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• The report should describe signicant nonvascular abnormalities.
• The criteria for common carotid and vertebral artery stenosis differ from internal
carotid artery criteria.
• A velocity threshold that indicates an external carotid stenosis is not established.
• A simple description indicating a stenosis, if present, may be reported.
• Identication of stenosis can be based on gray-scale and/or color ow narrowing,
elevated velocity through the stenosis and typical poststenotic waveforms.
• The velocity criteria for stenosis after interventions may require different criteria
than native vessels. Stents require different velocity criteria than native ves-
sels [20].
G. Pánczél et al.

26.13 Negative Report

Standardized examination and reporting is recommended to ensure that the exami­nation contains every necessary information. The report should include the course of the vessels, their wall structure, ow characteristics of the internal carotid and vertebral arteries, and comparison of the two sides. Every report should include an opinion. A graphic report that includes a preprinted schematic gure with velocities and any abnormalities can be drawn onto could be useful for comparison during follow-up.
Example: The course of the carotid arteries is normal on both sides. The wall of the vessels and the measured IMT are normal. Antegrade, equal ow can be detected in both common (left: right:) and internal (left: right:) carotid arteries with normal spectrum and normal velocity.
Opinion: No wall abnormalities or ow disturbances can be detected in the examined vessels. Signature, date.

26.14 Conclusion

Carotid ultrasound is a cost-effective bedside diagnostic tool for assessing carotid artery diseases without radiation hazard and risk of claustrophobia.
Doppler US is an important method for following mild to moderate stenoses and for follow-up after stent or endarterectomy. PSV and/or EDV may provide more accurate assessment of stenosis. Contrast-enhanced ultrasound further improves the accuracy. In case of contralateral stenosis, tandem lesions, nearly occlusive ICA stenosis the gray-scale and color Doppler ndings can be helpful. The carotid ultra­sound provides information regarding plaque characteristics (stability, homogene­ity, vascularization, etc.) The quantitative IMT measurement and follow-up (a marker of arteriosclerosis) is also possible using the modern equipment. Pitfalls: The accuracy of carotid ultrasound depends on the operator’s skill and image quality.
INTENSIVE CARE UNIT (ICU)
A[
Longitudinal Plane
26 Carotid Disease: Usefulness oftheUltrasound
459
In stenoses within the low (<50%) and moderate (50–70%) range, intrastenotic velocity increases only modestly relative to the luminal loss that requires additional morphologic estimation of stenosis using B-mode.

Algorithm

Clinical Status of Patient
ABCD
CAROTID STENT
Protocol
B-Mode (Gray-Scale)
Spectral Doppler
Color Doppler
Documentation
Lumen?
Stent Deployment?
Flow?
Site of Highest PSV?
Spectral Waveform?
1st STEP
B-MODE
CCA
Whole Segment
CAROTID BIFURCATION4 –5 cm Proximal
ICA
Whole SegmentHigh Frequency (7.5 MHz) ICA
ECA Proximal
Whole Segment Middle to distal Cervical
Atherosclerotic Plaque? CCA
Location
Extent
Characteristics
Other Abnormality? EC
DOCUMENTATION
Transverse Plane
Longitudinal Plane Atherosclerotic Plaque?
ABCD Airway-Breathing-Circulation-Disability, CCA Common carotid artery, ICA Internal carotid artery, ECA External carotid artery, Bb Below bifurcation, PSV Peak systolic velocity, EDV End-Diastolic velocity
Level of consciousness(GCS) Bilateral Pupillary reactivity Hemodynamic stability? Oxygenation?/ Mechanical Ventilation? Non-contrast Brain CT Scan?
DIAGNOSIS
STROKE SUSPECTED
CAROTID DISEASE SUSPECTED
CAROTID ULTRASOUND (CUS)
Probe Location
Dorsal to the Sternocleidomastoid
muscle above the clavicle
Depth
Probe (MHz)
2nd STEP
COLOR DOPPLER
Distal
ICA Significant Stenosis?
Proximal and Midinternal
Identification with Branch
Extent
Effect on the Color Flow
Color and/or Power Doppler image
Occlusion? Transverse Plane
Other Abnormality?
DOCUMENTATION
Transverse Plane
SPECTRAL WAVEFORM
MAXIMAL PSVRECORDED
Middle or Distal (3 cm Bb)
Location Site of maximum PSV]
Distal of Stenosis Disturbed Flow
DOCUMENTATION
Longitudinal Plane
CALCULATE
Velocity Ratios
EDV
3th STEP
CCA
ECA
Proximal
Presence?
Absence?
460
G. Pánczél et al.

