(Stroke. 1999;30:1450-1455.)
© 1999 American Heart Association, Inc.
Original Contributions |
From the Department of Vascular Surgery, Academic Medical Center, Amsterdam, the Netherlands. Correspondence to Dr. D.A. Legemate, Department of Vascular Surgery, G4-107, Academic Medical Center, Meibergdreef 9, 1105 AZ Amsterdam, Netherlands.
| Abstract |
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MethodsIn 112 atherosclerotic white patients >60 years of age, the anterior, middle, and posterior cerebral arteries and the vertebral and basilar arteries were insonated.
ResultsIn men, 99% of the temporal and 94% of the suboccipital windows could be penetrated by ultrasound compared with 77% and 95%, respectively, in women. The male versus female vessel detection rates were 91% versus 58% for the anterior cerebral artery, 97% versus 73% for the middle cerebral artery, 97% versus 68% for the posterior cerebral artery, 94% versus 93% for the vertebral artery, and 91% versus 79% for the basilar artery. In 77% of men but only 33% of women could all vascular segments be investigated. All intracranial arteries were insonated at a deeper level in men. The women showed significantly higher blood flow velocities than the men.
ConclusionsIn elderly white men the vessel detection rate is >90%. In women there is a much lower detection rate, due to impenetrable temporal windows. Visualization of all major intracranial arteries is possible in only one third of female patients >60 years of age.
Key Words: cerebral arteries cerebral blood flow diagnostic imaging ultrasonography
| Introduction |
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As clinically important cerebrovascular disease is found mainly in
elderly atherosclerotic patients, TCCD may well have the highest
potential diagnostic benefits in these patients. However,
the success rate of TCCD regarding visualization and adequate
Doppler examination of the basal cerebral arteries of the circle of
Willis (Figure 1
) in these patients is
largely unknown. Our goal was to assess the success rate of TCCD in the
examination of the basal cerebral arteries in atherosclerotic vascular
patients >60 years of age. A set of reference data of blood flow
velocities for this particular patient group is provided, and
differences between men and women are analyzed with respect to
the success rate of visualization, insonation depths, and blood flow
velocities.
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| Subjects and Methods |
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Technique
TCCD was performed with a 2.0- to 2.5-MHz phased-array
probe (Hewlett-Packard Sonos 2000). Examinations of the main trunk
of the middle cerebral artery (M1), the precommunicating part of
the anterior cerebral artery (A1), the precommunicating part of the
posterior cerebral artery (P1), and the postcommunicating part of the
posterior cerebral artery (P2) through the temporal window (Figure 2
) and of the vertebral arteries (VAs)
and basilar artery (BA) through the suboccipital window (Figure 3
) were performed in a standard manner,
details of which are reported elsewhere.13 14 15 Although in
case of unilateral temporal window failure it is sometimes possible to
insonate the M1, A1, and P1 through the contralateral temporal window,
this was not attempted. Common carotid artery compression tests to
assess the physiological presence of the anterior
and posterior communicating arteries were not performed.
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Blood flow velocity measurements were taken with the sample volume set as narrowly as possible and with the vector of the cursor positioned in the center of the bloodstream, parallel to the vessel axis. The angle of insonation was always <60°. An examination was considered adequate if the designated vessel could be visualized by color flow and a representative Doppler signal could be obtained on spectral analysis for the calculation of the peak systolic velocity (PSV), mean velocity (MV), end-diastolic velocity (EDV), and the pulsatility index (PI). The mean blood flow velocity is defined as the time-averaged maximum velocity during the cardiac cycle computed from the envelope of the Doppler spectrum. The PI is defined as (PSV-EDV)/MV. To avoid the influence of stenosis of the extracranial brain-supplying arteries on intracranial blood flow velocities, velocity data of patients with stenoses of >50% or occlusions of the internal carotid and/or vertebral arteries were not included in the analysis. The origins of the extracranial VAs were not routinely examined.
