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CC BY-NC-ND 4.0 · Int J Sports Med 2020; 41(04): 209-218
DOI: 10.1055/a-1028-7496
Physiology & Biochemistry
Eigentümer und Copyright ©Georg Thieme Verlag KG 2018

Effect of Lower Body Negative Pressure on Phase I Cardiovascular Responses at Exercise Onset

Nazzareno Fagoni
1   Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy
,
Paolo Bruseghini
1   Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy
,
Alessandra Adami
2   Department of Kinesiology, University of Rhode Island, United States
,
Carlo Capelli
3   Department of Physical Performances, Norwegian School of Sport Sciences, Oslo, Norway
,
Frederic Lador
4   Division de Pneumologie, Département des Spécialités de Médecine, Hôpitaux Universitaires de Genève, Geneva, Switzerland
,
Christian Moia
5   Département des Neurosciences Fondamentales, Université de Genève Centre Médical Universitaire, Geneve, Switzerland
,
Enrico Tam
6   Dipartimento di Scienze Neurologiche e della Visione, University of Verona, Verona, Italy
,
Aurélien Bringard
7   University Medical Center, Basic Neurosciences, Geneva, Switzerland
,
Guido Ferretti
5   Département des Neurosciences Fondamentales, Université de Genève Centre Médical Universitaire, Geneve, Switzerland
› Author Affiliations Funding This study was supported by Swiss National Science Foundation Grants 32003B_127620 and 3200B0-114033 to Guido Ferretti.
Further Information

Publication History



accepted 30 September 2019

Publication Date:
20 January 2020 (online)

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Abstract

We hypothesised that vagal withdrawal and increased venous return interact in determining the rapid cardiac output (CO) response (phase I) at exercise onset. We used lower body negative pressure (LBNP) to increase blood distribution to the heart by muscle pump action and reduce resting vagal activity. We expected a larger increase in stroke volume (SV) and smaller for heart rate (HR) at progressively stronger LBNP levels, therefore CO response would remain unchanged. To this aim ten young, healthy males performed a 50 W exercise in supine position at 0 (Control), −15, −30 and −45 mmHg LBNP exposure. On single beat basis, we measured HR, SV, and CO. Oxygen uptake was measured breath-by-breath. Phase I response amplitudes were obtained applying an exponential model. LBNP increased SV response amplitude threefold from Control to −45 mmHg. HR response amplitude tended to decrease and prevented changes in CO response. The rapid response of CO explained that of oxygen uptake. The rapid SV kinetics at exercise onset is compatible with an increased venous return, whereas the vagal withdrawal conjecture cannot be dismissed for HR. The rapid CO response may indeed be the result of two independent yet parallel mechanisms, one acting on SV, the other on HR.

Key words

cardiac output - stroke volume - heart rate - oxygen uptake - kinetics and exercise transient - LBNP
 

