SelfDirectedLearning CUSScan On NICU
SelfDirectedLearning CUSScan On NICU
SelfDirectedLearning CUSScan On NICU
guidance only.
Their interpretation and application remains the responsibility of
the individual clinician.
If in doubt always contact a senior colleague.
Caution is advised when using guidelines after a review date.
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Descriptions:
It is recommended that when reporting the result of the cranial ultrasound you provide a
description of what you see rather than use a grading system. This description should include
comments on the midline, ventricles and parenchyma. It should identify relevant normal
findings (e.g. intact midline structures) and describe the abnormal features. Although in wide
use the classification suggested by Papile is unhelpful for our purpose[1]. It is based on the
appearance on CT scanning of infants who where identified as having had a cerebral
intraventricular haemorrhage on cranial ultrasound.
A common early finding is the presence of increased echodensity in the region of the trigone.
This is usually referred to as increased periventricular echodensity and, if this resolves within
the first week, is not associated with adverse neurodevelopmental outcome. If the
echodensity persists beyond 2 weeks it may be associated with clumsiness and mild
diplegia[2, 3]. The persistent echodensity may undergo cystic change. This lesion is
associated with a high risk of cerebral palsy[4].
Communication of results
Performing a cranial ultrasound on a patient can cause great anxiety for parents and
communication of the results should be done in a sensitive manner. It is best that experience
of such discussions should be gained whilst sitting in on senior colleagues before attempting
to communicate the results of your scan. It is part of good clinical practice to document such
communication with parents.
The power On switch can be found at the left hand side of the machine.
All of the following should be the default settings i.e. automatically set when the
machine is switched on.
→ Select the “A” probe ( 7 MHz).
→ Pre-set program “A” for Neonatal head settings.
→ Confirm orientation, pink mark on probe usually indicates left-side.
Press “New patient “ key and enter the patient details. This should include the
patients name, date of birth and initials of the person performing the scan.
Label orientation (R on the left side of the image) and confirm the orientation by
testing the probe.
Apply sufficient gel to cover the head of the probe head. Note patients will have
their own individual gel pot.
NB, to reduce the risk of cross infection, standard hand and incubator hygiene
should be maintained. Clean the probe and cable with alcohol based wipes and
use good hand washing techniques before opening incubators.
Appropriate depth, gain (power) and slope (time gain curve) should be used to
produce a uniform echo pattern in the near and far fields.
→ The appropriate controls for this are; depth dial – adjusted so that the image
fills the view, gain is set by turning the dial that surrounds the centre track ball
(default is 80 – seen at the lower right of the monitor), slope - is set using the
sliding dials on the top right of the control panel.
Focal depth: this can be adjusted vertically (triangle on the right side of the
monitor and can be adjusted on the control panel, central buttons labelled focus).
Typically this should be adjusted so that the best resolution occurs at the depth
of the structures you are most interested in viewing.
Obtain the standard views that can then be frozen (button labelled as such
bottom right corner) and then printed (button bottom left corner).
Finally, document the results of the scan in the patient notes, Cranial ultrasound
folder and make a plan to communicate these results to the parents in an
appropriate manner.
Coronal Views
Note: The sequence does not include
view [4] Through the (level of the
quadrigeminal cisterns) but does
include [6] (occipital periventricular
view).
Sagittal Views
Sagittal Views – Midline (6)
Sagittal Views – Parasagittal (7)
Sagittal Views –Tangential Parasagittal (8)
Measuring the Ventricular Index
The above diagram illustrates the different measurements to estimate the size of the
ventricles. We use (A) which measures the lateral extent of the ventricle in a line
perpendicular to the midline. This is plotted on a centile chart and is used in combination with
the head circumference to assess the degree of hydrocephalus.
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Early Human Development (2006) 82, 827–835
a v a i l a b l e a t w w w. s c i e n c e d i r e c t . c o m
w w w. e l s e v i e r. c o m / l o c a t e / e a r l h u m d e v
KEYWORDS Abstract Cranial ultrasound is the most available and easily repeatable technique for imaging
Cranial ultrasound; the neonatal brain. Its quality and diagnostic accuracy depend on various factors; the suitability
Newborn infant; of the ultrasound machine for neonatal cranial work, the use of optimal settings and probes,
Brain; appropriate scanning protocols, the use of a variety of acoustic windows and, not least, the
Timing; scanning experience of the examiner. Knowledge of normal anatomy and the echogenicities of
Scanning protocols; different tissues in normal and pathological situations as well as familiarity with the physiological
Teaching and pathological processes likely to be encountered is vital. This paper assesses the value and
appropriate use, safety and diagnostic accuracy of modern, high-quality ultrasound in evaluating
the brain of the preterm and term born infant. Issues of concern regarding teaching, supervision
and experience of the examiner are also addressed.
© 2006 Elsevier Ireland Ltd. All rights reserved.
Contents
1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 828
2. Scanning protocols . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 828
2.1. Preterm infants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 828
2.2. Term born infants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 830
2.2.1. Hypoxic–ischaemic encephalopathy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 830
2.2.2. Infant with seizures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 832
2.3. The dysmorphic or floppy infant and those with metabolic disorders . . . . . . . . . . . . . . . . . . . . . 832
3. Acoustic windows . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 833
4. Safety . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 834
Abbreviations: BG, Basal ganglia; BW, Birth weight; CP, Cerebral palsy; CT, Computed tomography; cUS, Cranial ultrasound; ECS,
Extracerebral space; GA, Gestational age; HC, Head circumference; HIE, Hypoxic–ischaemic encephalopathy; HPI, Haemorrhagic parenchymal
infarction; IHF, Interhemispheric fissure; IVH, Intraventricular haemorrhage; MRI, Magnetic resonance imaging; PVE, Periventricular
echogenicity; PVL, Periventricular leukomalacia; TEA, Term equivalent age; WM, White matter.
⁎ Corresponding author. Tel.: +44 20 8383 8515; fax: +44 20 8383 2473.
E-mail addresses: [email protected] (L.M. Leijser), [email protected] (L.S. de Vries), [email protected] (F.M. Cowan).
1
Current address: Department of Paediatrics, Division of Neonatology, Leiden University Medical Center, Albinusdreef 2, P.O. Box 9600, 2300
RC Leiden, The Netherlands. Tel.: +31 71 5262909; fax: +31 71 5248199.
0378-3782/$ - see front matter © 2006 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.earlhumdev.2006.09.018
828 L.M. Leijser et al.
Cranial ultrasound (cUS) is the most readily available and Preterm infants have a high risk of hypoxic, haemorrhagic
easily repeatable technique for imaging the neonatal brain. and inflammatory cerebral lesions, mainly IVH, HPI, cystic
In contrast to other neuro-imaging tools such as magnetic and non-cystic PVL and more diffuse white matter (WM)
resonance imaging (MRI) and computed tomography (CT), it injury. Cerebellar abnormality is probably more common
can be done bedside with little disturbance to the infant. than realised [8–11]. These findings are of clinical impor-
Neonatal cUS has been used for over 25 years and early tance, making the use of appropriately timed screening
studies on intraventricular (IVH) and parenchymal haemor- protocols necessary.
rhage (HPI), post-haemorrhagic ventricular dilatation and Perlman et al. [12] recommended that preterm infants of
cystic periventricular leukomalacia (PVL) have helped birth weight (BW) <1000 g should be scanned between days
greatly our understanding of risk factors for neurodevelop- 3–5, 10–14, around day 28 and pre-discharge; that those
mental abnormalities. Advances in technology have between 1000 and 1250 g are scanned between days 3–5, day
improved the quality of cUS imaging such that it can be a 28 and pre-discharge and those between 1250 and 1500 g
reliable tool for following brain development and showing between days 3–5 and pre-discharge. This recommendation
the most frequently occurring forms of cerebral injury in was based on data obtained using this protocol in about 250
the preterm and term born infant brain. The range of cUS preterm neonates. 65% of IVH was detected in the 1st week
diagnoses has increased with the recognition of more subtle after birth, the remaining in the 2nd/3rd week. Cystic PVL
patterns of injury and the appreciation of features occurred in larger, more mature infants and was not always
suggestive of developmental, metabolic and infectious preceded by increased periventricular echogenicity (PVE). In
disorders. 2/9 infants it was only detected on the pre-discharge scan.
