TYPE Review

PUBLISHED 13 February 2023

DOI 10.3389/fneur.2023.1095280

Application of brain ultrasound in

OPEN ACCESS premature infants with brain injury
EDITED BY
Xiaodong Yang,
Xidian University, China Lu Liu*
REVIEWED BY
School of Cyberspace Security, Xi’an University of Posts and Telecommunications, Xi’an, Shaanxi, China
Haiyan Jin,
Xi’an University of Technology, China
Rong Fei,
Xi’an University of Technology, China Brain injury is the main factor affecting the development and prognosis of the nervous
*CORRESPONDENCE system in premature infants. Early diagnosis and treatment are of great significance in
Lu Liu reducing mortality and disability and improving the prognosis of premature infants.
lznn_980@163.com
Craniocerebral ultrasound has become an important medical imaging method for
SPECIALTY SECTION evaluating the brain structure of premature infants due to its advantages of being
This article was submitted to
Applied Neuroimaging, non-invasive, cheap, simple, and bedside dynamic monitoring since it was applied
a section of the journal to neonatal clinical practice. This article reviews the application of brain ultrasound to
Frontiers in Neurology common brain injuries in premature infants.
RECEIVED 11 November 2022
ACCEPTED 04 January 2023
KEYWORDS
PUBLISHED 13 February 2023

CITATION
cranial ultrasound, intracranial hemorrhage, periventricular leukomalacia, hypoxic-ischemic
Liu L (2023) Application of brain ultrasound in encephalopathy, premature infants
premature infants with brain injury.
Front. Neurol. 14:1095280.
doi: 10.3389/fneur.2023.1095280
1. Introduction
COPYRIGHT
© 2023 Liu. This is an open-access article
distributed under the terms of the Creative
In recent years, with the continuous improvement of medical levels and the rapid
Commons Attribution License (CC BY). The use, development of neonatal intensive care technology, the rescue success rate of critically ill
distribution or reproduction in other forums is newborns such as premature infants and very low birth weight infants (VLBW) has been
permitted, provided the original author(s) and
the copyright owner(s) are credited and that
significantly improved. However, due to immature cerebrovascular development and poor
the original publication in this journal is cited, in cerebral blood flow self-regulation, these types of neonates are prone to cerebral hemodynamic
accordance with accepted academic practice. disorders, thus, the incidence of brain injury is usually higher than in term infants (1, 2).
No use, distribution or reproduction is
permitted which does not comply with these The common brain injury in premature infants mainly includes intracranial hemorrhage,
terms. periventricular leukomalacia, and hypoxic-ischemic encephalopathy (3). However, these brain
diseases do not have significant or specific clinical symptoms at an early stage, thus, it is necessary
to use safe, reliable, and convenient imaging examinations for auxiliary diagnosis. As a simple,
convenient, and non-invasive examination method (4, 5), brain ultrasound plays an important
role in the early diagnosis, severity judgment, and prognosis evaluation of brain injury in
premature infants. This article reviews the application of brain ultrasound to common brain
injuries in premature infants.

2. Characteristics and advantages of craniocerebral

ultrasound
Brain ultrasound is a technique that uses specific sound waves to understand the structure
and pathological changes of brain tissue (6). At present, there are two common methods of brain
ultrasound, namely, B-mode ultrasound and color Doppler ultrasound (7). B-mode ultrasound
belongs to two-dimensional imaging. Real-time imaging is performed on the screen in grayscale.
We can clearly observe the intracranial structure and brain center lesions by sector scan (8).
Color Doppler ultrasound in the B-mode ultrasound on the basis of increased blood flow,

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Liu 10.3389/fneur.2023.1095280

