Comparing maximum rate and sustainability of pacing by mechanical vs. electrical stimulation in the Langendorff-perfused rabbit heart

Aims Mechanical stimulation (MS) represents a readily available, non-invasive means of pacing the asystolic or bradycardic heart in patients, but benefits of MS at higher heart rates are unclear. Our aim was to assess the maximum rate and sustainability of excitation by MS vs. electrical stimulation (ES) in the isolated heart under normal physiological conditions. Methods and results Trains of local MS or ES at rates exceeding intrinsic sinus rhythm (overdrive pacing; lowest pacing rates 2.5±0.5 Hz) were applied to the same mid-left ventricular free-wall site on the epicardium of Langendorff-perfused rabbit hearts. Stimulation rates were progressively increased, with a recovery period of normal sinus rhythm between each stimulation period. Trains of MS caused repeated focal ventricular excitation from the site of stimulation. The maximum rate at which MS achieved 1:1 capture was lower than during ES (4.2±0.2 vs. 5.9±0.2 Hz, respectively). At all overdrive pacing rates for which repetitive MS was possible, 1:1 capture was reversibly lost after a finite number of cycles, even though same-site capture by ES remained possible. The number of MS cycles until loss of capture decreased with rising stimulation rate. If interspersed with ES, the number of MS to failure of capture was lower than for MS only. Conclusion In this study, we demonstrate that the maximum pacing rate at which MS can be sustained is lower than that for same-site ES in isolated heart, and that, in contrast to ES, the sustainability of successful 1:1 capture by MS is limited. The mechanism(s) of differences in MS vs. ES pacing ability, potentially important for emergency heart rhythm management, are currently unknown, thus warranting further investigation.

[1]  Jing Zhang,et al.  Myocyte-fibroblast communication in cardiac fibrosis and arrhythmias: Mechanisms and model systems. , 2016, Journal of molecular and cellular cardiology.

[2]  T Alexander Quinn,et al.  Cardiac mechano-electric coupling research: fifty years of progress and scientific innovation. , 2014, Progress in biophysics and molecular biology.

[3]  T. Alexander Quinn,et al.  The importance of non-uniformities in mechano-electric coupling for ventricular arrhythmias , 2013, Journal of Interventional Cardiac Electrophysiology.

[4]  Peter Kohl,et al.  Effects of acute ventricular volume manipulation on in situ cardiomyocyte cell membrane configuration. , 2003, Progress in biophysics and molecular biology.

[5]  Bruce C. Towe,et al.  Ultrasonic cardiac pacing in the porcine model , 2006, IEEE Transactions on Biomedical Engineering.

[6]  F. Sachs,et al.  Mechanically Activated Currents in Chick Heart Cells , 1996, The Journal of Membrane Biology.

[7]  Rebecca A. B. Burton,et al.  Axial Stretch of Rat Single Ventricular Cardiomyocytes Causes an Acute and Transient Increase in Ca2+ Spark Rate , 2009, Circulation research.

[8]  M Lei,et al.  Sudden cardiac death by Commotio cordis: role of mechano-electric feedback. , 2001, Cardiovascular research.

[9]  S. Schwarz,et al.  Percussion pacing--an almost forgotten procedure for haemodynamically unstable bradycardias? A report of three case studies and review of the literature. , 2007, British journal of anaesthesia.

[10]  Peter Kohl,et al.  Novel therapeutic strategies targeting fibroblasts and fibrosis in heart disease , 2016, Nature Reviews Drug Discovery.

[11]  D. Dalecki,et al.  Thresholds for premature contractions in murine hearts exposed to pulsed ultrasound. , 1997, Ultrasound in medicine & biology.

[12]  C. Ward,et al.  Mechanical stretch-induced activation of ROS/RNS signaling in striated muscle. , 2014, Antioxidants & redox signaling.

[13]  P. Zoll,et al.  External mechanical cardiac stimulation. , 1976, The New England journal of medicine.

[14]  Leslie M. Loew,et al.  Single-sensor system for spatially resolved, continuous, and multiparametric optical mapping of cardiac tissue , 2011, Heart rhythm.

[15]  M. Link,et al.  Precordial thump for cardiac arrest is effective for asystole but not for ventricular fibrillation. , 2009, Heart rhythm.

[16]  D. Adam,et al.  Local effects of electrical and mechanical stimulation on the recovery properties of the canine ventricle. , 1982, The American journal of cardiology.

[17]  Gary R. Mirams,et al.  Minimum Information about a Cardiac Electrophysiology Experiment (MICEE): Standardised Reporting for Model Reproducibility, Interoperability, and Data Sharing , 2011, Progress in biophysics and molecular biology.

