INTRODUCTION

Fetal body movements give important information about the condition of the fetus. Analysis of the dynamics of fetal behavior has led to the conclusion that fetal behavioral patterns directly reflect developmental and maturational processes of the fetal central nervous system. As we learned from postnatal studies of neonatal behavior, assessment of behavior is a better predictor of neurodevelopmental disability than neurological examination. These findings implicated that understanding the relation between fetal behavior and developmental processes in different periods of gestation would make possible the distinction between normal and abnormal brain development, as well as the early diagnosis of various structural or functional abnormalities.There is an increasing number of results showing that, many neurological problems, such as minimal cerebral dysfunction, schizophrenia, epilepsy or autism, result at least in part from prenatal neurodevelopmental problems .

Fetal Behavior, Qualitative and Quantitative Approach:

Fetal behavior can be defined as any observable action or reaction (to an external stimulus) by the fetus. This may be recorded by maternal perception of movement or real time ultrasound imaging by means of which fetal behavior can be observed in the clearest and most detailed way. The quantitative as well as qualitative aspects of fetal behavior were analyzed by now. Quantity is the number of fetal movements expressed as a percentage of observation time or as the number of events per time period. 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. This is due to fetal behavior or in a way endogeneous motility and reactions towards stimuli are indicators of early neuromuscular development.

Why is it important to evaluate Fetal Behavior?

Assessment of fetal and neonatal behavior was developed mainly as a diagnostic tool for the early detection of brain dysfunction. Investigators have started to analyze fetal behavior to assess the development of the nervous system in normal and abnormal conditions . A recent study has shown that there is behavioral continuity from fetal to neonatal life . Continuity was shown from fetal to neonatal behavior, especially in terms of isolated eye blinking movements, mouth and eyelid opening, yawning, tongue expulsion, smiling, scowling, and hand movements directed to other parts of the face (There were no movements observed in fetal life that were not present in neonatal life, while the Moro reflex was present only in neonates.

What is Kurjak Antenatal Neurological Test (KANET)and why it is needed? (Table 1,2):

Many neurological disorders originate from intrauterine rather than perinatal or postnatal period . Clinical and epidemiological studies have shown that CP most frequently results from prenatal rather than perinatal or postnatal causes . This is one of the reasons why simple and applicable screening fetal neurological test is desperately needed.

KANET is a new scoring system which asseses fetal neurological status using 4D ultrasound in about 30 minutes examination. It is proposed by Kurjak et al in 2008. The KANET test has the potential to detect and discriminate normal from borderline and abnormal fetal behavior in normal and in high risk pregnancies, which means that it could become a valuable diagnostic tool for fetal neurological assessment. It is important to critically review and improve the test, making it more simple and applicable as the screening tool for prenatal neurological assessment.

By now KANET has been shown to be useful in standardization of neurbehavioural assessment with the potential for antenatal detection of fetuses with severe neurobehavioral impairment . Further research has been initiated in several centers with similar objectives: to assess practical clinical application of the test in both, normal and high risk pregnancies . The components of the KANET test is given in tha table 1 and 2 which show the criteria used to evaluatethe fetus and evaluation of the score as normal,borderline and abnormal (Table1,2).

Kurjak et al suggested that their results are promising and KANET requires further studies before being recommended for wider clinical application.

Why do we need normal standards of fetal behavior?

The preliminary results of multicentric studies of fetal brain function suggest that the study of fetal behavior should be standardized as much as possible. If behavioral analysis is to have a role in the routine clinical environment, then normal standard parameters and objective methods need to be developed. De Vries and colleagues were the first to provide a systematic and detailed classification and quantitative longitudinal analysis of fetal behavior during the first half of pregnancy using two-dimensional ultrasound (2D US). During the past 8 years, Kurjak et al. have initiated an extensive research about fetal behavior in normal and pathological pregnancies by both three-dimensional (3D US) and four-dimensional ultrasound (4D US). The availability of quantitative standards might be important for the experts to be aware of normal fetal behavior throughout the whole of gestation to assess the neurologic condition of the fetus. Therefore the normal standard parameter of the fetal movements and facial expressions in all three trimesters of normal pregnancy is constructed.