References

1. Benjamin EJ, Virani SS, Callaway CW, etal. Heart disease and stroke statistics– 2018 update: a report from the American Heart Association. Circulation. 2018;137:e67–e4921.
2. Clevert DA, Johnson T, Jung EM, etal. Color Doppler, power Doppler and B-ow ultrasound in the assessment of ICA stenosis: comparison with 64-MD-CT angiography. Eur Radiol. 2007;17(8):2149–59.
3. Bartels E. Color-coded duplex ultrasonography of the cerebral vessels. Atlas and manual. Schattauer: Stuttgart; 1999.
4. Csiba L, Baracchini C, editors. Manual of neurosonology. Cambridge University Press; 2016. p.1–214.
5. Grant EG, Benson CB, Moneta GL, etal. Carotid artery stenosis: gray-scale and Doppler US diagnosis-Society of Radiologists in Ultrasound Consensus Conference. Radiology. 2003;229(2):340–6.
6. Grant EG, Benson CB, Moneta GL, etal. Society of Radiologists in Ultrasound. Carotid artery stenosis: grayscale and Doppler ultrasound diagnosis–Society of Radiologists in Ultrasound consensus conference. Ultrasound Q. 2003;19:190–8.
7. Scoutt LM, Gunabushanam G.Carotid ultrasound. Radiol Clin N Am. 2019;57(3):501–18.
8. Rafailidis V, Charitanti A, Tegos T, etal. Contrast-enhanced ultrasound of the carotid system: a review of the current literature. J Ultrasound. 2017;20(2):97–109.
9. Touboul PJ, Hennerici MG, Meairs S.Mannheim carotid intima-media thickness and plaque consensus (2004–2006–2011). An update on behalf of the advisory board of the 3rd, 4th and 5th watching the risk symposia, at the 13th, 15th and 20th European Stroke Conferences, Mannheim, Germany, 2004, Brussels, Belgium, 2006, and Hamburg, Germany, 2011. Cerebrovasc Dis. 2012;34(4):290–6.
10. Saba L, Anzidei M, Marincola BC, et al. Imaging of the carotid artery vulnerable plaque. Cardiovasc Intervent Radiol. 2014;c37:572–85.
11. Reiter M, Horvat R, Puchner S, etal. Plaque imaging of the internal carotid artery– correlation of B-ow imaging with histopathology. AJNR Am J Neuroradiol. 2007;28(1):122–6.
12. Valdueza JM, Schreiber SJ, Roehl JE, Klingebiel R. Neurosonology and neuroimaging of stroke. Stuttgart: Georg Thieme Verlag; 2008.
13. Fridman S, Lownie SP, Mandzia J.Diagnosis and management of carotid free-oating throm­bus: a systematic literature review. Int J Stroke. 2019;14(3):247–56.
14. Ota H, Takase K, Rikimaru H, etal. Quantitative vascular measurements in arterial occlusive disease. Radiographics. 2005;25(5):1141–58.
15. Rafati M, Havaee E, Moladoust H, et al. Appraisal of different ultrasonography indices in patients with carotid artery atherosclerosis. EXCLI J. 2017;16:727–41.
16. von Reutern GM, Goertler MW, Bornstein NM, etal. Grading carotid stenosis using ultrasonic methods. Stroke. 2012;43(3):916–21.
17. Hathout GM, Fink JR, El-saden SM, et al. Sonographic NASCET index: a new dop­pler parameter for assessment of internal carotid artery stenosis. AJNR Am J Neuroradiol. 2005;26(1):68–75.
18. Varetto G, Gibello L, Castagno C, etal. Use of contrast-enhanced ultrasound in carotid athero­sclerotic disease: limits and perspectives. Biomed Res Int. 2015;2015:293163.
19. Csiba L.Ultrasonic methods used in the diagnosis of changes in the carotid artery system. Orv Hetil. 1990;131(27):1455–60.
20. AIUM practice parameter for the performance of an ultrasound examination of the extracranial cerebrovascular system. J Ultrasound Med. 2016;35(9):1–11.
Chapter 27
Acute Neurologic Injury intheICU: Role ofTranscranial Doppler inDisorders oftheVertebrobasilar Circulation
RickR.Gill, BrettL.Cucchiara, andMonishaA.Kumar
Key Points
1. TCD of the vertebrobasilar system helps guide clinical management in aneurys­mal subarachnoid hemorrhage. Sensitivity and specicity are better for the basi­lar artery than for the vertebral arteries; they are both enhanced when using thresholds >85cm/s or a BA/VA ratio greater than 3.0.
2. A novel approach combining mean ow velocity (MFV) and stenotic to pre­stenotic ratio (SPR) improves the sensitivity of transcranial Doppler (TCD) in the detection of intracranial stenosis.
3. Microembolus signal detection (MES) in the vertebrobasilar circulation is cor­related with both the presence of intracranial vertebrobasilar atherosclerosis and the degree of stenosis making it a useful tool in determining stroke etiology.
4. Intracardiac right to left shunt (RLS) has been implicated in cryptogenic stroke and closure has emerged as a viable therapeutic option. Detection of a RLS using gaseous contrast TCD of the vertebrobasilar circulation through a suboccipital window is both highly sensitive and specic when transtemporal windows are insufcient.
R. R. Gill Department of Neurology, Loyola University, Chicago, IL, USA e-mail: rrgill@lumc.edu
B. L. Cucchiara Department of Neurology, University of Pennsylvania, Philadelphia, PA, USA e-mail: cucchiar@pennmedicine.upenn.edu
M. A. Kumar ( HUP Neuro ICU, Philadelphia, PA, USA
HUP Neuro ICU, Departments of Neurology, Neurosurgery and Anesthesiology and Critical Care, Hospital of the University of Pennsylvania, Philadelphia, PA, USA
University of Pennsylvania Health System, Philadelphia, PA, USA e-mail: monisha.kumar@pennmedicine.uppen.edu
C. N. Rodríguez et al. (eds.), Neurosonology in Critical Care,
https://doi.org/10.1007/978-3-030-81419-9_27
*)
461© Springer Nature Switzerland AG 2022
462
5. TCD may assist in identifying disturbances in cerebral autoregulation, cerebral hypoperfusion, vasomotor reactivity, and stroke risk in patients with traumatic brain injury.
6. Examination of basilar artery ow characteristics is part of a complete TCD assessment for brain death.
R. R. Gill et al.

