Influence of Swaddling on Sleep and Arousal Characteristics of Healthy Infants
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《小儿科》
Pediatric Sleep Unit, University Children's Hospital, Free University of Brussels, Brussels, Belgium
Institut National de la Santé et de la Recherche Médicale 628, Lyon, France
Pediatric Sleep Unit, Centre Hospitalier Chrétien Site de l'Espérance, Liège, Belgium
ABSTRACT
Objective. Swaddling is an old infant care practice. It was reported to favor sleep and to reduce crying among irritable infants. There are few data on the physiologic effects of swaddling on infants' sleep-wake characteristics. This study was conducted to evaluate whether swaddling influences infants' arousal thresholds for environmental auditory stress.
Design. Sixteen healthy infants, with a median age of 10 weeks (range: 6–16 weeks), underwent polygraphic recording in their usual supine position during one night. The infants were successively recorded swaddled and nonswaddled, or vice versa. In both conditions, the infants were exposed to white noise of increasing intensity, from 50 to 100 dB(A), during rapid eye movement sleep, to determine their arousal thresholds.
Results. Swaddling was associated with increases in the infants' sleep efficiency and in the time spent in non–rapid eye movement sleep. When swaddled, the infants awakened spontaneously less often. However, significantly less-intense auditory stimuli were needed during rapid eye movement sleep to induce cortical arousals when swaddled than when not swaddled.
Conclusions. Swaddling promotes more-sustained sleep and reduces the frequency of spontaneous awakenings, whereas induced cortical arousals are elicited by less-intense stimuli. These findings could indicate that, although swaddling favors sleep continuity, it is associated with increased responsiveness to environmental auditory stress.
Key Words: arousal infant sleep swaddling sudden infant death syndrome
Abbreviations: HR, heart rate NREM, non–rapid eye movement REM, rapid eye movement SIDS, sudden infant death syndrome EEG, electroencephalographic
In many parts of the world, infants are swaddled to sleep, with their bodies tightly wrapped in tissue cloths, sheets, or light blankets. 1–4 Infant bundling or swaddling has been reported to pacify a crying infant, to reduce motor activity, and to favor sleep. 1–3, 5–9
Swaddling has also been considered to reduce the risk of sudden infant death syndrome (SIDS). The odds ratio for SIDS among swaddled infants sleeping supine has been reported to be 0.64 to 0.69. 10, 11 However, the risk shows a threefold increase if the infants sleep prone. 10 Eight to 30% of infants <9 months of age are still placed prone to sleep, despite the preventive campaigns against SIDS. 12–14 Excessive crying is one of the reasons not to place infants on their backs to sleep. If swaddling prevents excessive crying among infants, then it could become a method to promote supine sleep and to prevent SIDS. 6, 7
Sleep laboratory observations have associated SIDS with a decrease in the infant's arousal from sleep. 15 Healthy infants developed increased auditory arousal thresholds for a variety of stimuli in conditions known to favor SIDS, such as prenatal exposure to cigarette smoking, 16 sleeping prone, 17, 18 and sleeping in a heated room. 19 Arousal from sleep could be an important defense mechanism against potentially dangerous situations during sleep. 20 The purpose of this study was to evaluate the influence of swaddling on infants' sleep continuity and arousal thresholds for auditory environmental stress.
METHODS
Subjects
Sixteen healthy infants underwent polygraphic recording during one night. The infants were successively selected from a larger group of infants recruited for a research program on sleep-related behavior if they met the following inclusion criteria for study entry. The infants were born at term to nonsmoking parents who used no alcohol or drugs, with no family history of SIDS. The infants' hearing, evaluated with an audiometer (SCR Electronics, Paris, France) after birth, was normal. At the time of the study, the infants were <6 months of age, slept supine, were healthy, and took no medication. The infants were not sleep deprived within the 24 hours before the study, as reported by the parents. The aim and methods of the study were approved by the university ethics committee and were explained to the parents, who gave their informed consent.
Monitoring Procedures
Monitoring was conducted in a quiet room at an ambient temperature, ranging from 21 to 24°C (69.8–75.2°F). The infants wore their own pajamas and were covered with a blanket. The clothing and bedding corresponded to 3° tog insulation. The following variables were recorded simultaneously: 8 electroencephalographic (EEG) derivations applied according to the 10–20 system, 2 electrooculograms, a digastric electromyogram, and an electrocardiogram. Thoracic and abdominal respiratory movements were measured with inductance plethysmography, and airflow was measured with oral and nasal thermistors. Oxygen saturation was recorded continuously with a transcutaneous sensor (Nellcor, Pleasanton, CA). An actigraph was placed on one arm to measure body movements. The data were collected on computerized polygraph recorders (Morpheus System; Medatec, Brussels, Belgium).
Temperature Measurements
Core temperature was measured for 7 infants (4 boys and 3 girls) whose parents had agreed to the placement of a rectal probe 2 cm inside the infant's rectum. Body temperature was recorded before and after the swaddled and nonswaddled sleep periods.
Swaddling
When nonswaddled, the infants were sleeping supine and were free to move their legs and arms. Swaddling was obtained with sand bags and bed sheets tidily wrapped around the body, which prevented the infants from moving their arms and legs. Similar swaddling techniques have been used in other studies. 21 The study started at 9:00 PM, and the infants were allowed to fall asleep nonswaddled in their usual supine position. At 1:01 AM, the infants were gently wrapped as described before. To avoid any confounding effect resulting from nyctohemeral influences, 8 of the 16 infants were chosen at random to be initially studied nonswaddled and then swaddled. An inverse sequence was used for the other infants. At 9:00 PM, these infants were allowed to fall asleep nonswaddled and were wrapped when they were already asleep. At 1:01 AM, they were liberated from their constraints. Care was taken to avoid awakening the infants during swaddling and release measures. The infants were studied asleep in swaddled and nonswaddled conditions. This study evaluated the effect of swaddling on sleep continuity but not on the time to fall asleep.
