REVIEW URRENT C OPINION
Transcranial Doppler after traumatic brain injury: is there a role? Pierre Bouzat a,b,c, Mauro Oddo d, and Jean-Franc¸ois Payen a,b,c
Purpose of review To present the practical aspects of transcranial Doppler (TCD) and provide evidence supporting its use for the management of traumatic brain injury (TBI) patients. Recent findings TCD measures systolic, mean, and diastolic cerebral blood flow (CBF) velocities and calculates the pulsatility index from basal intracranial arteries. These variables reflect the brain circulation, provided there is control of potential confounding factors. TCD can be useful in patients with severe TBI to detect low CBF, for example, during intracranial hypertension, and to assess cerebral autoregulation. In the emergency room, TCD might complement brain computed tomography (CT) scan and clinical examination to screen patients at risk for further neurological deterioration after mild-to-moderate TBI. Summary The diagnostic value of TCD should be incorporated into other findings from multimodal brain monitoring and CT scan to optimize the bedside management of patients with TBI and help guide the choice of appropriate therapies. Keywords cerebral blood flow, intensive care, transcranial Doppler, traumatic brain injury
INTRODUCTION Neurological outcome after traumatic brain injury (TBI) depends on the severity of initial injuries and the extent of secondary cerebral damage [1]. Such secondary brain damage is mainly caused by ischemia and hypoxia induced by the imbalance between oxygen supply to the brain tissue and its utilization [2 ]. Prevention and treatment of such secondary injuries are the focus of modern TBI management. In this context, the maintenance of adequate cerebral blood flow (CBF) is critical to limit ischemia, that is, the decrease of CBF under the threshold to sustain essential cerebral functionality [3]. Although validated pharmacological interventions to treat TBI patients are still lacking, CBF manipulation and optimization remain a mainstay of therapy. However, measuring the real-time CBF changes during therapeutic intervention at the bedside is challenging, and cannot be achieved routinely using imaging techniques such as perfusion MRI and perfusion computed tomography (CT) scan [4]. Bedside multimodal monitoring is recommended to optimize brain hemodynamics, oxygenation, and brain metabolism after severe TBI. However, jugular venous oxygen saturation (SvjO2), &
brain tissue oxygen pressure (PbtO2), and microdialysis, although surrogate markers of the adequacy between energy supply and energy requirement [5], are not CBF monitors per se. Several bedside CBF monitors exist, for example, laser Doppler or thermal diffusion probe. These monitors, however, are invasive and estimate regional CBF only. By contrast, transcranial Doppler (TCD), introduced in 1982 [6], is noninvasive and measures real-time CBF velocities from basal cerebral arteries. Initially used to diagnose vasospasm after subarachnoid hemorrhage (SAH) [7], TCD is now used in other brain injuries such as TBI and stroke. Active research has been performed
a
Department of Anesthesiology and Critical Care, Grenoble University Hospital, bJoseph Fourier University, cGrenoble Neuroscience Institute, INSERM U836, Grenoble, France and dDepartment of Intensive Care Medicine, Lausanne University Hospital, Lausanne, Switzerland Correspondence to Dr Jean-Franc¸ois Payen, MD, PhD, Poˆle d’Anesthe´sie-Re´animation, CHU Grenoble, CS 10217, F-38043, Grenoble, France. Tel: +33 4 56 52 05 89; fax: +33 4 56 52 05 98; e-mail: [email protected] Curr Opin Crit Care 2014, 20:153–160 DOI:10.1097/MCC.0000000000000071
1070-5295 ß 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
www.co-criticalcare.com
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Neuroscience
KEY POINTS Transcranial Doppler (TCD) is a useful bedside noninvasive technique to manage patients with TBI in the ICU and the emergency room, provided the factors that may influence the interpretation of TCD signals are corrected for. In patients with severe TBI, TCD can detect inadequate CBF, assess cerebral autoregulation, and help indicate the need for invasive brain monitoring and of required therapies in a multimodal neuromonitoring approach. In patients with mild-to-moderate TBI, TCD can be used in the emergency room, in conjunction with CT scan, to identify patients at risk for secondary neurological deterioration.
on the use of TCD in anesthesia and intensive care (see reviews [8–11]). In brain trauma, the use of TCD appears particularly relevant, given the impact of posttrauma episodes of low brain perfusion on functional outcome. However, as TCD is not incorporated into the guidelines for the management of TBI, it is not widely used in practice. The purpose of this review is to present practical aspects of the technique, and provide evidence specifically favoring its use in patients with severe and mild-to-moderate TBI. The use of TCD to diagnose brain death and vasospasm in the context of TBI will not be covered.
