This study was conducted to examine the
behaviour and facial expressions of the fetus
after birth by 4-dimensional (4-D)
ultrasonography, and the association of the
biophysical profile (BPP) with the Doppler
scale. A total of 40 singleton pregnancies were
included. All 4-D ultrasonographies were
performed using the Accuvix XQ (Medison® Co.
Ltd, Seoul, Republic of Korea). The BPP and
Doppler were performed on gravidas using 2-D
ultrasonography. We recorded the newborn while
awake no later than 48 h after delivery. The
most frequent movement in fetuses and newborn
was yawning and isolated arm movements,
respectively. Sucking, swallowing (r= 0.78) and
isolated limb movements (r= 0.72) in fetuses as
observed by 4-D ultrasonography had a
relationship with isolated limb movements in the
newborn. Because of the limitation of
ultrasonography, an overall comparison could not
be made. There was a high correlation between
sucking, swallowing, and isolated limb movements
in fetuses and newborn.
Introduction
In pregnant women, the methods of assessing
fetal wellbeing include the biophysical profile
(BPP) and the measurement of arterial blood flow
volume in the uterus or umbilical cord; however,
the methods are limited (Kurjak et al. 2005a; Wu
et al. 2007). Facial expressions and movements
of the ferns are known to be an indirect
expression of the maturity of cerebral function
during the fetal period.
It has been reported that facial expression
during the fetal period corresponds to facial
expression during the neonatal period (Kurjak et
al. 2007a). If brain function after birth could
be predicted by antepartum 4D ultrasonography,
early management after birth may be
optimised.
Materials and methods
Between October 2007 and December 2008, 40
gravidas with singletons between 28 and 32
weeks' gestation underwent prenatal examinations
at a university hospital. After obtaining
approval from the Institutional Review Board
(IRB), the weight and size of the ferns were
measured by 3-5 MHz ultrasonography. By
measuring the Doppler waveforms of the umbilical
cord, uterine artery and middle cerebral artery
(MCA), abnormalities of the fetal intrauterine
environment were assessed. The fetal
facial expressions and movements were
assessed every 3 weeks by 4-D ultrasonography
(Accuvix XQ, Medison® Co. Ltd, Seoul,
Republic of Korea) for 30 min. A BPP was
performed twice. The exclusion criteria included
cigarette smoking during pregnancy, a history of
drug abuse, twin pregnancies, fetal deformities,
genetic diseases, intrauterine growth
retardation and fetal hydrops. Gestational age
was determined based on the first day of the
last menstrual period (LMP) or by
ultrasonographic dating of the early pregnancy.
Initially, the study was conducted on 45
gravidas. Five gravidas were high risk (diabetes
mellitus, hypertension, or oligohydramnios).
Among the high-risk gravidas, three gravidas
could not be assessed because of premature
rupture of membranes (PROM) and the resulting
oligohydramnios, and two gravidas underwent
early delivery due to pregnancy-induced
hypertension (PIH). The five newborn could not
be examined for neonatal movements due to
intubation, hence they were excluded from the
study.
The mean age of the gravidas was 31.7 ±
4.7 years and the parity was 0.2 ± 0.6. The
gestational age at delivery was an average of
38.0 ± 1.7 weeks. At the time of birth, the
Apgar scores were recorded and the weights and
head circumferences were measured. Physical
abnormalities, and the Moro, plantar, grasping,
sucking, and tonic neck reflexes were
assessed.
A video recording was performed for 30 min
using a video camera (Sony®, Sony Co. Ltd,
Tokyo, Japan) in the newborn nursery no later
than 48 h after birth. The video was compared
with the ultrasonographic images and analysed.
For the fetal facial expressions and movements,
the Kurjak classification (Table I) was used, as
defined in Figure 1 (Kuijak et al. 2003).
The neonates were separated from other
neonates, clothed, and while lying in the supine
position, the video recording was performed
while awake and moving the limbs freely. The
temperature of the newborn nursery was
25°C. Crying, nursing, hiccoughing, or
administering drugs to the newborn were excluded
from video recording. The video recording was
focused on the head area of the newborn, and the
video recording technicians were instructed not
to disturb the actions of the newborn. To
determine the association between the movements
of the fetuses with the newborn, SPSS 12.0K was
used, and a correlation and correlation
coefficient were determined with Spearman's rank
order correlation, and p values were
determined.
Table I. Classification of facial expression
and movement patterns - 12 different
activities.
1. Mouthing movement: consisted of a series
of rhythmic movements involving the mandible and
tongue, characterised by constant frequency and
duration until disappearance
2. Yawning: slow and prolonged wide
opening of the jaws followed by quick closure
with simultaneous retroflexion of the head and
sometimes elevation of the arms of exoration.
The duration is about ˆ3 s
3. Tongue expulsion: facial activity
characterised by mouth opening with protruding
of fetal tongue
4. Smiling: the expression consists of the
bilateral elevation of the mouth angle
5. Scowling and grimacing: the expression
consists of bilateral contraction of eyebrows
and mimic musculature between them
6. Sucking and swallowing: rhythmical bursts
of regular jaw opening and closing at a rate of
about 1/s may be followed by swallowing,
indicating that the fetus is drinking amniotic
fluid. Swallowing consists of displacements of
the tongue and/or larynx
7. General movements: this category is
applicable if the whole body is moved but no
distinctive patterning or sequencing of the body
parts can be recognised. The complex movements
of the limb, trunk and head are clearly visible
and cause a shift in fetal position
8. Startle: a startle is a quick generalised
movement, always initiated in the limbs and
sometimes spreading to the neck and trunk
9. Stretch: a stretch is a complex motor
pattern, which is always carried out at a slow
speed and consists of the following components:
forceful extension of the back, retroflexion of
head, and external rotation and elevation of the
arms 10. Isolated limb movement: these may be
rapid or slow movement, and may involve
extension, flexion, external and internal
rotation, or abduction and adduction of an
extremity, without movements in other body pans
11. Isolated retroflexion of the head:
retroflexions of the head are usually carried
out slowly, but they can also be fast and jerky.