Auditory Stimulation
In both swaddled and nonswaddled conditions, the infants were exposed to auditory challenges during rapid eye movement (REM) sleep, to determine their auditory arousal thresholds. 22 White noise of increasing intensity was presented for 3 seconds through a loudspeaker (SCR Electronics, Paris, France), at a distance of 3 cm from the infant’s ear. The level of the audiometer had been calibrated previously with a sonometer (Brul and Kjaer model 2209; B&K Medical, Copenhagen, Denmark), at an equivalent distance. Physical decibels were expressed as physiologic decibels (A). The sound level was increased by 10 dB, from 50 to 100 dB(A). The time between presentations was 1 minute. A complete auditory challenge lasted a maximum of 6 minutes. A challenge was interrupted when the infant awakened, as defined by opening of the eyes and/or crying, or when a stimulation level of 100 dB(A) was reached. The auditory signal was automatically identified on the sleep recording. In both normal and swaddled conditions, the infants were tested only during REM sleep, after a minimum of 5 minutes in this sleep stage. Staging of REM sleep requires the coincidence of specific activities in all 3 electrographic measures, ie, "desynchronized" EEG signals, bursts of REMs, and suppression of electromyographic activity. 23, 24 That stage of sleep was chosen because transient brain activations in response to auditory stimulations are seen more readily in REM sleep than in non–rapid eye movement (NREM) sleep. 19 The challenges were not repeated in other sleep stages, to reduce the risk of sleep fragmentation and secondary increases in arousal thresholds. 25 Similar methods have been used in previous studies. 16, 17, 19, 22
Data Analyses
Sleep Stages
Each 30-second period of the sleep recordings was scored as NREM, REM, wakefulness, or movement time according to standard criteria. 24 Before auditory stimulations, sleep efficiency was defined as the time spent sleeping divided by the total recording time, multiplied by 100. The frequencies of NREM, REM, wakefulness, and movement were measured and expressed as percentages, after division of the duration of each sleep state by the total duration of the period and multiplication by 100. 22 Evaluation of the recordings was performed without knowledge of the infant's condition and time of recording.
Cardiorespiratory Parameters and Oxygen Saturation
Episodes of sleep apnea were scored only if they lasted 3 seconds. Central apnea was scored when flat tracings were obtained simultaneously for thoracic movements and thermistors. Periodic breathing was defined as 3 episodes of central apnea separated by <20 seconds of breathing movements. Obstructive apnea was scored when continuous deflections were obtained for the thoracic movements and a flat tracing was recorded from the thermistors. Mixed apnea was defined as central apnea followed directly by obstructive episodes and was scored together with obstructive apnea. The frequency of apnea was calculated as an index by dividing the absolute number of events by the total sleep time of the period (in minutes) and then multiplying by 60. 22 Median values for oxygen saturation, heart rate (HR), and respiratory rate were calculated for 1-minute stable sleep epochs. Overall HR variability was defined as the SD of the R-R interval values calculated between successive QRS complexes. Decreases in HR and oxygen saturation refer to changes of >10% and >4% of basal values, respectively.
Spontaneous Arousals
Spontaneous arousals were subdivided into subcortical activation and cortical arousal. 26 A subcortical activation was scored if no change in EEG findings was seen but 2 of the following changes occurred: a gross body movement detected with movement sensors, seen as an artifact in the somatic channels (electrocardiographic, EEG, and respiratory parameters), or observed directly; changes in HR (10% of baseline values); or changes in breathing patterns (any change in frequency and/or amplitude). A cortical arousal was scored with the above criteria, with the addition of the occurrence of an abrupt change in EEG background frequency of 1 Hz, for a minimum of 3 seconds. Total arousal corresponded to the sum of cortical arousal and subcortical activation. The intervals between successive spontaneous arousals were calculated in total sleep time, REM sleep, and NREM sleep.
Baseline sleep states that preceded arousal or subcortical activation were established during 20-second time periods. At least 10 seconds of uninterrupted state were required between arousals. At least 15 seconds of continuous breathing were required after an episode of apnea and an arousal reaction for this to be defined as spontaneous. An awakening was scored when the infant opened the eyes and/or cried.
Induced Arousals and Determination of Arousal Thresholds
An induced arousal was scored if, within 10 seconds after the start of an auditory stimulation, abrupt changes occurred during a period of 3 seconds that corresponded to the definition of cortical arousals. 22, 26 The breathing and EEG signals were compared with those recorded during the 20 seconds preceding the auditory challenge, to reduce the risk of spontaneously occurring arousals. Arousal thresholds were defined by the lowest auditory stimulus, expressed in decibels (A), needed to induce an arousal.
HR Changes During Auditory Challenge
Changes in HR autonomic controls in response to an auditory challenge were calculated after the first auditory stimulus of 50 dB(A). R-R intervals, calculated between successive QRS complexes, were digitalized at 300 Hz, with an accuracy of 0.3 milliseconds. Basal median HR values were measured for 10 seconds before the stimulation. Maximal and minimal HR values were measured in the 20 seconds after the sound. The percentage HR increase was calculated as the maximal HR value during stimulation divided by the median basal HR value, multiplied by 100. The percentage HR decrease was calculated with the minimal values measured after stimulation. The percentage of total HR change corresponded to the difference between the maximal HR value and the minimal HR value after the stimulus divided by the median basal HR value, multiplied by 100.
Statistical Analyses
Statistical evaluation was performed with the use of Wilcoxon's matched-pairs, signed-ranks test and Friedman's statistics, with a level of significance of .05.
RESULTS
The 16 infants studied included 10 male and 6 female infants, with a median age of 10 weeks (range: 6–16 weeks). The median gestational age was 39 weeks (range: 38–40.5 weeks), the median birth weight was 3120 g (range: 2380–3890 g), and the median weight at the time of the study was 5490 g (range: 3800–7350 g). There were 3 small-for-gestational age infants. No mother reported the consumption of tobacco, alcohol, or illegal drugs.
The median time to resume sleep after swaddling was 30 seconds (range: 0–7 minutes). Most sleep and cardiorespiratory characteristics were similar in the swaddled and nonswaddled conditions (Tables 1 and 2). After central and obstructive apnea, no differences were seen between the 2 study conditions in the frequency of HR decelerations or in decreases in oxygen desaturation.
