mise à jour du
22 avril 2007
Infant Behav Dev.
Yawning frequency and distribution
in preterm and near term infants
assessed throughout 24-h recordings
Fiorenza Giganti, Marie J. Hayes, Giovanni Cioni, Piero Salzarulo
Department of Psychology, University of Maine, Orono, USA
Department of Developmental Neuroscience, Stella Maris Scientific Institute, University of Pisa, Italy
Sleep Lab, Department of Psychology, University of Florence, Italy


Introduction In the adult yawning is a relatively rare behavioral pattern (Baenninger, Binkley, & Baenninger, 1996; Ficca & Salzarulo, 2002) frequently associated with stretching (Provine, 1986). Yawning has been observed in all classes of vertebrates (Baenninger, 1997); in non-human primates it was related to the rest-activity cycle with incidence higher before than after sleep episode (Walusinski & Deputte, 2004). Studies performed in the eighties showed that yawning occurs as early as 12&endash;14 weeks of gestational age (de Vries, Visser, & Prechtl, 1982); in successive studies the incidence was not found to change between 20 and 36 weeks of gestational age (Roodenburg, Wladimiroff, van Es, & Prechtl, 1991). Yawns in foetuses has been confirmed recently by Walusinski, Kurjak, Andonotopo, and Azumendi (2005). In preterm infants between 30 and 35 weeks of post-conceptional age recorded for 5 h during the nocturnal period (Giganti, Hayes, Akilesh, & Salzarulo, 2002), the frequency of yawns was found to be quite low (c. 1/h) and different in some respect to the adult pattern in that yawns were rarely accompanied by stretching.
-Giganti F, Hayes MJ, Akilesh MR, Salzarulo P. Yawning and behavioral states in premature infants. Dev Psychobiol. 2002;41(3):289-96.
-Giganti F, Hayes MJ Cioni G, Salzarulo P Yawning frequency and distribution in preterm and near term infants assessed throughout 24-h recordings Infant Behav & Development 2007;30(4):641-647
-Giganti F, Ziello ME Contagious and spontaneous yawning in autistic and typically developing children CPL 2009
-Giganti F, Zilli I. The daily time course of contagious and spontaneous yawning among humans. J Ethol 2011;29(2):215-216
-Giganti F, Zilli I, Aboudan S, Salzarulo P. Sleep, sleepiness and yawning. Front Neurol Neurosci. 2010;28:42-6.
-Giganti F, Salzarulo P. Yawning throughout life. Front Neurol Neurosci. 2010;28:26-31
-Giganti F, Toselli M, Ramat S. Developmental trends in a social behaviour: contagious yawning in the elderly. Giornale di Psicologia dello Sviluppo. 2012;101:111-117
-Giganti F, Guidi S, Ramat S, Zilli I, Raglione LM, Sorbi S, Salzarulo P. Yawning: A behavioural marker of sleepiness in de novo PD patients. Parkinsonism Relat Disord 2013
-Zilli I, Giganti F, Salzarulo P. Yawning in morning and evening types. Physiol Behav 2007;91(2-3):218-222
-Zilli I, Giganti F, Uga V. Yawning and subjective sleepiness in the ederly. J Sleep Res 2008;17:3003-308
Both in the adult (Provine & Hamernik, 1986) and in preterm infants (Giganti et al., 2002) it has been suggested that yawning could be involved in the modulation of arousal processes. Yawning in the adult is frequent when subjects watch or participate in repetitive and monotonous activities (Provine & Hamernik, 1986) and in preterm infants is temporally linked to increased behavioural arousal as indicated by contemporaneous motor activation across states (Giganti et al., 2002). In preterm infants (Giganti et al., 2002) yawning was more common during drowsiness and waking state, whereas the presence of yawn in quiet sleep was extremely rare. In foetuses observed at 20&endash;22 weeks of gestational age, yawns did not show diurnal variations (de Vries, Visser, Mulder, & Prechtl, 1987). In the adult, yawning frequency increases in the early morning and in the late evening (Baenninger et al., 1996) and is strongly associated with sleep onset and awakening (Baenninger et al., 1996; Greco, Baenninger, & Govern, 1993; Provine, Hamernik, & Curchack, 1987).
