Sleep disordered breathing in children disrupts the maturation of autonomic control of heart rate and its association with cerebral oxygenation

Lisa M. Walter, Knarik Tamanyan, Aidan J. Weichard, Margot J. Davey, Gillian M. Nixon, Rosemary S.C. Horne

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Key points: Sleep disordered breathing (SDB) affects 4–11% of children and is associated with adverse neurocognitive, behavioural and cardiovascular outcomes, including reduced autonomic control. The relationship between heart rate variability (HRV; a measure of autonomic control) and age found in non-snoring control children was absent during sleep in children with SDB. Age significantly predicted increasing cerebral oxygenation during wake in non-snoring control children, whereas during sleep, HRV significantly predicted decreasing cerebral oxygenation. Cerebral oxygenation was not associated with either age or HRV in children with SDB during both wake and sleep. SDB significantly disrupts the normal maturation of autonomic control and the positive association between autonomic control and cerebral oxygenation found in non-snoring children, and we speculate that the dampened autonomic control exhibited by children with SDB may have an attenuating effect on cerebral autoregulation via the moderating influence of HRV on cerebral blood flow. Abstract: The repetitive episodes of hypoxia that are features of sleep disordered breathing (SDB) in children are associated with alterations in autonomic control of heart rate in an age-dependent manner. We aimed to relate heart rate variability (HRV) parameters to age and measures of cerebral oxygenation in children (3–12 years old) with SDB and non-snoring controls. Children (SDB, n = 117; controls, n = 42; 3–12 years) underwent overnight polysomnography. Total (TP), low- (LF) and high-frequency (HF) power, tissue oxygenation index (TOI) and fractional tissue oxygen extraction (FTOE) were analysed during wake and sleep. Pearson's correlations determined the association between age and HRV parameters, and multiple linear regressions between HRV, age and cerebral oxygenation parameters. During wake, age had a positive association with LF power, reflecting increased parasympathetic and sympathetic activity with increasing age for both control and SDB groups. This association was also evident during sleep in controls, but was absent in children with SDB. In controls, during wake TOI had a positive, and FTOE a negative association with age. During sleep, TP, LF and HF power were significant, negative determinants of TOI and positive determinants of FTOE. These associations were not seen in children with SDB during wake or sleep. SDB disrupts the normal maturation of the autonomic control of heart rate and the association between HRV and cerebral oxygenation exhibited by non-snoring control children of primary school age. These results highlight the impact SDB has on cardiovascular control and the potential impact on adverse cardiovascular outcomes.

Original languageEnglish
Pages (from-to)819-830
Number of pages12
JournalJournal of Physiology
Volume597
Issue number3
DOIs
Publication statusPublished - 1 Feb 2019

Keywords

  • autonomic control
  • cerebral oxygenation
  • paediatric
  • sleep disordered breathing

Cite this

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title = "Sleep disordered breathing in children disrupts the maturation of autonomic control of heart rate and its association with cerebral oxygenation",
abstract = "Key points: Sleep disordered breathing (SDB) affects 4–11{\%} of children and is associated with adverse neurocognitive, behavioural and cardiovascular outcomes, including reduced autonomic control. The relationship between heart rate variability (HRV; a measure of autonomic control) and age found in non-snoring control children was absent during sleep in children with SDB. Age significantly predicted increasing cerebral oxygenation during wake in non-snoring control children, whereas during sleep, HRV significantly predicted decreasing cerebral oxygenation. Cerebral oxygenation was not associated with either age or HRV in children with SDB during both wake and sleep. SDB significantly disrupts the normal maturation of autonomic control and the positive association between autonomic control and cerebral oxygenation found in non-snoring children, and we speculate that the dampened autonomic control exhibited by children with SDB may have an attenuating effect on cerebral autoregulation via the moderating influence of HRV on cerebral blood flow. Abstract: The repetitive episodes of hypoxia that are features of sleep disordered breathing (SDB) in children are associated with alterations in autonomic control of heart rate in an age-dependent manner. We aimed to relate heart rate variability (HRV) parameters to age and measures of cerebral oxygenation in children (3–12 years old) with SDB and non-snoring controls. Children (SDB, n = 117; controls, n = 42; 3–12 years) underwent overnight polysomnography. Total (TP), low- (LF) and high-frequency (HF) power, tissue oxygenation index (TOI) and fractional tissue oxygen extraction (FTOE) were analysed during wake and sleep. Pearson's correlations determined the association between age and HRV parameters, and multiple linear regressions between HRV, age and cerebral oxygenation parameters. During wake, age had a positive association with LF power, reflecting increased parasympathetic and sympathetic activity with increasing age for both control and SDB groups. This association was also evident during sleep in controls, but was absent in children with SDB. In controls, during wake TOI had a positive, and FTOE a negative association with age. During sleep, TP, LF and HF power were significant, negative determinants of TOI and positive determinants of FTOE. These associations were not seen in children with SDB during wake or sleep. SDB disrupts the normal maturation of the autonomic control of heart rate and the association between HRV and cerebral oxygenation exhibited by non-snoring control children of primary school age. These results highlight the impact SDB has on cardiovascular control and the potential impact on adverse cardiovascular outcomes.",
keywords = "autonomic control, cerebral oxygenation, paediatric, sleep disordered breathing",
author = "Walter, {Lisa M.} and Knarik Tamanyan and Weichard, {Aidan J.} and Davey, {Margot J.} and Nixon, {Gillian M.} and Horne, {Rosemary S.C.}",
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Sleep disordered breathing in children disrupts the maturation of autonomic control of heart rate and its association with cerebral oxygenation. / Walter, Lisa M.; Tamanyan, Knarik; Weichard, Aidan J.; Davey, Margot J.; Nixon, Gillian M.; Horne, Rosemary S.C.

