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Transcranial Doppler Ultrasonography: Clinical Applications in Cerebrovascular Disease
Subspecialty Clinics: Neurology Transcranial Doppler Ultrasonography: Clinical Applications in Cerebrovascular Disease
GEORGE W. PETTY, M.D., DAVID O. WIEBERS, M.D., IRENE MEISSNER, M,D., Department of Neurology
Transcranial D o p p l e r u l t r a s o n o g r a p h y w a s i n t r o d u c e d i n 1982 a s a n o n i n v a s i v e p r o c e d u r e for a s s e s s m e n t o f t h e intracranial cerebral circulation. T h e l i g h t w e i g h t a n d portable e q u i p m e n t u s e d for transcranial D o p p l e r e x a m i n a t i o n facilitates its u s e in t h e b e d s i d e a s s e s s m e n t of critically ill h o s p i t a l i z e d p a t i e n t s a n d o u t p a t i e n t s . Clinical a p p l i c a t i o n s i n c l u d e t h e d i a g n o s i s o f v a s o s p a s m i n p a t i e n t s w i t h subarach n o i d h e m o r r h a g e , a s s e s s m e n t of intracranial collateral flow i n p a t i e n t s w i t h extra cranial arterial o c c l u s i v e d i s e a s e , d e t e c t i o n of intracranial arterial s t e n o s i s , identi fication of t h e f e e d i n g a r t e r i e s of a r t e r i o v e n o u s malformations a n d m o n i t o r i n g t h e h e m o d y n a m i c effects of t h e i r t r e a t m e n t , confirmation of t h e clinical d i a g n o s i s of brain d e a t h , i n t e n s i v e - c a r e u n i t m o n i t o r i n g of brain-injured p a t i e n t s , a n d intraop e r a t i v e a n d p o s t o p e r a t i v e m o n i t o r i n g of n e u r o s u r g i c a l p a t i e n t s . Transcranial Dop pler technology is also providing n e w insights into the pathophysiologic mechanisms of a variety of c e r e b r o v a s c u l a r c o n d i t i o n s . Clinicians will find transcranial Doppler t e c h n o l o g y m o s t helpful if t h e y h a v e a specific q u e s t i o n about t h e s t a t u s of t h e intracranial c i r c u l a t i o n . F u r t h e r i n v e s t i g a t i o n s m a y e x p a n d t h e clinical a n d re s e a r c h utility of t h i s t e c h n o l o g y .
Transcranial Doppler ultrasonography is a relatively n e w technology that allows noninvasive a s s e s s m e n t of the intracranial cerebral circulation. Since i t s introduction by Aaslid a n d colleagues' at t h e U n i v e r s i t y of Bern i n Switzerland, neurologists a n d neurosurgeons have found a variety of clinical a n d research applications for transcranial Doppler studies, including
diagnosing v a s o s p a s m in patients with aneurysmal subarachnoid hemorrhage, a s s e s s i n g intracranial collateral flow i n patients with extracranial arterial occlusive disease, detecti n g intracranial arterial stenosis, identifying t h e feeding arteries of arteriovenous malformations a n d monitoring t h e hemodynamic effects of their treatment, confirming t h e clinical diagnosis of brain death, intensive-care unit monitoring of brain-injured patients, a n d in-
Address reprint requests to Dr. G. W. Petty, Department of Neurology, Mayo Clinic, Rochester, MN 55905.
traoperative a n d postoperative monitoring of neurosurgical patients.
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DESCRIPTION OF TRANSCRANIAL DOPPLER TECHNOLOGY Transcranial Doppler technology allows mea s u r e m e n t of blood velocity in cerebral arteries at the base of the brain by m e a n s of ultrasound technology.''^ Current de'vices consist of a pulsed range-gated probe that e m i t s a 2-MHz ultra sonic signal focused by a plastic lens (Fig. 1). The 2-MHz signal u s e d in transcranial Doppler tech nology is s o m e w h a t lower in frequency t h a n that used in duplex ultrasound devices (7 to 10 MHz) and thereby achieves the greater t i s s u e penetra tion needed to i n s o n a t e t h e arteries of the circle of Willis deep within t h e cranial vault. The ultrasound signal is e m i t t e d from t h e probe with use of a piezoelectric material that converts electrical signals into ultrasound signals. This signal is t h e n reflected off the erythrocytes trav eling through the vessel being studied and re ceived by the s a m e probe. After reception, the piezoelectric material converts the ultrasound signals into electrical signals that are processed with u s e of real-time fast Fourier transforma tion by a microcomputer. Given the emitted signal frequency (2 MHz) and the m e a s u r e d frequency of the signal received from the eryth rocytes coursing through the arteries, the trans cranial Doppler equipment u s e s the Doppler shift principle to calculate the velocity of the blood flow. The spectral analysis of the velocities during the cardiac cycle is presented on a gray scale as a waveform, and current devices calcu late and present the m e a n velocity and also the pulsatility index (PI = [systolic velocity - dia stolic velocity j/mean velocity), an index of vascu lar resistance. In general, the pulsatility index is decreased in conditions t h a t result in de creased intracranial vascular resistance (com pensatory vasodilation ipsilateral to carotid stenosis or severe occlusion, arteriovenous mal formations) and increased in conditions that result in increased intracranial vascular resis tance (increased intracranial pressure, brain death). The direction of flow (away from or toward the probe) is also indicated (Fig. 2). Because the transcranial Doppler technology incorporates a range-gated pulsed ultrasound signal, instead of a continuous signal, the depth
TRANSCRANIAL DOPPLER ULTRASONOGRAPHY
MCA PCA BA \
~\
(M)l A * ^ A ( A , ) ;
C IA
Siphon Oph
V
1351
A
^
Fig. 1. Diagram of transcranial Doppler ultrasound win dows. Transtemporal approach (A and B) is used to in sonate middle cerebral artery stem [MCA (Mj)], A seg ment of anterior cerebral artery [ACA (A^)], distalmost segment of internal carotid artery siphon (ICA Siphon), and P, and P^ segments of posterior cerebral artery (PCA). Transorbital window (C) is used for insonation of ophthal mic artery (OphA) and immediately supraclinoid and infraclinoid segments of internal carotid artery siphon. Suboc cipital transcranial window (D) is used for insonation of distal intracranial segments of both vertebral arteries (VA) and basilar artery (BA).
of insonation can be adjusted by changing the time between the emission and the reception of the signal by the probe. ^ This feature allows insonation of all major arteries at the base of the brain, as well as a s s e s s m e n t of flow velocity at different points along their intracranial course (Fig. 2). The transcranial Doppler probe may not be positioned indiscriminately on the skull to re ceive signals. In fact, only three "transcranial windows" are commonly used to perform clinical studies (Fig. 1 and 2). The transtemporal win dow is used by placing the probe immediately above the zygomatic arch and directing the sig nal through the thin temporal bone in this re gion. Through the transtemporal approach, the M, s e g m e n t of the middle cerebral artery, the A, s e g m e n t of the anterior cerebral artery, and the distalmost s e g m e n t s of the internal carotid ar tery siphon can be insonated. By angling the probe slightly backward through the transtem poral window, the P, s e g m e n t and, in some cases, the P2 s e g m e n t of the posterior cerebral artery can also be evaluated. The transorbital window is used by placing the probe over the eye
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R ACA
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R ICA Siphon
lAllll^Willil^' LPCA
R MCA
W-^ 46
BA
kkkkl R VA
Fig. 2. Normal transcranial Doppler findings in asymptomatic 34-year-old man. Note augmentation of flow in left posterior cerebral artery (L PCA) during eye opening. Flow is directed away from probe in right anterior cerebral artery A, segment (Λ ACA), right vertebral artery (7? VA), and basilar artery (BA). P / = pulsatility index; Λ/CA = right internal carotid artery; R MCA = right middle cerebral artery.
and directing the signal through the orbit. In this fashion, signals can be detected from the ipsilateral ophthalmic artery, from s e g m e n t s of the ipsilateral internal carotid artery siphon (genu), and from the contralateral A, s e g m e n t of the anterior cerebral artery. The suboccipital window is used by placing the probe beneath the inion and directing the signal through the fora m e n m a g n u m . In this way, signals can be obtained from the distal intracranial s e g m e n t s of both vertebral arteries and from the basilar artery along its length. The velocity m e a s u r e d by the transcranial Doppler technique is a func tion of the cosine of the angle that the Doppler
signal m a k e s with the artery being studied. Therefore, accurate velocities are easily obtained from the Mj s e g m e n t of the middle cerebral ar tery because the angle of insonation approaches zero. As the branches of the middle cerebral artery begin to turn u p into the sylvian fissure and course over the surface of the brain, how ever, the angle of insonation becomes closer to 90 degrees, and the signal diminishes substan tially or disappears. Similarly, transcranial Doppler ultrasonography cannot a s s e s s flow velocity in the A2 s e g m e n t of t h e anterior cere bral artery because the blood flow in this artery is directed at right angles to the probe signal
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w h e n the transtemporal approach is used. For the proximal s e g m e n t s of the major arteries leading to or e m a n a t i n g from t h e circle of Willis, however, the angle of the ultrasound b e a m with the artery being insonated is usually small, and the m e a s u r e d velocity approaches the actual blood velocity (Fig. 2). Normal reference v a l u e s for velocities and standard deviations have been published for each artery."*"' The patient's age,®'' partial arterial pressure of carbon dioxide, and hematocrit* all affect the velocity and m u s t be considered w h e n studies are interpreted. Like all noninvasive technologies, transcra nial Doppler ultrasonography h a s some limita tions. The temporal transcranial window is absent on one or both sides in approximately 4 to 10% of patients; the result is nondiagnostic studies.^'" Absence of a technically adequate transtemporal window s e e m s more common in elderly persons, women, and blacks, perhaps be cause of differences in skull configuration, thick ness, and bone ossification.'° '' Performing trans cranial Doppler s t u d i e s requires considerable patience, practice, and skill in terms of locating the ultrasonic windows and establishing the identities of the arteries being assessed. The nu merous permutations of normal vascular anat omy and of pathologic conditions in the intracra nial arteries of patients with cerebrovascular disease make transcranial Doppler ultrasonogra phy a more physician-intensive technology t h a n oculoplethysmography or duplex Doppler stud ies, which are primarily u s e d to evaluate the s t a t u s of the carotid bifurcation. N e v e r t h e l e s s , a commercially available device u s e s a gantry with bilateral probes affixed to the patient's head, which can be u s e d to produce a threedimensional m a p of t h e intracranial circulation; t h u s , vessel identification and determination of collateral patterns are simplified. Currently, no commercially available duplex transcranial devices are available, although prototypes are being tested.'-' CLINICAL APPLICATIONS In addition to the obvious advantage of being noninvasive, transcranial Doppler ultrasonogra phy is performed with lightweight and portable
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equipment; therefore, bedside a s s e s s m e n t of critically ill hospitalized patients and also out patients is possible. Depending on the specific question posed by t h e clinician, transcranial Doppler studies can take from 3 0 to 60 m i n u t e s and can easily be repeated w h e n indicated (for example, in patients with subarachnoid hemor rhage who have vasospasm). The Therapeutics and Technology A s s e s s m e n t Subcommittee of the American Academy of Neurology''' recently published a position s t a t e m e n t a s s e s s i n g the clinical utility of transcranial Doppler ultra sonography. They determined appropriate clini cal situations in which transcranial Doppler t e s t i n g is of established value (Table 1). The point emphasized in the following discus sion is that transcranial Doppler ultrasonogra phy is useful w h e n the clinician h a s posed a specific question, such as one of the following: Does the patient with a subarachnoid hemor rhage and obtundation have vasospasm? Does t h e patient with a large deep infarction in the middle cerebral artery territory have evidence of middle cerebral stem stenosis? Does the patient with carotid occlusion have collateral flow either from the contralateral carotid system through the anterior communicating artery or from the posterior circulation? Can arrest of the cerebral circulation be substantiated in the patient who m e e t s the clinical criteria for cerebral death? H a s blood flow velocity decreased in the feeding arteries of the arteriovenous malformation after embolization or radiotherapy? Unlike oculoplethysmography and duplex Doppler technology, which are appropriate screening t e s t s for large numbers of patients with asymptomatic carotid stenosis, transient ischemic attack, or stroke, the clinician is un likely to find transcranial Doppler ultrasonogra phy to be of value w h e n it is used to "screen" all patients who have ischemic cerebrovascular disease.'® Transcranial Doppler studies are of clinical value w h e n the clinician h a s a specific question about the causative mechanism for a stroke or the collateral s t a t u s in the intracra nial circulation, which m a y influence the ap proach to m a n a g e m e n t and treatment of the patient.
