Advertisement

Respiratory and heart rate dynamics during peripheral chemoreceptor deactivation compared to targeted sympathetic and sympathetic/parasympathetic (co-)activation

  • Author Footnotes
    1 Both authors contributed equally to this work.
    Katharina Apelt-Glitz
    Footnotes
    1 Both authors contributed equally to this work.
    Affiliations
    Division of Cardiology/Angiology/Intensive Care, EVK Düsseldorf, cNEP, cardiac Neuro- and Electrophysiology Research Consortium, Düsseldorf, Germany

    General Practice for Internal Medicine “Hausärzte im Stadtzentrum”, Schenefeld, Germany
    Search for articles by this author
  • Author Footnotes
    1 Both authors contributed equally to this work.
    Fares-Alexander Alken
    Correspondence
    Corresponding author at: Division of Cardiology/Angiology/Intensive Care, cNEP, Cardiac Neuro- and Electrophysiology Research Consortium, EVK Düsseldorf, Kirchfeldstr. 40, D-40217 Duesseldorf, Germany.
    Footnotes
    1 Both authors contributed equally to this work.
    Affiliations
    Division of Cardiology/Angiology/Intensive Care, EVK Düsseldorf, cNEP, cardiac Neuro- and Electrophysiology Research Consortium, Düsseldorf, Germany

    DZHK (German Center for Cardiovascular Research), partner site Hamburg/Kiel/Lübeck, Hamburg, Germany
    Search for articles by this author
  • Christiane Jungen
    Affiliations
    DZHK (German Center for Cardiovascular Research), partner site Hamburg/Kiel/Lübeck, Hamburg, Germany

    Department of Cardiology - University Heart & Vascular Centre, University Hospital Hamburg-Eppendorf, Hamburg, Germany
    Search for articles by this author
  • Katharina Scherschel
    Affiliations
    Division of Cardiology/Angiology/Intensive Care, EVK Düsseldorf, cNEP, cardiac Neuro- and Electrophysiology Research Consortium, Düsseldorf, Germany

    DZHK (German Center for Cardiovascular Research), partner site Hamburg/Kiel/Lübeck, Hamburg, Germany
    Search for articles by this author
  • Nikolaj Klöcker
    Affiliations
    Institute of Neural and Sensory Physiology, Medical Faculty and University Hospital Düsseldorf, Heinrich-Heine-University Düsseldorf, Germany.
    Search for articles by this author
  • Christian Meyer
    Affiliations
    Division of Cardiology/Angiology/Intensive Care, EVK Düsseldorf, cNEP, cardiac Neuro- and Electrophysiology Research Consortium, Düsseldorf, Germany

    DZHK (German Center for Cardiovascular Research), partner site Hamburg/Kiel/Lübeck, Hamburg, Germany

    Institute of Neural and Sensory Physiology, Medical Faculty and University Hospital Düsseldorf, Heinrich-Heine-University Düsseldorf, Germany.
    Search for articles by this author
  • Author Footnotes
    1 Both authors contributed equally to this work.

      Abstract

      Background

      The importance of peripheral chemoreceptors for cardiorespiratory neural control is known for decades. Pure oxygen inhalation deactivates chemoreceptors and increases parasympathetic outflow. However, the relationship between autonomic nervous system (ANS) activation and resulting respiratory as well as heart rate (HR) dynamics is still not fully understood.

      Methods

      In young adults the impact of (1) 100 % pure oxygen inhalation (hyperoxic cardiac chemoreflex sensitivity (CHRS) testing), (2) the cold face test (CFT) and (3) the cold pressor test (CPT) on heart rate variability (HRV), hemodynamics and respiratory rate was investigated in randomized order. Baseline ANS outflow was determined assessing respiratory sinus arrhythmia via deep breathing, baroreflex sensitivity and HRV.

