Neonatal Cranial US

106 Review Article
Neonatal Cranial Ultrasound: Advanced

Techniques and Image Interpretation
Erica L. Riedesel1
1 Division of Pediatric Radiology, Department of Radiology, University Address for correspondence Erica L. Riedesel, MD, Division of
of Wisconsin School of Medicine and Public Health, Madison, Pediatric Radiology, Department of Radiology, University of
Wisconsin, United States Wisconsin School of Medicine and Public Health, 600 Highland
Avenue, Madison, WI 53792, United States
J Pediatr Neurol 2018;16:106–124. (e-mail: [email protected]; [email protected]).
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
Abstract Neonatal cranial ultrasound has become an essential part of the routine care of
Keywords neonates. Ultrasound is noninvasive, relatively inexpensive, and can be performed at
► cranial ultrasound the bedside. Addition of advanced ultrasound techniques such as use of high-frequency
► Doppler linear transducers, additional acoustic windows, and color and pulsed wave Doppler
► B-flow imaging can significantly improve image quality and diagnostic accuracy of cranial ultrasound.
► intraventricular This review will focus on these techniques and their application in the detection of
hemorrhage central nervous system pathology in the high-risk preterm and term neonates.
► germinal matrix
hemorrhage
► hypoxic-ischemic
injury
► ventriculomegaly
► meningitis
Introduction at corrected gestational age 36 to 40 weeks (term equivalent)

to screen for evidence of more severe white matter injury.1
Neonatal cranial ultrasound has become an essential part of Findings on the term equivalent ultrasound in conjunction
routine care in high-risk preterm and term neonates. Ultra- with magnetic resonance imaging (MRI) can be used to predict
sound is noninvasive, requires no sedation, and is relatively neurodevelopment outcomes.
inexpensive, making it the ideal primary diagnostic screen- In term infants, cranial ultrasound is suggested for evalua-
ing tool for intracranial pathology. Most importantly, ultra- tion of suspected intracranial hemorrhage, brain parenchymal
sound can be performed at the bedside with minimal abnormality, hypoxic-ischemic injury (HII), suspected ventri-
disturbance to the infant early in neonatal life and may be culomegaly, evaluation of congenital or acquired central ner-
repeated as often as necessary for serial imaging of the brain. vous system (CNS) infection, and surveillance of previously
There are no contraindications for cranial ultrasound. documented abnormalities including prenatal abnormalities.1
Neonatal cranial ultrasound may be performed at any time
in the neonatal period. In preterm, <32 weeks’ gestation, and
Basic Techniques in Neonatal Cranial
extremely low birth weight (ELBW) infants <1.5 kg, an initial
Ultrasound
screening cranial ultrasound is suggested in the first 4 to 7 days
of life with a repeat screening cranial ultrasound at 10 to 14 Neonatal cranial ultrasound should be performed by an
days.1 When used in this manner, cranial ultrasound has a near experienced sonographer familiar with normal ultrasound
100% sensitivity for the detection of severe intraventricular anatomy and the most frequently encountered anomalies of
hemorrhage (IVH) and severe white matter injury.2 If initial the neonatal brain. Details of basic technique and technical
screening ultrasound is normal, follow-up exam is suggested parameters have been established by the American College of
received Issue Theme Advanced Approaches to Copyright © 2018 by Georg Thieme DOI https://doi.org/
March 1, 2017 Pediatric Neuroimaging; Guest Editor, Verlag KG, Stuttgart · New York 10.1055/s-0037-1604488.
accepted after revision Justin Brucker, MD ISSN 1304-2580.
June 5, 2017
published online
August 14, 2017
Neonatal Cranial Ultrasound Riedesel 107
Radiology, Society of Pediatric Radiology, Society of Radiol- still images, are helpful as complex or subtle findings may be
ogists in Ultrasound, and American Institute of Ultrasound in better appreciated in the “real-time scanning” context.2,3
Medicine.1
Cranial ultrasound begins with grayscale imaging of the
Advanced Techniques in Neonatal Cranial
brain using a sector transducer via the anterior fontanel. The
Ultrasound
anterior fontanel, located in the calvarial vertex at the
junction of the coronal and sagittal sutures, is the largest High-Frequency Linear Transducer
fontanel and provides an optimal sonographic window for Although the use of a low-frequency sector transducer allows a
global overview of the neonatal brain. The small footprint of more global view of cerebral architecture, this comes at a loss of
the sector transducer is well matched to the size of the image resolution. In contrast, coronal and sagittal images
anterior fontanel. In addition, the relatively low ultrasound through the anterior fontanel performed with a high-frequency
frequency (8–5 MHz) of the sector transducer allows visua- linear transducer (9 MHz or more) allows better resolution and
lization of intracranial structures that are relatively deep to more detailed visualization of structures in the near field and
the anterior fontanel such as the brain stem and cerebellum. midline.2–5 This technique allows optimal evaluation of the
In the coronal plane, images are obtained from anterior to deep gray structures of the basal ganglia, lateral ventricles, and
posterior, beginning at the frontal lobes just anterior to the periventricular white matter and allows more detailed assess-
frontal horns of the lateral ventricles and extending to the ment of gray–white matter differentiation in the cortex and
occipital lobes posterior to the lateral ventricles. Imaging in subcortical white matter (►Fig. 1). This additional imaging
the sagittal plane begins with a midline sagittal view that significantly increases diagnostic capability of neonatal cranial
includes the corpus callosum, third and fourth ventricles, ultrasound in both preterm and term infants.
brain stem, and cerebellar vermis. Sequential images are By decreasing the depth of field and optimizing focal zone
then obtained through the right and left cerebral hemi- depth, high-frequency linear transducers may also be used
spheres, respectively, sweeping through the lateral ventri- for detailed evaluation of the superficial extra-axial space
cles, periventricular white matter, and peripheral cortex to and the superior sagittal sinus just deep to the anterior
the Sylvain fissures.1 Cine clips, in addition to representative fontanel (►Fig. 2).3–6
Fig. 1 Routine neonatal cranial ultrasound. (A, B) Coronal and sagittal planes with 7-MHz sector transducer and (C, D) coronal and sagittal
planes with 9 MHz linear transducer. Imaging with higher frequency transducer allows more detailed evaluation of brain anatomy and gray-white
matter differentiation in the cortex and subcortical white matter.
Journal of Pediatric Neurology Vol. 16 No. 2/2018