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Table 1.—Established Clinical I n d i c a t i o n s for Transcranial D o p p l e r T e s t i n g
artery is detected with 86 to 88% sensitivity."*'' In patients in w h o m collateral flow had devel oped from t h e external carotid artery system through the ophthalmic artery to the carotid siphon, transcranial Doppler studies can detect reversal of flow in the homolateral ophthalmic artery with a sensitivity that approaches 100%," although a recent study in which transcranial Doppler technology w a s u s e d suggested that the presence of collateral flow from the external carotid circulation is probably not hemodynami cally significant and more likely represents chronically impaired perfusion to that hemi sphere.'® Monitoring t h e effect of compression of the common carotid artery on the waveforms in the ipsilateral middle cerebral artery stem or on the direction of flow in the ipsilateral A, segment of the anterior cerebral artery m a y provide fur ther information about the presence or the po tential for development of collateral flow, al though in patients with atherosclerotic vascular disease in t h e carotid system, such m a n e u v e r s m a y rarely cause transient ischemic attack or stroke and are not routinely performed in our laboratory. Transcranial Doppler ultrasonogra phy is also helpful in diagnosing subclavian steal p h e n o m e n a by detecting reversal of flow in the distal intracranial s e g m e n t of the vertebral artery ipsilateral to subclavian artery stenosis and, in some cases, reversal of flow in the basilar artery during part of the cardiac cycle.'^ Detection of Hemodynamically Signifi cant Intracranial Arterial Stenosis.—In s t a t e s of pathologic narrowing of arteries, the velocity of the blood flow increases in proportion to the decrease in the arterial luminal area. Therefore, pathologic increases in velocity facili tate transcranial Doppler detection of luminal narrowing in the intracranial arteries, whether due to atherosclerotic stenosis, recanalization or partial obstruction after embolization, or vaso s p a s m (Fig. 4, 5, and 6). In addition to increases in velocity, acoustical properties of the ultra sound signals from stenotic or vasospastic arter ies can be helpful in m a k i n g t h e s e diagnoses.^ Internal Carotid and Middle Cerebral A r t e r i e s . — W i t h use of the transorbital or transtemporal approach, hemodynamically signifi-
1. Assessment of patterns and extent of intracranial collateral circulation in patients with known regions of severe stenosis or occlusion in the internal carotid arteries, vertebral arteries, or subclavian arteries 2. Detection of hemodynamically significant stenosis in the major intracranial arteries at the base of the brain 3. Assessment and follow-up of patients with vasocon striction of any cause, especially vasospasm occurring after subarachnoid hemorrhage 4. Detection of arteriovenous malformations and study of their feeding arteries and the hemodynamic effects of treatment 5. Confirmation of the clinical diagnosis of brain death Modified from the American Academy of Neurology, Thera peutics and Technology Assessment Subcommittee.'''
Detection of Abnormal Collateral Flow.— Transcranial Doppler ultrasonography is a sen sitive and specific method for noninvasive detec tion of collateral flow in patients w i t h carotid artery occlusive disease. In patients with steno sis or occlusion of the internal carotid artery, collateral flow to the ipsilateral hemisphere m a y occur in a number of w a y s , most of which can be demonstrated w i t h transcranial Doppler tech niques. Figure 3 shows typical transcranial Doppler findings in such patients. Most com monly, hemodynamically significant collateral flow to the intracranial carotid territory above an occlusion in the internal carotid artery is accomplished by reversal of flow in the ipsi lateral Aj s e g m e n t of the anterior cerebral ar tery (collateral flow across the circle of Willis from the contralateral carotid s y s t e m through the anterior communicating artery) or a u g m e n tation of flow in the ipsilateral posterior cerebral artery (due to collateral flow through cortical anastomotic channels). Collateral flow from the contralateral internal carotid s y s t e m through the anterior communicating artery (reversal of flow in the ipsilateral Aj s e g m e n t of the anterior cerebral artery) is detected with approximately 94% sensitivity.'^'' Collateral flow from the posterior circulation either through the poste rior communicating artery or by augmentation of flow in the P, s e g m e n t of the posterior cerebral
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R ACA
si
RICA Siphon
Fig. 3. Transcranial Doppler findings in occlusion of right internal carotid artery. Velocities and pulsatility indices are substantially decreased in right distal internal carotid artery siphon {R ICA Siphon) and middle cerebral artery M, segment (R MCA). Collateral flow across circle of Willis is substantiated by the findings of augmented flow velocities in distal left internal carotid artery siphon (L ICA Siphon) and left; anterior cerebral artery A, segment (L ACA) contralateral to ICA occlusion, as well as reversal of flow in right ACA A, segment (R ACA) ipsilateral to ICA occlusion. Note that blood flow velocities are also augmented in right posterior cerebral artery Pj segment (R PCA); this finding suggests collateral flow from right PCA to right MCA territory through cortical anastomotic channels. L MCA = left middle cerebral artery; L PCA = left posterior cerebral artery.
cant stenosis or occlusion of the internal carotid artery siphon can be detected with a sensitivity of 73 to 94% by experienced clinicians.'"" Falsenegative studies m a y arise because transcranial Doppler technology cannot a s s e s s the siphon throughout its entire length but only in the immediately supraclinoid and infraclinoid seg m e n t s (through the transorbital approach) and in the distalmost s e g m e n t s (through the trans temporal approach). False-positive results m a y occur if the anterior communicating or the pos terior communicating artery is misidentified a s the siphon in situations in which collateral flow through t h e s e arteries is a u g m e n t e d because of
occlusive disease in the extracranial carotid ar t e r i e s . ' " " Hemodynamically significant steno sis or occlusion of the middle cerebral artery stem can be detected with 75 to 100% sensitiv i t y . ' * " " Such instances m a y also be accompa nied by augmentation of flow in the ipsilateral Aj s e g m e n t of the anterior cerebral artery.'^ Falsepositive diagnosis of occlusion of the middle cerebral artery can occur if the normal middle cerebral stem h a s an acute downward deflection early in its course (in which case the ultrasound signal may be lost) or if the transcranial window is so small that the probe m u s t be oriented such that the distal part of the middle cerebral stem
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cannot be insonated. In some instances of severe stenosis, the number of erythrocytes passing through the stenotic s e g m e n t may be so small that an adequate signal m a y not be received by the transcranial Doppler probe; the result would be a false-positive diagnosis of occlusion. Be cause transcranial Doppler ultrasonography cannot a s s e s s the distal s e g m e n t s of the middle cerebral artery, this technique is not sensitive for detecting middle cerebral artery branch oc clusion or stenosis beyond the M, segment. C a s e S t u d y . — 2 8 - y e a r - o l d woman taking oral contraceptives had sudden onset of rightsided headache, left hemiparesis, dysarthria, and right gaze preference. A computed tomo graphic scan of the head demonstrated an in farction of the right basal ganglia but no evi dence of hemorrhage. Oculoplethysmography showed normal findings bilaterally. Transcra nial Doppler examination, however, disclosed accelerated flow velocities in the distal right internal carotid artery siphon (Fig. 4 A) and proximal middle cerebral artery stem in com parison with normal signals received from the distal left internal carotid artery siphon (Fig. 4 B). Cerebral angiography (Fig. 4 C) demon strated a filling defect in the l u m e n of the distal right internal carotid artery and proximal middle cerebral artery stem, presumably due to embo lism. The proximal right carotid system w a s normal. An extensive evaluation for a cardiac source of embolus and a procoagulant state was unremarkable. She w a s treated first with hepa rin and t h e n warfarin, and use of oral contracep tives w a s discontinued. Vertebral a n d Basilar Arteries.—Hemo dynamically significant stenosis or occlusion in
Fig. 4. Transcranial Doppler demonstration of accelerated flow velocities in distal right internal carotid artery (ICA) siphon (A) and proximal middle cerebral artery (MCA) stem in a 28-year-old woman taking oral contraceptives who experienced sudden onset of left hemiparesis. Compare with normal signal received from lefl distal ICA siphon (B). Cerebral angiography (C) demonstrated a filling defect in lumen of distal right ICA and proximal MCA stem, pre sumably due to embolism. Proximal right carotid system was normal. PI = pulsatility index.
