The authors have declared that no competing interests exist.
Conceived and designed the experiments: NR. Performed the experiments: NR. Analyzed the data: BF NR. Wrote the paper: NR BF JM.
Although some research suggests that fetuses yawn, others disagree arguing that is it simple mouth opening. Furthermore there is no developmental account of fetal yawning compared with simple mouth opening. The aim of the present study was to establish in a repeated measures design the development of fetal yawning compared with simple mouth opening.
Video recordings were made of the fetal face and upper torso visualized by means of 4D full frontal or facial profile ultrasound recordings. Fifteen healthy fetuses were scanned four times at 24, 28, 32 and 36 weeks gestation. Yawning was distinguished from non-yawning in terms of the length of time it took to reach the apex of the mouth stretch, with yawns being defined as more than 50% of the total time observed. To assess changes in frequency, a Poisson mixed effects model was fitted to the count of number of yawn and simple mouth opening events with age and gender as fixed effects, and person as a random effect. For both yawns and simple mouth openings a smooth varying age effect was significant. The number of yawns observed declined with age from 28 weeks gestation, whereas simple mouth openings were less frequent and the decline was observed from 24 weeks. Gender was not significant either for yawn and simple mouth openings.
Yawning can be reliably distinguished from other forms of mouth opening with the potential of using yawning as an index of fetal healthy development.
The development of yawning, a movement which has been reported in humans and many vertebrates from fetal stages to old age (e.g.
Research suggests that there is a U-shaped developmental progression to yawning in that premature infants yawn more frequently than term babies
In summary, yawning has been reported from the end of the first trimester,
One reason for varied findings could be due to a lack of a precise definition of yawns compared with mouth opening. McMagnus, Devine, & Brandsetter
Provine (
The present longitudinal study examined the dynamics of yawning compared with non-yawn mouth opening in 15 healthy fetuses, 8 girls and 7 boys, observed four times over the second and third trimester of pregnancy. We expected that if yawning is a developmental process, then the frequency of yawning might change during gestation. Given previous research on human yawning we also did not expect to identify sex differences.
The Figure demonstrates that yawning and non-yawn mouth opening cannot be distinguished from a static image at the apex of the event.
Ethical permission was granted by the County Durham and Tees Valley 2 Research Ethics Committee (REC Ref: 08/H0908/31), James Cook University Hospital. All mothers gave informed written consent.
Fifteen healthy fetuses were scanned: 8 girls and 7 boys. The fetuses were observed four times based on their gestational age which was established at 12 weeks through measures of crown rump length and/or at the 20 week anomaly scan based on head circumference. The first scan was at a mean 24.2 weeks gestational age (range 23.5–25.0 weeks); the second at 28.0 weeks gestational age (range 27.4–28.5 weeks); the third at 32.1 gestational age (range 31.0–33.1 weeks); the fourth at 36.2 weeks gestational age (range 35.5–36.5 weeks). All participants were first time mothers with mean age 27 years (range 19–40 years), specifically recruited through the midwives of the antenatal unit of the James Cook University Hospital, Middlesbrough, UK and following ethical procedures. All fetuses were healthy, of Caucasian parents, with mean birth weight 3283 grams (ranging in weight from 2380 grams to 4160 grams). Gestational age at birth was 40 weeks (range 37–42); head circumference at birth was 34.5 cm (range 32.0 to 36.5 cm). Apgar scores resulted in a mean 9.06 at 1 minute (range 9–10) and mean 9.33 at 5 minutes (range 9–10). All new-borns were rated to be healthy by a paediatrician. One fetus born at 37 weeks and 1 day was in terms of weight at around the 10th percentile and hence seemed to be at the lower limit of the normal/small range for gestational age classification
Left panel: Mean observed number of yawn (red solid square) and non-yawn (blue unfilled triangle) mouth openings for each gestational age over 600 seconds of observation. Right panel: Fitted 600-second counts from Poisson mixed effects model for an average fetus for yawning (red solid line) and non-yawn (blue dashed line) mouth openings.
Following ethical guidelines, after mothers had completed normal 20 week anomaly scans, they were approached by the radiographer, for consent to participate in the study. Mothers who agreed received four additional scans in which fetuses were observed while active for approximately 20 minutes. During consent and again before each scan mothers were made aware that these additional scans were for research purposes and not routine medical scans and that they could withdraw from the study at any time. At the end of each scan mothers were provided with a DVD copy of their scans. The fetal face and upper torso were visualized by means of 4D full frontal or facial profile ultrasound recordings, and recorded for off line analysis with a GE Voluson 730 Expert Ultrasound System using a GE RAB4–8L Macro 4-D Convex Array Transducer. For each observation period, we coded 600 seconds of each scan (which were not necessarily consecutive) when the full face was visible; starting with the first moment when the full face could be coded. No external stimulation was applied in these observation periods. The first scan of one fetus and the last scan of a second fetus could not be coded because the complete cycle of mouth movements could not be observed during the scan. Hence the findings reflect 58 rather than 60 scans.
