Neuromodulation for the Treatment of Heart Rhythm Disorders

Highlights • Derangement of autonomic nervous signaling is an important contributor to cardiac arrhythmogenesis.• Modulation of autonomic nervous signaling holds significant promise for the prevention and treatment of cardiac arrhythmias.• Further clinical investigation is necessary to establish the efficacy and safety of autonomic modulatory therapies in reducing cardiac arrhythmias.

[1]  M. Fishbein,et al.  Intermittent left cervical vagal nerve stimulation damages the stellate ganglia and reduces the ventricular rate during sustained atrial fibrillation in ambulatory dogs. , 2016, Heart rhythm.

[2]  Richard N. Taylor,et al.  Treating electrical storm : sympathetic blockade versus advanced cardiac life support-guided therapy. , 2000, Circulation.

[3]  Y. Qadri,et al.  Stellate ganglion blockade for the treatment of refractory ventricular arrhythmias: A systematic review and meta‐analysis , 2017, Journal of cardiovascular electrophysiology.

[4]  L. Lo,et al.  Temporary Suppression of Cardiac Ganglionated Plexi Leads to Long‐Term Suppression of Atrial Fibrillation: Evidence of Early Autonomic Intervention to Break the Vicious Cycle of “AF Begets AF” , 2016, Journal of the American Heart Association.

[5]  S. McDougall,et al.  Central control of autonomic functions in health and disease , 2015, Front. Neurosci..

[6]  R. Lazzara,et al.  Ganglionated plexi modulate extrinsic cardiac autonomic nerve input: effects on sinus rate, atrioventricular conduction, refractoriness, and inducibility of atrial fibrillation. , 2007, Journal of the American College of Cardiology.

[7]  Y. Aizawa,et al.  Cardiac innervation and sudden cardiac death. , 2015, Circulation research.

[8]  U. Schotten,et al.  Catheter-Based Renal Denervation Reduces Atrial Nerve Sprouting and Complexity of Atrial Fibrillation in Goats , 2015, Circulation. Arrhythmia and electrophysiology.

[9]  Albert Hofman,et al.  Projections on the number of individuals with atrial fibrillation in the European Union, from 2000 to 2060. , 2013, European heart journal.

[10]  F. Gaita,et al.  Can spinal cord stimulation reduce ventricular arrhythmias? , 2012, Heart rhythm.

[11]  P. Neužil,et al.  Determining the Feasibility of Spinal Cord Neuromodulation for the Treatment of Chronic Systolic Heart Failure: The DEFEAT-HF Study. , 2016, JACC. Heart failure.

[12]  Jagmeet P. Singh,et al.  Novel Interventional Therapies to Modulate the Autonomic Tone in Heart Failure. , 2015, JACC. Heart failure.

[13]  He Huang,et al.  Effect of renal sympathetic denervation on the progression of paroxysmal atrial fibrillation in canines with long-term intermittent atrial pacing. , 2015, Europace : European pacing, arrhythmias, and cardiac electrophysiology : journal of the working groups on cardiac pacing, arrhythmias, and cardiac cellular electrophysiology of the European Society of Cardiology.

[14]  P. Andréll,et al.  Spinal cord stimulation effects on myocardial ischemia, infarct size, ventricular arrhythmia, and noninvasive electrophysiology in a porcine ischemia-reperfusion model. , 2011, Heart rhythm.

[15]  D. Zipes,et al.  Effects of selective vagal and stellate ganglion stimulation of atrial refractoriness. , 1974, Cardiovascular research.

[16]  T. Hökfelt,et al.  Renal sympathetic nerve activity modulates afferent renal nerve activity by PGE2-dependent activation of α1- and α2-adrenoceptors on renal sensory nerve fibers , 2007 .

[17]  Jens Jordan,et al.  Carotid Baroreceptor Stimulation, Sympathetic Activity, Baroreflex Function, and Blood Pressure in Hypertensive Patients , 2010, Hypertension.