In recent years concerns have been raised that cUS is not Ventriculomegaly was detected on the initial scan in 50% but
able to detect more subtle abnormality in the preterm infant only after day 28 in 33%. Significant lesions were detected on
[1–4] and that it is not reliable for detecting lesions in the term the pre-discharge examination in 9 infants for the first time.
infant with HIE and focal infarction. The arrival of MRI with its In this study 13% of neonates died in the first 24 h and were
multi-slice coverage of the whole brain and large range of not scanned.
sequences has led a very negative press as far as cUS is con- The American Academy of Neurology in 2001 reviewed
cerned. This negativity is not well supported by comparative neuro-imaging strategies for evaluating preterm and ence-
studies where both techniques receive the same time and phalopathic term born infants [13] and recommended
expertise regarding image acquisition and analysis [5,6]. practice parameters for imaging of the newborn infant
The quality of cUS imaging and its diagnostic accuracy, as brain. They suggested that in preterm infants <30 weeks'
with any other imaging technique, depends on many gestational age (GA), routine cUS should be performed once
factors. These include not only the suitability of the between 7 and 14 days of age and optimally repeated be-
equipment for neonatal cranial work and the use of tween 36 and 40 weeks' postmenstrual age. They argued that
appropriate settings and probes, but also scanning at with this strategy lesions that influence clinical care (e.g.
appropriate times depending on the pathology being sought, IVH) and provide information about long-term outcome (e.g.
the use of different acoustic windows and not least the PVL and ventriculomegaly) would be detected.
experience and expertise of the examiner. Both these scanning protocols give rise to concern.
This review assesses the value of appropriate timing of Neither recommends scanning on admission, which is
modern, high-quality cUS in evaluating both the preterm essential for detecting lesions of antenatal onset [14].
and term born infant brain and highlights the current areas Their recommendations were based on their existing proto-
of emphasis in this important field of neonatal medicine. col and thus they do not know whether a more extensive
protocol would have detected more abnormalities. The
2. Scanning protocols protocol by Ment et al. [13] is limited to preterm infants
< 30 weeks' gestation with no recommendations for older
There are some technical guidelines on scanning quality and preterm infants.
image acquisition [7] but there is no universal agreement Pierrat et al. [15] used frequent cUS examinations and
about optimal timing for neonatal cUS. Scanning protocols compared the evolution of localized and extensive cystic PVL
vary considerably between different neonatal units. This with neurodevelopmental outcome. Localized cysts devel-
variability reflects the different purposes for scanning which oped after the first month from birth in more than half of the
include diagnosis, assessing aetiology and predicting out- infants and were often no longer visible around term
come, and the population of infants examined, imaging skills equivalent age (TEA). De Vries et al. [16] in a tertiary unit
and interest of the examiner, the availability of an setting, used high-resolution, sequential cUS in preterm
ultrasound scanner on the neonatal unit and experienced infants for predicting cerebral palsy (CP). Infants were divided
staff, cost-effectiveness and potential hazards. into those <32 weeks' GA and those between 33 and 36 weeks'
Using cerebral ultrasound effectively in the newborn infant 829
Table 1 cUS scanning protocol for preterm infants used TEA. Horsch et al. [17] related signs of brain atrophy
at the neonatal unit of the Hammersmith and Queen (enlarged sub-arachnoid spaces (ECS), widened interhemi-
Charlotte's Hospital, London - a tertiary referral centre spheric fissure (IHF), reduced complexity of gyral folding) on
sequential cUS of preterm infants with neurodevelopmental
Gestational age at birth (weeks) outcome at 3 years' of age. Infants without major lesions but
23–26 27–29 29–32 32–35 with signs of atrophy at discharge had significantly poorer
Postnatal age 1, 2 and Day 1 Day 1 Day 1 neurocognitive outcomes. A recent paper by Anderson et al.
at which cUS 3 days [18] measuring the length of the corpus callosum and
should be 1 week 1 week 1 week 1 week cerebellar vermis has shown early changes that inform the
timing of the effects of preterm birth on brain development —
performed 2 weeks 2 weeks
Weekly to Weekly 3 weeks 3 weeks information that would be difficult to obtain by other imaging
31 weeks to means in such a large group.
31 weeks Based on these studies and the population admitted to our
Alternating At tertiary neonatal unit, we developed a scanning protocol for
weeks to 36 weeks preterm infants (Table 1). All infants admitted to the unit
36 weeks have a cUS scan done by the SpR (middle grade staff) and
Term Term Term Term reviewed the next day on the ward round. The purpose of this
admission scan is to ascertain that neurodevelopmental
anatomy looks normal, there are no features to suggest
congenital infection, metabolic disease or long-standing
GA, and scanned weekly until discharge and once more at TEA. brain injury and also to identify recently evolving problems
cUS detected abnormalities in the majority (94%) of children such as haemorrhage or white matter (WM) echogenicity.
in whom CP was evident by 2 years. The risk for CP was the Equally important is to note that the scan appears normal at
same for both groups of infants. Infants of 33–36 weeks' GA are this time.
a population of increasing neurodevelopmental concern that On the early cUS scans special attention should be paid to
frequently are not scanned at all in the UK. In 29% of infants the presence of IVH and periventricular flaring, while the later
<32 weeks' GA cystic PVL, the most predictive marker for CP, cUS scans identify evolving parenchymal lesions (cystic PVL or
was only detected after 28 days. This data gives evidence that HPI), the development and progression of post-haemorrhagic
cUS can detect most lesions leading to CP if scanning is ventricular dilatation and signs of atrophy (enlarged lateral or
performed frequently until discharge and again around TEA third ventricles especially without evidence of IVH, irregular
and supports the need for scanning all gestation preterm ventricular margins, a thinned rim of WM around the lateral
infants admitted to a neonatal unit. ventricles, a thin corpus callosum and widened IHF and ECS
Evidence of suboptimal brain growth or atrophy is and changes in the cerebellum (Fig. 1). When assessing the
frequently present in preterm infants, particularly around significance of enlarged ventricles and ECS it is necessary to
Figure 1 Series of ultrasound images from a 24-week IUGR infant. (a, b) Day 2 showing abnormal echogenicity and loss of definition
of the cerebellum suggestive of haemorrhage; (c, d) 4- to 6-week scans showing the development of echogenicity in the caudothalamic
notch (c) and lenticulostriate vasculopathy (d); (e) 8-week scan showing a widened 4th ventricle and persisting abnormal echogenicity
behind the cerebellum; and (f) areas of low echogenicity within small cerebellar hemispheres. (g, h) MRI scan at term equivalent age
showing an obvious 4th ventricle, small vermis and cerebellar hemispheres with haemorrhage and also an increased interhemispheric
fissure and widened extracerebral space (also seen on cUS, images not shown). All the abnormality that is seen on the MRI was seen on
cUS. Additionally the cUS showed the development of echogenicity in the caudothalamic notch and the LSV not seen on the term MRI.
