Cited by 1,401Heart Rate Variability and Autonomic ControlVagus Nerve Stimulation ResearchNon-Invasive Vital Sign Monitoring

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The LF/HF ratio does not accurately measure cardiac sympatho-vagal balance

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Billman, George E.·2013·Frontiers in Physiology

DOI 10.3389/fphys.2013.00026PMC PMC3576706

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OPINION article Front. Physiol., 20 February 2013Sec. Clinical and Translational Physiology Volume 4 - 2013 | https://doi.org/10.3389/fphys.2013.00026

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Figure 1 An illustration of the possible non-linear effects of varying cardiac sympathetic and cardiac parasympathetic nerve activity on LF/HF. This graph was constructed using the following formula (derived from a synthesis of the literature, particularly Randall et al., 1991; Taylor et al., 2001; Cohen and Taylor, 2002): LF/HF = (0.5 parasympathetic + 0.25 sympathetic nerve activity)/(0.9 parasympathetic + 0.1 sympathetic nerve activity). The nerve activity was varied from baseline (1 arbitrary unit each) increasing or decreasing by up to a factor of 10 (i.e., from 0.1 to 10 units).CC BY · PubMed Central

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Heart Rate Variability: Standards of Measurement, Physiological Interpretation, and Clinical Use
Electrophysiology, T. F. O. T. E. S. O. C. T. N. A. (1996) · Circulation · doi:10.1161/01.cir.93.5.1043 · Cited by 17,159
Heart rate variability: Standards of measurement, physiological interpretation, and clinical use
Malik, M., Bigger, J. T., Camm, A. J., Kleiger, R. E., Malliani, A., Moss, A. J., & Schwartz, P. J. (1996) · European Heart Journal · doi:10.1093/oxfordjournals.eurheartj.a014868 · Cited by 15,289
Heart rate variability: standards of measurement, physiological interpretation and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology.
(1996) · PubMed · Cited by 5,666
Power Spectrum Analysis of Heart Rate Fluctuation: A Quantitative Probe of Beat-to-Beat Cardiovascular Control
Akselrod, S., Gordon, D., Ubel, F. A., Shannon, D. C., Berger, A. C., & Cohen, R. J. (1981) · Science · doi:10.1126/science.6166045 · Cited by 5,079
Power spectral analysis of heart rate and arterial pressure variabilities as a marker of sympatho-vagal interaction in man and conscious dog.
Pagani, M., Lombardi, F., Guzzetti, S., Rimoldi, O., Furlan, R., Pizzinelli, P., Sandrone, G., Malfatto, G., Dell'Orto, S., & Piccaluga, E. (1986) · Circulation Research · doi:10.1161/01.res.59.2.178 · Cited by 4,130
Decreased heart rate variability and its association with increased mortality after acute myocardial infarction
Kleiger, R. E., Miller, J. P., Bigger, J. T., & Moss, A. J. (1987) · The American Journal of Cardiology · doi:10.1016/0002-9149(87)90795-8 · Cited by 3,995
Heart rate variability: origins, methods, and interpretive caveats
BERNTSON, G. G., THOMAS BIGGER, J., ECKBERG, D. L., GROSSMAN, P., KAUFMANN, P. G., MALIK, M., NAGARAJA, H. N., PORGES, S. W., SAUL, J. P., STONE, P. H., et al. (1997) · Psychophysiology · doi:10.1111/j.1469-8986.1997.tb02140.x · Cited by 3,962
Cardiovascular neural regulation explored in the frequency domain.
Malliani, A., Pagani, M., Lombardi, F., & Cerutti, S. (1991) · Circulation · doi:10.1161/01.cir.84.2.482 · Cited by 3,569
The relationship of autonomic imbalance, heart rate variability and cardiovascular disease risk factors
Thayer, J. F., Yamamoto, S. S., & Brosschot, J. F. (2010) · International Journal of Cardiology · doi:10.1016/j.ijcard.2009.09.543 · Cited by 2,276
