Influence of Hypoxia and Hypercapnia on Sleep State-Dependent Heart Rate Variability Behavior in Newborn Lambs

Although hypercapnia and/or hypoxia are frequently present during chronic lung disease of infancy and have also been implicated in sudden infant death syndrome (SIDS), their effect on cardiac autonomic regulation remains unclear. The authors' goal is to test that hypercapnia and hypoxia alter s...

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Published inSleep (New York, N.Y.) Vol. 35; no. 11; pp. 1541 - 9
Main Authors Beuchée, Alain, Hernández, Alfredo I., Duvareille, Charles, Daniel, David, Samson, Nathalie, Pladys, Patrick, Praud, Jean-Paul
Format Journal Article
LanguageEnglish
Published United States Oxford University Press 01.11.2012
Associated Professional Sleep Societies, LLC
Subjects
Online AccessGet full text
ISSN0161-8105
1550-9109
1550-9109
DOI10.5665/sleep.2206

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Abstract Although hypercapnia and/or hypoxia are frequently present during chronic lung disease of infancy and have also been implicated in sudden infant death syndrome (SIDS), their effect on cardiac autonomic regulation remains unclear. The authors' goal is to test that hypercapnia and hypoxia alter sleep-wake cycle-dependent heart rate variability (HRV) in the neonatal period. Experimental study measuring HRV during sleep states in lambs randomly exposed to hypercapnia, hypoxia, or air. University center for perinatal research in ovines (Sherbrooke, Canada). INSERM-university research unit for signal processing (Rennes, France). Six nonsedated, full-term lambs. Each lamb underwent polysomnographic recordings while in a chamber flowed with either air or 21% O(2) + 5% CO(2) (hypercapnia) or 10% O(2) + 0% CO(2) (hypoxia) on day 3, 4, and 5 of postnatal age. Hypercapnia increased the time spent in wakefulness and hypoxia the time spent in quiet sleep (QS). The state of alertness was the major determinant of HRV characterized with linear or nonlinear methods. Compared with QS, active sleep (AS) was associated with an overall increase in HRV magnitude and short-term self-similarity and a decrease in entropy of cardiac cycle length in air. This AS-related HRV pattern persisted in hypercapnia and was even more pronounced in hypoxia. Enhancement of AS-related sympathovagal coactivation in hypoxia, together with increased heart rate regularity, may be evidence that AS + hypoxia represent a particularly vulnerable state in early life. This should be kept in mind when deciding the optimal arterial oxygenation target in newborns and when investigating the potential involvement of hypoxia in SIDS pathogenesis.
AbstractList Although hypercapnia and/or hypoxia are frequently present during chronic lung disease of infancy and have also been implicated in sudden infant death syndrome (SIDS), their effect on cardiac autonomic regulation remains unclear. The authors' goal is to test that hypercapnia and hypoxia alter sleep-wake cycle-dependent heart rate variability (HRV) in the neonatal period. Experimental study measuring HRV during sleep states in lambs randomly exposed to hypercapnia, hypoxia, or air. University center for perinatal research in ovines (Sherbrooke, Canada). INSERM-university research unit for signal processing (Rennes, France). Six nonsedated, full-term lambs. Each lamb underwent polysomnographic recordings while in a chamber flowed with either air or 21% O(2) + 5% CO(2) (hypercapnia) or 10% O(2) + 0% CO(2) (hypoxia) on day 3, 4, and 5 of postnatal age. Hypercapnia increased the time spent in wakefulness and hypoxia the time spent in quiet sleep (QS). The state of alertness was the major determinant of HRV characterized with linear or nonlinear methods. Compared with QS, active sleep (AS) was associated with an overall increase in HRV magnitude and short-term self-similarity and a decrease in entropy of cardiac cycle length in air. This AS-related HRV pattern persisted in hypercapnia and was even more pronounced in hypoxia. Enhancement of AS-related sympathovagal coactivation in hypoxia, together with increased heart rate regularity, may be evidence that AS + hypoxia represent a particularly vulnerable state in early life. This should be kept in mind when deciding the optimal arterial oxygenation target in newborns and when investigating the potential involvement of hypoxia in SIDS pathogenesis.
Although hypercapnia and/or hypoxia are frequently present during chronic lung disease of infancy and have also been implicated in sudden infant death syndrome (SIDS), their effect on cardiac autonomic regulation remains unclear. The authors' goal is to test that hypercapnia and hypoxia alter sleep-wake cycle-dependent heart rate variability (HRV) in the neonatal period.STUDY OBJECTIVESAlthough hypercapnia and/or hypoxia are frequently present during chronic lung disease of infancy and have also been implicated in sudden infant death syndrome (SIDS), their effect on cardiac autonomic regulation remains unclear. The authors' goal is to test that hypercapnia and hypoxia alter sleep-wake cycle-dependent heart rate variability (HRV) in the neonatal period.Experimental study measuring HRV during sleep states in lambs randomly exposed to hypercapnia, hypoxia, or air.DESIGNExperimental study measuring HRV during sleep states in lambs randomly exposed to hypercapnia, hypoxia, or air.University center for perinatal research in ovines (Sherbrooke, Canada). INSERM-university research unit for signal processing (Rennes, France).SETTINGUniversity center for perinatal research in ovines (Sherbrooke, Canada). INSERM-university research