Advertisement

The frequency spectrum of sympathetic nerve activity and arrhythmogenicity in ambulatory dogs

  • Xiao Liu
    Affiliations
    Krannert Institute of Cardiology and Division of Cardiology, Department of Medicine, Indiana University School of Medicine, Indianapolis, Indiana

    Cedars-Sinai Medical Center, Los Angeles, California
    Search for articles by this author
  • Yuan Yuan
    Affiliations
    Krannert Institute of Cardiology and Division of Cardiology, Department of Medicine, Indiana University School of Medicine, Indianapolis, Indiana

    Department of Cardiothoracic Surgery, Xinhua Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, China
    Search for articles by this author
  • Johnson Wong
    Affiliations
    Krannert Institute of Cardiology and Division of Cardiology, Department of Medicine, Indiana University School of Medicine, Indianapolis, Indiana
    Search for articles by this author
  • Guannan Meng
    Affiliations
    Krannert Institute of Cardiology and Division of Cardiology, Department of Medicine, Indiana University School of Medicine, Indianapolis, Indiana

    Department of Cardiology, Renmin Hospital of Wuhan University, Wuhan, China
    Search for articles by this author
  • Akira Ueoka
    Affiliations
    Krannert Institute of Cardiology and Division of Cardiology, Department of Medicine, Indiana University School of Medicine, Indianapolis, Indiana

    Department of Cardiovascular Medicine, Okayama University Graduate School of Medicine Dentistry and Pharmaceutical Sciences, Okayama, Japan
    Search for articles by this author
  • Leanne M. Woiewodski
    Affiliations
    Krannert Institute of Cardiology and Division of Cardiology, Department of Medicine, Indiana University School of Medicine, Indianapolis, Indiana
    Search for articles by this author
  • Lan S. Chen
    Affiliations
    Department of Neurology, Indiana University School of Medicine, Indianapolis, Indiana
    Search for articles by this author
  • Changyu Shen
    Affiliations
    Richard and Susan Smith Center for Outcomes Research in Cardiology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts
    Search for articles by this author
  • Xiaochun Li
    Affiliations
    Department of Biostatistics, Indiana University School of Medicine & Richard M. Fairbanks School of Public Health, Indianapolis, Indiana
    Search for articles by this author
  • Shien-Fong Lin
    Affiliations
    Krannert Institute of Cardiology and Division of Cardiology, Department of Medicine, Indiana University School of Medicine, Indianapolis, Indiana

    Institute of Biomedical Engineering, National Chiao-Tung University, Hsin-Chu, Taiwan
    Search for articles by this author
  • Thomas H. Everett IV
    Affiliations
    Krannert Institute of Cardiology and Division of Cardiology, Department of Medicine, Indiana University School of Medicine, Indianapolis, Indiana
    Search for articles by this author
  • Peng-Sheng Chen
    Correspondence
    Address reprint requests and correspondence: Dr Peng-Sheng Chen, Cedars-Sinai Medical Center, 8700 Beverly Blvd, Davis 1016, Los Angeles, CA 90048.
    Affiliations
    Krannert Institute of Cardiology and Division of Cardiology, Department of Medicine, Indiana University School of Medicine, Indianapolis, Indiana

    Cedars-Sinai Medical Center, Los Angeles, California
    Search for articles by this author
Published:November 24, 2020DOI:https://doi.org/10.1016/j.hrthm.2020.11.023

      Background

      Sympathetic nerve activity, heart rate (HR), and blood pressure (BP) all have very low frequency (VLF), low frequency (LF), and high frequency (HF) oscillations.

      Objective

      The purpose of this study was to test the hypothesis that the frequency spectra of subcutaneous nerve activity (ScNA), stellate ganglion nerve activity (SGNA), HR, and BP are important to cardiac arrhythmogenesis.

      Methods

      We used radiotransmitters to record SGNA, ScNA, HR, and BP in 6 ambulatory dogs and determined the dominant frequency and paroxysmal atrial tachyarrhythmias (PATs) episodes in 3-minute windows over a 24-hour period.

      Results

      The frequency spectra determined in ScNA reflected that in SGNA. HF oscillations were present in both ScNA and SGNA at all time but could be overshadowed by the much larger LF and VLF burst activities. The dominant frequency could occur in any of the 3 frequency bands. There were circadian variations with more frequent occurrences of HF oscillations at night. HF oscillations in HR and BP matched HF oscillations in SGNA and ScNA. PATs occurred only when dominant frequencies of SGNA and ScNA were in the LF and VLF bands.