Respiratory sinus arrhythmia in humans: how breathing pattern modulates heart rate
Hirsch, J. A., & Bishop, B. (1981) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1981.241.4.h620 · Cited by 1,105
Sympathovagal Balance: A Critical Appraisal
Eckberg, D. L. (1997) · Circulation · doi:10.1161/01.cir.96.9.3224 · Cited by 1,087
Norepinephrine spillover to plasma in patients with congestive heart failure: evidence of increased overall and cardiorenal sympathetic nervous activity.
Hasking, G. J., Esler, M. D., Jennings, G. L., Burton, D., Johns, J. A., & Korner, P. I. (1986) · Circulation · doi:10.1161/01.cir.73.4.615 · Cited by 1,028
Respiratory Sinus Arrhythmia
Yasuma, F., & Hayano, J.-I. (2004) · Chest · doi:10.1378/chest.125.2.683 · Cited by 907
Brief Reviews
Levy, M. N. (1971) · Circulation Research · doi:10.1161/01.res.29.5.437 · Cited by 798
Heart Rate Variability ? A Historical Perspective
Billman, G. E. (2011) · Frontiers in Physiology · doi:10.3389/fphys.2011.00086 · Cited by 786
Self-citation
Important influence of respiration on human R-R interval power spectra is largely ignored
Brown, T. E., Beightol, L. A., Koh, J., & Eckberg, D. L. (1993) · Journal of Applied Physiology · doi:10.1152/jappl.1993.75.5.2310 · Cited by 770
Assessment of autonomic regulation in chronic congestive heart failure by heart rate spectral analysis
Saul, J. P., Arai, Y., Berger, R. D., Lilly, L. S., Colucci, W. S., & Cohen, R. J. (1988) · The American Journal of Cardiology · doi:10.1016/0002-9149(88)91172-1 · Cited by 706
Human sinus arrhythmia as an index of vagal cardiac outflow.
Eckberg, D. L. (1983) · Journal of Applied Physiology · doi:10.1152/jappl.1983.54.4.961 · Cited by 633
Beat to beat variability in cardiovascular variables: Noise or music?
Appel, M. L., Berger, R. D., Saul, J. P., Smith, J. M., & Cohen, R. J. (1989) · Journal of the American College of Cardiology · doi:10.1016/0735-1097(89)90408-7 · Cited by 557
Respiratory sinus arrhythmia: a frequency dependent phenomenon
Angelone, A., & Coulter, N. A. (1964) · Journal of Applied Physiology · doi:10.1152/jappl.1964.19.3.479 · Cited by 441 · cited 6×
“Conversely, reductions in respiratory frequency increase HRV (Angelone and Coulter, 1964; Melcher, 1976; Hirsch and Bishop, 1981; Brown et al., 1993) while decreases in tidal volume lead to reductions in the R–R interval variability (Davies and Neilson, 1967; Melcher, 1976; Hirsch and Bishop, 1981; Eckberg, 1983; Koll…”
BackgroundInfluential
Heart rate spectral analysis, cardiac norepinephrine spillover, and muscle sympathetic nerve activity during human sympathetic nervous activation and failure.
Kingwell, B. A., Thompson, J. M., Kaye, D. M., McPherson, G. A., Jennings, G., & Esler, M. (1994) · Circulation · doi:10.1161/01.cir.90.1.234 · Cited by 401
Short‐term cardiovascular oscillations in man: measuring and modelling the physiologies
Cohen, M. A., & Taylor, J. A. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.017483 · Cited by 359
Cardiac vagal efferent activity and heart period in the carotid sinus reflex
Katona, P. G., Poitras, J., Barnett, G., & Terry, B. (1970) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1970.218.4.1030 · Cited by 342
Methodological issues in the quantification of respiratory sinus arrhythmia.
Denver, J. W., Reed, S. F., & Porges, S. W. (2007) · Biological Psychology · doi:10.1016/j.biopsycho.2005.09.005 · Cited by 333
Point:Counterpoint: Cardiovascular variability is/is not an index of autonomic control of circulation