108 Neonatal Cranial Ultrasound Riedesel
PSV–EDV/PSV).3,7 The RI is influenced by many factors in-

cluding flow velocity, cerebral blood flow volume, peripheral
vascular resistance, and cerebral autoregulation. Thus, spec-
tral Doppler evaluation of the intracranial arteries may
provide important physiologic information in evaluation of
the neonatal brain.
Relatively low intracerebral diastolic flow velocities in the
premature circulation explain the relatively high ACA RI seen
in the normal preterm brain of 0.7 to 0.8 (►Fig. 4A).2,7,8 As
the brain matures and the neonate undergoes physiologic
transition from fetal to newborn intracerebral circulation,
the normal ACA Doppler RI decreases to 0.7 to 0.75
(►Fig. 4B). Over the first year of life, RI in the ACA will
continue to decrease to a normal value of 0.6 in children aged
Fig. 2 Detailed evaluation of the superficial cortex, corpus callosum, 1 year and eventually reaches a normal value of 0.45 to 0.6
and extra-axial space is possible with optimized depth of field and
in children aged >2 years.2,7–9
focal zone depth when imaging with high-frequency linear transducer.
The ACA RI will demonstrate changes in response to
alterations in end-diastolic flow. For example, cerebral vas-
Doppler cular dilatation in the setting of acute hypoxia or ischemia
Color Doppler images obtained via the anterior fontanel or will result in increased end-diastolic flow generating a lower
mastoid fontanel can be used to document normal intracra- ACA RI (►Fig. 5A). Conversely, in the setting of increased
nial vascular anatomy (►Fig. 3) or anatomic variants. intracranial pressures (ICPs), end-diastolic flow will de-
Imaging through the anterior fontanel in the sagittal plane crease generating a higher ACA RI (►Fig. 5B).7,8
provides an optimal view of the anterior cerebral artery Special care in interpretation of ACA RI must be observed
(ACA) along the genu of the corpus callosum (►Fig. 3A). in neonates with cardiac disease.10 In these circumstances,
Acquisition of spectral Doppler waveform at this site allows especially in the setting of left-to-right shunt, end-diastolic
optimal assessment of peak systolic velocity (PSV), end- flow in the intracerebral arteries will be variable. The most
diastolic velocity (EDV), and resistive index (RI; defined as common example encountered in the neonatal intensive care
Fig. 3 Color Doppler may be used to document normal intracranial vascular anatomy including (A) Anterior cerebral artery and deep veins,
(B) superior sagittal sinus imaged through the anterior fontanel, and (C) transverse sinus imaged through the mastoid fontanel.

Fig. 4 Normal pulsed wave Doppler evaluation of ACA including RI in (A) preterm (34 weeks) and (B) term infant. ACA, anterior cerebral artery;
RI, resistive index.
Fig. 5 Alterations of RI in the ACA reflect physiologic changes in intercerebral blood flow; (A) increased end-diastolic flow in the setting of acute
hypoxic ischemic injury in term infant results in decreased RI; (B) decreased end-diastolic flow in the setting of increased ICP results in elevated
RI. ACA, anterior cerebral artery; ICP, intracranial pressure; RI, resistive index.