27.1 Introduction

Transcranial Doppler (TCD) of the anterior circulation is a well-established non­invasive diagnostic imaging modality that has broad application in the intensive care unit (ICU). TCD may enable the clinical diagnosis of acute ischemic stroke, arterial vasospasm, and brain death and is a convenient way to monitor dynamic vascular changes in response to interventions at the bedside. TCD may evaluate brain tissue health by measuring cerebral autoregulation, cerebral vasoreactivity, and neurovas­cular coupling or functional hyperemia, which are all important physiologic assess­ments in the ICU, especially in patients with traumatic brain injury (TBI). TCD may have particular utility in hospitals with reduced access to neurovascular imaging such as CTA or MRA or advanced neuromonitoring. However, the role of TCD of the posterior circulation in the ICU is less well dened.
Assessment of the vertebrobasilar circulation is intuitively part of a complete assessment of the cerebral circulation. However, due to variations in vertebral artery (VA) anatomy, visualization can be technically difcult, and thus, its utility is lim­ited [1, 2]. TCD/TCCS is a reasonably accurate screening technique for size, patency, and direction of blood ow in the vertebral arteries when compared with angiography and can reasonably assess blood ow velocity and detect microemboli [3]. Similarly, TCD can be used to diagnose subclavian steal and pre-steal phenom­ena. As technology has evolved and new clinical applications have been rigorously evaluated, the utility of vertebrobasilar ultrasound to assess for stenosis, dissection, occlusion, vasospasm, and even brain death has also increased. TCD-based assess­ments augment physiological data gleaned from other multimodal neuro monitors and thus may provide important insights for patients with severe neurological injury, such as those with TBI.This chapter serves to review the application of TCD of the posterior circulation to critically ill patients in the neuro ICU.