can effectively show changes in brain lesions and lesion tissue (VLBW), the first brain ultrasound examination should be performed
blood flow velocity, vascular distribution, resistance index, and other within 24–48 h after birth to initially assess the brain condition.
hemodynamic signals (9), can more clearly reflect the severity of Thereafter, a review should be conducted every other week until
the disease. the full moon. If necessary, a 3–6 months follow-up review can
The emergence of brain ultrasound technology has opened up a be performed.
new way for clinicians to understand intracranial lesions in vivo (6).
This technology has the advantages of simple and rapid operation,
high accuracy, non-invasive, no radiation, intuitive reflection, and 4. Diagnostic value of brain ultrasound
bedside dynamic monitoring and has become the first choice for the in premature infants with brain injury
clinical diagnosis of brain injury (10).
4.1. Ultrasonic diagnosis of intracranial
hemorrhage in premature infants
3. Methods and timing of cranial
ultrasound examination Premature intracranial hemorrhage is one of the most common
pediatric diseases. The majority occurred within 3 days after birth.
3.1. Methods of cranial ultrasound The cause of the disease is usually perinatal hypoxia, which is
examination harmful. According to the study of Sawyer et al. (17), the mortality
rate caused by intracranial hemorrhage is as high as 50% in premature
Brain ultrasonography should be performed according to specific infants with a gestational age of fewer than 32 weeks and a weight
procedures. First, select the appropriate scanning probe, set the <1,500 g. However, in the early stages of cerebral hemorrhage,
corresponding probe frequency, and disinfect the probe; then, the children usually do not show obvious clinical symptoms, and
children are placed in this position, usually supine or prone, to we can only use imaging tools to diagnose. In many imaging
ensure that the children are in a quiet state and usually do not methods, craniocerebral ultrasound has the advantages of non-
take sedatives; after that, the examiner is located on the right invasive, high repeatability, bedside rapid, and effective evaluation
or top of the patient, and the patient is continuously scanned of the evolution of cerebral hemorrhage, which makes it the first
from front to back, from center to both sides on the coronal and choice for the diagnosis of a cerebral hemorrhage in premature
sagittal planes, through the deflection probe. During the examination, infants (18). Yue Xiangzhu can provide an imaging basis for
attention should be paid to the continuity of the scan to prevent clinical treatment.
missed diagnoses. According to the different bleeding sites, cerebral hemorrhage
According to the different scanning positions, craniocerebral in premature infants can be divided into a periventricular
ultrasound can be divided into four parts, namely, anterior fontanel intraventricular hemorrhage, cerebral hemorrhage, subdural
scanning, lateral fontanel scanning, mastoid fontanel scanning, and hemorrhage, and subarachnoid hemorrhage. (1) Ultrasonic diagnosis
posterior fontanel scanning. Among them, the anterior fontanelle of periventricular intraventricular hemorrhage: In 1978, Papile
is the preferred inspection site (11, 12). During scanning, attention et al. (19) performed computed tomography on very low birth
should be paid to comparing the parenchymal structure and echo weight infants (VLBW). According to the amount of intraventricular
of the two cerebral hemispheres and observing the changes in hemorrhage, periventricular intraventricular hemorrhage is divided
the shape and position of the ventricle and midline. Scans of the into four levels. Grade I: bleeding is limited to the germinal base.
posterior fontanelle reveal brain structures close to the horizontal Ultrasonography showed a large amount of high echo in the anterior
position, which can be used to compensate for the lack of detection horn of the lateral ventricle in the coronal plane and caudate nucleus
of acoustic images of the bottom of the brain when scanning sulcus in the sagittal plane. Grade II: intraventricular hemorrhage
the anterior fontanelle. Transcranial fontanel scanning, which is occurred, but the ventricle was not dilated. Ultrasonographic
equivalent to observing a cross-sectional view of the brain from manifestations were lateral ventricle or choroid plexus patchy or
one side, is often used as an acoustic window for cerebrovascular massive high echo. Grade III: intraventricular hemorrhage with
hemodynamics. The mastoid fontanelle can be used to observe ventricular dilatation. Ultrasonography showed that the lateral
the posterior fossa. During the scan, attention should be paid to ventricle was partially or completely filled with a large amount of
the boundary between the cerebellar hemisphere, cerebellar vermis, hyperechoic blood and would expand. Grade IV: intraventricular
cortex and medulla, material echoes, and changes in the cerebellar hemorrhage with periventricular hemorrhagic cerebral infarction;
medullary cistern (13). ultrasonography revealed a sectorial or spherical hyperechoic zone
in the periventricular white matter. Figure 1 shows the ultrasound
images of periventricular intraventricular hemorrhage at all levels,
3.2. Time of cranial ultrasound examination and the hemorrhage is classified from left to right as grades I–IV
(20). (2) Ultrasound diagnosis of cerebral hemorrhage: In the early
Brain ultrasound is used to diagnose intracranial structures and stage of hemorrhage, there was a strong echo mass in the brain
lesions through the unclosed salt gate. After birth, the salt door will parenchyma with a clear boundary. With the development of the
gradually close, thus, it is necessary to complete the craniocerebral disease, the old hematoma gradually liquefied absorption, and
ultrasound examination within a specific time period (14–16). brain parenchyma has a weak echo or a small echo-free zone. (3)
Usually, the first cranial ultrasound examination is performed Ultrasound diagnosis of subdural hemorrhage: there is a prominent
within 3 days after birth, no later than 1 week. For infants crescent-shaped, narrow, strong echo between the skull and brain
with a history of hypoxia, asphyxia, and very low birth weight tissue. With the decrease in the amount of bleeding in the later