Fig. 6 ACA Doppler in term infant with PDA. Extracardiac left-to-right shunting results in decreased end-diastolic flow in the ACA. This should not
be mistaken for elevated RI in the setting of increased intracranial pressure (note normal ventricular size and normal extra-axial spaces). ACA,
anterior cerebral artery; PDA, patent ductus arteriosus; RI, resistive index.
unit is a patent ductus arteriosus (PDA). In a physiologically superficial vascular imaging but has been quickly adopted into
symptomatic PDA, end-diastolic flow in the ACA will be imaging of deeper vascular structures such as the portal vein.
significantly decreased or even reversed (►Fig. 6), and this The addition of B-flow imaging to neonatal cranial ultra-
should not be mistaken for elevated ICP. sound can provide more detailed evaluation of intracranial
vascular anatomy (►Fig. 7). In addition, B-flow imaging can
B-Flow be used to detect regions of relative hyper- or hypovascular-
B-flow imaging is a non-Doppler technology that directly ity in the setting of HII.
displays flowing intravascular echoes during real-time grays-
cale sonography. These images are especially impressive when Additional Acoustic Windows: Mastoid Fontanel
viewed on real-time sonography or cine loops. B-flow imaging The anterior fontanel provides an excellent acoustic window
was first introduced on high-frequency linear transducers for for supratentorial structures, although it is less optimal for
Fig. 7 (A) Color Doppler and (B) B-flow imaging in the sagittal plane through the anterior fontanel demonstrates normal vascular anatomy in the
term neonate. B-flow is especially good at detecting intravascular echoes in small vessels, allowing optimal visualization of the terminal branches
of the ACA and the deep venous structures in the sagittal midline. Vascular structures routinely visualized on sagittal scan include the basilar,
internal carotid, and anterior cerebral arteries, as well as the internal cerebral veins, vein of Galen, the straight sinus, and the superior sagittal
sinus. ACA, anterior cerebral artery.

Fig. 8 (A) Possible acoustic windows for neonatal cranial ultrasound. Anterior and mastoid fontanels are the most commonly utilized in neonatal
cranial ultrasound; imaging through the mastoid fontanel using sector transducer with indicator notch toward calvarial vertex allows excellent
visualization of the posterior fossa structures in the coronal plane including (from anterior to posterior) (B) brain stem and cerebellar peduncles,
(C) fourth ventricle and cerebellar hemispheres, and (D) cerebellar hemispheres and cerebellar vermis. ACA, anterior cerebral artery.
the evaluation of deep brain and posterior fossa struc- 10 weeks with only scattered areas of residual GM seen in
tures.11,12 The mastoid fontanel is located at the junction of the caudothalamic groove at 36 to 38 weeks’ gestation.2
the squamosal, lambdoidal, and occipital sutures (►Fig. 8A) The GM is highly vascular, supplied by a network of fragile
just behind the pinna of the ear. Imaging through this capillaries originating from the recurrent artery of Hubner
acoustic window with a sector or small-footprint linear and from penetrating striate and anterior choroidal
transducer allows improved visualization of the posterior arteries.2,11 Fluctuations in systemic blood pressure and
fossa. Images can be obtained in the coronal and axial planes alterations in oxygenation, especially in the presence of
through both right and left mastoid fontanels for detailed increased venous pressure, lead to rupture of the fragile
evaluation of the cerebellar hemispheres, cerebellar vermis, GM capillaries with resultant hemorrhage. These physiologic
fourth ventricle, foramen magnum, cerebral peduncles, and changes are most profound around the time of delivery and
brain stem (►Fig. 8B–D). early neonatal life with up to 90% of GM hemorrhage
occurring within the first 4 days.13
GM hemorrhage has traditionally been classified by the
Application of Advanced Techniques in
anatomic location of blood products according to the Papile
Neonatal Cranial Ultrasound
grading system.2,14 The use of high-frequency linear trans-
Germinal Matrix–Intraventricular Hemorrhage ducers in neonatal cranial ultrasound has greatly improved
The germinal matrix (GM) is a highly cellular structure of the visualization of these hemorrhages with increased accuracy
embryologic brain from which neural and glial progenitor in grading.
cells migrate during brain development. The GM is centered Acute blood appears hyperechoic to the normal choroid
in the subependymal caudothalamic groove at the base of the plexus; however, as blood ages, it becomes more heterogeneous
lateral ventricles. The GM reaches maximal volume at 24 to and mayappear iso- to hypoechoic to the choroid plexus and thus
26 weeks’ gestation and then regresses over the next be more difficult to detect on ultrasound.

Fig. 9 Grade 1 GM hemorrhage, confined to the germinal matrix. (A) Coronal and sagittal imaging with a 9-MHz linear transducer allows
excellent visualization of acute, echogenic hemorrhage effacing the normal V-shaped caudothalamic groove, with no echogenic intraventricular
blood products; (B) resolving hemorrhage at the caudothalamic groove appears hypoechoic. ACA, anterior cerebral artery; GM, germinal matrix.
Grade 1 hemorrhage is localized to the GM and is bounded and “lumpy-bumpy” contour. Echogenicity in the anterior
by the overlying ependyma. On ultrasound, Grade 1 hemor- horns of the lateral ventricles should be recognized as
rhage is seen as an echogenic focus that effaces the normal V- evidence of intraventricular extension as choroid plexus
shaped caudothalamic groove, bulging upward into the does not extend anterior to the foramen of Monro. Similarly,
ventricle with no echogenic intraventricular blood products. echogenicity layering in the occipital horns should be re-
Grade I hemorrhages account for 75 to 80% of all GM-IVH cognized as IVH as the choroid plexus does not extend this far
(►Fig. 9). posterior.2
Grade 2 hemorrhage begins in the GM and extends Grade 3 hemorrhage involves a larger amount of intraven-
through the overlying ependyma into the lateral ventricle. tricular blood (filling more than 50% of lateral ventricle) and
By definition, Grade 2 GM-IVH echogenic blood products fill is associated with ventricular dilation (►Fig. 11). The third
less than 50% of the lateral ventricle and there is no asso- and fourth ventricles should be carefully evaluated for echo-
ciated ventricular dilation (►Fig. 10). Hemorrhage abutting genic blood products. The third ventricle is seen to maximal
the choroid plexus can be distinguished by its heterogeneity advantage in the coronal and sagittal imaging planes using
Fig. 10 Grade 2 GM hemorrhage/IVH. Coronal and sagittal imaging with a 9-MHz linear transducer allows excellent visualization of echogenic
hemorrhage extending into the right lateral ventricle with no associated ventricular enlargement. Note echogenic material in the lateral
ventricle anterior to the caudothalamic groove and in the occipital horns. ACA, anterior cerebral artery; GM, germinal matrix; IVH,
intraventricular hemorrhage.

