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Ultrasound in obstetrics and gynaecology
Fig. 14.7 Acquisition with STIC and surface mode rendering can be used at the level of the heart to visualize the spatial appearance of the heart cavities.
266
Fig. 14.8 Maximum mode rendering is used to visualize the fetal skeleton; here the bony face with the nasal bones and the metopic suture (left), the skull from the side with skull sutures (middle), and the fetal spine with the scapulae, long bones and pelvis (right).

MINIMUM MODE RENDERING

This mode is used to highlight the hypoechoic structures in the volume of inter­est and to demonstrate a 3D projection of vessels, cysts, bladders and others that appear black against a surrounding of more echogenic tissue (Fig. 14.9). It is pref- erable to make the rendering box narrow in order to focus on the region of inter­est. Within the box, the presence of amniotic fluid should be avoided as it casts a large black shadow. Images produced with this technique are similar to x-ray projection. Regions of interest are mainly the stomach (see Fig.14.9 right), the bladder, the brain ventricles and the heart with the corresponding vessels.
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Fig. 14.9 Minimum mode rendering demonstrating in the left and middle images the abdomen with bladder (BL), gallbladder (GB), umbilical vein (UV), stomach (ST), inferior vena cava (VCI) and aorta (AO). On the right, as comparison, a double bubble sign observed at 24 weeks in duodenal atresia.

INVERSION MODE RENDERING

This display mode inverts the colour of the anechoic information (similar to neg­ative/positive film), thus presenting the hypoechoic structures as echogenic sol-
12,13
ids.
It blackens most of the surrounding tissue information (Fig. 14.10). By changing certain preset parameters, the image can be improved. This technique was also called negative surface display and it was discovered that the images pro­duced were similar to postmortem casting. Artifacts may result from rib shadow­ing or from amniotic fluid, etc., but can be eliminated using the electronic scalpel during offline volume manipulation.
Three-dimensional and four-dimensional ultrasound application in prenatal diagnosis
Fig. 14.10
on 2D in a longitudinal view in a fetus with spina bifida. (Left bottom) Inversion mode demonstrating the shape of the dilated ventricles in the same fetus. The black areas are the lack of information of the choroid plexus. (Middle) A fetal bladder with dilated ureter and hydronephrosis. (Right) Inversion mode demonstrating the heart and the crossing of the great vessels.
Inversion mode in different fetal conditions. (Left top) A dilated ventricle
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The role of this technique has been analysed in visualizing cardiac and extra­cardiac fluid-filled structures in the fetus. Application fields are not only the heart and vessels (see Fig. 14.10 right) but also kidneys in hydronephrosis (see Fig. 14.10 middle), brain ventricles (see Fig. 14.10 left) and other hypoechoic cystic struc­tures. Regions of interest in the fetus could be the fluid-filled structures as the stomach, the urinary bladder or gallbladder. The shape of the stomach and duode­num in the presence of a double bubble in duodenal atresia could be a clinically important application. The kidneys can mainly be demonstrated in anteroposte­rior longitudinal projection and clinical benefit can be found in multicystic kidneys and hydronephrosis. Intracranial brain structures, especially the lateral ventricles in early pregnancy, can be clearly demonstrated and malformations with disturbed anatomy of the lateral ventricles can be seen with inversion mode.
One of the major fields of interest with inversion mode is the cardiovascular system. The examiner can visualize the heart and vessels in a manner similar to 3D power Doppler ultrasound at a better resolution and with a more rapid acqui­sition rate. Particularly easily demonstrated is the crossing of the vessels of the heart or the relationship of the ventricles and their size. The main advantage of
Ultrasound in obstetrics and gynaecology
this technique is that the image is similar to the one acquired by power Doppler but without the difficulties encountered in adjusting the image. The volume can be acquired in grey scale as 3D static or as a STIC, at a high frame rate and reso­lution, whereas volumes with power Doppler information are at low frame rates and subject to movement artifacts. Thus, the image quality with inversion mode is superior to the quality obtained by power Doppler; however, it lacks the informa­tion of neighbouring tissue demonstrated in the glass body mode. Since inversion mode can also be used for volume calculation, it could be more easily used to calcu­late volumes of structures with irregular shape than with the VOCAL technique.
268

GLASS BODY MODE RENDERING

This mode is used to demonstrate a volume with grey scale and colour or power Doppler information simultaneously. The acquisition can either be achieved as static 3D or as a STIC. Volume data can be displayed in three ways: the colour information alone, the grey-scale information alone or a combination of both as a so-called ‘glass body’ mode (Fig. 14.11). A prerequisite for a good volume is the optimal presetting of the colour during 2D scan before acquiring a volume. One of the main application fields of this mode is the demonstration of the cardiac chambers and the great vessels14 (see Fig. 14.11). Peripheral vessels such as the umbilical cord (see Fig. 14.11), intra-abdominal, thoracic and brain vessels can be well demonstrated.