TRANSCRANIAL DOPPLER: FROM THEORY TO PRACTICE In the mid-1800s, the Austrian physicist Christian Andreas Doppler observed that when a sound wave with a certain frequency strikes a moving object, it is reflected with a different frequency. The principle of this phenomenon, called the Doppler effect, was then applied to monitor red blood cell motion inside an insonated blood vessel by measuring the difference in ultrasound frequencies between emission and reception [6].
Relationship between blood velocity and cerebral blood flow Observed flow velocity is related to actual flow velocity through the cosine of the angle u of incidence between the ultrasound beam and the velocity vector: Observed FV ¼ Actual FV cosu Thus, the observed TCD velocity should never overestimate the actual velocity of red blood cells. 154
www.co-criticalcare.com
At an angle of 158, the cosine remains more than 0.96 and any error caused by changes in the angle is less than 4%. However, measurements of flow velocity are only estimators of CBF, and changes in flow velocity correlate with the changes in CBF only if the angle of insonation and the diameter of the insonated vessel remain constant. Indeed, CBF is related to flow velocity as follows: CBF ¼ HR TVI blood vessel cross-sectional area in which HR is heart rate and TVI the time velocity integral, that is, the area under the spectral curve. Despite the more recent use of two-dimensional echo-Doppler, some uncertainties remain in clinical practice concerning the vessel area measurements. TCD may fail to diagnose cerebral vasospasm if both CBF and blood vessel diameter decrease simultaneously [12]. However, cross-sectional areas of major cerebral arteries are mostly unaffected during the acute phase of TBI; this allows reasonable estimation of CBF from flow velocity measurements [13].
Practical considerations Most commonly insonated in clinical practice is the middle cerebral artery (MCA) which is easily accessible through the temporal window above the zygomatic arch. The MCA carries 60–70% of the ipsilateral carotid artery blood flow, so its TCD measurement can be taken to represent blood flow to that hemisphere. However, patient age, female sex, and other factors affecting the bone thickness can make exploration through the temporal window difficult or even impossible (10% of patients). In addition, insonation may be difficult after an ipsilateral craniotomy in the temporal region. In such situations, MCA may be insonated through the eyes. Alternatively, the intravenous injection of ultrasound contrast agents markedly increases the success rate of TCD examinations [14]. Other vessels such as the basilar artery can be explored through the foramen of magnum window or a submandibular approach [15]. There are two methods of TCD recording. The first is transcranial color-coded duplex sonography (TCCS), which displays a two-dimensional colorcoded image [16]. Once the desired blood vessel is found, blood flow velocities may be measured by a pulsed Doppler probe, which graphs velocities over time. The second method is the conventional TCD, using only the second probe function. Although the use of TCCS offers theoretical advantages over conventional TCD, no major differences were found when the two methods were compared in their accuracy to detect vasospasm after SAH [17]. Volume 20 Number 2 April 2014
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Transcranial Doppler after traumatic brain injury Bouzat et al.
V
.44
2
4
–.44
MCA PCA
ACA 6
BS
FIGURE 1. Illustrative example of two-dimensional transcranial Doppler imaging obtained through the temporal window. The brain stem (BS) appears as a hypoechogenic butterfly-shaped structure. All the arteries of the circle of Willis, the middle cerebral artery (MCA), the anterior cerebral artery (ACA), and the posterior cerebral artery (PCA) are located using the color mode.
In practice, the two MCAs are insonated at a depth of 45–60 mm, and the blood flow is directed toward the probe. The Doppler instrument operates at 2 MHz, and the angle and position of insonation are adjusted to provide the highest quality Doppler signal. The probe can then be
secured with a headband to maintain the same angle of insonation for continuous flow velocity recordings. Using transcranial color-coded duplex sonography, the clinoid process of the sphenoid bone and the brain stem are identified first. Color-coded sonography allows the identification of the circle of Willis (Fig. 1). The M1 segment of the MCA is located and manual angle correction is applied to measure flow velocity (cm/s). Bilateral tracings are recorded for at least 10 cardiac cycles after a 30-s stabilized recording period. Timeaveraged mean (FVm), systolic (FVs), and diastolic blood flow velocities (FVd) in cm/s and the pulsatility index [(FVs FVd)/FVm] are calculated [18] (Fig. 2). The main advantage of pulsatility index is that it is not affected by the angle of insonation.