[18]  A. Mahajan,et al.  Bilateral cardiac sympathetic denervation for the management of electrical storm. , 2012, Journal of the American College of Cardiology.

[19]  T. Chao,et al.  Impact of Renal Denervation on Atrial Arrhythmogenic Substrate in Ischemic Model of Heart Failure , 2018, Journal of the American Heart Association.

[20]  S. Mann.  Redefining beta-blocker use in hypertension: selecting the right beta-blocker and the right patient. , 2017, Journal of the American Society of Hypertension : JASH.

[21]  Hongmei Li,et al.  Neural Mechanisms of Paroxysmal Atrial Fibrillation and Paroxysmal Atrial Tachycardia in Ambulatory Canines , 2008, Circulation.

[22]  P. Schwartz,et al.  Sympathetic modulation of the relation between ventricular repolarization and cycle length. , 1991, Circulation research.

[23]  H. Nakagawa,et al.  Low-level transcutaneous electrical vagus nerve stimulation suppresses atrial fibrillation. , 2015, Journal of the American College of Cardiology.

[24]  E. Pokushalov,et al.  Pulmonary vein isolation with concomitant renal artery denervation is associated with reduction in both arterial blood pressure and atrial fibrillation burden: Data from implantable cardiac monitor , 2016, Cardiovascular therapeutics.

[25]  D. Harrison,et al.  The Endpoint on Measuring the Clinical Effects of Renal Denervation: What Are the Best Surrogates , 2015 .

[26]  T. Hökfelt,et al.  Renal sympathetic nerve activity modulates afferent renal nerve activity by PGE2-dependent activation of alpha1- and alpha2-adrenoceptors on renal sensory nerve fibers. , 2007, American journal of physiology. Regulatory, integrative and comparative physiology.

[27]  G. Dibona,et al.  Neural control of renal function. , 1997, Physiological reviews.

[28]  D P Zipes,et al.  Differential response to right and left ansae subclaviae stimulation of early afterdepolarizations and ventricular tachycardia induced by cesium in dogs. , 1988, Circulation.

[29]  H. Vinters,et al.  Electroanatomic remodeling of the left stellate ganglion after myocardial infarction. , 2012, Journal of the American College of Cardiology.

[30]  E. Pokushalov,et al.  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. , 2019, Heart rhythm.

[31]  J. Ioannidis,et al.  Autonomic denervation added to pulmonary vein isolation for paroxysmal atrial fibrillation: a randomized clinical trial. , 2013, Journal of the American College of Cardiology.

[32]  K. Deisseroth.  Optogenetics: 10 years of microbial opsins in neuroscience , 2015, Nature Neuroscience.

[33]  K. Shivkumar,et al.  Mechanisms and management of refractory ventricular arrhythmias in the age of autonomic modulation. , 2018, Heart rhythm.

[34]  A. Uy‐Evanado,et al.  Abstract 16081: What is the Societal Impact of Sudden Cardiac Death in the United States? , 2012 .

[35]  Bing Huang,et al.  Optogenetic Modulation of Cardiac Sympathetic Nerve Activity to Prevent Ventricular Arrhythmias. , 2017, Journal of the American College of Cardiology.

[36]  M. Laks,et al.  Modulation of regional dispersion of repolarization and T-peak to T-end interval by the right and left stellate ganglia. , 2013, American journal of physiology. Heart and circulatory physiology.

[37]  R. Lazzara,et al.  Triggered firing in pulmonary veins initiated by in vitro autonomic nerve stimulation. , 2005, Heart rhythm.

[38]  Hong Jiang,et al.  Low level tragus nerve stimulation is a non-invasive approach for anti-atrial fibrillation via preventing the loss of connexins. , 2015, International journal of cardiology.

