Abstract
Cranial ultrasound is a valuable diagnostic tool with distinct advantages compared to alternative imaging modalities such as computed tomography (CT) and magnetic resonance (MR) imaging, particularly in the young child, including easy accessibility, relatively low cost, no radiation, and a short examination time. In this chapter, up-to-date imaging techniques, development and anatomy, and common disorders encountered in clinical practice are discussed, as well as rare and challenging but important diagnoses in the pediatric population. Inherent limitations of cranial ultrasound as well as common pitfalls are reviewed.
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Keywords
- Cranial
- Head
- Brain
- Scalp
- Transcranial Doppler ultrasound (TCD)
- Hypoxic–ischemic injury (HII)
- Periventricular/intraventricular hemorrhage (PIVH)
- Intracranial bleed
- Periventricular leukomalacia (PVL)
- TORCH
- Hydrocephalus
Introduction
Cranial ultrasound is a valuable screening and diagnostic examination with distinct advantages compared to alternative imaging modalities, particularly in the young child. These advantages include easy accessibility, relatively low cost, no radiation, and a short examination time.
In this chapter, up-to-date imaging techniques, anatomy, embryology, and disorders of the brain commonly encountered in clinical practice are discussed. Rare and challenging but important diagnoses are also presented along with limitations of cranial ultrasound and common pitfalls. A clear understanding of the imaging techniques and abnormalities detected by cranial ultrasound is of great utility in the care of pediatric patients with congenital and acquired cranial disorders.
Technique
Cranial ultrasound is the imaging modality of choice to screen for intracranial pathology in the young child. The advantages of ultrasound include easy accessibility, portability allowing for bedside imaging in critically ill patients, noninvasiveness, lack of radiation exposure, lack of sedation, and relatively low cost. Disadvantages of ultrasound compared to other imaging modalities such as computed tomography (CT) and magnetic resonance (MR) imaging are operator dependence and limited assessment of some intracranial structures, especially the extra-axial spaces along the convexities of the brain and the posterior fossa.
Sound waves penetrate osseous structures poorly; therefore, ultrasound imaging of the brain needs to be performed through acoustic windows such as the anterior and posterior fontanelles, the temporal window, mastoid fontanelle, and the foramen magnum.
The most common acoustic window used in clinical practice is the anterior fontanelle. It is the widest window and can be easily localized on physical examination as a soft spot along the anterosuperior aspect of the skull in the newborn. The anterior fontanelle begins to close at approximately 9 months of age and is completely fused by the end of the second year of life [1]. It closes later in patients with prematurity, trisomy 13, trisomy 18, trisomy 21, and/or underlying poor bone mineralization from conditions such as achondroplasia, osteogenesis imperfecta, rickets, congenital hypothyroidism, and increased intracranial pressure [2].
The posterior fontanelle closes much earlier than the anterior fontanelle, typically by 2–3 months of age [3]. The trans-mastoid approach behind the ear is generally accessible until the age of 1.5 years.
Patient Positioning
Cranial ultrasound is often performed at the bedside in the neonatal intensive care unit. When imaging through the anterior and posterior fontanelles, the infant is examined in a supine position. When imaging through the mastoid fontanelle, the head is turned either to the right or to the left and the ultrasound transducer is placed directly behind the ear. For transcranial Doppler (TCD) ultrasound studies, the patient is examined in either a supine position or sitting upright. Images are obtained anterosuperior to the ear through the temporal bone.
Ultrasound Transducer Selection
Optimal intracranial images are obtained with a small footprint, high-frequency phased array transducer with frequencies on the order of 5–8 MHz. A sector field of view allows deeper penetration through a small acoustic window and the ability to change the focus of the ultrasound beam.
In premature babies, a 7–10 MHz or higher phased array transducer can be used [4]. In term babies and young infants, a 3.5–5-MHz phased array transducer may be necessary [5]. A 7.5–12-MHz high-frequency linear array transducer is used to assess superficial structures in a midsagittal plane, such as the superior sagittal sinus and the extra-axial spaces, as well as the subcutaneous layer of the scalp. In addition to static grayscale images, cine clips are especially helpful for problem-solving, especially when images are obtained portably in the neonatal intensive care unit when the physician responsible for image interpretation may not be physically present.
Color and pulsed Doppler ultrasound imaging is useful in assessing the intracranial vasculature and in the evaluation of vascular anomalies. Three-dimensional (3D) ultrasound of the brain permits single sweep volumetric data acquisition. This technology offers the possibility of reconstructing images in different planes to further aid in the diagnosis of pathology of the neonatal brain [6].
Imaging Approaches
A standardized cranial ultrasound protocol should be followed in order to optimize the quality of examination and to ensure consistency of imaging between studies (Fig. 2.1). A series of coronal and sagittal images are obtained through the anterior fontanelle. Additional information can be obtained as needed by acquiring images through the posterior fontanelle, temporal bone, squamosal suture, mastoid fontanelle, and foramen magnum at the posterior craniocervical junction.
Centering the probe over the fontanelle is essential for the acquisition of symmetric images of the cerebral hemispheres. Multiple coronal images are obtained by angling anteroposteriorly with a rocking motion while maintaining contact with the anterior fontanelle.
Standard images of the brain are obtained in a series of coronal (line A-G) and sagittal (line H-K) planes through the anterior fontanelle. Each line corresponds to the following ultrasound images (Fig. 2.2a–k). FH, Frontal horn; BV, body of lateral ventricle; OH, occipital horn; TH, temporal horn; CB, cerebellum; CC, corpus callosum; CS, cavum septum pellucidum; 3, third ventricle; 4, fourth ventricle; choroid plexuses are in yellow
A minimum of seven coronal images are obtained from anterior to posterior as follows (Figs. 2.2a–g): (a) the first image is acquired of the frontal cortex, anterior to the anterior horns of the lateral ventricles; (b) the second image is through the anterior horns of the lateral ventricles and includes the suprasellar cistern at the skull base; (c) the third image is through the body of the lateral ventricles at the level of the paired foramina of Monro with the brainstem in the far-field; (d) the fourth image is through the posterior aspect of the third ventricle; (e) the fifth image is at the level of the quadrigeminal cistern; (f) the sixth image is through the atria of the lateral ventricles with visualization of the choroid plexus in each lateral ventricle; (g) the seventh and final image is through the parieto-occipital lobes, posterior to the lateral ventricles.
Normal ultrasound anatomy of the brain. Images correspond to the anatomical planes shown in Fig. 2.1. (a) Line A. Coronal grayscale ultrasound image through the orbitofrontal lobes (F). Orbits (O) are also seen. (b) Line B. Coronal grayscale ultrasound image through the frontal horns (asterisks) of the lateral ventricles. Frontal horns are bounded inferolaterally by the caudate nuclei (C) and superiorly by the corpus callosum (CC). Parallel echogenic lines of the cavum septum pellucidum (arrowheads) are seen dividing the right from left lateral ventricles. Anterior temporal lobes (T) are seen bilaterally beneath the Sylvian fissures (arrows). (c) Line C. Coronal grayscale ultrasound image through the lateral ventricles (asterisks) at the level of the paired foramina of Monro (arrowheads). Corpus callosum (CC) crosses the midline and is seen above the lateral ventricles. Echogenic choroid plexus is seen in the roof of the third ventricle (3), extending through the foramina of Monro, and along the floor of the lateral ventricles. Pons (P) and medulla (M) are partially visualized in the far-field. Temporal lobes (T) are seen beneath the Sylvian fissures (arrows). (d) Line D. Coronal grayscale ultrasound image through the posterior aspect of the third ventricle and body of the lateral ventricles (asterisks). The third ventricle (3) is slit-like. Echogenic choroid plexus (arrowhead) is noted in the roof of the third ventricle (3) and the floor of the lateral ventricles. Paired thalami (TH) and cerebral peduncles (CP) are seen(e) Line E. Coronal grayscale ultrasound image through the quadrigeminal cistern. The bodies of the lateral ventricles (asterisks) are seen along with the echogenic choroid plexuses. The echogenic quadrigeminal cistern (Q) is bordered superiorly by the paired thalami (TH) and inferiorly by the cerebellum (CB). (f) Line F. Coronal grayscale ultrasound image through the atria of the lateral ventricles (asterisks) with prominent paired choroid plexuses (arrowheads). Cerebellum (CB) is partially visualized in the far-field. (g) Line G. Coronal grayscale ultrasound image through the parietal-occipital lobes posterior to the lateral ventricles. (h) Line H. Sagittal midline grayscale ultrasound image. The entire length of the corpus callosum is seen (arrowheads) with the cingulate gyrus (CG) located above the corpus callosum. Cavum septum pellucidum (asterisk) and anterior third ventricle (3) are seen. The massa intermedia (MI) is located posterior to the third ventricle. The anechoic fourth ventricle (4) is outlined by echogenic cerebellar vermis (V). Fluid-filled space of cisterna magna (CM) is seen in the far-field(i) Line I. Sagittal grayscale ultrasound image obtained at the caudothalamic junction (arrow). The caudothalamic junction is a shallow groove where the caudate (C) and thalamus (TH) meet at the floor of the lateral ventricle. Echogenic choroid plexus (asterisk) is seen along the body of the lateral ventricle. (j) Line J. Sagittal grayscale ultrasound image obtained at the lateral aspect of the lateral ventricles, with choroid plexus (asterisk) still visible. Caudate (C) and thalamus (TH) are seen. There is increased echogenicity of the posterior periventricular white matter (arrowhead), the peritrigonal blush, a normal finding. (k) Line K. Sagittal grayscale ultrasound image obtained lateral to the lateral ventricle. Sylvian fissure (arrow) is partially visualized
Sagittal images are acquired by placing the probe parallel to the sagittal suture across the anterior fontanelle. Multiple sagittal images are obtained by angling laterally from the midline to each side (Fig. 2.2h–k). The first sagittal image (Fig. 2.2h) obtained in the midline demonstrates the corpus callosum; the comma-shaped, fluid-filled cavum septum pellucidum between the lateral ventricles; and the cingulate gyrus above the corpus callosum. The normal sulci and gyri do not extend to the ventricles due to the presence of the cingulate gyrus. The tectum of the midbrain and the anechoic fourth ventricle outlined by echogenic cerebellar vermis are also seen.
The second parasagittal image (Fig. 2.2i) is obtained at the caudothalamic junction, a shallow groove where the caudate and thalamus meet at the floor of the lateral ventricle. The caudothalamic junction is clinically important as a site where subependymal, germinal matrix hemorrhage may occur that can subsequently lead to intraventricular hemorrhage in preterm infants; and it demarcates the anterior-most extent of the choroid plexus. Echogenic foci anterior to the caudothalamic junction therefore represent hemorrhage and not an extension of the choroid plexus (Fig. 2.3). The caudothalamic junction appears as a thin echogenic line by ultrasound. The caudate nucleus is slightly more echogenic compared to the thalamus.
Blood products in both frontal horns. Coronal grayscale ultrasound image anterior to the third ventricle displays heterogeneous echogenic foci (arrows) in the right and left frontal horns, corresponding to evolving intraventricular blood products. Of note, these foci of hemorrhage must not be mistaken for normal choroid plexus which does not extend into the frontal horns
The third parasagittal image (Fig. 2.2j) demonstrates the lateral extent of the lateral ventricles, where the choroid plexus is located. The last parasagittal image (Fig. 2.2k) includes the periphery of the frontotemporoparietal cortex beyond the lateral ventricles. The sylvian fissure is partially seen on this image.
The posterior fontanelle is useful for assessing the occipital horn and posterior periventricular white matter. Layering blood products along the dependent portion of the occipital horn can be visualized.
The transmastoid view provides significantly more detailed images of the posterior fossa in comparison to images obtained through the anterior or posterior fontanelles (Fig. 2.4). This view is especially helpful in assessing for cerebellar hemorrhage in patients treated with extracorporeal membrane oxygenation (ECMO).
Normal Development and Anatomy
Normal Development
In the 3rd week of gestation, embryos form a long linear band called the primitive streak (Fig. 2.5). At the cranial end of the primitive streak, the notochord forms which grows and migrates in a craniocaudal fashion [7]. The notochord induces the cranial end to develop into the central nervous system (CNS). The remainder of the notochord influences the development of the peripheral nervous system.In the 4th week of gestation, primary CNS development takes place, forming the prosencephalon (i.e., the forebrain) and the rhombomeres (that eventually develop into the mid- and hindbrain). The prosencephalon gives rise to the telencephalon and diencephalon. The telencephalon develops into the paired cerebral hemispheres, ventricles, and caudate nuclei. The diencephalon develops into the third ventricle, thalami, and hypothalamus.