Ultrasonic technology for evaluating fetal behavior:

Innovations in ultrasonic technology have created new possibilities in the study of fetal behavior . The introduction of four-dimensional ultrasound (4D US) led to very important conclusions about fetal behavior by enabling us, to produce measurable parameters for the assessment of normal neurobehavioral development. It is now possible to study a full range of facial expressions including smiling, crying, scowling and eyelid movements in almost real time by 4D US .

There have been many descriptions of conventional 2D sonographic assessment of fetal movements with respect to the assessment of fetal behavior. Although 2D US documents the origin, occurrence, and developmental course of specific fetal movements, simultaneous imaging of complex facial movements is impossible only by means of a 2D real-time technique.

The development of 4D US provided new opportunities for the study of fetal behavior . 4D US enables spatial surface rendering imaging in the near real-time and allows the studying of fetal facial anatomy as well as the dynamics of facial movements and expressions33. It is believed that one of the largest challenges for four-dimensional ultrasound is in the unexplored area of parental and fetal behavior. It also removed the question of subjectivity in the recording of information . In the first trimester using four-dimensional ultrasound one can simultaneously assess movements of the fetal head, body and all four extremities in three dimensions. Therefore, the earliest phases of the human anatomical and motor development can be visualized and studied simultaneously . It is possible to study nearly total fetal facial activities by 4D US. In addition to yawning, sucking and swallowing described by 2D real-time imaging, it is now possible to study a full range of facial expressions including smiling, crying, and eye-lid movements with this technology .

Furthermore, four-dimensional sonography seems to be the method of choice for detecting subtle changes such as superimposed rotations and changes in direction of the movementsFour-dimensional ultrasound offers the possibility of studying fetal behavior and general movements in a more global way than conventional two-dimensional ultrasound. In normal cases, the images obtained help to transmit a feeling of calmness to the parents and reinforce the affective bonds with their child.

Four-dimensional ultrasound or real-time three-dimensional ultrasound makes it straight forward to comprehend some morphological dynamics, such as yawning, sucking, smiling, crying and blinking. This offers a practical means for assessment of neurophysiological development, as well as for detection of anatomical pathology . The ability to observe a simultaneous generation of new movement patterns is the most prominent advantage of four-dimensional sonography. Four-dimensional ultrasonography (4D-US) provides a tool for movement observations not only for their differentiation but also to categorize specific patterns of behavior. The qualitative assessment might be even more informative because this method allows the simultaneous visualization of the whole fetal body. Two-dimensional realtime ultrasound and 4D sonography are complementary methods used for evaluation of fetal movements. It is clear that the quality of each fetal movement can be visualized and evaluated more reliably by 4D ultrasound. However in one studyseveral movement patterns, such as side-way bending, hiccup, breathing movement, mouth opening, and facial movement, could be observed only by the 2D ultrasonographic technique, and not by 4D ultrasound in 6-14weeks of gestation.

It is also known that 4D ultrasound is an important modality in future research on fetal neurobehavioral development and the prenatal identification of severely brain-damaged infants.

The technique:

After standard assessment in 2D B-mode ultrasound, one can switch to 4D mode and a live 3D image can be built by selecting the ideal representative 2D image placed in the region of interest (ROI). The crystal array of the transducer is moved mechanically over the defined ROI. The volume is automatically scanned every two seconds, and 4D images are displayed on the screen and recorded on CD recorder approximately 30 min. observation period. Fetal movement and fetal facial expression patterns from first, second and third trimesters can be evaluated.

Limitations:

In cases of oligohydramnios or the shadowing by hands, feet, umbilical cord or placenta it can be difficult to obtain high-quality images in surface mode. Also by 4D US very quick movements (within 1 to 2 sec) and subtle movements including rapid blinking, subtle lip movement, and dynamic lingual movement may not be recognized especially in the first trimester at the moment . This is because of the relatively slow repetition time for data acquisition to obtain a satisfactory image. 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 yet been described.