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Fig. 5. Transcranial Doppler demonstration of increased velocity and pulsatility index iPI) in left vertebral artery in a 77year-old man with bilateral posterior cerebral artery infarctions (A). Angiography demonstrated a long stenotic segment in left vertebral artery (B) that presumably resulted in "local embolism" to posterior cerebral arteries.
the distal intracranial s e g m e n t s of the vertebral arteries and in the basilar artery can also be demonstrated by transcranial Doppler ultra sonography, although the sensitivity and speci ficity m a y be s o m e w h a t l e s s t h a n for detecting stenotic lesions in the anterior circulation." Considerable patient-to-patient variation in the spatial configuration of the distal intracranial s e g m e n t s of the vertebral arteries and differ ences in neck thickness m a k e precise identifica tion of the vertebrobasilar junction difficult in m a n y instances. N e v e r t h e l e s s , for most clini cians, demonstration of stenosis in the distal vertebral arteries or in the basilar artery, re gardless of the precise location, would be suffi cient information for m a k i n g clinical decisions about selection of medical therapy. N e g a t i v e studies, however, m a y be l e s s helpful because the more proximal s e g m e n t s of the vertebral arteries cannot be a s s e s s e d with transcranial Doppler ultrasonography and can be a s s e s s e d only over short intervertebral s e g m e n t s with duplex Doppler technology. Furthermore, in i n s t a n c e s of occlusion of one of the vertebral arteries distal to the origin of the posterior inferior cerebellar artery, "runoff" into the pos
terior inferior cerebellar artery may result in false-negative examinations because of preser vation of relatively normal waveforms and blood flow velocities in the more proximal intracranial s e g m e n t s of the vertebral artery. C a s e S t u d y . — 7 7 - y e a r - o l d m a n had sudden onset of left hemianopia and gait ataxia. A computed tomographic scan o f t h e head demon strated a recent right occipital infarction and a presumably old left occipital infarction. An echocardiogram failed to disclose a cardiac source of embolus. Transcranial Doppler signals obtained at depths of 75 and 80 m m through the suboccipital approach demonstrated high ve locities, turbulence, and increased pulsatility indices (Fig. 5 A), which can be compared with normal vertebral and basilar waveforms and velocities in Figure 2. Angiography demon strated a long stenotic s e g m e n t in the left verte bral artery t h a t presumably resulted in "local embolism" to the posterior cerebral arteries (Fig. 5 B). Diagnosis of Vasospasm.—Perhaps the most common application of transcranial Dop pler ultrasonography is in the noninvasive de tection of arterial v a s o s p a s m after subarachnoid
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hemorrhage (Fig. 6). The highly portable and noninvasive characteristics of the technology m a k e it ideally suited for a s s e s s m e n t of critically ill patients in the intensive-care unit setting. Studies can be repeated at frequent intervals to a s s i s t in m a k i n g decisions about therapeutic m a n e u v e r s to prevent or treat vasospasm and the timing of surgical intervention. The rate of increase in blood flow velocity in vasospastic arteries s e e m s to correlate with the develop m e n t of delayed ischemic deficits in patients with subarachnoid hemorrhage.^'' In addition to clinical applications for diagnosing vasospasm in the setting of subarachnoid hemorrhage, transcranial Doppler technology h a s provided n e w insights into the time course of the develop m e n t of vasospasm^'^ and the effect of calcium antagonists on the severity of vasospasm.^** S p e c i f i c i t y a n d S e n s i t i v i t y . — T h e major clinical value of transcranial Doppler examina tion in diagnosing vasospasm after subarach noid hemorrhage is its high specificity (98 to 100%).^'·^" Therefore, w h e n transcranial Dop pler ultrasonography demonstrates vasospasm, the need for angiography may be obviated, and the clinician can confidently make decisions about treatment and timing of operation;^** however, caution should be exercised in relying on nega tive studies to make clinical decisions in this setting. As pointed out earlier, transcranial Doppler technology cannot be used to a s s e s s the anterior cerebral artery beyond its A^ s e g m e n t or to evaluate the distal branches of the middle cerebral a r t e r y . M o r e o v e r , in patients with poor clinical grades of subarachnoid hemorrhage with increased intracranial pressure, velocities m a y be globally reduced despite t h e presence of vasospasm. Consequently, the overall sensitiv-
Fig. 6. Transcranial Doppler detection of vasospasm in 35year-old man with subarachnoid hemorrhage. Transcra nial Doppler ultrasonography demonstrated considerably increased flow velocities and turbulence in right middle cerebral artery (MCA) stem (A) but only modest increases in velocities in left MCA stem (B). Angiography showed vasospasm in right MCA (C). Left carotid injections demon strated an aneurysm in anterior communicating artery. PI = pulsatility index.
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ity of transcranial Doppler studies in detecting v a s o s p a s m is low (33.3 to 58.6%),'^'* primarily because of the failure to detect s p a s m in the A2 s e g m e n t of the anterior cerebral artery and in the branches of t h e middle cerebral artery. Behavioral abnormalities in patients with ante rior cerebral artery v a s o s p a s m and ischemia m a k e examinations in t h e s e patients techni cally difficult and m a y contribute to the low sensitivity in this setting.'^ Further investiga tion is needed, however, to determine w h e t h e r different approaches to anterior cerebral artery insonation and examination of anterior cerebral artery pulsatility changes m a y increase the sensitivity of transcranial Doppler examinations in detecting v a s o s p a s m in t h i s artery. C a s e S t u d y . — 3 5 - y e a r - o l d m a n sought medical attention because of a severe headache and confusion. Cerebrospinal fluid examination disclosed a subarachnoid hemorrhage. A com puted tomographic scan of the head demon strated a large acute collection of subarachnoid blood in the middle right frontal lobe that ex tended posteriorly into the lamina terminalis and anteriorly into the third ventricle. Four days later, his level of consciousness slowly deteriorated, and he w a s transferred to our in stitution. Transcranial Doppler ultrasonogra phy revealed substantially increased flow ve locities and turbulence in the right middle cere bral artery s t e m consistent w i t h v a s o s p a s m (Fig. 6 A) but only modest increases in velocities in the left middle cerebral artery s t e m (Fig. 6 B). Angiography showed v a s o s p a s m of the right middle cerebral artery s t e m (Fig. 6 C). Left carotid injections demonstrated an a n e u r y s m in the anterior communicating artery. H e w a s in tubated and treated with volume expansion and nimodipine. His m e n t a l s t a t u s slowly improved, and the a n e u r y s m w a s clipped 12 days after the initial examination. Evaluation of Arteriovenous Malforma tions.—^Arteriovenous malformations are typ ically high-velocity, low-pressure, low-resistance arterial s h u n t s y s t e m s . These hemodynamic qualities result in the characteristic transcra nial Doppler findings of higher t h a n normal m e a n and peak blood flow velocities in conjunc
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tion with turbulence and lower than normal pulsatility indices (Fig. 7). By detecting charac teristic signal abnormalities, transcranial Dop pler studies can correctly diagnose arteriove nous malformations w i t h a sensitivity of 87 to 95%.''·^°·^' Small arteriovenous malformations that are located in the cortex and fed by single arterial branches m a y not be detected, however. Because magnetic resonance imaging probably affords an e v e n higher sensitivity t h a n transcra nial Doppler examination for diagnosing arte riovenous malformations, we do not routinely recommend transcranial Doppler testing for di agnostic purposes in patients suspected of hav ing t h e s e lesions. Nevertheless, transcranial Doppler ultrasonography is a convenient and re liable method for quantitatively evaluating the hemodynamic changes that occur in feeding and nonfeeding arteries of arteriovenous malforma tions after treatment (embolization, operation, or radiotherapy).'" After surgical treatment or embolization, transcranial Doppler studies con sistently and quantitatively substantiate in creases in the pulsatility index and decreases in the m e a n velocity in the feeding arteries of these lesions (Fig. 7).'" Such information m a y prove helpful in establishing therapeutic strategies and in determining the prognosis for individual patients. Moreover, depending on results of further investigation, the need for follow-up angiography m a y be obviated in some patients who have radiotherapy for these lesions. Confirmation ofthe Clinical Diagnosis of Cerebral Death.—The proliferation of organ transplantation programs and the high cost and maximal utilization of intensive-care unit treat m e n t have made the timely confirmation of cere bral death an important medical, legal, and economic issue. Most hospitals require confir mation of the clinical diagnosis of cerebral death, usually in the form of an electroencephalogram, before withdrawal of life support. Although widely accepted for this indication, electro encephalography h a s certain logistical disad v a n t a g e s because of the time required to per form and interpret the studies. Transcranial Doppler ultrasonography, which can be per formed within a few m i n u t e s at the bedside of a
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Fig. 7. Transcranial Doppler demonstration of hemodynamic changes after embolization of an arteriovenous malforma tion. A 16-year-old girl with a large arteriovenous malformation in cerebellar vermis fed by branches from basilar artery (A, preembolization angiogram) underwent superselective platinum coil embolization of feeding branches (B, postembolization angiogram). Preembolization transcranial Doppler study (C) demonstrated abnormally increased velocities and decreased pulsatility indices iPI) in proximal basilar artery (BA). After embolization, velocity in basilar artery decreased and pulsatility index increased (D). (From Petty and associates.''^ By permission of the American Heart Association, Inc.)
