doi:10.1111/jog.13099

J. Obstet. Gynaecol. Res. 2016

Current status of fetal neurodevelopmental assessment: Fourdimensional ultrasound study Toshiyuki Hata Department of Perinatology and Gynecology, Kagawa University Graduate School of Medicine, Miki, Japan

Abstract With the latest advent of four-dimensional (4-D) ultrasound, fetal neurobehavioral or neurodevelopmental assessment can be easily and readily performed. Using this technique, typical fetal movements and behavioral patterns have become apparent in all three trimesters of pregnancy. In twin pregnancy, 4-D ultrasound facilitates the precise evaluation of inter-twin contact and intra-pair stimulation. New fetal neurobehavioral assessment tests, such as Kurjak’s Antenatal Neurodevelopmental Test and the Fetal Observable Movement System, may reflect the normal and abnormal neurological development of the fetus, and will facilitate more precise assessments of fetal neurobehavior or neurodevelopment, and fetal brain and central nervous system functions. In this review article, I also discuss interesting topics regarding maternal and fetal stress, fetal pain, and fetal consciousness. Four-dimensional ultrasound has opened the door to new scientific fields, such as ‘fetal neurology’ and ‘fetal psychology,’ and fetal neurobehavioral science is at the dawn of a new era. Knowledge on fetal neurobehavior and neurodevelopment will be advanced through fetal behavioral research using this technique. Key words: 4-D ultrasound, fetal brain function, fetal consciousness, fetal neurobehavior, fetal pain, fetal stress.

Introduction Until now, there has been no modality to assess the fetal brain and central nervous system (CNS) functions directly in utero. However, fetal behavior is thought to be a product of the functioning brain and CNS.1 By observing fetal behavior, we can examine the functioning of the brain and CNS directly. Also, fetal movements and behaviors have been considered as indicators of fetal brain and CNS development.2,3 With the appearance and development of fourdimensional (4-D) ultrasound, fetal movements, behaviors, and facial expressions can now be observed.4–6 Moreover, maternal and fetal stress, fetal pain, and fetal consciousness are being discussed using this technique.7 In twin pregnancy, twin fetal developments and inter-

twin contacts and stimulations have been investigated using 4-D ultrasound.8 New fetal neurobehavioral assessment tests, such as Kurjak’s Antenatal Neurodevelopmental Test (KANET) and the Fetal Observable Movement System (FOMS), may reflect the normal and abnormal neurological development of the fetus, and will facilitate more precise assessments of fetal neurobehavior or neurodevelopment, as well as fetal brain and CNS functions.9,10 In this review article, we present the current status of fetal neurodevelopmental assessment using 4-D ultrasound, and, on this basis, make recommendations for future research on fetal neurobehavioral development, and inter-twin contacts and intra-pair stimulations in twin pregnancies.

Received: April 18 2016. Accepted: May 28 2016. Correspondence: Professor and Chairman Toshiyuki Hata, Department of Perinatology and Gynecology, Kagawa University Graduate School of Medicine, 1750-1 Ikenobe, Miki, Kagawa 761-0793, Japan. Email: [email protected]

© 2016 Japan Society of Obstetrics and Gynecology

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First Trimester Using the latest 4-D ultrasound, life-like images of the fetus and fluid fetal movements can be identified during the first trimester of pregnancy (Figs. 1 and 2).

Kurjak et al.11 were the first to identify three types of fetal movements (gross body movement at 7 8 gestational weeks [GW], limb movements after 10 GW, and complex limb movements after 11 GW) using 4-D ultrasound in the first trimester of pregnancy. The same group identified a tendency towards a decreased frequency of fetal facial expressions and movement patterns with advancing gestation, and the highest incidence of general movements was found in the first trimester of pregnancy.12 However, other investigators noticed that the incidence of all fetal movements except for the startle movement increased with advancing gestational age, and the frequency of the startle movement remained unchanged in the first trimester of pregnancy.13–15 Hata et al.16 found that the most frequent fetal movement was isolated arm movement at 10 11 GW, and jumping movement at 12–13 GW. There was a significant difference of jumping movement between 10–11 and 12–13 GW. These authors suggest that the difference in the frequency of fetal movements late in the first trimester may be caused by early neuromuscular development and differentiation of the neuromuscular system.