Fig. 11 Grade 3 GM hemorrhage/IVH. (A) Coronal and sagittal imaging with a 9-MHz linear transducer provides optimal visualization of acute
hemorrhage in the right lateral ventricle with associated ventricle enlargement plus echogenic acute hemorrhage in the third ventricle. Note the
extremely premature sulcation pattern in the cerebral hemispheres in this premature infant born at 26 weeks’ gestation. (B) Transmastoid
images in a different infant demonstrates echogenic blood products in the fourth ventricle. GM, germinal matrix; IVH, intraventricular
hemorrhage.
high-frequency linear transducer. Transmastoid views of the nized as periventricular hemorrhagic infarct (PVHI).2,8,9,13
posterior fossa allow for improved visualization of hemor- This injury is thought to result from compression or obstruc-
rhage within the fourth ventricle (►Fig. 11B).2,12 tion of terminal veins that drain the periventricular white
Grade 4 hemorrhage was classically defined by Papile et al as matter secondary to mass effect from ipsilateral GM hemor-
“extension of intraventricular blood into the surrounding rhage.2,8 This is the least common type of GM-IVH, occurring in
brain parenchyma” described as a fan-shaped region of in- approximately 5% of premature infants.
creased echogenicity in the periventricular white matter On ultrasound, Grade 4 GM-IVH/PVHI appears as a region
associated with IVH. However, as clinical understanding and of increased echogenicity in the periventricular white matter
imaging technology has advanced, this finding is now recog- along the atrium of the lateral ventricle (►Fig. 12B) and is
Fig. 12 Grade 4 GM-IVH/PVHI. (A) Coronal ultrasound images with sector transducer; (B) coronal and sagittal ultrasound images in the same
patient with 9-MHz linear transducer allows more detailed evaluation of the lateral ventricles and brain parenchyma, highlighting echogenic
intraventricular blood products and echogenic hemorrhage in the periventricular white matter with preservation of the lateral ventricle wall.
GM, germinal matrix; IVH, intraventricular hemorrhage; PVHI, periventricular hemorrhagic infarct.

always associated with an ipsilateral GM-IVH. Size of infarct posthemorrhagic ventricular dilation (►Fig. 14), thought
varies markedly depending on the area of drainage of the secondary to obliterative arachnoiditis and/or obstruction
occluded vein and amount of collateral venous drainage in the basilar cistern or fourth ventricle outflow tract that
present. Color Doppler may show lack of flow in the terminal blocks normal flow of CSF.13 Pulsed wave Doppler evaluation
vein. of the ACA in these infants, discussed in detail later, allows for
A scoring system has been proposed for PVHI at the time of early identification of increased ICP that may require ven-
initial diagnosis that has been shown to correlate with clinical tricular shunting (►Fig. 15).7
risk factors and outcomes (►Fig. 13).2,13 This system assigns a In the setting of Grade 4 GM-IVH/PVHI, as periventricular
score of 0 or 1 in three categories of findings on ultrasound in hemorrhage slowly resolves, the underlying brain parench-
PVHI. First, extent of periventricular white matter involvement yma may undergo liquefaction resulting in cyst formation
is scored. To do this, the cerebral hemisphere is divided into and volume loss. The adjacent ventricle may expand into the
five territories in the sagittal plane (►Fig. 13B). A territory is affected region, ex vacuo dilation with porencephalic cyst
considered “involved” when internal echogenicity measures formation (►Fig. 16). These findings are seen to best advan-
5 mm. If only a single territory is involved, PHVI is scored as tage on ultrasound imaging performed with a high-fre-
“localized.” If two or more territories are involved, PVHI is quency linear transducer.2,3
scored as “extensive.” Second, PVHI is scored as unilateral or Grade 3 GM-IVH and Grade 4 GM-IVH/PVHI are associated
bilateral. Finally, associated midline shift is scored as absent or with up to 50% probability of neurologic morbidity including
present. The score in each category is then added together. In cerebral palsy and developmental delay. In contrast, it ap-
the study reported by Bassan et al, the higher the total score of pears that the presence of a Grade 1 or Grade 2 GM-IVH does
PVHI injury, the more likely infants were to have poor long- not measurably alter overall risk of poor neurologic outcome
term outcomes.15 in premature infants.13
Once the initial diagnosis of GM-IVH is made, follow-up
ultrasound is typically performed 1 week later to evaluate Hypoxic-Ischemic Injury
for interval change. Serial ultrasounds may be performed HII affects both term and preterm infants in the clinical
until hemorrhage resolves. Resolving intraventricular blood setting of hypoxemia and altered cerebral blood flow. In
products become more heterogeneous as they undergo infants, hypoxemia may result secondary to several factors
cystic transformation and liquefaction.2,8,9 These changes including perinatal asphyxia, hypercapnia (retention of CO2)
are usually not encountered until the second or third week in the setting of lung disease, complex inflammatory pro-
following acute hemorrhage. cesses, and congenital heart disease.2,8 Alterations in cere-
Small Grade 1 GM-IVH commonly resolves without any bral blood flow may occur in the setting of both hypotension
residual abnormality on ultrasound. Approximately 30% of and hypertension. In addition, infants have limited capacity
premature infants with Grades 2 to 4 GM-IVH will develop for cerebral autoregulation, the process by which the brain
Fig. 13 Scoring system of PVHI proposed by Bassan et al. (A) Categories and scoring system and (B) cerebral territories for scoring of
periventricular hemorrhagic infarct. PVHI, periventricular hemorrhagic infarct.