We distinguished between yawning and non-yawn mouth opening, based only on duration of the mouth opening. We examined all events where a mouth stretch occurred. Mouth stretch was defined by the mandible being pulled down, changing the shape of the mouth opening from oval with the long axis in the horizontal plane to one in the vertical direction, and using the objective coding system which we tested previously
Using Cohen’s Kappa, reliability was established for these scans, which were coded independently by a new coder trained in the coding system. This resulted in reliability estimates for overall reliability for all AUs coded (overall mean = .91, overall mean range.79–1.00).
We used a Poisson mixed effects analysis
Over the 58 scans, 56 yawns and 27 non-yawn mouth openings were observed in total. The rate per hour for yawns was 6.02 (s.d.9.56); whereas that for non-yawn mouth openings was 2.79 (s.d. 5.64). A Wilcoxon signed–rank test showed significant differences in these two rates (Z = 3.008; two- sided p = 0.003 on 58 df).
Given that yawning is distinguished from non-yawn mouth openings by the opening part of the movement cycle being longer compared to the closing part of the cycle, we examined the ratio of opening duration to closing duration in our sample for the 56 yawns observed. 93% of the yawns had a ratio of over 1.5 (60∶40 split), and 77% of yawns had a ratio of over 2.33 (70∶30 split).
An exploratory analysis of the 15 fetuses showed a strong decline in the mean frequency of both yawns and non-yawn mouth openings as gestational age increased. Means (with standard deviations in parentheses) for yawns at 24, 28,32 and 36 weeks were respectively 1.93 (2.17); 1.40 (2.03); 0.73 (0.96) and 0.0(0.0); means and standard deviations for the same ages for non-yawn mouth openings were lower at 1.00(1.47); 0.53(0.83); 0.33(0.72) and 0.0 (0.0) The fetus born at 37 weeks had no yawns or non-yawn mouth openings; but two other fetuses in our sample born at 40 and 41 weeks also exhibited the same behaviour. The observational data for the fetus born at 37 weeks is therefore consistent with the rest of the sample and has been retained in the statistical analysis.
To assess the changing frequency of yawns over age and gender, a Poisson mixed effects model was fitted to the count of number of yawn events with age and gender as fixed effects, and person as a random effect, to account for the repeated measures design (
Gender was not significant, (chi-squared = 0.109 on 1 df; p = 0.74) but linear age was significant (chi-squared = 33.42 on 1 df; p<0.001), with the counts declining with age.
A non-linear age effect was fitted using a natural cubic spline with two degrees of freedom, and the non-linear model showed a significant improvement over the linear model (chi-squared = 7.01 on 1 df; p<0.01).
The same model was fitted to the number of non-yawn mouth opening events (
Gender was again not significant, (chi-squared = 0.584 on 1 df; p = 0.44) but linear age was significant (chi-squared = 17.18 on 1 df; p<0.001), with the counts again declining with age.
A non-linear age effect was fitted using a natural cubic spline with two degrees of freedom, but in this case there was no significant improvement over the linear model (chi-squared = 1.13 on 1 df; p = 0.29).
A combined generalised linear mixed model was fitted which allowed a comparison of the declining trajectories for yawn and non- yawn frequency rates over age. Three models were fitted, a model (Model 1) with non-linear age only, a model (Model 2) with non-linear age and an indicator variable representing the type of mouth opening (yawning = 1, non-yawning = 0), and a model fitting different intercepts and non-linear age functions to each type of mouth opening (Model 3). Model 2 showed a significant improvement over Model 1 (Chi-squared = 12.20 on 1 df, p<0.001) but Model 3 showed no significant improvement over Model 2. (Chi-squared = 0.43 on 2 df, p = 0.805). The estimate of the indicator variable effect in model 2 was 0.782 and the exponential of this number exp(0.782 = 2.19) can be interpreted as a multiplicative effect for yawning rate over the non-yawn effect, with both having the same trajectory shape over age, and with yawning rate just over double the non-yawning rate.
There are a number of hypotheses explaining the ubiquitous behaviour of yawning
Hence, this research could support the suggestions that yawning is related to CNS maturation e.g.
In summary, the importance and function of yawning is still unclear. Some researchers found an association of yawning with neurological functioning e.g.
We thank the mothers who took part in the study, Kendra Exley who performed the 4-D scans, Dr. Karen Lincoln for her support, as well as the independent coders of fetal facial movements.