Second and Third Trimesters

Figure 1 Four-dimensional ultrasound image of a 10-week fetus.

Fetal behavior in the second trimester and various fetal facial expressions in the second and third trimesters can be clearly depicted using 4-D ultrasound (Figs. 3–8). Kuno et al.17 were the first to evaluate fetal behavior early in the second trimester using 4-D ultrasound for 60 min. The active phase (time with fetal behavior) was 59.4%, and the resting phase was 40.6%. The most frequent fetal behavior was isolated arm movement, and the least was mouth movement. At 20–24 GW, fetal mouthing was significantly more frequent than the other

Figure 2 (a–d) Consecutive four-dimensional ultrasound observation of general fetal movement at 11 weeks of gestation.

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Fetal neurodevelopmental assessment

Figure 3 (a–d) Consecutive four-dimensional ultrasound observation of general fetal movement at 15 weeks and 1 day of gestation.

Figure 4 Four-dimensional ultrasound image of fetal smiling at 29 weeks and 5 days of gestation.

facial expressions.18 Yawning was significantly more frequent than smiling, scowling, and blinking, and sucking was significantly more frequent than smiling, scowling, and blinking. At 25–27 GW, mouthing was still the most common fetal facial expression, and yawning was significantly more frequent than the other facial expressions, apart from mouthing.19 At 28–34 GW, only fetal

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Figure 5 Fetal eye opening at 29 weeks and 5 days of gestation.

mouthing was significantly more frequent than the other facial expressions.20 All types of fetal facial expressions showed a peak frequency in the late second or early third trimester of pregnancy, and the fetus displayed a constant level or a slight decrease of facial expressions towards the end of pregnancy.13–15 Moreover, all types of hand-to-head or

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Figure 6 Fetal crying (scowling or grimacing) at 31 weeks of gestation.

hand-to-face movements and head movements decreased with advancing gestation in the second and third trimesters of pregnancy.13–15 With respect to behavioral pattern continuity from pre- to postnatal life, all movements observed in fetal life were also identified in neonatal life.12,21 The most frequent fetal and neonatal movements were eye blinking, mouthing, grimacing, hand-to-mouth, and hand-to-face movements. Andonotopo and Kurjak22 conducted a prospective study in 50 normal fetuses and 50 with fetal growth restriction (FGR) to evaluate whether the quantity of fetal facial expression and quality of body movements could be used as additional diagnostic information on prenatal brain impairment in FGR fetuses. These authors noted a tendency whereby FGR fetuses showed less behavioral activity than normal fetuses in all observed movement patterns. Several authors investigated fetal behavioral patterns in anencephalic fetuses using 4-D ultrasound.23,24 All frequencies of movement patterns in the anencephalic fetuses were suggested to decrease. Moreover, almost no movements of the lower extremities and no facial expressions were evident.

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Figure 7 Fetal yawning at 29 weeks and 5 days of gestation.

Figure 8 Fetal tongue expulsion at 33 weeks and 5 days of gestation.

© 2016 Japan Society of Obstetrics and Gynecology

Fetal neurodevelopmental assessment

Twin Studies In our series of 4-D ultrasound studies on inter-twin contact, intra-pair stimulation, and reactions to touch in utero between twin fetuses for 30 min late in the first trimester of pregnancy,25–27 there was a significant difference in the total number of all contacts between monochorionic diamniotic (MD) and dichorionic diamniotic (DD) twins at 10–11 GW, and there was also a significant difference in the total number of contacts between 10–11 and 12–13 GW in DD twins.25 The median rate of reaction movement (twins appear to touch each other and there is a clear reaction by the co-twin [Fig.9]) in twin fetuses at 12–13 GW was 33.9% (range, 27–64.1%).26 Our twin study showed that the difference in the frequency of the type of inter-twin contact at 10– 13 GW might be due to early fetal neuromuscular development and differentiation of the neuromuscular system.27 Moreover, a decreased number of inter-twin contacts was noted in a case of MD twins with acrania of one of them at 10–13 GW.28 Castiello et al.29 studied kinematic profiles of movements in twin fetuses using 4-D ultrasound at 14 and 18 GW. These authors concluded that the performance of movements towards the co-twin was not accidental, and twin fetuses executed movements specifically aimed at the co-twin already starting from 14 GW. Degani et al.30 measured fetal motor activity in twin fetuses at 11–14 GW using 4-D ultrasound, in order to study inter-twin differences in activity late in the first

trimester and to examine their relationship with infant twins’ subsequent temperament. Maternal reports on infants’ temperament after birth and the more active twin in each pair showed a close correlation with antenatal inter-twin differences in activity.