      Results

      Baseline ANS outflow was normal in all participants (23 ± 1 years, 7 females, 3 males). Hyperoxic CHRS testing decreased HR (after 60 ± 3 vs before 63 ± 3 min−1, p = 0.004), while increasing total peripheral resistance (1053 ± 87 vs 988 ± 76 dyne*s + m2/cm5, p = 0.02) and mean arterial blood pressure (93 ± 4 vs 91 ± 4 mm Hg, p = 0.02). HRV indicated increased parasympathetic outflow after hyperoxic CHRS testing accompanied by a decrease in respiratory rate (15 ± 1vs 19 ± 1 min−1, p = 0.001). In contrast, neither CFT nor CPT altered the respiratory rate (18 ± 1 vs 18 ± 2 min−1, p = 0.38 and 18 ± 1 vs 18 ± 1 min−1, p = 0.84, respectively).

      Conclusion

      Changes in HR characteristics during deactivation of peripheral chemoreceptors but not during the CFT and CPT are related with a decrease in respiratory rate. This highlights the need of respiratory rate assessment when evaluating adaptations of cardiorespiratory chemoreceptor control.

      Keywords

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

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      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 Autonomic Neuroscience: Basic and Clinical
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Agelink M.W.
        • Malessa R.
        • Baumann B.
        • Majewski T.
        • Akila F.
        • Zeit T.
        • Ziegler D.
        Standardized tests of heart rate variability: normal ranges obtained from 309 healthy humans, and effects of age, gender, and heart rate.
        Clin. Auton. Res. 2001; 11: 99-108https://doi.org/10.1007/Bf02322053
        • Ardell J.L.
        • Andresen M.C.
        • Armour J.A.
        • Billman G.E.
        • Chen P.S.
        • Foreman R.D.
        • Herring N.
        • O'Leary D.S.
        • Sabbah H.N.
        • Schultz H.D.
        • Sunagawa K.
        • Zucker I.H.
        Translational neurocardiology: preclinical models and cardioneural integrative aspects.
        J. Physiol. 2016; 594: 3877-3909https://doi.org/10.1113/jp271869
        • Becker H.
        • Polo O.
        • McNamara S.G.
        • Berthon-Jones M.
        • Sullivan C.E.
        Ventilatory response to isocapnic hyperoxia.
        J. Appl. Physiol. 1995; 1985: 696-701https://doi.org/10.1152/jappl.1995.78.2.696
        • Bernardi L.
        • Spallone V.
        • Stevens M.
        • Hilsted J.
        • Frontoni S.
        • Pop-Busui R.
        • Ziegler D.
        • Kempler P.
        • Freeman R.
        • Low P.
        • Tesfaye S.
        • Valensi P.
        • <collab>Toronto Consensus Panel on Diabetic N.</collab>
        Methods of investigation for cardiac autonomic dysfunction in human research studies.
        Diabetes Metab. Res. Rev. 2011; 27: 654-664https://doi.org/10.1002/dmrr.1224
        • Boyett M.
        • Wang Y.
        • D'Souza A.
        CrossTalk opposing view: heart rate variability as a measure of cardiac autonomic responsiveness is fundamentally flawed.
        J. Physiol. 2019; 597: 2599-2601https://doi.org/10.1113/jp277501
        • Brown T.E.
        • Beightol L.A.
        • Koh J.
        • Eckberg D.L.
        Important influence of respiration on human R-R interval power spectra is largely ignored.
        J. Appl. Physiol. 1993; 75: 2310-2317https://doi.org/10.1152/jappl.1993.75.5.2310
        • Buckler K.J.
        TASK channels in arterial chemoreceptors and their role in oxygen and acid sensing.
        Pflugers Arch. 2015; 467: 1013-1025https://doi.org/10.1007/s00424-015-1689-1
        • Bureau M.A.
        • Lamarche J.