830 L.M. Leijser et al.
Table 2 Clinical indications for additional scans to a 2.2. Term born infants
standard protocol
In term born infants, hypoxic–ischaemic encephalopathy
A sudden deterioration in clinical state
A sudden increase in the need for ventilatory support (HIE) and stroke are still the major causes of, respectively,
Necrotizing enterocolitis diffuse and focal brain injury and neurological morbidity.
Repeated episodes of apnoeas and/or bradycardias
A sharp fall in haemoglobin level 2.2.1. Hypoxic–ischaemic encephalopathy
Onset of seizures or change in neurological status cUS is often considered not very helpful in detecting
Increasing ventricular dilatation lesions occurring with HIE or predicting outcome, as the
Abnormal head growth initial swelling makes focal lesions difficult to detect and
Before and after lumbar puncture and for drainage of CSF precisely locate. The American Academy of Neurology [13]
Before and after surgery recommended that in encephalopathic term infants a CT
should be performed to detect haemorrhagic lesions and if
findings are inconclusive, MRI should be performed between
days 2 and 8 to assess the location and extent of injury. They
give no data supporting the diagnostic value of cUS in HIE.
measure the head circumference (HC) and review the pattern cUS in term born infants with suspected HIE has several
of head growth. A small group of infants develop an enlarged roles. Scanning as part of the admission procedure identifies
ECS associated with increased HC centiles and these children congenital structural cerebral abnormalities, detects evi-
are of less concern. dence for long-standing or more recently established injury
In addition to detecting lesions, assessing their site and initiated prior to the onset of labour, and detects abnorm-
extent is important for accurate prediction of outcome. In alities characteristic of non-HIE causes of encephalopathy,
preterm infants, unilateral HPI located at the trigone is e.g. a hypoplastic corpus callosum suggesting a diagnosis of
associated with a less favourable outcome than lesions in the non-ketotic hyperglycinaemia (Fig. 2) and germinolytic cysts
fronto-parietal region [19]. Multiple PVL cysts in the suggesting mitochondrial or peroxisomal disorders or con-
(parieto-)occipital but not the frontal regions are highly genital infection. This information is clearly important for
predictive of adverse motor outcome [20]. Even when cUS is early diagnosis and management. Additionally, with cUS, the
performed optimally, unexpected cases of CP occur. This may evolution of intrapartum injury can be followed and apart
in part be due to cerebellar lesions [21] which can be difficult from clinical implications this information is very important
to detect or to subtle injury that has occurred antenatally; in medicolegal issues.
awareness of the importance of assessing the posterior fossa Our protocol for scanning infants with suspected HIE is
structures and scanning through acoustic windows other than that a scan should be performed on admission, at 24 h ours
the anterior fontanelle may be needed (see below). after birth, days 3–4, days 7 and 14, and once again in clinic
Stroke occurs in preterm infants [22,23], often affecting at 4–6 weeks.
the central grey matter, and may only be detected by careful The initial cUS, mainly performed to exclude other causes
sequential scanning. It is more common in those with of encephalopathy, by identifying any abnormal anatomy,
congenital heart disease and twins (particularly with twin- evidence for established damage (e.g. presence of calcium,
to-twin transfusion syndrome), a high risk group that should marked echogenicity and parenchymal echolucency), lenti-
all have a postnatal cUS scan. It is also important to scan culostriate vasculopathy, germinal matrix cysts, diffuse WM
sequentially preterms who become sick or have unexpected echogenicity (Fig. 3) or signs of recent haemorrhage. In our
postnatal events and also to scan prior to surgery in case of experience, haemorrhage is well seen on cUS and the need for
complications (Table 2). Unusual patterns of WM echogeni- CT is restricted to infants with a traumatic assisted delivery,
city and the appearance of cysts may reflect infections in the where a midline shift is seen on cUS and neurological
central nervous system. These include fungal infections, intervention is considered. Data from Eken et al. [27] show
viruses [24,25] and a range of bacterial infections [26]. These that the majority of cUS scans in the first 6 h are normal in HIE
data apply both to preterm and term born infants. but if they are already abnormal the outcome is poor.
Figure 2 Hypoplastic corpus callosum (a, short arrow) and mildly echogenic white matter (b, longer arrow) in an encephalopathic
term infant with non-ketotic hyperglycinaemia (NKHG). Typical widely spaced ventricles from another patient with NKHG (c).
Using cerebral ultrasound effectively in the newborn infant 831
Figure 3 Term infant with evidence of acute asphyxia, retroplacental clot and severe encephalopathy. Initial cUS scans showed
small germinolytic cysts (a) and an unusual pattern of periventricular white matter echogenicity (a, b). Scans at 10 days show enlarging
cysts (c), and specks of calcification (shown on the axial view taken via the mastoid window (d)). Evolving acute lesions typical of
hypoxic ischaemia particularly to the basal ganglia are seen (arrows) in panels (e) and (f). There was a history of an acute
gastrointestinal illness associated with eating uncooked foods in France at 33 weeks GA. No evidence of a viral or metabolic disorder
was confirmed; the clinical course is that of a dystonic spastic quadriplegia consistent with the basal ganglia lesions seen in (e) and (f).
Acute changes on cUS suggestive of HIE may include Doppler ultrasound gives useful information in HIE [28].
diffuse brain swelling on days 1–2 (Fig. 4a), though for Measurements can be made at the time of the cUS imaging; it
infants with only a relatively short hypoxic insult swelling is not critical which intra-cerebral vessel is used — usually
may not be seen. There follows a loss of normal tissue the anterior cerebral artery via the anterior fontanelle or the
differentiation and increasing echogenicity of basal ganglia
(BG) and thalami and WM over the next 3–4 days. The cortex
often appears very echolucent compared to the adjacent
hyperechogenic WM and sulci (Fig. 4c) in the first days but
later may become hyperechogenic if severely damaged (Fig.
4b). BG and thalamic echogenicity typical of an acute
hypoxic–ischaemic insult is usually bilateral, increases daily
and has a characteristic appearance (Fig. 4b,c). Generalised
bilateral WM echogenicity is suggestive of a more long-
standing subacute insult; both central grey matter and white
matter are involved in more severe acute or mixed insults
when additionally the cortex appears abnormal. Milder
changes can be subtle and are often not seen before 7 days
after the insult. With severe widespread injury, the WM
becomes increasingly echogenic and then breaks down into
cysts. In a recent study by our own group reviewing
sequential early cUS of 139 term born infants with mild–
severe HIE (unpublished data), we found that the presence of
abnormal echogenicity in the BG and the visualization of the
internal capsule, seen as an echolucent line running through
the BG region (Fig. 4b,c), were highly predictive of an
abnormal motor outcome. Figure 4 (a, Coronal) Acute swelling with loss of grey-white
Late cUS findings after focal BG lesions include persisting matter differentiation. (b, Coronal and c, parasagittal) Evolving
echogenicity in the deep grey matter and dilatation of the abnormality in the lentiform nucleus (short black arrow) and the
third ventricle, signs significant for motor outcome (Fig. 4d). thalamus (long black arrow) with a line of low signal indication
Widening of the IHF suggests poor hemispheric growth and is the site of the internal capsule (indicated by the straight line
associated with poor cognitive outcome. These signs present between the arrows). (d, Coronal) Widening of the 3rd ventricle
on later scans are of concern despite apparent clinical (white star), and enlargement of the interhemispheric fissure
improvement in the first few weeks after birth. and the extracerebral space (arrows) at 6 weeks.