Interpretation of transcranial Doppler measurements Blood flow in the basal cerebral arteries, as in the arteries of other vital organs (liver, kidney, and heart), has a prominent diastolic component. FVd reflects the degree of downstream vascular resistance, whereas FVs depends on upstream determinants, that is, cardiac output, ipsilateral carotid blood flow, and arterial blood pressure. FVm is the weighted flow velocity that takes into account the different velocities of the formed elements in the blood vessel insonated, and decreases with low CBF. Flow velocity values obtained in normal individuals
V
.44
5 M1 10 –.44
2.0
FVs
1.5 FVd
1.0 0.5
FVm
[m/s] –4
–3
–2
–1
50 mm/s 0
–0.5
FIGURE 2. Two-dimensional transcranial Doppler imaging: the Doppler signal is recorded from the proximal segment of the middle cerebral artery (M1). FVd, diastolic blood flow velocity; FVm, mean blood flow velocity; FVs, systolic blood flow velocity. 1070-5295 ß 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
www.co-criticalcare.com
155
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Neuroscience Table 1. TCD values obtained in normal individuals Age (years)
FVs (cm/s)
FVm (cm/s)
FVd (cm/s)
20–60
90 20
60 10
45 10
>60
80 20
45 10
35 10
FVd, diastolic blood flow velocity; FVm, mean blood flow velocity; FVs, systolic blood flow velocity; TCD, transcranial Doppler.
are shown in Table 1. The flow velocity waveform is determined by the arterial blood pressure waveform, the visco-elastic properties of the cerebral vascular bed, and blood rheology. Therefore, in the absence of vessel stenosis or vasospasm, changes in arterial blood pressure, or profound anemia, pulsatility index reflects the distal cerebrovascular resistance. In TBI patients, a low FVd, a peaked waveform, and higher pulsatility index values can be observed during high vascular bed resistance induced by elevated intracranial pressure (ICP) or hypocapnia [19,20] (Fig. 3). The correlation between pulsatility index and ICP in patients with various intracranial disorders is still controversial [21,22]. Furthermore, in a large cohort of 290 head-injured patients, the value of pulsatility index to assess ICP and cerebral perfusion pressure (CPP) noninvasively was limited, except for extreme values (ICP >35 mmHg and CPP 25%) and a reduced ipsilateral pulsatility index (
Transcranial Doppler after traumatic brain injury: is there a role? Pierre Bouzat a,b,c, Mauro Oddo d, and Jean-Franc¸ois Payen a,b,c
Purpose of review To present the practical aspects of transcranial Doppler (TCD) and provide evidence supporting its use for the management of traumatic brain injury (TBI) patients. Recent findings TCD measures systolic, mean, and diastolic cerebral blood flow (CBF) velocities and calculates the pulsatility index from basal intracranial arteries. These variables reflect the brain circulation, provided there is control of potential confounding factors. TCD can be useful in patients with severe TBI to detect low CBF, for example, during intracranial hypertension, and to assess cerebral autoregulation. In the emergency room, TCD might complement brain computed tomography (CT) scan and clinical examination to screen patients at risk for further neurological deterioration after mild-to-moderate TBI. Summary The diagnostic value of TCD should be incorporated into other findings from multimodal brain monitoring and CT scan to optimize the bedside management of patients with TBI and help guide the choice of appropriate therapies. Keywords cerebral blood flow, intensive care, transcranial Doppler, traumatic brain injury
INTRODUCTION Neurological outcome after traumatic brain injury (TBI) depends on the severity of initial injuries and the extent of secondary cerebral damage [1]. Such secondary brain damage is mainly caused by ischemia and hypoxia induced by the imbalance between oxygen supply to the brain tissue and its utilization [2 ]. Prevention and treatment of such secondary injuries are the focus of modern TBI management. In this context, the maintenance of adequate cerebral blood flow (CBF) is critical to limit ischemia, that is, the decrease of CBF under the threshold to sustain essential cerebral functionality [3]. Although validated pharmacological interventions to treat TBI patients are still lacking, CBF manipulation and optimization remain a mainstay of therapy. However, measuring the real-time CBF changes during therapeutic intervention at the bedside is challenging, and cannot be achieved routinely using imaging techniques such as perfusion MRI and perfusion computed tomography (CT) scan [4]. Bedside multimodal monitoring is recommended to optimize brain hemodynamics, oxygenation, and brain metabolism after severe TBI. However, jugular venous oxygen saturation (SvjO2), &
