Piontelli
A. Fetal Yawning in Development of
Normal Fetal Movements. The first 25 weeks of
gestation. Spinger. 2010.
135p.
Abstract
To evaluate the frequencies of fetal facial
expressions in the third trimester of pregnancy,
when fetal brain maturation and development are
progressing in normal healthy fetuses.
Four-dimensional (4_D) ultrasound was used
to examine the facial expressions of 111 healthy
fetuses between 30 and 40_weeks of gestation.
The frequencies of seven facial expressions
(mouthing, yawning, smiling, tongue expulsion,
scowling, sucking, and blinking) during
15-minute recordings were assessed. The fetuses
were further divided into three gestational age
groups (25 fetuses at 30-31_weeks, 43 at
32-35_weeks, and 43 at ³36_weeks). Comparison of
facial expressions among the three gestational
age groups was performed to determine their
changes with advancing gestation.
Mouthing was the most frequent facial
expression at 30-40_weeks of gestation, followed
by blinking. Both facial expressions were
significantly more frequent than the other
expressions (p_<_.05). The frequency of
yawning decreased with the gestational age after
30_weeks of gestation (p_=_.031). Other facial
expressions did not change between 30 and
40_weeks. The frequency of yawning at
30-31_weeks was significantly higher than that
at 36-40_weeks (p_<_.05). There were no
significant differences in the other facial
expressions among the three gestational age
groups.
Our results suggest that 4D ultrasound
assessment of fetal facial expressions may be a
useful modality for evaluating fetal brain
maturation and development. The decreasing
frequency of fetal yawning after 30_weeks of
gestation may explain the emergence of distinct
states of arousal.
Introduction
Fetal brain development starts as early as
in the 7th week of gestation [1]. A
series of brain developmental changes takes
place throughout pregnancy [2]. In the
first and second trimesters, anatomical changes
are the hallmark [3,4], and therefore
can be directly assessed by two-dimensional (2
D) sonography [5].
On the other hand, functional brain
developmental changes predominate over
anatomical changes in the third trimester of
pregnancy [6]. Functional connections
between the cerebral cortex and peripheral
nervous system appear at 28 weeks of gestation,
as indicated by evoked potentials [7].
The upper motor control system (cerebral
hemispheres and basal ganglia) becomes mature at
34 weeks of pregnancy [8]. Development
of the six-layered lamination of the neocortex
takes place after 32 weeks, as a result of
neural differentiation and the laminar
distribution of thalamocortical axons
[9]. The third trimester is also
characterized by brain stem maturation with a
distinguished sleep&endash;wakefulness pattern
due to pontine maturation [10].
Facial expressions are not separate from
central nervous system (CNS) developmental
changes. They start to be observed at
10&endash;11 weeks of gestation [3].
Changes in their frequencies occur through
gestation [11]. Eye movement patterns
become more complex in the third trimester, due
to mid-brain maturation. At 36&endash;38 weeks,
eye movements become linked with the fetal heart
rate [12,13].
These changes in the frequencies of facial
expression, and their link with other body
functions represent a crucial part of a set of
behavioral states [14]. Previous
neurodevelopmental study concluded that these
behavioral states develop due to the functional
development of the fetal CNS [15].
Moreover, it is well documented that fetal
behavior represented by fetal movements and
facial expressions reflect well-being of the
fetal brain and CNS [16&endash;19].
Therefore, the evaluation of facial expressions,
especially in the third trimester of pregnancy,
might represent a direct method to assess
developmental changes of the fetal brain and
CNS. The change in frequencies of these
expressions at that stage might reflect maturity
of brain areas controlling these facial
expressions.
There have been numerous studies on
fourdimensional (4D) ultrasound assessment of
fetal facial expressions [20&endash;29].
However, the number of subjects studied in the
third trimester of pregnancy, especially after
36 weeks of gestation, was very small. Because
of the small amounts of amniotic fluid relative
to the fetal size, and the difficulty in
obtaining an ideal sagittal view of the fetal
face depending on the fetal position, there are
limitations regarding 4D ultrasound studies of
fetal facial expressions.
This study focuses on 4D ultrasound
evaluation of fetal facial expressions in the
third trimester as an indicator of brain
development at this critical stage, which is
believed to represent maturational stage of the
fetal brain and CNS functions [30].
Yawning was the only facial expression to
demonstrate a significant decrease in frequency
with advancing gestation (p<.05) (Figure 2),
although the correlation coefficient for yawning
and increasing gestational age was low (r_.184).
The other six facial expressions did not show a
significant change in frequency with gestational
age.