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critically ill or brain-dead patient, is a rapid and convenient alternative to the electroencephalo gram for confirming cerebral d e a t h . T h e typi cal transcranial Doppler waveform findings in patients with cerebral death are reversal of flow in diastole and a sharp systolic upstroke or small spike waveforms either above or both above and below the baseline at the beginning of systole (Fig. 8).^^·^^ Investigators have demon strated t h a t t h e s e waveform abnormalities oc cur a s the intracranial pressure increases above the cerebral perfusion pressure,^" in correlation with arrest of cerebral blood flow a s demon strated by radionuclide scanning techniques.'*'^ In a series of 54 comatose patients studied with transcranial Doppler ultrasonography, t h e waveforms were highly sensitive and specific for cerebral death (Fig. 8), as established by clinical and electroencephalographic criteria.'*^ Although H a s s l e r and associates'^'' have demon strated t h a t some patients with severely in creased intracranial pressure due to head trauma m a y rarely have this abnormal waveform with out m e e t i n g all the criteria for cerebral death, if the transcranial Doppler study is incorporat ed into institutional protocols and performed after patients m e e t the clinical criteria for cere bral death, false-positive results are unlikely to occur.'*^ POTENTIAL CLINICAL APPLICATIONS In addition to the foregoing clinical applications for transcranial Doppler ultrasonography, sev eral other applications are now being studied. Preoperative, intraoperative, and postoperative monitoring of neurosurgical patients is one po tential u s e of transcranial Doppler technology. For m a n y years, regional cerebral blood flow and electroencephalography have been u s e d to monitor patients during carotid endarterectomy and other revascularization procedures to iden tify patients at risk for postoperative ischemic deficits and those who m a y benefit from s h u n t placement after cross-clamping. Transcranial Doppler m e a s u r e m e n t s of the m e a n blood flow velocity in the middle cerebral artery have been used in attempts to identify such patients. Suppression of electroencephalographic activity
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h a s been correlated with low velocities in the middle cerebral artery.'*'*''' Studies in larger numbers of patients undergoing carotid endar terectomy m a y determine the sensitivity and specificity of transcranial Doppler ischemic ve locity thresholds in comparison with regional cerebral blood flow and electroencephalographic changes as well as clinical outcome. Transcra nial Doppler ultrasonography m a y also be useful in identifying patients in whom the postendarterectomy course is complicated by so-called h y p e r p e r f u s i o n syndromes."* Transcranial Doppler confirmation of impaired carbon diox ide-induced cerebral vasomotor response in patients with occlusion of the internal carotid artery m a y allow identification of subsets of patients with severely impaired hemispheric perfusion and decreased vasoreactivity who could benefit from extracranial-intracranial revascu larization procedures.'*^ •'° Transcranial Doppler technology m a y also be useful for studying the hemodynamic behavior of arteriovenous malfor mations intraoperatively and immediately post operatively and could be used to t e s t hypotheses about so-called perfusion breakthrough phenom ena after surgical resection.'" Further studies are also needed to determine w h a t role, if any, transcranial Doppler ultrasonography may have in monitoring patients with carotid stenosis or occlusion during cardiopulmonary bypass proce dures. One study suggested that the occurrence of postoperative neurologic deficits is unrelated to hypoperfusion of the cerebral circulation during such bypass procedures.''^ Transcranial Doppler studies might provide an ideal alternative to the current methods of monitoring intracranial pressure in patients with head injury, intracranial hemorrhage, brain tumor, or hypoxia.^'' Changes in the pulsatility and direction of transcranial Doppler waveforms during the cardiac cycle provide qualitative in formation about the intracranial pressure and the effect of increases in intracranial pressure on cerebral perfusion pressure. Quantitative correlations of transcranial Doppler pulsatility indices, waveforms, and velocities with actual intracranial pressure, however, are pending. Some investigators are currently attempting to
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Fig. 8. Transcranial Doppler confirmation of clinical diagnosis of cerebral death. Transcranial Doppler waveform abnormalities in brain-dead patients are characterized by either absent or reversed diastolic flow (A) or small early systolic spikes (B). These abnormalities correlate with arrest of cerebral circulation. L MCA and R MCA = left and right middle cerebral artery; PI = pulsatility index. (From Petty and associates.-^^ By permission of Edgell Communica tions, Inc.)
determine w h e t h e r transcranial Doppler exami C O N C L U S I O N nation m a y be useful during cardiopulmonary Although a relatively new technology, transcra resuscitation and in predicting the outcome of nial Doppler ultrasonography is an important tool for the a s s e s s m e n t of selected patients with cardiac arrest."*'^ Various research applications for transcra cerebrovascular disease. As with other noninva nial Doppler ultrasonography are also being sive techniques, the physician m u s t be familiar explored. Although transcranial Doppler mea with the capabilities and limitations of the trans surement of blood flow velocity in the middle cranial Doppler technology in order to make cerebral artery does not correlate well with clinical decisions based on test results. Clini hemispheric cerebral blood flow as m e a s u r e d by cians will find transcranial Doppler studies most the '-''Xe technique, a good correlation exists helpful if they have a specific question about the between changes in velocity and cerebral blood s t a t u s of the intracranial circulation. Clinically flow in response to changes in expiratory carbon useful applications have been established, and dioxide tension.'*'' Transcranial Doppler investi further investigations m a y expand the clinical gations of cerebral h e m o d y n a m i c changes in and research utility of this technology. response to physiologic and pharmacologic stim uli have been reported,'*® '*' although some con A C K N O W L E D G M E N T cern h a s been expressed about the validity of We thank Teresa J. Batzel, Gwen M. Harmon, using transcranial Doppler m e a s u r e m e n t of Cynthia L. Urban, and Sharon R. Ryg for their blood velocity as a surrogate for cerebral blood assistance in performing studies and preparing flow in certain instances.** Transcranial Dop the submitted manuscript. The transcranial pler studies m a y also provide n e w insights into Doppler studies depicted in the illustrations the pathophysiologic m e c h a n i s m s involved in were performed with u s e of an EME TC2-64B stroke occurring in patients with sickle-cell dis (Fig. 2 and 4 through 8) and an E M E Trans-scan ease,"*" migraine,®" cerebral vasculitis,®' and other (Fig. 3), Eden Medizinische Elektronik GmbH, conditions. Uberlingen, Germany.
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REFERENCES 1. Aaslid R, Markwalder T-M, Nomes H: Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg 57:769774, 1982 2. Aaslid R: The Doppler principle applied to measure ment of blood flow velocity in cerebral arteries. In Transcranial Doppler Sonography. Edited by R Aaslid. Wien, Austria, Springer-Verlag, 1986, pp 22-38 3. Aaslid R: Transcranial Doppler examination techniques. In Transcranial Doppler Sonography. Edited by R Aaslid. Wien, Austria, Springer-Verlag, 1986, pp 39-59 4. HardersA: Neurosurgical Applications of Transcra nial Doppler Sonography. Wien, Austria, SpringerVerlag, 1986, pp 24-26 5. Arnolds BJ, von Reutern G-M: Transcranial Dopplersonography: examination technique and normal ref erence values. Ultrasound Med Biol 12:115-123, 1986 6. Hennerici M, Rautenberg W, Sitzer G, Schwartz A: Transcranial Doppler ultrasound for the assessment of intracranial arterial flow velocity. P a r t i . Exami nation technique and normal values. Surg Neurol 27:439-448, 1987 7. Vriens EM, Kraaier V, Musbach M, Wieneke GH, van Huffelen AC: Transcranial pulsed Doppler measure ments of blood velocity in the middle cerebral artery: reference values at rest and during hyperventilation in healthy volunteers in relation to age and sex. Ultrasound Med Biol 15:1-8, 1989 8. Brass LM, Pavlakis SG, DeVivo D, Piomelli S, Mohr JP: Transcranial Doppler measurements of the middle cerebral artery: effect of hematocrit. Stroke 19:14661469, 1988 9. Niederkorn K, Myers LG, Nunn CL, Ball MR, McKinney WM: Three-dimensional transcranial Doppler blood flow mapping in patients with cerebrovascular disorders. Stroke 19:1335-1344, 1988 10. Feinberg WM, Devine J, Ledbetter E, Thigpen L, Castrillo A: Clinical characteristics of patients with inadequate temporal windows (abstract). In Proceed ings of the 4th International Symposium on Intracra nial Hemodynamics: Transcranial Doppler and Cere bral Blood Flow, Orlando, Florida, February 11 to 14, 1990 11. Gomez CR, Gomez SM, Hall IS: The elusive trans temporal window: a demographic and technical study (abstract). J Cardiovasc Technol 8:176-177, 1989 12. Halsey JH: Relative emitted signal intensity in different populations (abstract). J Cardiovasc Tech nol 8:176, 1989 13. SpencerMP: Transcranial duplex color Doppler imag ing (abstract). J Cardiovasc Technol 8:178-179,1989 14. American Academy of Neurology, Therapeutics and Technology Assessment Subcommittee: Assessment: transcranial Doppler. Neurology 40:680-681, 1990 15. Luo YM, Bondar RL, Norris JW: Clinical value of transcranial Doppler in stroke (abstract). J Cardio vasc Technol 8:180, 1989 16. Lindegaard K-F, Bakke SJ, Grolimund P, Aaslid R, Huber P, Nornes H: Assessment of intracranial