Kurjak’s Antenatal Neurodevelopmental Test In 2008, Kurjak et al.31 were the first to propose a new scoring system, Kurjak’s Antenatal Neurodevelopmental Test (KANET), for the antenatal assessment of the fetal neurological status using 4-D ultrasound, based on the concept that fetal behavioral patterns directly reflect developmental and maturational processes of the fetal brain and central nervous system. In 2011, Stanojević et al.32 proposed the new modified KANET scoring system to make this test more comprehensive, reproducible, and standardized. In 2013, Antsaklis et al.33 showed the latest KANET test for the assessment of fetal brain and CNS functions in clinical practice. As previously reported clearly,34 between 28 and 38 GW, the following eight types of movement are assessed: isolated head anteflexion, cranial sutures and head circumference, isolated eye blinking, facial alteration or mouth opening, isolated leg movement, isolated hand or hand-to-face movements, finger movements, and gestalt perception of general movements (Table 1). The fetuses undergo ultrasound examination while awake, and the examination duration is from 15 to

Figure 9 Inter-twin contacts in monochorionic diamniotic twin fetuses at 13 weeks and 2 days of gestation. (a) Arm-to-trunk contact. (b) Leg-to-leg contact.

© 2016 Japan Society of Obstetrics and Gynecology

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Table 1 Kurjak’s Antenatal Neurodevelopmental Test (Reprinted from Kurjak et al.32 with permission) Sign

Score 0

Sign score

1

2

Isolated head anteflexion

Abrupt

Small range (0–3 movements)

Variable in full range, many alterations (>3 movements)

Cranial sutures and HC

Overlapping of cranial sutures

Normal cranial sutures with normal measurement of HC according to GA

Isolated eye blinking

Not present

Normal cranial sutures with measurement of HC below or above the normal limit (–2 SD) according to GA Not fluent (blinking 1–5 times)

Facial alteration (grimace or tongue expulsion)

Not present

Not fluent (1–5 alterations)

Fluency (blinking > 5 times)

Isolated leg movement

Cramped

Poor repertoire or small in range (0–5 movements)

Variable in full range, many alterations (>5 movements)

Isolated hand movement

Cramped or abrupt

Poor repertoire or small in range (0–5 movements)

Variable in full range, many alterations (>5 movements)

Finger movements

Unilateral or bilateral clenched fist (neurological thumb)

Cramped invariable finger movements

Smooth and complex, variable finger movements

Gestalt perception of general movements Total score

Definitely abnormal

Borderline

Normal

Fluency (blinking > 5 times)

Mouth opening (yawning or mouthing)

Hand to face movements

GA, gestational age; HC, head circumference; SD, standard deviation.

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Fetal neurodevelopmental assessment

20 min. They are scored as follows: 0–5 is abnormal; 6–9 is borderline; and 10–16 is normal (Table 2). In normal fetuses, the total KANET score was normal between Japanese and Croatian fetuses, but there was a significant difference in total KANET scores in both populations.34 This study suggests that ethnicity should be considered when evaluating fetal behavior, especially during the assessment of fetal facial expressions. There was no difference in KANET scores between male and female fetuses in the third trimester of pregnancy.35 When evaluating the effect of parity on fetal behavior between primi- and multiparas, there was no significant difference in the total KANET score between the two groups.36 However, a significant difference in just one fetal movement, isolated eye blinking, between the groups was found. This investigation suggests that the level of relaxation of pregnant women may affect fetal behavior, particularly the rate of eye blinking. There was no significant difference in the number of normal, borderline, and abnormal KANET scores between singletons and twins, although differences were noted in certain parameters of the test between singletons and twins.37 These authors concluded that movements in twins become more complex, and occur more frequently, with advancing gestation. There were significant differences in KANET scores between normal and high-risk pregnancies.38–43 Interestingly, a large proportion of FGR fetuses with borderline or abnormal KANET scores still showed normal brain circulation when the middle cerebral artery pulsatility index was measured.44 This phenomena suggests that in the progress of pathophysiological events, fetoplacental insufficiency alterations of fetal behavior occur prior to fetal ‘brain sparing.’ There were no significant differences in KANET scores between normal fetuses and those with isolated mild or moderate ventriculomegaly.45 With respect to the prediction of adverse neurological outcomes, all cases with an abnormal KANET score proved to be abnormal postnatally.46 Therefore, the KANET test may have an important role in the antenatal assessment of fetal neurobehavior and prediction of an adverse neurological outcome.

