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Department of Neonatology, Isala Hospital, Zwolle, the Netherlands; 2Department of Neonatology. Wilhelmina
Childrens Hospital, University Medical Center Utrecht, The Netherlands
Abstract: Cranial ultrasonography (cUS) is a reliable tool to detect the most frequently occurring congenital and acquired
brain abnormalities in full-term and preterm neonates.
Appropriate equipment, including a dedicated ultrasound machine and appropriately sized transducers with special settings for cUS of the newborn brain, and ample experience of the ultrasonographist are required to obtain optimal image
quality. When, in addition, supplemental acoustic windows are used whenever indicated and cUS imaging is performed
from admission throughout the neonatal period, the majority of the lesions will be diagnosed with information on timing
and evolution of brain injury and on ongoing brain maturation. For exact determination of site and extent of lesions, for
detection of lesions that (largely or partially) remain beyond the scope of cUS and for depiction of myelination, a single,
well timed MRI examination is invaluable in many high risk neonates. However, as cUS enables bedside, serial imaging it
should be used as the primary brain imaging modality in high risk neonates.
1875-6336/14 $58.00+.00
how and when to perform cUS. We will focus on white matter (WM) injury and GMH-IVH, frequently encountered in
the preterm neonate. In addition, some other abnormalities
which can be detected by cUS both in the preterm and fullterm neonate, are described. Finally, attention is paid to the
limitations of cUS.
2. WHY AND WHEN TO PERFORM cUS?
The question is now sometimes raised why cUS should
be performed at all. The American Academy of Neurology
reviewed neuro-imaging strategies for evaluating preterm
and encephalopathic term born infants in 2001 and suggested
that in preterm infants <30 weeks' gestational age (GA), routine cUS should be performed once between 7 and 14 days
of age and optimally repeated between 36 and 40 weeks'
postmenstrual age [8]. Using these guidelines, large hemorrhages will be visualised on the first scan and may influence
care (for instance management of PHVD), while the second
cUS examination will recognise cystic lesions (c-PVL) in the
WM or ventriculomegaly (VM), which can provide information on long-term outcome.
Performing cUS following admission to the neonatal intensive care unit should however be seen as part of the admission procedure and has proven to be useful as it enables us to:
Ex-vacuo VM, following WM disease, often associated with increased width of the subarachnoid space
and widening of the interhemispheric fissure [22].
Table 1.
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23-26
27-29
29-32
32-35
day 1
day 1
day 1
1 week
1 week
1 week
1 week
2 weeks
2 weeks
weekly to 31 weeks
weekly to 31 weeks
3 weeks
3 weeks
at 36 weeks
term
term
term
term
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the resolution, but in larger infants this may be at the expense of penetration Fig. (1).
On the other hand, while imaging the brains of larger
neonates and infants, and/or for good visualisation of deeper
structures (posterior fossa), scan frequency should additionally be decreased to 5MHz, enabling better penetration, but
at the expense of resolution [24, 25].
Focus Points
For standard cUS examinations, it is recommended to use
two focus points, positioned respectively above and below
the periventricular and ventricular areas. These areas, vulnerable for injury, especially in the preterm neonate, should
be optimally focused. In cases with (suspected) abnormalities beyond the focus points, these should be repositioned
accordingly [25]. If a small structure or abnormality needs to
be visualised, alternatively one focus point can be used, aiming at that specific area.
Scan Procedure
While performing a standard cUS examination, the whole
brain is scanned in 2 planes (coronal and sagittal), from respectively frontal to occipital and right to left. Coronal
planes are obtained by positioning the transducer in the mid-
dle of the anterior fontanel with the marker in the right corner, pointing towards the right ear. The transducer is then
moved and angled forwards and backwards. To obtain the
sagittal planes, the transducer is subsequently rotated 90,
the marker pointing towards the infants face. It is then
moved and angled, from the middle to respectively the right
and the left. At least six standard coronal planes and five
standard sagittal planes are recorded and digitally saved. In
addition, images are recorded of each (suspected) abnormality.
For the standard coronal and sagittal planes and the brain
structures visualised in these planes see ref. 24 [24].
4. ADVANCED CRANIAL ULTRASONOGRAPHY:
THE SUPPLEMENTAL ACOUSTIC WINDOWS.
When using the AF as an acoustic window and optimal
cUS settings, good quality images can be obtained from the
supratentorial structures, including the ventricular system,
periventricular WM, basal ganglia and thalami and the cortex
and subcortical WM. However, the brain stem and posterior
fossa structures, being further away from the transducer, will
not be optimally visualised. Using the supplemental acoustic
windows, i.e. the temporal windows, posterior fontanel (PF)
and mastoid fontanels (MF), the transducer is positioned
closer to these structures, enabling better visualisation [7,23,
24, 25 - 27].
