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La parakinésie brachiale oscitante
Yawning: its cycle, its role
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Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
 
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
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mystery of yawning 

mise à jour du
30 septembre 2004
J Perinat Med
2005;33:46-53
lexique
The potential of four-dimensional (4D) ultrasonography in the assessment of fetal awareness
A Kurjak, M Stanojevic et al
Medical school University Zagreb, Croatia
 
Fetal yawning : a behavior's birth with 4D US revealed

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Abstract
The aim of the study was to observe different expressions and movements of a fetal face during investigation of fetal behavior in the second and the third trimester of normal pregnancies, as a probable manifestation of fetal awareness.
 
Over a 6-month period a study was conducted in three centers in Zagreb, Croatia and in Barcelona and Malaga, Spain. Women with singleton pregnancies (16-33 weeks) who were referred for ultrasound check-up for determination of gestational age, suspicious fetal malformations, polyhydramnios, and/or the assessment of biophysical profile or other possible pathology, were assigned to the study. After regular twodimensional (2D) ultrasound assessment at an antenatal clinic, pregnant women were offered the possibility of undergoing 4D ultrasound examination if the fetus and the mother were considered "normal", i.e., if ultrasound and clinical assessment were uneventful. If the newborn delivered at term had 1- and 5-min Apgar scores of 7 and 10, respectively, and if the newborn was considered "term and normal" (normal spontaneous activity, normal posture and tone, and presence of some primitive reflexes) at the first and subsequent regular check-ups, the inclusion criteria were deemed to have been met. Out of 119 patients, 99 fulfilled the inclusion criteria, 40 of whom were in the second, and 59 in the third trimester of pregnancy. A Voluson 730 Expert system with a transabdominaI 5-MHz transducer was used for 4D ultrasonography. After regular 2D scanning, the 4D mode was switched on, and a live 3D image was reconstructed by selecting ideal 2D mid-sagittal images of the face (the region of interest). The volume was automatically scanned every 2 s while the surface-rendered mode was switched on, and 4D images were displayed on the screen and recorded on videotape during a 30-min observation period. Movements of the following fetal face structures were analyzed: forehead, brows, nasal soft tissue and nasolabial folds, upper lip, oral cavity and tongue, lower lip and chin, eyelids and eyes, mouth and mouth angles, and facial expression. 4D ultrasonography allowed in utero observations of fetal facial expressions such as smiling, yawning, and swallowing.
 
The quality of 4D depiction of fetal facial expressions increased with gestational age. The frequency of fetal facial expressions such as yawning ranged from 1 and 6 with a median of 1.5 per 30-min observation period; smiling ranged from 2 and 8 with the median of 2; tongue expulsion ranged from 2 to 6, median 3; mouth and eye squeezing ranged from 5 to 10, median 6; scowling ranged from 1 to 3, median 0.5; and isolated eye blinking ranged from 4 to 12 with a median of 5.
 
Our study shows the ability of 4D sonography to depict different facial expressions and movements, which might represent fetal awareness. Nevertheless, long, precise and thorough observation of fetal faces by 4D sonography was hampered as the images were only near real-time. Thus, we were only able to study the quality and not the quantity of facial movement patterns.
 
fetal yawnfetal-yawn
 
Introduction
 
During recent years more has become known about various components of the development of the human nervous system and how these components act in concert during fetal life. This knowledge has led to a renewed discussion over whether the developing fetus is capable of being aware of its state and surroundings and, if so, when this awareness occurs during gestation.
 
For better understanding, it is useful to consider the fundamental parts of early brain development. Four critical regions start to develop from the forebrain after the fifth gestational week: the thalamus, cerebral cortex, hypothalamus, and limbic system. The thalamus becomes the reception area for most of the sensory input to the brain, which ascends the spinal cord, and relays it to the appropriate region of the cortex via its projection fibers. Thalamocortical fibers begin to develop at 17 weeks and penetrate the cortical plate to make permanent connections at 22-34 weeks.
 
The part of the brain associated with thinking, consciousness, emotions, etc., is the cerebral cortex, which forms the largest part of the developed brain, enveloping the lower structures in two cerebral hemispheres, the first signs of which are visible at 5-6 weeks. It has been indicated that facial reflexes in response to somatic stimuli, which could indicate an emotional reaction to pain, develop rather early in gestation. Nevertheless, it is still questionable whether it is possible to presume brain function only from fetal behavior. From the developmental point of view, it is clear that many facial and encephalic structures have the same embryologic origin, and therefore the consideration that "the face predicts the brain" seems to be true. Whether the fetal face is an "organ that expresses awareness" with very complex functions is still questionable, because we need more scientific confirmation of what constitutes fetal awareness.
 