In: Journal of Physiology, Vol. 597, No. 3, 01.02.2019, p. 819-830.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Sleep disordered breathing in children disrupts the maturation of autonomic control of heart rate and its association with cerebral oxygenation

AU - Walter, Lisa M.

AU - Tamanyan, Knarik

AU - Weichard, Aidan J.

AU - Davey, Margot J.

AU - Nixon, Gillian M.

AU - Horne, Rosemary S.C.

PY - 2019/2/1

Y1 - 2019/2/1

N2 - Key points: Sleep disordered breathing (SDB) affects 4–11% of children and is associated with adverse neurocognitive, behavioural and cardiovascular outcomes, including reduced autonomic control. The relationship between heart rate variability (HRV; a measure of autonomic control) and age found in non-snoring control children was absent during sleep in children with SDB. Age significantly predicted increasing cerebral oxygenation during wake in non-snoring control children, whereas during sleep, HRV significantly predicted decreasing cerebral oxygenation. Cerebral oxygenation was not associated with either age or HRV in children with SDB during both wake and sleep. SDB significantly disrupts the normal maturation of autonomic control and the positive association between autonomic control and cerebral oxygenation found in non-snoring children, and we speculate that the dampened autonomic control exhibited by children with SDB may have an attenuating effect on cerebral autoregulation via the moderating influence of HRV on cerebral blood flow. Abstract: The repetitive episodes of hypoxia that are features of sleep disordered breathing (SDB) in children are associated with alterations in autonomic control of heart rate in an age-dependent manner. We aimed to relate heart rate variability (HRV) parameters to age and measures of cerebral oxygenation in children (3–12 years old) with SDB and non-snoring controls. Children (SDB, n = 117; controls, n = 42; 3–12 years) underwent overnight polysomnography. Total (TP), low- (LF) and high-frequency (HF) power, tissue oxygenation index (TOI) and fractional tissue oxygen extraction (FTOE) were analysed during wake and sleep. Pearson's correlations determined the association between age and HRV parameters, and multiple linear regressions between HRV, age and cerebral oxygenation parameters. During wake, age had a positive association with LF power, reflecting increased parasympathetic and sympathetic activity with increasing age for both control and SDB groups. This association was also evident during sleep in controls, but was absent in children with SDB. In controls, during wake TOI had a positive, and FTOE a negative association with age. During sleep, TP, LF and HF power were significant, negative determinants of TOI and positive determinants of FTOE. These associations were not seen in children with SDB during wake or sleep. SDB disrupts the normal maturation of the autonomic control of heart rate and the association between HRV and cerebral oxygenation exhibited by non-snoring control children of primary school age. These results highlight the impact SDB has on cardiovascular control and the potential impact on adverse cardiovascular outcomes.

AB - Key points: Sleep disordered breathing (SDB) affects 4–11% of children and is associated with adverse neurocognitive, behavioural and cardiovascular outcomes, including reduced autonomic control. The relationship between heart rate variability (HRV; a measure of autonomic control) and age found in non-snoring control children was absent during sleep in children with SDB. Age significantly predicted increasing cerebral oxygenation during wake in non-snoring control children, whereas during sleep, HRV significantly predicted decreasing cerebral oxygenation. Cerebral oxygenation was not associated with either age or HRV in children with SDB during both wake and sleep. SDB significantly disrupts the normal maturation of autonomic control and the positive association between autonomic control and cerebral oxygenation found in non-snoring children, and we speculate that the dampened autonomic control exhibited by children with SDB may have an attenuating effect on cerebral autoregulation via the moderating influence of HRV on cerebral blood flow. Abstract: The repetitive episodes of hypoxia that are features of sleep disordered breathing (SDB) in children are associated with alterations in autonomic control of heart rate in an age-dependent manner. We aimed to relate heart rate variability (HRV) parameters to age and measures of cerebral oxygenation in children (3–12 years old) with SDB and non-snoring controls. Children (SDB, n = 117; controls, n = 42; 3–12 years) underwent overnight polysomnography. Total (TP), low- (LF) and high-frequency (HF) power, tissue oxygenation index (TOI) and fractional tissue oxygen extraction (FTOE) were analysed during wake and sleep. Pearson's correlations determined the association between age and HRV parameters, and multiple linear regressions between HRV, age and cerebral oxygenation parameters. During wake, age had a positive association with LF power, reflecting increased parasympathetic and sympathetic activity with increasing age for both control and SDB groups. This association was also evident during sleep in controls, but was absent in children with SDB. In controls, during wake TOI had a positive, and FTOE a negative association with age. During sleep, TP, LF and HF power were significant, negative determinants of TOI and positive determinants of FTOE. These associations were not seen in children with SDB during wake or sleep. SDB disrupts the normal maturation of the autonomic control of heart rate and the association between HRV and cerebral oxygenation exhibited by non-snoring control children of primary school age. These results highlight the impact SDB has on cardiovascular control and the potential impact on adverse cardiovascular outcomes.

KW - autonomic control

KW - cerebral oxygenation

KW - paediatric

KW - sleep disordered breathing

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U2 - 10.1113/JP276933

DO - 10.1113/JP276933

M3 - Article

VL - 597

SP - 819

EP - 830

JO - The Journal of Physiology

JF - The Journal of Physiology

SN - 0022-3751

IS - 3

ER -