Importance of ventilation in modulating interaction between sympathetic drive and cardiovascular variability

Philippe Van De Borne, Nicola Montano, Krzysztof Narkiewicz, Jean P. Degaute, Alberto Malliani, Massimo Pagani, Virend Somers

Research output: Contribution to journalArticle

45 Citations (Scopus)

Abstract

Chemoreflex stimulation elicits both hyperventilation and sympathetic activation, each of which may have different influences on oscillatory characteristics of cardiovascular variability. We examined the influence of hyperventilation on the interactions between changes in R-R interval (RR) and muscle sympathetic nerve activity (MSNA) and changes in neurocirculatory variability, in 14 healthy subjects. We performed spectral analysis of RR and MSNA variability during each of the following interventions: 1) controlled breathing, 2) maximal end-expiratory apnea, 3) isocapnic voluntary hyperventilation, and 4) hypercapnia-induced hyperventilation. MSNA increased from 100% during controlled breathing to 170 ± 25% during apnea (P = 0.02). RR was unchanged, but normalized low-frequency (LF) variability of both RR and MSNA increased markedly (P < 0.001). During isocapnic hyperventilation, minute ventilation increased to 20.2 ± 1.4 l/min (P < 0.0001). During hypercapnic hyperventilation, minute ventilation also increased (to 19.7 ± 1.7 l/min) as did end-tidal CO2 (both P < 0.0001). MSNA remained unchanged during isocapnic hyperventilation (104 ± 7%) but increased to 241 ± 49% during hypercapnic hyperventilation (P < 0.01). RR decreased during both isocapnic and hypercapnic hyperventilation (P < 0.05). However, normalized LF variability of RR and of MSNA decreased (P < 0.05) during both isocapnic and hypercapnic hyperventilation, despite the tachycardia and heightened sympathetic nerve traffic. In conclusion, marked respiratory oscillations in autonomic drive induced by hyperventilation may induce dissociation between RR, MSNA, and neurocirculatory variability, perhaps by suppressing central genesis and/or inhibiting transmission of LF cardiovascular rhythms.

Original languageEnglish (US)
JournalAmerican Journal of Physiology - Heart and Circulatory Physiology
Volume280
Issue number2 49-2
StatePublished - Feb 2001

Fingerprint

Hyperventilation
Ventilation
Muscles
Apnea
Respiration
Hypercapnia
Tachycardia
Healthy Volunteers

Keywords

  • Apnea
  • Autonomic nervous system
  • Chemoreflexes
  • Hyperventilation
  • Spectral analysis

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)

Cite this

Importance of ventilation in modulating interaction between sympathetic drive and cardiovascular variability. / Van De Borne, Philippe; Montano, Nicola; Narkiewicz, Krzysztof; Degaute, Jean P.; Malliani, Alberto; Pagani, Massimo; Somers, Virend.

In: American Journal of Physiology - Heart and Circulatory Physiology, Vol. 280, No. 2 49-2, 02.2001.

Research output: Contribution to journalArticle

Van De Borne, Philippe ; Montano, Nicola ; Narkiewicz, Krzysztof ; Degaute, Jean P. ; Malliani, Alberto ; Pagani, Massimo ; Somers, Virend. / Importance of ventilation in modulating interaction between sympathetic drive and cardiovascular variability. In: American Journal of Physiology - Heart and Circulatory Physiology. 2001 ; Vol. 280, No. 2 49-2.
@article{4c58927389f442d0acd9768c8975c241,
title = "Importance of ventilation in modulating interaction between sympathetic drive and cardiovascular variability",
abstract = "Chemoreflex stimulation elicits both hyperventilation and sympathetic activation, each of which may have different influences on oscillatory characteristics of cardiovascular variability. We examined the influence of hyperventilation on the interactions between changes in R-R interval (RR) and muscle sympathetic nerve activity (MSNA) and changes in neurocirculatory variability, in 14 healthy subjects. We performed spectral analysis of RR and MSNA variability during each of the following interventions: 1) controlled breathing, 2) maximal end-expiratory apnea, 3) isocapnic voluntary hyperventilation, and 4) hypercapnia-induced hyperventilation. MSNA increased from 100{\%} during controlled breathing to 170 ± 25{\%} during apnea (P = 0.02). RR was unchanged, but normalized low-frequency (LF) variability of both RR and MSNA increased markedly (P < 0.001). During isocapnic hyperventilation, minute ventilation increased to 20.2 ± 1.4 l/min (P < 0.0001). During hypercapnic hyperventilation, minute ventilation also increased (to 19.7 ± 1.7 l/min) as did end-tidal CO2 (both P < 0.0001). MSNA remained unchanged during isocapnic hyperventilation (104 ± 7{\%}) but increased to 241 ± 49{\%} during hypercapnic hyperventilation (P < 0.01). RR decreased during both isocapnic and hypercapnic hyperventilation (P < 0.05). However, normalized LF variability of RR and of MSNA decreased (P < 0.05) during both isocapnic and hypercapnic hyperventilation, despite the tachycardia and heightened sympathetic nerve traffic. In conclusion, marked respiratory oscillations in autonomic drive induced by hyperventilation may induce dissociation between RR, MSNA, and neurocirculatory variability, perhaps by suppressing central genesis and/or inhibiting transmission of LF cardiovascular rhythms.",
keywords = "Apnea, Autonomic nervous system, Chemoreflexes, Hyperventilation, Spectral analysis",
author = "{Van De Borne}, Philippe and Nicola Montano and Krzysztof Narkiewicz and Degaute, {Jean P.} and Alberto Malliani and Massimo Pagani and Virend Somers",
year = "2001",
month = "2",
language = "English (US)",
volume = "280",
journal = "American Journal of Physiology - Renal Fluid and Electrolyte Physiology",
issn = "1931-857X",
publisher = "American Physiological Society",
number = "2 49-2",