Table 2 Interpretation of the total KANETscore (Reprinted from Kurjak et al.32 with permission) Total score

Interpretation

0–5 6–9 10–16

Abnormal Borderline Normal

KANET, Kurjak’s Antenatal Neurodevelopmental Test.

© 2016 Japan Society of Obstetrics and Gynecology

However, further studies involving a larger sample size are needed to confirm the usefulness of this test in clinical practice.

Fetal Observable Movement System The Fetal Observable Movement System (FOMS) effectively identifies fetal muscle movements with a focus on facial and other head-related movements, such as head rotation and self-touch.47 Each individual anatomically distinct movement is encoded, facilitating the standardization of fetal facial movement investigation.10 So, the FOMS is a precise and reliable fetal facial scoring system to effectively compare data on fetal facial movements between observers or laboratories.47 Reissland et al.48 provided the first evidence of developmental progression from individual unrelated facial movements toward fetal facial expressions, such as smiling and crying, using the FOMS. With this technique, fetal yawning could be reliably distinguished from other forms of mouthing movements.49 The number of yawning actions declined at 28 GW, whereas mouthing movements were less frequent, and the decline was observed from 24 GW. Regarding fetal mouthing movement in more detail, the number of mouth stretches decreased with advancing gestation, whereas that of mouth puckers did not change between 24 and 36 GW.50 Moreover, there was a significant increase in the proportion of fetal lateralized mouth openings during pregnancy, and this was also evidence of left lateralization preference in mouth movement.51 Reissland et al.10 suggest that FOMS is more sensitive to subtle behavioral changes than KANET, which focuses on gross motor behavior. Therefore, FOMS may have a marked potential for clinical use in diagnosing abnormal fetal neurodevelopment, which KANET might fail to detect.

Maternal and Fetal Stress Conventional two-dimensional sonography showed that the jerkiness of fetal arm movements was significantly correlated with fetal stress,52 and found that an immediate increase of large, jerky movements following vibro-acoustic stimulation suggested instability in fetal capabilities.53 Reissland et al.54 examined the effects of maternal stress on lateralized fetal self-touch to the face/head using 4-D ultrasound. The maternally reported stress

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level was significantly positively correlated with fetal left-handed self-touches. The effect of recent maternal stress on predominant fetal hand use during self-touch was ascertained for the first time. Reissland et al.55 assessed whether subtle fetal movements observed by 4-D ultrasound differ between smoking and non-smoking mothers. Fetuses of smoking mothers showed a significantly higher rate of mouthing movements compared with those of non-smoking mothers, and these differences between the groups widened with advancing gestation. Differences between smoking and non-smoking mothers in the rate of fetal facial self-touch differed significantly, and remained constant during pregnancy. Lopez-Teijon et al.56 studied the fetal response to intravaginal musical stimuli using 4-D ultrasound between 14 and 39 GW. Intravaginal music was related to a higher occurrence of fetal mouthing movement and tongue expulsion. The frequency of tongue expulsion emitted with intravaginal music increased with advancing gestation. These authors suggest that neural pathways participating in the auditory-motor system are developed as early as at 16 GW.