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hemodynamics in carotid artery disease by transcra nial Doppler ultrasound. J Neurosurg 63:890-898, 1985 17. Grolimund P, Seller RW, Aaslid R, Huber P, Zurbruegg H: Evaluation of cerebrovascular disease by com bined extracranial and transcranial Doppler sonogra phy: experience in 1,039 patients. Stroke 18:10181024, 1987 18. Tatemichi TK, Chamorro A, Petty GW, Khandji A, Oropeza LA, Duterte DI, Mohr JP: Hemodynamic role of ophthalmic artery collateral in internal carotid artery occlusion. Neurology 40:461-464, 1990 19. Hennerici M, Klemm C, Rautenberg W: The sub clavian steal phenomenon: a common vascular disor der with rare neurologic deficits. Neurology 38:669673, 1988 20. Spencer MP, Whisler D: Transorbital Doppler diag nosis of intracranial arterial stenosis. Stroke 17:916921, 1986 21. Ringelstein EB: A practical guide to transcranial Doppler sonography. In Noninvasive Imaging of Cerebrovascular Disease. Edited by J Weinberger. New York, Alan R Liss, 1989, pp 75-121 22. De Bray JM, Joseph PA, Maugin D, Jeanvoine H, Emile J: Etude a long terme de 20 stenoses proximales de I'artere cerebrale moyenne role du Doppler transcranien. Rev Neurol 145:117-126,1989 23. Brass LM, Duterte DI, Mohr JP: Anterior cerebral artery velocity changes in disease of the middle cere bral artery stem. Stroke 20:1737-1740, 1989 24. Harders AG, Gilsbach JM: Time course of blood velocity changes related to vasospasm in the circle of Willis measured by transcranial Doppler ultrasound. J Neurosurg 66:718-728, 1987 25. Seller RW, Grolimund P, Zurbruegg HR: Evalua tion of the calcium-antagonist nimodipine for the prevention of vasospasm after aneurysmal sub arachnoid haemorrhage: a prospective transcranial Doppler ultrasound study. Acta Neurochir 85:7-16, 1987 26. Seller RW, Grolimund P, Aaslid R, Huber P, Nornes H: Cerebral vasospasm evaluated by transcranial ultrasound correlated with clinical grade and CTvisualized subarachnoid hemorrhage. J Neurosurg 64:594-600, 1986 27. Lennihan L, Petty GW, Mohr JP, Solomon RA, Fink ME, Beckford AR, Duterte DI: Transcranial Doppler detection of anterior cerebral artery vasospasm (abstract). Stroke 20:151, 1989 28. Sloan MA, Haley EC Jr, Kassell NF, Henry ML, Stewart SR, Beskin RR, Seville EA, Tomer JC: Sensitivity and specificity of transcranial Doppler ultrasonography in the diagnosis of vasospasm fol lowing subarachnoid hemorrhage. Neurology 39:15141518, 1989 29. Petty GW, Massaro AR, Tatemichi TK, Mohr JP, Hilal SK, Stein BM, Solomon RA, Duterte Dl, Sacco RL: Transcranial Doppler ultrasonographic changes after treatment for arteriovenous malformations. Stroke 21:260-266, 1990 30. Lindegaard K-F, Aaslid R, Nornes H: Cerebral ar teriovenous malformations. In Transcranial Doppler
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Sonography. Edited by R Aaslid. Wien, Austria, Springer-Verlag, 1986, pp 86-105 Lindegaard K-F, Grolimund P, Aaslid R, Nornes H: Evaluation of cerebral AVM's using transcranial Doppler ultrasound. J Neurosurg 65:335-344, 1986 Petty GW, Mohr JP, Pedley TA, Tatemichi TK, Lennihan L, Duterte Dl, Sacco RL: The role of transcra nial Doppler in confirming brain death: sensitivity, specificity, and suggestions for performance and inter pretation. Neurology 40:300-303, 1990 Ropper AH, Kehne SM, Wechsler L: Transcranial Doppler in brain death. Neurology 37:1733-1735, 1987 Hassler W, Steinmetz H, Gawlowski J: Transcranial Doppler ultrasonography in raised intracranial pres sure and in intracranial circulatory arrest. J Neuro surg 68:745-751, 1988 Newell DW, Grady MS, Sirotta P, Winn HR: Evalu ation of brain death using transcranial Doppler. Neurosurgery 24:509-513, 1989 Schneider PA, Ringelstein EB, Rossman ME, Dilley RB, Sobel DF, Otis SM, Bernstein EF: Importance of cerebral collateral pathways during carotid endar terectomy. Stroke 19:1328-1334, 1988 Halsey JH, McDowell HA, Gelmon S, Morawetz RB: Blood velocity in the middle cerebral artery and regional cerebral blood flow during carotid endar terectomy. Stroke 20:53-58, 1989 Powers AD, Smith RR: Hyperperfusion syndrome after carotid endarterectomy: a transcranial Doppler evaluation. Neurosurgery 26:56-59, 1990 Ringelstein EB, Sievers C, Ecker S, Schneider PA, Otis SM: Noninvasive assessment of CO^-induced cerebral vasomotor response in normal individuals and patients with internal carotid artery occlusions. Stroke 19:963-969, 1988 Widder B: The Doppler CO,^ test to exclude pa tients not in need of extracranial/intracranial bypass surgery. J Neurol Neurosurg Psychiatry 52:38-42, 1989 Young WL, Petty G, Prohovnik I, Ornstein E, Ostapkovich N, Mohr JP, Stein BM: Correlation of transcranial Doppler velocity and '•^''Xe cerebral blood flow before and after arteriovenous malformation resection. J Neurosurg Anesth 1:174-175,1989
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Von Reutern G-M, Hetzel A, Birnbaum D, Schlosser V: Transcranial Doppler ultrasonography during cardiopulmonary bypass in patients with severe ca rotid stenosis or occlusion. Stroke 19:674-680, 1988 Gomez CR, Lewis LM, Wade JB, Gomez SM, Stothert JC Jr, Kraus G, Hall IS: Transcranial Doppler moni toring of cardiopulmonary resuscitation: logistics of human and animal experimentation (abstract). In Proceedings of the 4th International Symposium on Intracranial Hemodynamics: Transcranial Doppler and Cerebral Blood Flow, Orlando, Florida, February 11 to 14, 1990, Bishop CCR, Powell S, Rutt D, Browse NL: Transcra nial Doppler measurement of middle cerebral artery blood flow velocity: a validation study. Stroke 17:913915, 1986 Dahl A, Russell D, Nyberg-Hansen R, Rootwelt K: Effect of nitroglycerin on cerebral circulation mea sured by transcranial Doppler and SPECT. Stroke 20:1733-1736, 1989 Aaslid R, Lindegaard K-F, Sorteberg W, Nornes H: Cerebral autoregulation dynamics in humans. Stroke 20:45-52, 1989 Droste DW, Harders AG, Rastogi E: A transcranial Doppler study of blood flow velocity in the middle cerebral arteries performed at rest and during mental activities. Stroke 20:1005-1011, 1989 Kontos HA: Validity of cerebral arterial blood flow calculations from velocity measurements. Stroke 20:1-3, 1989 Adams Rl, Aaslid R, el Gammal TE, Nichols FT, McKie V: Detection of cerebral vasculopathy in sickle cell disease using transcranial Doppler ultrasonogra phy and magnetic resonance imaging: case report. Stroke 19:518-520, 1988 Diener H-C, Peters C, Ruzio M, Reinhold H, Dichgans J: Transcranial Doppler sonography in migraine (abstract). In Proceedings of the 4th International Symposium on Intracranial Hemodynamics: Trans cranial Doppler and Cerebral Blood Flow, Orlando, Florida, February 11 to 14, 1990 Wong MCW, Haley EC Jr, Henry ML, Davis SS: A role for transcranial Doppler ultrasonography in iso lated cerebral vasculitis (poster presentation). Neu rology 40 (Suppl 1):434, 1990
GEORGE W. PETTY, M.D., DAVID O. WIEBERS, M.D., IRENE MEISSNER, M,D., Department of Neurology
Transcranial D o p p l e r u l t r a s o n o g r a p h y w a s i n t r o d u c e d i n 1982 a s a n o n i n v a s i v e p r o c e d u r e for a s s e s s m e n t o f t h e intracranial cerebral circulation. T h e l i g h t w e i g h t a n d portable e q u i p m e n t u s e d for transcranial D o p p l e r e x a m i n a t i o n facilitates its u s e in t h e b e d s i d e a s s e s s m e n t of critically ill h o s p i t a l i z e d p a t i e n t s a n d o u t p a t i e n t s . Clinical a p p l i c a t i o n s i n c l u d e t h e d i a g n o s i s o f v a s o s p a s m i n p a t i e n t s w i t h subarach n o i d h e m o r r h a g e , a s s e s s m e n t of intracranial collateral flow i n p a t i e n t s w i t h extra cranial arterial o c c l u s i v e d i s e a s e , d e t e c t i o n of intracranial arterial s t e n o s i s , identi fication of t h e f e e d i n g a r t e r i e s of a r t e r i o v e n o u s malformations a n d m o n i t o r i n g t h e h e m o d y n a m i c effects of t h e i r t r e a t m e n t , confirmation of t h e clinical d i a g n o s i s of brain d e a t h , i n t e n s i v e - c a r e u n i t m o n i t o r i n g of brain-injured p a t i e n t s , a n d intraop e r a t i v e a n d p o s t o p e r a t i v e m o n i t o r i n g of n e u r o s u r g i c a l p a t i e n t s . Transcranial Dop pler technology is also providing n e w insights into the pathophysiologic mechanisms of a variety of c e r e b r o v a s c u l a r c o n d i t i o n s . Clinicians will find transcranial Doppler t e c h n o l o g y m o s t helpful if t h e y h a v e a specific q u e s t i o n about t h e s t a t u s of t h e intracranial c i r c u l a t i o n . F u r t h e r i n v e s t i g a t i o n s m a y e x p a n d t h e clinical a n d re s e a r c h utility of t h i s t e c h n o l o g y .
Transcranial Doppler ultrasonography is a relatively n e w technology that allows noninvasive a s s e s s m e n t of the intracranial cerebral circulation. Since i t s introduction by Aaslid a n d colleagues' at t h e U n i v e r s i t y of Bern i n Switzerland, neurologists a n d neurosurgeons have found a variety of clinical a n d research applications for transcranial Doppler studies, including
diagnosing v a s o s p a s m in patients with aneurysmal subarachnoid hemorrhage, a s s e s s i n g intracranial collateral flow i n patients with extracranial arterial occlusive disease, detecti n g intracranial arterial stenosis, identifying t h e feeding arteries of arteriovenous malformations a n d monitoring t h e hemodynamic effects of their treatment, confirming t h e clinical diagnosis of brain death, intensive-care unit monitoring of brain-injured patients, a n d in-
Address reprint requests to Dr. G. W. Petty, Department of Neurology, Mayo Clinic, Rochester, MN 55905.
traoperative a n d postoperative monitoring of neurosurgical patients.
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DESCRIPTION OF TRANSCRANIAL DOPPLER TECHNOLOGY Transcranial Doppler technology allows mea s u r e m e n t of blood velocity in cerebral arteries at the base of the brain by m e a n s of ultrasound technology.''^ Current de'vices consist of a pulsed range-gated probe that e m i t s a 2-MHz ultra sonic signal focused by a plastic lens (Fig. 1). The 2-MHz signal u s e d in transcranial Doppler tech nology is s o m e w h a t lower in frequency t h a n that used in duplex ultrasound devices (7 to 10 MHz) and thereby achieves the greater t i s s u e penetra tion needed to i n s o n a t e t h e arteries of the circle of Willis deep within t h e cranial vault. The ultrasound signal is e m i t t e d from t h e probe with use of a piezoelectric material that converts electrical signals into ultrasound signals. This signal is t h e n reflected off the erythrocytes trav eling through the vessel being studied and re ceived by the s a m e probe. After reception, the piezoelectric material converts the ultrasound signals into electrical signals that are processed with u s e of real-time fast Fourier transforma tion by a microcomputer. Given the emitted signal frequency (2 MHz) and the m e a s u r e d frequency of the signal received from the eryth rocytes coursing through the arteries, the trans cranial Doppler equipment u s e s the Doppler shift principle to calculate the velocity of the blood flow. The spectral analysis of the velocities during the cardiac cycle is presented on a gray scale as a waveform, and current devices calcu late and present the m e a n velocity and also the pulsatility index (PI = [systolic velocity - dia stolic velocity j/mean velocity), an index of vascu lar resistance. In general, the pulsatility index is decreased in conditions t h a t result in de creased intracranial vascular resistance (com pensatory vasodilation ipsilateral to carotid stenosis or severe occlusion, arteriovenous mal formations) and increased in conditions that result in increased intracranial vascular resis tance (increased intracranial pressure, brain death). The direction of flow (away from or toward the probe) is also indicated (Fig. 2). Because the transcranial Doppler technology incorporates a range-gated pulsed ultrasound signal, instead of a continuous signal, the depth
TRANSCRANIAL DOPPLER ULTRASONOGRAPHY
MCA PCA BA \
~\
(M)l A * ^ A ( A , ) ;
C IA
Siphon Oph
V
1351
A
^
Fig. 1. Diagram of transcranial Doppler ultrasound win dows. Transtemporal approach (A and B) is used to in sonate middle cerebral artery stem [MCA (Mj)], A seg ment of anterior cerebral artery [ACA (A^)], distalmost segment of internal carotid artery siphon (ICA Siphon), and P, and P^ segments of posterior cerebral artery (PCA). Transorbital window (C) is used for insonation of ophthal mic artery (OphA) and immediately supraclinoid and infraclinoid segments of internal carotid artery siphon. Suboc cipital transcranial window (D) is used for insonation of distal intracranial segments of both vertebral arteries (VA) and basilar artery (BA).