Posterior Fontanel
The PF is located at the junction of the lambdoid and
sagittal sutures. This fontanel can easily be palpated in
neonates and young infants, by following the sagittal suture
posteriorly from the AF. The transducer is positioned in the
middle of the PF, horizontally with the marker pointing
towards the right ear to obtain coronal planes and vertically, the marker pointing towards the cranium, for
(para)sagittal planes. The PF allows good visualisation of
the occipital horns of the lateral ventricles, the occipital
parenchyma, the tentorium and cerebellum. As the occipital
horns do not contain choroid plexus, echogenicity seen in
this part of the lateral ventricles is highly suspect for intraventricular hemorrhage Fig. (2).
Temporal Windows
The temporal windows are located above the ears. Positioning the (smallest) transducer approximately 1cm above
and anterior to the external meatus, the marker horizontally,
a transverse view is obtained from the mesencephalon, brain
stem, circle of Willis and upper cerebellum. In this plane
Doppler flow measurements can be performed in the circle
of Willis. Image quality depends on bony thickness and thus
on age at scanning.
Mastoid Fontanels
The MF, located at the junction of the temporal, occipital
and posterior parietal bones, enable detailed visualisation of
the posterior fossa, including the cerebellum, 4th ventricle
and cisterna magna. We use these fontanels routinely to detect congenital and acquired abnormalities of the cerebellum,
hemorrhage in the 4th ventricle (mostly being an extension of
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Fig. (2). Preterm infant, GA 26 weeks, who developed PHVD. Coronal view through the anterior fontanel and parasagittal view through the
posterior fontanel. Note discrepancy between dilatation of frontal and occipital horns. The remains of the clot are clearly seen, when insonated through the posterior fontanel.
Fig. (3). Preterm infant, gestational age 27 weeks. cUS performed on day 1, day 4 and day 5, coronal views showing a normal cUS on admission, with subsequent development of an IVH and later evolution into a HPI.
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Once again the value of cUS comes from sequential imaging, showing the duration of the echogenicity and in some
cases the evolution to more echogenic and/or inhomogeneous echogenicity or to cystic lesions Fig. (4). The more
extensive cysts tend to occur within 2-3 weeks following an
insult, while the more localised cystic lesions may take as
Fig. (4). Three different preterm infants, showing increased echogenicity, PVL grade I (a, coronal and b, parasagittal views), localised cystic
PVL (grade II) (c) and extensive c-PVL (grade III) (d).
Ventricular dilatation
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Fig. (5). Coronal (a) and axial (b) cUS scans through MF in very preterm neonate (gestational age 26 weeks), showing cerebellar hemorrhage (arrows).
Fig. (6). a) Coronal cUS through MF in full-term neonate with severe HIE after massive feto maternal transfusion, showing increased echogenicity of the cerebellar hemispheres with loss of normal structures. (b) cUS scans of normal appearing cerebellum in near term infant (gestational age 36 weeks) for comparison.
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Fig. (7). (a, b) Preterm infant, gestational age 31 3/7 weeks, with antenatal diagnosis of Dandy-Walker malformation; cUS scans through AF
show a small vermis which is rotated upwards. (c, d) cUS images show normal cerebellum in preterm neonate, gestational age 32 weeks.
Fig. (8). Coronal (a) and parasagittal (b) cUS scans in full-term neonate with severe HIE, showing increased echogenicity of the basal ganglia and thalami. A line of lower echogenicity, representing the PLIC, can be recognised in between.
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Fig. (9). Coronal cUS scans in full-term neonate presenting with seizures, showing asymmetry of the sylvian fissure (arrow in a) and asymmetric cortical folding (arrow in b). MRI confirmed cUS diagnosis of left sided MCA infarction, the DWI showing diffusion restriction.
cephalopathy and/or seizures but without a history of perinatal asphyxia. cUS performed on admission may help to
make an appropriate diagnosis.
3) Arterial infarction. Although the experienced ultrasonographer will detect most of these lesions, especially if
clinical symptoms, such as hemiconvulsions and/or asymmetric tone or reflexes are present, MRI is superior to cUS
for the detection of arterial infarction. Smaller cortical infarcts or infarction in the territory of the posterior cerebral
artery may not be recognised by cUS. A vague area of increased echogenicity, asymmetry in echogenicity between
the two hemispheres and/or increased echogenicity around
the Sylvian fissure may lead to the diagnosis, but this is usually not immediately apparent Fig. (9). By the end of the
first week the increase in echogenicity will become more
obvious and will sometimes be wedge shaped with a linear
demarcation line [6].