832 L.M. Leijser et al.
Figure 5 (a) View through the temporal window enabling visualization of the middle cerebral artery; below are a normal Doppler
spectra with a PI of 0.8. (b) Abnormal Doppler spectra in HIE with a PI of 0.5.
middle cerebral artery via the temporal window (Fig. 5a). is not possible to obtain an MRI scan. However, there is no
Two parameters can be assessed, the total flow velocity doubt that an MRI in the first 1–3 weeks is superior for
(CBFV) and the pulsatility index (PI) (confusingly referred to defining lesions and giving more precise long-term prognosis
as the resistance index (RI) in obstetric papers). Normal in HIE but the value of cUS should not be underestimated in
values for the PI are between 0.65 and 0.85 the first days after birth and for monitoring at 4–6 weeks
when a normal cUS scan, clinical examination and head
peak systolic velocity the end diastolic velocity growth are good prognostic indicators.
PI ¼
peak systolic velocity
2.2.2. Infant with seizures
Abnormal values < 0.55 occur in severe HIE usually
Term infants with early neonatal seizures who had fairly
between days 2 and 4 after birth (Table 3) (Fig. 5b). The
normal Apgar scores and were not acidotic at birth are most
outcome of infants with abnormal values in the first 6 h after
likely to have had a neonatal stroke; other more common
birth is very poor and suggests a prolonged insult either
diagnoses are parasagittal infarction and focal haemorrhage.
intrapartum or 1–2 days prior to delivery [27]. The absolute
Neonatal stroke has an estimated prevalence of at least 1/
flow velocities are more difficult to assess as they require the
4000 live births. It is an important cause of hemiplegic CP and
angle of insonation on the vessel to be near to zero and the
other neurological disabilities. cUS is often said to have a poor
values vary with the vessel measured on. However, high
sensitivity for detecting focal infarction. We found that early
values carry a poor prognosis and are associated with a low PI.
cUS (days 1–3) showed abnormalities suggestive of infarction
Doppler measurements are useful in assessing venous flow
in 68% of cases and in 87% when cUS was performed after day 4
especially in the straight sinus in suspected venous throm-
[5]. Infants whose late cUS scans remained normal had rela-
bosis (often associated with IVH or thalamic haemorrhage
tively small, mostly posterior infarcts; none of these infants
[29]) and to document abnormal velocity patterns in
developed a hemiplegia. Thus, neonatal cUS does allow the
suspected vascular malformations.
detection of abnormality suggestive of focal ischaemic
We find cUS, both imaging and Doppler, of great use in
lesions, particularly those likely to lead to hemiplegia.
excluding non-HIE diagnoses and in following the timing and
We perform cUS scans on infants presenting with seizures
evolution of acute injury. cUS together with electrophysio-
on admission and then at 2 days, 5–7 days and 2 weeks after
logical data and clinical progress often allows early prognosis
the onset of seizures. Special attention should be paid to
and appropriate clinical management in a situation where it
presence of subtle asymmetrical parenchymal echogenicity,
a wedge shaped echogenic area suggestive of middle cerebral
artery (MCA) infarction (Fig. 6), a rounded very echogenic
Table 3 The predictive value of the pulsatility index (PI) lesion suggestive of haemorrhage (Fig. 7) and any abnormal
and cerebral blood flow velocities (CBFV) for adverse structural development suggestive of a developmental
neurological outcome in HIE in term born infants abnormality. We suggest however that for any infant with
Measurements made 2–4 days after birth Levene et al. [28] seizures a neonatal MRI examination is performed; precise
Abnormal CBFV Low PI <0.55 detail of lesion size, location and prognosis are better defined
Sensitivity 57% 60% on MRI [30,31] allowing more precise prognosis.
Specificity 88% 63%
PPV 94% 83% 2.3. The dysmorphic or floppy infant and those with
Early (< 6 h) measurements Eken et al. [27] metabolic disorders
Sensitivity Specificity
Ultrasound 42.1% 60% Dysmorphic features and the floppy infant syndrome can be
Doppler 23.5% 100% indicators of developmental disorders and congenital infec-
tion, genetic/chromosomal syndromes, congenital or
Using cerebral ultrasound effectively in the newborn infant 833
Figure 6 Full term infant with neonatal seizures. Large wedge-shaped area of echogenicity on the right (a, b, c parasagittal) is
shown including the basal ganglia typical of a middle cerebral artery territory stroke. MRI confirms the diagnosis (d) T1W, (e) diffusion-
weighted and (f) follow-up scans.
Figure 7 cUS of: (a) coronal, (b) parasagittal and (c) mastoid view from a 31-week infant with low platelets showing a large recent
focal haematoma with a midline shift (a, short arrow). 20 cm3 of blood removed by subdural drainage. MRI (d, e) following tap.
834 L.M. Leijser et al.
(junction of the lambdoid and sagittal sutures) and mastoid neonatal units in New Zealand. They showed that there was only
fontanelle (junction of the posterior parietal, temporal and moderate agreement between the reviewers' reports and those
occipital bones) can help to detect lesions and structural of the neonatal units and between the reviewers; the reviewers
malformations in these areas [19,21,33,34] (Fig. 7). Imaging reported 3–6 times more WM damage.
through the temporal window allows good views of the These studies highlight the need for more widespread
mesencephalon and brainstem. formal training in scanning techniques and that teaching of
cerebral anatomy, the appearance of normal structures, an
understanding of normal growth as well as knowledge of the
4. Safety appearances and evolution of different pathologies are
Although sequential cUS is clearly very important, its potential essential for those responsible for acquiring and interpret-
hazards and burden for the often sick and unstable newborn ing cUS scans. These skills need to be assessed and
infant should be kept in mind. These include extra handling, competencies maintained. Increased collaboration between
applying pressure and cold gel to the fontanelle, the risk of neonatologists, radiographers and radiologists with an
dislodging tubes or lines or introducing infection from equip- interest in neonatal scanning and prognosis is needed in
ment that is not kept clean or from the operator. Most of these order to improve and rationalise the use of this valuable
issues are relatively easy to prevent when appropriate safety technique.
and hygienic precautions are taken. All ultrasound equipment
for use on a neonatal unit must be kept regularly cleaned, the 6. Conclusions
probes wiped with a damp cloth. We also use hard surface wipes
that contain some alcohol but these are not suitable for all Current evidence is that cUS imaging using modern machines,
probes and the manufacturers should be consulted. probes, a variety of acoustic windows and sequential scanning
There are also concerns about potential hazards of the at optimal times gives high-quality images that are diagnos-
ultrasound waves. To date no adverse effects have been tically accurate. Issues of teaching, supervision and experi-
shown to result from the sequential use of ultrasound in ence for both paediatric and radiological staff need to be
newborn infants or fetuses, although a slightly increased risk addressed and collaboration between paediatric and radi-
of delayed speech [35], left handedness [36] and intrauterine ology departments is needed to improve protocols, image
growth restriction [37] after multiple fetal examinations has quality and interpretation. Whilst MRI does have advantages
been reported. However, ultrasound waves, especially when over cUS and clear clinical indications, especially in the term
used for colour Doppler imaging, may induce temperature born infant, cUS facilitates early bedside diagnosis and
elevations in human tissue over time that have the potential monitoring of pathology in a way that is relatively easy and
to cause damage. It is important to keep the duration of not disturbing and safe for the newborn infant. Awareness of
exposure as short as possible. The British Medical Ultrasound the timing of injury and its manifestation on cUS are vital and
Society (BMUS) has published guidelines for diagnostic routine scanning must be of high quality with maximal
ultrasound (www.bmus.org). The power used should be coverage of the whole brain, and appropriate to the
kept within the guidelines with the default setting as low population of infants under review.
as possible compatible with obtaining diagnostic images.
