Results

HEART RATE VARIABILITY

A summary of the statistical measures for heart rate variation is given in table 1. There were no significant differences between the mean heart rates for sleep position or sleep state. HRV, as measured by the standard deviation of R-R interval length (SD R-R), was significantly less when the babies were sleeping prone than when supine in both quiet and active sleep. The standard deviation of the amount of change from one interval to the next (SD▵R-R) was also significantly less in the prone position. These differences were not reflected in the aspect ratio (ratio of variance (or SD) of SDR-R to SD▵R-R). Poincaré plots illustrate visually this reduced variation in the decreased scatter of the points in the prone as compared to the supine position (fig 3). The plots shown are from the same individual and are each made up of about 500 consecutive R-R intervals.

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Figure 3

Example of the differences in Poincaré plots recorded from the same individual during prone and supine positioning in quiet and REM sleep.

All Poincaré variables had a significantly (p<0.001) higher variance in active sleep than in quiet sleep.

RESPIRATORY RATE

Sleep position was not associated with changes in respiratory rate. Respiratory rates recorded in quiet sleep were: prone 34.1(10.4) and supine 36.2 (8.8) breaths/minute. In active sleep respiratory rates were: prone 39.9 (9.2) and supine 42.3 (9.1) breaths/minute. Significantly higher respiratory rates were recorded in active sleep than in quiet sleep in both sleep positions (p<0.05).

R-R INTERVAL CHANGES IN RESPONSE TO TILT

A typical response of the R-R interval changes following a tilt is shown in fig 2. All infants responded to the tilt with an increase in heart rate (decrease in R-R) followed by a decrease in heart rate (increase in R-R) with a maximum :minimum R-R interval ratio greater than 1. The tilt often provoked the sigh reflex. No significant differences were found between the prone and supine position on the maximum :minimum R-R interval ratio (table 2). There was a trend for the rebound bradycardia (maximum R-R) to be less in the prone sleep position but this was not significant.

AROUSAL RESPONSE TO THE TILT

Figure 4 summarises the tilt test results according to arousal code, sleep position, and sleep state. Arousability was significantly less (p < 0.01) in the prone sleep position but not in quiet sleep. Arousal was much more common in active sleep in both sleep positions (p< 0.01). In quiet sleep about 72% of all tilt tests resulted in no arousal (grade 0) whereas in active sleep no arousal was noted in 30% of all tests when prone and 20 % when supine. Prone positioning significantly reduced the number of full awakenings (grade 2) recorded in response to the test (14.8% of prone tests compared with 54 % supine) in active sleep.

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Figure 4

Frequency histograms of the arousal codes scored following a 60° head-up tilt. (A) Quiet sleep in prone and supine positions; (B) REM sleep in prone and supine sleep positions. Arousal code 0: no movement at all; 0.5: startle response in tilt but remaining asleep; 1: awake with gross head movement and/or eyes open but asleep within 15 to 30 seconds and remaining so on return to horizontal; 2: full awakening with eyes open and usually crying.

Discussion

The main findings of this study of healthy 2–4 month old infants sleeping prone compared with supine were that HRV was reduced in active and quiet sleep and arousal responses were depressed in active sleep. Physiological correlates to explain a reduction in HRV (derived from time domain and frequency domain measures) are complex.16During rest R-R interval lengths are constantly modified by haemodynamic, neural, and hormonal influences. It is generally accepted that a reduction in HRV can be associated with cardiac autonomic dysfunction17 18 such as autonomic withdrawal resulting in a sympathovagal imbalance and/or high levels of sympathetic activity.19 A reduction in HRV can also result from decreased responsiveness of sinus nodal cells to neural modulation,20 and to increased respiratory rhythmicity.21

A reduction in HRV derived from Poincaré data has been reported by Schechtman et al 11 in infants who died of SIDS, the main findings being a reduction in beat to beat point dispersions at the longer intervals (lower heart rates) in comparison to data from age matched controls. They concluded that either sympathetic hyperactivity, parasympathetic hypoactivity, or a combination of the two underlie these findings. As sleep position was not reported, our study suggests that some of the differences may well be related to this. A recent report examining the instantaneous variation in respiratory pattern also found a difference between SIDS babies and age matched controls, with less variation occurring in SIDS babies at slow respiratory rates.22 The confounding effect of sleep position may be important here as well.

