Abstract
OBJECTIVE. The purpose of this article is to describe the
role of cerebral and abdominal sonography with color Doppler sonography,
including assessment of multiorgan tissue perfusion, in neonates with
hypoxic-ischemic injury.
CONCLUSION. Bedside sonography and color Doppler sonography
of the brain and abdominal organs can provide reliable and comprehensive
information in asphyxiated neonates with hypoxic-ischemic injury. This article,
which includes pathologic correlation, illustrates the major sonographic
findings in this critical population.
Perinatal
asphyxia is a major contributor to neonatal death and morbidity. Each year,
approximately 23% of the 4 million neonatal deaths and 8% of all deaths at
younger than 5 years of age throughout the world are associated with signs of
asphyxia [1]. Indeed, even at
referral centers in developed countries, death or moderate to severe disability
occurs in 53–61% of infants diagnosed as having moderate to severe hypoxic-ischemic
encephalopathy [2]. Several
randomized controlled trials have shown that therapeutic hypothermia is a
neuroprotective strategy that improves death and disability in neonates with
moderate to severe hypoxic-ischemic encephalopathy, and this treatment has been
adopted as the standard of care by most centers around the world [2].
During asphyxia,
gas exchange between the fetus and the placenta is compromised, resulting in
fetal hypoxia, hypercarbia, and acidosis. Subsequently, a marked redistribution
of blood flow occurs, with an increase in the flow to the brain, heart, and
adrenal glands and a decrease in the blood flow to the kidneys, bowel, and
skin. Indeed, multiple-organ failure has been reported in 50–60% of neonates
with severe perinatal asphyxia [3]. If this process
lasts long enough, cerebral blood flow decreases by a combination of abnormal
cerebral autoregulation and systemic hypotension, leading to cerebral
hypoperfusion and subsequent hypoxicischemic injury [4]. During the
postasphyxiated period, an increase in cerebral blood flow may unfold, with the
onset generally within the first few hours of life and duration of many hours
or days. This chain of events is called reperfusion or the hyperemic phase and
is responsible for secondary brain injury.
In neonates with
hypoxic-ischemic encephalopathy, high levels of cerebral blood flow measured at
12–24 hours of life have been associated with more severe brain injury [3]. A substantial
proportion of asphyxiated infants (35–85%) exhibit predominantly cerebral deep
nuclear neuronal involvement [5], and injury to
these areas has been associated with unfavorable neurologic outcome [5, 6]. Therefore,
measurements of brain perfusion with dynamic color Doppler sonography during
this period may provide information that correlates with reperfusion injury.
Dynamic Color Doppler Sonography for Tissue
Perfusion Measurements
Over the past few
years, we have used a recently developed software program (Pixelflux,
Chameleon-Software) to dynamically quantify the color Doppler signals and
obtain tissue perfusion measurements, specifically of the brain and bowel [7]. This color
Doppler quantification method provides dynamic blood flow data (during the
cardiac cycle) and perfusion velocity in a chosen region of interest (ROI) from
a standard color Doppler video, without IV contrast administration. Tissue
perfusion is quantified, taking into consideration the amount of blood flow
through a specific tissue during a complete cardiac cycle and therefore
reflecting the differences between systolic and diastolic perfusion in the
small vessels of the specified area. The average values of the flow velocity
and area inside the ROI are measured during the cycle and used for the
calculation of tissue perfusion intensity (PI):
where v
is the mean velocity of pixels, A is the area of all color pixels and A ROI is the area of the ROI.
All this calculation
is done automatically for images encompassing one full heart cycle, which is
also detected automatically by the software [7].