The aim of this study was to extend the analysis of yawning in preterm and near term infants to a 24 h period in order to investigate if there is a diurnal variation of the yawning frequency as observed in the adult. In addition, a wide age range was considered (31&endash;40 weeks of post-conceptional age) which allowed the capture of modifications in yawn frequency across early development.
Method Subjects Twelve low-risk preterm born infants (five females, seven males) were selected among those admitted to the neonatal units of the University of Pisa and of the University of Florence according to previously published criteria (Giganti et al., 2001), suitable to exclude any clinical complications. The low-risk condition was evaluated according the following criteria: reliably known postmenstrual age, birth weight >10 and <90 percentile, Apgar score >7 at 5 min, no chromosomal or other genetic abnormalities, no symptoms of cardiopulmonary complications, brain ultrasound scan with no signs of abnormalities, with the exception of intraventricular haemorrhage grade 1 according to Volpe (1995) or transient periventricular echodensity lasting less than 7 days (de Vries, Eken, & Dubowitz, 1992); EEG executed in the first days of life with no abnormalities related to brain lesions and/or unfavorable outcome (Biagioni et al., 1994; Biagioni, Boldrini, Bottone, Pieri, & Cioni, 1996), and neonatal neurological examination showing no abnormal signs (Cioni et al., 1997).
All subjects were in a stable physical condition at the time of the study, with no infective, metabolic or haematological abnormalities and no pharmacotherapy that could be potentially disruptive of behavior in the days preceding the recording. Follow up showed normal neurological examination at discharge from the NICU up to 12 months of corrected age. Characteristics of the sample are listed in Table 1. The mean gestational age was 33.6 (range 29&endash;39); postconceptional age (PCA) ranged from 31 to 40 weeks. The infants were recorded as soon after birth as their condition was clinically stable and optimal: postnatal age ranged from 3 days to 4 weeks. The research project was approved by the Ethical Committee. Informed consent was obtained from all parents.
Procedure Recording of infant behavior All infants were continuously observed and video-recorded in the incubator, which was located in a quiet room of the neonatal ward; older infants, already in a cot, were put into the incubator at neutral temperature for the recording, which began after about 30 min of adaptation. A S-VHS video-camera, set to real time was mounted approximately 1m above the incubator, at an angle of 45?, and a video-recorder (Panasonic SG-DP200) were used. Infant behavior and all the interventions (medications, feedings, etc.) carried out by the neonatal ward staff were video-recorded. Babies were fed either by oro-gastric tube or by bottle. Feedings were scheduled every 3&endash;4 h for all infants.
All observations lasted approximately 24 h (mean = 22 h; range = 19&endash;24 h). In the Neonatal Intensive Care Unit, light intensity was maintained at full light during the day (range of light intensity measured in lux: 1000&endash;2200 lm/m2), whereas during the night (between 21.00 and 08.00 h) it is reduced (range = 30&endash;1000 lm/m2). Off-line analysis of infant behavior was conducted on the entire session through video-recordings playback in the laboratory.
Behavior measures Yawn coding Spontaneous yawning was defined as opening of the mouth to its full extension in a dramatic stretch movements that included all facial muscles below the eyes, frequent closing of the eyes and brow and forehead contraction (Giganti et al., 2002). In some cases, yawning was accompanied by a general body stretch involving synchronized, bilateral arm and trunk extension movements occurring over several seconds. However, this "larger" set of movements was not usual and not a required component in our yawn coding criteria. Yawning bout structure was confined to a single isolated event in 97% of study observation. Bout of >1 yawn never exceeded two (3%) yawns per 1 min period. When more than one yawn occurred, multiple yawns were temporally contiguous.