Fig. 14 Complications of GM-IVH/PVHI. (A) Coronal and sagittal ultrasound images with 9-MHz linear transducer in infant with a history of Grade
3 GM-IVH demonstrate severe posthemorrhagic ventricular dilation, (B) transmastoid view with 7-MHz sector transducer demonstrates dilation
of the third and fourth ventricles, and (C) pulsed wave Doppler evaluation of the ACA demonstrates normal RI in the setting of normal ICP. ACA,
anterior cerebral artery; GM, germinal matrix; ICP, intracranial pressures; IVH, intraventricular hemorrhage; PVHI, periventricular hemorrhagic
infarct; RI, resistive index.
maintains a relatively constant cerebral blood flow, which life. The preterm brain parenchyma is supplied by a network
puts them at higher risk for HII. of penetrating arteries extending from the pial surface of the
The pattern of brain injury in HII depends on severity and brain and deep intracerebral arteries. This results in rela-
duration of hypoxic-ischemic event as well as degree of brain tively poor vascularization of the periventricular white
maturity at the time of injury.2 matter, the preterm “watershed zone.” The areas, most prone
Injury to the brain is thought to be a two-step process to injury lie along the dorsal and lateral margins of the lateral
occurring during ischemia and subsequent reperfusion. ventricles in the region of the centrum semiovale and the
During episodes of hypoxia and altered cerebral blood optic and acoustic radiations.2,16
flow, the brain compensates by shunting blood to the most The “watershed zones” gradually move more peripherally
metabolically active parts of the brain and to centers most with continued cerebral vascular ingrowth and by 38 weeks
crucial for maintenance of basal function including the brain gestational age are seen in the mature and more familiar
stem, basal ganglia, and cerebellum. Thus, short episodes of ACA/MCA and MCA/PCA distribution. Thus, mild-to-moder-
hypoxia and ischemia will predominantly affect the more ate HII at term gestation results in injury of the basal ganglia
peripheral “watershed zones” of cerebral perfusion.2,13 How- and peripheral cortex with relative sparing of the periven-
ever, more severe episodes lasting >15 to 25 minutes tricular white matter.
will result in injury to the deep gray matter. Reperfusion When performed with high-frequency linear transducers,
with the resolution of hypoxia and ischemia results in attention to detail, and careful technique, ultrasound is a
increased flow to the affected areas of the brain, predispos- powerful diagnostic tool that can be used at the bedside in
ing to hemorrhage. the detection of white matter injury in preterm and term
Before 32 weeks’ gestation, brain circulation is signifi- infants. In fact, a study by Epelman et al demonstrated that
cantly different than that seen in late gestation or neonatal normal cranial ultrasound in the setting of HII has a negative