Statistical Analysis
Statistical Package for the Social Sciences (SPSS
8.0; SPSS Inc) for Windows was used to analyze the results of
the study. Comparison of the differing rates of arterial
segment detection between the male and female groups was carried out
using the
2 test. Blood flow velocity in the
cerebral arteries was found to be normally distributed and is therefore
expressed as mean ±2SD. Mean insonation depths and their ranges were
also calculated. Comparison of velocity data and insonation depth was
performed using nonpaired t tests. Significance was assumed
at the 5% level.
| Results |
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All intracranial arteries were insonated at a deeper level in the
cranium in men than in women (Table 2
). The vertebrobasilar
arteries in particular were insonated at a deeper level in men, which
is presumably a reflection of the larger size of the male neck. As a
consequence of impenetrable bone windows and because of the exclusion
of patients with significant carotid and/or vertebrobasilar
stenosis, the velocity data of 72 patients (46 men and 26
women) remained to be analyzed. Overall arterial
blood flow velocity was not found to be significantly higher in either
the left or the right cerebral hemisphere. Therefore, to investigate
the influence of gender on blood flow velocity in the basal cerebral
arteries, the results from the left- and right-side studies were
combined and averaged. Blood flow velocity was higher in the anterior
(A1, M1) than in the posterior (VA, BA, P1, P2) cerebral circulation,
and the velocity in women was significantly higher than that in men,
with the exception of the P2. The PIs did not significantly
differ between men and women (Table 2
).
| Discussion |
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Because patients with transient ischemic attack or stroke were not included in this study, we do not think that insonation failure was caused by occlusion of intracranial vessels. The most probable explanation for temporal window failure is hyperostosis of the temporal bone, which is influenced by age, gender, and race.7 8 9 19 A likely explanation for not obtaining signals despite a penetrable acoustic window is severe hypoplasia or aplasia of basal cerebral arteries, which is not uncommon.20 21 22 Aplasia of the M1 or BA is extremely rare, but aplasia or hypoplasia of the A1 or VA, for example, is found in 1% to 4% and 5% of subjects, respectively.23 24 In the male patients we studied, this might explain the slightly worse detection rate of the A1 compared with the M1, P1, or P2.
The suboccipital window was found to be unsuitable in 6% of men and 5% of women in this study. Marinoni et al12 used conventional transcranial Doppler on 624 patients and found an 11.2% and 5.7% absence of suboccipital windows in men and women, respectively. They attributed this difference to the increased attenuation of the ultrasound beam caused by the larger and thicker tendons of males. In this study, detection of the VAs was equally successful, but the identification rate of the basilar artery was lower in women than in men. We assume that this difference is caused by short, stiff, arthrotic necks in elderly women, preventing adequate flexion of the head needed to insonate the deep-set basilar artery. Another reason could be the smaller cross-sectional area of the foramen magnum in females.25
Little has been published about cerebral blood flow velocities in
elderly atherosclerotic subjects with no neurological deficits. On
comparison with TCCD17 18 and conventional
transcranial Doppler studies26 27 28 29 in
healthy volunteers of the same age, we found blood flow velocities to
be 10 to 20% higher. Owing to the precise positioning of the sample
volume and assessment of the angle of insonation, TCCD provides
velocity values that are closer to the true values than those derived
with conventional transcranial
Doppler.30 31 32 33 Vascular narrowing of the cerebral
arteries due to general atherosclerosis in our patients
might also explain why we found higher velocities than those in the
comparable studies of Martin et al17 and Baumgartner et
al.18 Another reason might be compensatory vasodilatation
of the brain tissue as a pathophysiological
mechanism in atherosclerotic patients. Finally, technical differences
between the ultrasound devices and their instrumentation should also be
mentioned as a possible factor. The large SDs in the mean intracranial
blood flow velocities found in this study and by other
researchers17 18 26 27 28 29 show that a broad range of
velocities can still be considered normal (Table 2
). This is
important for all investigators of cerebral
hemodynamics and especially for those who use velocity
criteria for the definition of intracranial arterial
stenoses or detection of collateral flow. Interindividually
different diameters of the basal cerebral arteries34 are
probably the most important cause of the broad range of velocities,
because flow velocity is inversely related to vessel diameter. Another
cause is the inverse association between velocity and both hematocrit
and fibrinogen concentrations, which explains 29% of the variance in
mean velocity.29 Most transcranial ultrasound
studies in healthy volunteers report higher velocities in women than in
men.17 18 28 35 36 37 However, Martin et al17
and Vriens et al28 reported that this difference
disappeared in elderly subjects.