brain tissue oxygen pressure (PbtO2), and microdialysis, although surrogate markers of the adequacy between energy supply and energy requirement [5], are not CBF monitors per se. Several bedside CBF monitors exist, for example, laser Doppler or thermal diffusion probe. These monitors, however, are invasive and estimate regional CBF only. By contrast, transcranial Doppler (TCD), introduced in 1982 [6], is noninvasive and measures real-time CBF velocities from basal cerebral arteries. Initially used to diagnose vasospasm after subarachnoid hemorrhage (SAH) [7], TCD is now used in other brain injuries such as TBI and stroke. Active research has been performed
a
Department of Anesthesiology and Critical Care, Grenoble University Hospital, bJoseph Fourier University, cGrenoble Neuroscience Institute, INSERM U836, Grenoble, France and dDepartment of Intensive Care Medicine, Lausanne University Hospital, Lausanne, Switzerland Correspondence to Dr Jean-Franc¸ois Payen, MD, PhD, Poˆle d’Anesthe´sie-Re´animation, CHU Grenoble, CS 10217, F-38043, Grenoble, France. Tel: +33 4 56 52 05 89; fax: +33 4 56 52 05 98; e-mail: [email protected] Curr Opin Crit Care 2014, 20:153–160 DOI:10.1097/MCC.0000000000000071
1070-5295 ß 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
www.co-criticalcare.com
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Neuroscience
KEY POINTS Transcranial Doppler (TCD) is a useful bedside noninvasive technique to manage patients with TBI in the ICU and the emergency room, provided the factors that may influence the interpretation of TCD signals are corrected for. In patients with severe TBI, TCD can detect inadequate CBF, assess cerebral autoregulation, and help indicate the need for invasive brain monitoring and of required therapies in a multimodal neuromonitoring approach. In patients with mild-to-moderate TBI, TCD can be used in the emergency room, in conjunction with CT scan, to identify patients at risk for secondary neurological deterioration.
on the use of TCD in anesthesia and intensive care (see reviews [8–11]). In brain trauma, the use of TCD appears particularly relevant, given the impact of posttrauma episodes of low brain perfusion on functional outcome. However, as TCD is not incorporated into the guidelines for the management of TBI, it is not widely used in practice. The purpose of this review is to present practical aspects of the technique, and provide evidence specifically favoring its use in patients with severe and mild-to-moderate TBI. The use of TCD to diagnose brain death and vasospasm in the context of TBI will not be covered.
TRANSCRANIAL DOPPLER: FROM THEORY TO PRACTICE In the mid-1800s, the Austrian physicist Christian Andreas Doppler observed that when a sound wave with a certain frequency strikes a moving object, it is reflected with a different frequency. The principle of this phenomenon, called the Doppler effect, was then applied to monitor red blood cell motion inside an insonated blood vessel by measuring the difference in ultrasound frequencies between emission and reception [6].
Relationship between blood velocity and cerebral blood flow Observed flow velocity is related to actual flow velocity through the cosine of the angle u of incidence between the ultrasound beam and the velocity vector: Observed FV ¼ Actual FV cosu Thus, the observed TCD velocity should never overestimate the actual velocity of red blood cells. 154
www.co-criticalcare.com
At an angle of 158, the cosine remains more than 0.96 and any error caused by changes in the angle is less than 4%. However, measurements of flow velocity are only estimators of CBF, and changes in flow velocity correlate with the changes in CBF only if the angle of insonation and the diameter of the insonated vessel remain constant. Indeed, CBF is related to flow velocity as follows: CBF ¼ HR TVI blood vessel cross-sectional area in which HR is heart rate and TVI the time velocity integral, that is, the area under the spectral curve. Despite the more recent use of two-dimensional echo-Doppler, some uncertainties remain in clinical practice concerning the vessel area measurements. TCD may fail to diagnose cerebral vasospasm if both CBF and blood vessel diameter decrease simultaneously [12]. However, cross-sectional areas of major cerebral arteries are mostly unaffected during the acute phase of TBI; this allows reasonable estimation of CBF from flow velocity measurements [13].