Our finding that HRV is reduced in the prone sleep position in healthy infants confirms the findings of another group who reported a decrease in HRV in active sleep when measurements were made by spectral analyses in particular frequency bands.23 We noted a reduction in variability with the prone sleep position in both active and quiet sleep states, particularly in quiet sleep, although it also occurred in active sleep. In other words quiet sleep in the prone position produces the most inflexible heart rate. Quiet sleep is also associated with the least chance of arousal.

A postural change between supine and prone means a positional change in the level of the carotid sinus in relation to the heart, being below the level of the heart when supine, and above when prone. Whether this has any influence on baroreceptor gain is unknown. We suggest that a reduction in “breathing effort” observed in healthy full term infants on a shift from supine to prone24 might cause a reduction in respiratory sinus arrhythmia. This could have an impact on the autonomic nervous system by dampening beat-beat variation in the prone position.

That we found no effect of sleep position on the cardiac response of infants to the tilt is perhaps not surprising, given the combination of events following the gravitational stress—that is, fall in blood pressure, transient arousals, sighs and apnoeas. Transduction of these haemodynamic and neural effects to cardiac rate must overlap so that sleep position then becomes a negligible factor. A study in anaesthetised rats of comparative changes in blood pressure (taken from direct arterial recordings) in response to a 45° head-up tilt when prone and supine, reports a smaller fall in blood pressure when prone and a smaller rebound bradycardia after the tilt,25 the latter finding being consistent with the trend we found. In contrast, another study comparing blood pressure changes to a 60° head-up tilt in sleeping infants reports a significantly greater fall in blood pressure (measured from automated blood pressure cuffs) when positioned prone rather than supine.13 The authors concluded that sleeping prone adversely affects autonomic function in healthy infants. Our attempts to compare blood pressure changes in infants before and after the tilt, using the same automated technique, were unsuccessful because the technique was not accurate enough, the measures could not be taken frequently enough, and inflation and deflation of the cuff often provoked arousal (unpublished findings).

R-R interval measurements in response to the a head-up tilt (such as those used here) are most often used as a clinical tool for assessing autonomic function in adults with cardiovascular disorders.26 The test is always performed during the awake state so that the level of consciousness remains unchanged, ruling out any confounding effects of the changing sleep–wake patterns we encountered. The head-up tilt has been used to identify disturbances in autonomic function of sleeping infants that have sustained an ALTE.27 In control infants (and in the infants studied here), the response to the tilt is almost always an increase followed by a decrease in heart rate.12 27 A significant proportion of ALTE infants responded to the tilt test by a constant increase or decrease in heart rate, a decrease followed by an increase, or no change at all.27

The tilt test proved most useful for us as a tool to assess the differences in arousal responses of infants sleeping prone compared with those sleeping supine. The finding that prone sleeping depressed arousal of infants during active sleep supports data showing the sleep promoting effects of prone positioning in similar aged infants.23 28 Our method of scoring arousal based on observations graded from nil response to full awakening was important in terms of recognising that even slight head movement could be enough to protect the vulnerable infant from danger; the scenario being an infant who has to respond to the stress of sleeping face down into soft bedding where the simple response of head movement without full awakening may be enough to prevent rebreathing29 or airways obstruction,30 but obviously a full awakening would be most protective. The tilt test was not a useful predictor of arousal in quiet sleep as two thirds of all tests resulted in no arousal in both sleep positions and only one test provoked a full awakening response.

In conclusion, we have shown that prone sleeping reduces the variability of heart rate in normal healthy 3 month old infants during both active and quiet sleep. Furthermore, prone sleeping reduces the ability of the infant to wake from test stimuli during active sleep. The findings could help explain why prone sleeping seems to be such a dangerous sleeping position even for apparently healthy babies who have no risk factors for SIDS.