Embryology of the central nervous system (CNS). In the 3rd week of gestation, the embryo forms a long linear band known as the primitive streak. The notochord forms at the cranial end of the primitive streak, which grows and migrates in a craniocaudal fashion. The notochord induces the cranial end to develop into the CNS. The remainder of the notochord develops into the spinal cord.
In the 4th week of gestation, primary CNS development takes place, forming the prosencephalon (forebrain) and rhombomeres (mid- and hindbrain). The prosencephalon further develops into the telencephalon and diencephalon. The telencephalon develops into the paired cerebral hemispheres, ventricles, and caudate nuclei. The diencephalon develops into the third ventricle, thalami, and hypothalamus.
In the second and third trimesters, the brain structures develop further, including microscopic pathways such as neuronal migration, and macroscopic pathways including gyral and fissure formation. Brain volume increases steadily until early childhood
An appreciation of the structural changes associated with congenital anomalies of the brain is best approached through an understanding of cerebral cortical formation.
There are five stages of central nervous system (CNS) development (Table 2.1) [8]: (1) dorsal induction at 3 to 4 weeks of gestation; (2) ventral induction at 5–8 weeks of gestation; (3) neuronal proliferation at 8–18 weeks of gestation; (4) migration at 12–22 weeks of gestation; and (5) development after migration and organization. The last three developmental stages have been classified and updated on the basis of genetics, molecular biology, and imaging [9]. Errors in any one of the last three stages can lead to malformations of cortical development.
Normal Anatomy
The brain consists of the forebrain, midbrain, and hindbrain (Fig. 2.6). The forebrain structures include the cerebral hemispheres, thalamus, hypothalamus, and pituitary gland. The midbrain structures include cranial nerve nuclei, tectum, tegmentum, and colliculi. The hindbrain structures include the brainstem (midbrain, pons, and medulla), the cranial nerves, and the cerebellar hemispheres. In this section, the normal anatomy of the brain and its appearance on ultrasound imaging are discussed.
Normal sagittal anatomy of the brain in the midline. The brain consists of the forebrain, midbrain, and hindbrain. Forebrain structures include the cerebrum, corpus callosum, thalamus, hypothalamus, and pituitary gland. Midbrain structures include cranial nerve nuclei, tectum, tegmentum, and colliculi. Hindbrain structures include the brainstem (midbrain, pons, and medulla), cranial nerves, and the cerebellum. The ventricles are fluid-filled spaces within the brain which act as conduits for cerebrospinal fluid
Cerebral Cortex
Sulci are echogenic curvilinear lines separating the gyri, which appear relatively hypoechoic. The sulci appear echogenic due to the interface of collagen and blood vessels in the pia mater against the underlying brain parenchyma that consists largely of water. The subcortical white matter is more echogenic centrally and becomes less so as it extends peripherally (Fig. 2.7) [10].
The subcortical white matter myelinates in the postnatal period [11]. Therefore, in newborns, the subcortical white matter is more hyperechogenic compared to the cortical ribbon, deep gray nuclei, thalamus (especially ventrolateral thalamus), and posterior limb of internal capsule due to lack to myelination [12]. In normal full-term infants, the posterior limb of the internal capsule is myelinated at birth.
Basal Ganglia and Thalami
The basal ganglia are a group of subcortical nuclei that include the caudate, putamen, and globus pallidus in the cerebral hemispheres, the substantia nigra in the midbrain, and the subthalamic nucleus in the diencephalon. On ultrasound, the caudate, putamen, globus pallidus, and thalamus can be distinctly visualized. In healthy full-term neonates, the basal ganglia and thalamus are isoechoic to the cortical gray matter and hypoechoic to the subcortical white matter (Fig. 2.2i). In preterm infants born prior to 32 weeks of gestation, the basal ganglia and thalamus are homogenously hyperechoic relative to the adjacent white matter (Fig. 2.8) [13].
Echogenic thalami in a 25-week-old premature female infant . Coronal grayscale ultrasound image of the basal ganglia and thalami (T) demonstrates homogenous hyperechogenicity relative to the adjacent white matter. The surface of the brain appears smooth. Both findings are expected in preterm infants born at less than 32 weeks of gestation
Ventricles
The ventricles are anechoic fluid-filled cavities, which act as conduits for the cerebrospinal fluid (CSF). The lateral ventricles are composed of a body, an atrium, and anterior, temporal, and occipital horns. The lateral ventricle on each side abuts the caudate nucleus, thalamus, and cerebral peduncle. The foramen of Monro is a short connecting passage between each lateral ventricle and the third ventricle (Fig. 2.9).
The normal width of the body of the lateral ventricle is less than 10 mm. However, patient positioning can affect the size of the ventricle . Slit-like ventricles are observed in 60% of normal full-term newborns and in 30% of normal preterm infants (Fig. 2.10) [14]. Asymmetry of lateral ventricle size is a common finding; the left lateral ventricle is often slightly larger than the right (Fig. 2.11) [15, 16].
Connatal cysts, also known as coarctation of the lateral ventricles or frontal horn cysts, are small cystic areas adjacent to the superolateral walls of the frontal horns or body of the lateral ventricles (Fig. 2.12a). They are considered a normal anatomical variant. On ultrasound, multiple cysts can be seen, forming a string of pearls appearance (Fig. 2.12b). Connatal cysts are rare and are seen in up to 1.05% of premature or low birth weight infants [17]. They eventually resolve spontaneously without adverse neurological effects.
Connatal cysts in a 1-day-old male . (a) Coronal grayscale ultrasound image at the level of the third ventricle (3) shows bilateral connatal cysts (arrowheads) adjacent to the superolateral walls of the frontal horns of the lateral ventricles (asterisks). (b) Parasagittal grayscale ultrasound image of the brain shows two connatal cysts (arrowheads) along the body of the lateral ventricle, forming a string of pearls appearance
Cisterna Magna
The cisterna magna is an extra-axial fluid space located inferior to the echogenic cerebellar vermis and superior to the occipital bone (Fig. 2.2h). The normal cisterna magna measures less than 8–10 mm in the axial and sagittal planes [18]. Mega cisterna magna is a normal variant where the extra-axial fluid space measures more than 8–10 mm in the axial and mid-sagittal planes (Fig. 2.13). Mega cisterna magna can be differentiated from an abnormality such as an arachnoid cyst, by its lack of associated mass effect, and from a Dandy–Walker syndrome by the presence of the cerebellar vermis.
Mega cisterna magna in a 1-month-old male, a normal variant. (a) Sagittal midline grayscale ultrasound image shows an enlarged CSF subarachnoid space (asterisk) inferior and posterior to the cerebellum (C). (b) Axial FLAIR MR image depicts the mega cisterna magna (asterisk) posterior to the cerebellum (C) and vermis (V). There is no associated mass effect on the brain
Extra-Axial Fluid Spaces
Extra-axial fluid spaces are CSF spaces located between the brain and the skull. The extra-axial fluid spaces are bounded by the leptomeninges and traversed by blood vessels, which are highly echogenic. The extra-axial fluid spaces are best seen in the midline using a high-frequency linear array transducer on the order of 12 MHz. The lateral, anterior, and posterior aspects of the extra-axial fluid spaces are difficult to visualize with ultrasound. With color Doppler , cortical veins can normally be seen extending from the brain surface to the skull within the extra-axial space.
Congenital Brain Anomalies
Dorsal Induction Disorders
Chiari Malformations
Chiari malformations are characterized by caudal descent of the cerebellar tonsils inferior to the foramen magnum. Chiari I malformation is the most common and demonstrates descent of the cerebellar tonsils more than 5 mm below the foramen magnum without displacement of the medulla or fourth ventricle [19]. A common association is a small osseous posterior fossa, which results in crowding and inferior herniation of the cerebellar tonsils (Fig. 2.14). Other associations include multisutural craniosynostosis, as with Crouzon syndrome and Pfeiffer syndrome. Symptoms depend on the degree of inferior tonsillar herniation.
Ultrasound imaging of Chiari I malformation is challenging since the herniated cerebellar tonsils cannot be directly visualized with conventional transfontanellar ultrasound imaging. Indirect signs of Chiari I malformation include difficult visualization of an elongated fourth ventricle, an unusually low position of the cerebellar vermis, an enlarged massa intermedia, and obliteration of the cisterna magna.
Hydrocephalus is seen in up to 30% of cases [20], with dilated lateral and third ventricles that can be an indirect clue to Chiari I malformation . When there is a suspicion for Chiari 1 malformation, MR imaging of the brain and spine is needed for further assessment. MR imaging allows accurate assessment of the degree of inferior tonsillar descent, patency of CSF flow, and evaluation for associated hydrocephalus and/or syrinx [21]. Treatment depends on the symptoms, degree of ventriculomegaly, and presence of a syrinx.
Chiari II malformation is a complex malformation of the hindbrain, spine, and mesoderm of the skull base and spinal column. It is characterized by a small posterior fossa associated with caudal herniation of the lower part of the cerebellum and fourth ventricle (Fig. 2.15). It is present in all children with open spinal dysraphism. Other associated findings include hydrocephalus, callosal dysgenesis, gray matter heterotopia, and colpocephaly [22]. The fourth ventricle is usually small and narrowed in the anteroposterior dimension, vertically oriented and inferiorly displaced. The brainstem is abnormal with inferior displacement of the pons and medulla. The pons is hypoplastic and the medulla occasionally extends below the foramen magnum.
Since most patients with Chiari II malformation present with myelomeningocele, this neural tube defect is often detected by prenatal imaging. After birth, MR imaging is the modality of choice for precise evaluation of brain and spine morphology [22]. Ultrasound imaging is useful for monitoring the brain for hydrocephalus both prior to and after surgery, as well as to assess for post-surgical complications, including intracerebral and extra-axial hemorrhage and other fluid collections.
Chiari II malformation in a 5-day-old female following myelomeningocele repair. (a) Sagittal grayscale ultrasound image of the brain shows signs of Chiari II malformation, including a small posterior fossa with a low-lying cerebellum (C) and hydrocephalus (asterisk). A low position of the tentorium (arrows) and torcula (arrowhead) are also identified. (b) Coronal T2-weighted MR image of the brain confirms a low-lying cerebellum (C) and a small posterior fossa. The lateral ventricles (asterisks) are dilated. (c) Sagittal T2-weighted MR image of the spine shows inferior descent of the cerebellar tonsils (asterisk) with obliteration of the cisterna magna (arrow). There is a low-lying spinal cord (arrowhead) at the level of S2-S3. The exposed neural placode is not included on the image
The availability of fetal ultrasound and MR imaging has facilitated the prenatal diagnosis of Chiari II malformation and has been the major impetus for the development of fetal surgery. However, this new treatment option has generated a number of controversies, particularly with respect to maternal morbidity and premature birth of the fetus. Postnatal repair of myelomeningocele remains the standard of care in most institutions in the United States and around the world.
Anencephaly
Anencephaly is the absence of the forebrain, skull, and scalp with partial preservation of the posterior fossa. Anencephaly is the most severe form of neural tube defect in which the cephalic end of the neural tube fails to close. It is often diagnosed during antenatal ultrasound screening. Maternal serum alpha-fetoprotein is markedly elevated during pregnancy. On ultrasound imaging, no skull bones and parenchymal tissues are seen above the level of the orbits (Fig. 2.16). Portions of the occipital bones may be present, along with the posterior fossa. Anencephaly is incompatible with life. Therefore, if it is detected prenatally, termination of pregnancy is typically considered.
Fetus with anencephaly . (a) 3D reformatted ultrasound image shows absence of the brain, skull, and scalp (arrow) consistent with anencephaly. In addition, micrognathia (asterisk), low set ears (arrowhead), and edema of the remaining head are seen. (b) Sagittal T2-weighted MR image shows absent brain and skull (arrow) and intact globe (arrowhead). B, Bladder
Hydranencephaly
Hydranencephaly denotes destruction of the cerebral hemispheres. The skull is intact, in contrast to anencephaly. The cerebral hemispheres are liquefied and replaced by CSF within an intact membranous sac. The basal ganglia and brainstem are intact. There are numerous causes of hydranencephaly, including bilateral supraclinoid internal carotid arterial occlusion, extensive leukomalacia, diffuse hypoxic–ischemic injury leading to necrosis, and infection. Hydranencephaly may be diagnosed prenatally, although in the absence of a prenatal diagnosis, affected pediatric patients may present later in infancy with seizures, flaccidity, respiratory failure, or vegetative state.
