(Stroke. 1995;26:96-100.)
© 1995 American Heart Association, Inc.
Articles |
Assessment of Cerebral Vasomotor Reactivity by Transcranial Doppler Ultrasound and Breath-Holding
A Comparison With Acetazolamide as Vasodilatory Stimulus
From the Department of Neurology (M.M., K.S.) and Institute of Neuroradiology (M.V., U.P.), University of the Saarland, Homburg/Saar, Germany.
Correspondence to Martin Müller, MD, Nervenklinik, Department of Neurology, University of the Saarland, Oscar-Orth-Str 3, D-66421 Homburg/Saar, Germany.
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Abstract |
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 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
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Background and Purpose Evaluating cerebrovascular vasomotor reactivity seems to be of prognostic relevance for patients with occlusive internal carotid artery disease. To evaluate its clinical usefulness, the recently introduced breath-holding maneuver as a carbon dioxide–dependent vasodilatory stimulus was compared with the acetazolamide challenge by means of transcranial Doppler ultrasound and stable xenon-enhanced computed tomography.
Methods In a total of 134 middle cerebral arteries of 74 patients (mean±SD age, 62±9 years) with unilateral or bilateral occlusive carotid artery disease, vasomotor reactivity was estimated by the increase of middle cerebral artery mean blood velocity by transcranial Doppler ultrasound, comparing the breath-holding maneuver and 1 g IV acetazolamide as vasodilatory stimuli. The carotid artery findings were classified as normal, stenosis of 50% to <70%, 70% to <90%, 90% to 99%, and occlusion. Eighteen of the 74 patients additionally underwent stable xenon-enhanced computed tomography to calculate the increase of mean cortical regional cerebral blood flow in the middle cerebral artery territory after acetazolamide stimulation.
Results The percentage of mean regional cerebral blood flow
changes (n=36 hemispheres) correlated best with the absolute mean
blood velocity changes while breath-holding (P=.007,
r=.4332). The absolute mean regional cerebral blood flow
changes correlated best with the percentage of mean blood velocity
changes after acetazolamide stimulation (P=.004,
r=.4580). On all 134 middle cerebral arteries, both
vasodilatory stimuli correlated highly significantly
(P<.0001) when comparing increases in absolute
(r=.5448) or relative (r=.3516) mean blood
velocity. Both stimulation techniques similarly indicated significantly
reduced vasomotor reactivity with increasing degree of internal carotid
artery lesions (P
.01). However, the acetazolamide
challenge differentiated more accurately between the various groups of
internal carotid artery findings.
Conclusions The assessment of vasomotor reactivity by transcranial Doppler ultrasound correlates with cerebral blood flow changes even when different vasodilatory stimuli are used. In cooperative patients the breath-holding maneuver as vasodilatory stimulus seems clinically useful for a first estimation of cerebral vasomotor reactivity.
Key Words: autoregulation • cerebrovascular disorders • cerebral blood flow • carotid artery diseases • vasomotor reactivity
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Severe occlusive carotid artery disease may produce embolic or hemodynamic hemispheric brain infarction.1 2 While the risk of an embolic infarct increases with the degree of carotid stenosis,3 the hemodynamic risk correlates less well with the degree of stenosis because of the functional capacity of the collateral pathways.4 When cranial perfusion pressure is reduced, the cerebral resistance vessels compensatorily vasodilate (cerebrovascular autoregulation). In the condition of compensatorily maximal dilated cerebral arterioles, an additional vasodilatory stimulus will not increase cerebral blood flow (CBF) further.