Practical considerations Most commonly insonated in clinical practice is the middle cerebral artery (MCA) which is easily accessible through the temporal window above the zygomatic arch. The MCA carries 60–70% of the ipsilateral carotid artery blood flow, so its TCD measurement can be taken to represent blood flow to that hemisphere. However, patient age, female sex, and other factors affecting the bone thickness can make exploration through the temporal window difficult or even impossible (10% of patients). In addition, insonation may be difficult after an ipsilateral craniotomy in the temporal region. In such situations, MCA may be insonated through the eyes. Alternatively, the intravenous injection of ultrasound contrast agents markedly increases the success rate of TCD examinations [14]. Other vessels such as the basilar artery can be explored through the foramen of magnum window or a submandibular approach [15]. There are two methods of TCD recording. The first is transcranial color-coded duplex sonography (TCCS), which displays a two-dimensional colorcoded image [16]. Once the desired blood vessel is found, blood flow velocities may be measured by a pulsed Doppler probe, which graphs velocities over time. The second method is the conventional TCD, using only the second probe function. Although the use of TCCS offers theoretical advantages over conventional TCD, no major differences were found when the two methods were compared in their accuracy to detect vasospasm after SAH [17]. Volume 20 Number 2 April 2014
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Transcranial Doppler after traumatic brain injury Bouzat et al.
V
.44
2
4
–.44
MCA PCA
ACA 6
BS
FIGURE 1. Illustrative example of two-dimensional transcranial Doppler imaging obtained through the temporal window. The brain stem (BS) appears as a hypoechogenic butterfly-shaped structure. All the arteries of the circle of Willis, the middle cerebral artery (MCA), the anterior cerebral artery (ACA), and the posterior cerebral artery (PCA) are located using the color mode.
In practice, the two MCAs are insonated at a depth of 45–60 mm, and the blood flow is directed toward the probe. The Doppler instrument operates at 2 MHz, and the angle and position of insonation are adjusted to provide the highest quality Doppler signal. The probe can then be
secured with a headband to maintain the same angle of insonation for continuous flow velocity recordings. Using transcranial color-coded duplex sonography, the clinoid process of the sphenoid bone and the brain stem are identified first. Color-coded sonography allows the identification of the circle of Willis (Fig. 1). The M1 segment of the MCA is located and manual angle correction is applied to measure flow velocity (cm/s). Bilateral tracings are recorded for at least 10 cardiac cycles after a 30-s stabilized recording period. Timeaveraged mean (FVm), systolic (FVs), and diastolic blood flow velocities (FVd) in cm/s and the pulsatility index [(FVs FVd)/FVm] are calculated [18] (Fig. 2). The main advantage of pulsatility index is that it is not affected by the angle of insonation.
Interpretation of transcranial Doppler measurements Blood flow in the basal cerebral arteries, as in the arteries of other vital organs (liver, kidney, and heart), has a prominent diastolic component. FVd reflects the degree of downstream vascular resistance, whereas FVs depends on upstream determinants, that is, cardiac output, ipsilateral carotid blood flow, and arterial blood pressure. FVm is the weighted flow velocity that takes into account the different velocities of the formed elements in the blood vessel insonated, and decreases with low CBF. Flow velocity values obtained in normal individuals
V
.44
5 M1 10 –.44
2.0
FVs
1.5 FVd
1.0 0.5
FVm
[m/s] –4
–3
–2
–1
50 mm/s 0
–0.5
FIGURE 2. Two-dimensional transcranial Doppler imaging: the Doppler signal is recorded from the proximal segment of the middle cerebral artery (M1). FVd, diastolic blood flow velocity; FVm, mean blood flow velocity; FVs, systolic blood flow velocity. 1070-5295 ß 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
www.co-criticalcare.com
155
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Neuroscience Table 1. TCD values obtained in normal individuals Age (years)
FVs (cm/s)
FVm (cm/s)
FVd (cm/s)
20–60
90 20
60 10
45 10
>60
80 20
45 10
35 10
FVd, diastolic blood flow velocity; FVm, mean blood flow velocity; FVs, systolic blood flow velocity; TCD, transcranial Doppler.
are shown in Table 1. The flow velocity waveform is determined by the arterial blood pressure waveform, the visco-elastic properties of the cerebral vascular bed, and blood rheology. Therefore, in the absence of vessel stenosis or vasospasm, changes in arterial blood pressure, or profound anemia, pulsatility index reflects the distal cerebrovascular resistance. In TBI patients, a low FVd, a peaked waveform, and higher pulsatility index values can be observed during high vascular bed resistance induced by elevated intracranial pressure (ICP) or hypocapnia [19,20] (Fig. 3). The correlation between pulsatility index and ICP in patients with various intracranial disorders is still controversial [21,22]. Furthermore, in a large cohort of 290 head-injured patients, the value of pulsatility index to assess ICP and cerebral perfusion pressure (CPP) noninvasively was limited, except for extreme values (ICP >35 mmHg and CPP 25%) and a reduced ipsilateral pulsatility index (