27.2 Anatomy: Vertebrobasilar System

The two vertebral arteries consist of three extracranial segments (V1–3) and one intracranial segment (V4) before terminating in a single basilar artery (BA) at the level of the pons. Asymmetry is common, with hypoplasia seen more often on the
ab
V4
V3
V2
V1
V0
27 Acute Neurologic Injury in the ICU: Role of Transcranial Doppler in Disorders…
463
right. The V1 segment extends from the subclavian artery (SCA) which is a branch from the arch of the aorta; this segment can be tortuous and typically originates from the cranio-dorsal SCA.In a small minority of cases, the left VA may arise from the aortic arch directly or very rarely from the common carotid artery. The V2 seg­ment typically enters the transverse foramen of the cervical vertebral column at C6, although in variants it may enter at C5 or C7. The V3 segment exits the transverse foramen at C1 and traverses the posterior arch of C1 before entering the foramen magnum and the V4 (intradural) segments extend from the dura to their conuence as the basilar artery (Fig.27.1) [4].
Collateral blood ow can confound ultrasound evaluation of a vascular territory. In the vertebrobasilar circulation, the pre-Willisian collaterals include the deep cer­vical artery which can contribute antegrade lling of the VA in patients with proxi­mal stenosis. Within the Circle of Willis, the posterior communicating arteries (PCA) connect the left and right side of the posterior circulation, as well as the ipsilateral anterior and posterior circulation when a fetal PCA is present. Cortical anastomoses between distal branches of the PCA provide a post-Willisian commu­nication [4].
V4 V3
V2
V1 V0
Fig. 27.1 The vertebrobasilar circulation: (a) Lateral anatomical view and (b) Frontal anatomical view; V0-V4: segments of the vertebral artery: V0: the origin, V1: from the origin of VA to its entry into transverse foramen of C6 vertebra, V2: from the entry into transverse foramen of C6 vertebra until the exit from the C2 vertebra, V3: Atlas loop and V4: intracranial part. (Courtesy: Baltgaile [68])
464
R. R. Gill et al.

27.3 Vertebrobasilar Circulation: Ultrasound Examination

The VA is divided into four segments with segments 1–3 representing the extracra­nial components. The extracranial VA is best visualized by vascular ultrasound using a linear probe (5–7.5MHz) with the patient supine and the neck extended. Once the common carotid artery is visualized in longitudinal section on B-mode, the probe is slid posteriorly and the acoustic shadows of the cervical vertebral trans­verse processes are identied and the VA (V2 segment) can be insonated in between these acoustic shadows in approximately 95% of patients [5]. Normal peak systolic velocity (PSV), measured using pulsed wave Doppler, for the V2 segment is 20–60 cm/s, with velocities >100 cm/s consistent with a signicant stenosis. Knowledge of normal anatomical variants and asymmetry of the VA diameter, often larger on the left, can be useful in interpreting variations in peak systolic velocity (PSV). The most proximal V1 segment is visible with ultrasound in 65–85% of patients, with the right being more easily visualized than the left which tends to be deeper and originating from the aortic arch in a minority of cases [6]. The origin of the VA is susceptible to a variety of pathology including atherosclerotic disease making visualization and assessment of VA diameter and volume ow by tracking proximally from the V2 segment clinically useful. Alternatively, imaging of the supraclavicular subclavian artery can lead to visualization of the VA origin. The V3 segment of the VA may also be visualized as it exits the transverse process of C1. Color Doppler should be applied, and in a routine carotid assessment, it is often only the V2 segment that is visualized and assessed for direction of ow, which is always cephalad in normal subjects.
Insonation of the nal intracranial segment of the VA (V4) as well as the BA is achieved transcranially. Unlike extracranial insonation where a high-frequency probe can be used, for TCD a 2MHz probe better penetrates through the skull [7]. The suboccipital window can be found inferior and medial to the mastoid process with the probe oriented medially toward the bridge of the nose or the contralateral eye; turning the head to the contralateral side with or without the neck exed may aid visualization [7, 8]. This window utilizes the foramen magnum’s opening into the skull, and through this window at a depth of 50–75mm, ow signals of the ipsi­lateral VA can be obtained. Insonation of the BA is achieved by tracking the VA cephalad and medially through the suboccipital window and increasing the depth to 75–110mm [7]. Alternatively, placing the probe below the occipital protuberance and fanning the probe cephalad with a projection toward the bridge of the nose can also aid in visualizing the BA.Like the VA, the ow within the BA is always cepha­lad and away from the probe in normal healthy subjects. The greater variability of these vessels can often make insonation challenging in comparison to the anterior circulation [2, 7].
27 Acute Neurologic Injury in the ICU: Role of Transcranial Doppler in Disorders…
465