}

TY - JOUR

T1 - Importance of ventilation in modulating interaction between sympathetic drive and cardiovascular variability

AU - Van De Borne, Philippe

AU - Montano, Nicola

AU - Narkiewicz, Krzysztof

AU - Degaute, Jean P.

AU - Malliani, Alberto

AU - Pagani, Massimo

AU - Somers, Virend

PY - 2001/2

Y1 - 2001/2

N2 - Chemoreflex stimulation elicits both hyperventilation and sympathetic activation, each of which may have different influences on oscillatory characteristics of cardiovascular variability. We examined the influence of hyperventilation on the interactions between changes in R-R interval (RR) and muscle sympathetic nerve activity (MSNA) and changes in neurocirculatory variability, in 14 healthy subjects. We performed spectral analysis of RR and MSNA variability during each of the following interventions: 1) controlled breathing, 2) maximal end-expiratory apnea, 3) isocapnic voluntary hyperventilation, and 4) hypercapnia-induced hyperventilation. MSNA increased from 100% during controlled breathing to 170 ± 25% during apnea (P = 0.02). RR was unchanged, but normalized low-frequency (LF) variability of both RR and MSNA increased markedly (P < 0.001). During isocapnic hyperventilation, minute ventilation increased to 20.2 ± 1.4 l/min (P < 0.0001). During hypercapnic hyperventilation, minute ventilation also increased (to 19.7 ± 1.7 l/min) as did end-tidal CO2 (both P < 0.0001). MSNA remained unchanged during isocapnic hyperventilation (104 ± 7%) but increased to 241 ± 49% during hypercapnic hyperventilation (P < 0.01). RR decreased during both isocapnic and hypercapnic hyperventilation (P < 0.05). However, normalized LF variability of RR and of MSNA decreased (P < 0.05) during both isocapnic and hypercapnic hyperventilation, despite the tachycardia and heightened sympathetic nerve traffic. In conclusion, marked respiratory oscillations in autonomic drive induced by hyperventilation may induce dissociation between RR, MSNA, and neurocirculatory variability, perhaps by suppressing central genesis and/or inhibiting transmission of LF cardiovascular rhythms.

AB - Chemoreflex stimulation elicits both hyperventilation and sympathetic activation, each of which may have different influences on oscillatory characteristics of cardiovascular variability. We examined the influence of hyperventilation on the interactions between changes in R-R interval (RR) and muscle sympathetic nerve activity (MSNA) and changes in neurocirculatory variability, in 14 healthy subjects. We performed spectral analysis of RR and MSNA variability during each of the following interventions: 1) controlled breathing, 2) maximal end-expiratory apnea, 3) isocapnic voluntary hyperventilation, and 4) hypercapnia-induced hyperventilation. MSNA increased from 100% during controlled breathing to 170 ± 25% during apnea (P = 0.02). RR was unchanged, but normalized low-frequency (LF) variability of both RR and MSNA increased markedly (P < 0.001). During isocapnic hyperventilation, minute ventilation increased to 20.2 ± 1.4 l/min (P < 0.0001). During hypercapnic hyperventilation, minute ventilation also increased (to 19.7 ± 1.7 l/min) as did end-tidal CO2 (both P < 0.0001). MSNA remained unchanged during isocapnic hyperventilation (104 ± 7%) but increased to 241 ± 49% during hypercapnic hyperventilation (P < 0.01). RR decreased during both isocapnic and hypercapnic hyperventilation (P < 0.05). However, normalized LF variability of RR and of MSNA decreased (P < 0.05) during both isocapnic and hypercapnic hyperventilation, despite the tachycardia and heightened sympathetic nerve traffic. In conclusion, marked respiratory oscillations in autonomic drive induced by hyperventilation may induce dissociation between RR, MSNA, and neurocirculatory variability, perhaps by suppressing central genesis and/or inhibiting transmission of LF cardiovascular rhythms.

KW - Apnea

KW - Autonomic nervous system

KW - Chemoreflexes

KW - Hyperventilation

KW - Spectral analysis

UR - http://www.scopus.com/inward/record.url?scp=0034997596&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0034997596&partnerID=8YFLogxK

M3 - Article

C2 - 11158971

AN - SCOPUS:0034997596

VL - 280

JO - American Journal of Physiology - Renal Fluid and Electrolyte Physiology

JF - American Journal of Physiology - Renal Fluid and Electrolyte Physiology

SN - 1931-857X

IS - 2 49-2

ER -