Fetal Pain Painful stimuli can be perceived by the human brain at 20–22 GW.57 Most studies suggest the possibility of fetal pain in the third trimester of pregnancy.58 In some investigations, it was concluded that the human fetus can feel pain after 24 GW, and that the fetus may feel pain even before 24 GW.59,60 Reissland et al.61 suggested that healthy fetuses progress towards an increasingly complete pain/distress expression as they mature. These authors argued that the increasing frequency of fetal pain/distress with advancing gestation might be an adaptive process, being beneficial to the fetus after birth to obtain his/her parents’ love.

Fetal Consciousness, Awareness, and Emotion Does the human fetus have a consciousness, awareness, or emotion? This question is very interesting, but has not been answered.7 Kurjak et al.62 suggest the ability of 4-D ultrasound to demonstrate different facial expressions and movements, which may represent fetal awareness. In other words, fetal facial

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expressions and movements depicted by 4-D ultrasound may be able to be used as a sign of fetal awareness. In a previous study, 4-D ultrasound was used to assess arm/hand motions toward the face involving 27 human fetuses at 19–35 GW.63 Either directly or indirectly, greater than 50% of the arm movements culminated in the hand touching the mouth. Also, the fetuses opened their mouths prior to hand contact. This suggests that the human fetus understands how to move his/her hand to touch their mouth. In another 4-D ultrasound-based study, hand movements toward the mouth and eyes were assessed in eight singleton fetuses at 14, 18, and 22 GW, in order to examine if such movements are planned and how they are performed.64 It was suggested the fetuses understood that the mouth is bigger and less delicate than the eye by 22 GW. Thus, the fetus may have learned that the eye is smaller and more delicate, suggesting the presence of somatosensory sensitivity by 22 GW. At 22 GW, the movements were recognizably intentional, indicating advanced motor planning. Employing 4-D ultrasound at 14 and 18 GW in five pairs of twin fetuses, kinematic movement profiles were assessed.65 The movement duration and deceleration time were prolonged for other-directed movements compared with those targeting the wall of the uterus. Regarding movements directed towards the co-twin and those self-directed, targeting the eye-region, similar kinematics were noted. It was concluded that such movements aimed at the co-twin were planned, and so twin fetuses performed movements specifically aimed at the co-twin from the 14th GW. Namely, one of the twin fetuses may recognize the other twin as a human being, and behave based on this recognition from an early stage of pregnancy.7 Using 4-D ultrasound, Marx and Nagy66 examined fetal responses to the mother’s voice and maternal touch of the abdomen compared with a control condition. Arm, head, and mouthing movements increased when the mother touched her abdomen, with a decrease in arm and head movements in response to the mother’s voice. Fetuses in the third trimester showed regulatory (yawning), resting (crossing arms), and self-touch (hands touching body) responses to stimuli when compared with those in the second trimester. Kawakami and Yanaihara67 presented numerical data on fetal smiles using 4-D ultrasound. The fact that fetuses smile numerous times in the womb may change our attitude toward them, especially for the parents.

© 2016 Japan Society of Obstetrics and Gynecology

Fetal neurodevelopmental assessment

Conclusions With the advent of 4-D ultrasound, new scientific fields have developed, such as ‘fetal neurology’ or ‘fetal psychology,’ heralding the dawn of a new era in fetal neurobehavioral science.7 The results of 4-D ultrasound may reflect normal and abnormal fetal neurological development, allowing more accurate assessments of fetal neurobehavioral development and maturation, most notably fetal brain and CNS functions. New fetal neurobehavioral functions and inter-human relationships may also be identified with this modality.4 Our understanding of the fetal brain and CNS functions will be advanced through such fetal neurobehavioral or neurodevelopmental research.7 Now, larger studies are necessary to fully understand the present and future applications of 4-D ultrasound to fetal neurobehavior and neurodevelopment.68

Acknowledgments The work reported in this paper was supported by a Grant-in-Aid for Scientific Research on Innovative Areas ‘Constructive Developmental Science’ (No. 24119004) from the Ministry of Education, Culture, Sports, Science and Technology, Japan.

Disclosure The author declares no conflicts of interest.

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Current status of fetal neurodevelopmental assessment: Four-dimensional ultrasound study.

With the latest advent of four-dimensional (4-D) ultrasound, fetal neurobehavioral or neurodevelopmental assessment can be easily and readily performe...
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