  • References

  • 1 Whipp BJ, Ward SA, Lamarra N. et al. Parameters of ventilatory and gas exchange dynamics during exercise. J Appl Physiol 1982; 52: 1506-1513
    CrossrefPubMedGoogle Scholar
  • 2 Wasserman K, Whipp BJ, Castagna J.. Cardiodynamic hyperpnea: Hyperpnea secondary to cardiac output increase. J Appl Physiol 1974; 36: 457-464
    CrossrefPubMedGoogle Scholar
  • 3 di Prampero PE.. Energetics of muscular exercise. Rev Physiol Biochem Pharmacol 1981; 89: 143-222
    PubMedGoogle Scholar
  • 4 Poole DC, Jones AM.. Oxygen uptake kinetics. Compr Physiol 2012; 2: 933-996
    CrossrefPubMedGoogle Scholar
  • 5 Whipp BJ, Ward SA.. Physiological determinants of pulmonary gas exchange kinetics during exercise. Med Sci Sports Exerc 1990; 22: 62-71
    PubMedGoogle Scholar
  • 6 Ferretti G.. Energetics of Muscular Exercise. Cham: Springer International Publishing; 2015
    Google Scholar
  • 7 Barstow TJ, Molé PA.. Simulation of pulmonary O2 uptake during exercise transients in humans. J Appl Physiol (1985) 1987; 63: 2253-2261
    CrossrefPubMedGoogle Scholar
  • 8 Cummin AR, Iyawe VI, Mehta N. et al. Ventilation and cardiac output during the onset of exercise, and during voluntary hyperventilation, in humans. J Physiol 1986; 370: 567-583
    CrossrefPubMedGoogle Scholar
  • 9 De Cort SC, Innes JA, Barstow TJ. et al. Cardiac output, oxygen consumption and arteriovenous oxygen difference following a sudden rise in exercise level in humans. J Physiol 1991; 441: 501-512
    CrossrefPubMedGoogle Scholar
  • 10 Yoshida T, Yamamoto K, Udo M.. Relationship between cardiac output and oxygen uptake at the onset of exercise. Eur J Appl Physiol Occup Physiol 1993; 66: 155-160
    CrossrefPubMedGoogle Scholar
  • 11 Lador F, Azabji Kenfack M, Moia C. et al. Simultaneous determination of the kinetics of cardiac output, systemic O(2) delivery, and lung O(2) uptake at exercise onset in men. Am J Physiol Regul Integr Comp Physiol 2006; 290: R1071-R1079
    CrossrefPubMedGoogle Scholar
  • 12 Lador F, Tam E, Azabji Kenfack M. et al. Phase I dynamics of cardiac output, systemic O2 delivery, and lung O2 uptake at exercise onset in men in acute normobaric hypoxia. Am J Physiol Regul Integr Comp Physiol 2008; 295: R624-R632
    CrossrefPubMedGoogle Scholar
  • 13 Fagraeus L, Linnarsson D.. Autonomic origin of heart rate fluctuations at the onset of muscular exercise. J Appl Physiol 1976; 40: 679-682
    CrossrefPubMedGoogle Scholar
  • 14 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
    CrossrefPubMedGoogle Scholar
  • 15 Sundblad P, Haruna Y, Tedner B. et al. Short-term cardiovascular responses to rapid whole-body tilting during exercise. Eur J Appl Physiol 2000; 81: 259-270
    CrossrefPubMedGoogle Scholar
  • 16 Buchheit M, Richard R, Doutreleau S. Effect of acute hypoxia on heart rate variability at rest and during exercise. Int J Sports Med 2004; 25: 264-269
    Article in Thieme ConnectPubMedGoogle Scholar
  • 17 Xie A, Skatrud JB, Puleo DS. et al. Exposure to hypoxia produces long-lasting sympathetic activation in humans. J Appl Physiol (1985) 2001; 91: 1555-1562
    CrossrefPubMedGoogle Scholar
  • 18 Leyk D, Essfeld D, Hoffmann U. et al. Postural effect on cardiac output, oxygen uptake and lactate during cycle exercise of varying intensity. Eur J Appl Physiol Occup Physiol 1994; 68: 30-35
    CrossrefPubMedGoogle Scholar
  • 19 Sheriff DD, Zhou XP, Scher AM. et al. Dependence of cardiac filling pressure on cardiac output during rest and dynamic exercise in dogs. Am J Physiol 1993; 265: H316-H322
    PubMedGoogle Scholar
  • 20 Laughlin MH.. Skeletal muscle blood flow capacity: Role of muscle pump in exercise hyperemia. Am J Physiol 1987; 253: H993-H1004
    PubMedGoogle Scholar
  • 21 Linnarsson D, Sundberg CJ, Tedner B. et al. Blood pressure and heart rate responses to sudden changes of gravity during exercise. Am J Physiol 1996; 270: H2132-H2142
    PubMedGoogle Scholar
  • 22 Schneider SM, Watenpaugh DE, Lee SMC. et al. Lower-body negative-pressure exercise and bed-rest-mediated orthostatic intolerance. Med Sci Sports Exerc 2002; 34: 1446-1453
    CrossrefPubMedGoogle Scholar
  • 23 Nóbrega AC, Williamson JW, Garcia JA. et al. Mechanisms for increasing stroke volume during static exercise with fixed heart rate in humans. J Appl Physiol (1985) 1997; 83: 712-717
    CrossrefPubMedGoogle Scholar