Fig. 15 Normal pulsed wave Doppler of ACA in term infant. (A) Normal ACA RI in preterm infant (<0.85), (B) transient increase in ACA RI with
application of gentle anterior fontanel pressure, and (C) normalization of ACA RI after 10 seconds of anterior fontanel pressure, indicating
normal cerebral autoregulation in the setting of normal ICP. ACA, anterior cerebral artery; RI, resistive index.
predictive value of nearly 100% and may preclude the need graywhite matter differentiation (►Fig. 19). Imaging with
for neonatal brain MRI.13 a high-frequency transducer allows for excellent visualiza-
In preterm infants, ultrasound may demonstrate early tion of the cerebral cortex and increases sensitivity of
changes from HII as an ill-defined and poorly marginated echo- ultrasound in HII. However, findings may be subtle and
genicities in the periventricular white matter. Unlike PVHI, HII require specific attention by the interpreting radiolo-
is more often bilateral and symmetric (►Fig. 17).2,8,17 It should gist.2,19,20 Signs of diffuse cerebral edema include slit-like
be noted that severe HII may be complicated by secondary appearance of the lateral ventricles and effacement of the
hemorrhage and can be extremely difficult to differentiate extra-axial spaces.
from PVHI. Doppler imaging can be used to further evaluate cerebral
Follow-up ultrasound shows that most of these lesions blood flow in the setting of HII. Acutely, higher end-diastolic
resolve. Periventricular echogenicity lasting beyond the first flow velocities due to vasodilation in the setting of increased
week of life are more likely to be clinically significant. vascular demand, result in decreased RI (►Fig. 5A).2,7 Multi-
Severely injured periventricular brain parenchyma can ple studies have shown that an RI value below 0.55 measured
undergo cystic necrosis known as periventricular leukoma- in the ACA in the first 24 to 72 hours of life following HII
lacia (PVL). Specific patterns of echogenicity and cystic correlates with a poor neurodevelopment prognosis.7,17
necrosis in PVL have been classified by de Vries et al Later in the course of brain injury, as cerebral edema in-
(►Fig. 18).18 creases, increased ICP results in elevated RI.2,7
In term infants, mild-to-moderate HII results in diffuse In severe HII injury to deep brain structures is seen on
injury to the watershed zones of the cerebral hemispheres. ultrasound as diffusely increased echogenicity in the basal
On ultrasound, this is seen as diffusely increased echo- ganglia and thalami, well visualized using linear array
genicity of the white matter resulting in accentuated transducers.

Fig. 16 Complications of Grade 4 GM-IVH/PVHI. Serial ultrasound imaging performed with 9-MHz linear transducer of preterm infant with Grade
4 GM-IVH/PVHI at (A) first week of life, (B) 4 weeks, (C) 8 weeks, and (D) 12 weeks demonstrates progressive cystic change in the periventricular
white matter with eventual formation of a large porencephalic cyst and ex vacuo dilation of the right lateral ventricle. ACA, anterior cerebral
artery; GM, germinal matrix; IVH, intraventricular hemorrhage; PVHI, periventricular hemorrhagic infarct.
Fig. 17 HII in preterm infant. Ultrasound imaging with 9-MHz linear transducer in the (A) coronal, (B) right parasagittal, and (C) left parasagittal
planes demonstrates increased echogenicity in the periventricular white matter in “watershed” distribution consistent with HII. Note normal
appearance of the lateral ventricles with no intraventricular hemorrhage to distinguish this finding from Grade 4 GM-PVHI. GM, germinal matrix;
HII, hypoxic-ischemic injury; PVHI, periventricular hemorrhagic infarct.

Fig. 18 Patterns of PVL following HII. (A) Grade 1 PVL, periventricular echogenicity persisting more than 7 days, (B) Grade 2 PVL, small
periventricular cysts, (C) Grade 3 PVL, extensive periventricular cysts, and (d) Grade 4 PVL, extensive periventricular and subcortical cysts. Note
that parenchymal cystic change in PVL results in smaller cysts than those seen in preterm PVHI. HII, hypoxic-ischemic injury; PVHI, periventricular
hemorrhagic infarct; PVL, periventricular leukomalacia.
Cerebellar Injury to white matter atrophy following HII. When this occurs, the
Injury to the developing cerebellum has been described as an ventricles slowly enlarge over time and eventually stabilize.
additional complication of prematurity that can occur in the Obstructive hydrocephalus occurs when there is obstruction
setting of HII, most commonly in extreme prematurity and of CSF drainage pathways at the level of the aqueduct, fourth
ELBW in the setting of hypotension with major impact on ventricular outflow pathways, or arachnoid granulations.
neurodevelopmental outcome.16 When this occurs in the setting of GM/IVH, it may result
Infarct is most common at the watershed distribution in rapid enlargement of the ventricles on ultrasound
between superior cerebellar artery and PICA and may have (►Fig. 14A , B).2,8,9
hemorrhagic conversion. This finding may be extremely chal- Distinguishing between obstructive versus nonobstruc-
lenging to detect on standard imaging through the anterior tive hydrocephalus is clinically important, as the former
fontanel but may be easily identified with imaging through the necessitates neurosurgical consultation and potential inter-
mastoid fontanel (►Fig. 20).12 vention. Serial ultrasound with measurement of ventricular
size can identify rate and extent of ventricular enlargement.
Ventriculomegaly On postnatal cranial ultrasound, the biventricular, bifron-
Ventricular enlargement may be due to multiple etiologies in tal diameter of the lateral ventricles is measured at the
the neonatal period. When detected on prenatal ultrasound, level of the foramen of Monro in the coronal plane as the
ventriculomegaly is more likely due to congenital CNS distance between the lateral walls of both lateral ventricles
anomaly. Ventricular enlargement may also occur secondary (►Fig. 21).2 Transverse oblique measurements of the

Fig. 19 HII in term infant. Ultrasound imaging with 9-MHz linear transducer in the (A) coronal and parasagittal planes demonstrates diffusely
increased echogenicity of the white matter resulting in accentuated gray–white matter differentiation and (B) normal gray–white matter
differentiation in term infant provided for comparison. HII, hypoxic-ischemic injury.
Fig. 20 Cerebellar injury. (A) Abnormal echogenicity at the base of cerebellum ( ). This finding is challenging to identify on imaging via the
anterior fontanel, even with use of high-frequency linear transducer. (B) Transmastoid images performed with 7-MHz sector transducer better
demonstrate abnormal echogenicity at the base of both cerebellar hemispheres ( ) indicative of hemorrhagic or ischemic injury.