As shown in Table 3, the swaddled condition was associated with significantly greater sleep efficiency (P = .030), less time spent awake after sleep onset (P = .006), and more time spent in NREM sleep (P = .028), compared with the nonswaddled condition. Although all infants aroused from sleep in response to the auditory challenges, less-intense auditory stimuli were needed to arouse the infants when they were swaddled than when they were not swaddled (P = .005).
No relationship was found between auditory arousal thresholds and the order of the study, gestational age, gender, birth weight, or age or weight at the time of the study. No difference was seen in the time of night when the infants were exposed to the auditory challenge or the frequency or duration of awakenings in the 2 study conditions.
During cortical arousals, there were no significant differences in HR changes in the 2 conditions. In response to the first auditory noise of 50 dB(A), however, the maximal HR reached higher values in the swaddled condition than in the nonswaddled condition (swaddled condition: median: 146 beats per minute; range: 126–171 beats per minute; nonswaddled condition: median: 136.5 beats per minute; range: 125–148 beats per minute; P = .013). There were, however, no significant differences in minimal HR or percentage HR increases, decreases, or total changes in the 2 conditions.
DISCUSSION
The study showed that, when infants between 6 and 16 weeks of age sleep swaddled and supine, they sleep longer, spend more time in NREM sleep, and awake less spontaneously than when not swaddled. These findings are reminiscent of previous reports of an increase in sleep continuity among swaddled infants. 1, 5, 7 These observations have been attributed to the motor restraint imposed by swaddling. This motor restriction could reduce the proprioceptive stimulation to the reticular activating system and hence the frequency of spontaneous behavioral arousals. 1, 5, 7
When the infants were sleeping swaddled, significantly lower auditory intensities were needed to induce cortical arousals from REM sleep than when they were not swaddled. This finding is in agreement with previous reports on sleep state-related arousals. After swaddling, spontaneous cortical arousals increased in REM sleep and decreased in NREM sleep. 7 To explain this sleep stage difference, it was suggested that infants in REM sleep habituated more easily to the increased frequency and magnitude of proprioceptive stimuli in the nonswaddled condition than in the swaddled condition. 7, 25
The observed effects of swaddling on arousal could also be related to modification of autonomic controls. In response to the first auditory noise of 50 dB(A), the maximal HR reached higher values in the swaddled condition than in the nonswaddled condition. In a previous study designed to evaluate the effects of swaddling on cardiac autonomic reactivity, we found that, after a 90-dB(A) white-noise stimulation, the infants had greater changes in HR when swaddled than when nonswaddled. 27 Swaddling also increased short-term HR variability, which has been attributed to the vagal influence. 27 Similar findings were reported for newborns and infants. 21, 28–30 Movement restriction has been associated with an increase in parasympathetic activity 21, 28–30 that can be blocked by atropine. 28 For spontaneous arousals, the increase in HR appeared before cortical arousals and increased with the arousal intensity, which suggests a continuous spectrum of arousal mechanisms, starting at the brainstem level and progressing to cortical areas. 31 In response to auditory stimulations, increases in blood pressure and HR were also correlated with arousal intensity. 32, 33 These results have been found among adults 31, 32 and infants. 33, 34 The increased tendency to arouse from sleep after auditory challenges could be attributable to the greater autonomic changes seen after stimulation in the swaddled condition.
Several limitations should be noted for this study. First, the limited number of infants studied and the short durations of swaddling could have precluded statistical significance for some of the effects of swaddling, such as changes in core temperature. No change in central temperature was found during bundling, however. 35 If an increase in central temperature should occur, it would favor increases in sympathetic tone 36 and decreases in arousals from sleep. 19 Second, auditory challenges were administered only during REM sleep. Because conflicting results have been reported regarding the effects of swaddling in REM and NREM sleep, 7 additional studies are needed to determine whether changes in arousability associated with auditory stimulations are also found in NREM sleep. Third, because the infants were studied lying supine, the present results cannot be extrapolated to the prone position. Finally, only noise challenges were used as a surrogate for environmental stress. To confirm the facilitating effect of swaddling on arousal, the influence of other stressors, such as hypoxic or hypercapnic conditions, should be evaluated.
Despite the limitations of this study, it can be concluded that swaddling increases sleep efficiency and lowers arousal thresholds during REM sleep. It remains to be determined whether this increased arousability from sleep contributes to reduce the risk of sudden death during sleep. 37, 38 Another potential protective mechanism of swaddling for SIDS could be derived from the motor restraint of swaddling, preventing the infants from rolling from supine to prone 7, 12 and from getting their heads caught in loose blankets. 12 However, before swaddling is recommended as a routine infant care technique, its reported potential complications, such as respiratory infections, pneumonia-related deaths, congenital hip dislocation, and hyperthermia, 6, 39–42 should be evaluated.
FOOTNOTES
Accepted Sep 24, 2004.
No conflict of interest declared.