Parati, G., Mancia, G., Rienzo, M. D., & Castiglioni, P. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00446.2006 · Cited by 325
Low-frequency component of the heart rate variability spectrum: a poor marker of sympathetic activity
Houle, M. S., & Billman, G. E. (1999) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1999.276.1.h215 · Cited by 305
Self-citation
Respiratory sinus arrhythmia in the denervated human heart
Bernardi, L., Keller, F., Sanders, M., Reddy, P. S., Griffith, B., Meno, F., & Pinsky, M. R. (1989) · Journal of Applied Physiology · doi:10.1152/jappl.1989.67.4.1447 · Cited by 272
Sympathetic restraint of respiratory sinus arrhythmia: implications for vagal-cardiac tone assessment in humans
Taylor, J. A., Myers, C. W., Halliwill, J. R., Seidel, H., & Eckberg, D. L. (2001) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2001.280.6.h2804 · Cited by 249
Cardiac autonomic neural remodeling and susceptibility to sudden cardiac death: effect of endurance exercise training
Billman, G. E. (2009) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00534.2009 · Cited by 237
Self-citation
Influence of cardiac neural inputs on rhythmic variations of heart period in the cat
Chess, G. F., Tam, R., & Calaresu, F. R. (1975) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1975.228.3.775 · Cited by 217
Reproducibility and relation to mean heart rate of heart rate variability in normal subjects and in patients with congestive heart failure secondary to coronary artery disease
Hoogenhuyze, D. C. A. V., Weinstein, N., Martin, G. J., Weiss, J. S., Schaad, J. W., Sahyouni, X. N., Fintel, D. J., Remme, W. J., & Singer, D. H. (1991) · The American Journal of Cardiology · doi:10.1016/0002-9149(91)90327-h · Cited by 207
Supine low-frequency power of heart rate variability reflects baroreflex function, not cardiac sympathetic innervation
Moak, J. P., Goldstein, D. S., Eldadah, B. A., Saleem, A., Holmes, C., Pechnik, S., & Sharabi, Y. (2007) · Heart Rhythm · doi:10.1016/j.hrthm.2007.07.019 · Cited by 203
Human autonomic rhythms: vagal cardiac mechanisms in tetraplegic subjects.
Koh, J., Brown, T. E., Beightol, L. A., Ha, C. Y., & Eckberg, D. L. (1994) · The Journal of Physiology · doi:10.1113/jphysiol.1994.sp020039 · Cited by 186
Effect of physiologic and pharmacologic adrenergic stimulation on heart rate variability
Ahmed, M. W., Kadish, A. H., Parker, M. A., & Goldberger, J. J. (1994) · Journal of the American College of Cardiology · doi:10.1016/0735-1097(94)90874-5 · Cited by 173
Power spectral density of heart rate variability as an index of sympatho-vagal interaction in normal and hypertensive subjects.
Pagani, M., Lombardi, F., Guzzetti, S., Sandrone, G., Rimoldi, O. E., Malfatto, G., Cerutti, S., & Malliani, A. (1984) · PubMed · Cited by 157
Nonlinearities of the human carotid baroreceptor-cardiac reflex.
Eckberg, D. L. (1980) · Circulation Research · doi:10.1161/01.res.47.2.208 · Cited by 154
Respiratory sinus arrhythmia is a limited measure of cardiac parasympathetic control in man.
Kollai, M., & Mizsei, G. (1990) · The Journal of Physiology · doi:10.1113/jphysiol.1990.sp018070 · Cited by 146
Low-frequency Spectral Power of Heart Rate Variability Is Not a Specific Marker of Cardiac Sympathetic Modulation
Hopf, H., Skyschally, A., Heusch, G., & Peters, J. (1995) · Anesthesiology · doi:10.1097/00000542-199503000-00002 · Cited by 143
Sinus arrhythmia in man at rest.
Ct, D., & Neilson, J. M. M. (1967) · Journal of Applied Physiology · doi:10.1152/jappl.1967.22.5.947 · Cited by 142
Dissociation of heart rate variability from parasympathetic tone