VOLUME CALCULATION

Biometry is an integral part of the antenatal ultrasound examination and has been achieved for years by measuring distances, circumferences and areas. The acquisi­tion of a 3D volume data set allows easy reconstruction of a selected 2D plane to
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Fig. 14.11 Glass body mode. On the left, a longitudinal view of the brain with vessels (pericallosal artery and ramifications). In the middle, the heart and the great vessels from a STIC volume. On the right, the posterior placenta demonstrating the central insertion of the umbilical vessels.
perform well-known measurements such as nuchal translucency, biparietal diam­eter or femur length, but also offers the potential to accurately calculate the vol­ume of a selected region of interest. Volume measurements can be achieved using either the multiplanar mode or the VOCAL™ software (VOlume CALculation). Recently, another possibility has been developed for liquid-filled structures involv­ing the threshold principle in combination with the inversion mode. Volume mea­surements are still time-consuming and thus limited to research purposes. Volume measurements and charts were reported for the placenta, the amniotic cavity, the first trimester fetus, the fetal brain, liver and arm, but there was a special inter­est in measuring fetal lung volume.
15,16
Fields of interest in these measurements focused chiefly on the detection of difference in volume in pregnancies compli­cated by chromosomal anomalies, diabetes, intrauterine growth restriction and congenital diaphragmatic hernia.
Three-dimensional and four-dimensional ultrasound application in prenatal diagnosis

CONCLUSION

Three-dimensional ultrasound application in prenatal diagnosis should not be limited to the demonstration of the fetal face to please the parents. The concept of volume ultrasound demonstrated in this chapter enables the acquisition of a digital volume data set and the display of the information in different ways. The different display modes available can be used for the demonstration of the spatial appearance of surface structures as well as the projection of bony structures for a better understanding of skeletal and other findings. The multiplanar mode and tomographic imaging allow the reconstruction of planes not directly seen on the screen and offer new insight into fetal anatomy similar to images now demon­strated by MRI for brain structures.
The numerous enthusiastic articles on 3D written in recent years confirm that we are rapidly moving from the era of ‘sonography in 2D planes’ to ‘volume ultrasound’. New rendering modes and clinical features will appear in the near future and the development of faster processors in computer technology will enable the advent of matrix transducers with the possible instant application of these techniques.
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References

1. Chaoui R, Heling KS. Three-dimensional ultrasound in prenatal diagnosis. Curr Opin Obstet Gynecol 2006;18:292–302
2. Devore GR, Falkensammer P, Sklansky MS, Platt LD. Spatio-temporal image correlation (STIC): new technology for evaluation of the fetal heart. Ultrasound Obstet Gynecol 2003;22:480–487
3. Chaoui R, Heling KS. New developments in fetal heart scanning: three- and four­dimensional fetal echocardiography. Semin Fetal Neonatal Med 2005;10:567–577
4. Benacerraf BR, Shipp TD, Bromley B. How sonographic tomography will change the face of obstetric sonography: a pilot study. J Ultrasound Med 2005;24:371–378
5. Vinals F, Mandujano L, Vargas G, Giuliano A. Prenatal diagnosis of congenital
Ultrasound in obstetrics and gynaecology
heart disease using four-dimensional spatio-temporal image correlation (STIC) telemedicine via an Internet link: a pilot study. Ultrasound Obstet Gynecol 2005;25:15–31
6. Benoit B. The value of three-dimensional ultrasonography in the screening of the fetal skeleton. Child's Nerv Syst 2003;19 (7–8):403–409
7. Dikkeboom CM, Roelfsema NM, Van Adrichem LN, Wladimiroff JW. The role of three-dimensional ultrasound in visualizing the fetal cranial sutures and fontanels during the second half of pregnancy. Ultrasound Obstet Gynecol 2004;24:412–416
8. Benoit B, Chaoui R. Three-dimensional ultrasound with maximal mode rendering: a novel technique for the diagnosis of bilateral or unilateral absence or hypoplasia of nasal bones in second-trimester screening for Down syndrome. Ultrasound Obstet Gynecol 2005;25:19–24
9. Chaoui R, Levaillant JM, Benoit B, Faro C, Wegrzyn P, Nicolaides KH. Three­dimensional sonographic description of abnormal metopic suture in second- and third-trimester fetuses. Ultrasound Obstet Gynecol 2005;26:761–764
10. Faro C, Chaoui R, Wegrzyn P, Levaillant JM, Benoit B, Nicolaides KH. Metopic suture in fetuses with Apert syndrome at 22–27 weeks of gestation. Ultrasound Obstet Gynecol 2006;27:18–33
11. Faro C, Wegrzyn P, Benoit B, Chaoui R, Nicolaides KH. Metopic suture in fetuses with holoprosencephaly at 11 + 0 to 13 + 6 weeks of gestation. Ultrasound Obstet Gynecol 2006;27(2):162–166
12. Lee W, Goncalves LF, Espinoza J, Romero R. Inversion mode: a new volume analysis tool for 3-dimensional ultrasonography. J Ultrasound Med 2005;24:201–207
13. Benacerraf BR. Inversion mode display of 3D sonography: applications in obstetric and gynecologic imaging. Am J Roentgenol 2006;187(9):965–971
14. Chaoui R, Schneider MBE, Kalache KD. Right aortic arch with vascular ring and aberrant left subclavian artery: prenatal diagnosis assisted by three-dimensional power Doppler ultrasound. Ultrasound Obstet Gynecol 2003;22:661–663
15. Moeglin D, Talmant C, Duyme M, Lopez AC. Fetal lung volumetry using two- and three­dimensional ultrasound. Ultrasound Obstet Gynecol 2005;25:219–227
16. Peralta CF, Cavoretto P, Csapo B, Falcon O, Nicolaides KH. Lung and heart volumes by three-dimensional ultrasound in normal fetuses at 12–32 weeks' gestation. Ultrasound Obstet Gynecol 2006;27(2):128–133
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Fetal movement patterns and behavioural states

