Introduction
Ultrasonography (USG) provides real-time bedside information with high-spatial and
temporal resolution by using a variety of techniques which include two-dimensional
(2D) imaging, Doppler and color-coded Doppler, and contrast-enhanced USG imaging.[1] Point-of-care ultrasound has become an indispensable tool which provides a valuable
supplement to clinical observations in the intensive care mode by the high acoustic
impedance of the skull, and is a cornerstone in the diagnostic assessment of patients
with vascular brain disease.[2] At present, the important uses of ultrasonography in neurologically injured patients
include assessment of changes in intracranial pressure (ICP), cerebral blood flow
(CBF) and velocities, diagnosis of intracranial mass lesions and midline shifts, and
pupillary examination. This narrative review aims to evaluate the available evidence
of utility of ultrasound from the specific point of view of neurocritical care. This
was performed by a search of available literature on Ovid, PubMed, Google Scholar
and Medline, with MeSH terms like “ultrasound in neurocritical care,” “transcranial
Doppler” and “optic nerve sheath diameter,” keeping the focus on review articles.
Neurological Applications and Modalities
The discussion of use of USG in neurocritical care needs special focus on its neurological
applications, as the general applications have already found widespread use and acceptance
in critical care units. The two main modalities available for neurocritical care are
B-mode transcranial color-coded duplex (TCCD) and transcranial Doppler (TCD) sonography,
apart from two-dimensional (2D) sonography.[3]
These modalities find an invaluable role in estimation of raised ICP, assessment of
pupillary size and reaction, assessment of brain parenchyma, and diagnosis of vascular
abnormalities in the neuro intensive care unit. Apart from these, it has a role in
the detection of cerebral circulatory arrest, which is otherwise a clinical diagnosis.
[Table 1] lists some of the conditions which can be detected or diagnosed using ultrasonography.
These applications are discussed in greater detail below, outlining the usefulness
as well as limitations.
Table 1
Common findings and pathologies in neurocritical care patients
|
Pathology/condition
|
Role of USG/TCD
|
|
Abbreviations: CCP, cerebral perfusion pressure; ICP, intracranial pressure; TCD,
transcranial Doppler; USG, ultrasonography.
|
|
Traumatic brain injury
|
Noninvasive estimation of ICP and CPP
Cerebral autoregulation
Compliance and cerebrovascular dynamics
Posttraumatic vasospasm detection
Evaluation of effect of therapeutic intervention
Assessment of pupils
|
|
Subarachnoid hemorrhage
|
Vasospasm
Autoregulation and cerebrovascular reactivity
Noninvasive estimation of ICP
Evaluation of effect of therapeutic intervention
|
|
Stroke
|
Diagnosis and treatment of ischemic stroke
Emboli monitoring
Cardiac evaluation: shunts
|
|
Brain tumors
|
Noninvasive intracranial pressure
Midline shift estimation
|
|
Brain death
|
Presence of reverberating flow, systolic spikes or the disappearance of previously
registered Doppler flow signals
In conjunction with clinical diagnosis
|
Assessment of Intracranial Pressure
Raised ICP is a condition which can have devastating consequences if not diagnosed
and managed early. ICP measurement can be performed by invasive as well as noninvasive
methods. CT scan remains a popular noninvasive diagnostic modality to confirm signs
of rise in ICP and determine the need for ICP monitoring. In comparison, ocular USG
to measure the optic nerve sheath diameter (ONSD) offers a bedside alternative, which
is simple, noninvasive and can provide quick and reliable information about ICP, especially
in a clinical emergency.[4]
The optic nerve is an extension of the central nervous system (CNS), enclosed by cerebral
spinal fluid (CSF) and the meninges, which are collectively known as the optic nerve
sheath. The optic nerve is more distensible near the eyeball, as it is only loosely
attached to the dural sheath here. Due to this direct communication between the subarachnoid
space and the optic nerve, the pressure changes in the brain are closely reflected
in the optic nerve and its sheath. This phenomenon has been demonstrated to occur
within minutes of acute changes in ICP, and thus the ONSD poses an attractive target
for noninvasive ICP monitoring.[5] Measurement of the ONSD can be carried out serially over a period of time, as it
is easily available and poses no radiation hazard, so any changes in the status and
response to treatment can also be noted.