Goldberger, J. J., Ahmed, M. W., Parker, M. A., & Kadish, A. H. (1994) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1994.266.5.h2152 · Cited by 137
Time-series analysis of heart rate variability during submaximal exercise. Evidence for reduced cardiac vagal tone in animals susceptible to ventricular fibrillation.
Billman, G. E., & Hoskins, R. S. (1989) · Circulation · doi:10.1161/01.cir.80.1.146 · Cited by 133
Self-citation
SA nodal parasympathectomy delineates autonomic control of heart rate power spectrum
Randall, D. C., Brown, D. R., Raisch, R. M., Yingling, J. D., & Randall, W. C. (1991) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1991.260.3.h985 · Cited by 132
The diving response in man: effects on sympathetic activity in muscle and skin nerve fascicles.
Fagius, J., & Sundlöf, G. (1986) · The Journal of Physiology · doi:10.1113/jphysiol.1986.sp016196 · Cited by 131
Accentuated antagonism in the control of human heart rate
Uijtdehaage, S. H. J., & Thayer, J. F. (2000) · Clinical Autonomic Research · doi:10.1007/bf02278013 · Cited by 129
The high frequency component of heart rate variability reflects cardiac parasympathetic modulation rather than parasympathetic ‘tone’
Hedman, A. E., Hartikainen, J. E. K., Tahvanainen, K. U. O., & Hakumäki, M. O. K. (1995) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1995.tb09973.x · Cited by 128
Sympathovagal Balance: A Critical Appraisal
Malík, M. (1998) · Circulation · doi:10.1161/01.cir.98.23.2643 · Cited by 118
Power spectral analysis of heart rate variability and autonomic nervous system activity measured directly in healthy dogs and dogs with tachycardia-induced heart failure
Piccirillo, G., Ogawa, M., Song, J., Chong, V. J., Joung, B., Han, S., Magrì, D., Chen, L. S., Lin, S., & Chen, P. (2009) · Heart Rhythm · doi:10.1016/j.hrthm.2009.01.006 · Cited by 114
Alterations of an average heart rate change heart rate variability due to mathematical reasons
Sacha, J., & Pluta, W. (2007) · International Journal of Cardiology · doi:10.1016/j.ijcard.2007.06.047 · Cited by 107
Dynamic changes in cardiac vagal tone as measured by time-series analysis
Billman, G. E., & Dujardin, J. P. (1990) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1990.258.3.h896 · Cited by 97
Self-citation
Respiratory sinus arrhythmia in man. A study in heart rate regulating mechanisms.
Melcher, A. (1976) · PubMed · Cited by 90
The relation between respiration and the pulse‐rate
Bainbridge, F. A. (1920) · The Journal of Physiology · doi:10.1113/jphysiol.1920.sp001918 · Cited by 86
Limitations of the use of spectral analysis of heart rate variability for the estimation of cardiac sympathetic activity in heart failure
Notarius, C. F. (2001) · EP Europace · doi:10.1053/eupc.2000.0136 · Cited by 85
Contribution to Heart Rate Variability by Mechanoelectric Feedback
Horner, S. M., Murphy, C., Coen, B., Dick, D. J., Harrison, F. G., Vespalcova, Z., & Lab, M. J. (1996) · Circulation · doi:10.1161/01.cir.94.7.1762 · Cited by 83
Different methods of heart rate variability analysis reveal different correlations of heart rate variability spectrum with average heart rate
Sacha, J., & Pluta, W. (2005) · Journal of Electrocardiology · doi:10.1016/j.jelectrocard.2004.09.015 · Cited by 81
Carotid baroreceptor-muscle sympathetic relation in humans
Rea, R. F., & Eckberg, D. L. (1987) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1987.253.6.r929 · Cited by 78
Heart rate recovery after exercise: a predictor of ventricular fibrillation susceptibility after myocardial infarction