27.4 TCD: Aneurysmal Subarachnoid Hemorrhage

One of the most common applications of TCD in the Neuro ICU is the detection of cerebral vasospasm, or arterial narrowing, after aneurysmal subarachnoid hemor­rhage (SAH). TCD can be used to follow the onset, time course, and resolution of arterial narrowing, and it can be combined with other blood ow measurement tech­niques to provide useful information to clinicians managing patients with subarach­noid hemorrhage. Chapters 23 and 24 discuss the approach to delayed cerebral ischemia (DCI) and cerebral vasospasm and thus will not be discussed in detail here.
27.4.1 Delayed Cerebral Ischemia
The main indication of TCD after SAH is to monitor for the development of DCI, a syndrome that manifests as neurological deterioration typically occurring days after aneurysm rupture and potentially associated with cerebral infarction [9]. Although the pathophysiology of DCI remains unclear, an association between arterial nar­rowing and the development of DCI is frequently considered. It should be noted that the incidence of arterial narrowing nears 70%, but only a fraction of those patients are clinically symptomatic [10]. Therefore, since the incidence of TCD-diagnosed arterial narrowing is much higher than that of clinically signicant narrowing, ther­apy is not usually escalated on the basis of TCD ndings alone.
27.4.2 Vasospasm
Detection of vasospasm using TCD in the vertebrobasilar system after subarachnoid hemorrhage is routinely performed, but remains less sensitive compared to the ante­rior circulation. Elevated ow velocities may not always imply arterial narrowing, as increased blood ow and cerebral hyperemia may confound the diagnosis of cerebral vasospasm. The incidence of basilar artery vasospasm is approximately 40% [11, 12]. Sensitivity and specicity of cerebral vasospasm are better for the basilar artery than for the vertebral arteries [12]. BA mean velocities higher than 60cm/s are associated with 60% specicity and 100% sensitivity for vasospasm; however, increasing the MFV threshold reduces the sensitivity signicantly [11]. The specicity of TCD for arterial narrowing is improved when using ow velocity cutoffs of 80cm/s in the vertebral artery and 95cm/s in the basilar artery [11]. Increasing the MFV thresholds improves to discriminate between hyperemia and vasospasm and improves specicity but results in a loss of sensitivity.
A ratio of BA to extracranial VA ow velocities may help discriminate between BA vasospasm and vertebrobasilar hyperemia. This is similar to the function of the Lindegaard ratio in the anterior circulation. This enhances the utility of TCD in
466
()
–/
()
–/
detecting BA vasospasm, although well-dened thresholds do not exist [11, 13]. When the BA velocity is greater than 85cm/s, a BA/VA ratio greater than 2.5 is associated with 86% sensitivity and 97% specicity for a 25% reduction in BA diameter; a ratio greater than 3.0 is associated with 92% sensitivity and 97% speci­city for a 50% reduction in BA diameter [13]. Despite the lack of well-dened thresholds, BA vasospasm may be an independent prognostic factor associated with unfavorable outcome at 90days [14].
R. R. Gill et al.