In summary, our data show that in white men >60 years of age, TCCD is very successful, with vessel identification rates exceeding 90%. In white women of the same age there is a much higher failure rate, due to impenetrable temporal windows. Visualization of all major intracranial vascular segments is possible in only one third of women >60 years. Investigators of cerebral hemodynamics have to take into account that in subjects without cerebrovascular disease a broad range of intracranial blood flow velocities exists and that intracranial blood flow velocities are higher in women than in men. One answer to the problem of impenetrable temporal windows might be provided by ultrasound contrast-enhancing agents.38 39 40 The use of these relatively expensive agents, however, is of limited value in elderly men, because the vessel detection success rate in this group is already >90%.
| Acknowledgments |
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Received January 25, 1999; revision received March 25, 1999; accepted April 20, 1999.
| References |
|---|
|
|
|---|
2. Baumgartner RW, Mattle HP, Kothbauer K, Schroth G. Transcranial color-coded duplex sonography in cerebral aneurysms. Stroke. 1994;25:24292434.[Abstract]
3. Martin PJ, Gaunt ME, Naylor AR, Bell PRF. Diagnosis of intracranial occlusive disease: preliminary experience with transcranial colour-flow Doppler ultrasonography. Br J Surg. 1994;81:824826.[Medline] [Order article via Infotrieve]
4. Kimura K, Hashimoto Y, Hirano T, Uchino M, Ando M. Diagnosis of middle cerebral artery occlusion with transcranial color-coded real-time sonography. AJNR Am J Neuroradiol. 1996;17:895899.[Abstract]
5. Martin PJ, Smith JL, Gaunt ME, Naylor AR. Assessment of intracranial primary collaterals using transcranial color-coded real-time sonography. J Neuroimaging. 1995;5:199205.[Medline] [Order article via Infotrieve]
6. Baumgartner RW, Baumgartner I, Mattle HP, Schroth G. Transcranial color-coded duplex sonography in the evaluation of collateral flow through the circle of Willis. AJNR Am J Neuroradiol. 1997;18:127133.[Abstract]
7. Bruno A, Biller J, Silvidi JA. A reason for failure to obtain transcranial Doppler flow signals: hyperostosis of the skull. Stroke. 1988;19:274. Letter.[Medline] [Order article via Infotrieve]
8.
Halsey JH. Effect of emitted power on waveform
intensity in transcranial Doppler. Stroke. 1990;21:15731578.
9.
Grolimund P, Seiler RW, Aaslid R, Huber P, Zurbruegg
H. Evaluation of cerebrovascular disease by combined extracranial and
transcranial Doppler sonography: experience in 1039
patients. Stroke. 1987;18:10181024.
10.
Itoh T, Matsumoto M, Handa N, Maeda H, Hougaku H,
Hashimoto H, Etani H, Tsukamoto Y, Kamada T. Rate of successful
recording of blood flow signals in the middle cerebral artery
using transcranial Doppler sonography.
Stroke. 1993;24:11921195.
11. Comerota AJ, Katz ML, Hosking JD, Hashemi HA, Kerr RP, Carter AP. Is transcranial Doppler a worthwhile addition to screening tests for cerebrovascular disease? J Vasc Surg. 1995;21:9097.[Medline] [Order article via Infotrieve]
12. Marinoni M, Ginanneschi A, Forleo P, Amaducci L. Technical limits in transcranial Doppler recording: inadequate acoustic windows. Ultrasound Med Biol. 1997;8:12751277.
13.
Bogdahn U, Becker G, Winkler J, Greiner K, Perez J,
Meurers B. Transcranial color-coded real-time sonography in
adults. Stroke. 1990;21:16801688.
14. Tsuchiya T, Yasaka M, Yamaguchi T, Kimura K, Omae T. Imaging of the basal cerebral arteries and measurement of blood flow velocity in adults by using transcranial real-time color flow doppler sonography. AJNR. 1991;12:497502.[Abstract]
15.
Schöning M, Walter J. Evaluation of the
vertebrobasilar-posterior system by transcranial color
duplex sonography in adults. Stroke. 1992;23:12801286.
16. Gomez CR, Brass LM, Tegeler CH, Babikian VL, Sloan MA, Feldman E, Wechsler LR. The transcranial Doppler standardization project. J Neuroimaging. 1993;3:190192.[Medline] [Order article via Infotrieve]
17. Martin PJ, Evans DH, Naylor AR. Transcranial color-coded sonography of the basal cerebral circulation; reference data from 115 volunteers. Stroke. 1994;25:390396.[Abstract]
18. Baumgartner RW, Mattle HP, Aaslid R. Transcranial color-coded duplex sonography, magnetic resonance angiography, and computed tomography angiography: methods, ap-plications, advantages, and limitations. J Clin Ultrasound. 1995;23:89111.[Medline] [Order article via Infotrieve]
19. Henschen F. Classification of cranial hyperostoses. Acta Chir Scand. 1939;82:107116.
20.
Alpers BJ, Berry RG, Paddison RM. Anatomical studies of
the circle of Willis in normal brain. Arch Neurol
Psychiatry. 1959;81:409418.
