Berl). 2005;209(6):425–438.
   PubMedGoogle Scholar
• Po SS, Yu L, Scherlag BJ. Cardiac autonomic nervous system: a tug of war between the big brain and little brain–friends or foes? Heart Rhythm. 2009;6(12):1780–1781.
   PubMed Web of Science ®Google Scholar
• Clancy JA, Mary DA, Witte KK, et al. Non-invasive vagus nerve stimulation in healthy humans reduces sympathetic nerve activity. Brain Stimul. 2014;7(6):871–877.
   PubMed Web of Science ®Google Scholar
• Nomura S, Mizuno N. Central distribution of primary afferent fibers in the Arnold’s nerve (the auricular branch of the vagus nerve): a transganglionic HRP study in the cat. Brain Res. 1984;292(2):199–205.
   PubMed Web of Science ®Google Scholar
• Yu L, Scherlag BJ, Li S, et al. Low-level vagosympathetic nerve stimulation inhibits atrial fibrillation inducibility: direct evidence by neural recordings from intrinsic cardiac ganglia. J Cardiovasc Electrophysiol. 2011;22(4):455–463.
   PubMed Web of Science ®Google Scholar
• Shen MJ, Shinohara T, Park HW, et al. Continuous low-level vagus nerve stimulation reduces stellate ganglion nerve activity and paroxysmal atrial tachyarrhythmias in ambulatory canines. Circulation. 2011;123(20):2204–2212.
   PubMed Web of Science ®Google Scholar
• Sha Y, Scherlag BJ, Yu L, et al. Low-level right vagal stimulation: anticholinergic and antiadrenergic effects. J Cardiovasc Electrophysiol. 2011;22(10):1147–1153.
   PubMed Web of Science ®Google Scholar
• Lu Y, Sun J, Zhou X, et al. Effect of low-level vagus nerve stimulation on cardiac remodeling in a rapid atrial pacing-induced canine model of atrial fibrillation. J Cardiovasc Pharmacol. 2016;67(3):218–224.
   PubMed Web of Science ®Google Scholar
• Sheng X, Scherlag BJ, Yu L, et al. Prevention and reversal of atrial fibrillation inducibility and autonomic remodeling by low-level vagosympathetic nerve stimulation. J Am Coll Cardiol. 2011;57(5):563–571.
   PubMed Web of Science ®Google Scholar
• Yu L, Scherlag BJ, Sha Y, et al. Interactions between atrial electrical remodeling and autonomic remodeling: how to break the vicious cycle. Heart Rhythm. 2012;9(5):804–809.
   PubMed Web of Science ®Google Scholar
• Yu L, Scherlag BJ, Li S, et al. Low-level transcutaneous electrical stimulation of the auricular branch of the vagus nerve: a noninvasive approach to treat the initial phase of atrial fibrillation. Heart Rhythm. 2013;10(3):428–435.
   PubMed Web of Science ®Google Scholar
• Chen M, Zhou X, Liu Q, et al. Left-sided noninvasive vagus nerve stimulation suppresses atrial fibrillation by upregulating atrial gap junctions in canines. J Cardiovasc Pharmacol. 2015;66(6):593–599.
   PubMed Web of Science ®Google Scholar
• Yu L, Li X, Huang B, et al. Atrial fibrillation in acute obstructive sleep apnea: autonomic nervous mechanism and modulation. J Am Heart Assoc. 2017;6:9.
   Web of Science ®Google Scholar
• Stavrakis S, Humphrey MB, Scherlag BJ, et al. Low-level transcutaneous electrical vagus nerve stimulation suppresses atrial fibrillation. J Am Coll Cardiol. 2015;65(9):867–875.
   PubMed Web of Science ®Google Scholar
• Stavrakis S, Humphrey MB, Scherlag B, et al. Low-level vagus nerve stimulation suppresses post-operative atrial fibrillation and inflammation: a randomized study. JACC Clin Electrophysiol. 2017;3(9):929–938.
   PubMedGoogle Scholar
• Amar D, Zhang H, Miodownik S, et al. Competing autonomic mechanisms precede the onset of postoperative atrial fibrillation. J Am Coll Cardiol. 2003;42(7):1262–1268.
   PubMed Web of Science ®Google Scholar
• Bettoni M, Zimmermann M. Autonomic tone variations before the onset of paroxysmal atrial fibrillation. Circulation. 2002;105(23):2753–2759.