REFERENCES
Lipton EL, Steinschneider A, Richmond JB. Swaddling, a child care practice: historical, cultural and experimental observations. Pediatrics. 1965;35 :521 –567
Chisholm JS. Swaddling, cradle boards and the development of children. Early Hum Dev. 1978;2 :255 –275
Moss J, Solomons HC. Swaddling then, there and now: historical, anthropological and current practices. Matern Child Nurs J. 1979;8 :137 –151
Giacoman SL. Hunger and motor restraint on arousal and visual attention in the infant. Child Dev. 1971;42 :605 –614
Gerard CM, Harris KA, Thach BT. Physiological studies on swaddling: an ancient child care practice which may promote the supine position for infant sleep. J Pediatr. 2002;141 :398 –403
Campos RG. Soothing pain-elicited distress in infants with swaddling and pacifiers. Child Dev. 1989;60 :781 –792
Ohgi S, Akiyama T, Arisawa K, Shigemori K. Randomised controlled trial of swaddling versus massage in the management of excessive crying in infants with cerebral injuries. Arch Dis Child. 2004;89 :212 –216
Ponsonby AL, Dwyer T, Gibbons LE, Cochrane JA, Wang YG. Factors potentiating the risk of sudden infant death syndrome associated with the prone position. N Engl J Med. 1993;329 :377 –382
Wilson CA, Taylor BJ, Laing RM, Williams SM, Mitchell EA. Clothing and bedding and its relevance to sudden infant death syndrome: further results from the New Zealand Cot Death Study. J Pediatr Child Health. 1994;30 :506 –512
L'Hoir MP, Engelberts AC, van Well GT, et al. Risk and preventive factors for cot death in the Netherlands, a low incidence country. Eur J Pediatr. 1998;157 :681 –688
Willinger M, Ko CW, Hoffman HJ, Kessler RC, Corwin MJ. Factors associated with caregivers' choice of infant sleep position 1994–1998: the National Infant Sleep Position Study. JAMA. 2000;283 :2135 –2142
Gilson E, Dembofsky CA, Rubin S, Greenspan JS. Infant sleep position practices 2 years into the "back to sleep" campaign. Clin Pediatr (Phila). 2000;39 :285 –289
Kato I, Franco P, Groswasser J, Scaillet S, Kelmanson I, Togari H, Kahn A. Incomplete arousal processes in infants with sudden death. Am J Respir Crit Care Med. 2003;164 :1464 –1469
Franco P, Groswasser J, Hassid S, Lanquart JP, Scaillet S, Kahn A. Prenatal exposure to cigarettes is associated with decreased arousal propensity in infants. J Pediatr. 1999;135 :34 –38
Franco P, Pardou A, Hassid S, Lurquin P, Kahn A. Auditory arousal thresholds are higher when infants sleep in the prone position. J Pediatrics. 1998;132 :240 –243
Horne RSC, Ferens D, Watts A-M, et al. The prone position impairs arousability in healthy term infants. J Pediatr. 2001;138 :811 –816
Franco P, Scaillet S, Valente F, Chabanski S, Groswasser J, Kahn A. Ambient temperature is associated with changes in infants' arousability from sleep. Sleep. 2001;24 :325 –329
Phillipson EA, Sullivan CE. Arousal: the forgotten response to respiratory stimuli. Am Rev Respir Dis. 1978;118 :807 –809
Kahn A, Rebuffat E, Sottiaux M. Effects of body movement restraint on cardiac response to auditory stimulation in sleeping infants. Acta Paediatr. 1992;81 :959 –961.
Carskadon MA, Rechtschaffen A. Monitoring and staging human sleep. In: Kryger MH, Roth T, Dement WC, eds. Principles and Practice of Sleep Medicine. Philadelphia, PA: WB Saunders; 2000:1197 –1216
Guilleminault C, Souquet M. Sleep states and related pathology. In: Korobkin R, Guilleminault C, eds. Advances in Perinatal Neurology. New York, NY: Spectrum Publications; 1979:225 –247
McNamara F, Wulbrand H, Thach BT. Habituation of the infant arousal response. Sleep. 1998;22 :320 –326
International Paediatric North Group on Arousals. The scoring of arousals in healthy term infants (between the ages of 1 and 6 months). J Sleep Res. 2005;14 :37 –41
Franco P, Scaillet S, Groswasser J, Kahn A. Increased cardiac autonomic responses to auditory challenges in swaddled infants. Sleep. 2004;27 :1527 –1532
Anderssen SH, Nicolaisen RB, Gabrielsen GW. Autonomic response to auditory stimulation. Acta Paediatr. 1993;82 :913 –918
Kaada B. Why is there an increased risk for sudden infant death in prone sleeping Fear paralysis and atrial stretch reflexes impaired Acta Paediatr. 1994;83 :548 –557
Lagercrantz H, Edwards D, Henderson-Smart D, Hertzeberg T, Jeffry H. Autonomic reflexes in preterm infants. Acta Paediatr Scand. 1990;79 :721 –728
Sforza E, Jouny C, Ibanez V. Cardiac activation during arousal in humans: further evidence for hierarchy in the arousal response. Clin Neurophysiol. 2000;111 :1611 –1619
Davies RJO, Belt PJ, Roberts SJ, Ali NJ, Stradling JR. Arterial blood pressure responses to graded transient arousal from sleep in normal humans. J Appl Physiol. 1993;74 :1123 –1130
Franco P, Van de Borne P, Chabanski S, et al. Physiological relationship between autonomic reactions and arousals in infancy. Sleep Med. 2002;3 (suppl 2):S49–S52
Harrington C, Kirjavainen T, Teng A, Sullivan CE. Cardiovascular responses to three simple, provocative tests of autonomic activity in sleeping infants. J Appl Physiol. 2001;91 :561 –568
Grover G, Berkowitz CD, Lewis RJ, Thompson M, Berry L, Seidel J. The effects of bundling on infant temperature. Pediatrics. 1994;94 :669 –673
Franco P, Szliwowski H, Dramaix M, Kahn A. Influence of ambient temperature on sleep characteristics and autonomic nervous control in healthy infants. Sleep. 2000;23 :401 –407
Franco P, Scaillet S, Wermenbol V, Valente F, Groswasser J, Kahn A. The influence of a pacifier on infants' arousals from sleep. J Pediatr. 2000;136 :775 –779
Horne RSC, Parslow PM, Ferens D, Watts AM, Adamson TM. Comparison of evoked arousability in breast and formula-fed infants. Arch Dis Child. 2004;89 :22 –25
Yurdakok K, Yavuz T, Taylor CE. Swaddling and acute respiratory infections. Am J Public Health. 1990;80 :873 –875
Block A. The Kurdistani Cradle Story, a modern analysis of this centuries' old infant swaddling practice. Clin Pediatr. 1996;5 :641 –645
Kutlu A, Memik R, Mutlu M, Kutlu R, Arslan A. Congenital dislocation of the hip and its relation to swaddling used in Turkey. J Pediatr Orthop. 1992;12 :598 –602
Van Gestel JP, L'Hoir MP, ten Berge M, Jansen NJ, Plotz FB. Risks of ancient practices in modern times. Pediatrics. 2002;110 (6). Available at: www.pediatrics.org/cgi/content/full/110/6/e78(Patricia Franco, MD, PhD,)
Institut National de la Santé et de la Recherche Médicale 628, Lyon, France
Pediatric Sleep Unit, Centre Hospitalier Chrétien Site de l'Espérance, Liège, Belgium
ABSTRACT
Objective. Swaddling is an old infant care practice. It was reported to favor sleep and to reduce crying among irritable infants. There are few data on the physiologic effects of swaddling on infants' sleep-wake characteristics. This study was conducted to evaluate whether swaddling influences infants' arousal thresholds for environmental auditory stress.