        • Foulon P.
        • Dalle D.
        Postnatal maturation of respiration in intact and carotid body-chemodenervated lambs.
        J. Appl. Physiol. 1985; 1985: 869-874https://doi.org/10.1152/jappl.1985.59.3.869
        • Burr R.L.
        Interpretation of normalized spectral heart rate variability indices in sleep research: a critical review.
        Sleep. 2007; 30: 913-919https://doi.org/10.1093/sleep/30.7.913
        • Daly W.J.
        • Bondurant S.
        Effects of oxygen breathing on the heart rate, blood pressure, and cardiac index of normal men–resting, with reactive hyperemia, and after atropine.
        J. Clin. Invest. 1962; 41: 126-132https://doi.org/10.1172/JCI104454
        • Dejours P.
        Chemoreflexes in breathing.
        Physiol. Rev. 1962; 42: 335-358https://doi.org/10.1152/physrev.1962.42.3.335
        • Donati A.
        • Damiani E.
        • Zuccari S.
        • Domizi R.
        • Scorcella C.
        • Girardis M.
        • Giulietti A.
        • Vignini A.
        • Adrario E.
        • Romano R.
        • Mazzanti L.
        • Pelaia P.
        • Singer M.
        Effects of short-term hyperoxia on erythropoietin levels and microcirculation in critically ill patients: a prospective observational pilot study.
        BMC Anesthesiol. 2017; 17https://doi.org/10.1186/s12871-017-0342-2
        • Drexel T.
        • Eickholt C.
        • Muhlsteff J.
        • Ritz A.
        • Siekiera M.
        • Kirmanoglou K.
        • Schulze V.
        • Shin D.I.
        • Balzer J.
        • Rassaf T.
        • Kelm M.
        • Meyer C.
        Vagal heart rate control in patients with atrial fibrillation: impact of tonic activation of peripheral chemosensory function in heart failure.
        Adv. Exp. Med. Biol. 2013; 755: 287-297https://doi.org/10.1007/978-94-007-4546-9_37
        • Fisher J.P.
        • Young C.N.
        • Fadel P.J.
        Autonomic adjustments to exercise in humans.
        Compr. Physiol. 2015; 5: 475-512https://doi.org/10.1002/cphy.c140022
        • Gautier H.
        • Bonora M.
        • Gaudy J.H.
        Ventilatory response of the conscious or anesthetized cat to oxygen breathing.
        Respir. Physiol. 1986; 65: 181-196https://doi.org/10.1016/0034-5687(86)90049-6
        • Gole Y.
        • Gargne O.
        • Coulange M.
        • Steinberg J.G.
        • Bouhaddi M.
        • Jammes Y.
        • Regnard J.
        • Boussuges A.
        Hyperoxia-induced alterations in cardiovascular function and autonomic control during return to normoxic breathing.
        Eur. J. Appl. Physiol. 2011; 111: 937-946https://doi.org/10.1007/s00421-010-1711-4
        • Graff B.
        • Szyndler A.
        • Czechowicz K.
        • Kucharska W.
        • Graff G.
        • Boutouyrie P.
        • Laurent S.
        • Narkiewicz K.
        Relationship between heart rate variability, blood pressure and arterial wall properties during air and oxygen breathing in healthy subjects.
        Auton. Neurosci. 2013; 178: 60-66https://doi.org/10.1016/j.autneu.2013.04.009
        • Gratze G.
        • Fortin J.
        • Holler A.
        • Grasenick K.
        • Pfurtscheller G.
        • Wach P.
        • Schönegger J.
        • Kotanko P.
        • Skrabal F.
        A software package for non-invasive, real-time beat-to-beat monitoring of stroke volume, blood pressure, total peripheral resistance and for assessment of autonomic function.An updated and improved software version for windows 95/NT and the complete biosig.
        Comput. Biol. Med. 1998; 28: 121-142https://doi.org/10.1016/s0010-4825(98)00005-5