The compensatory response of the cerebral autoregulation can be assessed by imaging of regional CBF (rCBF) and cerebral blood volume by means of positron emission tomography and single-photon emission computed tomography (SPECT).2 5 6 7 Positron emission tomography provides additional information by measuring oxygen extraction fraction and metabolism. Other methods such as stable xenon-enhanced computed tomography (Xe-CT)8 9 or SPECT-related emission (clearance) techniques, which use as tracer either 133Xe or 99mTc-labeled hexamethylpropyleneamine oxime, respectively,10 11 12 13 14 15 16 17 or transcranial Doppler ultrasound (TCD)18 19 20 21 22 23 use CO2 or acetazolamide to stimulate cerebral vasodilation. Vasomotor reactivity (VMR) is then calculated from the CBF or blood velocity change. The evaluation of the cerebral hemodynamic response by the aforementioned methods is expensive and time-consuming with the exception of measuring blood velocity changes by TCD. When investigating VMR by TCD, the vasodilatory response to CO2 is comparable to the acetazolamide response.24 To evaluate VMR by the TCD CO2 test, hypercapnia is induced by adding CO2 to the inspired air via an anesthetic mask18 19 23 or by the breath-holding maneuver.21 25 VMR is then calculated either from the blood velocity changes in the hypercapnic condition only21 23 or from the full range of velocity changes in the hypercapnic and hypocapnic (hyperventilation) condition.18 19 Markus and Harrison21 found a good correlation between VMR calculated by the breath-holding method and VMR calculated either by the hypercapnic response only or by the combined response to both hypercapnia and hypocapnia. The aim of our study was to correlate the breath-holding method with other methods of assessing VMR that are independent of CO2. We used for our study blood velocity recorded by TCD and measured the CBF by stable Xe-CT, with acetazolamide as the vasodilatory stimulus.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Of the patients referred to our neurovascular laboratory for carotid artery screening by ultrasound, we prospectively enrolled into the study 74 consecutive patients (62 men, 12 women; mean±SD age, 62±9 years; range, 25 to 81 years) with occlusive carotid artery disease who fulfilled the following criteria: (1) unilateral or bilateral stenosis of
50% or occlusion of the internal carotid
artery (ICA); the degree of the stenosis was determined by
continuous-wave Doppler ultrasound (SPEAD 6, Spead Electronique, 4-MHz
probe) with use of published criteria,26 and cerebral
angiography was performed to confirm ICA occlusion; (2) adequate
temporal "bone window" for sufficient TCD examination, and in the
condition of bilateral occlusive ICA disease identification of an
adequate bone window on at least one side; and (3) exclusion of
additional intracranial stenosis of the carotid siphon or the middle
cerebral artery (MCA) and anterior cerebral artery by TCD or
angiography.
By continuous-wave Doppler the extracranial findings for each ICA were
classified as follows: normal (group 1), stenosis of 50% to <70%
(group 2), 70% to <90% (group 3), 90% to 99% (group 4), and
occlusion (group 5). The angiographic results were considered to
distinguish between groups 4 and 5 because continuous-wave Doppler
cannot always accurately differentiate between occlusion and stenoses
of 95%. The vertebral arteries were also insonated by
continuous-wave Doppler at the atlantal slope and its aortic origin,
but the vertebral artery findings were not taken into consideration for
this study. A cranial CT was performed in patients with a transient or
completed neurological syndrome as well as in patients designated for
cerebral angiography.
TCD Examination
The TCD examinations (EME TC 2-64, EME, 2-MHz pulsed handheld
probe) included the transtemporal insonation of the MCA, the anterior
carotid artery, and the carotid siphon to exclude additional
intracranial stenosis of a vessel supplied by the ICA. For technical
details of TCD and the identification of the intracranial arteries, see
previous reports.27 28 29 For the measurements of blood
velocities, the most powerful signal at the highest mean blood velocity
level that has been recorded constantly during a period of 10 cardiac
cycles was used.
The breath-holding maneuver (TCD breath-holding test) was performed according to the procedure of Markus and Harrison21 : after normal breathing of room air for approximately 4 minutes, the patients were instructed to hold their breath after a normal inspiration. During the maneuver the MCA mean blood velocity was recorded continuously. The mean blood velocity at the TCD display immediately after the end of the breath-holding period was registered as the maximal increase of the MCA mean blood velocity (while breath-holding). The time of breath-holding was also registered. This procedure was repeated after a rest of 2 to 3 minutes to allow the mean blood velocities to return to their initial values. For the maximal MCA mean blood velocity increase and for the time of breath-holding, the mean values of both trials were taken. The breath-holding index (BHI) was calculated from these data as percent increase in MCA mean blood velocity recorded by breath-holding divided by seconds of breath-holding ([Vbh-Vr/Vr] · 100 · s-1), where Vbh is MCA mean blood velocity at the end of breath-holding, Vr the MCA mean blood velocity at rest, and s-1 per second of breath-holding.