Design. Sixteen healthy infants, with a median age of 10 weeks (range: 6–16 weeks), underwent polygraphic recording in their usual supine position during one night. The infants were successively recorded swaddled and nonswaddled, or vice versa. In both conditions, the infants were exposed to white noise of increasing intensity, from 50 to 100 dB(A), during rapid eye movement sleep, to determine their arousal thresholds.
Results. Swaddling was associated with increases in the infants' sleep efficiency and in the time spent in non–rapid eye movement sleep. When swaddled, the infants awakened spontaneously less often. However, significantly less-intense auditory stimuli were needed during rapid eye movement sleep to induce cortical arousals when swaddled than when not swaddled.
Conclusions. Swaddling promotes more-sustained sleep and reduces the frequency of spontaneous awakenings, whereas induced cortical arousals are elicited by less-intense stimuli. These findings could indicate that, although swaddling favors sleep continuity, it is associated with increased responsiveness to environmental auditory stress.
Key Words: arousal infant sleep swaddling sudden infant death syndrome
Abbreviations: HR, heart rate NREM, non–rapid eye movement REM, rapid eye movement SIDS, sudden infant death syndrome EEG, electroencephalographic
In many parts of the world, infants are swaddled to sleep, with their bodies tightly wrapped in tissue cloths, sheets, or light blankets. 1–4 Infant bundling or swaddling has been reported to pacify a crying infant, to reduce motor activity, and to favor sleep. 1–3, 5–9
Swaddling has also been considered to reduce the risk of sudden infant death syndrome (SIDS). The odds ratio for SIDS among swaddled infants sleeping supine has been reported to be 0.64 to 0.69. 10, 11 However, the risk shows a threefold increase if the infants sleep prone. 10 Eight to 30% of infants <9 months of age are still placed prone to sleep, despite the preventive campaigns against SIDS. 12–14 Excessive crying is one of the reasons not to place infants on their backs to sleep. If swaddling prevents excessive crying among infants, then it could become a method to promote supine sleep and to prevent SIDS. 6, 7
Sleep laboratory observations have associated SIDS with a decrease in the infant's arousal from sleep. 15 Healthy infants developed increased auditory arousal thresholds for a variety of stimuli in conditions known to favor SIDS, such as prenatal exposure to cigarette smoking, 16 sleeping prone, 17, 18 and sleeping in a heated room. 19 Arousal from sleep could be an important defense mechanism against potentially dangerous situations during sleep. 20 The purpose of this study was to evaluate the influence of swaddling on infants' sleep continuity and arousal thresholds for auditory environmental stress.
METHODS
Subjects
Sixteen healthy infants underwent polygraphic recording during one night. The infants were successively selected from a larger group of infants recruited for a research program on sleep-related behavior if they met the following inclusion criteria for study entry. The infants were born at term to nonsmoking parents who used no alcohol or drugs, with no family history of SIDS. The infants' hearing, evaluated with an audiometer (SCR Electronics, Paris, France) after birth, was normal. At the time of the study, the infants were <6 months of age, slept supine, were healthy, and took no medication. The infants were not sleep deprived within the 24 hours before the study, as reported by the parents. The aim and methods of the study were approved by the university ethics committee and were explained to the parents, who gave their informed consent.
Monitoring Procedures
Monitoring was conducted in a quiet room at an ambient temperature, ranging from 21 to 24°C (69.8–75.2°F). The infants wore their own pajamas and were covered with a blanket. The clothing and bedding corresponded to 3° tog insulation. The following variables were recorded simultaneously: 8 electroencephalographic (EEG) derivations applied according to the 10–20 system, 2 electrooculograms, a digastric electromyogram, and an electrocardiogram. Thoracic and abdominal respiratory movements were measured with inductance plethysmography, and airflow was measured with oral and nasal thermistors. Oxygen saturation was recorded continuously with a transcutaneous sensor (Nellcor, Pleasanton, CA). An actigraph was placed on one arm to measure body movements. The data were collected on computerized polygraph recorders (Morpheus System; Medatec, Brussels, Belgium).
Temperature Measurements
Core temperature was measured for 7 infants (4 boys and 3 girls) whose parents had agreed to the placement of a rectal probe 2 cm inside the infant's rectum. Body temperature was recorded before and after the swaddled and nonswaddled sleep periods.
Swaddling
When nonswaddled, the infants were sleeping supine and were free to move their legs and arms. Swaddling was obtained with sand bags and bed sheets tidily wrapped around the body, which prevented the infants from moving their arms and legs. Similar swaddling techniques have been used in other studies. 21 The study started at 9:00 PM, and the infants were allowed to fall asleep nonswaddled in their usual supine position. At 1:01 AM, the infants were gently wrapped as described before. To avoid any confounding effect resulting from nyctohemeral influences, 8 of the 16 infants were chosen at random to be initially studied nonswaddled and then swaddled. An inverse sequence was used for the other infants. At 9:00 PM, these infants were allowed to fall asleep nonswaddled and were wrapped when they were already asleep. At 1:01 AM, they were liberated from their constraints. Care was taken to avoid awakening the infants during swaddling and release measures. The infants were studied asleep in swaddled and nonswaddled conditions. This study evaluated the effect of swaddling on sleep continuity but not on the time to fall asleep.
