Infant Arousals During Mother-Infant Bed Sharing: Implications for Infant Sleep and Sudden Infant Death Syndrome Research

DISCUSSION

These results demonstrate that there is a striking paucity of both EWs and TAs from stage 3–4 sleep, compared with either stage 1–2 or REM, in healthy infants within the peak age range for SIDS. Together with previous evidence that arousal threshold is relatively high in the EEG delta range,^23-25 this supports the premise that infant arousability is comparatively diminished in stage 3–4. This also further legitimizes our primary interest in any changes in stage 3–4 associated with bed sharing, as might pertain to the hypothesized role of arousal deficiency in susceptibility to SIDS.

In our mother-infant pairs, bed sharing promoted both more infant EWs and TAs selectively in stage 3–4. However, bed sharing's effects on EWs and TAs in this stage were somewhat different. EWs were more frequent on the BN, irrespective of whether infants routinely bedshared at home or not. TAs, in contrast, were more frequent in RB infants than RS infants, and this was observed in both the bed sharing and solitary sleeping conditions. This suggests that the bed sharing environment had a facilitory effect on infant EWs in stage 3–4 related to the mother's immediate presence. By contrast, bed sharing's facilitation of TAs depended on bed sharing being habitual but did not require the mother's presence for expression. Certainly a novelty effect (exposure to a new environment) does not explain either of these selective state 3–4 effects—the impact of the bed sharing night on EW frequency was seen in both infant groups (RB and RS), and the impact of routine bed sharing on TA frequency was seen in both laboratory conditions (BN and SN). This suggests involvement of other factors inherent to bed sharing, such as increased sensory stimulation involving potentially every sensory modality.

Although EWs were more frequent in stage 3–4 on the BN, the net effect across the entire night was that EW frequency was overall slightly lower on the BN compared with the SN by an average of 0.9/hour. This was because EWs were less frequent in stage REM on the BN. These opposite effects of bed sharing on EW frequency for stages 3–4 and REM, together with the absence of any significant night or group effects on either EW or TA frequency in stage 1–2 or on TA frequency in stage REM, emphasize further the selectively of bed sharing's facilitation of arousals in stage 3–4 sleep.

Meaningful comparisons of our findings with previous studies of infant arousal patterns are limited by important differences in aims, technology, and criteria used to identify arousals/awakenings. As early as 1957, Moore and Ecko⁴² quantified “night waking” in infants, defined by the infant signaling the mother. It was not until two decades later, using in-home video recording, that it was demonstrated that infants typically exhibit additional behavioral awakenings during the night without waking their parents.⁴³Since then, numerous polysomnographic studies that included EEG sleep-wake staging have been performed in normal infants within the first postnatal year, as well as in SIDS victims and in infants at high-risk for SIDS. Some of these studies indexed arousals by body movements and reported more frequent movements in REM sleep than non–rapid eye movement (NREM) sleep.^5,8,44 Furthermore, Hoppenbrouwers et al¹⁰ measured state transition probabilities based on sleep-wake staging and reported that infants are more likely to transition to the waking stage from active sleep (analogue of stage REM) than from quiet sleep (analogue of stage 3–4). The findings of these polysomnographic studies are in general agreement with the sleep stage differences in frequencies of EWs and TAs reported here. However, EEG arousals based on the standardized criteria more recently developed by the American Sleep Disorders Association⁴¹ that we used have not been applied previously in any infant studies. In addition, we are aware of no studies designed to contrast arousals/awakenings in bed sharing and solitary sleeping infants using any technology or criteria for arousals/awakenings. In fact, the only preexisting data available that shed any light on the impact of bed sharing on infant awakenings were based on simple parental interviews. Singh et al⁴⁵ found that awakenings requiring the parent to resettle the infant were reported more commonly among their sample of east Indian infants, all of whom bedshared with a parent or grand parent, compared with the solitary sleeping infants represented in previous studies of night-waking.

