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Hyperoxia-induced alterations in cardiovascular function and autonomic control during return to normoxic breathing

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Abstract

Hyperoxia causes hemodynamic alterations. We hypothesized that cardiovascular and autonomic control changes last beyond the end of hyperoxic period into normoxia. Ten healthy volunteers were randomized to breathe either medical air or 100% oxygen for 45 min in a double-blind study design. Measurements were performed before (baseline) and during gas exposure, and then 10, 30, 60, and 90 min after gas exposure. Hemodynamic changes were studied by Doppler echocardiography. Changes in cardiac and vasomotor autonomic control were evaluated through changes in spectral power of heart rate variability and blood pressure variability. Cardiac baroreflex sensitivity was assessed by the sequence method. Hyperoxia significantly decreased heart rate and increased the high frequency power of heart rate variability, suggesting a chemoreflex increase in vagal activity since the slope of cardiac baroreflex was significantly decreased during hyperoxia. Hyperoxia increased significantly the systemic vascular resistances and decreased the low frequency power of blood pressure variability, suggesting that hyperoxic vasoconstriction was not supported by an increase in vascular sympathetic stimulation. These changes lasted for 10 min after hyperoxia (p < 0.05). After the end of hyperoxic exposure, the shift of the power spectral distribution of heart rate variability toward a pattern of increased cardiac sympathetic activity lasted for 30 min (p < 0.05), reflecting a resuming of baseline autonomic balance. Cardiac output and stroke volume were significantly decreased during hyperoxia and returned to baseline values (10 min) later than heart rate. In conclusion, hyperoxia effects continue during return to normoxic breathing, but cardiac and vascular parameters followed different time courses of recovery.

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References

  • Bak Z, Sjöberg F, Rousseau A, Steinvall I, Janerot-Sjoberg B (2007) Human cardiovascular dose-response to supplemental oxygen. Acta Physiol 191:15–24

    Article  CAS  Google Scholar 

  • Bandali K, Belanger M, Wittnich C (2004) Hyperoxia causes oxygen free radical-mediated membrane injury and alters myocardial function and hemodynamics in the newborn. Am J Physiol 287:H553–H559

    CAS  Google Scholar 

  • Beauchamps KG (1973) Non-stationary processes. In: Allen G & Unwin Ltd (ed) Signal processing using analog and digital techniques, pp 505–535

  • Bouhaddi M, Delbosc B, Fortrat J, Henriet M, Cappelle S, Ducloux D, Chalopin J, Regnard J (2004) Six-month cardiovascular changes in cyclosporine-treated recipients of corneal grafts: serial baroreflex responses. Transpl Int 17:325–333

    Article  PubMed  CAS  Google Scholar 

  • Cabrales P, Tsai A, Intaglietta M (2006) Nitric oxide regulation of microvascular oxygen exchange during hypoxia and hyperoxia. J Appl Physiol 100:1181–1187

    Article  PubMed  CAS  Google Scholar 

  • Daly W, Bondurant S (1962) 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 41:126–132

    Article  PubMed  CAS  Google Scholar 

  • Eckenhoff R, Knight D (1984) Cardiac arrhythmias and heart rate changes in prolonged hyperbaric air exposures. Undersea Biomed Res 1:355–367

    Google Scholar 

  • Eggers G, Paley H, Leonard J, Warren J (1962) Hemodynamic response to oxygen breathing in man. J Appl Physiol 17:75–79

    CAS  Google Scholar 

  • Ganz W, Donoso R, Marcus H, Swan H (1972) Coronary hemodynamics and myocardial oxygen metabolism during oxygen breathing in patients with and without coronary artery disease. Circulation 65:763–768

    Google Scholar 

  • Houssière A, Najem B, Cuylits N, Cuypers S, Naeije R, Van De Borne P (2006) Hyperoxia enhances metaboreflexe sensitivity during static exercise in humans. Am J Physiol 291:H210–H215

    Google Scholar 

  • Jammes Y, Steinberg J, Bregeon F, Delliaux S (2004) The oxidative stress in response to routine incremental cycling exercise in healthy sedentary subjects. Respir Physiol Neurobiol 144:81–90

    Article  PubMed  CAS  Google Scholar 

  • La Rovere M, Pinna G, Raczak G (2008) Baroreflex sensitivity: measurement and clinical implications. Ann Noninvasive Electrocardiol 13:191–207