Coding of activity The coding system of infant behavior was based on the observation of infant body motility and on its relationship to behavioral states as described by Stefanski et al. (1984) in preterm infants and Hadders-Algra, Nakae,Van Eykern, Klip- Van den Nieuwendijk, and Prechtl (1993) in full term infants. Each minute of the recordingwas classified (Giganti et al., 2001) according to the prevalent motility pattern observed during that minute either continuously or discontinuously. Three motility patterns were distinguished: a pattern characteristic of quiet sleep (P1): no body movements and occasional occurrence of startle; a pattern characteristic of active sleep (P2): the presence of small body movements, including slow intermittent writhing movements, jerky startles and small movements of an extremity, smiles, grimaces and other facial activity and occasional whimpers; slow and fluent or sometimes fragmented generalized movements may be seen; and a pattern characteristic of wakefulness with and without crying (P3) characterized by the presence of gross generalized body movements, often forceful, varying in speed and amplitude, with prolonged startles, marked stretching and writhing. No codingwas given in case of technical problems (nurses standing in front of the camera, delay in the introduction of a new cassette in the recorder, etc.). Handling periods were excluded entirely from the analysis.
Data analysis We computed: (a) total and rate (yawns/h) across 24 h period for each subject (multiple yawns were included), total minutes scored for each of the three motility patterns for each subject, the quotient between number of minutes with yawns in each motility pattern and the number of minutes of each motility pattern in order to assess the probability of yawn occurrence in each motility pattern; (b) the yawning rate (yawns/h) during the 24 h period, and during the day (8.00&endash;20.00) and during the night (20.00&endash;8.00) for each subject; (c) the yawning rate (yawns/h) within 3-h interval splitting the 24 h period into eight 3-h intervals (08.00&endash;11.00 h; 11.00&endash;14.00 h; 14.00&endash;17.00 h; 17.00&endash;20.00 h; 20.00&endash;23.00 h; 23.00&endash;2.00 h; 2.00&endash;5.00 h; 5.00&endash;8.00 h
Because some recordings were lasting slightly longer or shorter than 24 h, data were normalized for the exact duration of the recording. The quotient between number of minutes with yawns in each motility pattern and the number of minutes of each motility pattern was used to assess the probability of yawn occurrence in each motility pattern independent of the inequalities in the proportion of each motility pattern. The Friedman test was used to show differences among the probabilities of yawning from each of the motility pattern. All possible pairings of the motility pattern quotients were examined with theWilcoxon test. In order to examine the age trend for number of yawns during the 24 h period, during the day and during the night a correlation analysis (Spearman's rho) was computed. Day&endash;night difference for number of yawns was examined with Wilcoxon test. The Friedman test was used to show differences in the yawning distribution across 24-h. Statistical significance was set at pē0.05.
Results Yawning incidence The rate of yawning across all infants in the 24 h recording period averaged 1.10±0.7 yawns/h. Fig. 1 shows that, using the quotient method, there were significant differences in the probabilities of yawning across the motility patterns (Friedman's £q2(2) = 20,66 p = .000). Comparison of yawn incidence in all possible pairings of motility patterns revealed that yawns in the waking motility pattern were greater than those in P1 (quiet sleep type: z =Å|3.05; p = .002) or P2 (active sleep type: z = 2.58; p = .01) motility patterns. In addition a higher incidence of yawns in P2 (active sleep motility pattern) than in P1 (quiet sleep motility pattern) was observed (z =Å|3.05; p = .002).
Age changes According to a regression analysis, the rate of yawns during the 24 h observation was found to decrease significantly as a function of age (rho =Å|.79, p = .002) as shown in Fig. 2. This decrease was observed during the day (rho =Å|.79, p = .002) (Fig. 3), but not during the night (rho =Å|.32, ns). 3.3. Yawning distribution The rate of yawns did not differ between day and night (z = 0; n.s.) as well as during the eight 3-h intervals across 24 h period (Friedman's £q2(7) = 10,27, n.s.).
Discussion This study utilized 24 h recordings which extends the analysis of yawns in preterm infants that we have previously reported in which our observation window was limited to 24.00&endash;05.00 h (Giganti et al., 2002). In addition, the wide range of ages considered allowed for capturing the attenuation of yawn frequency as a developmental change during the preterm period. As an extension of our previous work (Giganti et al., 2002), the results from this study determined the incidence and distribution of yawning to both a wider age range and for a full 24 h observation period. Between 31 and 40 weeks of PCA, yawning is not a frequent event.