  • 24 Convertino VA.. Endurance exercise training: Conditions of enhanced hemodynamic responses and tolerance to LBNP. Med Sci Sports Exerc 1993; 25: 705-712
    PubMedGoogle Scholar
  • 25 Hargens AR, Bhattacharya R, Schneider SM.. Space physiology VI: Exercise, artificial gravity, and countermeasure development for prolonged space flight. Eur J Appl Physiol 2013; 113: 2183-2192
    CrossrefPubMedGoogle Scholar
  • 26 Floras JS, Butler GC, Ando SI. et al. Differential sympathetic nerve and heart rate spectral effects of nonhypotensive lower body negative pressure. Am J Physiol Regul Integr Comp Physiol 2001; 281: R468-R475
    CrossrefPubMedGoogle Scholar
  • 27 Harriss DJ, Macsween A, Atkinson G.. Standards for ethics in sport and exercise science research: 2020 update. Int J Sports Med 2019; 40: 813-817
    Article in Thieme ConnectPubMedGoogle Scholar
  • 28 Wesseling KH, Jansen JR, Settels JJ. et al. Computation of aortic flow from pressure in humans using a nonlinear, three-element model. J Appl Physiol (1985) 1993; 74: 2566-2573
    CrossrefPubMedGoogle Scholar
  • 29 Barker RC, Hopkins SR, Kellogg N. et al. Measurement of cardiac output during exercise by open-circuit acetylene uptake. J Appl Physiol (1985) 1999; 87: 1506-1512
    CrossrefPubMedGoogle Scholar
  • 30 Azabji Kenfack M, Lador F, Licker M. et al. Cardiac output by Modelflow® method from intra-arterial and fingertip pulse pressure profiles. Clin Sci (Lond) 2004; 106: 365-369
    CrossrefPubMedGoogle Scholar
  • 31 Tam E, Azabji Kenfack M, Cautero M. et al. Correction of cardiac output obtained by Modelflow from finger pulse pressure profiles with a respiratory method in humans. Clin Sci (Lond) 2004; 106: 371-376
    CrossrefPubMedGoogle Scholar
  • 32 Grønlund J.. A new method for breath-to-breath determination of oxygen flux across the alveolar membrane. Eur J Appl Physiol Occup Physiol 1984; 52: 167-172
    CrossrefPubMedGoogle Scholar
  • 33 Capelli C, Cautero M, di Prampero PE.. New perspectives in breath-by-breath determination of alveolar gas exchange in humans. Pflugers Arch 2001; 441: 566-577
    CrossrefPubMedGoogle Scholar
  • 34 Capelli C, Carlo C, Cautero M. et al. Algorithms, modelling and VO₂ kinetics. Eur J Appl Physiol 2011; 111: 331-342
    PubMedGoogle Scholar
  • 35 van Lieshout JJ, Toska K, van Lieshout EJ. et al. Beat-to-beat noninvasive stroke volume from arterial pressure and Doppler ultrasound. Eur J Appl Physiol 2003; 90: 131-137
    CrossrefPubMedGoogle Scholar
  • 36 Adami A, Fagoni N, Ferretti G.. The Q˙-V˙O2 diagram: An analytical interpretation of oxygen transport in arterial blood during exercise in humans. Respir Physiol Neurobiol 2014; 193: 55-61
    CrossrefPubMedGoogle Scholar
  • 37 Ferretti G, Fagoni N, Taboni A. et al. The physiology of submaximal exercise: The steady state concept. Respir Physiol Neurobiol 2017; 246: 76-85
    CrossrefPubMedGoogle Scholar
  • 38 Bringard A, Adami A, Moia C. et al. A new interpolation-free procedure for breath-by-breath analysis of oxygen uptake in exercise transients. Eur J Appl Physiol 2014; 114: 1983-1994
    CrossrefPubMedGoogle Scholar
  • 39 Carson ER, Cobelli C, Finkelstein L.. The Mathematical Modeling of Metabolic and Endocrine Systems: Model Formulation, Identification, and Validation. Wiley; 1983
    CrossrefGoogle Scholar
  • 40 Fontolliet T, Pichot V, Bringard A. et al. Testing the vagal withdrawal hypothesis during light exercise under autonomic blockade: A heart rate variability study. J Appl Physiol 2018; DOI: 10.1152/japplphysiol.00619.2018.
    CrossrefPubMedGoogle Scholar
  • 41 McNarry MA, Kingsley MIC, Lewis MJ.. Relationship between changes in pulmonary V̇O2 kinetics and autonomic regulation of blood flow. Scand J Med Sci Sports 2014; 24: 613--621
    CrossrefPubMedGoogle Scholar
  • 42 Feroldi P, Belleri M, Ferretti G. et al. Heart rate overshoot at the beginning of muscle exercise. Eur J Appl Physiol Occup Physiol 1992; 65: 8-12
    CrossrefPubMedGoogle Scholar
  • 43 Elstad M, Nådland IH, Toska K. et al. Stroke volume decreases during mild dynamic and static exercise in supine humans. Acta Physiol (Oxf) 2009; 195: 289-300
    CrossrefPubMedGoogle Scholar
  • 44 Eriksen M, Waaler BA, Walløe L. et al. Dynamics and dimensions of cardiac output changes in humans at the onset and at the end of moderate rhythmic exercise. J Physiol 1990; 426: 423-437