It was reported that fetal behavior is time consuming, it needs expert sonographists and the facial expressions sometimes is somewhat subjective. They also proposed an easier way of analyzing fetal behavior should be developed for diagnostic and prognostic use (e.g., automated computer-based analysis for evaluating fetal movements). They have thought that These limitations of 4D ultrasonographic fetal imaging will be resolved as further technical advances such as high-frame rate 4D ultrasound devices with automated objective recognition systems, etc., are made”

Is it easy to study fetal behavior?

The major problem with the study of fetal behavior is that, it is very time consuming. Nevertheless, there is no other possibility of assessing the function of the CNS in utero, and this is needed for understanding of the hidden information in the neurodevelopmental pathways of the fetal CNS. Only if normal behavior is fairly understood, it is possible to identify and to perceive abnormal behavior before birth.

Fetal behavior in twins:

It is also possible to evaluate the twin to twin contact in utero by 4D us and potentially more advantageous in compare to 2D US. It can give us information regarding the functioning of tactile and proprioceptive sensitivity, which are impossible to ascertain with an intact single fetus Full range of movements can be studied in twin pregnancies . Some of the inter-twin contact movements are head to head, head to arm, head to trunk, head to leg, arm to arm, arm to trunk, arm to leg, trunk to trunk, trunk to leg, and leg to leg contact.

General movements, Startle, Stretching, Isolated arm movements, Isolated leg movements, Head retroflexion, Head rotation, Head anteflexion.

Isolated eye blinking, Mouthing, Yawning, Tongue expulsion, Grimacing, Swallowing, Smiling, Sucking. Fetal facial expressions are controlled by facial nerves in the brain, and some of them have also been documented by 2D ultrasound .

Head retroflexion, Head rotation, Head anteflexion, hand to head direction, Hand to eye direction, Hand to mouth direction, Hand to face direction, Hand to ear direction.

The Definitions of some fetal behaviour patterns:

According to the literature data movement patterns and expressions can be classified as follows:

General movements: The whole body is moved and series of movements with variable speed and amplitude, involve all parts of the body without distinctive patterning of body parts can be seen. Duration varies from a few seconds to about a minute.

• Just discernible movements: Between and 8.5 weeks postmenstrual age, a slow and small shifting of the fetal contours is seen, lasting from half a second to two seconds, which usually occurs as a single event.
• Startle: Quick generalized movements, starting in the limbs and sometimes spreading to the neck and trunk, only last about one second.
• Stretching: A complex motor pattern, always carried out at a slow speed and consists of the forceful extension of the back, retroflexion of head, and external rotation and elevation of the arms.
• Head retroflexion, rotation and anteflexion Isolated retroflexions, rotations and anteflexions of the head: Usually carried out slowly, but they can also be fast and jerky.
• Isolated retroflexion of the head: The displacement of the head can be small or large. The latter may cause over-extension of the spine of the fetus.
• Isolated anteflexion of the head: Anteflexion of the head is carried out only at a slow velocity. The displacement of the head is small.
• Isolated rotation of the head: Rotation of the head is carried out at a slow velocity and only exceptionally at a higher speed. The head may turn from a midline position to one side and back.
• Rotation of the fetus: Rotation of the fetus occurs around the sagittal or transverse axis. A complete change in position around the transverse axis, usually with a backwards and usually it is achieved by a complex general movement, including alternating leg movements, which resemble neonatal stepping.
• Isolated arm or leg movement: These may be rapid or slow movements, and may involve extension, flexion, external and internal rotation, or abduction and adduction of an extremity, without movements in other body parts.
• Hand to body contact (head, mouth, eye, face, ear): In this pattern of movement, the hand slowly touches the body parts, with extension and flexion of the fingers. All subtypes of hand to head movement could be seen from 13 weeks of gestation.
• Jaw movements: Jaw opening may be either slow or quick. The extent of jaw opening is variable. The duration of opening varies from less than 1 s to 5 s.
• Hiccup: A hiccup consists of a jerky contraction of the diaphragm. An abrupt displacement of the diaphragm, thorax and abdomen can be seen on the scanning image.
• Breathing: Fetal breathing movements in utero are paradoxical in nature, i.e. ‘inspirations’ consisting of fluent simultaneous movement of the diaphragm (caudal direction), leading to movements of the thorax (inwards) and abdomen (outwards).