On ultrasound , the falx is usually present. The cortical tissues are largely absent and replaced by CSF (Fig. 2.17). Some residual tissue can be seen in the occipital poles and medial temporal lobes. The basal ganglia, thalami, and posterior fossa are preserved. Hydranencephaly is generally not compatible with life after birth. Therefore, if detected prenatally, termination of pregnancy is typically considered.
Hydranencephaly in a 2-day-old male . (a) Coronal grayscale ultrasound image shows near-complete destruction of the cerebral hemispheres that are replaced by cerebrospinal fluid (CSF). Residual brain parenchyma (asterisks) is seen at the periphery of the skull, along with an intact midbrain (MB). (b) Coronal T2-weighted, fat-suppressed MR image demonstrates near-complete absence of the cerebral hemispheres with minimal residual brain parenchyma (asterisks). The falx and midbrain (MB) are present. In contrast to anencephaly, the cranial vault (arrow) is intact
Ventral Induction Disorders
Holoprosencephaly
Holoprosencephaly is a congenital brain malformation caused by incomplete cleavage of the forebrain and the face. There are varying degrees of fusion of the paired cerebral hemispheres, lateral ventricles, olfactory tracts, and thalami. Facial anomalies can include cyclopia, cleft lip/palate, hypertelorism, and a solitary median maxillary central incisor. Depending on the severity of the fusion anomalies, there are three subtypes of holoprosencephaly that range from mild to severe: lobar, semilobar, and alobar types. Holoprosencephaly is often detected prenatally, and life expectancy depends on the subtype.
On ultrasound imaging of alobar holoprosencephaly , the lateral ventricles are fused and form a monoventricle (Fig. 2.18). There are undivided cerebral hemispheres and fused thalami. There is lack of division between the frontal, parietal, temporal, and occipital lobes and the ventricular horns. The posterior fossa and brainstem remain relatively normal.
Semilobar holoprosencephaly demonstrates partial cleavage of the cerebral hemispheres posteriorly. The frontal lobes remain fused and malformed with a monoventricle. The thalami are fused. There are rudimentary-appearing temporal and occipital horns.
Lobar holoprosencephaly is the mildest form of holoprosencephaly where the cerebral hemisphere is divided posteriorly. However, there is fusion of the anterior horns of the lateral ventricles forming a squared and flattened roof beneath the corpus callosum. The septum pellucidum is absent. The remaining portions of the lateral ventricles are divided normally. The thalami appear normal and are not fused.
Septo-Optic (Pituitary) Dysplasia
Septo-optic dysplasia , or the currently preferred term “septo-optic pituitary dysplasia”, is a midline congenital brain malformation with abnormalities that include a partially or completely absent septum pellucidum, optic nerve hypoplasia, and hypopituitarism. All three abnormalities occur in approximately 30% of affected individuals. Absence of the septum pellucidum occurs in approximately 60% of patients [23]. There is also an association with schizencephaly and gray matter heterotopia. Clinical presentation can include seizures, visual abnormalities, developmental delay, and precocious puberty.
On ultrasound imaging, absence of the septum pellucidum is readily identified (Fig. 2.19a). To assess for optic nerve hypoplasia and pituitary abnormality, further evaluation with MR imaging is needed (Fig. 2.19b, c).
Treatment requires a multidisciplinary approach to address the associated neurodevelopmental, ophthalmological, and endocrinological abnormalities.
Septo-optic (pituitary) dysplasia in a 4-year-old male. (a) Coronal grayscale ultrasound image at birth reveals absence of the septum pellucidum (asterisk). (b) Coronal T2-weighted MR image shows hypoplasia (arrow) of the optic chiasm and absence (asterisk) of the septum pellucidum. There was right greater than left optic nerve hypoplasia as well (not shown). (c) Sagittal T1-weighted MR image shows an ectopic pituitary gland with a bright spot (arrow) at the proximal end of the infundibulum
Anomalies of the Corpus Callosum
The corpus callosum is a thick white matter tract that connects the cerebral hemispheres and enables communication between them. Between 8 and 20 weeks of gestation, the corpus callosum is formed in an anterior-to-posterior fashion, with the exception of the rostrum, which forms last [24]. The corpus callosum can be completely absent (agenesis) or only partially formed (callosal dysgenesis) [25].
There are more than 130 syndromes with associated anomalies of the corpus callosum. The more commonly encountered associations include cortical malformations (polymicrogyria, pachygyria, and heterotopia), Chiari II malformation, Dandy–Walker syndrome, holoprosencephaly, septo-optic pituitary dysplasia, and Aicardi syndrome [25].
Children with isolated corpus callosum anomalies often appear normal or near-normal by 3 years of age, but as the complexity of school tasks increases, subtle deficient cognitive functions often become noticeable.
Ultrasound imaging of callosal agenesis reveals separation of the lateral ventricles which run parallel to each other (sometimes referred to as the “Texas longhorn” sign or the “moose head” sign) (Fig. 2.20). The corpus callosum is partly or completely absent, best identified on sagittal images. The third ventricle is high-riding and there is associated colocephaly, or abnormal dilation of the occipital horns of the lateral ventricles. There is a radiating sulcal pattern of the gyri that converge on the third ventricle. In some cases, bundles of Probst are identified. These are re-routed callosal fibers seen in the medial aspect of the lateral ventricles. The anterior cerebral artery has an abnormal posterior course.
Agenesis of the corpus callosum in an 8-day-old male. (a) Coronal grayscale ultrasound image at the level of the third ventricle (3) demonstrates absence of the corpus callosum with widely separated anterior horns of the lateral ventricles (arrowheads). (b) Coronal grayscale ultrasound image obtained via the posterior fontanelle demonstrates a parallel configuration of the lateral ventricles (arrowheads). Asterisks, Choroid plexuses. Sagittal grayscale ultrasound image (c) and T1-weighted MR image (d) show a high-riding third ventricle (3) with radially oriented gyri and sulci (arrowheads) converging on the third ventricle (3) and the expected location of the corpus callosum (asterisks)
Intracranial lipoma occurs in about half of patients with callosal dysgenesis as a result of abnormal differentiation of the embryologic primordium of the meninges. It can be found anywhere in the brain, although the pericallosal region is the most common, followed by the quadrigeminal cistern, suprasellar cistern, cerebellopontine angle, Sylvian fissure, and rarely, in the choroid plexus [26]. On ultrasound, an intracranial lipoma is seen as a well-defined, hyperechoic mass that may demonstrate posterior acoustic shadowing due to punctate foci of calcification (Fig. 2.21).
Dandy–Walker Syndrome
Dandy–Walker syndrome is a spectrum of cystic posterior fossa malformations characterized by a hypoplastic vermis, a dilated fourth ventricle which communicates with a prominent CSF space of the posterior fossa, and elevation of the torcula [27].
In the postnatal period, hydrocephalus develops in 70–90% of patients, with macrocephaly being the most common presentation. In approximately 70% of cases, other intracranial abnormalities are seen, including holoprosencephaly, schizencephaly, callosal dysgenesis, cortical dysplasia, polymicrogyria, gray matter heterotopia, lipoma, and cephalocele [28].
Trisomies 13, 18, and 21, and other syndromes including Aicardi syndrome, Cornelia de Lange syndrome, and Walker–Warburg syndrome , can be associated with Dandy–Walker syndrome [29]. Motor-related symptoms are common, including spasticity, hypotonia, and delayed motor function, as well as intellectual disability.
The ultrasound features of Dandy–Walker syndrome include a hypoplastic or aplastic vermis, a dilated fourth ventricle communicating with the posterior fossa CSF space, a markedly prominent cisterna magna (greater than 10 mm diameter), and a CSF gap between the cerebellar hemispheres (Fig. 2.22).
Dandy–Walker malformation in a 1-month-old female. (a) Sagittal grayscale ultrasound image near the midline demonstrates absence of the vermis and a dilated fourth ventricle (4) communicating (arrow) with the posterior fossa (P) CSF. There is associated hydrocephalus with dilated lateral (asterisk) and third (3) ventricles. C, Cerebellum. (b) Axial FLAIR MR image demonstrates a “keyhole” appearance of the absent vermis and dilated fourth ventricle (4) communicating (arrow) with the posterior fossa (P) CSF
Hypoplastic vermis with rotation (previously referred to as “Dandy–Walker variant”) denotes a posterior fossa malformation where there is hypoplasia of the vermis and a dilated fourth ventricle that are less pronounced when compared to the classic Dandy–Walker syndrome. There is no enlargement of the posterior fossa.
Neuronal Proliferation Disorders
Hemimegalencephaly
Hemimegalencephaly is a rare cortical disorder characterized by hamartomatous overgrowth of the ipsilateral cerebral hemisphere. It is caused by abnormal neuronal proliferation and/or decreased neuronal apoptosis. Pediatric patients with hemimegalencephaly present with macrocephaly, developmental delay, and seizures. In addition to hamartomatous overgrowth of the ipsilateral cerebral hemisphere, other organizational and post-migration disorders can be seen, including lissencephaly, pachygyria, and polymicrogyria.
On ultrasound imaging, there is an enlarged and dysplastic appearance of the ipsilateral cerebral hemisphere. The affected cortex is thickened with irregular gyri, and pachygyria or polymicrogyria are often seen. Dystrophic calcifications occur at the gray–white matter junctions. There is enlargement of the ipsilateral lateral ventricle without hydrocephalus and midline shift.
Treatment is aimed at symptomatic control, particularly seizures. For refractory seizures, hemispherectomy can be considered if the contralateral cerebral hemisphere is not affected by the hemimegalencephaly.
Neuronal Migration Disorders
Lissencephaly
Lissencephaly , also known as agyria, is a rare disorder of cortical malformation resulting in a smooth brain surface. There is an arrest in the transmantle migration of neurons, which results in either a severe form of absent gyri (agyria or complete lissencephaly ) or the presence of a few gyri (pachygyria or incomplete lissencephaly). Agyria and pachygyria often coexist in different parts of the brain of an affected patient. In the setting of severe lissencephaly, callosal dysgenesis with a vertically oriented splenium can be seen. Lissencephaly can be sporadic or associated with disorders such as Miller–Dieker syndrome or Norman–Roberts syndrome.
On ultrasound imaging, a smooth brain surface is seen with a thickened cortex and a lack of, or paucity of sulcation. In addition, there is ventriculomegaly, especially colpocephaly, without hydrocephalus; the Sylvian fissures are widened; and the subarachnoid space is prominent. In pachygyria, abnormally formed gyri are typically broad with shallow sulci. Lissencephaly can be reliably diagnosed during or after the third trimester of pregnancy. Follow-up imaging in late pregnancy is therefore recommended if there is an early diagnosis of or suspicion for lissencephaly [30].
Gray Matter Heterotopia
Gray matter heterotopia is a frequently encountered neuronal migration disorder. Cortical neurons are arrested between 6 and 16 weeks of gestation along the radial pathway from the germinal matrix of the ventricle to the cortical surface [9]. Gray matter heterotopia is divided into three groups: subependymal, subcortical, and band heterotopia. Unless subependymal gray matter heterotopia bulges into the ventricles (Fig. 2.23), other forms of gray matter heterotopia are difficult to diagnose by ultrasound.
Gray matter heterotopia (subependymal type) in a 13-day-old female. (a) Sagittal grayscale ultrasound image shows multiple nodules (arrows) projecting into the body of the left lateral ventricle (V). (b) Sagittal T1-weighted and (c) axial T2-weighted MR images demonstrate subependymal gray matter heterotopia (arrowheads) adjacent to the bodies of the lateral ventricles (V) with the same signal characteristics as gray matter
Post-Migration Disorders
Polymicrogyria
Polymicrogyria is a congenital malformation characterized by excessive folding of the cerebral cortex. Neurons from the germinal matrix reach the cortex but are abnormally organized, forming multiple small and undulating gyri. Polymicrogyria is a feature of genetic disorders such as Aicardi and Joubert syndromes, metabolic processes such as Zellweger syndrome and mitochondrial diseases, in utero injury and infection [31]. If there are co-existing auditory or visual symptoms, infection such as cytomegalovirus (CMV) should be suspected.