Auditory Stimulation
In both swaddled and nonswaddled conditions, the infants were exposed to auditory challenges during rapid eye movement (REM) sleep, to determine their auditory arousal thresholds. 22 White noise of increasing intensity was presented for 3 seconds through a loudspeaker (SCR Electronics, Paris, France), at a distance of 3 cm from the infant’s ear. The level of the audiometer had been calibrated previously with a sonometer (Brul and Kjaer model 2209; B&K Medical, Copenhagen, Denmark), at an equivalent distance. Physical decibels were expressed as physiologic decibels (A). The sound level was increased by 10 dB, from 50 to 100 dB(A). The time between presentations was 1 minute. A complete auditory challenge lasted a maximum of 6 minutes. A challenge was interrupted when the infant awakened, as defined by opening of the eyes and/or crying, or when a stimulation level of 100 dB(A) was reached. The auditory signal was automatically identified on the sleep recording. In both normal and swaddled conditions, the infants were tested only during REM sleep, after a minimum of 5 minutes in this sleep stage. Staging of REM sleep requires the coincidence of specific activities in all 3 electrographic measures, ie, "desynchronized" EEG signals, bursts of REMs, and suppression of electromyographic activity. 23, 24 That stage of sleep was chosen because transient brain activations in response to auditory stimulations are seen more readily in REM sleep than in non–rapid eye movement (NREM) sleep. 19 The challenges were not repeated in other sleep stages, to reduce the risk of sleep fragmentation and secondary increases in arousal thresholds. 25 Similar methods have been used in previous studies. 16, 17, 19, 22
Data Analyses
Sleep Stages
Each 30-second period of the sleep recordings was scored as NREM, REM, wakefulness, or movement time according to standard criteria. 24 Before auditory stimulations, sleep efficiency was defined as the time spent sleeping divided by the total recording time, multiplied by 100. The frequencies of NREM, REM, wakefulness, and movement were measured and expressed as percentages, after division of the duration of each sleep state by the total duration of the period and multiplication by 100. 22 Evaluation of the recordings was performed without knowledge of the infant's condition and time of recording.
Cardiorespiratory Parameters and Oxygen Saturation
Episodes of sleep apnea were scored only if they lasted 3 seconds. Central apnea was scored when flat tracings were obtained simultaneously for thoracic movements and thermistors. Periodic breathing was defined as 3 episodes of central apnea separated by <20 seconds of breathing movements. Obstructive apnea was scored when continuous deflections were obtained for the thoracic movements and a flat tracing was recorded from the thermistors. Mixed apnea was defined as central apnea followed directly by obstructive episodes and was scored together with obstructive apnea. The frequency of apnea was calculated as an index by dividing the absolute number of events by the total sleep time of the period (in minutes) and then multiplying by 60. 22 Median values for oxygen saturation, heart rate (HR), and respiratory rate were calculated for 1-minute stable sleep epochs. Overall HR variability was defined as the SD of the R-R interval values calculated between successive QRS complexes. Decreases in HR and oxygen saturation refer to changes of >10% and >4% of basal values, respectively.
Spontaneous Arousals
Spontaneous arousals were subdivided into subcortical activation and cortical arousal. 26 A subcortical activation was scored if no change in EEG findings was seen but 2 of the following changes occurred: a gross body movement detected with movement sensors, seen as an artifact in the somatic channels (electrocardiographic, EEG, and respiratory parameters), or observed directly; changes in HR (10% of baseline values); or changes in breathing patterns (any change in frequency and/or amplitude). A cortical arousal was scored with the above criteria, with the addition of the occurrence of an abrupt change in EEG background frequency of 1 Hz, for a minimum of 3 seconds. Total arousal corresponded to the sum of cortical arousal and subcortical activation. The intervals between successive spontaneous arousals were calculated in total sleep time, REM sleep, and NREM sleep.
Baseline sleep states that preceded arousal or subcortical activation were established during 20-second time periods. At least 10 seconds of uninterrupted state were required between arousals. At least 15 seconds of continuous breathing were required after an episode of apnea and an arousal reaction for this to be defined as spontaneous. An awakening was scored when the infant opened the eyes and/or cried.
Induced Arousals and Determination of Arousal Thresholds
An induced arousal was scored if, within 10 seconds after the start of an auditory stimulation, abrupt changes occurred during a period of 3 seconds that corresponded to the definition of cortical arousals. 22, 26 The breathing and EEG signals were compared with those recorded during the 20 seconds preceding the auditory challenge, to reduce the risk of spontaneously occurring arousals. Arousal thresholds were defined by the lowest auditory stimulus, expressed in decibels (A), needed to induce an arousal.
HR Changes During Auditory Challenge
Changes in HR autonomic controls in response to an auditory challenge were calculated after the first auditory stimulus of 50 dB(A). R-R intervals, calculated between successive QRS complexes, were digitalized at 300 Hz, with an accuracy of 0.3 milliseconds. Basal median HR values were measured for 10 seconds before the stimulation. Maximal and minimal HR values were measured in the 20 seconds after the sound. The percentage HR increase was calculated as the maximal HR value during stimulation divided by the median basal HR value, multiplied by 100. The percentage HR decrease was calculated with the minimal values measured after stimulation. The percentage of total HR change corresponded to the difference between the maximal HR value and the minimal HR value after the stimulus divided by the median basal HR value, multiplied by 100.
Statistical Analyses
Statistical evaluation was performed with the use of Wilcoxon's matched-pairs, signed-ranks test and Friedman's statistics, with a level of significance of .05.
RESULTS
The 16 infants studied included 10 male and 6 female infants, with a median age of 10 weeks (range: 6–16 weeks). The median gestational age was 39 weeks (range: 38–40.5 weeks), the median birth weight was 3120 g (range: 2380–3890 g), and the median weight at the time of the study was 5490 g (range: 3800–7350 g). There were 3 small-for-gestational age infants. No mother reported the consumption of tobacco, alcohol, or illegal drugs.
The median time to resume sleep after swaddling was 30 seconds (range: 0–7 minutes). Most sleep and cardiorespiratory characteristics were similar in the swaddled and nonswaddled conditions (Tables 1 and 2). After central and obstructive apnea, no differences were seen between the 2 study conditions in the frequency of HR decelerations or in decreases in oxygen desaturation.