Facial expressions:

• Swallowing: Indicating that the fetus is drinking amniotic fluid. Swallowing consists of displacements of tongue and/or larynx. Swallowing activity develops earlier than sucking in the course of fetal development At ten weeks of gestation opening of the mouth was seen. Swallowing was seen from 12 weeks onwards.
• Sucking: Rhythmical bursts of regular jaw opening, and closing at a rate of about one per second. Placing the finger or thumb on the roof of the mouth behind the teeth and sucking with lips closed.
• Smiling: A facial expression characterized by turning up the corners of the mouth.
• Tongue expulsion: A facial expression characterized by expulsion of the tongue.
• Grimacing: The wrinkling of the brows or face in frowing to express of displeasure.
• Mouthing: A facial expression characterized by mouth manipulation to investigate an object. Mouthing is most common in fetus and it may develop into a persistent, stereotyped behavior pattern.
• Isolated eye blinking: A reflex that closes and opens the eyes rapidly. Brief closing of the eyelids by involuntary normal periodic closing, as a protective measure, or by voluntary action.
• Yawning: This movement is similar to the yawn observed after birth: An involuntary prolonged wide opening of the mouth, with maximal widening of the jaws followed by quick closure often with retroflexion of the head and sometimes elevation of the arms. This movement pattern is non-repetitive. Yawning and stretching reverse the muscular atonia of the REM-sleep and reopen the collapsed airways. Anemic fetuses were noted to yawn in an unusual bursts while IUGR fetuses demonstrated isolated yawning patterns similar to those seen in normal fetuses.

Fetal behavior during a normal pregnancy:

The neural activity leading to the first detectable movements is considered to originate from the spinal motor neurons at 6–7 postconceptional weeks, shortly before the onset of embryonic motility. The first spontaneous fetal movements can be observed at postconceptional 7 to 7.5 weeks . 4D US allows the visualization of fetal motility 1 week earlier. In the subsequent weeks (8th to 9th weeks of gestation), they are replaced by various, well-organized general movements, which include head, trunk and limb movements, as well as with the isolated limb movements. Hands become sensitive at 10.5 weeks and lower limbs begin to participate in these reflexes at approximately the 14th week35,37. General movements are the first complex fetal movement patterns observable by 2D US. According to Prechtl these are gross movements, involving the whole body. They can be recognized from 8–9 weeks of pregnancy and remain present until 16–20 weeks after birth.

General movements followed by isolated hand movements are the most frequent movement patterns at the first trimester. A tendency towards, increased frequency of fetal movement patterns with increasing gestational age is seen during the first trimester30,37. Some of the movement patterns could not be observed through all trimesters. For example, startle and stretching, which were observed in the first trimester, disappear with the progression of pregnancy27. As the pregnancy progresses, the random movements of fetal body, which are the earliest signs of fetal activity, change into the well-organized behavioral patterns. Breathing movements and hiccups, appears at the 9th week. Facial movements, which are also controlled by V and VII cranial nerves, appear around 10 and 11 weeks. Facial movements, swallowing, mouth opening and yawning appears at 10 weeks. The isolated limb movements seen at the 9th week are followed by the appearance of the movements in the elbow joint at 10 weeks, changes in finger position in the 11th week and by easily recognizable clenching and unclenching of the fist at weeks 12 to 13. Isolated finger movements as well as the increase in activity and strength of the hand/finger movements, can be seen at 13 to 14 weeks. By the 14th to 19th weeks, fetuses are highly active with the longest period between movements only 5–6 minutes. In the 15th week, 15 different types of movement can be observed. Besides the general body movements and isolated limb movements, retroflection, anteflection and rotation of the head can easily be seen. General movements in sick preterm infants are reduced in elegance and fluency, as well as in the variability and fluctuation of the intensity and speed of motor performances, rather than a change in the incidence of distinct motor patterns .

De Vries and colleagues studied fetal movements from 20 and from 24 postmenstrual weeks onward. During the second trimester of pregnancy, the incidence of body movements increased considerably. Fetuses from 17 to 20 weeks made slow flexion and extension movements of the trunk, sometimes accompanied by the movement of a single limb. At 18 to 20 weeks, fetuses performs slow, supple, and harmonious movements with isolated leg movements, in contrast to the synchronized movements of the whole body with twitches and kicking, as frequently found at 12 to 13 weeks.