Discussion
In our previous studies on 4D ultrasound
evaluations of fetal facial expressions at
20&endash;34 weeks of gestation, mouthing was
the sole most frequent facial expression
[26,33,34]. Kurjak et al. [23]
reported that blinking and mouthing movements
are dominant between 30 and 33 weeks of
gestation. However, there has been no 4D
ultrasound study on the patterns of the
frequency of fetal facial expressions late in
the third trimester. In this study, mouthing and
blinking were the most frequent facial
expressions at 30&endash;31, 32&endash;35,
36&endash;40, and 30&endash;40 weeks of
gestation, respectively. After 30 weeks of
gestation, there is an increase in long-duration
fetal movements, referred to as epochs and
episodes, and the neurobehavioral regulation of
fetal movements is crucial during this period
[35]. Horimoto et al. [30] found
that the concurrence of regular mouthing with
the non-rapid eye movement period after 35 to 36
weeks' gestation suggests the maturation of
fetal brain functioning seen in the newborn.
Brain functions also regulate the rate of
spontaneous eye blinking [36,37], and an
increase in the spontaneous eye blinking rate is
thought to be related to central dopamine system
maturation [38&endash;41]. These results
suggest that the concurrence of mouthing
movement and eye blinking may be related to the
maturation of fetal brain development after 30
weeks of gestation.
It was reported that there is no change in
the frequency of fetal yawning assessed by 2D
sonography between 20 and 36 weeks of gestation
[42]. In this study using 4D ultrasound,
yawning showed a decreased frequency with
advancing gestation in the third trimester of
pregnancy, coinciding with the results obtained
with 4D ultrasound by Reissland et al.
[43], as well as Kurjak et al.
[23]. Yawning is concerned with the
arousal process of the brain [44]. With
advancing gestation, the rhythmic control of
sleep and wake times becomes more established.
This results in frequent waking episodes and
less of a need for yawning as a stimulus for
brain arousal. "Yawning indicates a harmonious
progress in the development of both the
brainstem and the peripheral neuromuscular
function, testifying to the induction of an
ultradian rhythm of vigilance" [45].
Giganti et al. [44] also demonstrated a
decreased frequency of yawning in preterm and
near-term infants with the advancement of age.
Therefore, the period of 30 weeks of gestation
might represent the emergence of distinct states
of fetal brain arousal, as indicated by the
significant decrease in the frequency of
yawning. However, the low correlation
coefficient for yawning and increasing
gestational age as well as the overlapping
ranges of numbers of yawning episodes among the
three gestational age groups might indicate that
the emergence of distinct states of fetal brain
arousal after 30 weeks is very slowly
progressing.
Reissland et al. [46] speculated
that the increased frequency of fetal scowling
with advancing gestation might be an adaptive
process, which is beneficial after birth. Fetal
scowling may represent the fetal response to
pain [46,47]. In this study, its
frequency did not change after 30 weeks of
gestation. The somatosensory evoked potentials
(translating pain processing in the
somatosensory cortex) develop at 29 weeks
[48], and this might indicate the
constant frequency of scowling in the third
trimester of pregnancy.
Sato et al. [33] showed that the
frequency of fetal smiling increased with
advancing gestation between 20 and 34 weeks of
gestation. In this study, the frequency of
smiling did not change after 30 weeks of
gestation. Fetal smiling may facilitate the
development of facial muscles in utero, and may
enhance a positive parental attitude
[49]. The development of smiling in
utero may represent an adaptive process to
postnatal life. In this study, the frequency of
fetal suckling remained unchanged between 30 and
40 weeks of gestation. Previous 4D ultrasound
studies reported its constant frequency between
20 and 34 weeks [33], and the results
reported by Yigiter and Kavak [25], and
Reissland et al. [50] also confirmed the
stable frequency of fetal lip puckering in the
second half of pregnancy [39].
Intrauterine sucking lacks the real postnatal
stimulus (breast or bottle). However, its stable
frequency with gestation indicates its
importance as an essential training step in
preparation for postnatal feeding.
The frequency of tongue expulsion was found
to be constant between 30 and 40 weeks of
gestation in this study. Kurjak et al.
[23] also found that its frequency is
constant after 28 weeks of gestation. This
constant frequency may represent a maintenance
state of tongue training as an essential
preparatory step for its use in lactation, as
well as speech functions in postnatal life.
Limitations of this study may be the small
sample size and the lack of two investigators
assessing the movements independently and
blindly to gestational age. Therefore, intra-
and inter-observer reproducibility for 4D
ultrasound assessment of fetal facial
expressions should be investigated in further
research. In this investigation, most of the
examinations were performed in the morning with
few cases in the afternoon. This cannot allow
analysis of the difference in fetal activity
based on time/timing of the examinations. Future
studies involving a larger sample size are
needed to investigate the reproducibility of 4D
ultrasound assessment of fetal facial
expressions and the difference in fetal activity
at the time/timing of the examination.
In conclusion, this study provided the
normal parameters of fetal facial expressions in
the third trimester of pregnancy, and suggests
the possible link between facial expressions and
brain development at this stage, when the fetal
brain reaches advanced stage of maturity.
Therefore, the full realization of fetal facial
expressions and fetal behavior in different
stages of gestation might enable us to better
understand the functional development of the
fetal brain and CNS. The developmental changes
of facial expressions can selectively indicate
the maturation and development of different
parts of the fetal brain and CNS.
