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22 Recent Advances inNeonatal CEUS
269
UCA signal may enable decreased contrast dose
especially in small neonates. As the dose is often
≤0.1–2mL in neonates, it is useful to prepare a
smaller caliber syringe in order to avoid under- or
over-injection of the UCA.Care should be taken
in the neonatal brain when performing a CEUS
examination; avoid switching from CEUS setting
(MI of <0.2) to grayscale setting (MI approximately 1.0) prior to complete contrast washout.
This is due to the possibility of causing unwanted
microbubble destruction in the presence of immature vasculature in select brain regions such as
the germinal matrix. Hence, complete washout of
the UCA prior to resuming grayscale or color
Doppler US evaluation is recommended.
22.3.2 Brain Death
The extreme case of hypoxic ischemic injury is
brain death. While brain death is a clinical diagnosis based on the apnea test, an infant’s inability
to tolerate test necessitates clinicians to rely on
ancillary imaging tests. In the 2011 revised pediatric brain death guidelines, the two most commonly used ancillary studies for validation of
circulatory arrest (CCA) were a radionuclide
examination and four-vessel cerebral angiography [4]. Note that both studies require transportation out of the intensive care unit, which can be
challenging during the critical period. Not all
hospitals are equipped with to perform such studies outside the working day. Compared to these
studies, brain CEUS can be performed at the bedside and promptly at the time of suspicion of
CCA. Furthermore, the examination is costeffective and can readily be adopted into existing
clinical practice.
While further work is needed to introduce
CEUS as an alternative tool to a radionuclide
examination or cerebral angiography in validating brain death, there is evidence that it may help
conrm the absence of brain perfusion and therefore the diagnosis of brain death. In a case report
of an infant with cardiac arrest, brain CEUS was
performed to assess for brain perfusion [5]. In
this infant, perfusion was nearly absent in the
whole brain except for few parasagittal vessels,
and the typical prompt washin and washout of the
UCA (lasting less than 10 min total) were not
observed (Fig.22.3). Instead, UCA washin was
signicantly delayed and washout did not occur
up to 30min at which point the examination was
terminated. Likely, the near absent brain perfusion state was accompanied by increased intracranial pressure due to the severe hypoxic
ischemic injury, which altered both the washin
and washout perfusion kinetics parameters.
Future studies comparing brain CEUS with the
reference standard nuclear examination for the
diagnosis of brain death will be necessary to
advance this novel application.
22.3.3 Intracranial Lesions
In the presence of an acoustic window, such as
the fontanelle or open cranial window during
surgery or craniotomy, CEUS can be valuable
for detailed evaluation of benign and malignant
intracranial lesions. Contrast-enhanced ultrasound offers dynamic perfusion kinetics of
intracranial lesions with excellent spatial and
temporal resolution and enhances the conspicuity of lesional borders [6]. In the case of a tumor,
CEUS can be valuable for distinguishing benign
from malignant tumors, discerning the tumor–
parenchymal border, differentiating edema from
tumor, grading tumor, guiding biopsy, and following treatment response [7–18] (Fig. 22.4).
There is preliminary evidence that CEUS may
aid with tumor grading although its accuracy
needs to be further validated. In the case of vascular malformation, the extent of shunting and
blood volume within the lesion can be qualitatively and quantitatively evaluated with
CEUS.In infants or in the case of cranial window, CEUS permits quantitative assessment of
residual ow post endovascular intervention of
vascular malformation without the need for contrast-enhanced computed tomography (CT),
MR imaging, or angiography. In the case of
multiple lesions such as with abscesses or vascular malformations not readily apparent with
conventional grayscale US, CEUS can enhance
the conspicuity of these lesions.
270
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M. Hwang
Fig. 22.3 Brain CEUS: near brain death. A midcoronal
CEUS image (a) shows avid enhancement of the cervical
extracranial vessels (arrows). For comparison, (b) is a
coronal slice from a 2-month-old male admitted for respiratory distress but without intracranial injury showing
normal enhancement of brain. Within 7min of administration, the UCA had a near-complete washout in the comparison case; however, washout from few intracranial
22.3.4 Bowel Disease ofPrematurity
vessels had not occurred 30min after administration in the
post-cardiac arrest patient, signifying extremely poor
cerebral circulation. There was no further imaging possible following the death (declared dead as per clinical
assessment for brain death) of the child. (Reproduced
with permission from Neuroradiology Journal 2018
Dec;31(6):578–580)
preterm infants, although rare in term infants.