For all studies,
the color Doppler parameters are standardized and kept constant for comparison
between studies (color gain, 40; scale, 7.5 cm/s). Color Doppler videos with
major motion artifacts are excluded, and the ROI is only determined in areas
without artifacts through-out the duration of the video. All neonates who have
congenital heart disease or are hemodynamically unstable are excluded. During
these studies, it is critical to obtain information on several physiologic
parameters, such as oxygenation (SpO2 or Pao2), carbon dioxide levels (Pco2 or TcPco2), blood pressure (systolic, mean, and diastolic),
and body temperature (skin and esophageal). Information on the use of
medications, such as inotropes, vasoconstrictors, vasodilators, and sedatives,
is also important because it can affect tissue perfusion. Clinical or
electroencephalography seizures should also be recorded.
In asphyxiated
neonates, brain monitoring and assessment are usually done by
electroencephalography and MRI [5, 8]. However,
ultrasound is an attractive tool given its portability and lack of ionizing
radiation. In this article, we will illustrate the most common findings of
sonography performed at the bedside to assess the brain and abdominal organs in
asphyxiated neonates. We will also describe our experience with the use of
dynamic color Doppler sonography. Although the clinical usefulness of the
information obtained with dynamic color Doppler sonography has not yet been
established in this population, such tissue perfusion measurements have been
applied in many different settings with positive and encouraging results. Indeed,
tissue perfusion measurements using dynamic color Doppler sonography have been
proven useful to describe local inflammatory activity in bowel segments
affected by Crohn disease in pediatric patients [9], assess
perfusion of transplanted kidneys [10], and
differentiate stages on metastatic lymph nodes [11].
Brain
As indicated
previously, MRI is the standard imaging modality of the brain in neonates with
perinatal asphyxia because it provides anatomic and functional information that
help determine the severity of the disease and the prognosis. It depicts
different patterns of injury, such as watershed injury or involvement of basal
ganglia and thalami, as seen in the more severe cases. Although head sonography
is thought to be less accurate than MRI, in a recent study, a good correlation
between studies and MRI of the brain parenchyma was shown in the assessment of
hypoxic-ischemic injury [8]. This suggests
that head sonography may be a more effective modality than previously
described. Moreover, head sonography remains an excellent screening tool for
use in neonates too critically ill to be transported to the MRI suite.
In our
institution, head sonography is performed in neonates with hypoxic-ischemic
encephalopathy, using a 9S4-MHz sector transducer. The most common head
sonography findings in neonates with hypoxic-ischemic injury are brain swelling
with echogenic subcortical white matter (Fig. 1A), increased
cerebral echogenicity with or without loss of gray-white matter
differentiation, and basal ganglia involvement (Fig. 2A).
Intraventricular bleed (Figs. 3A, 3B, and 3C), although
uncommon, has also been described in term neonates with hypoxic-ischemic
injury. Head sonography can also assess pulsed Doppler flow velocities and the
resistive index of the cerebral arteries [3].
During the head
sonography examination, we also perform dynamic color Doppler sonography (color
gain, 40; scale, 7.5 cm/s) with an 11LW4-MHz linear transducer. DICOM color
Doppler videos of the basal ganglia blood flow are obtained and recorded in the
coronal plane (Figs. S1B and S2B, supplemental videos, can be viewed from the
information box in the upper right corner of this article). These videos are
later analyzed using dedicated software [7] to quantify the
cerebral perfusion intensity of the area (Figs. 1A, 1B, 1C, 1D, 2A, 2B, 2C, 2D, 2E, and 2F). Data obtained
with this technique are currently under investigation, with encouraging
results, as a potential marker of reperfusion injury (Faingold R et al,
presented at the 2011 annual meeting of the International Paediatric Radiology
Congress).
Bowel
Perinatal
asphyxia may also have devastating consequences to the gastrointestinal tract,
and gastrointestinal dysfunction has been described in 29% of neonates with
perinatal asphyxia [12]. Sonographic
evaluation of the intestinal tract can provide information on intestinal
appearance, blood flow velocities, and mural perfusion. At our institution,
gray-scale abdominal sonographic images of the bowel are acquired with linear
transducers ranging from 11 to 18 MHz. The spectrum of sonographic findings
varies with the severity of disease and includes normal bowel wall echotexture,
bowel wall edema, and presence of sloughed mucosa. Sloughed mucosa is defined
as the presence of a halo or echogenic material with echotexture similar to the
mucosa within the intestinal lumen (Figs. 4A, 4B, 4C, and 4D).