There is a predilection of polymicrogyria for the perisylvian region , and syndromic cases may be bilateral. Symptoms include seizures and developmental delay. The severity of symptoms correlates with the extent of polymicrogyria and associated anomalies.
On ultrasound imaging, the excessively small and undulating gyri are difficult to detect. High-resolution MR imaging is typically needed for diagnosis.
Schizencephaly
Schizencephaly is a congenital post-migrational and organizational disorder characterized by clefts in the cerebral hemisphere extending from the ventricle to the cortical surface [32]. The cleft is lined with heterotopic gray matter, often forming polymicrogyria. There are two types which are defined by whether or not there is apposition of the gray matter lining the cleft: closed-lip (gray matter apposition) or open-lip (gray matter separation).
Schizencephaly is bilateral in up to 50% of cases. Pediatric patients with closed-lip schizencephaly can be asymptomatic but often present with seizures and developmental delay. Patients with open-lip schizencephaly have increased morbidity and present with macrocephaly, seizures, or developmental delay.
On ultrasound imaging, open-lip schizencephaly demonstrates a fluid-filled cleft extending from the ventricle to the cortex (Fig. 2.24). There may be a nipple-like outpouching of the ventricle at the origin of the cleft. Closed-lip schizencephaly is difficult to visualize by ultrasound. MR imaging is therefore needed for definitive diagnosis.
Schizencephaly in a newborn male . (a) Coronal grayscale ultrasound image demonstrates a large open-lip schizencephaly (arrow) of the right cerebral hemisphere, with the lateral ventricle (V) in direct communication with an enlarged extra-axial CSF space (CSF). The septum pellucidum is absent. (b) Coronal T2-weighted MR image shows the open-lip schizencephaly (arrow) lined with heterotopic gray matter (arrowheads)
Intracranial Hemorrhage
In premature infants, particularly those of low birth weight, germinal matrix and intraventricular hemorrhage are commonly seen. In term infants, extra-axial hemorrhage, including epidural, subdural, and subarachnoid bleeds, are typically related to birth trauma. Intra-parenchymal hemorrhage can occur in both term and pre-term infants as a result of numerous underlying causes.
Preterm Infants
In preterm infants, neonatal hemorrhage occurs in the germinal matrix because the subependymal lining is highly vascular. Neonatal periventricular/intraventricular hemorrhage (PIVH) occurs in up to 25% of preterm infants who are less than 33 weeks of gestation or infants weighting less than 1500 grams [33]. The Papile classification [34] is the most commonly used system to grade PIVH (Table 2.2). Grade 1 PIVH is confined to the caudothalamic groove, without extension into the ventricular system.
On ultrasound, echogenic foci consistent with hemorrhage are seen at or anterior to the caudothalamic groove (Fig. 2.25). Grade 2 PIVH extends outside the caudothalamic groove, and into a non-dilated ventricle (Fig. 2.26). Grade 3 PIVH is hemorrhage within the ventricle with associated ventricular dilation, or hemorrhage occupying more than 50% of the ventricular volume (Fig. 2.27). It is important to note that progression of a Grade 2 to a Grade 3 PIVH requires follow-up assessment for post-hemorrhagic hydrocephalus where intervention might be considered.
Periventricular/intraventricular hemorrhage (PIVH) grade 1. (a) Normal caudothalamic groove. Sagittal grayscale ultrasound image demonstrates the shallow groove (arrow) where the caudate (C) and thalamus (T) meet at the floor of the lateral ventricle. (b) PIVH grade 1. Sagittal (left panel) and coronal (right panel) grayscale ultrasound images show an ovoid, echogenic focus of hemorrhage (arrowheads) at the caudothalamic groove
Periventricular/intraventricular hemorrhage (PIVH) grade 2. Sagittal grayscale ultrasound image shows a loss of the groove at the caudothalamic junction (black arrow) and hypoechoic material consistent with blood products. Echogenic material in keeping with blood extends adjacent and inferior (white arrow) to the choroid plexus without ventricular dilation
Serial cranial ultrasound examinations are an excellent method to assess the evolution of hemorrhage and to monitor for the development of hydrocephalus. In addition, posterior fontanelle images are useful to assess for layering of blood in the occipital horns that is difficult to visualize from an anterior fontanelle approach.
Periventricular Hemorrhagic Infarction
Periventricular hemorrhagic infarction (PVHI) is also known as Grade 4 PIVH in the original Papile classification. The mechanism of Grade 4 PIVH is different from the other grades of PIVH. The periventricular white matter is drained by the deep medullary veins, which are fan-shaped vessels draining into the terminal veins along the ventricular margins (Fig. 2.28). PVHI is caused by bleeding in the germinal matrix, which causes stasis and engorgement of the terminal veins and subsequently the medullary veins. Eventually, venous thrombosis and parenchymal venous hemorrhagic infarction occur (Fig. 2.29).
Approximately 10–15% of preterm neonates with PIVH will develop PVHI [35]. The chronic neuroimaging manifestation of PVHI is a porencephalic cyst replacing the injured periventricular white matter and cortex (Fig 2.29e). PVHI can also occur in isolation as well as in utero, without associated germinal matrix hemorrhage.
Diagram of the deep medullary veins . These vessels fan out to drain the white matter of the cerebral hemispheres into the terminal veins of the germinal matrix along the lateral ventricular margins. Germinal matrix hemorrhage interferes with this drainage leading to engorgement and thrombosis. LV, Lateral ventricle
Periventricular hemorrhagic infarction (PVHI) , or grade 4 periventricular/intraventricular hemorrhage (PIVH) in a 3-day-old male. (a) Coronal grayscale ultrasound image shows left germinal matrix hemorrhage (asterisk) as well as blood filling most of the left lateral ventricle. (b) Axial T1-weighted MR image shows blood products extending from the germinal matrix into the left lateral ventricle (asterisk) and the adjacent periventricular white matter (arrow). (c) Axial susceptibility-weighted MR image shows blooming artifact related to blood products in the germinal matrix and ventricle (asterisk), as well as in the adjacent periventricular white matter (white arrow). There is engorgement of the periventricular terminal medullary veins (black arrow). (d) Follow-up coronal grayscale ultrasound image obtained 2 weeks after the initial insult demonstrates clot retraction (asterisk) in the lateral ventricle and adjacent periventricular white matter (arrow). The clot is now heterogeneously hypoechoic, an expected change. (e) Follow-up coronal grayscale ultrasound image at 3 months demonstrates a porencephalic cyst (arrow) replacing the injured periventricular white matter and communicating with the left lateral ventricle
Post-hemorrhagic hydrocephalus is seen in 20–25% of preterm infants, particularly following Grade 3 or PVHI/Grade 4 PIVH . Preterm infants are at higher risk for multi-compartmental obstructive hydrocephalus because they have a relative deficiency of fibrinolytic function and they are therefore prone to fibroproliferative subependymal gliosis. Grade 3 and PVHI/Grade 4 PIVH typically require ventricular shunting while this rarely required for grades 1 and 2.
Cerebellar Hemorrhage
Cerebellar hemorrhage is more frequently seen in preterm infants than in term infants, and occurs in up to 19% of preterm infants of less than 32 weeks’ gestational age [36]. Cerebellar hemorrhage is best imaged through the trans-mastoid fontanelle. Hemorrhage is usually localized to the cerebellar hemisphere and less frequently in the vermis. Etiologies include primary parenchymal hemorrhage, venous infarction , and intraventricular bleed extending to the cerebellar hemisphere. The patient is often asymptomatic. However, when the intracerebellar hemorrhage is large, it can cause mass effect on the adjacent brainstem leading to apnea or respiratory symptoms . With the increasing use of extracorporeal membrane oxygenation (ECMO) in infants, cerebellar hemorrhage has been increasing in incidence (Fig. 2.30).
Term Infants
In term infants, birth-related intracranial hemorrhage is relatively common and generally benign. Extra-axial hemorrhage can be epidural, subdural, or subpial in location. Intracerebral hemorrhage can be localized to the parenchymal, subependymal, cerebellar, or choroid plexus regions.
Epidural Hemorrhage
Epidural hemorrhage is an accumulation of blood in the potential space between the dura mater and the overlying skull. Epidural hemorrhage is relatively uncommon in newborns but can be seen in the setting of traumatic or instrument-assisted birth injury. In infants, epidural hemorrhage is more often due to venous tears than to arterial tears because there are abundant dural and diploic veins in the rapidly growing skull [37].
The epidural blood cannot cross suture lines and therefore manifests as a lentiform collection adjacent to the skull. It is difficult to differentiate epidural from subdural hemorrhages by ultrasound and, therefore, additional cross-sectional imag-ing with CT is needed for diagnosis.
Subdural Hemorrhage
Subdural hemorrhage is an accumulation of blood that results from tearing of the bridging veins in the potential space between the dura mater and the arachnoid mater as they cross the subdural space, or of the dural sinuses. Subdural hemorrhage is seen in up to 8% of term deliveries, particularly in traumatic or instrument-assisted births [38]. Unlike epidural hematoma, subdural hematoma can cross suture lines and typically forms a hematoma that overlies and conforms to the shape of the parenchymal convexity (Fig. 2.31).Ultrasound evaluation of a subdural hemorrhage requires use of a high-frequency linear transducer with color Doppler to assess the position of the cortical veins. A subdural hematoma displaces the cortical veins toward the cerebral cortex. A subdural space filled with blood lacks blood vessels and none is seen with color Doppler. A small subdural hematoma without mass effect on the adjacent brain parenchyma has an excellent prognosis. However, when a subdural hematoma is located in the infratentorial region or there is mass effect on adjacent vital structures, especially the brainstem, the potential consequences are dire and surgical evacuation must be considered.
Subdural fluid collections in a 2-month-old male with suspected non-accidental trauma. (a) Coronal grayscale ultrasound image demonstrates bilateral subdural fluid collections (asterisks) of different echogenicity suggesting hemorrhage of different ages from repetitive injury. (b) Coronal T2-weighted MR image shows the bilateral subdural fluid collections (asterisks) with associated displacement of a cortical vein (arrowhead) from the inner table of the skull
Subpial Hemorrhage
Subpial hemorrhage is rare and refers to the accumulation of blood in the potential space between the pia mater with sparing of and the cerebral cortex. The etiology of subpial hemorrhage is controversial but may include birth-related trauma or cortical vein stasis and thrombosis. Pediatric patients with subpial hemorrhage present with a variable degree of neurological symptoms.
On ultrasound, subpial hemorrhage is generally difficult to distinguish from subarachnoid hemorrhage. It is often localized to the cortical surface (Fig. 2.32a) without spread over the convexity as occurs with subarachnoid hemorrhage. There may be associated cerebral ischemia with hemorrhagic infarction occurring deep to the subpial bleed (Fig. 2.32b).
Subpial hemorrhage in a premature infant female with apnea. (a) Coronal grayscale ultrasound image demonstrates a small, echogenic subpial hemorrhage (asterisk) localized to the space between the pia mater and the cortical surface without spread over the convexity. (b) Coronal grayscale ultrasound image demonstrates a second focus of subpial hemorrhage (asterisk) with associated cerebral ischemia and hemorrhagic infarction (H)
Parenchymal Hemorrhage
There are many potential causes of parenchymal hemorrhage in term infants, including birth trauma, hypoxic–ischemic injury (HII), infection, emboli, vein of Galen malformation (VOGM), and treatment with ECMO. On ultrasound, an acute hemorrhage appears echogenic. As a hematoma evolves, it will liquefy and appear hypoechoic to anechoic. Patients on ECMO are at risk of parenchymal bleed due to the routine use of anticoagulation. Multi-compartmental and intra-parenchymal hemorrhages can be seen in these patients with a predilection for the cerebellar hemispheres.
Choroid Plexus Hemorrhage
On ultrasound, the normal choroid plexus is highly echogenic with a lobular configuration. Choroid plexus hemorrhage is often difficult to diagnose due to the similar echogenicity of acute hemorrhage and the choroid plexus. Choroid plexus hemorrhage is suspected when there is ipsilateral occipital horn enlargement, asymmetrical enlargement of the choroid plexus, or serial ultrasound examinations demonstrate a sequential decrease in the apparent size of the choroid plexus.
