PRENATAL DIAGNOSIS Prenat Diagn 2009; 29: 326–339. Published online 10 November 2008 in Wiley InterScience (www.interscience.wiley.com) DOI: 10.1002/pd.2146 REVIEW Normal sonographic development of the central nervous system from the second trimester onwards using 2D, 3D and transvaginal sonography Ana Monteagudo* and Ilan E. Timor-Tritsch Division of Obstetrical and Gynecological Ultrasound, Department of Obstetrics and Gynecology, Professor of Obstetrics and Gynecology, NYU School of Medicine, 530 First Avenue NB9N26, New York, NY 10016, USA The developmental changes of the fetal central nervous system (CNS) during the second and third trimesters, specifically the brain, relate mostly to changes in size. However, other changes do occur in the fetal brain during the second and third trimester such as: the union of the cerebellar hemispheres, development of the corpus callosum (CC), and increasing complexity of the cerebral cortex. These changes follow a well-defined developmental timeline recognizable by sonography. The fetal neuroscan can be divided into a ‘basic scan’ which is performed transabdominally and a ‘targeted Exam or neurosonogram’ which uses a multiplanar approach, which preferably should be performed transvaginally. During the ‘basic scan’, several brain structures are imaged in addition to obtaining important biometric measurements. The ‘neurosonogram’ is a more extensive or detailed fetal study during which the emphasis is on the addition of coronal and sagittal planes. The easiest way to obtain these planes, if the fetus is in a cephalic presentation, is the transvaginal route. Three-dimensional (3D) sonography should, if possible, be performed transvaginally using the multiplanar approach. An added benefit of 3D sonography is the ability to display and render the volume in a variety of ways which may enhance the detection of pathology. Copyright 2008 John Wiley & Sons, Ltd. KEY WORDS: neurosonography; transvaginal sonography INTRODUCTION drawback of the transvaginal technique was that the axial plane could rarely be imaged and that serial sections had to be obtained one at a time. At present, volume scanning Sonography is the best and most used tool to docu- (3D sonography) allows us to scan transabdominally or ment, study and understand the anatomy, pathology and transvaginally, obtaining images in all three classic scan- developmental changes of the fetal central nervous sys- ning planes and thus giving us the ability to view the tem (CNS). Over the past 30 years, as the technology brain through serial sections in all three classic planes has evolved so has our understanding and our ability as well as in any other desired planes of our choice to image the fetal brain. When the first ultrasound (US) (Monteagudo et al., 2000). In addition, several post- machines were introduced, the bony skull was the first to processing features assist us in highlighting pathology be imaged; this enabled the development of nomograms that may not be otherwise obvious. Therefore, in current of fetal growth. Since at that time only transabdomi- obstetrical scanning, especially as it relates to the fetal nal probes were used, the fetal brain was studied using CNS, multiple technical approaches are simultaneously only or mostly the axial planes. One major draw back used (i.e. 2D and 3D transabdominal and transvaginal was that as the gestational age increased, the density sonography). (ossification) of the cranial bones increased; therefore, the hemisphere close to the transducer appeared blurred permitting to study mainly the hemisphere distal to the probe which was clearly imaged. The introduction of the THE FIRST TRIMESTER transvaginal probes allowed us to place the transducer in close proximity to the head and obtain coronal and sagit- tal views through the acoustic window provided by the A detailed description of the CNS in the first trimester is fontanels and sutures. This way both hemispheres could not the central topic of this review; however, before we be seen simultaneously (Monteagudo et al., 1991). The proceed several important issues about the development of the CNS necessary to set the stage for this review should be mentioned. *Correspondence to: Ana Monteagudo, Division of Obstetrical The first trimester ends at the 14th week of the and Gynecological Ultrasound, Department of Obstetrics and Gynecology, Professor of Obstetrics and Gynecology, NYU pregnancy. It is during this period of its development, School of Medicine, 530 First Avenue NB9N26, New York, NY that the CNS undergoes tremendous transformation. The 10016, USA. E-mail: [email protected] embryo starts as a flat disc that undergoes cranial, Copyright 2008 John Wiley & Sons, Ltd. Received: 1 July 2008 Revised: 25 September 2008 Accepted: 25 September 