[39]  G. Hindricks,et al.  Renal denervation for treatment of ventricular arrhythmias: data from an International Multicenter Registry , 2016, Clinical Research in Cardiology.

[40]  U. Schotten,et al.  Effects of Electrical Stimulation of Carotid Baroreflex and Renal Denervation on Atrial Electrophysiology , 2013, Journal of cardiovascular electrophysiology.

[41]  M. Fishbein,et al.  Cryoablation of stellate ganglia and atrial arrhythmia in ambulatory dogs with pacing-induced heart failure. , 2009, Heart rhythm.

[42]  L. Barajas,et al.  Myelinated nerves of the rat kidney. A light and electron microscopic autoradiographic study. , 1978, Journal of ultrastructure research.

[43]  W. Craig,et al.  Efficacy and Efficiency of Perioperative Stellate Ganglion Blocks in Cardiac Surgery: A Pilot Study. , 2017, Journal of cardiothoracic and vascular anesthesia.

[44]  V. Fuster,et al.  Cardiac Autonomic Dysfunction and Incidence of Atrial Fibrillation: Results From 20 Years Follow-Up. , 2017, Journal of the American College of Cardiology.

[45]  K. Shivkumar,et al.  Remodeling of stellate ganglion neurons after spatially targeted myocardial infarction: Neuropeptide and morphologic changes. , 2015, Heart rhythm.

[46]  Jeremy N Ruskin,et al.  Evaluation of catheter ablation of periatrial ganglionic plexi in patients with atrial fibrillation. , 2008, The American journal of cardiology.

[47]  U. Schotten,et al.  Role of autonomic nervous system in atrial fibrillation. , 2019, International journal of cardiology.

[48]  M. Böhm,et al.  Renal denervation suppresses ventricular arrhythmias during acute ventricular ischemia in pigs. , 2013, Heart rhythm.

[49]  M. Eghbali,et al.  Progression of myocardial ischemia leads to unique changes in immediate-early gene expression in the spinal cord dorsal horn. , 2018, American journal of physiology. Heart and circulatory physiology.

[50]  S. S. Hull,et al.  Vagal stimulation and prevention of sudden death in conscious dogs with a healed myocardial infarction. , 1991, Circulation research.

[51]  A. Massumi,et al.  Effect of botulinum toxin on inducibility and maintenance of atrial fibrillation in ovine myocardial tissue , 2017, Pacing and clinical electrophysiology : PACE.

[52]  G. Breithardt,et al.  Effects of Thoracic Epidural Anesthesia with and without Autonomic Nervous System Blockade on Cardiac Monophasic Action Potentials and Effective Refractoriness in Awake Dogs , 2001, Anesthesiology.

[53]  P. Schwartz,et al.  Prevention of Sudden Cardiac Death After a First Myocardial Infarction by Pharmacologic or Surgical Antiadrenergic Interventions , 1992 .

[54]  I. Kardys,et al.  Atrial fibrillation reduction by renal sympathetic denervation: 12 months’ results of the AFFORD study , 2018, Clinical Research in Cardiology.

[55]  M. Böhm,et al.  Modulation of renal sympathetic innervation: recent insights beyond blood pressure control , 2018, Clinical Autonomic Research.

[56]  K. Iijima,et al.  Blood Pressure and Autonomic Responses to Electrical Stimulation of the Renal Arterial Nerves Before and After Ablation of the Renal Artery , 2013, Hypertension.

[57]  Francesca Pistoia,et al.  The Epidemiology of Atrial Fibrillation and Stroke. , 2016, Cardiology clinics.

[58]  U. Kopp.  Role of renal sensory nerves in physiological and pathophysiological conditions. , 2015, American journal of physiology. Regulatory, integrative and comparative physiology.

[59]  S. Mittal,et al.  Ganglionated plexus ablation vs linear ablation in patients undergoing pulmonary vein isolation for persistent/long-standing persistent atrial fibrillation: a randomized comparison. , 2013, Heart rhythm.