In severe
hypoxic-ischemic injury, a significant decrease in mean blood flow velocities
and increase in the resistive index were reported in the superior mesenteric
artery using pulse Doppler evaluation [3]. However,
end-organ involvement has not been described. Tissue perfusion is a crucial
prerequisite for normal function; therefore, quantification of bowel perfusion
is important in the assessment of these critical patients. Indeed, intestinal
mural perfusion patterns have been described before in patients with Crohn
disease [9] and neonates
with necrotizing enterocolitis [13] using color
Doppler sonography and dynamic color Doppler sonography. Intestinal perfusion
findings of these studies were classified as preserved intramural perfusion,
bowel hyperemia, or decreased bowel perfusion (Figs. 5A, 5B, 5C, 5D, and 5E). During
abdominal sonography, we have also obtained DICOM color Doppler videos of the
mural blood flow (Figs. S5A and S5D, supplemental videos, can be viewed from
the information box in the upper right corner of this article) using an
11LW4-MHz linear transducer (color gain, 40; scale, 7.5 cm/s) to assess
intestinal perfusion intensity (Cassia G et al, presented at the 2011 annual
meeting of the International Paediatric Radiology Congress). These data are
also currently under investigation to evaluate whether accurate assessments of
bowel perfusion in asphyxiated infants can help in staging the disease and
understanding the mechanisms of intestinal autoregulation.
Kidneys
Perinatal
asphyxia is one of the most common causes of acute kidney injury in neonates.
The prevalence range has been reported between 30% and 56%, probably an
underestimation given the limitations in the diagnostic criteria [14]. Acute kidney
injury may develop with or without oliguria or increase in serum creatinine
levels. Imaging is not routinely used; however, gray-scale sonography may show
parenchymal hyperechogenicity and loss of corticomedullary differentiation.
Decreased blood flow velocity in the renal artery with pulse Doppler imaging
has been described in severe hypoxic-ischemic injury [3] (Figs. 6A, 6B, 6C, 7A, and 7B).
Adrenal Glands
Adrenal swelling
and thickening have been described in neonates with asphyxia and other causes
of perinatal stress [15].
Sonographically, they may be enlarged or may loose their central echogenic
stripe (Fig. 8A).
Congestion and depletion of cortical lipids are the typical histologic changes
of perinatal asphyxia.
Adrenal
hemorrhage is relatively uncommon in neonates (Figs. 8B and 8C) but has been
described in association with asphyxia, birth trauma, septicemia, and bleeding
diathesis. The incidence ranges from approximately 1.7 per 1000 of autopsied
neonates to approximately 3% in abdominal ultrasound studies [16].
Liver
Perinatal
asphyxia is known to be a possible cause hepatic injury. However, the real
incidence of liver injury is not well established because studies have used
different definitions on the basis of abnormalities of liver enzymes or autopsy
findings. Histologic changes in the liver are seen only with the most severe
degrees of asphyxia. One study reported hepatic injury in up to 39% of neonates
with asphyxia [17]. Imaging of the
liver does not play an important role in the evaluation of these neonates. The
liver is usually homogenous or may show geographic hyperechogenic areas (Figs. 9A and 9B).
Conclusion
Sonography of the
brain and abdominal organs can provide reliable and comprehensive information
in asphyxiated neonates with hypoxic-ischemic injury. Dynamic color Doppler
sonography is a simple bedside technique and a promising tool to be used in the
assessment of multiorgan perfusion injury, monitoring the response to several
drugs or interventions, and helping with the prediction of long-term outcomes
in asphyxiated neonates. It also may provide the necessary information to
improve the understanding of the changes in cerebral and visceral perfusion
occurring in these infants over time.
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