27.5 TCD: Vertebrobasilar Dissection

Vertebral and basilar artery dissection are associated with posterior circulation ter­ritory stroke and transient ischemic attack (TIA) as well as subarachnoid hemor­rhage (SAH). Stroke occurs in 63% of cases of vertebral artery dissection (VAD), more commonly related to extracranial than intracranial VAD (66% vs 32%), and is most common in those aged 18–45years carrying an overall annual incidence of 1–1.5 per 100.000 [15]. Some degree of ischemic symptoms (TIA or stroke) involv­ing the brainstem, thalamus, cerebral or cerebellar hemispheres, or rarely the cervi­cal spinal cord occur in upwards of 90% of patients [16]. Subarachnoid hemorrhage occurs in 10% of cases of VAD and it is seen exclusively in intracranial dissection. Basilar dissection is rare, but it carries a high morbidity and mortality from associ­ated SAH.Similarly, intracranial vertebral dissection carries a high morbidity and mortality, and there is a male predominance [17, 18]. Additional diagnostic clues include a young age at onset, severe occipital or neck pain, preceding stroke, and a progressive onset of ischemic symptoms.
While there are no pathognomonic ultrasound ndings for VAD in the V2–V4 segments (and the V1 segment has a high failure rate of examination with both Doppler and duplex sonographic techniques), a patient with high grade stenosis or occlusion and a history and examination consistent with vertebral dissection or pos­terior circulation stroke should prompt further evaluation with CTA, MRA, or DSA [19]. Typical analysis of the vertebral circulation includes extracranial and transcra­nial pulsed-wave Doppler sonography for the V3–4 segments and duplex sonogra­phy for the evaluation of the prelesional intertransverse V2 segment at cervical spine levels 5 and 6. During ultrasound analysis, systolic (PSV) and end-diastolic (EDV) blood ow velocities as well as time mean ow velocity (MFV) should be recorded for each vessel typically using pulsed Doppler gate with correction for insonation angle and the resistive index (RI) and pulsatility index (PI) calculated [18] (Eqs27.1 and 27.1):
RI PSV EDV PSV=
PI PSV EDVMFV=
(27.1)
(27.2)
27 Acute Neurologic Injury in the ICU: Role of Transcranial Doppler in Disorders…
467
Despite a lack of uniform diagnostic criteria, studies have established the sensi­tivity of neurovascular ultrasound in the detection of VA dissection at 70–92% [20]. Data remains limited for the evaluation of primary isolated BA dissection. Microembolic signals, diminished pulsatility index in the posterior cerebral arteries and increased CBFV in the BA can all be clues to the presence of a basilar dissec­tion [21, 22].
Direct signs of vessel abnormality include increased MFV (>120 cm/s) or a >50% increase in velocity compared with an unaffected segment of the vessel. Severely reduced or absent MFV, increased PI, and increased contralateral MFV may be an indirect sign of VA dissection; however, variability in VA diameter is common in the population confounding this examination observation. Occlusion of the vessel detected by a focal absence of ow particularly in the intertransverse seg­ments should raise concern for vertebral dissection. An intraluminal abnormality such as an echo-lucent hematoma or double lumen sign may also suggest dissection in the right clinical context [23]. In this respect, color-coded Doppler can be useful in visualizing segmental dilation or an eccentric channel in the proximal or distal parts of the artery with an increased velocity in the residual channel [18]. Segmentally, the proximal VA (V1–V2) can have distinct ndings of increased arte­rial diameter and decreased PI.The atlas loop is a vulnerable, mobile segment of the VA to which additional attention should be paid, and signs of absent ow signals, low bidirectional ow signals or low post-stenotic ow signals should prompt fur­ther investigation with angiography [19]. Ultrasound has also been shown to be useful in determining the length of dissection in addition to being a practical means of follow-up in cases of angiographic conrmed dissection [18]. The sensitivity of sonographic evaluation of the posterior circulation for dissection is preserved only when all potential abnormalities are considered, and sensitivity decreases when denite abnormal ndings of absent or severely reduced ow velocities, absent dia­stolic ow, bidirectional ow or stenotic signals are used as strict criteria [19].
Pitfalls in the detection of dissection with ultrasound include the detection of pseudoaneurysms of the VA as well as small hematomas or hematomas not within the visible vertebral arterial segment, such as those obscured by the transverse pro­cesses of the cervical spine. Finally, a normal ultrasound evaluation in a patient presenting with a history or exam ndings concerning for posterior circulation dis­section requires further workup, as a negative ultrasound study does not reliably exclude arterial dissection.

27.6 TCD: Intracranial Stenosis

Intracranial atherosclerotic disease (IAD) is responsible for an estimated 8–10% of ischemic strokes globally and remains an independent risk factor for the high recur­rence rate of stroke seen in these patients [2427]. Recurrent stroke risk can be as high as 15% per year in the territory of the stenotic artery with subgroups with severe disease (70–99% stenosis) or those with vertebrobasilar disease at a