Effects of sleep position, sleep state and age on heart rate responses following provoked arousal in term infants
Introduction
The control of the cardiorespiratory system undergoes functional maturation after birth, and until this process is completed, the control of breathing and the cardiovascular system is unstable, placing infants at risk for cardiorespiratory disturbances, especially during sleep [1]. Evidence of autonomic dysfunction or autonomic maturational delay is a feature of some infants who succumb to Sudden Infant Death Syndrome (SIDS). Infants dying of SIDS exhibited a higher heart rate, lower overall heart rate variability and disturbed long-term coordination of cardiac and respiratory measures when compared with age matched control infants [2], [3], [4]. Despite the dramatic decline in the incidence of SIDS over recent years, it is still the major cause of death in infants between 1 month and 1 year of age [5]. Recent data recorded from infants dying whilst being monitored has demonstrated that infants appear to loose the ability to integrate cardiac and respiratory function. Initially, bradycardia occurs in the presence of continued respiration followed by gasping, but heart rate does not recover [6], [7].
The prone sleeping position and maternal smoking have been demonstrated in a number of studies in different countries to be two of the major risk factors for SIDS [8], [9], [10], [11], [12], [13], [14], [15]. It has been hypothesised that the ability to arouse from sleep is an important survival mechanism, which may be impaired in SIDS infants [16]. In support of this idea, studies have now demonstrated that arousal responses are impaired in the prone position [17], [18], [19] and also in infants whose mothers smoked during pregnancy [20], [21], [22]. In addition, it has been suggested that sleep position [17], [18] and maternal smoking [20], [23] alter autonomic control in infants.
In this study, we examined the effects of sleeping position and maternal smoking on the postnatal maturation of autonomic function by examining heart rate responses following arousal in healthy term infants. Our hypothesis was that the prone sleeping position and maternal smoking would impair changes in heart rate at arousal, and these would be most marked at 2–3 months of age, when SIDS incidence is highest.
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Methods
The Monash Medical Centre Human Ethics Committee granted ethical approval for this project. All subjects were volunteers recruited from the maternity wards and Jessie McPherson Private Hospital, Monash Medical Centre, Melbourne. Written informed consent was obtained from parents prior to commencement of the study, and no monetary incentive was provided for participation.
Subjects
We recruited 24 infants born at term with normal birth weights and Apgar scores and without any congenital abnormalities (Table 1). All 24 infants were studied at 2–3 weeks postnatal age, 22 infants were studied at 2–3 months of age and 18 infants were studied at 5–6 months of age. Mothers were asked to complete a questionnaire regarding their smoking habits at the first study detailing the number of cigarettes smoked during and after pregnancy and whether or not other members of the household
Recording methods
Infants were studied using daytime polysomnography. Electrodes for recording physiological variables were attached to each infant during feeding and, when drowsy, the infant was placed in a bassinet under dim lighting and constant room temperature (22–23 °C). Infants generally had both a morning and afternoon sleep interrupted by a midday feed, when sleep position was changed. Each infant slept both prone and supine during each study, the initial sleep position was randomised both between
Stimulus and arousal criteria
A pulsatile air-jet (frequency 3 Hz for 5 s) delivered to the nostrils of the infant was used to induce arousal both in active sleep (AS) and quiet sleep (QS) [27], [28]. The stimulus was presented alternately to the left and right nostrils; if the infant failed to arouse, the air-jet pressure was increased when the stimulus was again presented to that nostril. Whenever an arousal response occurred, the pressure was decreased. In determining whether a presentation elicited an arousal response,
Data analysis
Baseline heart rate (BHR) data were collected over 20 beats prior to each stimulus presentation that induced arousal. Heart rate typically increased following the arousing stimulus, and data for 30 beats after the stimulus were analysed to measure the maximum heart rate (Max HR) (Fig. 1). Maximum heart rate was the average of three beats prior to and three beats after peak heart rate. The increase in heart rate (ΔHR%) was calculated as the difference between maximum heart rate and baseline
Results
There was no significant difference between the smoking and non-smoking groups for any of the demographic measures recorded (Table 1).
Maternal smoking
Mothers of the non-smoking group (n=13) reported that they did not smoke and that no one else in the household smoked. This was confirmed by infant urinary cotinine levels measured at the 2–3 months study, which were all <10 ng/ml. Eight of these infants were breast-fed. In the maternal smoking group (n=11), mothers reported routinely smoking 3–20 cigarettes/day (mean 15±6/day). Seven of the infants were breast-fed. Two mothers reported stopping smoking when pregnancy was confirmed at 6–8 weeks
Effects of sleeping position
BHR was elevated in the prone compared to the supine position in QS at 2–3 weeks and 5–6 months (p<0.001) and in AS at 2–3 and 5–6 months (p<0.05) (Fig. 2A).
Effects of sleep state
BHR was significantly elevated in AS compared to QS when infants slept in the supine position at 2–3 weeks, 2–3 and 5–6 months of age (p<0.01). In the prone sleeping position, BHR was elevated in AS compared to QS at 2–3 (p<0.001) and 5–6 months (p<0.05) (Table 2).
Effects of postnatal age
In the supine position, BHR was significantly greater at 2–3 weeks compared
Effects of sleeping position
Max HR was higher in the prone compared to the supine position in QS at 2–3 (p<0.01) and 5–6 months (p<0.05) (Fig. 2B).
Effects of sleep state
Max HR was higher in AS compared to QS at all three ages when infants slept supine (2–3 weeks p<0.001, 2–3 months p<0.001, 5–6 months p<0.01) and at 2–3 weeks p<0.001 and 2–3 months p<0.05) when infants slept prone (Table 2).
Effects of postnatal age
In AS, Max HR was significantly greater at 2–3 weeks compared to 5–6 months in both supine (p<0.05) and prone positions (p<0.01). Max HR was also
Effects of sleeping position
ΔHR% was significantly greater in the supine compared to the prone position in QS at 2–3 weeks (p<0.05) and in AS at both 2–3 (p<0.01) and 5–6 months (p<0.05) (Fig. 2C).
Effects of sleep state
ΔHR% was significantly greater in AS compared to QS in both supine (p<0.05) and prone (p<0.001) positions at 2–3 weeks. At 2–3 months, the difference between sleep states was only seen when infants slept supine (p<0.001). There was no significant difference in either position at 5–6 months (Table 2).
Effects of postnatal age
ΔHR% was significantly
Effects of sleeping position
Max HB was significantly elevated in the prone position in QS at 2–3 months (p<0.05) and at 5–6 months (p<0.05) compared to the supine position (Fig. 2D).
Effects of sleep state
Max HB was significantly elevated in AS compared to QS at 2–3 weeks when infants slept in both supine (p<0.001) and prone positions (p<0.001), and at 2–3 months in the supine position (p<0.01) (Table 2).
Effects of postnatal age
Max HB was elevated at 2–3 weeks compared to 5–6 months when infants slept supine (p<0.05) in AS (Table 3).
Discussion
This study has demonstrated that cardiac responses of sleeping infants when aroused are altered by sleep state, sleep position and postnatal age. However, we found that maternal smoking did not affect cardiac responses in either sleeping position, in contrast to previous studies suggesting that maternal smoking alters autonomic function in infants, as assessed by power spectral analysis of R–R interval [20], [23]. Alterations in autonomically mediated cardiovascular function may indicate subtle
Acknowledgements
The authors wish to thank the staff of the maternity wards at the Monash Medical Centre and Jessie McPherson Private Hospital and the parents and infants who participated in this study.
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