[18]  A. Albano,et al.  [Rhythmic percussion of the precordium with the closed fist as the first procedure in therapy of cardiac arrest]. , 1967, Minerva medica.

[19]  P. Kohl,et al.  Utility of pre-cordial thump for treatment of out of hospital cardiac arrest: a prospective study. , 2009, Resuscitation.

[20]  D. Adam,et al.  Premature cardiac contractions produced efficiently by external high-intensity focused ultrasound. , 2011, Ultrasound in medicine & biology.

[21]  M. Morad,et al.  ‘Pressure–flow‘‐triggered intracellular Ca2+ transients in rat cardiac myocytes: possible mechanisms and role of mitochondria , 2008, The Journal of physiology.

[22]  Gary R. Mirams,et al.  High resolution structural evidence suggests the Sarcoplasmic Reticulum forms microdomains with Acidic Stores (lysosomes) in the heart , 2017, Scientific Reports.

[23]  E. White,et al.  The role of calcium in the response of cardiac muscle to stretch. , 1999, Progress in biophysics and molecular biology.

[24]  M R Franz,et al.  Electrophysiological Effects of Myocardial Stretch and Mechanical Determinants of Stretch‐Activated Arrhythmias , 1992, Circulation.

[25]  A D McCulloch,et al.  Strain softening in rat left ventricular myocardium. , 1997, Journal of biomechanical engineering.

[26]  W WardChristopher,et al.  Mechanical Stretch-Induced Activation of ROS/RNS Signaling in Striated Muscle , 2014 .

[27]  P. Kohl,et al.  Living cardiac tissue slices: an organotypic pseudo two-dimensional model for cardiac biophysics research. , 2014, Progress in biophysics and molecular biology.

[28]  Peter Kohl,et al.  Abstract 13098: Mechanically-Induced Premature Ventricular Excitation is Mediated by Cation Non-Selective Stretch-Activated Channels and Depends on the Extent of Local Tissue Deformation in Isolated Rabbit Heart , 2011 .

[29]  E. White,et al.  Caveolae Act as Membrane Reserves Which Limit Mechanosensitive I Cl,swell Channel Activation during Swelling in the Rat Ventricular Myocyte , 2009, PloS one.

[30]  D. Scherf,et al.  Thumping of the precordium in ventricular standstill. , 1961, The American journal of cardiology.

[31]  A. McCulloch,et al.  Caveolae in ventricular myocytes are required for stretch-dependent conduction slowing. , 2014, Journal of molecular and cellular cardiology.

[32]  W. Brady,et al.  Emergent precordial percussion revisited--pacing the heart in asystole. , 2011, The American journal of emergency medicine.

[33]  Dan Adam,et al.  Extracorporeal acute cardiac pacing by high intensity focused ultrasound. , 2014, Progress in biophysics and molecular biology.

[34]  R. Stanford,et al.  Precordial percussion in cardiac asystole. , 1963, Lancet.

[35]  P. Kohl,et al.  Soft tissue impact characterisation kit (STICK) for ex situ investigation of heart rhythm responses to acute mechanical stimulation. , 2006, Progress in biophysics and molecular biology.

[36]  W. R. Smith.  The management of cardiac arrest. , 1962, Medical science.

[37]  B. Befeler.  Mechanical stimulation of the heart: its therapeutic value in tachyarrhythmias. , 1978, Chest.

[38]  E. Carstensen,et al.  Effects of pulsed ultrasound on the frog heart: I. Thresholds for changes in cardiac rhythm and aortic pressure. , 1993, Ultrasound in medicine & biology.

[39]  Menahem Y. Rotenberg,et al.  Feasibility of Leadless Cardiac Pacing Using Injectable Magnetic Microparticles , 2016, Scientific Reports.

[40]  M. Lab,et al.  Mechanical modulation of stretch-induced premature ventricular beats: induction of mechanoelectric adaptation period. , 1998, Cardiovascular research.

[41]  Peter Kohl,et al.  Combining wet and dry research: experience with model development for cardiac mechano-electric structure-function studies , 2013, Cardiovascular research.

[42]  P. Nielsen,et al.  Strain softening is not present during axial extensions of rat intact right ventricular trabeculae in the presence or absence of 2,3-butanedione monoxime. , 2004, American journal of physiology. Heart and circulatory physiology.

[43]  J. Nerbonne,et al.  Cardiac Mechano-Gated Ion Channels and Arrhythmias. , 2016, Circulation research.