of insonation can be adjusted by changing the time between the emission and the reception of the signal by the probe. ^ This feature allows insonation of all major arteries at the base of the brain, as well as a s s e s s m e n t of flow velocity at different points along their intracranial course (Fig. 2). The transcranial Doppler probe may not be positioned indiscriminately on the skull to re ceive signals. In fact, only three "transcranial windows" are commonly used to perform clinical studies (Fig. 1 and 2). The transtemporal win dow is used by placing the probe immediately above the zygomatic arch and directing the sig nal through the thin temporal bone in this re gion. Through the transtemporal approach, the M, s e g m e n t of the middle cerebral artery, the A, s e g m e n t of the anterior cerebral artery, and the distalmost s e g m e n t s of the internal carotid ar tery siphon can be insonated. By angling the probe slightly backward through the transtem poral window, the P, s e g m e n t and, in some cases, the P2 s e g m e n t of the posterior cerebral artery can also be evaluated. The transorbital window is used by placing the probe over the eye
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R ACA
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R ICA Siphon
lAllll^Willil^' LPCA
R MCA
W-^ 46
BA
kkkkl R VA
Fig. 2. Normal transcranial Doppler findings in asymptomatic 34-year-old man. Note augmentation of flow in left posterior cerebral artery (L PCA) during eye opening. Flow is directed away from probe in right anterior cerebral artery A, segment (Λ ACA), right vertebral artery (7? VA), and basilar artery (BA). P / = pulsatility index; Λ/CA = right internal carotid artery; R MCA = right middle cerebral artery.
and directing the signal through the orbit. In this fashion, signals can be detected from the ipsilateral ophthalmic artery, from s e g m e n t s of the ipsilateral internal carotid artery siphon (genu), and from the contralateral A, s e g m e n t of the anterior cerebral artery. The suboccipital window is used by placing the probe beneath the inion and directing the signal through the fora m e n m a g n u m . In this way, signals can be obtained from the distal intracranial s e g m e n t s of both vertebral arteries and from the basilar artery along its length. The velocity m e a s u r e d by the transcranial Doppler technique is a func tion of the cosine of the angle that the Doppler
signal m a k e s with the artery being studied. Therefore, accurate velocities are easily obtained from the Mj s e g m e n t of the middle cerebral ar tery because the angle of insonation approaches zero. As the branches of the middle cerebral artery begin to turn u p into the sylvian fissure and course over the surface of the brain, how ever, the angle of insonation becomes closer to 90 degrees, and the signal diminishes substan tially or disappears. Similarly, transcranial Doppler ultrasonography cannot a s s e s s flow velocity in the A2 s e g m e n t of t h e anterior cere bral artery because the blood flow in this artery is directed at right angles to the probe signal
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w h e n the transtemporal approach is used. For the proximal s e g m e n t s of the major arteries leading to or e m a n a t i n g from t h e circle of Willis, however, the angle of the ultrasound b e a m with the artery being insonated is usually small, and the m e a s u r e d velocity approaches the actual blood velocity (Fig. 2). Normal reference v a l u e s for velocities and standard deviations have been published for each artery."*"' The patient's age,®'' partial arterial pressure of carbon dioxide, and hematocrit* all affect the velocity and m u s t be considered w h e n studies are interpreted. Like all noninvasive technologies, transcra nial Doppler ultrasonography h a s some limita tions. The temporal transcranial window is absent on one or both sides in approximately 4 to 10% of patients; the result is nondiagnostic studies.^'" Absence of a technically adequate transtemporal window s e e m s more common in elderly persons, women, and blacks, perhaps be cause of differences in skull configuration, thick ness, and bone ossification.'° '' Performing trans cranial Doppler s t u d i e s requires considerable patience, practice, and skill in terms of locating the ultrasonic windows and establishing the identities of the arteries being assessed. The nu merous permutations of normal vascular anat omy and of pathologic conditions in the intracra nial arteries of patients with cerebrovascular disease make transcranial Doppler ultrasonogra phy a more physician-intensive technology t h a n oculoplethysmography or duplex Doppler stud ies, which are primarily u s e d to evaluate the s t a t u s of the carotid bifurcation. N e v e r t h e l e s s , a commercially available device u s e s a gantry with bilateral probes affixed to the patient's head, which can be u s e d to produce a threedimensional m a p of t h e intracranial circulation; t h u s , vessel identification and determination of collateral patterns are simplified. Currently, no commercially available duplex transcranial devices are available, although prototypes are being tested.'-' CLINICAL APPLICATIONS In addition to the obvious advantage of being noninvasive, transcranial Doppler ultrasonogra phy is performed with lightweight and portable
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equipment; therefore, bedside a s s e s s m e n t of critically ill hospitalized patients and also out patients is possible. Depending on the specific question posed by t h e clinician, transcranial Doppler studies can take from 3 0 to 60 m i n u t e s and can easily be repeated w h e n indicated (for example, in patients with subarachnoid hemor rhage who have vasospasm). The Therapeutics and Technology A s s e s s m e n t Subcommittee of the American Academy of Neurology''' recently published a position s t a t e m e n t a s s e s s i n g the clinical utility of transcranial Doppler ultra sonography. They determined appropriate clini cal situations in which transcranial Doppler t e s t i n g is of established value (Table 1). The point emphasized in the following discus sion is that transcranial Doppler ultrasonogra phy is useful w h e n the clinician h a s posed a specific question, such as one of the following: Does the patient with a subarachnoid hemor rhage and obtundation have vasospasm? Does t h e patient with a large deep infarction in the middle cerebral artery territory have evidence of middle cerebral stem stenosis? Does the patient with carotid occlusion have collateral flow either from the contralateral carotid system through the anterior communicating artery or from the posterior circulation? Can arrest of the cerebral circulation be substantiated in the patient who m e e t s the clinical criteria for cerebral death? H a s blood flow velocity decreased in the feeding arteries of the arteriovenous malformation after embolization or radiotherapy? Unlike oculoplethysmography and duplex Doppler technology, which are appropriate screening t e s t s for large numbers of patients with asymptomatic carotid stenosis, transient ischemic attack, or stroke, the clinician is un likely to find transcranial Doppler ultrasonogra phy to be of value w h e n it is used to "screen" all patients who have ischemic cerebrovascular disease.'® Transcranial Doppler studies are of clinical value w h e n the clinician h a s a specific question about the causative mechanism for a stroke or the collateral s t a t u s in the intracra nial circulation, which m a y influence the ap proach to m a n a g e m e n t and treatment of the patient.
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Table 1.—Established Clinical I n d i c a t i o n s for Transcranial D o p p l e r T e s t i n g
artery is detected with 86 to 88% sensitivity."*'' In patients in w h o m collateral flow had devel oped from t h e external carotid artery system through the ophthalmic artery to the carotid siphon, transcranial Doppler studies can detect reversal of flow in the homolateral ophthalmic artery with a sensitivity that approaches 100%," although a recent study in which transcranial Doppler technology w a s u s e d suggested that the presence of collateral flow from the external carotid circulation is probably not hemodynami cally significant and more likely represents chronically impaired perfusion to that hemi sphere.'® Monitoring t h e effect of compression of the common carotid artery on the waveforms in the ipsilateral middle cerebral artery stem or on the direction of flow in the ipsilateral A, segment of the anterior cerebral artery m a y provide fur ther information about the presence or the po tential for development of collateral flow, al though in patients with atherosclerotic vascular disease in t h e carotid system, such m a n e u v e r s m a y rarely cause transient ischemic attack or stroke and are not routinely performed in our laboratory. Transcranial Doppler ultrasonogra phy is also helpful in diagnosing subclavian steal p h e n o m e n a by detecting reversal of flow in the distal intracranial s e g m e n t of the vertebral artery ipsilateral to subclavian artery stenosis and, in some cases, reversal of flow in the basilar artery during part of the cardiac cycle.'^ Detection of Hemodynamically Signifi cant Intracranial Arterial Stenosis.—In s t a t e s of pathologic narrowing of arteries, the velocity of the blood flow increases in proportion to the decrease in the arterial luminal area. Therefore, pathologic increases in velocity facili tate transcranial Doppler detection of luminal narrowing in the intracranial arteries, whether due to atherosclerotic stenosis, recanalization or partial obstruction after embolization, or vaso s p a s m (Fig. 4, 5, and 6). In addition to increases in velocity, acoustical properties of the ultra sound signals from stenotic or vasospastic arter ies can be helpful in m a k i n g t h e s e diagnoses.^ Internal Carotid and Middle Cerebral A r t e r i e s . — W i t h use of the transorbital or transtemporal approach, hemodynamically signifi-
1. Assessment of patterns and extent of intracranial collateral circulation in patients with known regions of severe stenosis or occlusion in the internal carotid arteries, vertebral arteries, or subclavian arteries 2. Detection of hemodynamically significant stenosis in the major intracranial arteries at the base of the brain 3. Assessment and follow-up of patients with vasocon striction of any cause, especially vasospasm occurring after subarachnoid hemorrhage 4. Detection of arteriovenous malformations and study of their feeding arteries and the hemodynamic effects of treatment 5. Confirmation of the clinical diagnosis of brain death Modified from the American Academy of Neurology, Thera peutics and Technology Assessment Subcommittee.'''