Etiology is thought to be due to intestinal invaBowel disease of prematurity encompasses a
wide variety of bowel pathology affecting preterm infants, including necrotizing enterocolitis,
prenatal volvulus, or atresia. Etiologies could be
due to prenatal or perinatal insult leading to compromise of the blood supply to the bowel. While
conventional grayscale and color Doppler US
have enhanced the diagnostic sensitivity of bowel
disease of prematurity as compared to a
radiograph alone, there are limitations. There is
an inability to quantitate bowel perfusion with
color Doppler US in the presence of an oscillator
or other external vibrator, which is common in
the intensive care unit setting, due to motion degradation. In such case, CEUS which is relatively
motion insensitive can be performed to better
characterize bowel perfusion.
Necrotizing enterocolitis affects up to one in
2000 births and occurs in approximately 10% of
sion of bacteria followed by local infection and
inammation leading to bowel wall destruction,
perforation, overwhelming sepsis, and death.
Diagnosis is made using the Bell’s staging crite-
ria aided by radiographic ndings, which can
vary in manifestation to xed and/or dilated
bowel loops, pneumatosis, portal venous air, and/
or pneumoperitoneum. The diagnostic sensitivity
of the clinical and radiographic criteria combined
is low, and many cases of even advanced necro-
tizing enterocolitis can be missed. In this regard,
color Doppler US has been used to characterize
the evolution of necrotizing enterocolitis to
potentially augment the diagnostic sensitivity.
Prior studies have shown that in the evolution of
necrotizing enterocolitis, avid perfusion to the
bowel wall has been observed. The hyperperfu-
sion seen during the evolution of necrotizing
enterocolitis could be attributable to local inam-
Anaplastic Glioma
Glioblastoma
Phase
Phase
22 Recent Advances inNeonatal CEUS
Low Grade Glioma
271
Baseline
Fig. 22.4 CEUS for tumor characterization. Time frame
of how different grades of glioma are visualized with
CEUS.In the rst column of each row, low mechanical
index US and baseline CEUS (CA arrival − t0) are displayed; then different CEUS phases (time is shown in the
top right corner of each image) are displayed only. The
Arterial
Phase
mation leading to vasodilatation, reperfusion
response to ischemic insult, and/or alterations in
vaso-regulatory mechanisms.
With CEUS a case series has demonstrated
that in necrotizing enterocolitis bowel hyperperfusion, as previously demonstrated with color
Doppler US, follows a similar pattern [19]. The
hyperperfused bowel segment demonstrated
hypoperistalsis and dilatation, as compared to
other bowel loops in the abdomen. On surgical
pathology, both viable and ischemic bowel were
observed. The exact timing and extent of perfusion changes in the affected bowel segment are
not known, but further studies to gather information regarding CEUS behavior would greatly
Peak
image clearly shows the differences in terms of timing,
degree of enhancement, and CEUS patterns for different
types of glioma, with a continuous and dynamic modality.
(Reproduced with permission from Biomedical Research
International 2014;2014:484261)
Parenchymal
Venous
augment the diagnostic sensitivity of CEUS in
necrotizing enterocolitis (Fig.22.5). A diagnosis of early disease can help institute therapies
preventing further cascade of infection/
inammation.