[60]  A. Mahajan,et al.  Neuraxial Modulation for Refractory Ventricular Arrhythmias: Value of Thoracic Epidural Anesthesia and Surgical Left Cardiac Sympathetic Denervation , 2010, Circulation.

[61]  Michael A. Henninger,et al.  High-Performance Genetically Targetable Optical Neural Silencing via Light-Driven Proton Pumps , 2010 .

[62]  Pradeep S Rajendran,et al.  Cardiac neuroanatomy - Imaging nerves to define functional control , 2017, Autonomic Neuroscience.

[63]  M. Chung,et al.  Atrial Fibrillation Burden: Moving Beyond Atrial Fibrillation as a Binary Entity A Scientific Statement From the American Heart Association , 2018, Circulation.

[64]  George A. Mensah,et al.  Sudden Cardiac Death in the United States, 1989 to 1998 , 2001, Circulation.

[65]  A. Mahajan,et al.  Thoracic Epidural Anesthesia Can Be Effective for the Short‐Term Management of Ventricular Tachycardia Storm , 2017, Journal of the American Heart Association.

[66]  B. Scherlag,et al.  Low-Level Vagus Nerve Stimulation Suppresses Post-Operative Atrial Fibrillation and Inflammation: A Randomized Study. , 2017, JACC. Clinical electrophysiology.

[67]  S. Narayan,et al.  Percutaneous Stellate Ganglion Block Suppressing VT and VF in a Patient Refractory to VT Ablation , 2013, Journal of cardiovascular electrophysiology.

[68]  D. Huang,et al.  ClC-3 chloride channel is involved in isoprenaline-induced cardiac hypertrophy. , 2018, Gene.

[69]  L. Allen,et al.  Impact of obstructive sleep apnea and continuous positive airway pressure therapy on outcomes in patients with atrial fibrillation-Results from the Outcomes Registry for Better Informed Treatment of Atrial Fibrillation (ORBIT-AF). , 2015, American heart journal.

[70]  Bing Huang,et al.  Chronic Intermittent Low-Level Stimulation of Tragus Reduces Cardiac Autonomic Remodeling and Ventricular Arrhythmia Inducibility in a Post-Infarction Canine Model. , 2016, JACC. Clinical electrophysiology.

[71]  D. Zipes,et al.  Effects of Sympathetic and Vagal Nerves on Recovery Properties of the Endocardium and Epicardium of the Canine Left Ventricle , 1980, Circulation research.

[72]  A. Speir,et al.  Postoperative atrial fibrillation significantly increases mortality, hospital readmission, and hospital costs. , 2014, The Annals of thoracic surgery.

[73]  O. F. Sharifov,et al.  Roles of adrenergic and cholinergic stimulation in spontaneous atrial fibrillation in dogs. , 2004, Journal of the American College of Cardiology.

[74]  S. Mittal,et al.  A randomized comparison of pulmonary vein isolation with versus without concomitant renal artery denervation in patients with refractory symptomatic atrial fibrillation and resistant hypertension. , 2012, Journal of the American College of Cardiology.

[75]  D. Hopkins,et al.  Gross and microscopic anatomy of the human intrinsic cardiac nervous system , 1997, The Anatomical record.

[76]  M. Kay,et al.  Optogenetic release of norepinephrine from cardiac sympathetic neurons alters mechanical and electrical function. , 2015, Cardiovascular research.

[77]  M. Fishbein,et al.  Low-level vagus nerve stimulation upregulates small conductance calcium-activated potassium channels in the stellate ganglion. , 2013, Heart rhythm.

[78]  K. Anstrom,et al.  Adaptive servo-ventilation reduces atrial fibrillation burden in patients with heart failure and sleep apnea. , 2019, Heart rhythm.

[79]  A. Buxton,et al.  Percutaneous stellate ganglia block for acute control of refractory ventricular tachycardia. , 2012, Heart rhythm.