Nevertheless, the frequency of yawns at this stage of development is much higher (c. 25 yawns/24 h) than in the adult, who yawns about 7&endash;8 times over 24 h (Baenninger et al., 1996). Similarly, as has been observed for eye movements (Birnholz, 1981; Curzi-Dascalova, 2002), in preterm and near term infants, yawns are typically isolated events and are not yet organised into consistent bursts as is observed in the adult. In the adult the presence of yawning has been related to central nervous system (CNS) arousal modulation, e.g. yawning increases before and after sleep episode (Provine et al., 1987) and when subjects are involved in repetitive or monotonous activities (Provine & Hamernik, 1986). As found previously (Giganti et al., 2002) in preterm infants yawning is associated with an increase in nonspecific motoric activation, arguing further for an activation role.
In the present study, yawning was observed to be more frequent during the waking motility pattern, suggesting a relationship between yawns and high levels of activity. In contrast, the presence of yawns is inhibited during a quiescence periods, i.e. during the P1 quiet sleep motility pattern. The hypothesis that with low motoric activation "the necessary and sufficient conditions for the elicitation of yawns are not present, or may be actively inhibited" (Giganti et al., 2002, p. 294) is confirmed in the present study which used the entire 24 h period for observation. Between 31 and 40 weeks the incidence of yawns, during the 24 h period, significantly decreases, which is different from several spontaneous motor patterns that did not modify between 28 and 39 weeks postmenstrual age (Cioni & Prechtl, 1990).
In our study the developmental decrease in yawn incidence is accounted for mainly by yawns during the day. This marked reduction parallels the increase of waking episode duration during the day (Giganti, Ficca, Cioni, & Salzarulo, 2006). Hence, the improvement in wake stability during the diurnal period may reflect the decreased need of yawning to support or stabilize the arousal levels. Whit regard to the yawning distribution across the 24 h circadian day,we found that preterm infants differed from the adults who yawn mainly at the sleep&endash;wake transitions in circadian time, i.e. awakening in the morning and approaching sleep time in the evening. Preterm and near term infants did not show a temporal modulation of the yawn distribution across the 24 h period. The high frequency of sleep and wake episodes observed in this period of life could explain this result. Indeed, as in the adult (Provine et al., 1987) and the neonates (Wolff, 1987), and also in preterm and near term infants, yawns may localize before and after a sleep episode.
However, since in the early epochs of life there is not a main sleep episode in the night, yawns are not concentrated in the evening or in the early morning as in the adult. A more fine-grain analysis investigating yawning distribution for each sleep and waking episode is necessary to confirm this hypothesis and to shed light on the specific role of yawns during the first epochs of development. The uniform temporal distribution of yawns during 24 h is in agreement with previous results showing that in preterm infants there is poor circadian control of some physiological variables (Mirmiran & Kok, 1991).
The establishment of the relationship between yawn and high levels of motoric activation seems to be more precocious than the establishment of a preferential distribution of yawns across the 24 h period. The marked decrease in yawn frequency with age may be related to the development of circadian and homeostatic control of sleep and wake periods which become longer as the neonates approache term age (Giganti et al., 2006). However the respective contribution of the circadian and homeostatic control should be assessed by further studies.
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-Giganti F, Hayes MJ, Akilesh MR, Salzarulo P. Yawning and behavioral states in premature infants Developmental Psychobiology 2002; 41; 3; 289-96
-Giganti F, Hayes MJ Cioni G, Salzarulo P Yawning frequency and distribution in preterm and near term infants assessed throughout 24-h recordings Infant Behav & Development 2007;30(4):641-647
-Guggisberg AG, Mathis J, Herrmann US, Hess CW.The functional relationship between yawning and vigilance. Behav Brain Res 2007;179(1):159-166
-Zilli I, Giganti F, Salzarulo P. Yawning in morning and evening types. Physiol Behav 2007;91(2-3):218-222
-Zilli I, Giganti F, Uga V. Yawning and subjective sleepiness in the ederly. J Sleep Res 2008;17;3003-308
 Gianluca Ficca & Piero Salzarulo "Lo Sbadiglio Dello Struzzo" , Bollati Boringhieri, Torino, 2002
fetal yawn