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Analytic Review

Journal of Intensive Care Medicine


1-8
Clinical Applications of Ultrasonography in ª The Author(s) 2020
Article reuse guidelines:
sagepub.com/journals-permissions
Neurocritically Ill Patients DOI: 10.1177/0885066620905796
journals.sagepub.com/home/jic

Andrés Fabricio Caballero-Lozada, MD1 , Kapil Laxman Nanwani, MD2,


Favio Pavón, MD1, Andrés Zorrilla-Vaca, MD1 , and Carolina Zorrilla-Vaca, MD1

Abstract
Ultrasonography is part of the multimodal monitoring of the neurocritical patient. Through transcranial color Doppler ultra-
sound, carotid-color Doppler ultrasound, and ocular ultrasound it is possible to diagnose and monitor a multitude of pathological
conditions, such as cerebrovascular events, vasospasm, Terson syndrome, carotid atheromatosis, and brain death. Furthermore,
these techniques enable the monitoring of the intracranial pressure, the cerebral perfusion pressure, and the midline deviation,
which allows us to understand the patient’s neurocritical pathology at their bedside, in a noninvasive way. Although none of these
tools have yet been shown to improve patient prognosis, the dissemination of knowledge and management of neurovascular
ultrasonography could significantly improve the comprehensive management of neurocritical patients.

Keywords
Doppler, critical care, ultrasonography, neurology

Introduction future,” through it, we would learn to “auscultate the brain.”5


In the present review, the concepts and applications of ultra-
Since time immemorial, neurocritical patients have aroused sci-
sonography in the neurocritical patient are examined.
entific interest due to their complex semiology, morbidity, and
mortality. Evidence of this interest can be found from the archae-
ological remains of trepanations practiced in the Greek Bronze Transcranial Color Doppler Ultrasound
Age (1900-1600 BC) and the pre-Columbian era.1 However, it is
The performance of TCD Ultrasound requires a low frequency
only in the last century that we have experienced important
transducer (1.75-3.5 MHz), the convex probe being generally the
developments in the knowledge and management of the neuro-
most useful in this context. The most commonly used ultrasound
critical patient, with multimodal neurological monitoring tech-
windows are the transtemporal (in the region before the tragus of
niques, which range from anatomy to specific metabolic
the ear and above the zygomatic arch on the pterion), the sub-
alterations: computerized axial tomography, magnetic resonance
occipital or transforaminal (in the midline below the occipital
imaging, ultrasonography, monitoring of intracranial pressure
scale and on the transverse process of the cervical vertebra with
(ICP), oximetry in the jugular bulb, tissue oxygen pressure, cer-
semi flexed or cocked head) and orbital (through eyeball).6
ebral microdialysis, and electroencephalography.2,3 Despite In order to perform this ultrasound, it is also necessary to
advances and combinations of techniques, few measures have know the anatomy of the circle of Willis (Figure 1) and the
actually been shown to improve the prognosis of these patients, main cerebral arteries. The circle of Willis is a vascular ring
which implies in some way that neurocritical pathology remains that results from the union of branches of the internal carotid
a mystery, and in medicine, every mystery is a challenge. arteries (ICAs) and the basilar artery (BA) which in turn is
Unlike other multimodal neurological monitoring measures,
ultrasonography allows the noninvasive diagnosis and monitor-
ing of these patients at their bedside, without irradiation. In 1
Department of Anaesthesiology, Universidad del Valle, Cali, Colombia
2
addition to the many other advantages of ultrasonography in Department of Intensive Medicine, University Hospital La Paz-Cantoblanco-
the critical patient, it is widely available and relatively low Carlos III, Madrid, Spain

cost. All this makes it a “Point-Of-Care” tool for the attending Received September 15, 2019. Received revised January 20, 2020.
physician, who through transcranial color Doppler (TCD) Accepted January 22, 2020.
ultrasound, carotid-color Doppler ultrasound, and ocular ultra-
Corresponding Author:
sound (OU) would be able to identify deviations of the cerebral Andrés Fabricio Caballero-Lozada, Department of Anaesthesiology,
midline, echographic signs of vasospasm, among others.4 In Universidad del Valle, Street 4b 36-00, Cali, 76001, Colombia.
short, if ultrasound is considered the “stethoscope of the Email: andres.caballero@correounivalle.edu.co
2 Journal of Intensive Care Medicine XX(X)