individual lateral ventricles and transverse measurements

of the third ventricle are also made at the same
level (►Fig. 21).2
Pulsed-wave Doppler measurement of RI in the ACA in
patients with ventriculomegaly may be used to assess for
increased ICP in the setting of obstructive hydrocephalus.2,7
As ICP rises, extravascular pressure results in increased
vascular resistance, decreased end-diastolic flow, and in-
creased RI (►Fig. 14C). When extravascular pressure exceeds
systemic intravascular pressure, end-diastolic flow may be
reversed.
Sensitivity of pulsed wave Doppler evaluation for elevated
ICP is improved with application of compression on the ante-
rior fontanel.7 Gentle downward pressure applied with ultra-
sound transducer to the anterior fontanel will result in mild
increase in ICP. Pulsed wave Doppler of the ACA during and
immediately after pressure application will demonstrate tran-
siently decreased end-diastolic flow with increased RI. In the
normal infant, cerebral autoregulation will correct for the
Fig. 21 Measurement of the lateral ventricles in the coronal plane at
slight increase in ICP and flow within the ACA will normalize
the level of the foramen of Monro in infant with ventriculomegaly within 5 seconds with return to a normal RI (►Fig. 15).
including biventricular, bifrontal diameter ( !), transverse oblique When ICP is already increased, as in severe hydrocephalus,
diameter (#–#), and transverse diameter of the third ventricle (¼¼¼). compression of the anterior fontanel will more drastically
Fig. 22 Abnormal pulsed wave Doppler of ACA in the setting of preterm infant with posthemorrhagic hydrocephalus. (A) Normal ACA RI in
preterm infant (<0.85) at rest, (B) increased ACA RI with compression of anterior fontanel which persists beyond 10 seconds, indicating loss of
normal cerebral autoregulation in the setting of increased ICP, and (C) pulsed wave Doppler of ACA in the same infant following intraventricular
shunt placement demonstrates normal ACA RI with compression of anterior fontanel, indicating relief of elevated ICP. ACA, anterior cerebral
artery; ICP, intracranial pressures; RI, resistive index.

Fig. 22 (Continued)
change the cerebral blood flow velocities. Alteration of the RI by Neonatal Meningitis
more than 45% between baseline and imaging with compres- Bacterial meningitis is a rare but serious condition in the
sion is suggestive of baseline elevated ICP and sustained newborn that occurs as a result of bacteremia and sepsis.
elevation of the RI beyond 5 seconds can be used to The most common organisms associated with meningitis in
predict which patients would benefit from ventricular shunt the newborn are group B streptococcus, Escherichia coli,
placement (►Fig. 22A , B).7 and Listeria monocytogenes. Infection spreads to the CNS
The use of ACA Doppler evaluation in infants with ven- via the highly vascular choroid plexus and in turn spreads
triculomegaly is clinically helpful as change on Doppler often to the CSF resulting in ventriculitis, meningitis, and
precedes clinical symptoms by days to weeks.2,7 Doppler arachnoiditis.
evaluation may also be used to monitor therapeutic effect Early diagnosis and recognition of complications are
of intraventricular shunting and further guide clinical imperative to prevention of neurodevelopmental seque-
care (►Fig. 22C). lae.14 Cranial ultrasound is an excellent imaging modality

Fig. 23 Cranial ultrasound findings in neonatal meningitis. (A) Coronal and sagittal grayscale images with high frequency linear transducer
demostrate thickening and increased echogenicity of the ependyma in both lateral ventricles consistent with ventriculitis. (B) Images optimized
for evaluation of the extra-axial space demonstrates complex, echogenic fluid consistent with empyema in patient with Escherichia coli
meningitis. (C) Color Doppler evaluation of the superior sagittal sinus in a different patient demonstrates echogenic intraluminal thrombus with
lack of color flow.
for identification of important early findings including The extra-axial spaces may become enlarged in several
thickening and increased echogenicity of the meninges clinical situations in the neonate including the setting of
and ependymal lining of the ventricles cerebral edema communicating hydrocephalus or underlying brain atrophy.
(►Fig. 23A). Ventriculomegaly can be seen in the acute or Benign enlargement of the subarachnoid spaces in infancy
chronic phase of disease due to impaired CSF drainage. may also be seen in older infants with macrocephaly.9 On
Color Doppler may demonstrate increased flow in the pial grayscale ultrasound, simple anechoic fluid can be seen in
and subarachnoid vessels (►Fig. 23B). These findings are all the subarachnoid space deep to the anterior fontanel which
seen to best effect with imaging using a high-frequency is contiguous with fluid extending along the midline falx.
linear transducer. Color Doppler imaging demonstrates normal vessels running
A rare but significant complication of meningitis includes along the cortical surface of the brain as well as small caliber
intracranial empyema with echogenic debris seen in the vessels crossing the subarachnoid space (►Fig. 24).
ventricles and extra-axial spaces (►Fig. 23C). Superior sa- Subdural hemorrhage can result from birth trauma. Ac-
gittal sinus venous thrombosis results from direct contact of cumulation of blood products in the subdural space will
subdural collections with the cortical vessels and venous cause inferior displacement of the arachnoid membrane
sinuses, leading to thrombus and venous infarct.18 from the dura along the inner table of the calvarium.
Grayscale ultrasound with high-frequency linear transducer
Extra-axial Spaces can identify the displaced linear, hyperechoic arachnoid
Advanced cranial ultrasound techniques including imaging membrane (►Fig. 25).6 Acute subdural blood products will
with high-frequency linear transducer and color Doppler has appear hyperechoic, while subacute or chronic blood pro-
significantly improved ultrasound evaluation of the extra- ducts may appear hypo- to anechoic, which may make
axial spaces. diagnosis difficult. The addition of color Doppler images
In normal, term infants, the width of the subarachnoid can identify a lack of crossing vessels in the subdural space
space ranges from 0 to 3 mm with a mean width of 1.6 mm.6 (►Fig. 25), confirming subdural fluid collection.