    CrossrefPubMedGoogle Scholar
  • 45 Faisal A, Beavers KR, Robertson AD. et al. Prior moderate and heavy exercise accelerate oxygen uptake and cardiac output kinetics in endurance athletes. J Appl Physiol (1985) 2009; 106: 1553-1563
    CrossrefPubMedGoogle Scholar
  • 46 Fu Q, Shibata S, Hastings JL. et al. Evidence for unloading arterial baroreceptors during low levels of lower body negative pressure in humans. Am J Physiol Heart Circ Physiol 2009; 296: H480-H488
    CrossrefPubMedGoogle Scholar
  • 47 Nishiyasu T, Shi X, Gillen CM. et al. Effects of dynamic exercise on cardiovascular regulation during lower body negative pressure. Aviat Space Environ Med 1993; 64: 517-521
    PubMedGoogle Scholar
  • 48 Spaak J, Montmerle S, Sundblad P. et al. Long-term bed rest-induced reductions in stroke volume during rest and exercise: Cardiac dysfunction vs. volume depletion. J Appl Physiol (1985) 2005; 98: 648-654
    CrossrefPubMedGoogle Scholar
  • 49 Beck KC, Randolph LN, Bailey KR. et al. Relationship between cardiac output and oxygen consumption during upright cycle exercise in healthy humans. J Appl Physiol (1985) 2006; 101: 1474-1480
    CrossrefPubMedGoogle Scholar
  • 50 Chung DC, Niranjan SC, Clark JW. et al. A dynamic model of ventricular interaction and pericardial influence. Am J Physiol 1997; 272: H2942-H2962
    PubMedGoogle Scholar
  • 51 Naeije R, Badagliacca R.. The overloaded right heart and ventricular interdependence. Cardiovasc Res 2017; 113: 1474-1485
    CrossrefPubMedGoogle Scholar
  • 52 Sundblad P, Spaak J, Kaijser L.. Time courses of central hemodynamics during rapid changes in posture. J Appl Physiol (1985) 2014; 116: 1182-1188
    CrossrefPubMedGoogle Scholar
  • 53 Su J, Manisty C, Simonsen U. et al. Pulmonary artery wave propagation and reservoir function in conscious man: Impact of pulmonary vascular disease, respiration and dynamic stress tests. J Physiol 2017; 595: 6463-6476
    CrossrefPubMedGoogle Scholar
  • 54 Machhada A, Marina N, Korsak A. et al. Origins of the vagal drive controlling left ventricular contractility. J Physiol 2016; 594: 4017-4030
    CrossrefPubMedGoogle Scholar
  • 55 Drescher U, Koschate J, Schiffer T. et al. Analysis of cardio-pulmonary and respiratory kinetics in different body positions: Impact of venous return on pulmonary measurements. Eur J Appl Physiol 2016; 116: 1343-1353
    CrossrefPubMedGoogle Scholar
  • 56 Hoffmann U, Drescher U, Benson AP. et al. Skeletal muscle VO2 kinetics from cardio-pulmonary measurements: Assessing distortions through O2 transport by means of stochastic work-rate signals and circulatory modelling. Eur J Appl Physiol 2013; 113: 1745-1754
    CrossrefPubMedGoogle Scholar
  • 57 Chang CM, Cassuto Y, Pendergast DR. et al. Cardiorespiratory response to lower body negative pressure. Aviat Space Environ Med 1994; 65: 615-620
    PubMedGoogle Scholar
  • 58 Eiken O, Bjurstedt H.. Cardiac responses to lower body negative pressure and dynamic leg exercise. Eur J Appl Physiol Occup Physiol 1985; 54: 451-455
    CrossrefPubMedGoogle Scholar
  • 59 Pawelczyk JA, Raven PB.. Reductions in central venous pressure improve carotid baroreflex responses in conscious men. Am J Physiol 1989; 257: H1389-H1395
    PubMedGoogle Scholar
  • 60 Phillips AA, Bredin SSD, Cote AT. et al. Aortic distensibility is reduced during intense lower body negative pressure and is related to low frequency power of systolic blood pressure. Eur J Appl Physiol 2013; 113: 785-792
    CrossrefPubMedGoogle Scholar
  • 61 Cooke WH, Rickards CA, Ryan KL. et al. Muscle sympathetic nerve activity during intense lower body negative pressure to presyncope in humans. J Physiol 2009; 587: 4987-4999
    CrossrefPubMedGoogle Scholar
  • 62 Bringard A, Adami A, Fagoni N. et al. Dynamics of the RR-interval versus blood pressure relationship at exercise onset in humans. Eur J Appl Physiol 2017; 117: 619-630
    CrossrefPubMedGoogle Scholar
  • 63 Mack G, Nose H, Nadel ER.. Role of cardiopulmonary baroreflexes during dynamic exercise. J Appl Physiol (1985) 1988; 65: 1827-1832
    CrossrefPubMedGoogle Scholar
  • 64 Cui J, Wilson TE, Crandall CG.. Muscle sympathetic nerve activity during lower body negative pressure is accentuated in heat-stressed humans. J Appl Physiol (1985) 2004; 96: 2103-2108
    CrossrefPubMedGoogle Scholar