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Cranial Ultrasound – Teaching package
Orientation:
A side-identifying mark should be recorded on each image (e.g. Rt Coronal, midline, Rt or Lt)
For consistency with MRI and CT practice, coronal images should be viewed with the right
side of the baby on the left hand side of the screen, and sagittal images with the nose
towards the left hand side of the screen (when looking at the screen).
Descriptions:
It is recommended that when reporting the result of the cranial ultrasound you provide a
description of what you see rather than use a grading system. This description should include
comments on the midline, ventricles and parenchyma. It should identify relevant normal
findings (e.g. intact midline structures) and describe the abnormal features. Although in wide
use the classification suggested by Papile is unhelpful for our purpose[1]. It is based on the
appearance on CT scanning of infants who where identified as having had a cerebral
intraventricular haemorrhage on cranial ultrasound.
A common early finding is the presence of increased echodensity in the region of the trigone.
This is usually referred to as increased periventricular echodensity and, if this resolves within
the first week, is not associated with adverse neurodevelopmental outcome. If the
echodensity persists beyond 2 weeks it may be associated with clumsiness and mild
diplegia[2, 3]. The persistent echodensity may undergo cystic change. This lesion is
associated with a high risk of cerebral palsy[4].
Communication of results
Performing a cranial ultrasound on a patient can cause great anxiety for parents and
communication of the results should be done in a sensitive manner. It is best that experience
of such discussions should be gained whilst sitting in on senior colleagues before attempting
to communicate the results of your scan. It is part of good clinical practice to document such
communication with parents.
The power On switch can be found at the left hand side of the machine.
All of the following should be the default settings i.e. automatically set when the
machine is switched on.
→ Select the “A” probe ( 7 MHz).
→ Pre-set program “A” for Neonatal head settings.
→ Confirm orientation, pink mark on probe usually indicates left-side.
Press “New patient “ key and enter the patient details. This should include the
patients name, date of birth and initials of the person performing the scan.
Label orientation (R on the left side of the image) and confirm the orientation by
testing the probe.
Apply sufficient gel to cover the head of the probe head. Note patients will have
their own individual gel pot.
NB, to reduce the risk of cross infection, standard hand and incubator hygiene
should be maintained. Clean the probe and cable with alcohol based wipes and
use good hand washing techniques before opening incubators.
Appropriate depth, gain (power) and slope (time gain curve) should be used to
produce a uniform echo pattern in the near and far fields.
→ The appropriate controls for this are; depth dial – adjusted so that the image
fills the view, gain is set by turning the dial that surrounds the centre track ball
(default is 80 – seen at the lower right of the monitor), slope - is set using the
sliding dials on the top right of the control panel.
Focal depth: this can be adjusted vertically (triangle on the right side of the
monitor and can be adjusted on the control panel, central buttons labelled focus).
Typically this should be adjusted so that the best resolution occurs at the depth
of the structures you are most interested in viewing.
Obtain the standard views that can then be frozen (button labelled as such
bottom right corner) and then printed (button bottom left corner).
Finally, document the results of the scan in the patient notes, Cranial ultrasound
folder and make a plan to communicate these results to the parents in an
appropriate manner.
Coronal Views
Note: The sequence does not include
view [4] Through the (level of the
quadrigeminal cisterns) but does
include [6] (occipital periventricular
view).
Sagittal Views
Sagittal Views – Midline (6)
Sagittal Views – Parasagittal (7)
Sagittal Views –Tangential Parasagittal (8)
Measuring the Ventricular Index
The above diagram illustrates the different measurements to estimate the size of the
ventricles. We use (A) which measures the lateral extent of the ventricle in a line
perpendicular to the midline. This is plotted on a centile chart and is used in combination with
the head circumference to assess the degree of hydrocephalus.
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Early Human Development (2006) 82, 827–835
a v a i l a b l e a t w w w. s c i e n c e d i r e c t . c o m
w w w. e l s e v i e r. c o m / l o c a t e / e a r l h u m d e v
KEYWORDS Abstract Cranial ultrasound is the most available and easily repeatable technique for imaging
Cranial ultrasound; the neonatal brain. Its quality and diagnostic accuracy depend on various factors; the suitability
Newborn infant; of the ultrasound machine for neonatal cranial work, the use of optimal settings and probes,
Brain; appropriate scanning protocols, the use of a variety of acoustic windows and, not least, the
Timing; scanning experience of the examiner. Knowledge of normal anatomy and the echogenicities of
Scanning protocols; different tissues in normal and pathological situations as well as familiarity with the physiological
Teaching and pathological processes likely to be encountered is vital. This paper assesses the value and
appropriate use, safety and diagnostic accuracy of modern, high-quality ultrasound in evaluating
the brain of the preterm and term born infant. Issues of concern regarding teaching, supervision
and experience of the examiner are also addressed.
© 2006 Elsevier Ireland Ltd. All rights reserved.
Contents
1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 828
2. Scanning protocols . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 828
2.1. Preterm infants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 828
2.2. Term born infants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 830
2.2.1. Hypoxic–ischaemic encephalopathy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 830
2.2.2. Infant with seizures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 832
2.3. The dysmorphic or floppy infant and those with metabolic disorders . . . . . . . . . . . . . . . . . . . . . 832
3. Acoustic windows . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 833
4. Safety . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 834
Abbreviations: BG, Basal ganglia; BW, Birth weight; CP, Cerebral palsy; CT, Computed tomography; cUS, Cranial ultrasound; ECS,
Extracerebral space; GA, Gestational age; HC, Head circumference; HIE, Hypoxic–ischaemic encephalopathy; HPI, Haemorrhagic parenchymal
infarction; IHF, Interhemispheric fissure; IVH, Intraventricular haemorrhage; MRI, Magnetic resonance imaging; PVE, Periventricular
echogenicity; PVL, Periventricular leukomalacia; TEA, Term equivalent age; WM, White matter.
⁎ Corresponding author. Tel.: +44 20 8383 8515; fax: +44 20 8383 2473.
E-mail addresses: [email protected] (L.M. Leijser), [email protected] (L.S. de Vries), [email protected] (F.M. Cowan).
1
Current address: Department of Paediatrics, Division of Neonatology, Leiden University Medical Center, Albinusdreef 2, P.O. Box 9600, 2300
RC Leiden, The Netherlands. Tel.: +31 71 5262909; fax: +31 71 5248199.
0378-3782/$ - see front matter © 2006 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.earlhumdev.2006.09.018
828 L.M. Leijser et al.
Cranial ultrasound (cUS) is the most readily available and Preterm infants have a high risk of hypoxic, haemorrhagic
easily repeatable technique for imaging the neonatal brain. and inflammatory cerebral lesions, mainly IVH, HPI, cystic
In contrast to other neuro-imaging tools such as magnetic and non-cystic PVL and more diffuse white matter (WM)
resonance imaging (MRI) and computed tomography (CT), it injury. Cerebellar abnormality is probably more common
can be done bedside with little disturbance to the infant. than realised [8–11]. These findings are of clinical impor-
Neonatal cUS has been used for over 25 years and early tance, making the use of appropriately timed screening
studies on intraventricular (IVH) and parenchymal haemor- protocols necessary.
rhage (HPI), post-haemorrhagic ventricular dilatation and Perlman et al. [12] recommended that preterm infants of
cystic periventricular leukomalacia (PVL) have helped birth weight (BW) <1000 g should be scanned between days
greatly our understanding of risk factors for neurodevelop- 3–5, 10–14, around day 28 and pre-discharge; that those
mental abnormalities. Advances in technology have between 1000 and 1250 g are scanned between days 3–5, day
improved the quality of cUS imaging such that it can be a 28 and pre-discharge and those between 1250 and 1500 g
reliable tool for following brain development and showing between days 3–5 and pre-discharge. This recommendation
the most frequently occurring forms of cerebral injury in was based on data obtained using this protocol in about 250
the preterm and term born infant brain. The range of cUS preterm neonates. 65% of IVH was detected in the 1st week
diagnoses has increased with the recognition of more subtle after birth, the remaining in the 2nd/3rd week. Cystic PVL
patterns of injury and the appreciation of features occurred in larger, more mature infants and was not always
suggestive of developmental, metabolic and infectious preceded by increased periventricular echogenicity (PVE). In
disorders. 2/9 infants it was only detected on the pre-discharge scan.
