Utility of the Color-Coded Duplex Neurosonographic Spectrum in Critically Ill Children in Resource-Limited Centers: A Case Series

Ultrasound in pediatric neurocritical care has a wide variety of indications, such as the study of vasospasm in subarachnoid hemorrhage, ow changes in intracranial stenosis, endocranial hypertension and to evaluate some therapeutic measures. The following is a series of ve most relevant cases collected from Pediatric Intensive Care with abnormal images in transcranial duplex (TCD) and their typical ndings in this type of studies. Transcranial duplex offers a diagnostic method of rapid evaluation that provides reliable information for decision making in pediatric intensive care, but it is a tool with which there is little experience in the country, so these ndings are didactic and should be complemented with studies of greater diagnostic relevance. on hospital admission shows laminar epidural hematoma in the right frontal region with small hemorrhagic contusions in the frontal region and global edema. Intracranial pressure sensor registers ICP < 20 mmhg.


Introduction
Since 1975 thanks to the work of Fritz Thurstone and David Phillips from Duke University, the re ned and real-time version of Doppler with a two-dimensional ultrasound image called Duplex Doppler was given [1].
Brain injuries and other neurological conditions are frequently encountered in pediatric intensive care units (PICUs) and are the most common proximate causes of death in children admitted to these units, in which severe encephalocranial trauma is prevalent.
Transcranial color-coded duplex sonography (TCCS), unlike conventional transcranial Doppler (TCD) sonography, allows the sonographer to delineate intracranial bony and parenchymal structures, visualize the basal cerebral arteries in color, and measure angle-corrected blood, ow velocities at a speci c site in the artery in question. This makes ow velocity measurements more valid than those obtained with conventional TCD [2]. Transcranial color-coded ultrasound (TCCS) allows bedside evaluation of these patients; it is a noninvasive and readily available technique for real-time assessment and monitoring of cerebral blood ow. The following therapeutic interventions are reported as hemodynamic optimization ( uid resuscitation or vasopressor/inotropic administration), de-escalation (discontinuation or dose reduction) of neurological pharmacological treatments such as osmotherapy agents, sedatives and neuromuscular blocking agents, and escalation (initiation, addition, or intensi cation) of the afore mentioned neurological pharmacological treatments [3].

Clinical Case Presentation
We report 5 cases of usefulness and teaching with color-coded ultrasound in pediatric critical units, which would help us guide diagnostic and therapeutic management in centers that do not have high-resolution imaging equipment and neurosurgical interventionism, and the decision to be referred to centers of greater complexity. Case 1 7-year-old schoolboy suffers fall from 2-meter height. Admitted to our institution with neurological deterioration with Glasgow scale 9 on admission, neuroprotection is provided due to severe encephalic trauma, After 24 hours brain tomography showed infarction in the entire region of the right middle cerebral artery with a small intraparenchymal hematoma with signs of endocranial hypertension, then subjected to right decompressive craniectomy and hard plasty with placement of left intraparenchymal pressure sensor, no pulse waves were visualized. After 36 hours postoperatively, anisocoria was evidenced due to third cranial nerve lesion, endovascular therapy was not performed and he did not receive anticoagulation due to hematoma. Transcranial color-coded duplex (TCCS) was performed and no ow was found in the right middle cerebral artery compatible with probable thrombosis of the right middle cerebral artery with decreased average velocities and high pulsatility indices in the left middle cerebral artery and basilar artery compatible with hypoperfusion due to high progressive cerebrovascular resistance, He was induced to barbiturate coma and monitored with TCCS and with adequate hemodynamics, cerebral angiography with reconstruction was performed, nding thrombosis of the right middle cerebral artery with decreased cerebral edema compared to admission. After 6 days he was extubated with left hemiplegia, currently with home physical therapy [ Figure 1].

Case 2
16-year-old male schoolboy admitted to pediatric intensive care for refractory status epilepticus. On admission, cerebral tomography without contrast shows mild cerebral edema without intraparenchymal bleeding. Transcranial color-coded duplex scan (TCCS) shows vessels dependent on the M2 segment of the middle cerebral artery with multicolor pattern in different shades of blue and red corresponding to different directions of blood ow compatible with an arteriovenous malformation, then underwent cerebral panangiography and embolization con rming the nding of arteriovenous malformation dependent on the middle cerebral artery [ Figure 2].