[80]  E. Pokushalov,et al.  Long-Term Suppression of Atrial Fibrillation by Botulinum Toxin Injection Into Epicardial Fat Pads in Patients Undergoing Cardiac Surgery: One-Year Follow-Up of a Randomized Pilot Study , 2015, Circulation. Arrhythmia and electrophysiology.

[81]  C. Patel,et al.  Autonomic Modulation for the Treatment of Ventricular Arrhythmias: Therapeutic Use of Percutaneous Stellate Ganglion Blocks , 2017, Journal of cardiovascular electrophysiology.

[82]  M. Burgess,et al.  Effects of sympathetic stimulation on refractory periods of ischemic canine ventricular myocardium. , 1982, Journal of electrocardiology.

[83]  F. Abboud,et al.  Sympathetic neural mechanisms in obstructive sleep apnea. , 1995, The Journal of clinical investigation.

[84]  Y. Shimada,et al.  Features of intrinsic ganglionated plexi in both atria after extensive pulmonary isolation and their clinical significance after catheter ablation in patients with atrial fibrillation. , 2015, Heart rhythm.

[85]  P. Schwartz,et al.  Rationale and design of a prospective study to assess the effect of left cardiac sympathetic denervation in chronic heart failure. , 2017, International journal of cardiology.

[86]  P. Schwartz,et al.  Left cardiac sympathetic denervation for catecholaminergic polymorphic ventricular tachycardia. , 2008, The New England journal of medicine.

[87]  K. Mandal,et al.  Minimally invasive transtracheal cardiac plexus block for sympathetic neuromodulation. , 2019, Heart rhythm.

[88]  B. Zrenner,et al.  Selective Proximal Renal Denervation Guided by Autonomic Responses Evoked via High-Frequency Stimulation in a Preclinical Canine Model , 2015, Circulation. Cardiovascular interventions.

[89]  A. Mahajan,et al.  Cardiac sympathetic denervation in patients with refractory ventricular arrhythmias or electrical storm: intermediate and long-term follow-up. , 2014, Heart rhythm.

[90]  Peng-Sheng Chen,et al.  Autonomic nerve activity and atrial fibrillation. , 2007, Heart rhythm.

[91]  P. Schwartz,et al.  Effects of unilateral cardiac sympathetic denervation on the ventricular fibrillation threshold. , 1976, The American journal of cardiology.

[92]  M. Fishbein,et al.  Effects of Vagal Nerve Stimulation on Ganglionated Plexi Nerve Activity and Ventricular Rate in Ambulatory Dogs With Persistent Atrial Fibrillation. , 2018, JACC. Clinical electrophysiology.

[93]  J. Dixon,et al.  Neuroadrenergic Dysfunction Along the Diabetes Continuum , 2012, Diabetes.

[94]  T. Opthof,et al.  Dispersion of refractoriness in normal and ischaemic canine ventricle: effects of sympathetic stimulation. , 1993, Cardiovascular research.

[95]  J. Haze,et al.  Obstructive sleep apnea. , 1987, Cranio : the journal of craniomandibular practice.

[96]  Eue-Keun Choi,et al.  Botulinum Toxin Injection in Epicardial Autonomic Ganglia Temporarily Suppresses Vagally Mediated Atrial Fibrillation , 2011, Circulation. Arrhythmia and electrophysiology.

[97]  R. Lopes,et al.  6-Month Outcomes in Patients With Implantable Cardioverter-Defibrillators Undergoing Renal Sympathetic Denervation for the Treatment of Refractory Ventricular Arrhythmias. , 2015, JACC. Cardiovascular interventions.

[98]  R. Virmani,et al.  Sudden cardiac death. , 1987, Human pathology.

[99]  Stanley Nattel,et al.  Role of the Autonomic Nervous System in Atrial Fibrillation: Pathophysiology and Therapy , 2014, Circulation research.