considered. It is necessary to remember that the cerebral circu-


lation has a low cerebral vascular resistance (CVR) so the
diastolic flow will be determinant, and therefore, in comparison
with the rest of arteries of the organism, the diastolic flow
velocities (DV) will be higher, and the difference between the
peak systolic velocity (SV) and DV will be smaller.8 As for the
other parameters, they are explained below.
The transtemporal window allows the evaluation of ACAs,
MCAs, and PCAs. The patient is placed in the supine position
with a cephalic inclination of 15 to 30 , orienting the transdu-
cer toward the tip of the patient’s nose (in such a way that in the
image, the anterior side is shown on the left side of the screen).
The first thing to identify is a semicircular hyperechoic line that
corresponds to the contralateral skull, since it allows adjust-
ment of image depth. With the transducer perpendicular to the
bone, a double hypoechoic structure in the form of a butterfly
corresponding to the mesencephalon should be identified. In
front of it, is the sella turcica and the temporal bone, a region in
which it is possible to locate the circle of Willis by applying the
color Doppler.
Below the temporal bone is the internal carotid artery (ACI)
in its portion of the carotid siphon along with the MCA. Ante-
rior to the MCA and going to the frontal lobe is the ACA, and
after the MCA embracing the mesencephalon toward the pos-
terior region, the PCA is found. By tilting the transducer 10
toward cephalic, it is possible to identify 2 hyperechoic lines
which correspond to the midline in the area of the diencepha-
lon, and if we continue tilting toward cephalic, we will identify
the lateral ventricles and the thalamus.6,8,9
Figure 1. Vascular anatomy of the circle of Willis.
It is important to bear in mind that with the transtemporal
window, the circle of Willis is accessed from the side, therefore
the ultrasound image will not be the same as that of the computed
formed by the union of the 2 vertebral arteries (VAs). In the tomography (CT), but will be rotated 90 . This is important since
anterior region and originating in the ICAs, there are the ante- the Doppler-color allows determination of the flow direction, in
rior cerebral arteries (ACAs), united by the anterior commu- such a way that, depending on the configuration of the ultrasound
nicating artery (ACoA). In the middle region and originating in equipment, it is possible to identify by means of a color system,
the ICAs, there are the middle cerebral arteries (MCAs) with whether the blood vessel approaches or moves away from the
their more horizontal proximal trajectory (M1), and their distal transducer. In addition, it is important to identify the middle line
and more tortuous path which is introduced by the Silvio sulcus so as not to be confused with the vessels on the opposite side to the
(M2). Finally, in the posterior region and originating in the BA, one being studied, since they will present opposite flow direc-
the posterior cerebral arteries (PCAs) are found with their pre- tions. In that order of ideas, the artery closest to the insonated zone
communicating (P1) and postcommunicating (P2), in reference would be the MCA that is characterized by approaching the trans-
to the posterior communicating arteries (PCoAs), which join ducer (30-55 mm, MFV: 55-80 cm/s), while both the ACA and the
the ICAs with the PCAs, and in this way form a 7-sided poly- PCA would be found deeper (60-80 mm). The ACA is character-
gon. It is important to note that P1 and P2 exhibit different ized by moving away from the transducer in the anterior region
directions, since P1 initially goes to the middle region and then (MFV: 50-60 cm/s) while the PCA in its P1 portion approaches
in portion P2 it rotates and changes course toward the posterior the transducer, and in its P2 portion it moves away from the
zone. The ophthalmic artery, on the other hand, is a direct transducer (MFV: 42-53 cm/s).6,8,9 Figure 2 shows the increased
branch of the ICA and is directed toward the eyeball. This peak velocity in temporoparietal windows.
complex structure that surrounds the sella turcica protects the The suboccipital or transforaminal window allows the
brain from ischemic events since it can reverse the direction visualization of both VAs that come together to form the
and increase the flow of certain arteries, in order to replace a basilar. Since it is insonated in the cephalic direction and the 3
perfusion defect.7 mentioned arteries are directed toward the foramen magnum,
When identifying the cerebral arteries, the characteristics of both the VA (55 mm, MFV: 33-44 cm/s) and the BA (60-80
the cerebral circulation, the ultrasound window, its depth, the mm, MFV: 35-50 cm/s) will move away from the transducer,
direction of flow, and its mean flow velocity (MFV) must be with the VA being closest to it (see Figure 3). Finally, the
Caballero-Lozada et al 3

Figure 2. Transducer orientation in temporal window (A) showing the blood flow velocity chart (B) in transcranial Doppler ultrasound of the
middle cerebral artery (C).