Case 3
10-year-old male schoolboy suffers severe traumatic injury due to a tra c accident. Brain tomography on hospital admission shows laminar epidural hematoma in the right frontal region with small hemorrhagic contusions in the frontal region and global edema. Intracranial pressure sensor registers ICP < 20 mmhg. 24 hours after admission, he presented sudden neurological deterioration associated with mydriasis, bradycardia and arterial hypertension above the 95th percentile, he was stabilized in the emergency room and then admitted to the operating room due to rebleeding in cerebral tomography with severe endocranial hypertension, it was decided to evacuate the hematoma and decompressive craniectomy plus right duroplasty, Upon admission to the pediatric intensive care unit, the patient showed clinical signs of encephalic death, for which transcranial color-coded duplex (TCCS) was performed under lowdose sedation and analgesia. Reverberant ow spectra (cerebral circulatory arrest pattern) were observed in both middle cerebral arteries and basilar artery, then isolated systolic spikes and mortality were observed after 98 hours of hospital admission [ Figure 3].

Case 4
School girl, 7 years old, female, admitted for severe headache and vomiting of 72 hours of evolution, Glasgow scale 14. On admission, cerebral tomography with angiography was performed, showing subarachnoid hemorrhage Fisher II scale, probable aneurysmal origin, in transcranial color-coded duplex (TCCS) on admission, right MCA showed mean velocity 72 cm/s with pulsatility index 0.62, left MCA showed mean velocity 70 cm/s with pulsatility index 0. 60, 24 hours after admission the MV of the right MCA was elevated from 72 cm/s to 110.3 cm/s and there was no variation in velocities of the left MCA, ipsilateral/contralateral MCA index >1.5, Lindegaard index >3 (3.8-4.2) compatible with mild vasospasm so nimodipine was started in continuous infusion, the next day panangiography and embolization of 4 mm aneurysm located in the anterior communicating artery, with favorable evolution [ Figure 4].

Case 5
13 year old school girl, suffers severe traumatic brain injury due to tra c accident, GSC 8 points, brain tomography shows global brain edema, no bleeding, monitor intraparenchymal pressure of 30 mmHg, in transcranial color-coded Duplex, shows pattern of low velocity and high resistance in anterior circulation and posterior circulation pattern of high pulsatility without hypoperfusion, received bolus of 3% hypertonic solution followed by infusion at 1 ml / kg / hour and optimization of sedoanalgesia. Controls with color-coded transcranial Duplex, improvement of ow velocities and progressive decrease of pulsatility index until normalization [ Figure 5].