It is believed that choroid plexus hemorrhage is more common in full-term infants than in preterm infants. However, choroid plexus hemorrhage is difficult to detect in premature infants, especially those with grade 2 or higher PIVH. The incidence of choroid plexus bleed in premature infants is, therefore, probably more common than previously appreciated. Studies are needed to further evaluate the incidence of choroid plexus hemorrhage in premature infants with pathologic/ultrasound correlation [39].
Hypoxic–Ischemic Injury
Hypoxic–ischemic injury (HII) remains a major cause of mortality and morbidity in neonates. HII refers to brain damage caused by low oxygen supply (hypoxia) and diminished perfusion (ischemia) in the pre- and postnatal periods. HII can lead to hypoxic–ischemic encephalopathy (HIE).
HIE is a clinical diagnosis of neonatal encephalopathy, based on the following diagnostic criteria: hypoxia or ischemia by Apgar score of < 5 at 10 mins, fetal umbilical artery acidemia (cord pH < 7.0), encephalopathy, presence of multi-organ failure and/or neuroimaging evidence of acute brain injury. Importantly, imaging represents just one of the multiple diagnostic criteria for HIE.
HII depends on three factors: gestational age (Fig. 2.33), the severity of injury, and the underlying mechanism of the insult, such as stroke or meningitis. Although there is a substantial overlap between the neuroimaging characteristics of the different types of HII, different patterns are seen in preterm and term infants that depend on the severity and duration of the insult.
Global Hypoxic–Ischemic Injury
Preterm Infants
Preterm infants are prone to ischemic injury due to poor autoregulation of cerebral blood flow, an immature cardiorespiratory system, and immature myelination of the central nervous system. The vascular supply of preterm infants less than 32 weeks of gestation is unique and different from that of older preterm or full-term infants. Instead of cerebral blood flow from the circle of Willis being directed to the periphery as occurs in children and adults, the periventricular white matter is supplied by perforating vessels originating from the pia mater that are directed centrally. The periventricular white matter is therefore located further from the origin of the blood supply, resulting in increased susceptibility to vascular insult.
When mild to moderate hypotension occurs in premature neonates less than 32 weeks of gestation, periventricular white matter ischemic injury leads to periventricular leukomalacia (PVL). Bilateral, fairly symmetrical foci of white matter necrosis develop around the lateral ventricles, particularly in the frontal and occipital lobes. Large necrotic lesions undergo cavitation in 2–4 weeks and remain cystic (cystic PVL). Small necrotic lesions do not undergo cavitation or form small cysts that collapse into glial scars (non-cystic PVL).
The corticospinal tracts and optic radiations are located at the common sites of periventricular white matter injury, and therefore the sequelae of PVL can include quadriplegia and/or visual deficits. Injury occurs not only at the time of the original insult but also during reperfusion.
Cranial ultrasound is an excellent imaging modality for the detection and assessment of the severity and evolution of PVL injury. Immediately after injury, ultrasound findings are generally normal. Within 2 weeks of injury, periventricular white matter echogenicity increases (Fig. 2.34). Between 2 and 6 weeks after the insult, cystic cavities may develop. Cysts can be single or multiple, varying in degree from a focal cyst adjacent to the ventricle, to diffuse cystic change throughout the deep white matter (Fig. 2.35).
Typical chronic imaging manifestations of PVL include a decrease in thickness of the deep white matter with dilation of the lateral ventricles which often display undulating margins. The changes of PVL need to be distinguished from a normal peritrogonal echogenic “blush” (Fig. 2.2j) and Grade 4 PIVH [40].
Periventricular leukomalacia (PVL) in a male born at 29 weeks of gestation. (a) Coronal grayscale ultrasound image of the brain obtained at 1 day of age reveals increased echogenicity (arrows) of the right and left periventricular white matter posterior to the bodies of the lateral ventricles. (b) Coronal grayscale ultrasound image of the brain obtained at 4 weeks of age shows small cystic spaces (arrowheads) within the zones of abnormal white matter, more numerous on the left
Cystic periventricular leukomalacia (PVL) in an 11-day-old female born at 28 weeks of gestation. (a) Sagittal color Doppler ultrasound image obtained with a linear high-frequency transducer demonstrates extensive cyst formation (arrow) extending from the periventricular white matter to the subcortical white matter. (b) Axial FLAIR MR image obtained 3 months later demonstrates volume loss (asterisks) of the deep white matter with ex vacuo dilation of the lateral ventricles (V). CV, Cavum vergae. Note the smooth brain contours in keeping with marked prematurity
When severe hypotension occurs in premature neonates less than 32 weeks of gestation, the most metabolically active regions of the brain where myelination occurs are prone to insult. These regions include the thalami, basal ganglia, corticospinal tract, hippocampi, and brainstem. The cerebral cortex is relatively spared , including the perirolandic cortex, because there are collaterals from the meningeal arterial anastomoses, which involute at term [41]. In addition, myelination of the perirolandic white matter does not occur until 35 weeks of gestation.
Term Infants
When mild to moderate hypotension develops in term neonates, blood is shunted to the vital structures of the brain, including the deep gray nuclei and the brainstem. The vulnerable watershed or border zones of the cerebral cortex are located between the territories supplied by the anterior, posterior, and middle cerebral arteries. The motor cortex is often affected, especially the innervation to the upper limb, that can lead to spastic quadriplegia, cognitive deficits, and seizures in later life.
In the setting of severe hypotension, other metabolically active regions of the brain are affected as well, including the thalami (especially their ventrolateral aspects), corticospinal tracts, basal ganglia (especially the posterior putamina), perirolandic cortex, hippocampi, and the dorsal brainstem.
In mild to moderate cerebral edema, there is increased echogenicity of the subcortical white matter, which accentuates gray–white matter differentiation (Fig. 2.36a) [42, 43]. In severe cerebral edema, there is loss of gray–white matter differentiation along with blurring of the sulci, interhemispheric and Sylvian fissures, slit-like ventricles, and decreased size of the extra-axial spaces (Figs. 2.36b, c and 2.37) [43].
Cerebral edema in two different 1-day-old full term males. (a) Longitudinal grayscale ultrasound image of the right cerebral hemisphere shows diffusely increased white matter echogenicity as well as accentuated gray-white matter differentiation. (b) Coronal grayscale ultrasound image of the brain in a second patient reveals diffusely increased parenchymal echogenicity with decreased gray-white matter differentiation and slit-like frontal horns of the lateral ventricles (arrowheads). (c) Axial diffusion-weighted MR image depicts restricted diffusion involving the frontal lobes, the insulae, left occipital lobe and thalami (arrowheads)
Severe cerebral edema in a 12-day-old full-term male . (a) Coronal grayscale ultrasound image demonstrates diffusely abnormal increased echogenicity of the cortical gyri (asterisks) and effacement of the CSF spaces consistent with cerebral hypoxic–ischemic injury. (b) Axial CT image of the brain demonstrates generalized loss of gray–white matter differentiation and sulcal effacement consistent with severe hypoxic–ischemic injury. A small amount of layering blood (arrowhead) is seen in the left occipital horn
Focal Hypoxic–Ischemic Injury
Arterial Ischemic Stroke
Acute ischemic stroke (AIS) is an acute disturbance of neurological function with symptoms lasting more than 24 hours. Once thought of as a rare condition in the pediatric population, AIS is now recognized as one of the top ten leading causes of death in children [44]. Clinical presentation differs depending on age. Infants present with nonspecific symptoms such as seizures, hypotonia, lethargy, or, most often, no clinical symptoms at all. Older children can present in a fashion similar to adults, but due to nonspecific symptoms, the diagnosis of stroke is often delayed.
There are two categories of neonatal acute ischemic stroke (NAIS): perinatal or presumed perinatal. Perinatal NAIS is an acute arterial ischemic stroke event occurring anywhere from 20 weeks of fetal life to the end of the neonatal period (28 days). Presumed perinatal NAIS is an acute arterial ischemic stroke event presenting clinically in an infant more than 28 days of age with signs of chronic infarction on neuroimaging. Therefore, presumed perinatal NAIS is diagnosed retrospectively.
Patients with perinatal stroke are often male. Approximately 70% of the time, the perinatal stroke occurs via the anterior circulation and 73% of the time it involves the left hemisphere (especially the MCA territory) [45]. Pediatric patients with presumed perinatal stroke either have no clinical symptoms or present with hemiparesis. Etiologies of presumed NAIS include congenital heart disease and hypercoagulable states. The etiology remains unknown in about half of the cases [45].
The ultrasound findings of early NAIS are subtle. Asymmetric echogenicity of a focal region of the brain such as the thalamus (Fig. 2.38) or the periventricular white matter can be identified (Fig. 2.39). MR imaging is recommended for confirmation and further characterization of abnormalities.
Thalamic stroke in a 2-day-old female. (a) Coronal grayscale ultrasound image shows subtle increased echogenicity (arrowhead) of the right thalamus in comparison to the normal hypoechoic left thalamus. (b) Axial diffusion-weighted MR image demonstrates a small area of restricted diffusion (arrow) in the right thalamus consistent with acute ischemia or infarction
Perinatal middle cerebral artery (MCA) stroke in a 2-day-old male. (a) Coronal grayscale ultrasound image at the level of the posterior third ventricle displays an asymmetrical slit-like left lateral ventricle (arrowhead) and increased echogenicity (arrow) of the left frontoparietal periventricular white matter. (b) Axial diffusion-weighted MR image demonstrates restricted diffusion involving the left MCA territory (asterisk) consistent with acute infarction
Venous Sinus Thrombosis
Venous sinus thrombosis is rare in the pediatric population, with neonates accounting for up to 40% of venous sinus thrombosis cases [46]. There is under-diagnosis of venous sinus thrombosis due to the nonspecific and variable presentation of patients, suboptimal diagnostic imaging techniques, and rapid recanalization of the cerebral veins. Sagittal sinus thrombosis is the underlying cause in 65% of cases.
Clinical presentation is nonspecific and varies greatly, but may include seizures, altered mental status, focal neurological symptoms, headache, lethargy, and vomiting. In neonates, birth trauma can cause cortical vein disruption and venous sinus thrombosis. In older children, common head and neck infections causing fever, dehydration, and anemia can lead to venous sinus thrombosis. Chronic illnesses such as a hypercoagulable state, systemic lupus erythematosus, congenital heart disease, and nephrotic syndrome, also increase the risk of venous sinus thrombosis.
On ultrasound, venous thrombosis typically appears as a hyper- to hypoechoic intraluminal focus, depending on the age of the hemorrhage, with associated absence of flow on color and spectral Doppler evaluation (Fig. 2.40a–c). When the thrombus is non-occlusive, it is outlined on color Doppler imaging. Parenchymal venous infarction is a complication of cerebral venous thrombosis. On ultrasound, venous infarction demonstrates increased patchy parenchymal echogenicity extending toward the cortex.
Superior sagittal sinus thrombosis in a 6-week-old male. Coronal (a) and sagittal (b) high-resolution grayscale ultrasound images demonstrate abnormally increased echogenicity (arrowhead, asterisks) within the superior sagittal sinus. (c) Sagittal color Doppler ultrasound image shows a complete lack of flow (asterisks) in the superior sagittal sinus consistent with occlusive thrombosis. (d) Sagittal T1-weighted MR image demonstrates extensive heterogeneously hyperintense signal (arrows) within the superior sagittal sinus
Ultrasound can be an excellent imaging modality to detect thrombosis when the involved vessels can be adequately identified and imaged. However, due to the limited acoustic windows of the cranial vault, it can be challenging to detect and visualize the entire extent of thrombosis involving the posterior aspects of the dural sinuses and the small cortical veins. When cortical vein thrombosis is identified by ultrasound, MR imaging should subsequently be performed to fully characterize the extent of thrombosis (Fig. 2.40d).
Treatment of dural sinus thrombosis is often conservative with attention paid to correcting the underlying cause of thrombosis. When indicated, anticoagulant and thrombolytic therapy can be administered.