        • Guyenet P.G.
        Regulation of breathing and autonomic outflows by chemoreceptors.
        Compr.Physiol. 2014; : 1511-1562https://doi.org/10.1002/cphy.c140004
        • Hayano J.
        • Yasuma F.
        • Okada A.
        • Mukai S.
        • Fujinami T.
        Respiratory sinus arrhythmia. A phenomenon improving pulmonary gas exchange and circulatory efficiency.
        Circulation. 1996; 94: 842-847https://doi.org/10.1161/01.cir.94.4.842
        • Hennersdorf M.G.
        • Hillebrand S.
        • Perings C.
        • Strauer B.E.
        Chemoreflexsensitivity in chronic heart failure patients.
        Eur. J. Heart Fail. 2001; 3: 679-684https://doi.org/10.1016/s1388-9842(01)00189-1
        • Hennersdorf M.G.
        • Niebch V.
        • Perings C.
        • Strauer B.E.
        Chemoreflex sensitivity as a predictor of arrhythmia relapse in ICD recipients.
        Int. J. Cardiol. 2002; 86: 169-175https://doi.org/10.1016/s0167-5273(02)00191-2
        • Hertzberg T.
        • Lagercrantz H.
        Postnatal sensitivity of the peripheral chemoreceptors in newborn infants.
        Arch. Dis. Child. 1987; 62: 1238-1241https://doi.org/10.1136/adc.62.12.1238
        • Hilz M.J.
        • Dütsch M.
        Quantitative studies of autonomic function.
        Muscle Nerve. 2006; 33: 6-20https://doi.org/10.1002/mus.20365
        • Honzíková N.
        • Závodná E.
        Baroreflex sensitivity in children and adolescents: physiology, hypertension, obesity,diabetes mellitus.
        Physiol. Res. 2016; : 879-889https://doi.org/10.33549/physiolres.933271
        • Iturriaga R.
        • Alcayaga J.
        • Chapleau M.W.
        • Somers V.K.
        Carotid body chemoreceptors: physiology, pathology, and implications for health and disease.
        Physiol. Rev. 2021; 101: 1177-1235https://doi.org/10.1152/physrev.00039.2019
        • Iturriaga R.
        • Del Rio R.
        • Idiaquez J.
        • Somers V.K.
        Carotid body chemoreceptors, sympathetic neural activation, and cardiometabolic disease.
        Biol. Res. 2016; 49https://doi.org/10.1186/s40659-016-0073-8
        • Khurana R.K.
        • Watabiki S.
        • Hebel J.R.
        • Toro R.
        • Nelson E.
        Cold face test in the assessment of trigeminal-brainstem-vagal function in humans.
        Ann. Neurol. 1980; 7: 144-149https://doi.org/10.1002/ana.410070209
        • Khurana R.K.
        • Wu R.
        The cold face test: a non-baroreflex mediated test of cardiac vagal function.
        Clin. Auton. Res. 2006; 16: 202-207https://doi.org/10.1007/s10286-006-0332-9
        • Kiss B.
        • Polska E.
        • Dorner G.
        • Polak K.
        • Findl O.
        • Mayrl G.F.
        • Eichler H.G.
        • Wolzt M.
        • Schmetterer L.
        Retinal blood flow during hyperoxia in humans revisited: concerted results using different measurement techniques.
        Microvasc. Res. 2002; 64: 75-85https://doi.org/10.1006/mvre.2002.2402
        • Kizuk S.A.D.
        • Vuong W.
        • Maclean J.E.
        • Dickson C.T.
        • Mathewson K.E.
        Electrophysiological correlates of hyperoxia during resting-state EEG in awake human subjects.
        Psychophysiology. 2019; 56e13401https://doi.org/10.1111/psyp.13401
        • Kuusela T.
        Methodological Aspects of Heart Rate Variability Analysis. 2012: 9-42
        • Lahiri S.
        • Edelman N.H.
        • Cherniack N.S.
        • Fishman A.P.
        Role of carotid chemoreflex in respiratory acclimatization to hypoxemia in goat and sheep.