Figure 3. Transducer orientation in suboccipital window (A) suboccipital approach of ultrasound measuring the blood flow velocity of basilar
artery (B and C).

ophthalmic window would allow identification of the ophthal- Carotid Color Doppler Ultrasound
mic artery (40 mm, MFV: 20-30 cm/s and morphology of the The performance of Carotid Color Doppler Ultrasound
peripheral artery), and the internal carotid at the height of the (CCD Ultrasound) requires a high frequency linear transducer
carotid siphon (60-80 mm), both going toward the transducer (10-12 MHz) that is placed in the lateral cervical region to
6,8,9
(Figure 4). identify the common carotid artery (CCA) and its posterior
4 Journal of Intensive Care Medicine XX(X)

Figure 4. Transducer orientation in ophthalmic window (A) ocular ultrasonography estimating the measurements of the ophthalmic artery (B
and C).

bifurcation in the external carotid artery (ECA) and the ICA. In is drawn perpendicular to the vitreoretinal junction and from
the longitudinal plane, it is possible to evaluate the existence of there the diameter of the optic nerve sheath (ONSD) is mea-
atheromatous plaques, and whether or not they produce signif- sured (reported as being pathological from 5-5.9 mm15), along
icant stenosis as a function of flow velocities by means of with the ONSD. In addition, this technique allows the evalua-
Doppler.10,11 Likewise, the measurement of the thickness of tion of pupillary reflexes, as well as an examination of the
the intima-media of the CCA could be performed on its poster- integrity of the retina and vitreous humor to rule out Terson
ior wall at 1 cm from the bulb, since it constitutes an indepen- syndrome, which consists of the presence of a vitreous hemor-
dent factor of coronary risk, its normal value being less than 0.9 rhage associated with a subarachnoid hemorrhage (SAH) that
mm.12 Finally, the ECA differs from the ICA since it is directed could cause blindness if left untreated. The presence of vitreous
toward the jaw, because it has an increased systolic and a lower hemorrhages generates suspicion of this entity, so a regulated
diastolic peak velocity (unlike the ICA which behaves like a assessment by ophthalmology must be requested.16,17
cerebral artery), and responds to the “tapping,” which consists
in percussing the temporal artery (branch of the ECA) and
objectifying the percussion transmitted in the ECA.10,11 The Clinical Applications of Ultrasonography in
measurement of the average speed of the ICA makes it possible the Neurocritical Patient
to calculate the Lindegaard index (LI), as will be seen later.13
In Figure 5, measurement of flow at the level of the carotid and Cerebral Vascular Pathology
measurement of the intima are shown. As a first step, it should be remembered that the Doppler func-
tion does not measure flow but flow velocities in cm/s, the use of
the average velocities of the cerebral arteries being standardized
Ocular Ultrasound to detect vascular pathology. Indirectly, brain perfusion pressure
Ocular Ultrasound is performed with a high-frequency linear (BPP) could be estimated using mean arterial pressure (MAP)
transducer (10-12 MHz) that is placed with abundant ultra- using the formula BPP ¼ (MAP  DV/MFV) þ 14.18 In the
sound gel on the closed eye to visualize the optic nerve and presence of a cerebrovascular event due to an intracranial ste-
determine the existence of papillary edema, which has been nosis or an embolism, very high intrastent velocities would be
associated with the presence of ICP.14 To do this, a 3-mm line observed (SV > 120 cm/s or MFV > 75 cm/s), while the pre and
Caballero-Lozada et al 5

Figure 5. Longitudinal plane in cervical window showing the common carotid artery, the thickness of its intima-media and its normal blood flow
velocity (A and B).