Sickle Cell Disease
Sickle cell disease is an inherited red blood cell disorder that at low oxygen levels distorts the red blood cells into a crescentic or sickle shape. Sickle-shaped red blood cells adhere to one other, causing arterial wall damage and blockage. Pediatric patients with sickle cell disease have a risk of stroke that is approximately 250 times higher than that of a healthy child [47]. The risk of stroke increases after 2 years of age, once the protective effect of fetal hemoglobin is no longer present. One in ten patients with homozygous sickle cell disease experiences a stroke before the age of 20 years with often devastating consequences [48].Stroke Prevention in Sickle Cell Anemia (STOP) was a multicenter randomized trial initiated in 1995 that successfully demonstrated the reliability of transcranial Doppler (TCD) to stratify patients with sickle cell disease at risk for developing stroke. Furthermore, it showed the efficacy of blood transfusion as a treatment to reduce risk.
TCD is a simple, inexpensive, fast, and effective way to monitor the cerebral vessels and guide therapeutic decisions regarding blood transfusion treatment to reduce the risk of stroke in patients with sickle-cell disease. TCD ultrasound is performed through the temporal squamosal bone via a 2–6 MHz transducer in children between 2 and 16 years of age. With color Doppler, the circle of Willis (Fig. 2.41) can be identified to sample the velocities of the major cerebral arteries, particularly the distal internal carotid artery and middle cerebral artery.
Based on the STOP I [49] and STOP II [50] trials, the time-averaged mean of the maximum velocity (TAMMX) of the terminal internal carotid artery or middle cerebral artery is measured and interpreted as follows (Table 2.3): normal if all mean velocities are less than 170 cm/sec, therefore repeat annually; low conditional if at least one mean velocity is 170–185 cm/sec, therefore repeat in 3–6 months; high conditional if at least one mean velocity is 186–199 cm/sec, therefore repeat in 1–3 months; abnormal if at least one mean velocity is 200 cm/sec or higher, therefore repeat within 1–2 weeks; and inadequate if no readings from the right or left middle cerebral or internal carotid arteries could be obtained. An abnormal TAMMX greater than 200 cm/s has been associated with a 40% chance of stroke within 3 years [51].
Diagram of the arterial supply to the brain . The circle of Willis forms a circulatory anastomosis between the anterior and the posterior arterial systems via the anterior and the posterior communicating arteries. The internal carotid arteries supply the anterior circulatory system. The vertebral arteries supply the posterior circulatory system. During transcranial Doppler (TCD) examination, the circle of Willis is identified with color Doppler, and velocities of the major cerebral arteries are sampled, with particular attention paid to the distal internal carotid and middle cerebral arteries
It is thought that an elevated TAMMX (Fig. 2.42) in patients with sickle cell disease is due to anemia, vessel stenosis caused by a damaged wall , and/or vessel dilation caused by hypoxia. Transfusion reduces TAMMX by improving these abnormalities to some degree and may explain the successful treatment response of reducing the stroke risk in these patients [52, 53].
Transcranial Doppler (TCD) ultrasound images of a 6-year-old male with sickle cell anemia. (a) Color and spectral Doppler ultrasound image obtained via a transtemporal window demonstrates the circle of Willis. Normal arterial waveforms are depicted in the right terminal internal carotid artery with the time-averaged mean of the maximum velocity (TAMMX) measuring 110 cm/s. (b) Color and spectral Doppler ultrasound image obtained via a transtemporal window reveals an abnormally increased TAMMX in the right middle cerebral artery measuring 202 cm/s
Infectious Brain Disorders
Overall, 2–3% of congenital brain anomalies are due to perinatal infection [54]. When the infection is transmitted in the first or second trimesters of pregnancy, the neuroepithelium is destroyed, leading to a spectrum of hypoplasia, defective organogenesis, congenital malformations, and migration disorders. When the infection is transmitted in the third trimester, destructive processes occur in the brain parenchyma, such as gliosis, necrosis, and dystrophic parenchymal calcifications.
Viral Infections
The most common congenital viral infections are referred to as TORCH infections: Toxoplasmosis, Other, Rubella, Cytomegalovirus (CMV), and Herpes simplex virus (HSV). The “Other” infections include syphilis, varicella-zoster, mumps, parvovirus B19, and human immunodeficiency virus (HIV). Most TORCH infections cause mild symptoms in pregnant mothers but can lead to serious morbidity and mortality in the fetus. TORCH infections are transmitted via the placenta with the exception of HSV and HIV which are acquired during passage through an infected birth canal at the time of delivery.
Most of the imaging findings of TORCH infections are nonspecific, and diagnosis generally requires specific antibody detection and viral cultures. However, there are certain features that are characteristic of the different congenital infections that can help guide further patient evaluation. CMV is the most common TORCH infection, affecting almost 1% of all newborns in the United States [55]. The second most common TORCH infection is toxoplasmosis.
The pre- and postnatal ultrasound imaging findings of CMV infection include periventricular calcification and subependymal cysts (Fig. 2.43) [56]. Eventually, gliosis occurs leading to brain atrophy, which then causes prominent CSF spaces, ventricular dilation, and microcephaly. Mineralized thalamostriate arteries appear as echogenic, linear branching structures (Fig. 2.44). This appearance of the thalamostriate vessels is not specific to CMV infection and has been reported in infants with a variety of other conditions [57], as well as a normal variant.
Other imaging findings seen in infants with congenital CMV infection include lissencephaly and localized polymicrogyria. Toxoplasmosis causes similar imaging findings but more characteristically results in cortical and basal ganglia calcifications, as well as hydrocephalus in some cases. Inflammation of the ventricles causes hydrocephalus due to obstruction of CSF flow.
Congenital cytomegalovirus (CMV) in a 13-day-old boy. (a) Sagittal grayscale ultrasound image reveals an enlarged lateral ventricle with subependymal cysts (arrowhead) and calcifications (arrow). (b) Coronal T2-weighted MR image demonstrates punctate dark signal (arrow) corresponding to calcification in the periventricular region. Hyperintense subependymal cysts (black arrowhead) are noted along with gliosis. There is polymicrogyria (white arrowheads) in both frontal lobes. (c) Sagittal T1-weighted MR image shows extensive subependymal cysts and gliosis (arrows) in the periventricular region, with associated ex vacuo dilation of the lateral ventricle (V)
Mineralized thalamostriate vessels in a 32-week gestational age male with congenital cytomegalovirus (CMV) infection. Sagittal grayscale ultrasound image shows a branching pattern of linear, echogenic vessels (arrows) in the thalamus. This is a nonspecific finding that can be seen in a number of clinical settings, including CMV infection as well as a normal variant
HSV type 2 (HSV-2) is a leading cause of neonatal meningoencephalitis transmitted via an infected birth canal. HSV-2 infection is a more common cause of meningoencephalitis in neonates, while HSV type 1 (HSV-1) infection is more common in immunocompromised older children and adults. Newborns infected with HSV-2 have a late-onset presentation, often 2 weeks after birth, with symptoms of lethargy, irritability, seizures, apnea, and fever. The mortality rate is up to 15% [58]. HSV-2 causes nonspecific zones of cerebral edema, which can destroy gray and white matter and lead to cystic changes (Fig. 2.45) [59]. Unlike HSV-1, the temporal lobes are not involved.
Herpes simplex virus type 2 (HSV-2) meningoencephalitis in a 17-day-old male. (a) Coronal grayscale ultrasound image shows abnormalities of both cerebral hemispheres, more on the left, characterized by increased echogenicity of the white matter and cystic changes (asterisk) extending from the ependymal surface to the subcortical white matter. There is sulcal (S) thickening of the left cerebral hemisphere with loss of normal gray–white matter differentiation. (b) Coronal contrast-enhanced, T1-weighted, fat-suppressed MR image demonstrates diffuse leptomeningeal enhancement (arrowheads), consistent with meningitis
Newly emerging viruses affecting newborns include Zika virus, enterovirus, and human parechovirus-3. Zika virus is a member of the mosquito-borne flavivirus family. Infection during pregnancy causes microcephaly and congenital brain lesions, including cortical malformations, callosal dysgenesis, and ventriculomegaly [60].
Bacterial Infections
Meningitis, an inflammation of the pia-arachnoid and CSF spaces, is a late manifestation of neonatal sepsis. Since the introduction of Haemophilus influenzae type b (Hib) vaccination, H. influenzae is no longer the leading cause of neonatal meningitis in the United States. Common causative organisms are Group B streptococci (50%), Escherichia coli (20%), and Listeria monocytogenes (10%) [61]. Less common bacterial infections include Enterococci and Staphylococcus aureus. Cronobacter sakazakii is a class of Enterobacteriaceae which has been recently linked to powdered infant formula. C. sakazakii can cause periventricular hemorrhage, ischemic injury, and cerebral abscess [62].
In sepsis, there is bacterial seeding to the choroid plexus, resulting in CSF infection and ventriculitis. As an initial response to the infection in the brain, inflammatory exudate accumulates in the sulci, causing sulcal thickening (>2 mm) and increased echogenicity [63]. Sulcal thickening is the earliest cranial ultrasound finding of meningitis (Fig. 2.46).
In the acute phase of bacterial meningitis, there is increased CSF production and decreased CSF resorption, causing enlargement of the ventricles. In the later phase of meningitis, exudates in the ventricles can form septations resulting in obstructive hydrocephalus. On ultrasound, ventriculitis manifests as thickened, irregular walls of the ependymal lining of the ventricles. Once infection spreads to the meninges and subarachnoid spaces, other complications occur, such as empyema formation, cerebritis, cerebral abscess, venous thrombosis, and infarction.
On ultrasound imaging, these complications (especially small empyemas) are difficult to differentiate from subdural effusions. However, use of a high-frequency linear transducer permits delineation of a large empyema and its internal complexity (Fig. 2.47), which is helpful in differentiation from a simple, anechoic subdural effusion. A subdural effusion is generally reactive, sterile, and of no clinical significance. A brain abscess is a rare complication of meningitis. On ultrasound, an abscess appears as a heterogeneous collection within the brain parenchyma with a thick rim and hypoechoic contents that may include a fluid-fluid level or debris (Fig. 2.48).
Fungal Infections
CNS fungal infections are a less common cause of meningoencephalitis compared to bacterial infections in neonates. The most common is Candida albicans, which affects premature and immunocompromised infants. Premature infants with candida infection can present with seizures, poor feeding, irritability, and bradycardia. Microabscesses are difficult to visualize with ultrasound, but complications of obstructive hydrocephalus or infarction can be seen. Treatment includes antifungal and supportive therapy and if there is obstructive hydrocephalus, shunting is considered.
Neoplastic Brain and Ventricular Disorders
Neoplasms of the Brain
Although brain neoplasms are a leading cause of death in the pediatric population, brain neoplasms in neonates are rare, accounting for less than 1% of brain tumors in children [64]. With the advent of prenatal ultrasound and MR imaging, the prenatal diagnosis of brain tumors has been increasing in frequency. In these patients, postnatal MR imaging of the brain is acquired for management purposes. Depending on the location and grade of the brain tumor, therapy includes a combination of surgery, chemotherapy, and/or radiation.
Two-thirds of brain neoplasms in neonates occur in the supratentorial region, whereas in older children there is a predilection for the infratentorial region [65]. Common neonatal brain neoplasms include teratoma, astrocytoma, embryonal tumors, and choroid plexus papilloma. Affected children present with a rapidly increasing head circumference, bulging fontanelles, vomiting, and focal neurological symptoms, including seizures.
Cranial ultrasound is helpful for the screening of CNS neoplasms but has a limited role in pretreatment characterization, which is best accomplished by MR imaging. However, identification of the location of the tumor can help narrow the differential diagnosis. Teratomas commonly occur in the suprasellar and pineal regions and contain mixed solid and cystic foci with calcification and fat. Astrocytomas arise from the optic pathways, particularly in patients with neurofibromatosis type 1, as well as from the thalamus and hypothalamus. Less frequent tumors include ependymoma, germinoma, ganglioglioma, and meningioma.
Neoplasms of the Ventricle
Ventricular tumors arise from the choroid plexus, particularly from the trigone of the lateral ventricle in children as compared to the fourth ventricle in adults [66]. The majority of choroid plexus tumors are papillomas rather than carcinomas.
Ultrasound demonstrates an enlarged, lobulated choroid plexus mass with associated ventriculomegaly due to increased CSF volume and/or obstruction (Fig. 2.49). Prominent vascularity can be seen within the tumor with color Doppler. Spinal drop metastases occur with both papilloma and carcinoma, although they are more common with carcinoma [67]. MR imaging of the brain and spine must be performed prior to surgical intervention.