The American Sleep Disorders Association criteria for identifying transient arousals⁴¹ have been applied recently to healthy older children and adults by Acebo et al.⁴⁶ In their study, however, arousals were not broken down by sleep stage. The TAs (≤15 seconds) they reported were comparable to the TAs we measured. Collapsing across sleep stages in our subjects allowed recalculation of TAs as overall frequency per hour of total sleep. When the two study groups and two laboratory conditions also were collapsed, we found that the infants in our study averaged 14.7 TAs per hour of sleep. Contrasted with the means ranging from 3.2/hour to 5.3/hour reported in older children and adults by Acebo et al,⁴⁶ this indicates that short-lived EEG arousals are generally far more common in infancy.

There are two important implications of the augmentation of arousals with bed sharing demonstrated in our subjects. The first concerns the relationship of normative values for infant sleep patterns to the sleep environment in which norms are established. Without exception, polysomnographic norms for infant sleep have been obtained in the solitary sleeping environment. This experimental design bias no doubt reflects the western cultural practice of solitary infant sleeping. Notwithstanding, most of the world's cultures still practice some form of parent-infant room sharing, including sharing the same bed or sleeping surface.⁴⁷ Even within the United States, bed sharing is not an uncommon practice, contrary to popular perception. For example, for infants and toddlers, frequent all-night or part-night bed sharing was reported in 19% of whites, 59% of blacks, and 26% of Hispanics in families sampled from New York City and Cleveland.^48,49 In a previous report of sleep architecture in the same 35 infants described herein, we revealed that the amount of stage 3–4 sleep and the duration of stage 3–4 episodes were significantly reduced on the bed sharing night compared with the solitary night, regardless of the infants' routine sleeping arrangement.³⁰ Together with the immediate effects of bed sharing on EW frequency and the long-term effects on TA frequency discussed presently, these findings demonstrate that normative values for infant sleep established in solitary sleeping infants are not necessarily representative of infants in social sleeping environments. Separate norms should be established.

The second implication concerns the etiology of and risk factors for SIDS. The peak age for SIDS corresponds to a developmental stage when infant sleep in the solitary environment is undergoing consolidation, the amount of quiet sleep is increasing, and sustained bouts of quiet sleep are lengthening.^7,8,10,17-22 Many SIDS researchers believe that arousal deficiency plays an important role in the etiology of SIDS (see beginning of article). If this is true, then manipulations or conditions that facilitate arousability might be protective against SIDS. This might be especially true for quiet sleep, given the ongoing consolidation process, the comparatively low rate of spontaneous arousals, and the relatively high arousal threshold in this stage. The curtailment of stage 3–4 sleep and the facilitation of TAs and EWs in this stage resulting from bed sharing might minimize the occurrence of long periods of consolidated sleep from which infants with deficient arousal mechanisms might have difficulty arousing in response to any potentially life-threatening condition. Furthermore, we have speculated that, during the critical period when infants are vulnerable to SIDS, bed sharing might insure a basal level of “practice” required for the integration or coordination of the neural mechanisms that underlie the arousal response.^28,31 The present finding that TA frequency was higher even on the solitary night in routinely bed sharing infants than in infants who routinely slept alone supports the notion that practice has a sustained impact on arousability.

We speculate further that there are other means through which bed sharing might be protective against SIDS. The one with perhaps the most face value concerns the proximity of the mother to the infant, which should enable her to more effectively monitor changes in the infant's status. We recently reported, in these same mother-infant pairs, that mothers aroused 30% more often when they bed shared than when they slept alone.²⁹ Furthermore, the present results demonstrated an approximate doubling on the bed sharing night in the temporal overlap of infant with maternal arousals. Given that the largest increase in overlapping arousals by far reflected instances where the infant aroused first, these findings imply a high level of responsivity on the mother's part to the infant that did not habituate with routine bed sharing. A high degree of maternal attentiveness is also strongly suggested by the close proximity and face-to-face orientation generally maintained by these mothers during bed sharing.⁵⁰ Another way that bed sharing might be protective against SIDS could be through facilitation of breastfeeding. Bed sharing significantly increased the frequency and total duration of nighttime breastfeeding in our subjects, whether or not they were routine bed sharers.⁵¹ Several epidemiologic studies have found that breastfeeding reduces the risk for SIDS.^52-55By facilitating breastfeeding, bed sharing might confer some degree of risk reduction. Also, prone sleeping is now widely accepted as a risk factor for SIDS.⁵⁶ That prone positioning was minimized in our subjects when they bedshared⁵⁰ suggests another avenue through which bed sharing might be protective.

