INTRODUCTION
The brain is a 3D structure and should be assessed in three basic planes: Sagittal, coronal, and axial sections. Transvaginal observation of the fetal brain offers sagittal and coronal views of the brain from fetal parietal direction through the fontanelles and/or the sagittal suture as ultrasound windows. This method has contributed to the prenatal assessment of congenital CNS anomalies and acquired brain damage in utero.
Three-dimensional ultrasound is one of the most attractive modality in the field of fetal ultrasound imaging. By recent advances of 3D HDlive, HDlive silhouette, and HDlive flow, the brain morphology and vascular structure can be demonstrated more objectively and accurately.
Combination of transvaginal approach and 3D ultrasound technologies provides us more and more information of fetal brain development, congenital anomalies as well as intrauterine acquired injuries.
TRANSVAGINAL APPROACH TO FETAL BRAIN
Imaging technologies have been remarkably improved and contributed to prenatal evaluation of fetal CNS development and assessment of CNS abnormalities in utero.
Conventional transabdominal ultrasonography, by which it is possible to observe fetuses through maternal abdominal wall, uterine wall, and sometimes placenta, has been most widely utilized for antenatal imaging diagnosis. By transabdominal approach, whole CNS of fetuses can be well demonstrated; for instance, the brain in the axial section and the spine in the sagittal section. However, transabdominal approach to the fetal CNS has several obstacles, such as maternal abdominal wall, placenta, and fetal cranial bones, and it is difficult to obtain clear and detailed images of fetal CNS structure.
High-frequency transvaginal transducer has contributed to establishing “sonoembryology,”1 and recent general use of transvaginal sonography in early pregnancy enabled early diagnoses of various fetal anomalies.2 In the second and third trimesters, fetal brain scan is generally evaluated through maternal abdominal wall and mostly fetal brain is demonstrated in the axial section. The brain, however, is a 3D structure and should be assessed in three basic planes: Sagittal, coronal, and axial sections. Sonographic assessment of the fetal brain in the sagittal and coronal sections requires an approach from fetal parietal direction. Transvaginal sonography of the fetal brain opened a new field in medicine, “neurosonography.”3 Transvaginal approach to the normal fetal brain during the second and third trimester was introduced in the beginning of the 1990s. It was the first practical application of 3D CNS assessment by two-dimensional ultrasound.4 Transvaginal observation of the fetal brain offers sagittal and coronal views of the brain from fetal parietal direction5-8 through the fontanelles and/or the sagittal suture as ultrasound windows. Serial oblique sections3 via the same ultrasound window reveal the intracranial morphology in detail. Transvaginal approach to the fetal brain has contributed to the prenatal assessment of brain morphology.
TRANSVAGINAL 3D NEUROSCAN
Three-dimensional ultrasound is one of the most attractive modality in the field of fetal ultrasound imaging. Automatic scan by dedicated 3D transducer produces motor-driven automatic sweeping and is called as a fan scan. With this method, a shift and/or angle change of the transducer is not required during scanning, and the scan duration needs only several seconds. Immediately after acquisition of the targeted organ, multiplanar imaging analysis and tomographic imaging analysis are possible. Combination of both transvaginal sonography and 3D ultrasound9-14 (Fig. 1) may be a great diagnostic tool for evaluation of 3D structure of fetal CNS. Recent advanced 3D ultrasound equipments have several useful functions, such as surface anatomy imaging; multiplanar imaging of the intracranial structure (Fig. 2); tomographic ultrasound imaging of fetal brain in the any cutting section (Fig. 3); bony structural imaging of the calvaria (Fig. 4) and vertebrae; thick slice imaging of the intracranial structure; simultaneous volume contrast imaging of the same section or vertical section of fetal brain structure; volume calculation of target organs, such as intracranial cavity, ventricle, choroid plexus, and intracranial lesions; and 3D sonoangiography of the brain circulation (3D power or color Doppler).
Figure 5 demonstrates tomographic ultrasound imaging of the fetal ventriculomegaly at 18 weeks in the sagittal and axial sections. Parallel sectional imaging similar to magnetic resonance imaging is quite helpful for evaluation of the brain structure. From a single volume dataset, any cutting section can be extracted. For example, bilateral enlarged ventricles, foramen of Monro, and the third ventricle can be exactly demonstrated in a single cutting section, as shown in Figure 6. By inversion mode (Fig. 7), those structures are depicted with more 3D appearance.
HDlive AND SILHOUETTE ULTRASOUND IN FETAL NEUROLOGY
The great achievement in the field of 3D/four-dimensional (4D) ultrasound is HDlive technology.15 This technology is a novel ultrasound technique that improves the 3D/4D images. HDlive uses an adjustable light source and software that calculates the propagation of light through surface structures in relation to the light direction.16 The virtual light source produces selective illumination, and the respective shadows are created by the structures where the light is reflected. There have been several reports on HDlive demonstration of fetal surface.17-20 By use of HDlive of fetal brain, intraventricular morphology, such as choroid plexus is clearly demonstrated as shown in Figure 8. In a case of intraventricular hemorrhage, coagula can be observed (Fig. 9).