        Respir. Physiol. 1981; 46: 367-382https://doi.org/10.1016/0034-5687(81)90132-8
        • Lund V.E.
        • Kentala E.
        • Scheinin H.
        • Klossner J.
        • Helenius H.
        • Sariola-Heinonen K.
        • Jalonen J.
        Heart rate variability in healthy volunteers during normobaric and hyperbaric hyperoxia.
        Acta Physiol. Scand. 1999; 167: 29-35https://doi.org/10.1046/j.1365-201x.1999.00581.x
        • Magagnin V.
        • Bassani T.
        • Bari V.
        • Turiel M.
        • Maestri R.
        • Pinna G.D.
        • Porta A.
        Non-stationarities significantly distort short-term spectral, symbolic and entropy heart rate variability indices.
        Physiol. Meas. 2011; 32: 1775-1786https://doi.org/10.1088/0967-3334/32/11/s05
        • Mak S.
        • Azevedo E.R.
        • Liu P.P.
        • Newton G.E.
        Effect of hyperoxia on left ventricular function and filling pressures in patients with and without congestive heart failure.
        Chest. 2001; 120: 467-473https://doi.org/10.1378/chest.120.2.467
        • Meyer C.
        • Heiss C.
        • Drexhage C.
        • Kehmeier E.S.
        • Balzer J.
        • Muhlfeld A.
        • Merx M.W.
        • Lauer T.
        • Kuhl H.
        • Floege J.
        • Kelm M.
        • Rassaf T.
        Hemodialysis-induced release of hemoglobin limits nitric oxide bioavailability and impairs vascular function.
        J. Am. Coll. Cardiol. 2010; 55: 454-459https://doi.org/10.1016/j.jacc.2009.07.068
        • Meyer C.
        • Morren G.
        • Muehlsteff J.
        • Heiss C.
        • Lauer T.
        • Schauerte P.
        • Rassaf T.
        • Purerfellner H.
        • Kelm M.
        Predicting neurally mediated syncope based on pulse arrival time: algorithm development and preliminary results.
        J. Cardiovasc. Electrophysiol. 2011; 22: 1042-1048https://doi.org/10.1111/j.1540-8167.2011.02030.x
        • Meyer C.
        • Rana O.R.
        • Saygili E.
        • Ozuyaman B.
        • Latz K.
        • Rassaf T.
        • Kelm M.
        • Schauerte P.
        Hyperoxic chemoreflex sensitivity is impaired in patients with neurocardiogenic syncope.
        Int. J. Cardiol. 2010; 142: 38-43https://doi.org/10.1016/j.ijcard.2008.12.081
        • Miao G.J.
        Signal Processing in Digital Communications. Artech House, Boston2007: 94-96
        • Milone S.D.
        • Newton G.E.
        • Parker J.D.
        Hemodynamic and biochemical effects of 100% oxygen breathing in humans.
        Can. J. Physiol. Pharmacol. 1999; 77: 124-130
        • Montano N.
        • Cogliati C.
        • Porta A.
        • Pagani M.
        • Malliani A.
        • Narkiewicz K.
        • Abboud F.M.
        • Birkett C.
        • Somers V.K.
        Central vagotonic effects of atropine modulate spectral oscillations of sympathetic nerve activity.
        Circulation. 1998; 98: 1394-1399https://doi.org/10.1161/01.cir.98.14.1394
        • Mourot L.
        • Bouhaddi M.
        • Regnard J.
        Effects of the cold pressor test on cardiac autonomic control in normal subjects.
        Physiol. Res. 2009; 83–91https://doi.org/10.33549/physiolres.931360
        • Niskanen J.P.
        • Tarvainen M.P.
        • Ranta-Aho P.O.
        • Karjalainen P.A.
        Software for advanced HRV analysis.
        Comput. Methods Prog. Biomed. 2004; 76: 73-81https://doi.org/10.1016/j.cmpb.2004.03.004
        • Paleczny B.
        • Seredynski R.
        • Tubek S.
        • Adamiec D.
        • Ponikowski P.