Gerard H A Visser Eduard J H Mulder
ABSTRACT
Fetal movements appear early in pregnancy, are from their inception specific and closely resemble movements after birth. This makes them candidates for diagnostic purposes. In this chapter the normal development of fetal motor patterns and of behavioural states is discussed and clinical implications of altered behaviour are emphasized.
KEYWORDS
Fetal behaviour, fetal monitoring, fetal movements, maternal diseases, medication.

INTRODUCTION

Ultrasound in obstetrics focuses on morphology and Doppler waveform patterns of fetal and maternal vessels. Fetal motility usually gets less attention. However, some knowledge regarding incidence, quality and periodicity of fetal movement patterns is necessary in order to:
obtain insight into normal developmental aspects of nervous system
•
functioning (and related phenomena such as fetal heart rate patterns, Doppler flow profiles and fetal micturition) identify situations with a negative impact on nervous system development and
•
identify individual fetuses with abnormal brain or neuromuscular
•
functioning.
In this chapter the normal development of fetal motor patterns and of fetal sleep or behavioural states is discussed and clinical implications of altered behaviour are emphasized.
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METHODOLOGY

Observation of fetal movements can best be done by using a real-time linear array transducer with a long probe (>9 cm) or a curved array transducer, with a high frame rate (>30 pictures per second). One transducer is sufficient until about 20 weeks of gestation, but thereafter two transducers are necessary if it is intended to observe all movement patterns. Also, for the recording of fetal behavioural states, two transducers are necessary: one for the observation of body movements and one for eye movements.
Due to the episodic occurrence of the different movement patterns and the development of fetal behavioural states, it is necessary to make relatively long observations (0.5–2 h). With a recording of 1 hour's duration and a spatial peak temporal average of the equipment of 0.4 mw/cm2, the product of intensity and exposure time is 1.4 J/cm2, which is far below the accepted 50 J/cm2.