In the same CEUS case series, a preterm infant
with total bowel ischemia due to prenatal volvulus was illustrated (Fig.22.6). Color Doppler US
evaluation in this case was equivocal due to the
presence of an oscillator. Grayscale US of the
bowel loops demonstrated decreased peristalsis
but without evidence of pneumatosis or signicant thickening. With a UCA injection, complete
lack of enhancement of the bowel walls throughout the abdomen was demonstrated, conrming
272
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cd
M. Hwang
Fig. 22.5 CEUS for necrotizing enterocolitis. A 39-dayold formerly premature girl was born at 26 weeks with
abdominal distention and bloody stool. (a) Grayscale US
of the right lower quadrant shows a distended loop of
bowel with wall thickening that was hypoperistaltic in real
time. (b) Corresponding color Doppler US image shows
Fig. 22.6 CEUS for bowel ischemia of prematurity. A
1-day-old formerly premature girl was born at 29 weeks
with gaseous distention on abdominal radiography. (a)
Grayscale US in the left upper quadrant shows multiple
dilated loops of bowel with wall thickening and hypoperistalsis to aperistalsis in real time. (b) Corresponding color
Doppler US image shows apparent ow in the mesentery
but no appreciable ow in the bowel. However, the inter-
hyperemia within the thickened bowel wall. (c, d), Dualscreen display with grayscale US (c) and corresponding
CEUS (d) reveals hyperemia of the bowel wall. On all
images, large volume ascites is present. (Permission to
reproduce from Journal of Ultrasound in Medicine 2019
Nov 9. https://doi.org/10.1002/jum.15168)
pretation was limited by pulsatile motion from the
patient’s high-frequency oscillator. (c, d) Dual-screen
CEUS display shows loops of bowel (c, arrowheads) in
the right upper quadrant that do not enhance (d, arrowheads) regardless of the high-frequency oscillator.
(Permission to reproduce from Journal of Ultrasound in
Medicine 2019 Nov 9. https://doi.org/10.1002/jum.15168)
cd
22 Recent Advances inNeonatal CEUS
Fig. 22.6 (continued)
273
global bowel ischemia, conrmed at subsequent
surgery. Likewise, CEUS can be a useful troubleshooting tool for conrmation of bowel perfusion
in cases where prenatal ischemic insult is suspected and color Doppler US is suboptimal.
enhancement of the femoral head on postoperative MR imaging is strongly correlated with the
future development of AVN [25]. However, there
are challenges with relying on postoperative MR
imaging including the need to leave the operating
room and decreased sensitivity to microcirculatory ow, which is below the resolution of MR
22.3.5 Developmental Dysplasia
oftheHip
imaging. The potential discovery of compromised femoral head perfusion immediately post
reduction could lead to prompt surgical intervenDevelopment dysplasia of the hip (DDH) is the
most common developmental deformity of the
lower extremity in children. It affects 28.5 per
1000 infants [20, 21] and timely diagnosis and
correction are critical to preventing worsening
dysplasia and associated morbidity. While
approximately 80% of infants with frankly dislocated hips can be successfully reduced with a
Pavlik harness or other bracing treatment, some
do not respond to nonsurgical treatment and need
to undergo closed or open reduction followed by
Spica cast immobilization in the operating room.
A major source of morbidity in patients requiring
surgical intervention is iatrogenic avascular
necrosis (AVN), which could result from excessive hip abduction within the cast [22]. AVN can
disrupt normal epiphyseal growth and lead to
premature osteoarthritis, ultimately requiring
total hip arthroplasty [23, 24].
In order to conrm the preservation of femoral
head perfusion post reduction, postoperative
gadolinium- enhanced MR imaging can be performed. It has been shown that decreased
tion prior to departure from the operating room.
In this regard, CEUS may serve as an effective
alternative to contrast-enhanced MR imaging
that can be used in the operating room pre and
post hip reduction.
A prior article described preliminary experience with intraoperative hip CEUS in 17 children with DDH [26]. A scoring system used to
quantify the number of vessels visualized in the
femoral head revealed a decrease in vessel number post reduction as qualitatively evaluated
using CEUS, while all CEUS showed preserved
blood ow in the femoral epiphysis before and
after reduction. All MR imaging studies were
similar to the CEUS examination and showed
femoral head enhancement post reduction. The
article not only demonstrates the feasibility of
safely performing intraoperative hip CEUS in
infants but also suggests the need for a larger
prospective study exploring the long-term
implications of the femoral head perfusion patterns observed on intraoperative CEUS
(Fig.22.7).
274
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M. Hwang
Fig. 22.7 CEUS for hip dysplasia. Imaging landmarks
for epiphyseal blood ow assessment with CEUS in a
20-month-old boy before reduction: CEUS images of the
left hip in a coronal plane. (a) Landmarks used to assess
the vascular ow in the femoral epiphysis. (b) Circle
drawn over the epiphysis, bisected by a line parallel to the
22.4 Conclusion andFuture
epiphysis, traversing the ossic nucleus when visible.
Arrowhead indicates epiphysis; and arrows, epiphyseal
vessels. (Reproduced with permission Journal of
Ultrasound in Medicine 2019 Jul 23. https://doi.
org/10.1002/jum.15097)
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