        • Ponikowska B.
        Hypoxic tachycardia is not a result of increased respiratory activity in healthy subjects.
        Exp. Physiol. 2019; 104: 476-489https://doi.org/10.1113/EP087233
        • Parati G.
        • Di Rienzo M.
        • Bertinieri G.
        • Pomidossi G.
        • Casadei R.
        • Groppelli A.
        • Pedotti A.
        • Zanchetti A.
        • Mancia G.
        Evaluation of the baroreceptor-heart rate reflex by 24-hour intra-arterial blood pressure monitoring in humans.
        Hypertension. 1988; 12: 214-222https://doi.org/10.1161/01.hyp.12.2.214
        • Pijacka W.
        • Moraes D.J.A.
        • Ratcliffe L.E.K.
        • Nightingale A.K.
        • Hart E.C.
        • Da Silva M.P.
        • Machado B.H.
        • McBryde F.D.
        • Abdala A.P.
        • Ford A.P.
        • Paton J.F.R.
        Purinergic receptors in the carotid body as a new drug target for controlling hypertension.
        Nat. Med. 2016; 22: 1151-1159https://doi.org/10.1038/nm.4173
        • Prabhakar N.R.
        • Peng Y.J.
        Peripheral chemoreceptors in health and disease.
        J. Appl. Physiol. 2004; 1985: 359-366https://doi.org/10.1152/japplphysiol.00809.2003
        • Prasad B.
        • Morgan B.J.
        • Gupta A.
        • Pegelow D.F.
        • Teodorescu M.
        • Dopp J.M.
        • Dempsey J.A.
        The need for specificity in quantifying neurocirculatory vs. respiratory effects of eucapnic hypoxia and transient hyperoxia.
        J. Physiol. 2020; 598: 4803-4819https://doi.org/10.1113/jp280515
        • Purves M.J.
        Respiratory and circulatory effects of breathing 100 per cent oxygen in the new-born lamb before and after denervation of the carotid chemoreceptors.
        J. Physiol. 1966; 185: 42-59https://doi.org/10.1113/jphysiol.1966.sp007971
        • Rassaf T.
        • Schueller P.
        • Westenfeld R.
        • Floege J.
        • Eickholt C.
        • Hennersdorf M.
        • Merx M.W.
        • Schauerte P.
        • Kelm M.
        • Meyer C.
        Peripheral chemosensor function is blunted in moderate to severe chronic kidney disease.
        Int. J. Cardiol. 2012; 155: 201-205https://doi.org/10.1016/j.ijcard.2010.09.054
        • Rodriguez E.
        • Echeverria J.C.
        • Alvarez-Ramirez J.
        Detrended fluctuation analysis of heart intrabeat dynamics.
        Phys.AStat.Mech.Applic. 2007; 384: 429-438https://doi.org/10.1016/j.physa.2007.05.022
        • Sato M.
        • Severinghaus J.W.
        • Powell F.L.
        • Xu F.D.
        • Spellman Jr., M.J.
        Augmented hypoxic ventilatory response in men at altitude.
        J. Appl. Physiol. 1992; 1985: 101-107https://doi.org/10.1152/jappl.1992.73.1.101
        • Schelegle E.S.
        • Green J.F.
        An overview of the anatomy and physiology of slowly adapting pulmonary stretch receptors.
        Respir. Physiol. 2001; 125: 17-31https://doi.org/10.1016/s0034-5687(00)00202-4
        • Seals D.R.
        • Johnson D.G.
        • Fregosi R.F.
        Hyperoxia lowers sympathetic activity at rest but not during exercise in humans.
        Am. J. Phys. 1991; 260: R873-R878https://doi.org/10.1152/ajpregu.1991.260.5.R873
        • Shaffer F.
        • Ginsberg J.P.
        An overview of heart rate variability metrics and norms.
        Front. Public Health. 2017; 5https://doi.org/10.3389/fpubh.2017.00258
        • Shykoff B.E.
        • Naqvi S.S.
        • Menon A.S.
        • Slutsky A.S.
        Respiratory sinus arrhythmia in dogs. Effects of phasic afferents and chemostimulation.