In recent years concerns have been raised that cUS is not Ventriculomegaly was detected on the initial scan in 50% but
able to detect more subtle abnormality in the preterm infant only after day 28 in 33%. Significant lesions were detected on
[1–4] and that it is not reliable for detecting lesions in the term the pre-discharge examination in 9 infants for the first time.
infant with HIE and focal infarction. The arrival of MRI with its In this study 13% of neonates died in the first 24 h and were
multi-slice coverage of the whole brain and large range of not scanned.
sequences has led a very negative press as far as cUS is con- The American Academy of Neurology in 2001 reviewed
cerned. This negativity is not well supported by comparative neuro-imaging strategies for evaluating preterm and ence-
studies where both techniques receive the same time and phalopathic term born infants [13] and recommended
expertise regarding image acquisition and analysis [5,6]. practice parameters for imaging of the newborn infant
The quality of cUS imaging and its diagnostic accuracy, as brain. They suggested that in preterm infants <30 weeks'
with any other imaging technique, depends on many gestational age (GA), routine cUS should be performed once
factors. These include not only the suitability of the between 7 and 14 days of age and optimally repeated be-
equipment for neonatal cranial work and the use of tween 36 and 40 weeks' postmenstrual age. They argued that
appropriate settings and probes, but also scanning at with this strategy lesions that influence clinical care (e.g.
appropriate times depending on the pathology being sought, IVH) and provide information about long-term outcome (e.g.
the use of different acoustic windows and not least the PVL and ventriculomegaly) would be detected.
experience and expertise of the examiner. Both these scanning protocols give rise to concern.
This review assesses the value of appropriate timing of Neither recommends scanning on admission, which is
modern, high-quality cUS in evaluating both the preterm essential for detecting lesions of antenatal onset [14].
and term born infant brain and highlights the current areas Their recommendations were based on their existing proto-
of emphasis in this important field of neonatal medicine. col and thus they do not know whether a more extensive
protocol would have detected more abnormalities. The
2. Scanning protocols protocol by Ment et al. [13] is limited to preterm infants
< 30 weeks' gestation with no recommendations for older
There are some technical guidelines on scanning quality and preterm infants.
image acquisition [7] but there is no universal agreement Pierrat et al. [15] used frequent cUS examinations and
about optimal timing for neonatal cUS. Scanning protocols compared the evolution of localized and extensive cystic PVL
vary considerably between different neonatal units. This with neurodevelopmental outcome. Localized cysts devel-
variability reflects the different purposes for scanning which oped after the first month from birth in more than half of the
include diagnosis, assessing aetiology and predicting out- infants and were often no longer visible around term
come, and the population of infants examined, imaging skills equivalent age (TEA). De Vries et al. [16] in a tertiary unit
and interest of the examiner, the availability of an setting, used high-resolution, sequential cUS in preterm
ultrasound scanner on the neonatal unit and experienced infants for predicting cerebral palsy (CP). Infants were divided
staff, cost-effectiveness and potential hazards. into those <32 weeks' GA and those between 33 and 36 weeks'
Using cerebral ultrasound effectively in the newborn infant 829
Table 1 cUS scanning protocol for preterm infants used TEA. Horsch et al. [17] related signs of brain atrophy
at the neonatal unit of the Hammersmith and Queen (enlarged sub-arachnoid spaces (ECS), widened interhemi-
Charlotte's Hospital, London - a tertiary referral centre spheric fissure (IHF), reduced complexity of gyral folding) on
sequential cUS of preterm infants with neurodevelopmental
Gestational age at birth (weeks) outcome at 3 years' of age. Infants without major lesions but
23–26 27–29 29–32 32–35 with signs of atrophy at discharge had significantly poorer
Postnatal age 1, 2 and Day 1 Day 1 Day 1 neurocognitive outcomes. A recent paper by Anderson et al.
at which cUS 3 days [18] measuring the length of the corpus callosum and
should be 1 week 1 week 1 week 1 week cerebellar vermis has shown early changes that inform the
timing of the effects of preterm birth on brain development —
performed 2 weeks 2 weeks
Weekly to Weekly 3 weeks 3 weeks information that would be difficult to obtain by other imaging
31 weeks to means in such a large group.
31 weeks Based on these studies and the population admitted to our
Alternating At tertiary neonatal unit, we developed a scanning protocol for
weeks to 36 weeks preterm infants (Table 1). All infants admitted to the unit
36 weeks have a cUS scan done by the SpR (middle grade staff) and
Term Term Term Term reviewed the next day on the ward round. The purpose of this
admission scan is to ascertain that neurodevelopmental
anatomy looks normal, there are no features to suggest
congenital infection, metabolic disease or long-standing
GA, and scanned weekly until discharge and once more at TEA. brain injury and also to identify recently evolving problems
cUS detected abnormalities in the majority (94%) of children such as haemorrhage or white matter (WM) echogenicity.
in whom CP was evident by 2 years. The risk for CP was the Equally important is to note that the scan appears normal at
same for both groups of infants. Infants of 33–36 weeks' GA are this time.
a population of increasing neurodevelopmental concern that On the early cUS scans special attention should be paid to
frequently are not scanned at all in the UK. In 29% of infants the presence of IVH and periventricular flaring, while the later
<32 weeks' GA cystic PVL, the most predictive marker for CP, cUS scans identify evolving parenchymal lesions (cystic PVL or
was only detected after 28 days. This data gives evidence that HPI), the development and progression of post-haemorrhagic
cUS can detect most lesions leading to CP if scanning is ventricular dilatation and signs of atrophy (enlarged lateral or
performed frequently until discharge and again around TEA third ventricles especially without evidence of IVH, irregular
and supports the need for scanning all gestation preterm ventricular margins, a thinned rim of WM around the lateral
infants admitted to a neonatal unit. ventricles, a thin corpus callosum and widened IHF and ECS
Evidence of suboptimal brain growth or atrophy is and changes in the cerebellum (Fig. 1). When assessing the
frequently present in preterm infants, particularly around significance of enlarged ventricles and ECS it is necessary to
Figure 1 Series of ultrasound images from a 24-week IUGR infant. (a, b) Day 2 showing abnormal echogenicity and loss of definition
of the cerebellum suggestive of haemorrhage; (c, d) 4- to 6-week scans showing the development of echogenicity in the caudothalamic
notch (c) and lenticulostriate vasculopathy (d); (e) 8-week scan showing a widened 4th ventricle and persisting abnormal echogenicity
behind the cerebellum; and (f) areas of low echogenicity within small cerebellar hemispheres. (g, h) MRI scan at term equivalent age
showing an obvious 4th ventricle, small vermis and cerebellar hemispheres with haemorrhage and also an increased interhemispheric
fissure and widened extracerebral space (also seen on cUS, images not shown). All the abnormality that is seen on the MRI was seen on
cUS. Additionally the cUS showed the development of echogenicity in the caudothalamic notch and the LSV not seen on the term MRI.