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Liu 10.3389/fneur.2023.1095280

FIGURE 1
Periventricular intraventricular hemorrhage (Papile classification) (20).

period, the echo will gradually change into a narrow silent space. (4)
Ultrasound diagnosis of subarachnoid hemorrhage usually occurs
at the edge of the brain. A large number of studies (21–23) have
shown that brain ultrasound is less sensitive to identify these areas
of bleeding, easy to missed diagnosis, which is the weak link of brain
ultrasound diagnosis.

4.2. Ultrasonographic diagnosis of

periventricular leukomalacia in premature
infants

Periventricular leukomalacia is a disease closely related to motor

function, audiovisual function, and cognitive function. It is the
most serious case of brain injury in premature infants and one
FIGURE 2
of the important causes of neonatal cerebral palsy (24). Li Jinhui Ultrasonography of periventricular leukomalacia in the same part of
et al. (25) showed that periventricular leukomalacia is related to the same child (20).
the following three interactive factors: (1) the development of
cerebral white matter vessels in premature infants is not perfect;
(2) immature cerebral blood flow autoregulation function; and
(3) white matter oligodendrocytes and their precursors are very
fragile; the smaller the gestational age, the higher the incidence distinguishing white matter echoes from those of normal preterm
of periventricular leukomalacia. Most premature infants with infants. In general, the echo of the former is rough and uneven,
periventricular leukomalacia have no obvious clinical symptoms, while the echo of the latter is thin and uniform without an obvious
and the diagnosis usually depends on an imaging examination. boundary. Grade II: strong echo around the ventricles gradually
Magnetic resonance imaging (MRI) is the best method to diagnose evolves into a local small cyst. The location and extent of cysts are
periventricular leukomalacia. However, MRI examination requires key to predicting the prognosis. According to the study of Gotardo
moving children, which takes a long time and has limited application et al. (30), cysts located around the central sulcus may lead to bilateral
value for critically ill children. A brain ultrasound examination spastic cerebral palsy, while cysts located in the frontal lobe are
can not only be completed at the bedside but also involve real- usually not related to cerebral palsy. Grade III: multiple cysts of the
time observation of the brain condition in order to facilitate forehead and occipital white matter. Grade IV: multiple subcortical
a timely understanding of the development of the disease. In cysts formed in the deep white matter hyperechoic area around the
recent years, with the rapid development of ultrasound equipment ventricle. Studies (31) have shown that periventricular leukomalacia
and technology, the accuracy, sensitivity, and specificity of brain occurs in children with a cyst formation time of 4 weeks after
ultrasound for periventricular leukomalacia reached 91, 100, and birth. When MRI is used at term, it usually shows that the lesion
33%, respectively (26), which has become the main means of has been absorbed. Therefore, in the diagnosis of periventricular
diagnosis of periventricular leukomalacia (27). leukomalacia, it is necessary to continuously use brain ultrasound
At present, according to different periods of periventricular scans to track and observe the changes in cysts within 4–6 weeks
leukomalacia ultrasound performance, it is generally divided into after birth. Figure 2 shows the sonogram of different degrees of
four levels (28). Grade I: bilateral periventricular white matter echo- periventricular leukomalacia in the same part of the same patient, in
transient enhancement (1, 29), duration of more than a week. This which the echo of bilateral occipital white matter in the left figure
is a reversible disease with an ideal prognosis. When diagnosing this was significantly enhanced; the right image shows multiple vesicles of
degree of periventricular leukomalacia, attention should be paid to different sizes (20).