Detection of Abnormal Collateral Flow.— Transcranial Doppler ultrasonography is a sen sitive and specific method for noninvasive detec tion of collateral flow in patients w i t h carotid artery occlusive disease. In patients with steno sis or occlusion of the internal carotid artery, collateral flow to the ipsilateral hemisphere m a y occur in a number of w a y s , most of which can be demonstrated w i t h transcranial Doppler tech niques. Figure 3 shows typical transcranial Doppler findings in such patients. Most com monly, hemodynamically significant collateral flow to the intracranial carotid territory above an occlusion in the internal carotid artery is accomplished by reversal of flow in the ipsi lateral Aj s e g m e n t of the anterior cerebral ar tery (collateral flow across the circle of Willis from the contralateral carotid s y s t e m through the anterior communicating artery) or a u g m e n tation of flow in the ipsilateral posterior cerebral artery (due to collateral flow through cortical anastomotic channels). Collateral flow from the contralateral internal carotid s y s t e m through the anterior communicating artery (reversal of flow in the ipsilateral Aj s e g m e n t of the anterior cerebral artery) is detected with approximately 94% sensitivity.'^'' Collateral flow from the posterior circulation either through the poste rior communicating artery or by augmentation of flow in the P, s e g m e n t of the posterior cerebral
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R ACA
si
RICA Siphon
Fig. 3. Transcranial Doppler findings in occlusion of right internal carotid artery. Velocities and pulsatility indices are substantially decreased in right distal internal carotid artery siphon {R ICA Siphon) and middle cerebral artery M, segment (R MCA). Collateral flow across circle of Willis is substantiated by the findings of augmented flow velocities in distal left internal carotid artery siphon (L ICA Siphon) and left; anterior cerebral artery A, segment (L ACA) contralateral to ICA occlusion, as well as reversal of flow in right ACA A, segment (R ACA) ipsilateral to ICA occlusion. Note that blood flow velocities are also augmented in right posterior cerebral artery Pj segment (R PCA); this finding suggests collateral flow from right PCA to right MCA territory through cortical anastomotic channels. L MCA = left middle cerebral artery; L PCA = left posterior cerebral artery.
cant stenosis or occlusion of the internal carotid artery siphon can be detected with a sensitivity of 73 to 94% by experienced clinicians.'"" Falsenegative studies m a y arise because transcranial Doppler technology cannot a s s e s s the siphon throughout its entire length but only in the immediately supraclinoid and infraclinoid seg m e n t s (through the transorbital approach) and in the distalmost s e g m e n t s (through the trans temporal approach). False-positive results m a y occur if the anterior communicating or the pos terior communicating artery is misidentified a s the siphon in situations in which collateral flow through t h e s e arteries is a u g m e n t e d because of
occlusive disease in the extracranial carotid ar t e r i e s . ' " " Hemodynamically significant steno sis or occlusion of the middle cerebral artery stem can be detected with 75 to 100% sensitiv i t y . ' * " " Such instances m a y also be accompa nied by augmentation of flow in the ipsilateral Aj s e g m e n t of the anterior cerebral artery.'^ Falsepositive diagnosis of occlusion of the middle cerebral artery can occur if the normal middle cerebral stem h a s an acute downward deflection early in its course (in which case the ultrasound signal may be lost) or if the transcranial window is so small that the probe m u s t be oriented such that the distal part of the middle cerebral stem
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cannot be insonated. In some instances of severe stenosis, the number of erythrocytes passing through the stenotic s e g m e n t may be so small that an adequate signal m a y not be received by the transcranial Doppler probe; the result would be a false-positive diagnosis of occlusion. Be cause transcranial Doppler ultrasonography cannot a s s e s s the distal s e g m e n t s of the middle cerebral artery, this technique is not sensitive for detecting middle cerebral artery branch oc clusion or stenosis beyond the M, segment. C a s e S t u d y . — 2 8 - y e a r - o l d woman taking oral contraceptives had sudden onset of rightsided headache, left hemiparesis, dysarthria, and right gaze preference. A computed tomo graphic scan of the head demonstrated an in farction of the right basal ganglia but no evi dence of hemorrhage. Oculoplethysmography showed normal findings bilaterally. Transcra nial Doppler examination, however, disclosed accelerated flow velocities in the distal right internal carotid artery siphon (Fig. 4 A) and proximal middle cerebral artery stem in com parison with normal signals received from the distal left internal carotid artery siphon (Fig. 4 B). Cerebral angiography (Fig. 4 C) demon strated a filling defect in the l u m e n of the distal right internal carotid artery and proximal middle cerebral artery stem, presumably due to embo lism. The proximal right carotid system w a s normal. An extensive evaluation for a cardiac source of embolus and a procoagulant state was unremarkable. She w a s treated first with hepa rin and t h e n warfarin, and use of oral contracep tives w a s discontinued. Vertebral a n d Basilar Arteries.—Hemo dynamically significant stenosis or occlusion in
Fig. 4. Transcranial Doppler demonstration of accelerated flow velocities in distal right internal carotid artery (ICA) siphon (A) and proximal middle cerebral artery (MCA) stem in a 28-year-old woman taking oral contraceptives who experienced sudden onset of left hemiparesis. Compare with normal signal received from lefl distal ICA siphon (B). Cerebral angiography (C) demonstrated a filling defect in lumen of distal right ICA and proximal MCA stem, pre sumably due to embolism. Proximal right carotid system was normal. PI = pulsatility index.
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Fig. 5. Transcranial Doppler demonstration of increased velocity and pulsatility index iPI) in left vertebral artery in a 77year-old man with bilateral posterior cerebral artery infarctions (A). Angiography demonstrated a long stenotic segment in left vertebral artery (B) that presumably resulted in "local embolism" to posterior cerebral arteries.
the distal intracranial s e g m e n t s of the vertebral arteries and in the basilar artery can also be demonstrated by transcranial Doppler ultra sonography, although the sensitivity and speci ficity m a y be s o m e w h a t l e s s t h a n for detecting stenotic lesions in the anterior circulation." Considerable patient-to-patient variation in the spatial configuration of the distal intracranial s e g m e n t s of the vertebral arteries and differ ences in neck thickness m a k e precise identifica tion of the vertebrobasilar junction difficult in m a n y instances. N e v e r t h e l e s s , for most clini cians, demonstration of stenosis in the distal vertebral arteries or in the basilar artery, re gardless of the precise location, would be suffi cient information for m a k i n g clinical decisions about selection of medical therapy. N e g a t i v e studies, however, m a y be l e s s helpful because the more proximal s e g m e n t s of the vertebral arteries cannot be a s s e s s e d with transcranial Doppler ultrasonography and can be a s s e s s e d only over short intervertebral s e g m e n t s with duplex Doppler technology. Furthermore, in i n s t a n c e s of occlusion of one of the vertebral arteries distal to the origin of the posterior inferior cerebellar artery, "runoff" into the pos
terior inferior cerebellar artery may result in false-negative examinations because of preser vation of relatively normal waveforms and blood flow velocities in the more proximal intracranial s e g m e n t s of the vertebral artery. C a s e S t u d y . — 7 7 - y e a r - o l d m a n had sudden onset of left hemianopia and gait ataxia. A computed tomographic scan o f t h e head demon strated a recent right occipital infarction and a presumably old left occipital infarction. An echocardiogram failed to disclose a cardiac source of embolus. Transcranial Doppler signals obtained at depths of 75 and 80 m m through the suboccipital approach demonstrated high ve locities, turbulence, and increased pulsatility indices (Fig. 5 A), which can be compared with normal vertebral and basilar waveforms and velocities in Figure 2. Angiography demon strated a long stenotic s e g m e n t in the left verte bral artery t h a t presumably resulted in "local embolism" to the posterior cerebral arteries (Fig. 5 B). Diagnosis of Vasospasm.—Perhaps the most common application of transcranial Dop pler ultrasonography is in the noninvasive de tection of arterial v a s o s p a s m after subarachnoid
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hemorrhage (Fig. 6). The highly portable and noninvasive characteristics of the technology m a k e it ideally suited for a s s e s s m e n t of critically ill patients in the intensive-care unit setting. Studies can be repeated at frequent intervals to a s s i s t in m a k i n g decisions about therapeutic m a n e u v e r s to prevent or treat vasospasm and the timing of surgical intervention. The rate of increase in blood flow velocity in vasospastic arteries s e e m s to correlate with the develop m e n t of delayed ischemic deficits in patients with subarachnoid hemorrhage.^'' In addition to clinical applications for diagnosing vasospasm in the setting of subarachnoid hemorrhage, transcranial Doppler technology h a s provided n e w insights into the time course of the develop m e n t of vasospasm^'^ and the effect of calcium antagonists on the severity of vasospasm.^** S p e c i f i c i t y a n d S e n s i t i v i t y . — T h e major clinical value of transcranial Doppler examina tion in diagnosing vasospasm after subarach noid hemorrhage is its high specificity (98 to 100%).^'·^" Therefore, w h e n transcranial Dop pler ultrasonography demonstrates vasospasm, the need for angiography may be obviated, and the clinician can confidently make decisions about treatment and timing of operation;^** however, caution should be exercised in relying on nega tive studies to make clinical decisions in this setting. As pointed out earlier, transcranial Doppler technology cannot be used to a s s e s s the anterior cerebral artery beyond its A^ s e g m e n t or to evaluate the distal branches of the middle cerebral a r t e r y . M o r e o v e r , in patients with poor clinical grades of subarachnoid hemorrhage with increased intracranial pressure, velocities m a y be globally reduced despite t h e presence of vasospasm. Consequently, the overall sensitiv-
Fig. 6. Transcranial Doppler detection of vasospasm in 35year-old man with subarachnoid hemorrhage. Transcra nial Doppler ultrasonography demonstrated considerably increased flow velocities and turbulence in right middle cerebral artery (MCA) stem (A) but only modest increases in velocities in left MCA stem (B). Angiography showed vasospasm in right MCA (C). Left carotid injections demon strated an aneurysm in anterior communicating artery. PI = pulsatility index.