830 L.M. Leijser et al.
Table 2 Clinical indications for additional scans to a 2.2. Term born infants
standard protocol
In term born infants, hypoxic–ischaemic encephalopathy
A sudden deterioration in clinical state
A sudden increase in the need for ventilatory support (HIE) and stroke are still the major causes of, respectively,
Necrotizing enterocolitis diffuse and focal brain injury and neurological morbidity.
Repeated episodes of apnoeas and/or bradycardias
A sharp fall in haemoglobin level 2.2.1. Hypoxic–ischaemic encephalopathy
Onset of seizures or change in neurological status cUS is often considered not very helpful in detecting
Increasing ventricular dilatation lesions occurring with HIE or predicting outcome, as the
Abnormal head growth initial swelling makes focal lesions difficult to detect and
Before and after lumbar puncture and for drainage of CSF precisely locate. The American Academy of Neurology [13]
Before and after surgery recommended that in encephalopathic term infants a CT
should be performed to detect haemorrhagic lesions and if
findings are inconclusive, MRI should be performed between
days 2 and 8 to assess the location and extent of injury. They
give no data supporting the diagnostic value of cUS in HIE.
measure the head circumference (HC) and review the pattern cUS in term born infants with suspected HIE has several
of head growth. A small group of infants develop an enlarged roles. Scanning as part of the admission procedure identifies
ECS associated with increased HC centiles and these children congenital structural cerebral abnormalities, detects evi-
are of less concern. dence for long-standing or more recently established injury
In addition to detecting lesions, assessing their site and initiated prior to the onset of labour, and detects abnorm-
extent is important for accurate prediction of outcome. In alities characteristic of non-HIE causes of encephalopathy,
preterm infants, unilateral HPI located at the trigone is e.g. a hypoplastic corpus callosum suggesting a diagnosis of
associated with a less favourable outcome than lesions in the non-ketotic hyperglycinaemia (Fig. 2) and germinolytic cysts
fronto-parietal region [19]. Multiple PVL cysts in the suggesting mitochondrial or peroxisomal disorders or con-
(parieto-)occipital but not the frontal regions are highly genital infection. This information is clearly important for
predictive of adverse motor outcome [20]. Even when cUS is early diagnosis and management. Additionally, with cUS, the
performed optimally, unexpected cases of CP occur. This may evolution of intrapartum injury can be followed and apart
in part be due to cerebellar lesions [21] which can be difficult from clinical implications this information is very important
to detect or to subtle injury that has occurred antenatally; in medicolegal issues.
awareness of the importance of assessing the posterior fossa Our protocol for scanning infants with suspected HIE is
structures and scanning through acoustic windows other than that a scan should be performed on admission, at 24 h ours
the anterior fontanelle may be needed (see below). after birth, days 3–4, days 7 and 14, and once again in clinic
Stroke occurs in preterm infants [22,23], often affecting at 4–6 weeks.
the central grey matter, and may only be detected by careful The initial cUS, mainly performed to exclude other causes
sequential scanning. It is more common in those with of encephalopathy, by identifying any abnormal anatomy,
congenital heart disease and twins (particularly with twin- evidence for established damage (e.g. presence of calcium,
to-twin transfusion syndrome), a high risk group that should marked echogenicity and parenchymal echolucency), lenti-
all have a postnatal cUS scan. It is also important to scan culostriate vasculopathy, germinal matrix cysts, diffuse WM
sequentially preterms who become sick or have unexpected echogenicity (Fig. 3) or signs of recent haemorrhage. In our
postnatal events and also to scan prior to surgery in case of experience, haemorrhage is well seen on cUS and the need for
complications (Table 2). Unusual patterns of WM echogeni- CT is restricted to infants with a traumatic assisted delivery,
city and the appearance of cysts may reflect infections in the where a midline shift is seen on cUS and neurological
central nervous system. These include fungal infections, intervention is considered. Data from Eken et al. [27] show
viruses [24,25] and a range of bacterial infections [26]. These that the majority of cUS scans in the first 6 h are normal in HIE
data apply both to preterm and term born infants. but if they are already abnormal the outcome is poor.
Figure 2 Hypoplastic corpus callosum (a, short arrow) and mildly echogenic white matter (b, longer arrow) in an encephalopathic
term infant with non-ketotic hyperglycinaemia (NKHG). Typical widely spaced ventricles from another patient with NKHG (c).
Using cerebral ultrasound effectively in the newborn infant 831
Figure 3 Term infant with evidence of acute asphyxia, retroplacental clot and severe encephalopathy. Initial cUS scans showed
small germinolytic cysts (a) and an unusual pattern of periventricular white matter echogenicity (a, b). Scans at 10 days show enlarging
cysts (c), and specks of calcification (shown on the axial view taken via the mastoid window (d)). Evolving acute lesions typical of
hypoxic ischaemia particularly to the basal ganglia are seen (arrows) in panels (e) and (f). There was a history of an acute
gastrointestinal illness associated with eating uncooked foods in France at 33 weeks GA. No evidence of a viral or metabolic disorder
was confirmed; the clinical course is that of a dystonic spastic quadriplegia consistent with the basal ganglia lesions seen in (e) and (f).
Acute changes on cUS suggestive of HIE may include Doppler ultrasound gives useful information in HIE [28].
diffuse brain swelling on days 1–2 (Fig. 4a), though for Measurements can be made at the time of the cUS imaging; it
infants with only a relatively short hypoxic insult swelling is not critical which intra-cerebral vessel is used — usually
may not be seen. There follows a loss of normal tissue the anterior cerebral artery via the anterior fontanelle or the
differentiation and increasing echogenicity of basal ganglia
(BG) and thalami and WM over the next 3–4 days. The cortex
often appears very echolucent compared to the adjacent
hyperechogenic WM and sulci (Fig. 4c) in the first days but
later may become hyperechogenic if severely damaged (Fig.
4b). BG and thalamic echogenicity typical of an acute
hypoxic–ischaemic insult is usually bilateral, increases daily
and has a characteristic appearance (Fig. 4b,c). Generalised
bilateral WM echogenicity is suggestive of a more long-
standing subacute insult; both central grey matter and white
matter are involved in more severe acute or mixed insults
when additionally the cortex appears abnormal. Milder
changes can be subtle and are often not seen before 7 days
after the insult. With severe widespread injury, the WM
becomes increasingly echogenic and then breaks down into
cysts. In a recent study by our own group reviewing
sequential early cUS of 139 term born infants with mild–
severe HIE (unpublished data), we found that the presence of
abnormal echogenicity in the BG and the visualization of the
internal capsule, seen as an echolucent line running through
the BG region (Fig. 4b,c), were highly predictive of an
abnormal motor outcome. Figure 4 (a, Coronal) Acute swelling with loss of grey-white
Late cUS findings after focal BG lesions include persisting matter differentiation. (b, Coronal and c, parasagittal) Evolving
echogenicity in the deep grey matter and dilatation of the abnormality in the lentiform nucleus (short black arrow) and the
third ventricle, signs significant for motor outcome (Fig. 4d). thalamus (long black arrow) with a line of low signal indication
Widening of the IHF suggests poor hemispheric growth and is the site of the internal capsule (indicated by the straight line
associated with poor cognitive outcome. These signs present between the arrows). (d, Coronal) Widening of the 3rd ventricle
on later scans are of concern despite apparent clinical (white star), and enlargement of the interhemispheric fissure
improvement in the first few weeks after birth. and the extracerebral space (arrows) at 6 weeks.