Choroid plexus papilloma in a 3-month-old female. Sagittal (a) and coronal (b) grayscale ultrasound images demonstrate a well-circumscribed, homogenously echogenic mass (asterisks) extending from the trigone (arrowhead) to the temporal horn of the right lateral ventricle (LV). The left lateral ventricle is dilated. (c) Sagittal contrast-enhanced, T1-weighted MR image shows avid enhancement of the mass (asterisk) extending from the trigone of the right lateral ventricle to the temporal horn (arrow). There is surrounding edema (arrowheads) in the right parietal, temporal, and occipital lobes. (d) Coronal contrast-enhanced, T1-weighted, fat-suppressed MR image shows the mass (asterisk) with surrounding edema (arrowheads), leftward midline shift, and left lateral ventricular (LV) enlargement
Vascular Brain Disorders
The International Society for the Study of Vascular Anomalies (ISSVA) classification of vascular anomalies is an attempt to categorize the two main groups of disorders, vascular tumors and malformations, using a consistent nomenclature. Since Mulliken and Glowacki first classified these lesions in 1982 [68], their description has been repeatedly updated, most recently in 2018 [69], by incorporating new knowledge of genetic disorders into the classification.
The most important vascular neoplasm affecting the cranium is infantile hemangioma, which is discussed later in this chapter under vascular scalp lesions. Vascular malformations are further categorized into high-flow and low-flow lesions. High-flow malformations include arteriovenous malformation (AVM) and arteriovenous fistula (AVF). Low-flow malformations include venous malformation (VM), lymphatic malformation (LM), and capillary malformation (CM). These high- and low-flow malformations can be solitary (simple) or occur as part of a more complex disorder (combined). Many syndromes are associated with vascular anomalies, including Klippel–Trenaunay syndrome and Sturge–Weber syndrome.
High-Flow Malformations
AVM is a congenital high-flow vascular anomaly that lacks a normal capillary network, and has innumerable small, abnormal AV connections that bypass a normally controlled, high-resistance vascular bed. AVF is a direct connection between an artery and a vein without an intervening capillary bed. Patients with a high-flow malformation typically present with high-output cardiac failure, neurological deficits, and seizures. There is an increased risk of hemorrhage and vascular steal phenomena, resulting in ischemia and hydrocephalus.
Vein of Galen malformation (VOGM) consists of dilation of the median prosencephalic vein associated with AVFs within the wall of the vein or multiple shunts communicating with the anterior portion of the vein. There are two main types of VOGM: choroidal (type 1) and mural (type 2) based on feeding vessels and location of the shunts. Approximately 80% of VOGM are of the choroidal type [70].
Choroidal VOGM has multiple arterial feeders from the thalamoperforator, choroidal, pericallosal, and anterior cerebral arteries, forming AVFs to the median prosencephalic vein. This is a high-flow lesion that can lead to high-output congestive heart failure and hydrops immediately after birth. In the rarer mural type of VOGM, there are fewer arterial feeders connecting to the median prosencephalic vein. Mural VOGM presents later in life with clinical symptoms of hydrocephalus or seizure and does not cause high output heart failure.
On fetal and postnatal ultrasound, a markedly dilated, cystic vascular lesion is seen in the midline, posterior to the third ventricle (Fig. 2.50). Spectral Doppler evaluation reveals disordered, arterialized blood flow within the aneurysmally dilated portion of the malformation and arterialization of the draining veins (Fig. 2.50d). In the choroidal type, significantly increased flow within the arterial feeders supplying the lesion is seen. On parasagittal or mastoid views, abnormal dilation of the falcine and straight sinuses and torcular herophili is seen.
On grayscale images, parenchymal calcifications and encephalomalacia related to chronic ischemic brain injury are sometimes observed. Subarachnoid and intraparenchymal hemorrhage are occasionally seen, as the vessels of the malformation are fragile and tend to bleed easily.
Vein of Galen malformation in a 3-day-old male. (a) Coronal grayscale ultrasound image shows a dilated cystic lesion (asterisk) posterior to the third ventricle. (b) Coronal color Doppler ultrasound image demonstrates the vascular nature (asterisk) of the lesion. (c) Sagittal color Doppler ultrasound image shows multiple arterial feeders from thalamoperforator, choroidal, pericallosal (arrowhead), and anterior cerebral arteries supplying the malformation (asterisk). (d) Sagittal color and spectral Doppler ultrasound image of the brain reveals arterialized flow in the straight sinus. (e) Frontal radiograph of the chest shows cardiomegaly related to high-output congestive heart failure
Management of VOGM includes treatment of congestive heart failure and endovascular coiling of the lesion. Ultrasound imaging is useful in follow-up to assess the response to endovascular treatment.
Dural AVF is an abnormal direct connection between an artery and a draining vein, usually involving the meningeal arteries, with drainage into the transverse or sigmoid sinuses.
Low-Flow Malformations
The most commonly encountered low-flow malformations in the brain are developmental venous anomaly (DVA), cavernous malformation, and capillary telangiectasia. None of these lesions is detectable with ultrasound and they are typically diagnosed by MR imaging.
Hydrocephalus
CSF is mainly produced by the ependymal lining and choroid plexus of the lateral, third, and fourth ventricles, with the remainder produced by the arachnoid lining of the brain and spine. CSF flows from the lateral ventricles into the third ventricle via the foramen of Monro, into the fourth ventricle via the cerebral aqueduct, and through the cisterna magna and basal cisterns via the foramina of Magendie and Luschka.
Hydrocephalus develops when there is an obstruction to the flow of CSF, or when there is an imbalance between CSF production and resorption. There are two types of obstructive hydrocephalus: non-communicating and communicating.
Non-communicating hydrocephalus occurs when there is a blockage along the ventricular pathway of CSF flow, typically at the narrowest sites such as the foramina of Monro, cerebral aqueduct, and the outlet of the fourth ventricle.
Communicating hydrocephalus occurs when there is inadequate reabsorption of CSF, with obstruction in the non-ventricular pathway of CSF flow, typically as a result of scarring or fibrosis in the subarachnoid space that can follow hemorrhage or infection (e.g., meningitis), or by CSF seeding of tumor. Rarely, it may be due to functional impairment of the arachnoidal granulations which are located along the superior sagittal sinus and are the site of CSF reabsorption into the venous system.
Ventricular size can be monitored through serial cranial ultrasound examinations. Ultrasound imaging is also helpful in differentiating between ex vacuo dilation from periventricular white matter loss and progressive hydrocephalus due to an obstructive lesion.The Levene index is used to measure ventricular size in infants up to 40 weeks of gestational age [71]. It is measured on a coronal image at the level of the foramen of Monro as the horizontal length from the midline falx to the most lateral margin of the frontal horn. After 40 weeks of gestational age, the ventricular index (VI) is used. This is the ratio of the distance between the most lateral aspect of the ventricles divided by the bi-parietal diameter.
Additional popular methods include the anterior horn width (AHW) and thalamo-occipital distance (TOD) [72]. AHW is measured as the oblique distance of the widest width of the anterior horn of the lateral ventricle on a coronal image (Fig. 2.51a). Thalamo-occipital distance (TOD) is measured from the outer margin of the thalamus abutting the choroid plexus to the outer margin of the occipital horn on a parasagittal image (Fig. 2.51b). AHW and TOD are more sensitive in detecting progressive ventricular dilation compared with VI [73]. AHW greater than 6 mm is considered abnormal. Given that the occipital horn is often the first to dilate after hemorrhage, the measurement of TOD has a potentially important clinical role [74, 75].
Measurement of the anterior horn width (AHW) and thalamo-occipital distance (TOD). (a) Coronal grayscale ultrasound image demonstrates AHW which is the oblique distance (solid white line) of the widest width of the anterior horn of the lateral ventricle. (b) Sagittal grayscale ultrasound image demonstrates the TOD which is the oblique distance (solid white line) from the outer margin of the thalamus abutting the choroid plexus to the outer margin of the occipital horn
Fifteen percent of preterm infants with severe PIVH develop progressive hydrocephalus [76]. In this group of patients, CSF drainage can improve cerebral blood flow and possibly reduce further brain injury. Treatment involves shunt catheter placement to divert the flow of CSF and thereby decrease intracranial pressure . A ventriculoperitoneal catheter is commonly used to divert CSF to the peritoneal cavity. In patients with cerebral aqueductal stenosis, endoscopic third ventriculostomy can be performed.
Benign External Hydrocephalus
Benign external hydrocephalus (BEH) , also known as benign macrocrania of infancy, is a condition defined as prominent CSF spaces with associated macrocephaly in infancy. The etiology is unclear but is thought to be due to delayed CSF reabsorption by immature arachnoid villi. There is often a family history of macrocephaly. Males are affected more frequently than females. BEH is the most common cause of macrocephaly, with infants presenting from 2 to 7 months of age with a head circumference above the 95th percentile. These patients are typically neurologically normal other than an occasional transient delay of psychomotor development [77]. The condition usually resolves by the age of 2 years.
Ultrasound is the modality of choice for evaluating suspected BEH . Findings include prominent, bilaterally symmetric subarachnoid spaces along the frontoparietal convexities and a widened interhemispheric space (Fig. 2.52a). The remainder of the study is normal, with no evidence of obstructive hydrocephalus.Use of a high-frequency linear array transducer with Doppler is helpful in demonstrating the cortical veins crossing a prominent CSF space to enter the superior sagittal sinus and thereby excluding a chronic subdural fluid collection or hygroma (Fig. 2.52b). In addition, an interhemispheric width (IHW) measurement can be obtained. An IHW greater than 5.0 mm in neonates or 8.5 mm in 1-year-olds is considered abnormal [78]. BEH is a self-limited condition that typically does not require intervention. Rarely, patients with benign external hydrocephalus can present with a subdural hematoma [79].
Benign external hydrocephalus in a 2-month-old male with a rapidly enlarging head circumference. (a) Coronal grayscale ultrasound image demonstrates prominent symmetric CSF spaces (asterisks) over the frontoparietal convexities with widening of the interhemispheric space. (b) Coronal color Doppler ultrasound image demonstrates cortical veins (arrowheads) coursing through the prominent CSF spaces. There is no displacement of these veins to suggest a chronic subdural fluid collection or hygroma. S, Superior sagittal sinus
Scalp Masses
“Lumps and bumps” of the scalp are a common complaint and a source of concern for many parents. Scalp lesions tend to be small, and ultrasound provides superb resolution when compared to other imaging modalities.
Since scalp lesions are often superficial, a high-frequency (9–3 MHz, 12–5 MHz, or 17–5 MHz) linear array transducer is typically used with a copious amount of transducer gel. Imaging can be optimized by centering the focal zone of the ultrasound transducer at the depth of the lesion. For soft tissue or vascular scalp masses, color and spectral Doppler imaging should be performed to assess for vascular flow and to identify the waveforms as arterial and/or venous.
Characterization of a scalp lesion depends on patient age, laterality, and imaging appearance. Some lesions may require biopsy or resection in order to obtain a final diagnosis. Congenital scalp lesions usually present under the age of 5 years [80, 81]. Most are benign and include birth trauma-related hematoma (including ossified cephalohematoma), dermoid/epidermoid cyst, cephalocele, reactive lymph nodes, hemangioma, and sinus pericranii. In patients older than 5 years of age, aggressive lesions are more frequently seen, such as Langerhans cell histiocytosis, metastasis, and primary bone tumor of the cranial vault.
Congenital Scalp Lesions
Dermoid/Epidermoid Cyst
Dermoid and epidermoid cysts are the most commonly encountered masses in the scalp and skull in the pediatric population [82]. They are not true neoplasms, consisting of sequestrations of stratified squamous epithelium. The main difference between the two lesions is the presence of epithelial appendages in dermoid cysts [83]. Dermoid cysts tend to occur near the midline and close to sutures [84], while epidermoid cysts occur further from the midline in the lateral skull/scalp. Affected patients often present for imaging after a mass is incidentally noted by care providers. Patients are generally asymptomatic, and the lesion is non-tender when palpated.
Based on ultrasound imaging alone, the two entities cannot be differentiated. Both lesions appear as a well-circumscribed, thin-walled cyst without vascular flow (Fig. 2.53). The internal contents are anechoic to slightly echogenic. The cyst tends to abut the skull, which causes smooth bone remodeling without cortical destruction. Surgical excision is performed for both diagnosis and treatment [82].