[100]  J. Piccini,et al.  Temporary autonomic modulation with botulinum toxin type A to reduce atrial fibrillation after cardiac surgery. , 2019, Heart rhythm.

[101]  A. Pearlman,et al.  Beneficial Effects of Vagal Stimulation and Bradycardia During Experimental Acute Myocardial Ischemia , 1974, Circulation.

[102]  S. Pocock,et al.  Effect of renal denervation on blood pressure in the presence of antihypertensive drugs: 6-month efficacy and safety results from the SPYRAL HTN-ON MED proof-of-concept randomised trial , 2018, The Lancet.

[103]  J. Staessen,et al.  Blood pressure response to renal nerve stimulation in patients undergoing renal denervation: a feasibility study , 2014, Journal of Human Hypertension.

[104]  M. Esler,et al.  Selective vs. Global Renal Denervation: a Case for Less Is More , 2018, Current Hypertension Reports.

[105]  M. Haïssaguerre,et al.  Pulmonary vein triggers, focal sources, rotors and atrial cardiomyopathy: implications for the choice of the most effective ablation therapy , 2016, Journal of internal medicine.

[106]  Douglas P. Zipes,et al.  Role of the Autonomic Nervous System in Modulating Cardiac Arrhythmias , 2014, Circulation research.

[107]  J. Feliciano,et al.  Inducibility of atrial fibrillation during electrophysiologic evaluation is associated with increased dispersion of atrial refractoriness. , 2009, International journal of cardiology.

[108]  J. Mathew,et al.  A multicenter risk index for atrial fibrillation after cardiac surgery. , 2004 .

[109]  T. Mammoto,et al.  Thoracic Epidural Anesthesia Attenuates Halothane-induced Myocardial Sensitization to Dysrhythmogenic Effect of Epinephrine in Dogs , 1995 .

[110]  E. Pokushalov,et al.  Renal denervation for improving outcomes of catheter ablation in patients with atrial fibrillation and hypertension: early experience. , 2014, Heart rhythm.

[111]  Bing Huang,et al.  Spinal cord stimulation protects against ventricular arrhythmias by suppressing left stellate ganglion neural activity in an acute myocardial infarction canine model. , 2015, Heart rhythm.

[112]  Hong Liu,et al.  Sodium-calcium exchange initiated by the Ca2+ transient: an arrhythmia trigger within pulmonary veins. , 2006, Journal of the American College of Cardiology.

[113]  A. Camm,et al.  Guidelines for the management of atrial fibrillation: the Task Force for the Management of Atrial Fibrillation of the European Society of Cardiology (ESC). , 2010, European heart journal.

[114]  V. Napadow,et al.  The Autonomic Brain: An Activation Likelihood Estimation Meta-Analysis for Central Processing of Autonomic Function , 2013, The Journal of Neuroscience.

[115]  Marmar Vaseghi,et al.  Cardiac Sympathetic Denervation for Refractory Ventricular Arrhythmias. , 2017, Journal of the American College of Cardiology.

[116]  N. Salakhutdinov,et al.  Botulinum toxin injection in epicardial fat pads can prevent recurrences of atrial fibrillation after cardiac surgery: results of a randomized pilot study. , 2014, Journal of the American College of Cardiology.

[117]  Marco Bettoni,et al.  Autonomic Tone Variations Before the Onset of Paroxysmal Atrial Fibrillation , 2002, Circulation.

[118]  W. Maixner,et al.  Contribution of Baroreceptor Function to Pain Perception and Perioperative Outcomes , 2019, Anesthesiology.

[119]  T. Dickfeld,et al.  Safety and efficacy of renal denervation as a novel treatment of ventricular tachycardia storm in patients with cardiomyopathy. , 2014, Heart rhythm.

[120]  A. Mahajan,et al.  Inflammatory and apoptotic remodeling in autonomic nervous system following myocardial infarction , 2017, PloS one.