The authors are careful to point out that any potential benefits of bed sharing as pertains to susceptibility to SIDS are theoretical at this time. In fact, in a recent epidemiologic study from New Zealand, bed sharing (defined as bed sharing with anyone) was found to increase significantly the risk for SIDS when practiced in association with maternal smoking.⁵⁷ A subsequent epidemiologic study in southern California⁵⁸ failed to find increased risk for SIDS associated with similarly defined bed sharing when passive smoking was controlled for in the analysis; and a recent epidemiologic study in the United Kingdom⁵⁹ found that bed sharing with a parent(s) was associated with increased risk only in conjunction with parental smoking. It is also noteworthy that the New Zealand study found that room sharing (as opposed to bed sharing) with one or more adults conferred significant protection against SIDS, whereas room sharing with children did not.⁶⁰ This suggests that, at least under some circumstances, proximity to the parent(s) during sleep may be protective, as we are proposing. Further epidemiologic studies that additionally control for potentially important factors that could affect how bed sharing impacts infants ultimately will be needed to define in what contexts bed sharing (or room sharing) might be benefical or detrimental to infants with regard to SIDS risk. Such factors include the relationship of the bed partner to the infant, cultural differences in attitudes toward bed sharing with infants,^38,61 individual differences in reasons for bed sharing, differences in parental attitudes about responding to and physical contact with the infant during the day as well as at night,⁶² and the type of surface used for bed sharing.

As this is the first study to measure the impact of bed sharing on infant sleep and arousals, appreciation of its limitations is especially important. Some have been discussed in detail previously^29,30 and include the small bed size used for bed sharing and limitations on the extent to which the results would generalize to other subject populations. It is unlikely that a passive effect of bed size alone explains the facilitation of infant arousals with bed sharing, given (a) the close face-to-face proximity maintained by mothers,⁵⁰ (b) the observations that mothers typically managed the infant's position relative to her during periods of breastfeeding, often actively enclosing the infant within their arms (unpublished observations), and (c) that mother-infant bed sharing in a single bed (or couch of similar size) is probably not an uncommon occurrence in the population we sampled. Further studies in other populations will be required to determine the extent to which our findings generalize to nonbreastfeeding mothers, to other cultural groups and to bed sharing with the father or other family members.

Another limitation stems from the absence of information on the architecture of daytime sleep in the infants we studied. Conceivably, more bed sharing-induced arousals might undermine infant arousability in the daytime by causing a “rebound” reduction of arousals during daytime solitary sleep. Such a rebound seems unlikely, however, at least for TAs insofar as that TAs were facilitated in RB infants when the mother was absent on the SN.

In conclusion, stage 3–4 sleep in infants was associated with a striking paucity of EWs and TAs, compared with the other sleep stages. Bed sharing increased the frequency of EWs from stage 3–4 sleep, whether or not infants habitually bedshared at home. Infants who routinely bedshared also exhibited more frequent TAs in stage 3–4, whether or not the mother was present on a given night. There was also an approximate doubling during bed sharing in the number of infant arousals that temporally overlapped arousal in the mother. The largest increase in overlapping arousals reflected those where the infant aroused first, suggesting that mothers maintained a high degree of sensitivity to their infants during bed sharing, even when practiced habitually. These differences between bed sharing and solitary sleeping infants indicate that normative values for infant sleep must be interpreted within the context of the sleeping environment in which they were established. We speculate that the selective facilitation of infant arousals in stage 3–4 sleep might be protective to infants at risk for SIDS because of an arousal deficit. Enhanced maternal sensitivity during bed sharing to changes in the infant's status might also be protective.