The preferred probe to measure ONSD is a high frequency (5–10 MHz) linear probe, with
the depth setting adjusted to 5 to 6 cm.[6] The examination is performed in the supine position, with eyes closed, and midline
position of the eyes can be maintained in awake or cooperative patients. After applying
a generous amount of ultrasound gel over the closed eyelids, the transducer is placed
gently on the closed eye, and adjusted to obtain an image of the globe and the optic
nerve (
[Fig. 1]
). The ONSD is measured 3 mm posterior to the globe, with the normal value being 4.5
mm (
[Fig. 2]
). A value more than 5.0 mm is suggestive of an ICP > 20 mm Hg in ventilated patients.[7]
Fig. 1 Position of transducer for measurement of ONSD. OSND, optic nerve sheath diameter.
Fig. 2 Sonographic image of optic nerve and eyeball. For measurement of ONSD, a 3 mm line
(A–A) is drawn from junction of eyeball and optic nerve. At this point another line
is drawn perpendicular to the first line (B–B) to measure the ONSD. OSND, optic nerve
sheath diameter.
Care must be taken to avoid the use of ONSD in patients with orbital trauma, hematoma
and exophthalmos.[8] It may be erroneous in patients with optic neuritis, optic nerve atrophy and glaucoma,
and hence better avoided. It must also be noted that its use in the pediatric population
is limited, as the relationship between ONSD and raised ICP is dependent on establishing
and validating threshold values above which ICP is considered elevated. These values
have been less specifically established in children, due to more inter individual
variations.
It has been demonstrated that combining ONSD measurement with other ultrasound modalities,
like venous transcranial Doppler assessment of the straight sinus, may provide better
prognostic accuracy for the detection of intracranial hypertension.[9]
Pupillary Assessment
USG may be a useful tool in pupillary assessment in patients with grossly swollen
eyelids, trauma or soft tissue damage which prevents the eyelids from opening. The
simple evaluation of the consensual pupillary reflex can test the integrity of the
retina, optic nerve, part of the midbrain, and the oculomotor nerve. The technique
described by Sargsyan et al and can be performed by either superior or inferior approach.[10]
[11] The superior approach uses a high frequency (5–12 MHz) linear probe and the supine
patient is directed to gaze downward toward the feet. On the superior aspect of the
orbit, the probe is aligned with the plane of the iris to obtain the anechoic pupillary
image ([Figs. 3] and 4). The inferior approach differs in the placement of the probe on the lower
eyelid, with an upward tilt of the probe.[12]
Fig. 3 Position of transducer for assessment of pupillary reflex.
Fig. 4 B-mode image of ultrasonography showing image of pupil.
Another potential application for ocular ultrasound could be evaluation of the pupillary
light reflex in situations where direct observation of the pupil may be difficult
or impossible, such as ocular trauma. An oblique section of the globe is obtained
using the USG probe, and further tilting into a near- coronal plane allows the clinician
to visualize the iris and pupil. Once this view is obtained, consensual pupillary
light reflex may be evaluated by contralateral stimulation with light, using the M
mode to document pupillary motion. This response may also be charted against time,
allowing evaluation of finer details.
Insonation of Brain Parenchyma: Transcranial B-mode Imaging
Transcranial sonography (TCS) can be used to evaluate structural changes within the
brain, which allows the identification of several structures within the brain parenchyma.
The first step while performing TCS is to accurately identify the mesencephalic brain
stem. This is done by placing the phased array probe over the temporal bone window,
which is parallel the orbitomeatal line. In this view, a hypoechoic butterfly-shaped
structure corresponds to an axial section through the midbrain. Tilting the probe
10 to 20 degrees upward enables visualization of the ventricular plane. The landmark
for orientation in this plane is the pineal gland, which is strongly hyperechoic due
to calcification. The pineal gland is located adjacent to the posterior border of
the third ventricle.
TCS can be used to detect as well as estimate midline shift in the cerebral parenchyma.
Two techniques have been described by Seidel at al[13] and Caricato et al.[14] The former involves the identification of the third ventricle as a marker for the
brain midline, followed by measuring the distance between the external side of the
temporal bone and the third ventricle, repeating the same process on the other side.[13] The midline shift can be estimated by obtaining the difference between these two
measurements and halving it. This technique has been found to have a good correlation
with values derived from CT.[15] However, the accuracy of this technique is limited in patients with decompressive
craniectomy.
The technique described by Caricato et al uses a curvilinear probe in the axial plane.[14] The boundary between the two lateral ventricles is identified as the midline, followed
by the falx cerebri from frontal to occipital area (
[Fig. 5]
). The distance between these two landmarks can give an estimate of the midline shift
(MLS).
Fig. 5 Ultrasound image showing the interventricular line and falx cerebri.