Approximately 5 minutes after the last blood velocity measurements of the breath-holding test the mean blood velocity in the MCA was recorded again as a resting value before acet- azolamide stimulation was induced by administration of 1 g IV acetazolamide over 5 minutes (TCD acetazolamide test). Acetazolamide is a potent vasodilator of cerebral resistance vessels, leading to a smooth increase of blood velocity with plateauing of blood velocity after 10 to 15 minutes.20 30 Fifteen minutes after the injection of acetazolamide, the mean blood velocities were measured again with the ultrasound sample volume in the same depth of the MCA compared with the resting examination, again measuring the highest mean blood velocity that could have been recorded constantly during a period of 10 seconds. The percent VMR after acetazolamide stimulation (%VMRacet) was calculated as percent change in MCA mean blood velocity after stimulus application compared with mean blood velocity at rest ([Vacet-Vr/Vr] · 100), where Vacet is the maximal increase of the MCA mean blood velocity after acetazolamide application and Vr the mean blood velocity at rest.
Stable Xe-CT Examination
All Xe-CT CBF studies were performed on a GE 9800 CT scanner
(General Electric) in combination with a commercially available xenon
hardware and software system (Diversified Diagnostic Products). The
patients inhaled 30% stable xenon gas and 25% oxygen over 4 to 5
minutes. Exposure technique at 80 kV and 120 mA, 10-mm slice thickness,
exposure time of 4 seconds, and a 512x512 matrix were used in all
studies. For a two-level study 16 xenon-enhanced scans were performed
for CBF calculation. In all studies two levels over the region of the
basal ganglia before and after administration of 1 g IV acet- azolamide
were investigated. The total time afforded to both studies was
approximately 1 hour for each patient, including a break of 30 minutes
between the baseline study and the acetazolamide study, which started
15 minutes after the administration of acetazolamide. During the study
blood pressure, arterial oxygen saturation, end-tidal xenon and
CO2 concentrations, and heart and respiratory rates were
monitored by a medical observer. To calculate the CBF, 10 regions of
interest (ROIs), 6 of which represented the MCA territory, were
installed cortically over each hemisphere at each level. The mean
cortical rCBF of each MCA territory was calculated by summing the CBF
values of the 6 ROIs that represented the MCA territory divided by
the number of ROIs. The mean cortical MCA rCBF increase was calculated
as the difference between the baseline and the acetazolamide
studies.
Statistical Analysis
All values are given as mean±SD. To compare the BHI and the
%VMRacet in the subgroups defined by the ICA findings, the ANOVA
procedure was used on all subgroups. The ability of both TCD methods to
differentiate between the groups of ICA findings was analyzed by
one-way ANOVA for multiple comparisons (Scheffé's test; a value
of P=.05 was considered significant). The same analysis
was also used to compare asymptomatic hemispheres with symptomatic
hemispheres. A multivariate analysis to analyze whether VMR depends
on both the ICA findings and the clinical subgroup
(symptomatic/asymptomatic) could not be performed because of empty
categories that resulted from the small number of symptomatic
hemispheres. Therefore, a stepwise regression analysis on all
symptomatic hemispheres was used to evaluate the effects of the ICA
findings and of the presence or absence of the clinical syndrome on VMR
parameters. Blood velocity changes by the TCD breath-holding test were
compared with changes of blood velocity or of CBF after acetazolamide
by linear regression analysis and Pearson correlation coefficients
to estimate the agreement of the different techniques. Finally, the BHI
and the %VMRacet were compared with respect to their ability to
reclassify patients into their groups of ICA lesions by separate linear
discriminant analysis. Their joint classification properties were
not considered for examination.
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Both VMR tests were performed in all 74 patients, starting with the TCD breath-holding test. Sixty of the 74 patients could be examined bilaterally; 14 patients had a suitable temporal bone window that was unilateral. Thus, a total of 134 MCAs (hemispheres) were investigated. Occlusive carotid artery disease was unilateral in 39 and bilateral in 35 of the 74 patients. With respect to the classification of groups 1 through 5, group 1 consisted of 39 hemispheres, group 2 of 23, group 3 of 43, group 4 of 7, and group 5 of 22.
Additionally, 18 of the 74 patients (14 men, 4 women; mean±SD age, 64±8 years) underwent stable Xe-CT investigation after having been examined by TCD bilaterally 1 to 7 days before the Xe-CT examination.