poststent velocities would both decrease with asymmetry makes the combination of TCD ultrasound and CCD ultra-
between the right and left sides, and differences of SV >20% sound necessary. In the case of the MCA, a high MVF (and
between the healthy side and the affected side. In addition, as especially an MVF > 180 cm/s) should generate suspicion of
previously explained, changes are observed in other vascular the presence of vasospasm, making it necessary to calculate the
territories. For example, in the case of an MCA obstruction, the LI dividing the MVF of the MCA between the MVF of the
MFV of the contralateral ACA, as well as the ipsilateral PCA ipsilateral ICA. An increase in velocities by itself can indicate
and PCoA would be elevated, with inversion of the ipsilateral in a practical way hyperemia or vasospasm/stenosis, which is
ACA. It is possible to classify these alterations according to the why the MVF of the MCA is compared to the MVF in the ICA,
thrombolysis in brain ischemia (TIBI) scale or the consensus on to discern between both entities.
grading intracranial flow obstruction (COGIF) scale, which will In the event that both MFVs increase in parallel, the LI would
serve to assess the direct recanalization during fibrinolysis.19-21 remain below 3, indicating a situation of hyperemia, where both
In the presence of a carotid obstruction due to an atheroma- MFVs are elevated or normal. Conversely, an elevation of the
tous plaque or trauma, a decrease in the speed of the ipsilateral MFV of the MCA that is not accompanied by an increase in
MCA, an inversion of the flow of the ipsilateral ACA, an the MFV of the ICA would imply an LI > 3 which would suggest
inversion of the flow of the ipsilateral ophthalmic artery, and the presence of vasospasm and would allow it to be classified as
a flow through the ACoA should be observed toward the mild, moderate, severe, or critical depending on the MFV of the
injured side, and a generalized increase in speeds on the con- MCA and the LI. With the BA, the calculations are similar
tralateral side.21 Given these findings, CCD ultrasound would except that in this case, the MFV of the BA4,23,24 would be used.
be performed to confirm the existence of a carotid obstruction
that would be classified according to the percentage of obstruc-
tion consistent to the velocity of the obstruction.21,22 Structural Brain Pathology
Another frequent entity in the neurocritical patient is the In terms of cerebral and systemic structural pathology, the Gosl-
vasospasm. Although the physiopathological mechanism is ing pulsatility index (PI) and the Pourcelot resistance index (RI)
unknown, it is more frequent in patients who have a SAH, due calculated by Doppler should be considered. The PI is calculated
to either a spontaneous or traumatic aneurysm. It is a vasocon- as (SV-DV)/MFV, with the normal range between 0.85 and 1.1.
striction of a brain territory that can lead to ischemia of this The PI indirectly shows the cerebral vascular resistance, indicat-
region in a secondary way, and its presence worsens the prog- ing the maximum variability of the flow in the cardiac cycle and
nosis in these patients, given that its management is also not the cerebral receptivity to the blood bolus, in such a way that it is
clear. Because the presentation time from the neurovascular proportional (though not linearly) to the compliance of the cere-
event is variable, the patient should be scanned ultrasonogra- bral vascular tissue, heart rate, and CVR. Furthermore, the RI is
phically in a serial manner in order to be able to identify it, calculated as (SV-DV)/SV, with the normal range between 0.42
especially in the first 3 weeks following the event. For the and 0.62. The RI allows estimation of the resistance of the
diagnosis of vasospasm, the MFV of the MCA or the BA and circulatory system to the flow.
the Lindegaard index should be considered, and can be done on Both parameters will be elevated before ICP, with
the MCA or on the BA by comparing the average speeds of decreased BPP, hypocapnia, hypothermia, brain death, hyper-
these with the MFV of the internal carotid artery (ICA) (which viscosity syndrome, intracranial occlusion, and advanced age
is calculated similarly to the MAP as 1/3SV þ 2/3DV). This (arteriosclerosis). Conversely, both parameters decrease in
6 Journal of Intensive Care Medicine XX(X)