Ultrasound assessment of MLS, correlating well with findings on CT, is an early outcome
predictor in acute stroke patients.[16] An excellent correlation has also been observed between TCS and CT measurements
of the width of the third ventricle and the lateral ventricles, and therefore early
detection of development of hydrocephalus.[13] Ventricular width monitoring with TCS may, in selected patients and in the hands
of an experienced operator, also be useful to visualize the position of the external
ventricular drain tip, especially in patients who have had a decompressive craniectomy.[17]
The main limiting factor for 2D USG imaging of the brain in adults is dependent on
frequently inadequate acoustic windows. However, in patients with skull defects, for
example with decompressive craniectomy, valuable information may be obtained about
the position of the ventricular catheter, hydrocephalus and other postoperative complications
like hemorrhagic lesions.[18] An acoustic window can also be used as a guide for insertion or repositioning of
ventricular catheter during ventriculostomy.[19]
[20] Its use has been shown to help reduce multiple attempts and confirm correct placement,
especially in patients with distorted anatomy. It has also been reported to be used
to monitor intracranial bleeding and brain tumors with edema in selected patients.
Research has also shown that TCS may have a role in the identification of conditions
such as idiopathic Parkinson’s disease, wherein patients with Parkinson’s demonstrated
an enlargement of the Substantia Nigra echogenic signal.
Role of TCD: Diagnosis of Cerebral Vascular Abnormalities
The detection and diagnosis of cerebral vascular abnormalities rely largely on the
specific modality of transcranial Doppler (TCD). A detailed discussion which is beyond
the scope of this review is not possible, but the relevant applications are discussed
briefly. TCD is based on the Doppler effect, and the common insonation windows used
along with their applications are summarized in [Table 2].
Table 2
Acoustic windows used for TCD examination
|
Name of acoustic window
|
Applications/Uses
|
Limitations
|
|
Transtemporal
|
Thin portion of temporal bone
|
Unsuitable in 10% patients due to thick bone or osteoporosis
|
|
Abbreviations: ACA, anterior cerebral artery; BA, basilar artery; ICA, internal carotid
artery; MCA, median cerebral artery; PCA, posterior cerebral artery; TCD, transcranial
Doppler; VA, vertebral artery.
|
|
Between external canthus of eye and external acoustic meatus
|
|
|
Most frequently used
|
|
|
Proximal segment of MCA, ACA, PCA, and final segment of ICA
|
|
|
Transorbital
|
Ophthalmic artery, carotid siphon and contralateral MCA
|
Avoided in patients with recent artificial lens placement
|
|
Probe on closed eyelid
|
|
|
Doppler power must be reduced by 20%
|
|
|
Suboccipital
|
Posteriorly, highest point of the neck
|
Inadequate in 9% of patients
|
|
Suboccipital and intracranial portion of both VA and BA
|
|
|
Retromandibular
|
Extracranial approach to assess distal segment of extracranial ICA
|
|
|
Probe at angle of mandible
|
|
Using the TCD to study cerebrovascular dynamics can facilitate clinical management
of conditions such as neurocritical care pathologies, including traumatic brain injury
(TBI), aneurysmal subarachnoid hemorrhage, intracranial arterial stenosis, acute ischemic
stroke, and sickle cell disease,[9] leading to its designation as “stethoscope for the brain.”[21]
Among the several components of the waveform derived from TCD, diastolic flow velocity
has now emerged as a clinically relevant parameter, as changes in cerebral perfusion
pressure with systemic blood pressure are well-documented.[22] Simultaneous monitoring with ICP and arterial blood pressure (ABP) can provide a
valuable perspective in various intracranial pathologies.[23] The use of TCD in patients with cerebrovascular compromise is gaining popularity,
especially for the assessment of ICP and cerebral perfusion pressure (CPP), as well
as detection of impairment of cerebral autoregulation.[24]
[25] Assessment of autoregulatory capacity of the injured brain may permit more optimal
blood pressure management in an individualized manner.
Detection of Cerebral Circulatory Arrest: TCD
TCD has a role in the detection of cerebral circulatory arrest, whereas the diagnosis
of brain death is primarily clinical. The main pathophysiology underlying brain death
is raised ICP and a loss in cerebral autoregulation, which affects cerebral blood
flow, leading to cerebral circulatory arrest. TCD criteria for the diagnosis of cerebral
circulatory arrest include the presence of reverberating flow patterns, systolic spikes,
or the disappearance of previously registered Doppler flow signals.[26] It is desirable to record these patterns in both the anterior circulation (middle
cerebral artery) and posterior circulation (basilar artery and intracranial vertebral
arteries) to confirm the diagnosis. If two separate readings taken 30 minutes apart
show these patterns, then circulatory arrest can be confirmed as irreversible.[27]
This technique does have some limitations. In patients with subarachnoid hemorrhage,
sudden changes in ICP and resulting cardiac arrest can lead to a false positive diagnosis,
while it may be missed in patients with fractures, decompressive craniectomy and ventriculostomy.[28] To avoid false-positive results of cerebral circulatory arrest, it is recommended
that patient must be hemodynamically stable and conditions like hypoxemia, hypercarbia,
hypothermia or metabolic derangements must be corrected.[28]
Applications in Pediatric Neurocritical Care
In neonates and infants, due to the presence of open fontanelles, 2D brain USG is
useful to diagnose intracranial malignancies and congenital malformations. In preterm
infants, cerebral hemorrhage and its different patterns (intraventricular hemorrhage
and periventricular hemorrhagic infarction) can also be detected.[29] Hydrocephalus is commonly diagnosed using USG, which can also be used for guided
ventricular catheter placement. The role of ONSD in pediatric population has been
discussed earlier in the text.