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Liu 10.3389/fneur.2023.1095280

4.3. Ultrasonographic diagnosis of those of the control group, and the difference was P < 0.05.
hypoxic-ischemic encephalopathy in The follow-up study of Guan (36) and Liao Huifang (37) was
premature infants similar to theirs. It is suggested that color Doppler ultrasound
detection of neonatal hypoxic-ischemic encephalopathy can
Neonatal hypoxic-ischemic encephalopathy is hypoxic-ischemic effectively understand the changes in cerebral hemodynamics in
brain damage caused by perinatal hypoxia and asphyxia. It is children and has important reference significance for predicting
one of the most common brain injuries in premature infants and pre-evaluating the degree of brain injury in children. In the
and one of the leading causes of neonatal neurodevelopmental previous content, relevant studies have demonstrated the value of
abnormalities and death (32). According to the statistics of Cai craniocerebral ultrasound in the diagnosis of neonatal symptoms
Qing et al. (33), the incidence of neonatal hypoxic-ischemic (38, 39).
encephalopathy is 1/1,000–1/2,000 live full-term infants, of which
15–20% died in the neonatal period, 25–30% of survivors have
permanent neurological deficits, such as cerebral palsy and mental
5. Conclusion
disability. Early diagnosis and intervention are important ways
In conclusion, craniocerebral ultrasound, as a non-invasive,
to reduce brain injury and improve the prognosis for children.
cheap, simple, and bedside brain medical imaging method, can be
However, as early neonatal hypoxic ischemic encephalopathy
used to screen and diagnose intracranial lesions in infants who have
usually has no obvious clinical symptoms, imaging methods
not yet closed the halo. Especially in the diagnosis of brain injury
must rely on further examination and diagnosis. Craniocerebral
in premature infants, brain ultrasound shows good accuracy and
ultrasound can not only dynamically observe the two-dimensional
specificity, which can clearly show the condition of brain injury
structure of the brain but also provide help for the classification of
and the hemodynamic changes of diseased tissues. Therefore, as an
neonatal hypoxic-ischemic encephalopathy. It can also obtain
important screening project for brain injury in premature infants,
cerebral hemodynamic parameters through color Doppler
it is conducive to the early detection of intracranial lesions in
technology, providing a richer diagnostic basis for clinical
children and can provide an accurate basis for early clinical diagnosis
diagnosis. Compared with brain CT and MRI, brain ultrasound
and prognosis evaluation. In recent years, with the continuous
can detect abnormal changes in brain time, which is of great
improvement of brain ultrasound imaging, brain ultrasound has
significance for the early diagnosis and treatment of neonatal
become the preferred diagnosis of brain disease in premature infants.
hypoxic-ischemic encephalopathy.
The brain ultrasound diagnosis of hypoxic ischemic
encephalopathy is based on the pathological process of the
disease. In the early stages of the disease, the main pathological
Author contributions
change is brain edema. Ultrasound showed diffuse and uneven
The author confirms being the sole contributor of this work and
echo enhancement in both cerebral hemispheres, with the most
has approved it for publication.
obvious enhancement in the periventricular white matter, even
equal to the intensity of the choroid plexus. In the late stages of
the disease, cystic or atrophic changes occur in the brain structure, Funding
and the ultrasound images can be clearly seen after 3–4 weeks.
Cystic changes usually occur after extensive and severe brain The work was supported by Xianyang Science and Technology
edema. Ultrasound showed cysts of different sizes in the original Bureau key research and development program NO. 2021ZDYF-GY-
echo-enhanced area. Atrophic changes are secondary to extensive 0025.
brain injury. Ultrasound examination showed the extensive division
of the brain, deep sulci, widened extra-frontal space, and atrophy of
the gyrus (34). Conflict of interest
Pathological changes of neonatal hypoxic ischemic
encephalopathy are a dynamic evolution process, mainly based The author declares that the research was conducted in the
on cerebral blood. Blood flow changes can be used for diagnosis. absence of any commercial or financial relationships that could be
Color Doppler ultrasound can directly reflect the blood perfusion construed as a potential conflict of interest.
of lesions through the changes in the blood flow spectrum (35). By
comparing the cerebral blood flow of 38 neonates with hypoxic-
ischemic encephalopathy and 30 full-term healthy neonates, Yang Publisher’s note
Guanghui found that within 48 h after hemorrhage, the peak
systolic velocity (Vs), end diastolic velocity (Vd), resistance index All claims expressed in this article are solely those of the
(RI), and pulsatility index (PI) of children with mild hypoxic- authors and do not necessarily represent those of their affiliated
ischemic encephalopathy were close to those of the control group. organizations, or those of the publisher, the editors and the reviewers.
The Vs and Vd of children with moderate and severe hypoxic- Any product that may be evaluated in this article, or claim that may
ischemic encephalopathy were significantly lower than those of be made by its manufacturer, is not guaranteed or endorsed by the
the control group, while RI and PI were significantly higher than publisher.

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Liu 10.3389/fneur.2023.1095280

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