Smith, L. L., Kukielka, M., & Billman, G. E. (2004) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00785.2004 · Cited by 77
Self-citation
Circulatory responses from lung inflation in anesthetized dogs
HAINSWORTH, R. (1974) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1974.226.2.247 · Cited by 76
Sympathetic-parasympathetic interaction and accentuated antagonism in conscious dogs
Stramba‐Badiale, M., Vanoli, E., Ferrari, G. M. D., Cerati, D., Foreman, R. D., & Schwartz, P. J. (1991) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1991.260.2.h335 · Cited by 76
Increased cardiac sympathetic nerve activity in heart failure is not due to desensitization of the arterial baroreflex
Watson, A. M. D., Hood, S. G., Ramchandra, R., McAllen, R. M., & May, C. N. (2007) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00147.2007 · Cited by 68
Trigeminal‐baroreceptor reflex interactions modulate human cardiac vagal efferent activity.
Eckberg, D. L., Mohanty, S. K., & Raczkowska, M. (1984) · The Journal of Physiology · doi:10.1113/jphysiol.1984.sp015054 · Cited by 66
Effect of endurance exercise training on heart rate onset and heart rate recovery responses to submaximal exercise in animals susceptible to ventricular fibrillation
Billman, G. E., & Kukielka, M. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00793.2006 · Cited by 62
Self-citation
Supine low-frequency power of heart rate variability reflects baroreflex function, not cardiac sympathetic innervation
Moak, J. P., Goldstein, D. S., Eldadah, B. A., Saleem, A., Holmes, C. S., Pechnik, S., & Sharabi, Y. (2009) · Cleveland Clinic Journal of Medicine · doi:10.3949/ccjm.76.s2.11 · Cited by 60
Importance of ventilation in modulating interaction between sympathetic drive and cardiovascular variability
van de Borne, P., Montano, N., Narkiewicz, K., Degaute, J.-P., Malliani, A., Pagani, M., & Somers, V. K. (2001) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2001.280.2.h722 · Cited by 58
Continual recordings of cardiac sympathetic nerve activity in conscious sheep
Jardine, D. L., Charles, C. J., Melton, I. C., May, C. N., Forrester, M. D., FRAMPTON, C. M. A., Bennett, S. I., & Ikram, H. (2002) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2002.282.1.h93 · Cited by 43
The correlation between heart period variability and mean period length
Fleiss, J. L., Bigger, J. T., & Rolnitzky, L. M. (1992) · Statistics in Medicine · doi:10.1002/sim.4780110111 · Cited by 29

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Authors: Billman, G. E.
Affiliations: The Ohio State University (US)
Corresponding author: Billman, George E.
Venue: Frontiers in Physiology
Publisher: Frontiers Media SA
Published: 2013
Volume: 4
Pages: 26-26
ISSN: 1664-042X (ISSN-L)
DOI: 10.3389/fphys.2013.00026
PMC: PMC3576706
OpenAlex: W2107161633
Cited by: 1,401
References: 65
Citations by year: 2026: 177 · 2025: 140 · 2024: 122 · 2023: 123 · 2022: 134 · 2021: 130 · 2020: 115 · 2019: 107 · 2018: 121 · 2017: 98 · 2016: 54 · 2015: 36 · 2014: 29 · 2013: 14
FWCI: 30.11
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Frontiers in Physiology (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Topics: Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
Physical Sciences › Engineering › Biomedical Engineering › Non-Invasive Vital Sign Monitoring
Keywords: LF/HF ratio, heart rate variability, autonomic nervous system

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The LF/HF ratio does not accurately measure cardiac sympatho-vagal balance

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