      Conclusion

      HF oscillations in BP and HR correlate with HF oscillations in sympathetic nerve activity and are present at all time. HF oscillations can be overshadowed by the much larger LF and VLF burst activities. PATs occur only when LF or VLF, but not when HF, is the dominant frequency. The frequency spectra determined in ScNA reflect that in SGNA.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic and Personal
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Heart Rhythm
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Barman S.M.
        2019 Ludwig Lecture: rhythms in sympathetic nerve activity are a key to understanding neural control of the cardiovascular system.
        Am J Physiol Regul Integr Comp Physiol. 2019; 318: R191-R205
        • Usui H.
        • Nishida Y.
        The very low-frequency band of heart rate variability represents the slow recovery component after a mental stress task.
        PLoS One. 2017; 12e0182611
        • Sassi R.
        • Cerutti S.
        • Lombardi F.
        • et al.
        Advances in heart rate variability signal analysis: joint position statement by the e-Cardiology ESC Working Group and the European Heart Rhythm Association co-endorsed by the Asia Pacific Heart Rhythm Society.
        Europace. 2015; 17: 1341-1353
        • St Croix C.M.
        • Satoh M.
        • Morgan B.J.
        • Skatrud J.B.
        • Dempsey J.A.
        Role of respiratory motor output in within-breath modulation of muscle sympathetic nerve activity in humans.
        Circ Res. 1999; 85: 457-469
        • Cogliati C.
        • Magatelli R.
        • Montano N.
        • Narkiewicz K.
        • Somers V.K.
        Detection of low- and high-frequency rhythms in the variability of skin sympathetic nerve activity.
        Am J Physiol Heart Circ Physiol. 2000; 278: H1256-H1260
        • Reyes del Paso G.A.
        • Langewitz W.
        • Mulder L.J.
        • 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: 477-487
        • Burr R.L.
        Interpretation of normalized spectral heart rate variability indices in sleep research: a critical review.
        Sleep. 2007; 30: 913-919
        • Pagani M.
        • Malliani A.
        Interpreting oscillations of muscle sympathetic nerve activity and heart rate variability.
        J Hypertens. 2000; 18: 1709-1719
        • Rizas K.D.
        • Nieminen T.
        • Barthel P.
        • et al.
        Sympathetic activity-associated periodic repolarization dynamics predict mortality following myocardial infarction.
        J Clin Invest. 2014; 124: 1770-1780
        • Liu X.
        • Rabin P.L.
        • Yuan Y.
        • et al.
        Effects of anesthetic and sedative agents on sympathetic nerve activity.
        Heart Rhythm. 2019; 16: 1875-1882
        • Hart E.C.
        • Head G.A.
        • Carter J.R.
        • et al.
        Recording sympathetic nerve activity in conscious humans and other mammals: guidelines and the road to standardization.
        Am J Physiol Heart Circ Physiol. 2017; 312: H1031-H1051
        • Robinson E.A.
        • Rhee K.S.
        • Doytchinova A.
        • et al.
        Estimating sympathetic tone by recording subcutaneous nerve activity in ambulatory dogs.
        J Cardiovasc Electrophysiol. 2015; 26: 70-78
        • Tsai W.-C.
        • Chan Y.H.
        • Chinda K.
        • et al.
        Effects of renal sympathetic denervation on the stellate ganglion and the brain stem in dogs.
        Heart Rhythm. 2017; 14: 255-262
        • Wan J.
        • Chen M.
        • Yuan Y.
        • et al.
        Antiarrhythmic and proarrhythmic effects of subcutaneous nerve stimulation in ambulatory dogs.
        Heart Rhythm. 2019; 16: 1251-1260
        • Rajendra Acharya U.
        • Paul Joseph K.
        • Kannathal N.
        • Lim C.M.
        • Suri J.S.
        Heart rate variability: a review.
        Med Biol Eng Comput. 2006; 44: 1031-1051
        • Choi E.K.
        • Shen M.J.
        • Han S.
        • et al.
        Intrinsic cardiac nerve activity and paroxysmal atrial tachyarrhythmia in ambulatory dogs.
        Circulation. 2010; 121: 2615-2623
        • Cao J.M.
        • Fishbein M.C.
        • Han J.B.
        • et al.
        Relationship between regional cardiac hyperinnervation and ventricular arrhythmia.
        Circulation. 2000; 101: 1960-1969
        • Pagani M.
        • Lombardi F.
        • Guzzetti S.
        • et al.
        Power spectral analysis of heart rate and arterial pressure variabilities as a marker of sympatho-vagal interaction in man and conscious dog.
        Circ Res. 1986; 59: 178-193
        • Kabir R.A.
        • Doytchinova A.
        • Liu X.
        • et al.
        Crescendo skin sympathetic nerve activity and ventricular arrhythmia.
        J Am Coll Cardiol. 2017; 70: 3201-3202
        • Kusayama T.
        • Wan J.
        • Doytchinova A.
        • et al.
        Skin sympathetic nerve activity and the temporal clustering of cardiac arrhythmias.
        JCI Insight. 2019; 4e125853
        • Priori S.G.
        • Wilde A.A.
        • Horie M.
        • et al.
        HRS/EHRA/APHRS expert consensus statement on the diagnosis and management of patients with inherited primary arrhythmia syndromes.
        Heart Rhythm. 2013; 10: 1932-1963
        • Vaseghi M.
        • Barwad P.
        • Malavassi Corrales F.J.
        • et al.
        Cardiac sympathetic denervation for refractory ventricular arrhythmias.
        J Am Coll Cardiol. 2017; 69: 3070-3080
        • Taniguchi T.
        • Morimoto M.
        • Taniguchi Y.
        • Takasaki M.
        • Totoki T.
        Cutaneous distribution of sympathetic postganglionic fibers from stellate ganglion: a retrograde axonal tracing study using wheat germ agglutinin conjugated with horseradish peroxidase.
        J Anesth. 1994; 8: 441-449
        • Doytchinova A.
        • Hassel J.L.
        • Yuan Y.
        • et al.
        Simultaneous noninvasive recording of skin sympathetic nerve activity and electrocardiogram.
        Heart Rhythm. 2017; 14: 25-33
        • Uradu A.
        • Wan J.
        • Doytchinova A.
        • et al.
        Skin sympathetic nerve activity precedes the onset and termination of paroxysmal atrial tachycardia and fibrillation.
        Heart Rhythm. 2017; 14: 964-971