The
Application of Color Doppler Technology to the
Study of Fetal
Swallowing
B Petrikovsky, GP Kaplan, H
Pestrak
Maternal-Fetal
Medicine, Department of Obstetrics and
Gynecology, North Shore University Hospital
Cornell University Medical College, Manhasset,
New York
Swallowing activity develops earlier than
sucking in the course of fetal development. The
human fetus demonstrates swallowing movements as
early as 11 weeks gestation, whereas more
complex sucking movements can be identified at
18-20 weeks. Swallowing has been studied
electrophysiologically in fetal sheep, which
have been documented to swallow 20-200 mL of
amniotic fluid (AF) in two to seven separate
swallowing episodes over a 24-hour period of
observation. Recently, Sherman et al evaluated
swallowing in singleton gestations in
chronically instrumented ewes, both
electromyographically and by assessing
esophageal fluid flow. Fetuses swallowed an
average of 35+-9 ml/hour during the 12-hour
study. Total daily volume of swallowed fluid was
840+- 224 ml.
Neurologic control of fetal swallowing
included coordinated contractions of the
thyroid, nuchal, and thoracic segments of the
esophagus, which averaged 43+-3 contractions per
hour. Recent advances in ultrasonography have
allowed adequate imaging of fetal structures
involved in the mechanisrn of swallowing, namely
the fetal mouth, tongue, pharynx, larynx,
trachea, and esophagus. We present our
observations of fetal swallowing obtained by
superimposing color-flow Doppler signals on the
regular gray-scale sonographic image. Thorough
knowledge of the physiology of fetal swallowing
may allow us to achieve a better understanding
of abnormal swallowing in neurologically
impaired fetuses.
Materials and Methods : A sagittal
view through the fetal face and a profile were
imaged in ten fetuses at 36-41 weeks gestation.
All mothers were referred for fetal assessment,
including a biophysical profile, for the
following indications: decreased fetal movement
in three, previous stillborn in two, suspected
postmaturity in five. Studies were performed in
the postprandial state at 9 Am and 12 noon in a
quiet room with the woman in the lateral
recumbent position. All ultrasound examinations
were performed using a 3.5-MHz Acuson 128 PX
curvilinear probe. All observations were made in
the absence of fetal breathing.
Fetal lips, mouth, tongue, pharynx, larynx,
trachea, and esophagus were surveyed in serial
coronal planes. Color-flow Doppler signals were
superimposed on each gray-scale image to assess
the direction and location of AF flow with
respect to anatomic structures of the fetal
upper gastrointestinal and respiratory tracts
during the act of swallowing. All fetal
movements were analyzed by a review of the
videotape in slow motion. All neonates were born
at term in satisfactory condition. One- and
5-minute Apgar scores were greater than 7 and 9,
respectively, in all cases.
Results : Two to six sucking
movements preceded every swallow in eight of the
ten fetuses. The remaining two fetuses exhibited
one sucking movement before each swallow. The
swallowing process itself was initiated by
opening of the fetal mouth and the introduction
of AF into the oral cavity. At this stage of
swallowing, no active tongue movements were
detected. At each such mouth opening, the fetus
continued to fill the oral cavity. Minimal
spillage of AF back into the amnion was seen.
The soft palate superiorly and the tongue
posteriorly and inferiorly obstructed the
further flow of AF at this stage of
swallowing.
Low-frequency tongue movements in the caudal
direction were associated with further movement
of AF toward the pharynx. Elevation of the soft
palate and its opposition to the posterior wall
of the pharynx were incomplete, as evidenced by
a tiny stream of AF directed superiorly to the
nasopharynx. A small stream of AF was directed
into the trachea as well. Upward movement of the
larynx and epiglottic movement were seen next,
in association with narrowing of the lumen of
the pharynx. These dynamic changes were
accompanied by downward flow of AF into the
esophagus.
Discussion : Previously, we studied
the effect of fetal swallowing on the AF index
in response to acoustic stimulation and found
that AF decreases after extensive fetal
swallowing. However, the mechanism of normal
fetal swallowing has remained obscure. We report
here the use of color Doppler technology to
describe the swallowing cycle in a term human
fetus. The cornbination of color flow and
spectral Doppler analyses was used by Chiba et
al ,Isaacson and Birnholz, and Badalian et al to
study fetal breathing. They demonstrated a
positive correlation between breathing-related
nasal peak flow velocity and advancing fetal
maturity. Isaacson and Birnholz were able to
visualize the oropharynx and observed its
rhythmic expansions 200 msec before the onset of
inspiration and 100 msec before glottic opening.
They also described upward displacement of the
larynx and speculated that it was related to
fetal swallowing. Fox et al modified the
technique of Isaacson and Birnholz by scanning
in sagittal and transverse planes of the fetal
nose, assessing the perinasal flow using color
Doppler technique in fetuses with diaphragmatic
hernia. Bowie and Clair observed fetal
swallowing and regurgitation in normal fetuses
and in those with polyhydramnios. They reported
distinct pharyngeal and tongue movements related
to swallowing activity. However, the use of
grayscale imaging alone did not allow the
investigators to follow the movements of an AF
bolus at different stages of fetal
swallowing.
Using a color Doppler technique, we were
able to observe a flow of AF through the fetal
mouth, oropharynx, pharynx, and esophagus. We
were particularly careful to videotape fetal
swallowing when there were no fetal breathing
movements, in order to avoid potential
confusion. The swallowing pattern in a normal
fetus near term differs from that in the infant
and adult. The three phases of swallowing (oral,
pharyngeal, and esophageal) are the same, but
the oral and pharyngeal phases appear to be less
completely developed. In a mature fetus, two to
six sucking movements usually precede the
initiation of the oral stage of swallowing,
whereas in an adult, during the oral phase the
tongue opposes the hard palate to propel a
liquid or solid bolus into the oropharynx. The
base of the tongue moves upward to the posterior
pharyngeal wall to seal off the nasopharynx
effectively. In the fetus, tongue opposition to
the hard palate is not evident, although AF is
propelled by the tongue into the oropharynx. In
addition, the oropharynx is not sealed
completely, allowing some of the AF to escape
into the nasopharynx. The normal pharyngeal
stage of swallowing in an adult includes glottal
closure to prevent aspiration, and opening of
the esophageal sphincter. In the mature fetus,
the trachea is not sealed completely by glottal
closure and swallowed AF is directed not only
into the esophagus, but into the trachea as
well.
A detailed study of the normal development
of swallowing over the course of fetal life may
lead to the early identification of potential
neonatal swallowing difficulties and may shed
further light on the mechanisms of
polyhydramnios and oligohydramnios