   PubMed Web of Science ®Google Scholar
• Patterson E, Lazzara R, Szabo B, et al. Sodium-calcium exchange initiated by the Ca2+ transient: an arrhythmia trigger within pulmonary veins. J Am Coll Cardiol. 2006;47(6):1196–1206.
   PubMed Web of Science ®Google Scholar
• Patterson E, Po SS, Scherlag BJ, et al. Triggered firing in pulmonary veins initiated by in vitro autonomic nerve stimulation. Heart Rhythm. 2005;2(6):624–631.
   PubMed Web of Science ®Google Scholar
• Martins JB, Zipes DP. Effects of sympathetic and vagal nerves on recovery properties of the endocardium and epicardium of the canine left ventricle. Circ Res. 1980;46(1):100–110.
   PubMed Web of Science ®Google Scholar
• Ng GA, Brack KE, Coote JH. Effects of direct sympathetic and vagus nerve stimulation on the physiology of the whole heart–a novel model of isolated Langendorff perfused rabbit heart with intact dual autonomic innervation. Exp Physiol. 2001;86(3):319–329.
   PubMed Web of Science ®Google Scholar
• Ng GA, Brack KE, Patel VH, et al. Autonomic modulation of electrical restitution, alternans and ventricular fibrillation initiation in the isolated heart. Cardiovasc Res. 2007;73(4):750–760.
   PubMed Web of Science ®Google Scholar
• Yanowitz F, Preston JB, Abildskov JA. Functional distribution of right and left stellate innervation to the ventricles. Production of neurogenic electrocardiographic changes by unilateral alteration of sympathetic tone. Circ Res. 1966;18(4):416–428.
   PubMed Web of Science ®Google Scholar
• Einbrodt PP. Ueber Herzreizung und ihr Verhaeltnis zum Blutdruck. Akademie der Wissenschaften (Vienna) Sitzungsberichte. 1859;38:345.
   Google Scholar
• Myers RW, Pearlman AS, Hyman RM, et al. Beneficial effects of vagal stimulation and bradycardia during experimental acute myocardial ischemia. Circulation. 1974;49(5):943–947.
   PubMed Web of Science ®Google Scholar
• Goldstein RE, Karsh RB, Smith ER, et al. Influence of atropine and of vagally mediated bradycardia on the occurrence of ventricular arrhythmias following acute coronary occlusion in closed-chest dogs. Circulation. 1973;47(6):1180–1190.
   PubMed Web of Science ®Google Scholar
• Kent KM, Smith ER, Redwood DR, et al. Electrical stability of acutely ischemic myocardium. Influences of heart rate and vagal stimulation. Circulation. 1973;47(2):291–298.
   PubMed Web of Science ®Google Scholar
• Kerzner J, Wolf M, Kosowsky BD, et al. Ventricular ectopic rhythms following vagal stimulation in dogs with acute myocardial infarction. Circulation. 1973;47(1):44–50.
   PubMed Web of Science ®Google Scholar
• Scherlag BJ, Helfant RH, Haft JI, et al. Electrophysiology underlying ventricular arrhythmias due to coronary ligation. Am J Physiol. 1970;219(6):1665–1671.
   PubMedGoogle Scholar
• Zuanetti G, De Ferrari GM, Priori SG, et al. Protective effect of vagal stimulation on reperfusion arrhythmias in cats. Circ Res. 1987;61(3):429–435.
   PubMed Web of Science ®Google Scholar
• Vanoli E, De Ferrari GM, Stramba-Badiale M, et al. Vagal stimulation and prevention of sudden death in conscious dogs with a healed myocardial infarction. Circ Res. 1991;68(5):1471–1481.
   PubMed Web of Science ®Google Scholar
• Ando M, Katare RG, Kakinuma Y, et al. Efferent vagal nerve stimulation protects heart against ischemia-induced arrhythmias by preserving connexin43 protein. Circulation. 2005;112(2):164–170.
   PubMed Web of Science ®Google Scholar
• Katare RG, Ando M, Kakinuma Y, et al. Vagal nerve stimulation prevents reperfusion injury through inhibition of opening of mitochondrial permeability transition pore independent of the bradycardiac effect. J Thorac Cardiovasc Surg. 2009;137(1):223–231.