unit for signal processing (Rennes, France).Six nonsedated, full-term lambs.PARTICIPANTSSix nonsedated, full-term lambs.Each lamb underwent polysomnographic recordings while in a chamber flowed with either air or 21% O(2) + 5% CO(2) (hypercapnia) or 10% O(2) + 0% CO(2) (hypoxia) on day 3, 4, and 5 of postnatal age.INTERVENTIONSEach lamb underwent polysomnographic recordings while in a chamber flowed with either air or 21% O(2) + 5% CO(2) (hypercapnia) or 10% O(2) + 0% CO(2) (hypoxia) on day 3, 4, and 5 of postnatal age.Hypercapnia increased the time spent in wakefulness and hypoxia the time spent in quiet sleep (QS). The state of alertness was the major determinant of HRV characterized with linear or nonlinear methods. Compared with QS, active sleep (AS) was associated with an overall increase in HRV magnitude and short-term self-similarity and a decrease in entropy of cardiac cycle length in air. This AS-related HRV pattern persisted in hypercapnia and was even more pronounced in hypoxia.MEASUREMENTS AND RESULTSHypercapnia increased the time spent in wakefulness and hypoxia the time spent in quiet sleep (QS). The state of alertness was the major determinant of HRV characterized with linear or nonlinear methods. Compared with QS, active sleep (AS) was associated with an overall increase in HRV magnitude and short-term self-similarity and a decrease in entropy of cardiac cycle length in air. This AS-related HRV pattern persisted in hypercapnia and was even more pronounced in hypoxia.Enhancement of AS-related sympathovagal coactivation in hypoxia, together with increased heart rate regularity, may be evidence that AS + hypoxia represent a particularly vulnerable state in early life. This should be kept in mind when deciding the optimal arterial oxygenation target in newborns and when investigating the potential involvement of hypoxia in SIDS pathogenesis.CONCLUSIONEnhancement of AS-related sympathovagal coactivation in hypoxia, together with increased heart rate regularity, may be evidence that AS + hypoxia represent a particularly vulnerable state in early life. This should be kept in mind when deciding the optimal arterial oxygenation target in newborns and when investigating the potential involvement of hypoxia in SIDS pathogenesis.
STUDY OBJECTIVES: Although hypercapnia and/or hypoxia are frequently present during chronic lung disease of infancy and have also been implicated in sudden infant death syndrome (SIDS), their effect on cardiac autonomic regulation remains unclear. The authors' goal is to test that hypercapnia and hypoxia alter sleep-wake cycle-dependent heart rate variability (HRV) in the neonatal period. DESIGN: Experimental study measuring HRV during sleep states in lambs randomly exposed to hypercapnia, hypoxia, or air. SETTING: University center for perinatal research in ovines (Sherbrooke, Canada). INSERM-university research unit for signal processing (Rennes, France). PARTICIPANTS: Six nonsedated, full-term lambs. INTERVENTIONS: Each lamb underwent polysomnographic recordings while in a chamber flowed with either air or 21% O(2) + 5% CO(2) (hypercapnia) or 10% O(2) + 0% CO(2) (hypoxia) on day 3, 4, and 5 of postnatal age. MEASUREMENTS AND RESULTS: Hypercapnia increased the time spent in wakefulness and hypoxia the time spent in quiet sleep (QS). The state of alertness was the major determinant of HRV characterized with linear or nonlinear methods. Compared with QS, active sleep (AS) was associated with an overall increase in HRV magnitude and short-term self-similarity and a decrease in entropy of cardiac cycle length in air. This AS-related HRV pattern persisted in hypercapnia and was even more pronounced in hypoxia. CONCLUSION: Enhancement of AS-related sympathovagal coactivation in hypoxia, together with increased heart rate regularity, may be evidence that AS + hypoxia represent a particularly vulnerable state in early life. This should be kept in mind when deciding the optimal arterial oxygenation target in newborns and when investigating the potential involvement of hypoxia in SIDS pathogenesis.
Author Samson, Nathalie
Daniel, David
Praud, Jean-Paul
Duvareille, Charles
Beuchée, Alain
Hernández, Alfredo I.
Pladys, Patrick
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crossref_primary_10_1159_000351035
crossref_primary_10_3389_fphys_2019_00468
crossref_primary_10_1007_s11517_018_1827_y
crossref_primary_10_1088_0967_3334_36_10_2089
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2012 Associated Professional Sleep Societies, LLC. 2012
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Issue 11
Keywords frequency domain analysis
Entropy
quiet sleep
sympathovagal coactivation
REM sleep
scale-invariance
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Snippet Although hypercapnia and/or hypoxia are frequently present during chronic lung disease of infancy and have also been implicated in sudden infant death syndrome...
STUDY OBJECTIVES: Although hypercapnia and/or hypoxia are frequently present during chronic lung disease of infancy and have also been implicated in sudden...
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SubjectTerms Animals
Animals, Newborn
Anoxia
Bioengineering
Heart Rate
Human health and pathology
Hypercapnia
Hypercapnia - physiopathology
Hypoxia - physiopathology
Hypoxia and Hypercapnia Effects on Sleep Heart Rate Variability in Lambs
Life Sciences
Pediatrics
Polysomnography
Polysomnography - methods
Sheep
Sleep
Wakefulness
Title Influence of Hypoxia and Hypercapnia on Sleep State-Dependent Heart Rate Variability Behavior in Newborn Lambs
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