Four-dimensional (4D) ultrasound technology, introduced in recent years, is a novel tool for the observation of fetal behavior and the fetal face. Although two-dimensional (2D) ultrasonography documents the origin, occurrence and developmental course of specific fetal movements, simultaneous imaging of complex facial movements was impossible using only a 2D real-time technique. A technique was needed to enable three-dimensional (3D) imaging of fetal facial movements in real-time mode. This technique can be called "live" 3D ultrasound or 4D ultrasound, as coined by a manufacturer, because time becomes a parameter within the 3D imaging sequence. Human eyes are able to differentiate between images with a frequency of up to 12 images per second; consequently, production of an appropriate frame rate with specially designed probes and a fast computer device is required. At the moment, 4D ultrasound scanning is not real-time and the machines available can reach up to approximately 20 images per second, depending on the volume size, resolution and the mechanics of the probe. Nevertheless, even at these relatively slow frame rates the ability to study fetal activity and superficial structures is remarkably good compared to 2D ultrasonic devices. This means that 4D ultrasonography integrates the advantage of the spatial imaging of fetal structures, especially the face, with the addition of time, allowing depiction of the appearance and measurement of the duration of each movement. This new diagnostic tool allows continuous monitoring of the fetal face and other surface features of the fetus, thus opening exciting new possibilities for the study of the relatively unexplored area of fetal facial expressions as a possible manifestation of fetal awareness.
 
Is it the facial expression of the fetus that can help us understand what the fetus would like to communicate?
 
As our recent investigation showed, there is behavioral continuity from fetal to neonatal life, which probably includes facial expressions. We can see on the fetal face whether it is satisfied or unhappy, smiling or worried, self-confident or uncertain, but does the expression of the fetal face predict its normal neurological development ? To many of these questions there are few answers as yet.
 
In our systematic study of fetal behavior by 4D sonography we were able to observe different expressions and movements of the fetal face, but the question is whether they indicate fetal awareness. To the best of our knowledge, the present study is the first attempt to use 4D sonography in the evaluation of facial expressions and facial movements to demonstrate fetal awareness.
 
Subjects
 
Over a period of 6 months (November 2003-April 2004) a study was conducted in three centers: "Sveti Duh" General Hospital, Department of Obstetrics and Gynecology, Medical School University of Zagreb, Croatia (Zagreb); Department of Obstetrics and Gynecology, Institut Universitari Dexeus, Barcelona, Spain (Barcelona); and in Centro Gutenberg, Malaga, Spain (Malaga). Pregnant women of gestational age between 16 and 33 weeks and with a singleton pregnancy, who were referred for ultrasound examination to a tertiary outpatient clinic due to undetermined gestational age, suspected fetal malformations, polyhydramnios, and/or for assessment of the biophysical profile or other possible pathology, were recruited for the investigation. Fetuses before 16 and after 33 weeks of gestation were not excluded, but we had some technical problems with the visualization of their faces. The optimal and most satisfactory visualization of fetal faces was obtained in the second and third trimesters of pregnancy. After regular 2D ultrasound assessment at the antenatal clinic, the pregnant women were offered the possibility of undergoing 4D ultrasound examination. All participants provided written informed consent and approval for the investigation. The local ethical committees in all centers approved the study. Patients were offered 4D ultrasonography if both fetus and mother were considered "normal", i.e., if the initial ultrasound and clinical assessment were uneventful. If the newborn, eventually delivered at term, had normal 1- and 5-min Apgar scores, was considered "term and normal" and demonstrated, at the first and subsequent regular check-ups (at least two), normal spontaneous activity, normal posture and tone, and the presence of some primitive reflexes, then the inclusion criteria were deemed to have been met. Out of 119 patients, 99 fulfilled the inclusion criteria, 40 of whom were in the second and 59 in the third trimester of pregnancy.
 