   PubMed Web of Science ®Google Scholar
• Brack KE, Patel VH, Coote JH, et al. Nitric oxide mediates the vagal protective effect on ventricular fibrillation via effects on action potential duration restitution in the rabbit heart. J Physiol. 2007;583(Pt 2):695–704.
   PubMed Web of Science ®Google Scholar
• Herring N, Golding S, Paterson DJ. Pre-synaptic NO-cGMP pathway modulates vagal control of heart rate in isolated adult guinea pig atria. J Mol Cell Cardiol. 2000;32(10):1795–1804.
   PubMed Web of Science ®Google Scholar
• Lee SW, Li Q, Libbus I, et al. Chronic cyclic vagus nerve stimulation has beneficial electrophysiological effects on healthy hearts in the absence of autonomic imbalance. Physiol Rep. 2016;4:9.
   Web of Science ®Google Scholar
• Yu L, Wang S, Zhou X, et al. Chronic intermittent low-level stimulation of tragus reduces cardiac autonomic remodeling and ventricular arrhythmia inducibility in a post-infarction canine model. JACC Clin Electrophysiol. 2016;2(3):330–339.
   PubMedGoogle Scholar
• Nasi-Er BG, Wenhui Z, HuaXin S, et al. Vagus nerve stimulation reduces ventricular arrhythmias and increases ventricular electrical stability. Pacing Clin Electrophysiol. 2019;42(2):247–256.
   PubMed Web of Science ®Google Scholar
• Yellon DM, Hausenloy DJ. Myocardial reperfusion injury. N Engl J Med. 2007;357(11):1121–1135.
   PubMed Web of Science ®Google Scholar
• Uemura K, Zheng C, Li M, et al. Early short-term vagal nerve stimulation attenuates cardiac remodeling after reperfused myocardial infarction. J Card Fail. 2010;16(8):689–699.
   PubMed Web of Science ®Google Scholar
• Calvillo L, Vanoli E, Andreoli E, et al. Vagal stimulation, through its nicotinic action, limits infarct size and the inflammatory response to myocardial ischemia and reperfusion. J Cardiovasc Pharmacol. 2011;58(5):500–507.
   PubMed Web of Science ®Google Scholar
• Shinlapawittayatorn K, Chinda K, Palee S, et al. Low-amplitude, left vagus nerve stimulation significantly attenuates ventricular dysfunction and infarct size through prevention of mitochondrial dysfunction during acute ischemia-reperfusion injury. Heart Rhythm. 2013;10(11):1700–1707.
   PubMed Web of Science ®Google Scholar
• Chen M, Zhou X, Yu L, et al. Low-level vagus nerve stimulation attenuates myocardial ischemic reperfusion injury by antioxidative stress and antiapoptosis reactions in canines. J Cardiovasc Electrophysiol. 2016;27(2):224–231.
   PubMed Web of Science ®Google Scholar
• Yu L, Huang B, Po SS, et al. Low-level tragus stimulation for the treatment of ischemia and reperfusion injury in patients with st-segment elevation myocardial infarction: a proof-of-concept study. JACC Cardiovasc Interv. 2017;10(15):1511–1520.
   PubMed Web of Science ®Google Scholar
• Florea VG, Cohn JN. The autonomic nervous system and heart failure. Circ Res. 2014;114(11):1815–1826.
   PubMed Web of Science ®Google Scholar
• Li M, Zheng C, Sato T, et al. Vagal nerve stimulation markedly improves long-term survival after chronic heart failure in rats. Circulation. 2004;109(1):120–124.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Popovic ZB, Bibevski S, et al. Chronic vagus nerve stimulation improves autonomic control and attenuates systemic inflammation and heart failure progression in a canine high-rate pacing model. Circ Heart Fail. 2009;2(6):692–699.
   PubMed Web of Science ®Google Scholar
• Wang Z, Yu L, Wang S, et al. Chronic intermittent low-level transcutaneous electrical stimulation of auricular branch of vagus nerve improves left ventricular remodeling in conscious dogs with healed myocardial infarction. Circ Heart Fail. 2014;7(6):1014–1021.
   PubMed Web of Science ®Google Scholar
• Zhou L, Filiberti A, Humphrey MB, et al. Low-level transcutaneous vagus nerve stimulation attenuates cardiac remodelling in a rat model of heart failure with preserved ejection fraction. Exp Physiol. 2019;104(1):28–38.