    Article  PubMed  Google Scholar 

  • Laitinen T, Hartikainen J, Niskanen L, Geleen G, Länsimies E (1999) Sympatovagal balance is major determinant of short-term blood pressure variability in healthy subjects. Am J Physiol 276:H1245–H1252

    PubMed  CAS  Google Scholar 

  • Larsson A, Uusijärvi J, Eksborg S, Lindholm P (2010) Tissue oxygenation measured with near-infrared spectroscopy during normobaric and hyperbaric oxygen breathing in healthy subjects. Eur J Appl Physiol 109:757–761. doi:10.1007/s00421-008-0955-8

    Article  PubMed  CAS  Google Scholar 

  • Liard J, Kunert M (1993) Hemodynamic changes induced by low blood oxygen affinity in dogs. Am J Physiol 33:R396–R401

    Google Scholar 

  • Lund V, Kentala E, Scheinin H, Klossner J, Helenius H, Sariola-Heinonen K, Jalonen J (1999) Heart rate variability in healthy volunteers during normobaric and hyperbaric hyperoxia. Acta Physiol 167:29–35

    Article  CAS  Google Scholar 

  • Mak S, Azevedo E, Liu P, Newton G (2001) Effect of hyperoxia on left ventricular function and filling pressures in congestive patients with and without heart failure. Chest 120:467–473

    Article  PubMed  CAS  Google Scholar 

  • Milone S, Newton G, Parker J (1999) Hemodynamic and biochemical effects of 100% oxygen breathing in humans. Can J Physiol Pharmacol 77:124–130

    Article  PubMed  CAS  Google Scholar 

  • Molenat F, Boussuges A, Grandfond A, Rostain J, Sainty J, Robinet C, Galland F, Meliet J (2004) Modifications of cardiovascular function secondary to hyperbaric hyperoxia in healthy volunteers: an echocardiographic and Doppler study. Clin Sci 106:389–395

    Article  PubMed  Google Scholar 

  • Pagani M, Lombardi F, Guzzandi S, Rimoldi O, Furlan R, Pizzinelli P, Sandrone G, Malfatto G, Dell’Orto S, Piccaluga E, Turiel M, Baselli G, Cerutti S, Malliani A (1986) Power spectral analysis of heart rate and arterial pressure variabilities as a marker of sympatho–vagal interaction in man and conscious dog. Circ Res 59:178–193

    PubMed  CAS  Google Scholar 

  • Pasgaard T, Stankevicius E, Jorgensen M, Ostergaard L, Simonsen U, Frobert O (2007) Hyperoxia reduces basal release of nitric oxide and contracts porcine coronary arteries. Acta Physiol 191:285–296

    Article  CAS  Google Scholar 

  • Rossi P, Boussuges A (2005) Hyperoxia-induced arterial compliance decrease in healthy man. Clin Physiol Funct Imag 25:10–15

    Article  Google Scholar 

  • Rousseau A, Bak Z, Janerot-Sjöberg B, Sjöberg F (2005) Acute hyperoxaemia-induced effects on regional blood flow, oxygen consumption and central circulation in man. Acta Physiol Scand 183:231–240

    Article  PubMed  CAS  Google Scholar 

  • Rubanyi G, Vanhoutte P (1986) Superoxide anions and hyperoxia inactivate endothelium-derived relaxing factor. Am J Physiol 250:H822–H827

    PubMed  CAS  Google Scholar 

  • Seals D, Johnson G, Fregosi R (1991) Hyperoxia lowers sympathetic activity at rest but not during exercise in humans. Am J Physiol 260:R873–R878

    PubMed  CAS  Google Scholar 

  • Shepherd A, Granger H, Smith E, Guyton C (1973) Local control of tissue oxygen delivery and its contribution to the regulation of cardiac output. Am J Physiol 225:747–755

    PubMed  CAS  Google Scholar 

  • Shibata M, Kairong Q, Ichioka S, Kamiya A (2006) Vascular wall energetics in arterioles during nitric oxide-dependent and-independent vasodilation. J Appl Physiol 100:1793–1798

    Article  PubMed  CAS  Google Scholar 

  • Sole J, Hussain M (1977) A simple specific radioenzymatic assay for the simultaneous measurement of pictogram quantities of norepinephrine, epinephrine and dopamine in plasma and tissues. Biochem Med 18:301–304