Fig. 24 Extra-axial space. Optimized images through the anterior fontanel using high-frequency linear transducer demonstrate classic findings
of BESSI including (A) enlarged subarachnoid space with normal crossing arachnoid vessels, (B) B-flow imaging of the extra-axial space can better
depict small crossing vessels, and (C) pulsed wave Doppler of the ACA demonstrates normal RI indicative of normal ICP. ACA, anterior cerebral
artery; BESSI, benign enlargement of the subarachnoid spaces in infancy; ICP, intracranial pressures; RI, resistive index.
Fig. 25 Extra-axial space. Optimized images through the anterior fontanel using high-frequency linear transducer demonstrate findings of subacute
subdural hemorrhage. (A) Inferior displacement of linear, hyperechoic arachnoid membranes in the right extra-axial space. Note crossing vessels in the deep
subarachnoid space and lack of crossing vessels in the subdural space, (B) findings are confirmed on MRI. MRI, magnetic resonance imaging.

Conclusion 8 Hintz SR, O’Shea M. Neuroimaging and neurodevelopmental

outcomes in preterm infants. Semin Perinatol 2008;32(01):11–19
9 Seigel M. Pediatric Sonography. 3rd ed. Philadelphia, PA: Lippin-
Neonatal cranial ultrasound is an excellent tool for imaging
cott Williams and Wilkins; 2002
of intracranial pathology in the preterm and term neonates.
10 Daneman A, Epelman M, Blaser S, Jarrin JR. Imaging of the brain in
The addition of advanced techniques such as imaging with full-term neonates: does sonography still play a role? Pediatr
high-frequency linear transducers, additional acoustic win- Radiol 2006;36(07):636–646
dows, and Doppler can improve image quality and diagnostic 11 North K, Lowe L. Modern head ultrasound: normal anatomy,
accuracy of cranial ultrasound in the common pathologies variants, and pitfalls that may simulate disease. Ultrasound Clin
2009;4:497–512
such as GM/IVH, HII, cerebellar injury, ventriculomegaly,
12 Yikilmaz A, Taylor GA. Sonographic findings in bacterial meningitis
neonatal meningitis, and subdural hemorrhage.
in neonates and young infants. Pediatr Radiol 2008;38(02):129–137
13 O’Shea TM, Counsell SJ, Bartels DB, Dammann O. Magnetic re-
sonance and ultrasound brain imaging in preterm infants. Early
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106 Review Article

Neonatal Cranial Ultrasound: Advanced

Introduction at corrected gestational age 36 to 40 weeks (term equivalent)

Journal of Pediatric Neurology Vol. 16 No. 2/2018

PSV–EDV/PSV).3,7 The RI is inﬂuenced by many factors in-

Journal of Pediatric Neurology Vol. 16 No. 2/2018

Journal of Pediatric Neurology Vol. 16 No. 2/2018

Journal of Pediatric Neurology Vol. 16 No. 2/2018

Journal of Pediatric Neurology Vol. 16 No. 2/2018

Journal of Pediatric Neurology Vol. 16 No. 2/2018

Journal of Pediatric Neurology Vol. 16 No. 2/2018

Journal of Pediatric Neurology Vol. 16 No. 2/2018

Journal of Pediatric Neurology Vol. 16 No. 2/2018

Journal of Pediatric Neurology Vol. 16 No. 2/2018

Journal of Pediatric Neurology Vol. 16 No. 2/2018

Journal of Pediatric Neurology Vol. 16 No. 2/2018

Journal of Pediatric Neurology Vol. 16 No. 2/2018

individual lateral ventricles and transverse measurements

Journal of Pediatric Neurology Vol. 16 No. 2/2018

Journal of Pediatric Neurology Vol. 16 No. 2/2018

Journal of Pediatric Neurology Vol. 16 No. 2/2018

Journal of Pediatric Neurology Vol. 16 No. 2/2018

Conclusion 8 Hintz SR, O’Shea M. Neuroimaging and neurodevelopmental

Journal of Pediatric Neurology Vol. 16 No. 2/2018

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