832 L.M. Leijser et al.
Figure 5 (a) View through the temporal window enabling visualization of the middle cerebral artery; below are a normal Doppler
spectra with a PI of 0.8. (b) Abnormal Doppler spectra in HIE with a PI of 0.5.
middle cerebral artery via the temporal window (Fig. 5a). is not possible to obtain an MRI scan. However, there is no
Two parameters can be assessed, the total flow velocity doubt that an MRI in the first 1–3 weeks is superior for
(CBFV) and the pulsatility index (PI) (confusingly referred to defining lesions and giving more precise long-term prognosis
as the resistance index (RI) in obstetric papers). Normal in HIE but the value of cUS should not be underestimated in
values for the PI are between 0.65 and 0.85 the first days after birth and for monitoring at 4–6 weeks
when a normal cUS scan, clinical examination and head
peak systolic velocity the end diastolic velocity growth are good prognostic indicators.
PI ¼
peak systolic velocity
2.2.2. Infant with seizures
Abnormal values < 0.55 occur in severe HIE usually
Term infants with early neonatal seizures who had fairly
between days 2 and 4 after birth (Table 3) (Fig. 5b). The
normal Apgar scores and were not acidotic at birth are most
outcome of infants with abnormal values in the first 6 h after
likely to have had a neonatal stroke; other more common
birth is very poor and suggests a prolonged insult either
diagnoses are parasagittal infarction and focal haemorrhage.
intrapartum or 1–2 days prior to delivery [27]. The absolute
Neonatal stroke has an estimated prevalence of at least 1/
flow velocities are more difficult to assess as they require the
4000 live births. It is an important cause of hemiplegic CP and
angle of insonation on the vessel to be near to zero and the
other neurological disabilities. cUS is often said to have a poor
values vary with the vessel measured on. However, high
sensitivity for detecting focal infarction. We found that early
values carry a poor prognosis and are associated with a low PI.
cUS (days 1–3) showed abnormalities suggestive of infarction
Doppler measurements are useful in assessing venous flow
in 68% of cases and in 87% when cUS was performed after day 4
especially in the straight sinus in suspected venous throm-
[5]. Infants whose late cUS scans remained normal had rela-
bosis (often associated with IVH or thalamic haemorrhage
tively small, mostly posterior infarcts; none of these infants
[29]) and to document abnormal velocity patterns in
developed a hemiplegia. Thus, neonatal cUS does allow the
suspected vascular malformations.
detection of abnormality suggestive of focal ischaemic
We find cUS, both imaging and Doppler, of great use in
lesions, particularly those likely to lead to hemiplegia.
excluding non-HIE diagnoses and in following the timing and
We perform cUS scans on infants presenting with seizures
evolution of acute injury. cUS together with electrophysio-
on admission and then at 2 days, 5–7 days and 2 weeks after
logical data and clinical progress often allows early prognosis
the onset of seizures. Special attention should be paid to
and appropriate clinical management in a situation where it
presence of subtle asymmetrical parenchymal echogenicity,
a wedge shaped echogenic area suggestive of middle cerebral
artery (MCA) infarction (Fig. 6), a rounded very echogenic
Table 3 The predictive value of the pulsatility index (PI) lesion suggestive of haemorrhage (Fig. 7) and any abnormal
and cerebral blood flow velocities (CBFV) for adverse structural development suggestive of a developmental
neurological outcome in HIE in term born infants abnormality. We suggest however that for any infant with
Measurements made 2–4 days after birth Levene et al. [28] seizures a neonatal MRI examination is performed; precise
Abnormal CBFV Low PI <0.55 detail of lesion size, location and prognosis are better defined
Sensitivity 57% 60% on MRI [30,31] allowing more precise prognosis.
Specificity 88% 63%
PPV 94% 83% 2.3. The dysmorphic or floppy infant and those with
Early (< 6 h) measurements Eken et al. [27] metabolic disorders
Sensitivity Specificity
Ultrasound 42.1% 60% Dysmorphic features and the floppy infant syndrome can be
Doppler 23.5% 100% indicators of developmental disorders and congenital infec-
tion, genetic/chromosomal syndromes, congenital or
Using cerebral ultrasound effectively in the newborn infant 833
Figure 6 Full term infant with neonatal seizures. Large wedge-shaped area of echogenicity on the right (a, b, c parasagittal) is
shown including the basal ganglia typical of a middle cerebral artery territory stroke. MRI confirms the diagnosis (d) T1W, (e) diffusion-
weighted and (f) follow-up scans.
Figure 7 cUS of: (a) coronal, (b) parasagittal and (c) mastoid view from a 31-week infant with low platelets showing a large recent
focal haematoma with a midline shift (a, short arrow). 20 cm3 of blood removed by subdural drainage. MRI (d, e) following tap.
834 L.M. Leijser et al.
(junction of the lambdoid and sagittal sutures) and mastoid neonatal units in New Zealand. They showed that there was only
fontanelle (junction of the posterior parietal, temporal and moderate agreement between the reviewers' reports and those
occipital bones) can help to detect lesions and structural of the neonatal units and between the reviewers; the reviewers
malformations in these areas [19,21,33,34] (Fig. 7). Imaging reported 3–6 times more WM damage.
through the temporal window allows good views of the These studies highlight the need for more widespread
mesencephalon and brainstem. formal training in scanning techniques and that teaching of
cerebral anatomy, the appearance of normal structures, an
understanding of normal growth as well as knowledge of the
4. Safety appearances and evolution of different pathologies are
Although sequential cUS is clearly very important, its potential essential for those responsible for acquiring and interpret-
hazards and burden for the often sick and unstable newborn ing cUS scans. These skills need to be assessed and
infant should be kept in mind. These include extra handling, competencies maintained. Increased collaboration between
applying pressure and cold gel to the fontanelle, the risk of neonatologists, radiographers and radiologists with an
dislodging tubes or lines or introducing infection from equip- interest in neonatal scanning and prognosis is needed in
ment that is not kept clean or from the operator. Most of these order to improve and rationalise the use of this valuable
issues are relatively easy to prevent when appropriate safety technique.
and hygienic precautions are taken. All ultrasound equipment
for use on a neonatal unit must be kept regularly cleaned, the 6. Conclusions
probes wiped with a damp cloth. We also use hard surface wipes
that contain some alcohol but these are not suitable for all Current evidence is that cUS imaging using modern machines,
probes and the manufacturers should be consulted. probes, a variety of acoustic windows and sequential scanning
There are also concerns about potential hazards of the at optimal times gives high-quality images that are diagnos-
ultrasound waves. To date no adverse effects have been tically accurate. Issues of teaching, supervision and experi-
shown to result from the sequential use of ultrasound in ence for both paediatric and radiological staff need to be
newborn infants or fetuses, although a slightly increased risk addressed and collaboration between paediatric and radi-
of delayed speech [35], left handedness [36] and intrauterine ology departments is needed to improve protocols, image
growth restriction [37] after multiple fetal examinations has quality and interpretation. Whilst MRI does have advantages
been reported. However, ultrasound waves, especially when over cUS and clear clinical indications, especially in the term
used for colour Doppler imaging, may induce temperature born infant, cUS facilitates early bedside diagnosis and
elevations in human tissue over time that have the potential monitoring of pathology in a way that is relatively easy and
to cause damage. It is important to keep the duration of not disturbing and safe for the newborn infant. Awareness of
exposure as short as possible. The British Medical Ultrasound the timing of injury and its manifestation on cUS are vital and
Society (BMUS) has published guidelines for diagnostic routine scanning must be of high quality with maximal
ultrasound (www.bmus.org). The power used should be coverage of the whole brain, and appropriate to the
kept within the guidelines with the default setting as low population of infants under review.
as possible compatible with obtaining diagnostic images.
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