As shown in Table 3, the swaddled condition was associated with significantly greater sleep efficiency (P = .030), less time spent awake after sleep onset (P = .006), and more time spent in NREM sleep (P = .028), compared with the nonswaddled condition. Although all infants aroused from sleep in response to the auditory challenges, less-intense auditory stimuli were needed to arouse the infants when they were swaddled than when they were not swaddled (P = .005).
No relationship was found between auditory arousal thresholds and the order of the study, gestational age, gender, birth weight, or age or weight at the time of the study. No difference was seen in the time of night when the infants were exposed to the auditory challenge or the frequency or duration of awakenings in the 2 study conditions.
During cortical arousals, there were no significant differences in HR changes in the 2 conditions. In response to the first auditory noise of 50 dB(A), however, the maximal HR reached higher values in the swaddled condition than in the nonswaddled condition (swaddled condition: median: 146 beats per minute; range: 126–171 beats per minute; nonswaddled condition: median: 136.5 beats per minute; range: 125–148 beats per minute; P = .013). There were, however, no significant differences in minimal HR or percentage HR increases, decreases, or total changes in the 2 conditions.
DISCUSSION
The study showed that, when infants between 6 and 16 weeks of age sleep swaddled and supine, they sleep longer, spend more time in NREM sleep, and awake less spontaneously than when not swaddled. These findings are reminiscent of previous reports of an increase in sleep continuity among swaddled infants. 1, 5, 7 These observations have been attributed to the motor restraint imposed by swaddling. This motor restriction could reduce the proprioceptive stimulation to the reticular activating system and hence the frequency of spontaneous behavioral arousals. 1, 5, 7
When the infants were sleeping swaddled, significantly lower auditory intensities were needed to induce cortical arousals from REM sleep than when they were not swaddled. This finding is in agreement with previous reports on sleep state-related arousals. After swaddling, spontaneous cortical arousals increased in REM sleep and decreased in NREM sleep. 7 To explain this sleep stage difference, it was suggested that infants in REM sleep habituated more easily to the increased frequency and magnitude of proprioceptive stimuli in the nonswaddled condition than in the swaddled condition. 7, 25
The observed effects of swaddling on arousal could also be related to modification of autonomic controls. In response to the first auditory noise of 50 dB(A), the maximal HR reached higher values in the swaddled condition than in the nonswaddled condition. In a previous study designed to evaluate the effects of swaddling on cardiac autonomic reactivity, we found that, after a 90-dB(A) white-noise stimulation, the infants had greater changes in HR when swaddled than when nonswaddled. 27 Swaddling also increased short-term HR variability, which has been attributed to the vagal influence. 27 Similar findings were reported for newborns and infants. 21, 28–30 Movement restriction has been associated with an increase in parasympathetic activity 21, 28–30 that can be blocked by atropine. 28 For spontaneous arousals, the increase in HR appeared before cortical arousals and increased with the arousal intensity, which suggests a continuous spectrum of arousal mechanisms, starting at the brainstem level and progressing to cortical areas. 31 In response to auditory stimulations, increases in blood pressure and HR were also correlated with arousal intensity. 32, 33 These results have been found among adults 31, 32 and infants. 33, 34 The increased tendency to arouse from sleep after auditory challenges could be attributable to the greater autonomic changes seen after stimulation in the swaddled condition.
Several limitations should be noted for this study. First, the limited number of infants studied and the short durations of swaddling could have precluded statistical significance for some of the effects of swaddling, such as changes in core temperature. No change in central temperature was found during bundling, however. 35 If an increase in central temperature should occur, it would favor increases in sympathetic tone 36 and decreases in arousals from sleep. 19 Second, auditory challenges were administered only during REM sleep. Because conflicting results have been reported regarding the effects of swaddling in REM and NREM sleep, 7 additional studies are needed to determine whether changes in arousability associated with auditory stimulations are also found in NREM sleep. Third, because the infants were studied lying supine, the present results cannot be extrapolated to the prone position. Finally, only noise challenges were used as a surrogate for environmental stress. To confirm the facilitating effect of swaddling on arousal, the influence of other stressors, such as hypoxic or hypercapnic conditions, should be evaluated.
Despite the limitations of this study, it can be concluded that swaddling increases sleep efficiency and lowers arousal thresholds during REM sleep. It remains to be determined whether this increased arousability from sleep contributes to reduce the risk of sudden death during sleep. 37, 38 Another potential protective mechanism of swaddling for SIDS could be derived from the motor restraint of swaddling, preventing the infants from rolling from supine to prone 7, 12 and from getting their heads caught in loose blankets. 12 However, before swaddling is recommended as a routine infant care technique, its reported potential complications, such as respiratory infections, pneumonia-related deaths, congenital hip dislocation, and hyperthermia, 6, 39–42 should be evaluated.
FOOTNOTES
Accepted Sep 24, 2004.
No conflict of interest declared.