THE EMERGENCE OF FETAL MOVEMENT PATTERNS

Ultrasound in obstetrics and gynaecology
Endogenously generated (i.e. spontaneous) fetal movements can first be observed after 7 weeks postmenstrual age (i.e. 5 weeks after conception).8 At this early age these movements are difficult to classify because of the small size of the embryo (1–2 cm) and the limited resolution of the ultrasound equipment. All types of movements emerging after 8 weeks are, however, specific and easily recogniz­able. Surprisingly, all these early emerging movements closely resemble those
272
observed in preterm and full-term newborn infants, which makes it possible to classify them accordingly. ment patterns and at 15 weeks of gestation 12 distinct patterns can already be distinguished (startle, general movements, hiccup, breathing, isolated arm or leg movement, isolated retroflexion/rotation and anteflexion of the head, jaw move­ments, sucking and swallowing, hand–face contact, stretch, yawn, body rotation). The developmental profile of these movements plotted according to their first appearance in a group of 12 normal fetuses is shown in Figure 15.1. In addition, slow eye movements can be observed from 18 weeks onwards, while rapid eye movements emerge somewhat later. present during the course of pregnancy and their appearance hardly changes. All these data were obtained in the early 1980s with the equipment available at that time, but are still unchallenged.
This early emergence of highly organized, specific movement patterns, long before birth, seems surprising, even more so when the minimal development of the nervous system at that age is taken into account. Studies on the ultrastructure of the nervous system of the young fetus are still scarce. The available data sug­gest, however, that movements commence as soon as the first connective struc­tures are formed.
8
The reason why the different movement patterns emerge so early is still unclear. Certain movement patterns have an adaptive effect on the survival or development of the fetus. Frequent and active changes of the intrauterine
8,32
There is an early emergence of different move-
5,15
These movements, once observed, remain
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Just discern. mov.
Startle
General mov.
Hiccup
Isol. arm mov.
Isol. leg mov.
Head retroflexion
Head rotation
Hand–face contact
Breathing mov.
Jaw opening
Stretch
Head anteflexion
Yawn
Sucking+swallow.
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weeks
Fetal movement patterns and behavioural states
Fig. 15.1 Timetable of emergence of specific movement patterns in a longitudinal study of 12 fetuses. Each dot indicates the first observation of a particular pattern in an individual from the weekly observation. Postmenstrual age is given in weeks and days (reproduced from reference 1, with permission).
position may prevent adhesions and local stasis of the circulation of the skin. Individual movements may prevent the occurrence of contractures, as can be found after prolonged oligohydramnios following leakage of amniotic fluid. Sucking and swallowing movements are necessary for the regulation of the amount of amniotic fluid. Another reason for the early emergence of fetal movements is anticipation of postnatal functions. Some motor patterns emerge during early prenatal development and are regularly performed spontaneously long before they fulfil a meaningful task as part of a complex adaptive function. For example, fetal breathing movements are already present at 10 weeks. These movements might also have a profound influence on lung growth, as in animal experiments spinal cord transection results in fetal lung hypoplasia;18 however, this link is still unclear in the human.
The frequent occurrence of many specific movements during the first trimester of pregnancy can be depicted in a complex actogram, as is shown in an example of a 1-hour recording at 13 weeks (Fig. 15.2). At all ages there are large interindi- vidual differences in the incidence of the various types of movements.9 There are, however, specific developmental trends in the quantity (incidence) of the various types of movements. For example, the incidence of general movements increases rapidly until a plateau is reached at 10 weeks (about 12% of recording time), with a slight fall towards term age. The incidence of startles and hiccups declines
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Startle
General mov.
Hiccup
Isol. arm mov.
Isol. leg mov.
Head retroflexion
Head rotation
Head anteflexion
Hand–face contact
Breathing mov.
Jaw opening
Stretch
Yawn
Minutes 03060
13 weeks
Sucking+swallow.
Ultrasound in obstetrics and gynaecology
274
Fig. 15.2 Compiled actogram of 1 h observation of a fetus at 13 weeks of gestation. Note the periodicities and the multitude of specific movement patterns (data extracted from references 1 and 6, with permission).
after 12 weeks of gestation, while breathing movements gradually increase until 30 weeks; at the latter age breathing movements are on average present during 30% of recording time.
9,36

BODY MOVEMENTS IN NORMAL PREGNANCY

Several authors have reported on the incidence of fetal body movements. However, because of the absence of a uniform definition and differences in study design and data analysis, the reported mean/median values and ranges of normality differ greatly among the various studies.
Figure 15.3 shows nomograms of four incidence parameters of fetal body
movements from 24 weeks till term. These data are from a longitudinal study in 29 normal fetuses. Fetal movements were recorded serially for 60 minutes at fortnightly intervals between 24 weeks and 36 weeks of gestation and for 120 minutes weekly from 36 weeks until delivery. Body movements which
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Percentage of fetal movementsMean duration of fetal movements (sec)
Median interval duration (sec) Number of fetal movements per hour
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32 34 36 38 40 42
24 26 28 30 32 34 36 38 40 42
24 26 28 30 32 34 36 38 40 42
Fetal movement patterns and behavioural states
Fig. 15.3 Nomograms of the four incidence parameters of fetal body movements. Presented are the median (solid line), 2.5th and 97.5th centiles (dashed lines), and individually measured values in relation to gestational age for (A) the percentage of time spent making body movements, (B) the number of body movements per hour, (C) their mean duration, and (D) the median onset–onset interval (reproduced from reference 8, with permission).
occurred within 1 second apart were considered as a single burst of movement. The duration of individual fetal body movements remained stable with gesta­tion whereas the onset–onset interval increased, resulting in a gradual decline in the number of movements per hour. The median percentage incidence of fetal body movements decreased from 17% at 24 weeks to about 7% near term. This overall decline in incidence appears to be a developmental phenomenon, rather than the result of developing sleep states, since the declining trends are similar during ‘active’ and ‘quiet’ sleep.40 There is some degree of intrafetal consistency in the incidence of body movements, but intra- (and inter-) fetal variances are generally high, for instance much higher than those for fetal heart rate and its variation.
The incidence of fetal body movements is the same for boys and girls.35 Maternal meals do not affect the incidence of body movements. During the second half of gestation there is a diurnal variation in the incidence of general movements, with peak values occurring around midnight.34 This diurnal rhythm as well as those in fetal heart rate variation is related to maternal adrenal activity (cortisol).
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