The displacement of the head can be small or
large. The latter may cause over-extension of
the spine of the fetus 12. Isolated anteflexion
of the head: anteflexion of the head is carried
out only at a slow velocity. The displacement of
the head is small. The duration is about 1
s.
Discussion
This study was conducted to provide a
standard screening method to predict the
development of the nervous system of newborn by
measuring facial expressions and behaviour
changes using 4-D ultrasonography, BPP and
Doppler. If we can predict that newborn infants
progress to cerebral palsy by 4-D
ultrasonography, it may be associated with fetal
sucking, swallowing, and isolated limb
movements. Using 4-D ultrasonography, fetal
movement was measured quantitatively from 14
weeks' gestation. Indeed, 4-D ultrasonography
has been used as a method to observe limb
movement before fetal movements are perceived
(Kuno et al. 2001b; Timor-Tritsch and Platt
2002; Kuijak et al. 2005; Tonni et al. 2005; Yan
et al. 2006). Using 4-D ultrasonography, the
fetal limbs in gravidas with diabetes mellitus
could be observed at about 8 weeks' gestation.
Fetal movements in gravidas with diabetes
mellitus develop slower than in healthy
gravidas. By 4-D ultrasonography, the assessment
of fetal movement in the first or second
trimester is an important method to assess
wellbeing (Kuijak et al. 2002, 2006).
The complex developmental process of the CNS
and the dynamics of the development of the
sensory system are not well understood
(Sepulveda and Mangiamarchi 1995; Hadders-Algra
1997; Zuk et al. 2008). Recently, it has been
reported that fetal facial expression
corresponds to behaviour and sensory system of
the newborn, as observed by 4-D ultrasonography
(Kuijak et al. 2004; Hata et al. 2005). The
differences in the movement of fetuses can be
assessed. It has been reported that the general
movements (swallowing, stretching, and
yawning) are associated with the number
of axodendritic and axosomatic synapses
(Sepulveda and Mangiamarchi 1995; Hata et al.
1998; Andonotopo and Kuijak 2006; Luchinger et
al. 2008).
Between 28 and 32 weeks' gestation, the
entire image of fetus cannot be seen on a
monitor; only a portion of the trunk or the
limbs can be observed. Thus, the movement of the
entire body is difficult to observe by 4-D
ultrasonography. To understand fetal movements,
the period before the third trimester is
desirable. Therefore, we recommend evaluating
the function of the fetal CNS by observing
facial expression rather than the movement of
the entire body during the third trimester of
pregnancy. In previous studies, tongue expulsion
was difficult to observe (Yigiter and Kayak
2006); however, in the current study, tongue
expulsion was observed. It is speculated that
fetal tongue expulsion can be used as an index
to observe changes in fetal facial
expression.
The ultimate purpose of evaluating the
development of the CNS by 4-D ultrasonography is
to determine whether 4-D ultrasonography could
serve as a prenatal diagnostic method to detect
cerebral palsy prior to birth. In addition, 4-D
ultrasonography may become a method to assess
fetal wellbeing (Kuijak et al. 2007b; Kuijak et
al. 2008a). New fetal nervous behaviours were
observed in the fetuses of healthy and high-risk
gravidas by examining two cranial closure areas
by 3-D ultrasonography, and by scoring facial
expression and fetal movement (Kuijak et al.
2008b). A postnatal follow-up study was
performed, and it became the basic research that
facilitates detection of anomalies involving the
nerves and CNS; however, in cerebral palsy, it
is not easy to clearly detect abnormal
development of the CNS (Salihagic-Kadic et al.
2005).
In the current study, because of the
limitation of 4-D ultrasonography, an overall
comparison was impossible. The ferns was
analysed based on the images of fetal movement
recorded on ultrasonography (sucking,
swallowing, and isolated limb movements), which
were highly correlated with newborn
measurements.
The current study was limited by the small
study population and consisted of healthy
gravidas without obstetric or medical problems.
It was not easy to perform ultrasonography for
30 min. Due to PROM and pre-term birth after
performing 4-D ultrasonography, five pregnant
women were excluded in our study. We were not
able to include high-risk pregnant women with
deterioration of labour pain when we performed
4-D ultrasonography for 30 min. We should
consider the necessary time to perform 4-D
ultrasonography on high-risk pregnant women
because >30 min may aggravate pre-term labour
in our study.
We suggest that obstetricians should perform
4-D ultrasonography on pregnant women with
normal BPP and Doppler between 28 and 32
gestational weeks. Four-D ultrasonography may
predict nervous system development in the fetus
by confirming sucking, swallowing and isolated
limb movements.
Our study is the first report from the
Republic of Korea in which fetal behaviour was
assessed by BPP, Doppler, and 4-D
ultrasonography, and compared with the
newborn.