REFERENCES
Lipton EL, Steinschneider A, Richmond JB. Swaddling, a child care practice: historical, cultural and experimental observations. Pediatrics. 1965;35 :521 –567
Chisholm JS. Swaddling, cradle boards and the development of children. Early Hum Dev. 1978;2 :255 –275
Moss J, Solomons HC. Swaddling then, there and now: historical, anthropological and current practices. Matern Child Nurs J. 1979;8 :137 –151
Giacoman SL. Hunger and motor restraint on arousal and visual attention in the infant. Child Dev. 1971;42 :605 –614
Gerard CM, Harris KA, Thach BT. Physiological studies on swaddling: an ancient child care practice which may promote the supine position for infant sleep. J Pediatr. 2002;141 :398 –403
Campos RG. Soothing pain-elicited distress in infants with swaddling and pacifiers. Child Dev. 1989;60 :781 –792
Ohgi S, Akiyama T, Arisawa K, Shigemori K. Randomised controlled trial of swaddling versus massage in the management of excessive crying in infants with cerebral injuries. Arch Dis Child. 2004;89 :212 –216
Ponsonby AL, Dwyer T, Gibbons LE, Cochrane JA, Wang YG. Factors potentiating the risk of sudden infant death syndrome associated with the prone position. N Engl J Med. 1993;329 :377 –382
Wilson CA, Taylor BJ, Laing RM, Williams SM, Mitchell EA. Clothing and bedding and its relevance to sudden infant death syndrome: further results from the New Zealand Cot Death Study. J Pediatr Child Health. 1994;30 :506 –512
L'Hoir MP, Engelberts AC, van Well GT, et al. Risk and preventive factors for cot death in the Netherlands, a low incidence country. Eur J Pediatr. 1998;157 :681 –688
Willinger M, Ko CW, Hoffman HJ, Kessler RC, Corwin MJ. Factors associated with caregivers' choice of infant sleep position 1994–1998: the National Infant Sleep Position Study. JAMA. 2000;283 :2135 –2142
Gilson E, Dembofsky CA, Rubin S, Greenspan JS. Infant sleep position practices 2 years into the "back to sleep" campaign. Clin Pediatr (Phila). 2000;39 :285 –289
Kato I, Franco P, Groswasser J, Scaillet S, Kelmanson I, Togari H, Kahn A. Incomplete arousal processes in infants with sudden death. Am J Respir Crit Care Med. 2003;164 :1464 –1469
Franco P, Groswasser J, Hassid S, Lanquart JP, Scaillet S, Kahn A. Prenatal exposure to cigarettes is associated with decreased arousal propensity in infants. J Pediatr. 1999;135 :34 –38
Franco P, Pardou A, Hassid S, Lurquin P, Kahn A. Auditory arousal thresholds are higher when infants sleep in the prone position. J Pediatrics. 1998;132 :240 –243
Horne RSC, Ferens D, Watts A-M, et al. The prone position impairs arousability in healthy term infants. J Pediatr. 2001;138 :811 –816
Franco P, Scaillet S, Valente F, Chabanski S, Groswasser J, Kahn A. Ambient temperature is associated with changes in infants' arousability from sleep. Sleep. 2001;24 :325 –329
Phillipson EA, Sullivan CE. Arousal: the forgotten response to respiratory stimuli. Am Rev Respir Dis. 1978;118 :807 –809
Kahn A, Rebuffat E, Sottiaux M. Effects of body movement restraint on cardiac response to auditory stimulation in sleeping infants. Acta Paediatr. 1992;81 :959 –961.
Carskadon MA, Rechtschaffen A. Monitoring and staging human sleep. In: Kryger MH, Roth T, Dement WC, eds. Principles and Practice of Sleep Medicine. Philadelphia, PA: WB Saunders; 2000:1197 –1216
Guilleminault C, Souquet M. Sleep states and related pathology. In: Korobkin R, Guilleminault C, eds. Advances in Perinatal Neurology. New York, NY: Spectrum Publications; 1979:225 –247
McNamara F, Wulbrand H, Thach BT. Habituation of the infant arousal response. Sleep. 1998;22 :320 –326
International Paediatric North Group on Arousals. The scoring of arousals in healthy term infants (between the ages of 1 and 6 months). J Sleep Res. 2005;14 :37 –41
Franco P, Scaillet S, Groswasser J, Kahn A. Increased cardiac autonomic responses to auditory challenges in swaddled infants. Sleep. 2004;27 :1527 –1532
Anderssen SH, Nicolaisen RB, Gabrielsen GW. Autonomic response to auditory stimulation. Acta Paediatr. 1993;82 :913 –918
Kaada B. Why is there an increased risk for sudden infant death in prone sleeping Fear paralysis and atrial stretch reflexes impaired Acta Paediatr. 1994;83 :548 –557
Lagercrantz H, Edwards D, Henderson-Smart D, Hertzeberg T, Jeffry H. Autonomic reflexes in preterm infants. Acta Paediatr Scand. 1990;79 :721 –728
Sforza E, Jouny C, Ibanez V. Cardiac activation during arousal in humans: further evidence for hierarchy in the arousal response. Clin Neurophysiol. 2000;111 :1611 –1619
Davies RJO, Belt PJ, Roberts SJ, Ali NJ, Stradling JR. Arterial blood pressure responses to graded transient arousal from sleep in normal humans. J Appl Physiol. 1993;74 :1123 –1130
Franco P, Van de Borne P, Chabanski S, et al. Physiological relationship between autonomic reactions and arousals in infancy. Sleep Med. 2002;3 (suppl 2):S49–S52
Harrington C, Kirjavainen T, Teng A, Sullivan CE. Cardiovascular responses to three simple, provocative tests of autonomic activity in sleeping infants. J Appl Physiol. 2001;91 :561 –568
Grover G, Berkowitz CD, Lewis RJ, Thompson M, Berry L, Seidel J. The effects of bundling on infant temperature. Pediatrics. 1994;94 :669 –673
Franco P, Szliwowski H, Dramaix M, Kahn A. Influence of ambient temperature on sleep characteristics and autonomic nervous control in healthy infants. Sleep. 2000;23 :401 –407
Franco P, Scaillet S, Wermenbol V, Valente F, Groswasser J, Kahn A. The influence of a pacifier on infants' arousals from sleep. J Pediatr. 2000;136 :775 –779
Horne RSC, Parslow PM, Ferens D, Watts AM, Adamson TM. Comparison of evoked arousability in breast and formula-fed infants. Arch Dis Child. 2004;89 :22 –25
Yurdakok K, Yavuz T, Taylor CE. Swaddling and acute respiratory infections. Am J Public Health. 1990;80 :873 –875
Block A. The Kurdistani Cradle Story, a modern analysis of this centuries' old infant swaddling practice. Clin Pediatr. 1996;5 :641 –645
Kutlu A, Memik R, Mutlu M, Kutlu R, Arslan A. Congenital dislocation of the hip and its relation to swaddling used in Turkey. J Pediatr Orthop. 1992;12 :598 –602
Van Gestel JP, L'Hoir MP, ten Berge M, Jansen NJ, Plotz FB. Risks of ancient practices in modern times. Pediatrics. 2002;110 (6). Available at: www.pediatrics.org/cgi/content/full/110/6/e78(Patricia Franco, MD, PhD,)