Kurjak et al reported the first study which described the 4D US techniques used for obtaining longitidunal standard parameters of fetal neurological development in all trimesters of a normal pregnancy. They found a tendency to increase in the frequency of fetal movement pattern at the beginning of the second trimester by 4D US. However, all types of head movements and hand to body contact movements indicated a decrease in frequency from the beginning of the second trimester to the end of the third trimester. The periods of fetal quiescence begin to increase and the rest–activity cycles become recognizable. By term, in a study the average number of general movements per hour was found 31 (range 16–45) with the longest period between movements ranging from 50 to 75 min which is quite long in compare to the second trimester. The qualitative and quantitative aspects of behavioral patterns expand rapidly as the pregnancy progresses.

It is also suggested that there is a tendency towards decreased frequency of observed facial expressions and movement patterns with increasing gestational age. The observation of facial expression may be of scientific and diagnostic value and this scientific approach opens an entirely new field. For example one of the diagnostic goals of observing facial expression is prenatal diagnosis of facial paresis. Criteria for the identification are asymmetrical facial movements and detection of the movements restricted to only one side of the face. In a study, the most frequent fetal and neonatal movements registered in the third trimester and in the neonatal period were scowling, eye and mouth opening, and hand to face, hand to eye, and hand to head movements49. There was a tendency towards a decrease in frequencies of observed facial expressions (isolated eye blinking, mouthing) and some hand movement patterns (hand to head, hand to mouth, hand to face, hand to eye, hand to ear) with increasing gestational age. Significant trends in fetal eye movement organization can also be observed during the second half of pregnancy, especially during the third trimester27,33,35. The earliest eye movements appear at the 16th to 18th weeks of gestation. At 24 to 26 weeks of gestation, they appear more frequently. At 36 to 38 weeks of gestation, they become integrated with other parameters of fetal activity .

Kurjak et al in another study, evaluated fetal behavioral patterns in the third trimester between 30 and 33 weeks of gestation in ten gravidas. They noted that among facial activities observed by 4D US, simultaneous eyelid and mouthing movements dominate between 30 and 33 weeks of gestation38. In our group’s study all types of facial expressions displayed a peak frequency at the end of the second trimester similarly except in isolated eye blinking which increased at the beginning of the 24th week.The fetuses displayed a decreasing or stagnant incidence of fetal facial expression from the beginning of the third trimester. Also, while mouthing, yawning, tongue expulsion, smiling, sucking, swallowing expressions displayed a peak frequency between 24th to 32nd gestational weeks, grimacing and eye blinking expressions displayed peak frequency between 28th to 36 weeks and after 32nd weeks respectively. The fetuses displayed decreasing or stagnant incidence of fetal facial expression at the middle of the third trimester, except for eyeblinking which showed increased frequency with increasing gestational age. Recently Talic et al has reviewed about the studies on fetal behavior and indicated the main findings in these studies.

Conclusion:

KANET is very important test and it seems very promising to identify neurologically abnormal babies. KANET test needs to be studied in all high risk centers to be even more improved and by this way possibly in the near future it will be possible to screen the pregnant women in terms of neurological status of the fetus. Full range of quantitative fetal facial expressions and fetal movement patterns can be assessed successfully by 4D sonography. Many excellent studies have been done about fetal behavior in quite a recent time using 4D Ultrasonography which give us the possibility to find the hidden information of CNS by analyzing the fetal behavior It is important to be able to assess normal fetal behavior throughout the whole gestation to identify and to perceive abnormal behavior before birth.

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Miškoviæ B, Vasilj O, Stanojeviæ M, Ivankoviæ D, Kerner M, Tikvica A. The comparison of fetal behavior in high risk and normal pregnancies assessed by four dimensional ultrasound. J Matern Fetal Neonatal Med 2010 [Epub ahead of print]

Acknowledgements: Special thanks to Murat Albert Yigiter for his techniqual help in constructing this chapter. All the ultrasound pictures in this chapter were taken by Alin Basgul Yigiter Assoc. Prof. M.D.