situations of hyperemia, hypertension, hypercapnia, vasos- As any diagnostic technique, the transcranial ultrasonography
pasm, intracranial stenosis, arteriovenous malformation, and in critical patients has its limitations which can be diminished
rewarming due to cardiorespiratory arrest. These parameters with an adequate physics-based understanding of the technique
are important for differentiating cerebral vascular pathology and an adequate training curve for the hands-on component. The
from cerebral and systemic structural pathology, for example, technique is operator-dependent, that is why it is important the
a patient with ICP secondary to a brain space-occupying correct data analysis, the sufficient time for the study, and the
lesion (SOL) will have a decreased MFV with a high PI, since expertise of the operator. In many occasions, the windows are
it produces an increase in CVR due to the ICP and extrinsic not adequate due to individual features of the bone; in general,
compression of the vascular system. Instead, a patient with an the percentage of this situation is around 5% to 15% of the
intracranial stenosis will present decreased MFV with a low patients. In women older than 60 years, the window is difficult
(IP) in the poststenotic area, given that the CVR is lower in for the study, especially the temporal window. Given this cir-
this zone.4-6 The relationship between the PI and the ICP has cumstance, it is necessary to analyze other possibilities such as
been studied, establishing a relationship between both in such the orbital window or the occipital window among others. In
a way that ICP ¼10.93  PI  1.28 (E92%; S89%), that is, an most cases, the individual anatomic variations of the patient,
PI >13 correlates with a ICP >22 mm Hg.4 Additionally, there of the Circle of Willis, may cause errors of inexpert people such
are studies that suggest using TCD ultrasound for the moni- as the wrong identification of the vessel and a mistaken inter-
toring of BPP and CVR in the septic patient to individualize pretation of the fluxes analysis. The interferences with other
hemodynamic goals.25 electronic devices are minimum.28-32
The TCD ultrasound also allows the monitoring of intracra-
nial lesions and cerebral SOLs without the need to perform
Conclusions
serial CT scans, substantially improving the quality of the
image if the patient has undergone a craniectomy. It makes it Ultrasound in the neurocritical patient allows, through TCD
possible to evaluate the dimension of the lesion and if it pro- ultrasound, carotid-color Doppler ultrasound, and OU, the
duces mass effect, the deviation of the midline and the presence diagnosis and monitoring of multiple pathological conditions,
of subfacial herniation. To measure the volume of the lesion, both neurological and non-neurological. The knowledge of
the height, width, and length of the lesion would be multiplied both vascular and structural brain pathology is part of the multi-
and the result would be divided by 2. To measure the deviation modal monitoring of the neurocritical patient, and although it
of the midline, the transtemporal window is accessed to iden- has not been shown to improve the prognosis of these patients,
tify the double hyperechoic line ahead of the mesencephalon it has allowed for a better understanding of this pathology,
corresponding to the third ventricle, comparing the measure- therefore further studies are needed to demonstrate the benefits
ments from the beginning of the insonated region and from the of ultrasonography in this context.
midline to the contralateral cranium (which should correspond
to half of the previously performed measurement), thus permit- Authors’ Note
ting determination of whether or not there is a deviation from All authors contributed to the study conception and design. Material
the midline and enabling its quantification.4,6 preparation, data collection and analysis were performed by Andrés
Furthermore, TCD ultrasound identifies inappropriate flows Fabricio Caballero-Lozada, Kapil Laxman Nanwani, Favio Pavón,
Andrés Zorrilla-Vaca, and Carolina Zorrilla-Vaca. The first draft of the
related to “encephalic death.” The progressive decrease of the
manuscript was written by Andrés Fabricio Caballero-Lozada and
BPP, either in relation to a decrease in the MAP or an increase in
Andrés Zorrilla-Vaca, and all authors commented on previous versions
the ICP, generates cerebral flow waves that will be distinguished of the manuscript. All authors read and approved the final manuscript.
from the normal pattern, since they will gradually present a
decrease in the DV until they are reversed, and disappear pro- Acknowledgments
ducing a separation between systole and diastole with a rever- The authors would like to thank to all the members of the Anaesthe-
berant flow, isolated systolic spikes and finally absence of siology and Resuscitation research group of Universidad del Valle.
cerebral flow. The PI begins to rise progressively and in parallel
with the evolution of the waves previously described.21,26 Declaration of Conflicting Interests
In short, ultrasonography in neurocritical patients allows the The author(s) declared no potential conflicts of interest with respect to
physician to monitor ICP and BPP, to assess self-regulation, the research, authorship, and/or publication of this article.
detect vasospasm, vascular stenosis and occlusions, as well as
recanalizations, thereby facilitating the diagnosis of brain death, Funding
the detection of shunts, cardiac events, cerebrovascular events in The author(s) received no financial support for the research, author-
patients with sickle cell anemia, to assess hydrocephalus and ship, and/or publication of this article.
ICP, among other things. However, all these applications cur-
rently present relatively low evidence compared to the reference ORCID iD
techniques (except for sickle cell anemia in pediatric age), which Andrés Fabricio Caballero-Lozada, MD https://orcid.org/0000-
invites us to continue working on the dissemination and knowl- 0002-4161-4805
edge of ultrasonography in the neurocritical patient.5,27 Andrés Zorrilla-Vaca, MD https://orcid.org/0000-0001-8140-8486
Caballero-Lozada et al 7

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