    Article  PubMed  CAS  Google Scholar 

  • Stickland M, Morgan B, Dempsey J (2008) Carotid chemoreceptor modulation of sympathetic vasoconstrictor outflow during exercise in healthy humans. J Physiol 586:1743–1754

    Article  PubMed  CAS  Google Scholar 

  • Task Force of the European Society of Cardiology and the North American Society of Pacing Electrophysiology (1996) Heart rate variability: standards of measurement, physiological interpretation, and clinical use. Circulation 93:1043–1065

    Google Scholar 

  • Teisseire B, Ropars C, Vallez M, Herigault R, Nicolau C (1985) Physiological effects of high-P50 erythrocyte transfusion on piglets. J Appl Physiol 58:1810–1817

    PubMed  CAS  Google Scholar 

  • Thomson A, Drummond G, Waring S, Webb D, Maxwell S (2006) Effects of short-term isocapnic hyperoxia and hypoxia on cardiovascular function. J Appl Physiol 101:809–816

    Article  PubMed  CAS  Google Scholar 

  • Uchiyama M, Mihara M (1978) Determination of malonedialdehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 86:271–278

    Article  PubMed  CAS  Google Scholar 

  • Waring W, Thomson A, Adwani S, Rosseel A, Potter J, Webb D, Maxwell S (2003) Cardiovascular effects of acute oxygen administration in healthy adults. J Cardiovasc Pharmacol 42:245–250

    Article  PubMed  CAS  Google Scholar 

  • Weaver L, Curchill S (2001) Pulmonary edema associated with hyperbaric oxygen therapy. Chest 120:1407–1409

    Article  PubMed  CAS  Google Scholar 

  • Wilson J, Kligfield P, Adams G, Harvey C, Schaefer K (1977) Human ECG changes during prolonged hyperbaric exposures breathing N2–O2 mixtures. J Appl Physiol 42:614–623

    PubMed  CAS  Google Scholar 

  • Yamamoto Y, Hughson R (1991) Coarse-graining spectral analysis: new method for studying heart rate variability. J Appl Physiol 71:1143–1150

    PubMed  CAS  Google Scholar 

  • Yamazaki F, Takahara K, Sone R, Johnson J (2007) Influence of hyperoxia on skin vasomotor control in normothermic and head-stressed humans. J Appl Physiol 103:2026–2033

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Christine Humbert-Téna (Explorations Fonctionnelles Respiratoires, Hôpital Marseille Nord, Marseille, France) and Jessica Vincent, Patricia Jan and Christiane Vincent (Explorations fonctionnelles-Physiologie, Centre Hospitalier Universitaire Minjoz, Besançon, France) for their expert technical assistance. This work was supported by the French Ministry of Defence (contract no. 08co708).

Conflict of interest

The authors have no conflicts of interest.

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Authors and Affiliations

  1. Département des Environnements Opérationnels-Environnements Extrêmes, Institut de Recherche Biomédicale des Armées (IRBA)-Antenne Toulon, Boulevard Sainte Anne BP 20548, 83041, Toulon Cedex 9, France

    Yoann Gole, Ombeline Gargne & Alain Boussuges

  2. UMR-MD2, Physiologie et Physiopathologie en Conditions d’Oxygénation Extrême (P2COE), Institut de Recherche Biomédicale des Armées et Université de la Méditerranée, Marseille, France

    Yoann Gole, Ombeline Gargne, Mathieu Coulange, Jean-Guillaume Steinberg, Yves Jammes & Alain Boussuges

  3. Service de Médecine Subaquatique et Hyperbare, Pôle RUSH, Assistance Publique Hôpitaux de Marseille, CHU Sainte Marguerite, Marseille, France

    Mathieu Coulange

  4. EA3920, Université de Franche Comté et Centre Hospitalier Universitaire de Besançon, Besançon, France

    Malika Bouhaddi & Jacques Regnard

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  1. Yoann Gole
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  2. Ombeline Gargne
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  7. Jacques Regnard
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  8. Alain Boussuges
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Correspondence to Yoann Gole.

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Communicated by Guido Ferretti.

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Gole, Y., Gargne, O., Coulange, M. et al. Hyperoxia-induced alterations in cardiovascular function and autonomic control during return to normoxic breathing. Eur J Appl Physiol 111, 937–946 (2011). https://doi.org/10.1007/s00421-010-1711-4

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