Methods
 
4D ultrasound : All 4D examinations were carried out using a Voluson 730 Expert system (GE Medical Systems, Milwaukee, WI, USA and Solingen, Germany) using a transabdominal 5-MHz transducer. After standard assessment using 2D B-mode ultrasound, the 4D mode was switched on and "live" 3D images were reconstructed by selecting an ideal 2D mid-sagittal image of the face (the region of interest; ROI). The crystal array of the transducer swept mechanically over the ROI. The volume was automatically scanned every 2 s while the surface-rendered mode was switched on, and 4D images were displayed on the screen and recorded on videotape during a 30-min observation period. This procedure was used for the observation of fetal face movements and expression. From top to bottom, the following landmarks were analyzed: forehead, brows, nasal soft tissue and nasolabial folds, upper lip, oral cavity and tongue, lower lip and chin, eyelids and eyes, mouth and mouth angles, and facial expression. All recordings were performed between 14.00 and 17.30 h, and no meal was taken within the 2-h period of the study.
 
Definitions
 
Awareness was defined as the ability to notice something using senses - a phenomenon incorporating both cognitive and physiological elements. There is urgent need for more scientific confirmation of fetal awareness, starting from its definition through to reproducible evaluation. Very early in pregnancy fetuses are reactive to stimuli, but the reaction does not provide any evidence that the fetus actually experienced the stimulus. It has been shown that noxious stimuli can initiate physiological, hormonal, and metabolic responses, but these neither imply nor preclude suffering, pain, or awareness.
 
4D ultrasonography allowed in utero observations of fetal facial expressions of smiling, yawning, and swallowing.
 
Yawning consists of breathing through the mouth and nose, whereby a long inhalation with the mouth wide open is followed by a slow exhalation. A single, continuous opening of the mouth can last for 4-6 s. The anatomical criterion for fetal yawning is retraction of the tongue, whereas yawning in adults is characterized by an extended tongue. Yawning develops at 11.5-15.5 weeks' gestation.
 
The three phases of swallowing (oral, pharyngeal, and esophageal) are the same during fetal life and afterwards. The oral and pharyngeal phases appear to be less well developed in fetuses. In a mature fetus, two-six sucking movements usually precede the initiation of the oral stage of swallowing; thus, the swallowing pattern in a normal fetus near term differs from that in the infant and in the adult. The human fetus demonstrates swallowing movements as early as 11-12.5 weeks' gestation, whereas more complex sucking movements can be identified at 18-20 weeks. Neurobiological control of fetal swallowing includes coordinated contractions of the thyroid, nuchal, and thoracic segments of the esophagus. Although swallowing may bring satisfaction to the fetus, it is very difficult to correlate 4D sonography with a possible indication of fetal awareness.
 
Scowling, smiling, isolated eye-blinking, tongue expulsion, and mouth and eye squeezing are obvious facial expressions or activities that can also be observed by 4D sonography.
 
Although there are reports in the literature that the "quality" and not the "quantity" of general movements in neonates is a better predictor of neurological outcome, the quality of facial movements has been neither described nor studied. Positive observation has been defined as a facial expression or movement noted at least once during the observation of one examinee.
 
Results
 
 
We noted a tendency towards increased frequency of observed facial expressions with increasing gestational age, but the difference between second- and third-trimester fetuses was not significant due to the low frequency of movements. Therefore, all observed facial expressions and movements (i.e. yawning, smiling, tongue expulsion, mouth and eye squeezing, scowling, and isolated eye blinking) are presented collectively in Figure 2, with maximum, minimum, and median frequencies during a 30-min observation period. Some fetal facial expressions are shown in Figures.
 
Discussion
 
Ultrasound is one of the most rapidly developing medical technologies that can extend the physician's inspection, palpation and auscultation. Ultrasound has been very important for the developmental assessment of the fetal central nervous system and its behavioral patterns throughout gestation , and it is generally accepted that patterns of fetal activity reflect the development and maturation of the central nervous system.
 
We are aware that some postnatal studies distinguish between "quantity" and "quality" of motor patterns. Quantity is the number of fetal movements expressed as a percentage of observation time or as the number of events per time epoch. The quality of each individual movement includes speed, amplitude, and force combined in one complex perception. It has been suggested that the observation of behavioral quality is a better predictor of neurological impairment than neurological examination. In this respect, we are unable to study the quality of facial movements in fetuses, because this parameter has not been described yet.
 