[121]  H. Pürerfellner,et al.  Pulmonary vein isolation combined with spironolactone or renal sympathetic denervation in patients with chronic kidney disease, uncontrolled hypertension, paroxysmal atrial fibrillation, and a pacemaker , 2017, Journal of Interventional Cardiac Electrophysiology.

[122]  Kenji F. Tanaka,et al.  Long-lasting silencing of orexin/hypocretin neurons using archaerhodopsin induces slow-wave sleep in mice , 2013, Behavioural Brain Research.

[123]  G. Paxinos,et al.  Anatomic approach for ganglionic plexi ablation in patients with paroxysmal atrial fibrillation. , 2008, The American journal of cardiology.

[124]  K. Peter,et al.  Reverse cardiac remodeling after renal denervation: Atrial electrophysiologic and structural changes associated with blood pressure lowering. , 2015, Heart rhythm.

[125]  John P. Greenwood,et al.  Non-invasive Vagus Nerve Stimulation in Healthy Humans Reduces Sympathetic Nerve Activity , 2014, Brain Stimulation.

[126]  S. Narayan,et al.  Spatial relationship of organized rotational and focal sources in human atrial fibrillation to autonomic ganglionated plexi. , 2017, International journal of cardiology.

[127]  P. Sutton,et al.  Effect of Adrenergic Stimulation on Action Potential Duration Restitution in Humans , 2003, Circulation.

[128]  Jeroen J. Bax,et al.  Guidelines for the management of atrial fibrillation: the Task Force for the Management of Atrial Fibrillation of the European Society of Cardiology (ESC). , 2010, Europace : European pacing, arrhythmias, and cardiac electrophysiology : journal of the working groups on cardiac pacing, arrhythmias, and cardiac cellular electrophysiology of the European Society of Cardiology.

[129]  G. Vasilopoulos,et al.  Propranolol Versus Metoprolol for Treatment of Electrical Storm in Patients With Implantable Cardioverter-Defibrillator. , 2018, Journal of the American College of Cardiology.

[130]  L. Schramm,et al.  The conduction velocities and spinal projections of single renal afferent fibers in the rat , 1987, Brain Research.

[131]  A. Raza,et al.  Treating obstructive sleep apnea with continuous positive airway pressure reduces risk of recurrent atrial fibrillation after catheter ablation: a meta-analysis. , 2018, Sleep medicine.

[132]  Bing Huang,et al.  Low-level baroreceptor stimulation suppresses atrial fibrillation by inhibiting ganglionated plexus activity. , 2015, The Canadian journal of cardiology.

[133]  P. Puddu,et al.  Prevention of postischemic ventricular fibrillation late after right or left stellate ganglionectomy in dogs. , 1988, Circulation.

[134]  D. Chan Pin Yin,et al.  Ganglion Plexus Ablation in Advanced Atrial Fibrillation: The AFACT Study. , 2016, Journal of the American College of Cardiology.

[135]  Prashanthan Sanders,et al.  The impact of atrial fibrillation type on the risk of thromboembolism, mortality, and bleeding: a systematic review and meta-analysis. , 2016, European heart journal.

[136]  D. Hopkins,et al.  Anatomy of human extrinsic cardiac nerves and ganglia. , 1986, The American journal of cardiology.

[137]  J. Lekakis,et al.  Acute effects of unilateral temporary stellate ganglion block on human atrial electrophysiological properties and atrial fibrillation inducibility. , 2016, Heart rhythm.

[138]  J. Daubert,et al.  Obstructive sleep apnea is associated with increased rotor burden in patients undergoing focal impulse and rotor modification guided atrial fibrillation ablation. , 2018, Europace : European pacing, arrhythmias, and cardiac electrophysiology : journal of the working groups on cardiac pacing, arrhythmias, and cardiac cellular electrophysiology of the European Society of Cardiology.