Forty-seven of the 74 patients were asymptomatic (107 asymptomatic hemispheres) by both history and actual clinical findings. With respect to the ICA findings, the asymptomatic group consisted of the following: group 1, n=35 (33%); group 2, n=23 (21%); group 3, n=34 (32%); group 4, n=3 (3%); and group 5, n=12 (11%). Twenty-seven patients had experienced ischemic symptoms unilaterally (transient ischemic attack in 6, minor stroke in 14, major stroke in 6, and amaurosis fugax attack in 1). With the exception of three events, all ischemic events had occurred within 3 months before the actual investigations. In the symptomatic group the ICA findings were distributed as follows: group 1, n=4 (15%); group 2, n=1 (4%); group 3, n=8 (30%); group 4, n=4 (15%); and group 5, n=10 (37%). The BHI and the %VMRacet were significantly reduced in the 20 hemispheres with a major or minor stroke (BHI, .68±.34; %VMRacet, 32±27%) compared with asymptomatic hemispheres (BHI, .89±.34; %VMRacet, 51±21%; P<.05) and hemispheres with a transient deficit. By stepwise regression analysis the reduced VMR in the symptomatic hemispheres was significantly related to the ICA findings (P<.01) but was insignificantly related to the presence of the clinical syndrome.
By regression analysis between the acetazolamide challenge and the
breath-holding stimulation on all 134 hemispheres, the Pearson
correlation coefficient r was .5448 (P<.0001)
for the absolute increase and .3516 (P<.001) for the
percent increase of mean blood velocities. The results for the absolute
and percent increase of mean blood velocities and rCBF in those
hemispheres as investigated by all three methods are reported in Table 1
. For both the absolute and the percent changes the TCD
acetazolamide test correlated slightly better with the rCBF changes
than the TCD breath-holding test. The best regression analysis
results were found for the absolute mean blood velocity increase by the
TCD breath-holding test with the percent MCA rCBF increase
(r=.4332, P=.007) and for the %VMRacet with the
absolute MCA rCBF increase (r=.4580, P=.004).
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The mean %VMRacet and the mean BHI for each group of ICA findings
irrespective of the contralateral ICA findings are given in the
Figure. Both the mean BHI and the mean %VMRacet
significantly decreased with increasing degree of the carotid artery
lesion (P.01). There was no significant difference between
the VMR results in the different groups of ICA findings when comparing
the groups of ICA findings separately with respect to the presence of
unilateral or bilateral ICA disease (P>.10).
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Comparing the TCD breath-holding test with the TCD acetazolamide test regarding their ability to differentiate between groups 1 through 5 by Scheffé's test for multiple comparisons, groups 1 and 2 were significantly (P<.05) differentiated from groups 4 and 5 by the TCD acetazolamide test, whereas the BHI failed to differentiate between any of the groups.
The ability of both VMR tests to correctly reclassify the hemispheres
into the subgroups of ICA lesions was demonstrated by linear
discriminant analysis (Table 2). The differences
were only marginal, but the TCD acet- azolamide test reclassified
slightly more accurately normal hemispheres and those distal to an
occlusion of the ICA.
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Patients with occlusive carotid artery disease can suffer from cerebral ischemia caused either by arterioarterial embolism, leading to territorial infarcts, or by hemodynamic low-flow conditions, leading to infarcts characteristically located at the frontoparasagittal border zone between the MCA and the anterior cerebral artery or the temporoparieto-occipital watershed area between the MCA, the anterior cerebral artery, and the posterior cerebral artery. Additionally, small hemodynamic infarcts are found in the terminal supply areas of the large deep perforating arteries.1 2 31 32 Prognostically, it is not yet clearly established whether a severely compromised hemodynamic state of the cerebral vasculature in patients with hemodynamically symptomatic occlusion of the ICA is2 9 33 or is not4 34 associated with a high rate of future ipsilateral stroke.
In comparing the techniques we used to evaluate VMR, we must consider differences in the patients' comfort and level of cooperation as well as the methodical procedures. In our study the time of the procedures was similar (30 minutes) for the TCD acetazolamide test and the TCD breath-holding test investigating both hemipheres in each patient, while the Xe-CT test took 1 hour. The breath-holding maneuver was without side effects, but the procedure had to be explained repeatedly to some patients to achieve the desired level of cooperation. The TCD acetazolamide test does not depend on the patients' cooperation but involves some slight and completely reversible side effects such as dizziness, slight headache, and dysesthesia (perioral or at the fingertips, usually persisting for not more than 30 minutes). The xenon by itself can alter the sensorium of the patients and provoke unsteadiness, vertigo, vomiting, dizziness, or respiratory depression35 ; the risk involved in respiratory depression might necessitate termination of the study. Therefore, with respect to the clinical management of patients with occlusive carotid artery disease, the evaluation of VMR by TCD seems to be the more practical screening method. However, with TCD one has to bear in mind that the angle of insonation of an artery is unknown and may vary in repeated insonations of the same artery,36 thus providing uncertainties for calculating relative blood velocity increases. Acetazolamide by itself may have some disadvantages, such as a suggested direct narrowing of the basal arteries37 or the rare reports of false-positive and false-negative results in the evaluation of VMR.16 38 Although xenon by itself can elevate the mean blood velocity recorded by TCD,39 the accuracy of the CBF measurements does not seem to be markedly influenced by this xenon effect.40 Estimating VMR by TCD correlates with CBF imaging techniques when comparing the relative increase of mean blood velocity with the relative increase of CBF after administration of a vasodilatory stimulus.16 41 But, as in other studies,16 24 41 42 one has to consider the large variance between the measurements of reactivity by the three different methods.