2008 Published online: 10 November 2008 DEVELOPMENT OF THE CNS BEYOND THE FIRST TRIMESTER 327 lateral and caudal folding. This process is completed (BPD)] are performed. The three most clinically useful by approximately the 6th postmenstrual week. levels or sections at which the axial images are produced Using sonography, we can begin to examine the devel- are: transventricular, transthalamic and transcerebellar oping embryonic brain from the 7th postmenstrual week, (ISUOG Guidelines, 2007) (Figure 1). when the head becomes discernible from the rest of the body and the primitive embryonic ventricular system can • The landmarks for the transventricular axial plane be imaged. The 8th postmenstrual week reveals the four from anterior-to-posterior are as follows: the CSP, convoluted sequential sonolucencies in the embryonic flanked in each side by the anterior horns (AHs) head that correspond to the telencephalon, diencephalon, of the lateral ventricles; caudally the PHs of the mesencephalon and metencephalon. From approximately lateral ventricle, which contain the hyperechoic CPs. the 9th postmenstrual week, the fetal period begins and The walls of the ventricles are echogenic and are the falx cerebri and the choroid plexuses (CPs) in the clearly demarcated by the fluid contained within the lateral ventricles can be imaged; these are important ventricles. At this level, the lateral ventricles are landmark in the development of the CNS. measured at its widest part; at the level of the glomus. In this section, the CP is seen filling bilaterally the cavity of the ventricles. The calipers are placed SECOND AND THIRD TRIMESTER perpendicular to the axis of the ventricles touching DEVELOPMENTAL CHANGES OF THE FETAL the inner aspect. A measurement of up to 10 mm is BRAIN deemed normal (Almog et al., 2003) (Figure 1A). • Inferior to the transventricular plane, the transtha- The second trimester begins during the 14th week of lamic plane can be obtained. The landmarks from the pregnancy and extends through the 27th week of the anterior-to-posterior are: the frontal horns of the lat- gestation. During the second and the third trimesters, the eral ventricles, CSP, thalami and the hippocampal CNS slows its developmental pace. However, this period gyri (HG). It is at this level that most of the bio- is characterized by an unparalleled growth of the brain metric measurements of the head are obtained: BPD, volume; there is nearly a 40-fold increase in the weight head circumference (HC) and occipitofrontal diameter of the brain between the end of the embryonic period and (OFD) (Figure 1B). birth (O’Rahilly and Muller, 2008). In addition, some of • The transcerebellar axial plane is inferior to the the brain structures, which began their developmental transthalamic plane and is slightly tilted posteriorly to journey during the first trimester, continue to evolve or adequately image the posterior fossa. The landmarks change through the second and third trimester. Some from anterior-to-posterior are: frontal horns of the structures may not reach their full ‘mature state’ until lateral ventricles, CSP, thalami, cerebellum, and the several months after the birth of the infant. Changes that cerebello-peduncular cistern [cisterna magna (CM)]. occur in the fetal brain are: the union of the cerebellar A CM measuring greater than 10 mm is considered hemispheres, development of the corpus callosum (CC), abnormal; also considered abnormal is the lack of the cerebral cortex, which becomes thickly populated its visualization strongly suggesting a spinal defect by neuronal migration and more complex, the insula (Figure 1C). which becomes buried by the opercula. There is a backward projection of the occipital lobes and formation In contrast to the axial plane easily obtainable by of the posterior horns (PHs) of the lateral ventricles, transabdominal sonography, the coronal and sagittal development of gyri and sulci, and asymmetry of the planes are easier to obtain by transvaginal sonography; right and left hemispheres (O’Rahilly and Muller, 2008). that is, if the fetus is in cephalic presentation. However, Some of these changes can be imaged by US especially transabdominally the frontal suture can be used as an those that relate to the CC, cavum septi pellucidi (CSP), acoustic window to obtain the transfrontal view of the ventricular system, cerebellum, vermis, and finally the brain. This view can be use to image the median brain development of gyri and sulci. structures such as CC, CSP, and cerebellum (Visentin Before we go over the developmental changes that et al., 2001). This view can be routinely obtained during occur in the fetal brain during the second and third the screening anatomical scan; however, when a targeted trimesters of pregnancy,