21. Riggs HE, Rupp C. Variation in form of circle of Willis: the relation of the variations to collateral circulation: anatomic analysis. Arch Neurol. 1963;8:814.
22.
Battacharji SK, Hutchinson EC, McCall AJ. The circle of
Willis: the incidence of developmental abnormalities in normal and
infarcted brains. Brain. 1967;90:747758.
23. Tulleken CAF, Luiten MLFB. The basilar bifurcation: microscopical anatomy. Acta Neurochir. 1987;85:5055.[Medline] [Order article via Infotrieve]
24. Yasargil MG, ed. Microneurosurgery, Vol I. Stuttgart, Germany: Georg Thieme Verlag; 1984:92143.
25. Catalina-Herrera CJ. Study of the anatomic metric values of the foramen magnum and its relation to sex. Acta Anat (Basel). 1987;130:344347.[Medline] [Order article via Infotrieve]
26. Arnolds BJ, von Reutern GM. Transcranial Doppler sonography: examination technique and normal reference values. Ultrasound Med Biol. 1986;12:115123.[Medline] [Order article via Infotrieve]
27. Hennerici H, Rautenberg W, Sitzer G, Schwartz A. Transcranial Doppler ultrasound for the assessment of intracranial arterial flow velocity, part I: examination of technique and normal values. Surg Neurol. 1987;27:439448.[Medline] [Order article via Infotrieve]
28. Vriens EM, Kraaier V, Musbach M, Wieneke GH, van Huffelen AC. Transcranial pulsed Doppler measurements 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. 1989;15:18.
29.
Ameriso SF, Paganini-Hill A, Meiselman HJ, Fisher M.
Correlates of middle cerebral artery blood velocity in the elderly.
Stroke. 1990;21:15791583.
30. Bartels E, Flügel KA. Quantitative measurements of blood flow velocity in basal cerebral arteries with transcranial duplex color-flow imaging: a comparative study with conventional transcranial Doppler sonography. J Neuroimaging. 1994;4:7781.[Medline] [Order article via Infotrieve]
31. Eicke BM, Tegeler CH, Dalley G, Myers LG. Angle correction in transcranial Doppler sonography. J Neuroimaging. 1994;4:2933.[Medline] [Order article via Infotrieve]
32. Martin PJ, Evans DH, Naylor AR. Measurement of blood flow velocity in the basal cerebral circulation: advantages of transcranial color-coded sonography over conventional transcranial Doppler. J Clin Ultrasound. 1995;23:2126.[Medline] [Order article via Infotrieve]
33. Schöning M, Buchholz R, Walter J. Comparative study of transcranial color duplex sonography and transcranial Doppler sonography in adults. J Neurosurg. 1993;78:776784.[Medline] [Order article via Infotrieve]
34. Gabrielsen TO, Greitz T. Normal size of the internal carotid, middle cerebral and anterior cerebral arteries. Acta Radiol. 1970;10:110.
35. Grolimund P, Seiler RW. Age dependence of the flow velocity in the basal cerebral arteries- a transcranial Doppler ultrasound study. Ultrasound Med Biol. 1988;14:191198.[Medline] [Order article via Infotrieve]
36. Ackerstaff RG, Keunen RW, van Pelt W, Montauban van Swijndrecht AD, Stijnen T. Influence of biological factors on changes in mean cerebral blood flow velocity in normal ageing: a transcranial Doppler study. Neurol Res. 1990;12:187191.[Medline] [Order article via Infotrieve]
37. Müller M, Schimrigk K. A comparative assessment of cerebral haemodynamics in the basilar artery and carotid territory by transcranial Doppler sonography in normal subjects. Ultrasound Med Biol. 1994;20:677687.[Medline] [Order article via Infotrieve]
38.
Otis S, Rush M, Boyajian R. Contrast-enhanced
transcranial imaging; results of an American phase-two
study. Stroke. 1995;26:203209.
39.
Kaps M, Schaffer P, Beller K-D, Seidel G, Bliesath H,
Diletti E. Characteristics of transcranial Doppler
signal enhancement using a phospholipid-containing echocontrast agent.
Stroke. 1997;28:10061008.
40. Postert T, Federlein J, Przuntek H, Büttner T. Insufficient and absent acoustic temporal bone window: potential and limitations of transcranial contrast-enhanced color-coded sonography and contrast-enhanced power-based sonography. Ultrasound Med Biol. 1997;23:857862.[Medline] [Order article via Infotrieve]
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