Discussion
Color-coded transcranial Duplex, a noninvasive real-time method, can be used as a pediatric bedside tool to identify compromised intracranial hemodynamics. Its utility is described to identify blood ow more reliably in speci c intracranial vessel segments; allows for more detailed assignment of vascular pathologies; and offers the opportunity for angle correction, resulting in more accurate measurement of ow velocities [4].
In case 1 with color-coded transcranial duplex evaluation, it is reliable and noninvasive of patients with cerebral artery stenosis becomes feasible, avoiding the potential adverse effects of cerebral angiography. Transcranial ultrasound provides reliable assessment of cross-ow through the circle of Willis and stenosis, occlusions and vasospasm of the main basal cerebral arteries. It also identi es intracranial hemorrhage but is inferior to neuro radiological techniques [5].
In patients with traumatic brain injury with endocranial hypertension, transcranial Doppler can be a useful tool to estimate cerebral perfusion pressure in a noninvasive manner, and there are studies that show a good correlation between invasive and noninvasive determination of cerebral perfusion pressure [12]. On the other hand, attempts have also been made to estimate intracranial pressure from the pulsatility index, with a good correlation [13]. Transcranial Doppler could not only be useful in the diagnosis of increased intracranial pressure, but also in its follow-up, which is demonstrated through changes in the morphology of the spectral wave, where there is a progressive decrease mainly in the velocities at the end of diastole and a tendency to systolicization of the spectral wave, nally reaching patterns of encephalic death [12], [14], [15], [16], [17], [18].
One of the most notable advantages of CBCT over blind Doppler is that the direction of blood ow can be precisely known and thus align the ultrasound beam as close as possible to an angle of zero degrees with respect to the direction of the erythrocytes, obtaining the velocities with great precision [19], [20], [21], [23]. DCT not only has the advantage of obtaining accurate blood ow velocities in the vessels of the polygon of Willis but also provides information about any structural or pathophysiological anatomical alteration of the skull base vessels [20]. In addition, this technique allows insonation of segments of cranial vessels inaccessible by conventional Doppler through the temporal window (e.g., insonation of segment A2 of the anterior cerebral artery) [22].
In case 2 we describe TCCS as a valuable method for the detection and follow-up of hemodynamic changes of AVM in children, before and after treatment, but further studies are needed to establish the bene ts of this approach, for the use of color-coded transcranial duplex ultrasound (TCCS). As mentioned above, DCT not only has the advantage of obtaining more accurate erythrocyte velocities, but also provides information about any structural anatomical alteration of the blood vessels [20].
In case 3 we describe sonographic ndings of cerebral circulatory arrest. Color-coded duplex ultrasonography and CT angiography have recently been incorporated in the fourth update of the German Medical Association guidelines for the determination of irreversible cessation of brain function ("brain death"), as of July 2015 [6].
Although the diagnosis of encephalic death is clinical [24], on some occasions the clinical examination cannot be performed, as in cases of severe facial trauma or in situations where it is impossible to perform the apnea test, it is in these cases where ancillary tests become fundamental tools for making the diagnosis of encephalic death [24], [25]. Within the ancillary tests, cerebral angiography is one of the tools with the greatest diagnostic certainty and when CDCT was compared with cerebral angiography, CDCT was a sensitive tool for diagnosing brain death, offering a reliable alternative to cerebral angiography [26].
Case 4 describes TCCS signs of cerebral vasospasm and nding of cerebral aneurysm. TCCS is useful for the detection and follow-up of intracranial vasospasm, can visualize larger supratentorial hematomas with subcortical localization and hemorrhagic transformation of ischemic infarcts, and provides incidental detection of cerebral aneurysms and arteriovenous malformations [7]. Findings in cerebral occlusive disease, TCCS provides information on the location of the stenosis. An increase in ow velocity is also measured in the case of vasospasm [8]. It should be noted that the reliability to detect the real magnitude of the velocities is much more accurate with CBCT than with blind Doppler, however it should be noted that the Lindergard Index was described by this author with a 2MHz transducer, both to insonate the midbrain and to insonate the extracranial portion of the ipsilateral internal carotid [27],[28]; this frequency may vary slightly when performing CBCT.
Case 5 Intracranial hypertension is described using color Doppler can localize intracranial vessels and simpli es the acquisition of the pulsed wave Doppler spectrum. Elevation of the pulsatility index may be useful as a diagnostic support tool when very high intracranial pressure or cerebral hypoperfusion is suspected [9].
The intracranial arteriovenous index is a reliable parameter that can be used to assess vasospasm after subarachnoid hemorrhage. Its reliability in differentiating vasospasm and hyperperfusion is slightly higher than that of the established Lindegaard index, and this method has the additional advantage of a markedly lower failure rate [10].
An aneurysm is visualized as a color-coded appendage next to a normal vessel. The most typical colorcoded feature is the presence of two areas with inversely directed ow: half of the aneurysm is colorcoded blue and the other half is color-coded red, with the colors corresponding to the direction of blood in ow and out ow [11].
The early use of TCCS (within 24 h of admission), its status as a rst line neuromonitoring tool, and the frequency of use during night shifts highlighted the immediate availability of this technique. Thus, TCCS has the potential to become an in uential neuromonitoring strategy in the PICU.

Conclusions
Color-coded transcranial duplex is useful in the face of diagnostic suspicion of cerebral vascular events in critically ill children and allows us to guide our surgical medical conduct. Although it is not superior to high resolution sonographic imaging studies, nevertheless, it adds to the studies for an adequate diagnosis.

Declarations
Con ict of Interest Disclosures: The authors have indicated they have no con icts of interest to this article to disclose.
Abbreviations: Transcranial color-coded duplex sonography (TCCS), pediatric intensive care units (PICUs), Funding / Support: No funding was secured for this study.