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ity of transcranial Doppler studies in detecting v a s o s p a s m is low (33.3 to 58.6%),'^'* primarily because of the failure to detect s p a s m in the A2 s e g m e n t of the anterior cerebral artery and in the branches of t h e middle cerebral artery. Behavioral abnormalities in patients with ante rior cerebral artery v a s o s p a s m and ischemia m a k e examinations in t h e s e patients techni cally difficult and m a y contribute to the low sensitivity in this setting.'^ Further investiga tion is needed, however, to determine w h e t h e r different approaches to anterior cerebral artery insonation and examination of anterior cerebral artery pulsatility changes m a y increase the sensitivity of transcranial Doppler examinations in detecting v a s o s p a s m in t h i s artery. C a s e S t u d y . — 3 5 - y e a r - o l d m a n sought medical attention because of a severe headache and confusion. Cerebrospinal fluid examination disclosed a subarachnoid hemorrhage. A com puted tomographic scan of the head demon strated a large acute collection of subarachnoid blood in the middle right frontal lobe that ex tended posteriorly into the lamina terminalis and anteriorly into the third ventricle. Four days later, his level of consciousness slowly deteriorated, and he w a s transferred to our in stitution. Transcranial Doppler ultrasonogra phy revealed substantially increased flow ve locities and turbulence in the right middle cere bral artery s t e m consistent w i t h v a s o s p a s m (Fig. 6 A) but only modest increases in velocities in the left middle cerebral artery s t e m (Fig. 6 B). Angiography showed v a s o s p a s m of the right middle cerebral artery s t e m (Fig. 6 C). Left carotid injections demonstrated an a n e u r y s m in the anterior communicating artery. H e w a s in tubated and treated with volume expansion and nimodipine. His m e n t a l s t a t u s slowly improved, and the a n e u r y s m w a s clipped 12 days after the initial examination. Evaluation of Arteriovenous Malforma tions.—^Arteriovenous malformations are typ ically high-velocity, low-pressure, low-resistance arterial s h u n t s y s t e m s . These hemodynamic qualities result in the characteristic transcra nial Doppler findings of higher t h a n normal m e a n and peak blood flow velocities in conjunc
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tion with turbulence and lower than normal pulsatility indices (Fig. 7). By detecting charac teristic signal abnormalities, transcranial Dop pler studies can correctly diagnose arteriove nous malformations w i t h a sensitivity of 87 to 95%.''·^°·^' Small arteriovenous malformations that are located in the cortex and fed by single arterial branches m a y not be detected, however. Because magnetic resonance imaging probably affords an e v e n higher sensitivity t h a n transcra nial Doppler examination for diagnosing arte riovenous malformations, we do not routinely recommend transcranial Doppler testing for di agnostic purposes in patients suspected of hav ing t h e s e lesions. Nevertheless, transcranial Doppler ultrasonography is a convenient and re liable method for quantitatively evaluating the hemodynamic changes that occur in feeding and nonfeeding arteries of arteriovenous malforma tions after treatment (embolization, operation, or radiotherapy).'" After surgical treatment or embolization, transcranial Doppler studies con sistently and quantitatively substantiate in creases in the pulsatility index and decreases in the m e a n velocity in the feeding arteries of these lesions (Fig. 7).'" Such information m a y prove helpful in establishing therapeutic strategies and in determining the prognosis for individual patients. Moreover, depending on results of further investigation, the need for follow-up angiography m a y be obviated in some patients who have radiotherapy for these lesions. Confirmation ofthe Clinical Diagnosis of Cerebral Death.—The proliferation of organ transplantation programs and the high cost and maximal utilization of intensive-care unit treat m e n t have made the timely confirmation of cere bral death an important medical, legal, and economic issue. Most hospitals require confir mation of the clinical diagnosis of cerebral death, usually in the form of an electroencephalogram, before withdrawal of life support. Although widely accepted for this indication, electro encephalography h a s certain logistical disad v a n t a g e s because of the time required to per form and interpret the studies. Transcranial Doppler ultrasonography, which can be per formed within a few m i n u t e s at the bedside of a
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Fig. 7. Transcranial Doppler demonstration of hemodynamic changes after embolization of an arteriovenous malforma tion. A 16-year-old girl with a large arteriovenous malformation in cerebellar vermis fed by branches from basilar artery (A, preembolization angiogram) underwent superselective platinum coil embolization of feeding branches (B, postembolization angiogram). Preembolization transcranial Doppler study (C) demonstrated abnormally increased velocities and decreased pulsatility indices iPI) in proximal basilar artery (BA). After embolization, velocity in basilar artery decreased and pulsatility index increased (D). (From Petty and associates.''^ By permission of the American Heart Association, Inc.)
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critically ill or brain-dead patient, is a rapid and convenient alternative to the electroencephalo gram for confirming cerebral d e a t h . T h e typi cal transcranial Doppler waveform findings in patients with cerebral death are reversal of flow in diastole and a sharp systolic upstroke or small spike waveforms either above or both above and below the baseline at the beginning of systole (Fig. 8).^^·^^ Investigators have demon strated t h a t t h e s e waveform abnormalities oc cur a s the intracranial pressure increases above the cerebral perfusion pressure,^" in correlation with arrest of cerebral blood flow a s demon strated by radionuclide scanning techniques.'*'^ In a series of 54 comatose patients studied with transcranial Doppler ultrasonography, t h e waveforms were highly sensitive and specific for cerebral death (Fig. 8), as established by clinical and electroencephalographic criteria.'*^ Although H a s s l e r and associates'^'' have demon strated t h a t some patients with severely in creased intracranial pressure due to head trauma m a y rarely have this abnormal waveform with out m e e t i n g all the criteria for cerebral death, if the transcranial Doppler study is incorporat ed into institutional protocols and performed after patients m e e t the clinical criteria for cere bral death, false-positive results are unlikely to occur.'*^ POTENTIAL CLINICAL APPLICATIONS In addition to the foregoing clinical applications for transcranial Doppler ultrasonography, sev eral other applications are now being studied. Preoperative, intraoperative, and postoperative monitoring of neurosurgical patients is one po tential u s e of transcranial Doppler technology. For m a n y years, regional cerebral blood flow and electroencephalography have been u s e d to monitor patients during carotid endarterectomy and other revascularization procedures to iden tify patients at risk for postoperative ischemic deficits and those who m a y benefit from s h u n t placement after cross-clamping. Transcranial Doppler m e a s u r e m e n t s of the m e a n blood flow velocity in the middle cerebral artery have been used in attempts to identify such patients. Suppression of electroencephalographic activity
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h a s been correlated with low velocities in the middle cerebral artery.'*'*''' Studies in larger numbers of patients undergoing carotid endar terectomy m a y determine the sensitivity and specificity of transcranial Doppler ischemic ve locity thresholds in comparison with regional cerebral blood flow and electroencephalographic changes as well as clinical outcome. Transcra nial Doppler ultrasonography m a y also be useful in identifying patients in whom the postendarterectomy course is complicated by so-called h y p e r p e r f u s i o n syndromes."* Transcranial Doppler confirmation of impaired carbon diox ide-induced cerebral vasomotor response in patients with occlusion of the internal carotid artery m a y allow identification of subsets of patients with severely impaired hemispheric perfusion and decreased vasoreactivity who could benefit from extracranial-intracranial revascu larization procedures.'*^ •'° Transcranial Doppler technology m a y also be useful for studying the hemodynamic behavior of arteriovenous malfor mations intraoperatively and immediately post operatively and could be used to t e s t hypotheses about so-called perfusion breakthrough phenom ena after surgical resection.'" Further studies are also needed to determine w h a t role, if any, transcranial Doppler ultrasonography may have in monitoring patients with carotid stenosis or occlusion during cardiopulmonary bypass proce dures. One study suggested that the occurrence of postoperative neurologic deficits is unrelated to hypoperfusion of the cerebral circulation during such bypass procedures.''^ Transcranial Doppler studies might provide an ideal alternative to the current methods of monitoring intracranial pressure in patients with head injury, intracranial hemorrhage, brain tumor, or hypoxia.^'' Changes in the pulsatility and direction of transcranial Doppler waveforms during the cardiac cycle provide qualitative in formation about the intracranial pressure and the effect of increases in intracranial pressure on cerebral perfusion pressure. Quantitative correlations of transcranial Doppler pulsatility indices, waveforms, and velocities with actual intracranial pressure, however, are pending. Some investigators are currently attempting to
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Fig. 8. Transcranial Doppler confirmation of clinical diagnosis of cerebral death. Transcranial Doppler waveform abnormalities in brain-dead patients are characterized by either absent or reversed diastolic flow (A) or small early systolic spikes (B). These abnormalities correlate with arrest of cerebral circulation. L MCA and R MCA = left and right middle cerebral artery; PI = pulsatility index. (From Petty and associates.-^^ By permission of Edgell Communica tions, Inc.)
determine w h e t h e r transcranial Doppler exami C O N C L U S I O N nation m a y be useful during cardiopulmonary Although a relatively new technology, transcra resuscitation and in predicting the outcome of nial Doppler ultrasonography is an important tool for the a s s e s s m e n t of selected patients with cardiac arrest."*'^ Various research applications for transcra cerebrovascular disease. As with other noninva nial Doppler ultrasonography are also being sive techniques, the physician m u s t be familiar explored. Although transcranial Doppler mea with the capabilities and limitations of the trans surement of blood flow velocity in the middle cranial Doppler technology in order to make cerebral artery does not correlate well with clinical decisions based on test results. Clini hemispheric cerebral blood flow as m e a s u r e d by cians will find transcranial Doppler studies most the '-''Xe technique, a good correlation exists helpful if they have a specific question about the between changes in velocity and cerebral blood s t a t u s of the intracranial circulation. Clinically flow in response to changes in expiratory carbon useful applications have been established, and dioxide tension.'*'' Transcranial Doppler investi further investigations m a y expand the clinical gations of cerebral h e m o d y n a m i c changes in and research utility of this technology. response to physiologic and pharmacologic stim uli have been reported,'*® '*' although some con A C K N O W L E D G M E N T cern h a s been expressed about the validity of We thank Teresa J. Batzel, Gwen M. Harmon, using transcranial Doppler m e a s u r e m e n t of Cynthia L. Urban, and Sharon R. Ryg for their blood velocity as a surrogate for cerebral blood assistance in performing studies and preparing flow in certain instances.** Transcranial Dop the submitted manuscript. The transcranial pler studies m a y also provide n e w insights into Doppler studies depicted in the illustrations the pathophysiologic m e c h a n i s m s involved in were performed with u s e of an EME TC2-64B stroke occurring in patients with sickle-cell dis (Fig. 2 and 4 through 8) and an E M E Trans-scan ease,"*" migraine,®" cerebral vasculitis,®' and other (Fig. 3), Eden Medizinische Elektronik GmbH, conditions. Uberlingen, Germany.
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