Infections
The presence of a congenital infection, especially CMV,
is often suggested by cUS findings, such as germinolytic
cysts, subependymal pseudocysts and lenticulostriate vasculopathy Fig. (10). Bilateral occipital cysts are highly suggestive for CMV while temporal horn cysts are also seen in
congenital rubella infection [11]. Increased echogenicity in
the WM in an infant presenting with neonatal seizures and
sometimes a rash and/or fever, can be suggestive of an enterovirus or parechovirus infection and changes on MRIDWI will be seen in these two entities [58, 59, 59a] Fig.
(11). In infants who present with a bacterial infection, either
a meningitis-ventriculitis or encephalitis, cUS abnormalities
are common and easy to recognise. Ventricular dilatation and
strands in the ventricles as well as increased echogenicity of
the ventricular ependyma may be seen in the milder cases,
while abscesses or rapid destruction of the WM can be seen
to develop in more severely affected infants Fig. (12). Infection with Citrobacter koseri is well known to be associated with abscess development. Bacillus cereus meningitis/encephalitis is rare but can destroy the WM within hours,
often not allowing time to perform MR imaging [60] (see
Fig. (12)).
Fig. (10). Coronal (a) and parasagittal (b) views in a full-term infant with congenital CMV infection, showing extensive lenticulostriate vasculopathy and germinolytic cysts.
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Fig. (11). Preterm neonate (gestational age 36 weeks) with enterovirus sepsis and encephalitis. Coronal (a) and parasagittal (b) cUS scans
show patchy, inhomogeneously increased echogenicty of the periventricular and subcortical WM. T2 weighted MR image (c) shows abnormal signal intensity in the WM. The DWI (d) showed restricted diffusion in the WM and corpus callosum and also in the corticospinal tracts,
hippocampi and cerebellum (not shown).
Fig (12). Preterm infant, gestational age 30 weeks, who developed Bacillus Cereus septicaemia with rapid liquefaction of the white matter.
Echogenicity seen on coronal view (a), liquefaction on parasagittal view (b).
Metabolic Disorders
In an infant, presenting with neonatal encephalopathy in
the absence of a history of perinatal asphyxia, a metabolic
disorder may be considered. Several cUS findings may help
in the diagnosis as was reviewed by Leijser et al. [10]. Germinolytic cysts in a floppy infant with a large anterior fontanel, can help with the diagnosis of a peroxisomal disorder
Fig. (13), but are for instance also seen in mitochondrial
disorders. It is important to realise that these cysts are better
visualised with cUS than MRI [14]. A hypoplastic corpus
callosum in an encephalopathic infant with hiccups would
help to suggest a diagnosis of non-ketotic hyperglycinaemia.
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Fig. (13). Full-term infant with Zellweger syndrome, presenting with hypotonia and talipes. Multiple bilateral germinolytic cysts and ventriculomegaly.
overlooked, especially in the first days after the event; hypoglycemic parenchymal injury involving the occipital lobes is
often not recognized unless cUS is performed through the
posterior fontanel and punctate lesions may be suspected but
are better detected with MRI [1, 6, 21, 28, 61]. Some lesions
resulting from infection, such as (micro) abscesses and encephalitis may not be optimally recognized by cUS [11].
Involvement of the (posterior limb of the) internal capsula in
lesions, of major importance for neurological outcome, cannot be determined with certainty by cUS [55, 62]. However,
the PLIC can be reliably recognised as a rim of low echogenicity on cUS in infants with HIE and moderate-severe basal
ganglia injury (See Fig. (8)).
MRI, if well timed, performed under optimal circumstances and while using special neonatal scan protocols (including high field strengths, specially adapted sequences,
thin slices without or with small gaps), is invaluable to determine the exact origin, extent and location of lesions, to
detect lesions that are not well detected by cUS and to assess
myelination [1- 4, 6, 20, 21, 28, 55, 61, 62, 63]. We therefore
recommend to perform MRI examinations for the following
indications:
Metabolic disease
Prematurity, gestational age < 30 weeks (reliable detection of WM and cerebellar injury)
When the criteria mentioned above are met, the experienced ultrasonographer can detect the most frequently occurring congenital and acquired brain abnormalities, both
in full-term and preterm neonates. However, cUS is not
suitable to determine the exact origin, location and extent
of lesions, some abnormalities may be missed or overlooked and myelination can not be depicted. As image
quality of both ultrasound and MRI is superior to that of
CT for imaging the neonatal brain and both modalities are
much safer than CT, we feel that the use of CT of the brain
in neonates should be restricted to acute situations, where a
rapid diagnosis may lead to neurosurgical intervention. A
single, well-timed MRI examination, performed under optimal circumstances is indicated in most neonates with
neurological symptoms or (suspected) cUS abnormalities
and in neonates born very prematurely.
CONFLICT OF INTEREST
The authors confirm that this article content has no conflict of interest.
ACKNOWLEDGEMENTS
Declared none.
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