Systemic Applications
USG is useful to detect underlying cardiac conditions which may or may not be related
to the neurological pathology. It is useful in the detection of atrial septal defects
and patent foramen ovale, which can result in paradoxical embolism through right to
left cardiopulmonary shunts, and in stroke patients presenting with acute ischemic
stroke.[30] Evaluation for right to left shunts can be done by injecting agitated saline into
a peripheral vein, and visualizing the microembolic signals observed on the TCD. USG
evaluation of cardiac anatomy and function to guide fluid management and vasoactive
drug infusion, as a part of a ‘goal-directed’ systemic and cerebral hemodynamic management
protocol, can help reduce mortality and improve outcomes in neurocritical care patients.[31] Acute ventricular dysfunction is a common finding after subarachnoid hemorrhage,
which can be detected on echocardiography and managed actively, to prevent further
cerebral ischemia.[32] USG can also be used to detect Takutsubo cardiomyopathy, which is not uncommon in
patients in neurointensive units.[33] It is critical to diagnose this condition early on, as the usual treatment of hypotension
with vasopressors, can result in worsening of the condition. [Table 3] lists some other common cardiac indications for ultrasound in neurocritical care
unit.
Table 3
Cardiac ultrasound evaluation in neurocritical patients
|
Cardiopulmonary shunts: Atrial septal defect/patent foramen ovale
|
|
Ventricular function: Global and focal
|
|
Pericardial effusion and tamponade
|
|
Thrombus and emboli (infective endocarditis)
|
|
Evaluation of hypotension: volume status
|
|
New onset arrhythmias
|
|
Cardiomyopathy, especially Takutsubo
|
The role of USG in trauma patients has been well-established for several years now.
Various protocols in eFAST (extended focused assessment with sonography) can help
detect pneumothorax and bleeding in the pericardial, thoracic as well as peritoneal
cavity. Any initial findings in the emergency room can be followed up in the critical
care unit to assess need for intervention. USG can also be used as a guide to insert
drains as catheters, using the Seldinger technique, thereby improving the safety of
these procedures.
Point-of-care ultrasound in the neurocritical care enables the diagnosis of conditions
like pleural effusion, pneumothorax, lung consolidation, pulmonary abscess, interstitial–alveolar
syndrome, and lung recruitment/derecruitment. It offers an easy alternative to bed
side radiology, being available and repeated evaluation being feasible. It also has
the advantage of being able to detect smaller amounts of fluid when compared with
a chest X-ray.[34]
The use of the BLUE and FALLS protocols in critical care is a testament to the true
versatility and usefulness of USG.[35] While the BLUE protocol uses profiles for the respiratory diseases like pneumonia,
congestive heart failure, chronic obstructive pulmonary disease (COPD), asthma, pulmonary
embolism, pneumothorax with an accuracy > 90%, the FALLS-protocol, puts to use the
change from A-lines to lung rockets, providing a direct biomarker of clinical volume.
Its key use lies in ruling out obstructive, then cardiogenic and finally hypovolemic
shock, any of which can be an accompaniment in a neurocritical patient.
Ultrasound plays an invaluable role in several procedures among critical care patients.
In neurocritical care patients, vascular USG imaging has three especially relevant
indications: screening for atherosclerotic plaques and flow characteristics in the
aortic root and extracranial supra-aortic arteries; early diagnosis of deep vein thrombosis
in the lower limbs; and guiding central venous catheterization to minimize the risk
of procedure-related complications.[36] The use of tracheal USG imaging before percutaneous tracheostomy effectively reduces
anatomical complications, including the risk of bleeding from pretracheal vascular
structures. It also contributes to decreasing the risk of puncture above the first
tracheal ring, injury to surrounding structures including the posterior tracheal wall,
and cranial misplacement of the tracheostomy.