Fig. 5
Tomographic ultrasound imaging of the fetal ventriculomegaly at 18 weeks in the sagittal and axial sections
Fig. 6
An anterior coronal cutting section extracted from brain volume dataset (same case as Fig. 5). Bilateral enlarged ventricles, foramen of Monro (M), and the third ventricle (3rd) can be exactly demonstrated
Fig. 7
Ventricular system by inversion mode in a case of ventriculomegaly at 18 weeks. Bilateral enlarged ventricles, foramen of Monro (M), and the third ventricle (3rd) can be exactly demonstrated
Fig. 8
Inside view of enlarged ventricle by HDlive imaging (same case as Fig. 7). Appearance of choroid plexus (CP) and smooth ventricular wall is well demonstrated
Applications of HDlive silhouette and HDlive flow21 were introduced at the end of 2014. Algorithm of HDlive silhouette creates a gradient at organ boundaries, fluid-filled cavity, and vessels walls, where an abrupt change of the acoustic impedance exists within tissues.21-24 The examiner can adjust HDlive silhouette percentage with controlling threshold and gain simultaneously for visualizing target organs of interest. HDlive silhouette emphasizes the borderlines between organs with different echogenicity; therefore, both the target of interest floating within fluid correction and cystic area in echogenic organs are simultaneously demonstrated. By HDlive silhouette mode, an inner cystic structure with fluid collection can be depicted through the outer surface structure of the body and it can be appropriately named as “see-through fashion.”21-26 Silhouette ultrasound shows comprehensive structure demonstrating inner and outer morphology simultaneously. Figure 10 shows enlarged ventricular system by silhouette ultrasound in a case of Dandy—Walker malformation at 16 weeks. Bilateral enlarged ventricles as well as third ventricle and enlarged fourth ventricle are clearly demonstrated inside intracranial volume. Three-dimensional orientation of ventricular system is easily understandable. Figure 11 is the frontal view of ventricular system in a case of ventriculomegaly at 18 weeks. Three-dimensional location of enlarged bilateral ventricles, third ventricle, and foramen of Monro is demonstrated comprehensively. Lateral view (Fig. 12) of the same case demonstrates the location of choroid plexus and foramen of Monro.
Figs 9A and B
Inside view of enlarged ventricle by HDlive imaging in a case of intraventricular hemorrhage: (A) Single parasagittal cutting section; and (B) inside view of enlarged ventricle with coagula (arrows)
Fig. 10
HDlive silhouette imaging of ventriculomegaly in a case of Dandy—Walker malformation at 16 weeks. Bilateral enlarged ventricles as well as third ventricle (3rd) and enlarged fourth ventricle (4th) are clearly demonstrated inside intracranial volume
Fig. 11
HDlive silhouette imaging of ventriculomegaly, frontal view. Bilateral enlarged ventricles, foramen of Monro (M), and the third ventricle (3rd) can be exactly demonstrated
Fig. 12
HDlive silhouette imaging of ventriculomegaly, lateral view. The volume demonstrates the location of choroid plexus (CP) and foramen of Monro, and the third ventricle (3rd)
Although silhouette ultrasound neuroimaging is quite helpful, it occasionally seems to demonstrate too many inner structures overlapping one another to understand their relations inside cranial volume. The author has cut the volume dataset with a rectangle cube and rendered the cut slice with silhouette ultrasound and called this silhouette ultrasound demonstration of thick slice of 3D volume dataset as “thick-slice silhouette.”27 Frontal/occipital ventriculomegaly at 19 weeks by the thick-slice silhouette images from the same 3D volume dataset are shown in Figure 13.
Figs 13A and B
Ventriculomegaly at 19 weeks imaged by the thick-slice silhouette images: (A) Anterior coronal cutting section; and (B) posterior coronal cutting section
Figs 14A to D
Difference of angiostructure by 3D sonoangiogram in normal and abnormal cases. (A) Normal sagittal cutting section. The corpus callosum is demonstrated. (B) The same cutting section in a case of agenesis of the corpus callosum (AOCC). (C) Typical radial sulcus formation is seen instead of normal cingulate sulcus and gyrus formed with normal development of the corpus callosum. Angiostructure by 3D power Doppler. Normal callosomarginal artery (CMA) is clearly demonstrated. (D) Angiostructure of AOCC. The CMA does not exist and radial formation of the branches of anterior cerebral arteries (ACA) is seen
BRAIN VASCULAR IMAGING
Cerebral vascularity has been demonstrated three-dimensionally, as shown in Figures 14 and 15, for more than a decade. Recent technology has added HDlive flow,24,25 which provides 3D view of the blood flow with a realistic rendering of fine vascular structure. Combination of HDlive silhouette and HDlive flow can be described as a “see-through fashion”24,26,28 because of its comprehensive orientation and persuasive localization of inner structure as well as of fetal angiostructure inside the morphological structure. Figure 16 demonstrates normal intracranial angiostructure by 3D HDlive silhouette/flow imaging with power Doppler at 18 weeks of gestation. Fine venous vascular structure, such as medullary veins can also be well demonstrated by HDlive flow imaging between pia mater and subependymal zone (Fig. 17).
Fig. 15
Three-dimensional B-flow view of vein of Galen aneurysmal malformation (VGAM). Dilated vein of Galen and straight sinus, and arteriovenous shunts are clearly seen
FUTURE ASPECT
Neuro-sonoembryology and neurosonology have been established by transvaginal 3D neuroimaging. By utilizing 3D ultrasound, HDlive, and HDlive silhouette imaging, further detailed information of fetal brain can be obtained.
Up-to-date 3D technologies described in this study allow extending the detection of congenital brain maldevelopment, and it is beyond description that noninvasive direct viewing of the embryo/fetus by all-inclusive ultrasound technology is definitely the first modality in a field of fetal neurology and help our goal of proper perinatal care and management, even in the era of molecular genetics and advanced sequencing of fetal DNA in the maternal blood.26,28
As a future aspect, collaboration of both molecular genetics and 3D neuroimaging will reveal responsible gene mutation of neuronal migration disorder, and this fetal neuro-sono-genetics will be able to contribute to accurate diagnoses, proper management, possible genetic therapy, and prophylaxis.