        J. Clin. Invest. 1991; 87: 1621-1627https://doi.org/10.1172/JCI115176
        • Siniaia M.S.
        • Young D.L.
        • Poon C.S.
        Habituation and desensitization of the Hering-Breuer reflex in rat.
        J. Physiol. 2000; 523: 479-491https://doi.org/10.1111/j.1469-7793.2000.t01-1-00479.x
        • Sinski M.
        • Lewandowski J.
        • Przybylski J.
        • Zalewski P.
        • Symonides B.
        • Abramczyk P.
        • Gaciong Z.
        Deactivation of carotid body chemoreceptors by hyperoxia decreases blood pressure in hypertensive patients.
        Hypertens. Res. 2014; 37: 858-862https://doi.org/10.1038/hr.2014.91
        • Somers V.K.
        • Mark A.L.
        • Abboud F.M.
        Interaction of baroreceptor and chemoreceptor reflex control of sympathetic nerve activity in normal humans.
        J. Clin. Invest. 1991; 87: 1953-1957https://doi.org/10.1172/JCI115221
        • Stewart J.M.
        • Rivera E.
        • Clarke D.A.
        • Baugham I.L.
        • Ocon A.J.
        • Taneja I.
        • Terilli C.
        • Medow M.S.
        Ventilatory baroreflex sensitivity in humans is not modulated by chemoreflex activation.
        Am. J. Physiol. Heart Circ. Physiol. 2011; 300: H1492-H1500https://doi.org/10.1152/ajpheart.01217.2010
        • Sundkvist G.
        • Almer L.
        • Lilja B.
        Respiratory influence on heart rate in diabetes mellitus.
        Br. Med. J. 1979; 1: 924-925https://doi.org/10.1136/bmj.1.6168.924
        • Task Force of the European Society of Cardiology
        • the North American Society of Pacing and Electrophysiology
        Heart rate variability: standards of measurement, physiological interpretation and clinical use..
        Circulation. 1996; 93: 1043-1065https://doi.org/10.1161/01.cir.93.5.1043
        • Tsuji H.
        • Venditti Jr., F.J.
        • Manders E.S.
        • Evans J.C.
        • Larson M.G.
        • Feldman C.L.
        • Levy D.
        Determinants of heart rate variability.
        J. Am. Coll. Cardiol. 1996; 28: 1539-1546https://doi.org/10.1016/s0735-1097(96)00342-7
        • Tulppo M.P.
        • Kiviniemi A.M.
        • Hautala A.J.
        • Kallio M.
        • Seppanen T.
        • Makikallio T.H.
        • Huikuri H.V.
        Physiological background of the loss of fractal heart rate dynamics.
        Circulation. 2005; 112: 314-319https://doi.org/10.1161/CIRCULATIONAHA.104.523712
        • Wang W.-Z.
        • Gao L.
        • Pan Y.-X.
        • Zucker I.H.
        • Wang W.
        Differential effects of cardiac sympathetic afferent stimulation on neurons in the nucleus tractus solitarius.
        Neurosci. Lett. 2006; 409: 146-150https://doi.org/10.1016/j.neulet.2006.09.032
        • Waring W.S.
        • Thomson A.J.
        • Adwani S.H.
        • Rosseel A.J.
        • Potter J.F.
        • Webb D.J.
        • Maxwell S.R.
        Cardiovascular effects of acute oxygen administration in healthy adults.
        J. Cardiovasc. Pharmacol. 2003; 42: 245-250https://doi.org/10.1097/00005344-200308000-00014
        • Whelan R.F.
        • Young I.M.
        The effect of adrenaline and noradrenaline infusions on respiration in man.
        Br. J. Pharmacol. Chemother. 1953; 8: 98-102https://doi.org/10.1111/j.1476-5381.1953.tb00759.x
        • Yeh R.G.
        • Shieh J.S.
        • Chen G.Y.
        • Kuo C.D.
        Detrended fluctuation analysis of short-term heart rate variability in late pregnant women.
        Auton. Neurosci. 2009; 150: 122-126https://doi.org/10.1016/j.autneu.2009.05.241