Although the advancement of technology enables depiction of the fetal face in real time and observation of its facial expression, there are still many improvements to be made. Since 4D ultrasonography provides only a near real-time reconstruction of the fetal face, some very subtle facial movements may have been missed. To avoid this obstacle, faster frame rates should be achieved. A prolonged observation period could possibly determine if the fetus being observed is either quietly or actively sleeping, drowsy, or alert and inactive. Otherwise, the fetal face will frequently be missed and be unavailable for proper observation.
 
4D sonography, introduced in recent years, is a completely new tool for observing fetal behavior and the fetal face. However, as for any other new technology, there is much room for improvement. Furthermore, accurate and reliable fetal face evaluation is still time-consuming. However, this is the only available method enabling continuous monitoring of the fetal face and other surface features of the fetus - facial expressions - as possible measures of fetal awareness. Our study shows the possible visualization of several facial expressions, but it is still unknown if fetal face expressions can help us in understanding what the fetus would like to communicate.
 
Yawning can occasionally be observed during the first and second half of a normal pregnancy. It has also been shown that term human fetuses yawn predominantly during active sleep, but not during quiet sleep. Sherer and associates described in detail a single yawning movement in a 20-week fetus; they observed that the fetal mouth, previously closed, opened widely and remained so for 2-3 min in association with simultaneous extension of the fetal arms and flexion of the fetal head. The physiological role of yawning during intrauterine life remains speculative. A respiratory function is less probable, since thp surrounding environment is liquid rather than air. However, since a forced inspirium is a critical component of yawning, a potential role for expanding the terminal alveoli in the fetal lungs by the inspired fluid is possible, consistent with the hypothesis that yawning may serve as a mechanism to protect against alveolar collapse in extrauterine life.
 
Far too many interpretations of an open mouth as yawning have been described in the recent literature. The range of variation includes, for example, a single continuous opening of the mouth for 4-6 s. There is also controversy about the use of the anatomical criterion of tongue retraction to characterize the fetal yawn. It seems that there is no physiological reason why the fetus should yawn. Doppler studies found no connection to hypoxia. Furthermore, yawning confers no protection against atelectasis in a fluid-filled lung. With 2D sonograpic visualization of fetal yawning, one of the most uncommon behavioral states in human fetuses could be incidentally observed during ultrasonic examination of the fetal face. Yawning is a poorly understood complex movement present in almost all mammals. Although it can be induced by several physiological processes, such as hunger, fatigue, sleepiness, boredom, and drowsiness, a number of neurological disorders and drugs can also trigger this reflex. The physiological function and neuroanatomical pathways involved in yawning are still unknown. It is presumed that yawning in humans can be used as an index of dopaminergic system functioning.
 
A detailed study of the normal development of swallowing over the course of fetal life may lead to early identification of potential neonatal swallowing difficulties and may clarify the mechanism of polyhydramnios and oligohydramnios. The normal pharyngeal stage of swallowing in adults 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 any amniotic fluid swallowed is directed not only into the esophagus, but into the trachea as well. According to our observations, the frequency of swallowing movements was the same, irrespective of gestational age.
 
The introduction of 3D/4D sonography is a turning point in fetal facial examination. Once the midsagittal plane is obtained, the volume dataset can be acquired. First, the surface-rendering mode is used to search for facial dysmorphogenesis. Then the multiplanar re-slicing mode is used, and the three reference planes, sagittal, axial and coronal, are simultaneously displayed and scrutinized. Up to now, examination of the fetal face was only an integral part of fetal ultrasound examination during pregnancy, whether in a screening setting or during targeted analysis. Our study is the first attempt to use 4D sonography in the evaluation of fetal facial expressions and facial movements in order to observe fetal awareness. Postnatal investigation of facial expressions of premature infants will help us in choosing prenatal observations of fetal facial movements.
 
Conclusion
 
Our study shows the ability of 4D sonography to depict different facial expressions and movements, which might represent fetal awareness. Nevertheless, long, precise and thorough observation of the fetal face by 4D sonography is hampered by the only near-real-time images. Development of the technology will allow even better depiction of fetal facial expressions and movements. At present, fetal facial expressions and movements depicted by 4D sonography can be used as a sign of fetal awareness. There is an urgent need for further studies in order to compare the existence of fetal awareness by 4D ultrasonography in normal and abnormal fetuses, which might be helpful in the evaluation of fetal neurological status. In the meantime, the new technique should be neither overestimated nor underestimated.
 
fetal movements