   PubMed Web of Science ®Google Scholar
• Wang Z, Yu L, Huang B, et al. Low-level transcutaneous electrical stimulation of the auricular branch of vagus nerve ameliorates left ventricular remodeling and dysfunction by downregulation of matrix metalloproteinase 9 and transforming growth factor beta1. J Cardiovasc Pharmacol. 2015;65(4):342–348.
   PubMed Web of Science ®Google Scholar
• Schwartz PJ, De Ferrari GM, Sanzo A, et al. Long term vagal stimulation in patients with advanced heart failure: first experience in man. Eur J Heart Fail. 2008;10(9):884–891.
   PubMed Web of Science ®Google Scholar
• De Ferrari GM, Crijns HJ, Borggrefe M, et al. Chronic vagus nerve stimulation: a new and promising therapeutic approach for chronic heart failure. Eur Heart J. 2011;32(7):847–855.
   PubMed Web of Science ®Google Scholar
• Hauptman PJ, Schwartz PJ, Gold MR, et al. Rationale and study design of the increase of vagal tone in heart failure study: INOVATE-HF. Am Heart J. 2012;163(6):954–962e951.
   PubMed Web of Science ®Google Scholar
• Gold MR, Van Veldhuisen DJ, Hauptman PJ, et al. Vagus nerve stimulation for the treatment of heart failure: the INOVATE-HF trial. J Am Coll Cardiol. 2016;68(2):149–158.
   PubMed Web of Science ®Google Scholar
• Premchand RK, Sharma K, Mittal S, et al. Autonomic regulation therapy via left or right cervical vagus nerve stimulation in patients with chronic heart failure: results of the ANTHEM-HF trial. J Card Fail. 2014;20(11):808–816.
   PubMed Web of Science ®Google Scholar
• Premchand RK, Sharma K, Mittal S, et al. Extended follow-up of patients with heart failure receiving autonomic regulation therapy in the ANTHEM-HF study. J Card Fail. 2016;22(8):639–642.
   PubMed Web of Science ®Google Scholar
• Tran N, Asad Z, Elkholey K, et al. Autonomic neuromodulation acutely ameliorates left ventricular strain in humans. J Cardiovasc Transl Res. 2019;12(3):221-230. doi: 10.1007/s12265-018-9853-6.
   PubMed Web of Science ®Google Scholar
• Bhatt DL, Kandzari DE, O’Neill WW, et al. A controlled trial of renal denervation for resistant hypertension. N Engl J Med. 2014;370(15):1393–1401.
   PubMed Web of Science ®Google Scholar
• Krum H, Schlaich M, Whitbourn R, et al. Catheter-based renal sympathetic denervation for resistant hypertension: a multicentre safety and proof-of-principle cohort study. Lancet. 2009;373(9671):1275–1281.
   PubMed Web of Science ®Google Scholar
• Bisognano JD, Bakris G, Nadim MK, et al. Baroreflex activation therapy lowers blood pressure in patients with resistant hypertension: results from the double-blind, randomized, placebo-controlled rheos pivotal trial. J Am Coll Cardiol. 2011;58(7):765–773.
   PubMed Web of Science ®Google Scholar
• Winter B, Whipp BJ. Immediate effects of bilateral carotid body resection on total respiratory resistance and compliance in humans. Adv Exp Med Biol. 2004;551:15–21.
   PubMed Web of Science ®Google Scholar
• Annoni EM, Xie X, Lee SW, et al. Intermittent electrical stimulation of the right cervical vagus nerve in salt-sensitive hypertensive rats: effects on blood pressure, arrhythmias, and ventricular electrophysiology. Physiol Rep. 2015;3:8.
   Web of Science ®Google Scholar
• Chapleau MW, Rotella DL, Reho JJ, et al. Chronic vagal nerve stimulation prevents high-salt diet-induced endothelial dysfunction and aortic stiffening in stroke-prone spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol. 2016;311(1):H276–285.
   PubMed Web of Science ®Google Scholar
• Plachta DT, Gierthmuehlen M, Cota O, et al. Blood pressure control with selective vagal nerve stimulation and minimal side effects. J Neural Eng. 2014;11(3):036011.
   PubMed Web of Science ®Google Scholar
• Gierthmuehlen M, Plachta DT. Effect of selective vagal nerve stimulation on blood pressure, heart rate and respiratory rate in rats under metoprolol medication. Hypertens Res. 2016;39(2):79–87.
   PubMed Web of Science ®Google Scholar