With respect to the aforementioned considerations, the TCD breath-holding test is most attractive, having additionally been shown to be as reliable as the other TCD CO2 tests by adding CO2 to the inspired air and calculating VMR either from the hypercapnic condition only or from the full range between hypercapnia and hypocapnia. In a previous study24 the latter TCD CO2 tests correlated well with VMR evaluated by the TCD acetazolamide test and, as in our study, the TCD acetazolamide test differentiated more accurately between those different groups of high-grade stenoses and occlusions of the ICA for which the hemodynamic compromise is considered most relevant. Also, for correct reclassification of the ICA findings, again the TCD acetazolamide test was slightly superior to the TCD breath-holding test when reclassifying high-grade ICA stenoses (groups 3 and 4) and ICA occlusions correctly. Overall, however, there are only slight differences between the CO2-dependent and the acetazolamide-dependent TCD methods.
Surprisingly, both TCD methods could not differentiate between ICA
stenosis <70% and ICA stenosis 70% to <90%. This result
indicates that the collateral supply was hemodynamically sufficient
with increasing narrowing of the ICA. Because most of our patients were
asymptomatic patients with stable cerebrovascular conditions, a
possible effect of patient selection has to be considered to interpret
this result. In conclusion, the TCD breath-holding test correlates well
with rCBF changes and is comparable to the TCD acetazolamide test.
Therefore, it seems to be a useful first step to evaluate cerebral
VMR.
Received May 30, 1994; revision received October 7, 1994; accepted October 7, 1994.
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 J. F. Soustiel, E. Levy, M. Zaaroor, R. Bibi, S. Lukaschuk, and D. Manor A New Angle-Independent Doppler Ultrasonic Device for Assessment of Blood Flow Volume in the Extracranial Internal Carotid Artery J. Ultrasound Med., December 1, 2002; 21(12): 1405 - 1412. [Abstract] [Full Text] [PDF]
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 T. J. Tegos, E. Kalodiki, S.-S. Daskalopoulou, and A. N. Nicolaides Stroke: Epidemiology, Clinical Picture, and Risk Factors: Part I of III Angiology, October 1, 2000; 51(10): 793 - 808. [Abstract] [PDF]
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A. Kastrup, T.-Q. Li, A. Takahashi, G. H. Glover, and M. E. Moseley Functional Magnetic Resonance Imaging of Regional Cerebral Blood Oxygenation Changes During Breath Holding Stroke, December 1, 1998; 29(12): 2641 - 2645. [Abstract] [Full Text] [PDF]
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S. Dallinger, B. Bobr, O. Findl, H.-G. Eichler, and L. Schmetterer Effects of Acetazolamide on Choroidal Blood Flow Stroke, May 1, 1998; 29(5): 997 - 1001. [Abstract] [Full Text] [PDF]
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G. H. Visser, A. C. van Huffelen, G. H. Wieneke, and B. C. Eikelboom Bilateral Increase in CO2 Reactivity After Unilateral Carotid Endarterectomy Stroke, May 1, 1997; 28(5): 899 - 905. [Abstract] [Full Text]
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M. Silvestrini, E. Troisi, M. Matteis, L. M. Cupini, and C. Caltagirone Transcranial Doppler Assessment of Cerebrovascular Reactivity in Symptomatic and Asymptomatic Severe Carotid Stenosis Stroke, November 1, 1996; 27(11): 1970 - 1973. [Abstract] [Full Text]
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M. Muller and K. Schimrigk Vasomotor Reactivity and Pattern of Collateral Blood Flow in Severe Occlusive Carotid Artery Disease Stroke, February 1, 1996; 27(2): 296 - 299. [Abstract] [Full Text]
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