Dermoid cyst in a 5-month-old male . Transverse grayscale ultrasound image demonstrates a well-circumscribed, thin-walled cystic structure (D) in the subcutaneous tissues of the scalp without vascular flow (not shown). The lesion abuts the skull without associated cortical destruction. An intact right lambdoid suture (arrow) is identified
Cephalocele
A cephalocele is an umbrella term used to describe outward herniation of the intracranial contents through osseous defects in the cranial vault or skull base. Depending on the herniated intracranial contents, cephaloceles are further categorized as meningoencephalocele or encephalocele (brain parenchyma); meningocele (meninges and CSF); gliocele (CSF); and atretic (dura, fibrous tissue, and atretic brain tissue). Common locations are near the midline in the occipital , parietal, and frontonasal regions. When a cephalocele is small, it is difficult to differentiate from a dermoid or epidermoid cyst on physical examination, especially when it is located in the midline.
The role of ultrasound imaging is to assess for underlying osseous defects of the cranial vault and to characterize the herniated intracranial contents. Unlike a dermoid or epidermoid cyst, a cephalocele is associated with a skull defect that allows the cephalocele to communicate with the underlying intracranial structures.
A nasal glioma is similar to a cephalocele but with an absence of intracranial connections. Nasal glioma contains dysplastic glial cells and typically occurs at the bridge of the nose (Fig. 2.54). Surgical resection is the treatment of choice [85].
Nasal glioma in a 6-day-old male. (a) Transverse grayscale ultrasound image demonstrates a left paramedian heterogeneous soft tissue mass (G), which extends into the nasal cavity (N) through a defect (arrow) in the nasal bone. (b) Sagittal T2-weighted, fat-suppressed MR image shows a soft tissue mass (G) at the bottom of the nasal bridge with extension into the nasal cavity (N). A thin fibrous stalk (arrow) arising from the mass and connecting to the dura is identified without an associated CSF component. The signal characteristics of the lesion were similar to gray matter on all MR imaging sequences
Lymph Node
A benign lymph node in the scalp is a common lump noticed by parents and caretakers. As elsewhere in the body, a benign lymph node demonstrates a central fatty hilum, a short axis length of less than 10 mm (except for submental and submandibular nodes that can measure up to 15 mm in short axis), and a smooth cortical contour. Abnormal size, loss of the central fatty hilum, and a cystic or necrotic appearance warrant further investigation.
Extracranial Birth Trauma
There are unique extracranial scalp and cranial vault injuries that occur in the setting of birth trauma. Hematoma can develop between the various layers of the scalp and cranial vault, including the subcutaneous fat of the scalp, the galea aponeurotica, the subgaleal fascia, and the periosteum of the cranial vault [86].
A hematoma localized to the subcutaneous tissues of the scalp is a caput succedaneum. Caput succedaneum occurs in up to 25% of vaginal births [87]. It is associated with a small volume of blood loss and resolves after 48–72 hours . On ultrasound imaging, a subcutaneous fluid collection is seen that crosses suture lines.
A subgaleal hematoma develops when bleeding occurs beneath the galea aponeurotica and is often associated with a vacuum-assisted vaginal delivery [88]. Subgaleal hematoma can result in massive blood loss within the subgaleal potential space that extends from the orbits to the occipital region . On ultrasound imaging, a sharply demarcated hematoma is seen crossing suture lines, and can shift with gravity or manual compression (Fig. 2.55).
A cephalohematoma occurs in the subperiosteal space of the outer table of the cranial vault, where the blood accumulates between the pericranium and the cranial bone. Analogous to an epidural hematoma, a cephalohematoma is confined by the periosteum and therefore does not cross suture lines (Fig. 2.56). Cephalohematoma occurs in 2–3% of newborns [89] and often resolves spontaneously after 2–3 weeks. When it persists beyond the perinatal period, a cephalohematoma can ossify (Fig. 2.57) and be incorporated into the outer table of the cranial vault; such patients present with a palpable, hard lump.
Partially ossifying cephalohematoma in a 20-day-old male born via vacuum-assisted extraction. Coronal color Doppler ultrasound image demonstrates a subperiosteal fluid collection (F) overlying the occipital bone. There is partial ossification (arrowhead) of the collection with associated posterior acoustic shadowing
Vascular Scalp Lesions
Infantile Hemangioma
Infantile hemangioma is a benign vascular tumor of small capillary-sized blood vessels. It is the most common head and neck vascular tumor of childhood. On the scalp, it appears as a bright red strawberry-like firm nodule, which is generally absent or small at birth but usually appears within the first 6 weeks of life.
On ultrasound, hemangioma demonstrates a well-circumscribed hypo- or hyperechoic mass with hyper-vascularity consisting of both arterial and venous waveforms on spectral Doppler analysis (Fig. 2.58). Unlike other vascular tumors, infantile hemangiomas usually involute spontaneously. Unless there are associated complications such as rapid growth with bleeding and/or ulceration, most infantile hemangiomas do not require treatment. When necessary, the majority of infantile hemangiomas will respond to oral beta-blockers (propranolol) [90].
Infantile scalp hemangioma in a 5-month-old male . (a) Longitudinal grayscale ultrasound image of the scalp demonstrates a well-circumscribed, hypoechoic mass (H) with mildly lobulated margins. (b) Longitudinal color Doppler ultrasound image reveals enlarged blood vessels both within and surrounding the mass. (c) Longitudinal color Doppler ultrasound image with spectral analysis shows low resistance arterial blood flow within the lesion
Infantile scalp hemangioma can occur as a component of PHACE syndrome, an association of disorders characterized by a large infantile hemangioma on the face, scalp, and/or neck, as well as defects in the brain, blood vessels, eyes, heart, and chest.
Sinus Pericranii
Sinus pericranii is an abnormal venous lake within the scalp that drains into the dural sinus through the transdiploic space of the skull [91]. It develops as a result of an abnormal communication between the intra- and extra-cranial veins, usually via an emissary transosseous vein. It is commonly located in the midline of the frontal bones of the skull or at the vertex. Affected patients present with a soft and boggy scalp mass, which dilates when the child cries and with any other maneuver that increases intra-abdominal pressure.
Anechoic tubular structures are seen on grayscale imaging, which demonstrate vascular flow on color Doppler imaging and venous waveforms on spectral waveform analysis (Fig. 2.59). Associated skull defects can be seen on plain radiography or CT.
Management is typically conservative as embolization or surgical resection can lead to complications such as parenchymal venous infarction [92].
Sinus pericranii in a 3-year-old female. (a) Coronal grayscale ultrasound image shows a well-defined anechoic lesion (S) in the subcutaneous tissues of the scalp. There is no underlying bone destruction. A patent sagittal suture (arrow) is seen abutting the lesion. (b) Coronal color Doppler ultrasound image reveals the vascular nature of the lesion (S) which is connected to a transcalvarial vessel (arrow) extending through the left parietal skull. The extra-calvarial portion of the lesion overlies the patent sagittal suture (asterisk). (c) Longitudinal color Doppler ultrasound image with spectral analysis reveals venous flow within the vessel. (d) Sagittal contrast-enhanced, T1-weighted, fat-suppressed MR image shows a homogenously enhancing vascular lesion (arrow) in the scalp near the vertex. Tiny transcranial vessels coursing through the left parietal skull are better visualized by ultrasound
Suture Evaluation
Craniosynostosis
Craniosynostosis is an abnormal early closure of the cranial sutures resulting in skull deformity. Craniosynostosis can be primary or secondary. Primary craniosynostosis is often idiopathic and can be further divided into syndromic and non-syndromic (isolated) forms, while secondary craniosynostosis is due to identifiable causes, such as underlying metabolic bone disease, skeletal dysplasia, or decreased intracranial volume from shunting or extensive brain injury.
The incidence of craniosynostosis is low: three to ten cases per 10,000 live births [93]. The syndromic form of primary craniosynostosis often involves more than one suture and presents with other clinical and radiographic findings, such as midface hypoplasia, hypertelorism, and/or limb abnormalities. Apert, Crouzon, Pfeiffer, and Saethre–Chotzen syndromes are commonly associated with craniosynostosis [94]. Patients with primary craniosynostosis typically present in the neonatal period with a misshapen skull. The secondary form of craniosynostosis can present later in infancy.
Requests for suture evaluation with ultrasound to exclude craniosynostosis have increased substantially following the advent of the “Safe to Sleep” and “Back to Sleep” campaigns to prevent sudden infant death syndrome (SIDS), which launched in 1994 with resultant increased rates of positional posterior plagiocephaly.
The cranial sutures are evaluated using a high-frequency transducer to assess the outer and inner tables of the skull. With craniosynostosis, there will be bony ridges instead of an outer and inner skull table due to premature suture closure (Fig. 2.60). Sagittal craniosynostosis is the most common abnormality, accounting for roughly 50% of non-syndromic primary craniosynostosis [95].
It is important to note that the metopic suture can normally close at as early as 3 months of age [96]. In infants more than 3 months of age, extreme caution should be exercised when diagnosing metopic suture craniosynostosis . A prominent osseous ridge in the expected location of the metopic suture should be observed, along with a trigonocephalic configuration of the skull.
Unilateral coronal craniosynostosis in a 6-week-old female. Transverse grayscale ultrasound images of the left coronal suture (a) near the midline demonstrate an abnormal bony ridge (arrow) in the expected location of the suture, and (b) complete bony fusion (arrow) near the left ear. (c) Transverse grayscale ultrasound image of the normal right coronal suture (arrow) demonstrates patency. (d) Frontal radiograph of the skull shows elevation of the superolateral corner of the left orbital wall (arrow), the so-called “harlequin eye” deformity due to near-complete fusion of the left coronal suture (arrowhead). (e) 3D reformatted CT image confirms near-complete fusion of the left coronal suture (arrowhead)
Positional Plagiocephaly
Positional plagiocephaly has increased in incidence in association with supine positioning of infants during sleep. It is defined as a deformation of the posterior or dependent portions of the skull without true craniosynostosis. It is important to exclude craniosynostosis in infants with plagiocephaly and to educate care providers to manage this entity conservatively by changing the sleep position of the infant [97].
Abbreviations
- 3D:
-
Three-dimensional
- AHW:
-
Anterior horn width
- AIS:
-
Acute ischemic stroke
- AVF:
-
Arteriovenous fistula
- AVM:
-
Arteriovenous malformation
- BEH:
-
Benign external hydrocephalus
- CM:
-
Capillary malformation
- CMV:
-
Cytomegalovirus
- CNS:
-
Central nervous system
- CSF:
-
Cerebrospinal fluid
- CT:
-
Computed tomography
- DVA:
-
Developmental venous anomaly
- ECMO:
-
Extracorporeal membrane oxygenation
- Hib:
-
Haemophilus influenza type b
- HIE:
-
Hypoxic ischemic encephalopathy
- HII:
-
Hypoxic ischemic injury
- HIV:
-
Human immunodeficiency virus
- HSV:
-
Herpes simplex virus
- IHW:
-
Interhemispheric width
- ISSVA:
-
International Society for the Study of Vascular Anomalies
- IVH:
-
Intraventricular hemorrhage
- LM:
-
Lymphatic malformation
- MCA:
-
Middle cerebral artery
- MR:
-
Magnetic resonance
- NAIS:
-
Neonatal arterial ischemic stroke
- PIVH:
-
Periventricular/intraventricular hemorrhage
- PVHI:
-
Periventricular hemorrhagic infarction
- PVL:
-
Periventricular leukomalacia
- SIDS:
-
Sudden infant death syndrome
- STOP:
-
Stroke Prevention in Sickle Cell Anemia
- TAMMX:
-
Time-averaged mean of the maximum velocity
- TCD:
-
Transcranial Doppler
- TOD:
-
Thalamo-occipital distance
- VI:
-
Ventricular index
- VM:
-
Venous malformation
- VOGM:
-
Vein of Galen Malformation
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Kim, H.H.R., Kim, W.G., Lee, E.Y., Phillips, G.S. (2021). Brain. In: Paltiel, H.J., Lee, E.Y. (eds) Pediatric Ultrasound. Springer, Cham. https://doi.org/10.1007/978-3-030-56802-3_2
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