Premature Ventricular Contraction Coupling Interval Variability Destabilizes Cardiac Neuronal and Electrophysiological Control: Insights From Simultaneous Cardioneural Mapping

David Hamon; Pradeep S Rajendran; Ray W Chui; Olujimi A Ajijola; Tadanobu Irie; Ramin Talebi; Siamak Salavatian; Marmar Vaseghi; Jason S Bradfield; J Andrew Armour; Jeffrey L Ardell; Kalyanam Shivkumar

doi:10.1161/CIRCEP.116.004937

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Premature Ventricular Contraction Coupling Interval Variability Destabilizes Cardiac Neuronal and Electrophysiological Control: Insights From Simultaneous Cardioneural Mapping

Journal article

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Peer reviewed

Premature Ventricular Contraction Coupling Interval Variability Destabilizes Cardiac Neuronal and Electrophysiological Control: Insights From Simultaneous Cardioneural Mapping

David Hamon, Pradeep S Rajendran, Ray W Chui, Olujimi A Ajijola, Tadanobu Irie, Ramin Talebi, Siamak Salavatian, Marmar Vaseghi, Jason S Bradfield, J Andrew Armour, …

Circulation. Arrhythmia and electrophysiology, Vol.10(4), pp.e004937-e004937

04/2017

DOI: 10.1161/CIRCEP.116.004937

PMCID: PMC5407491

PMID: 28408652

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Abstract

Variability in premature ventricular contraction (PVC) coupling interval (CI) increases the risk of cardiomyopathy and sudden death. The autonomic nervous system regulates cardiac electrical and mechanical indices, and its dysregulation plays an important role in cardiac disease pathogenesis. The impact of PVCs on the intrinsic cardiac nervous system, a neural network on the heart, remains unknown. The objective was to determine the effect of PVCs and CI on intrinsic cardiac nervous system function in generating cardiac neuronal and electric instability using a novel cardioneural mapping approach. In a porcine model (n=8), neuronal activity was recorded from a ventricular ganglion using a microelectrode array, and cardiac electrophysiological mapping was performed. Neurons were functionally classified based on their response to afferent and efferent cardiovascular stimuli, with neurons that responded to both defined as convergent (local reflex processors). Dynamic changes in neuronal activity were then evaluated in response to right ventricular outflow tract PVCs with fixed short, fixed long, and variable CI. PVC delivery elicited a greater neuronal response than all other stimuli ( <0.001). Compared with fixed short and long CI, PVCs with variable CI had a greater impact on neuronal response ( <0.05 versus short CI), particularly on convergent neurons ( <0.05), as well as neurons receiving sympathetic ( <0.05) and parasympathetic input ( <0.05). The greatest cardiac electric instability was also observed after variable (short) CI PVCs. Variable CI PVCs affect critical populations of intrinsic cardiac nervous system neurons and alter cardiac repolarization. These changes may be critical for arrhythmogenesis and remodeling, leading to cardiomyopathy.

Action Potentials

Animals

Autonomic Nervous System - physiopathology

Cardiac Pacing, Artificial

Cardiomyopathies - etiology

Cardiomyopathies - physiopathology

Disease Models, Animal

Electrophysiologic Techniques, Cardiac

Female

Heart - innervation

Heart Rate

Male

Myocardial Contraction

Sus scrofa

Time Factors

Ventricular Function

Ventricular Premature Complexes - complications

Ventricular Premature Complexes - diagnosis

Ventricular Premature Complexes - physiopathology

Details

Title: Subtitle: Premature Ventricular Contraction Coupling Interval Variability Destabilizes Cardiac Neuronal and Electrophysiological Control: Insights From Simultaneous Cardioneural Mapping
Creators: David Hamon - University of California, Los Angeles
Pradeep S Rajendran - University of California, Los Angeles
Ray W Chui - University of California, Los Angeles
Olujimi A Ajijola - University of California, Los Angeles
Tadanobu Irie - Texas Cardiac Arrhythmia
Ramin Talebi - University of California, Los Angeles
Siamak Salavatian - University of California, Los Angeles
Marmar Vaseghi - University of California, Los Angeles
Jason S Bradfield - University of California, Los Angeles
J Andrew Armour - University of California, Los Angeles
Jeffrey L Ardell - University of California, Los Angeles
Kalyanam Shivkumar - University of California, Los Angeles
Resource Type: Journal article
Publication Details: Circulation. Arrhythmia and electrophysiology, Vol.10(4), pp.e004937-e004937
DOI: 10.1161/CIRCEP.116.004937
PMID: 28408652
PMCID: PMC5407491
ISSN: 1941-3149
eISSN: 1941-3084
Grant note: K08 HL125730 / NHLBI NIH HHS OT2 OD023848 / NIH HHS R01 HL084261 / NHLBI NIH HHS U18 EB021799 / NIBIB NIH HHS F31 HL127974 / NHLBI NIH HHS
Language: English
Date published: 04/2017
Academic Unit: Internal Medicine
Record Identifier: 9984694746402771

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