Departments of Neurology and Radiology,
Ruhr-University Bochum,
Stroke Unit,
Bochum, Germany
To the Editor:
Baumgartner et al1 recently reported on the
diagnostic value of contrast-enhanced
transcranial color-coded duplex sonography (CE-TCCS) in
ischemic cerebrovascular disease. In this study, 33 patients
with insufficient temporal insonation conditions (21 patients had
ischemic stroke and 12 suffered from transient ischemic
attack) were investigated after application of a galactose-based echo
contrast agent. The presence of an insufficient temporal bone window
was indicated when two sonographers estimated that they were unable to
evaluate the basal cerebral arteries by means of color and spectral
Doppler imaging in unenhanced examinations. After application of a
galactose-based echo contrast agent, 66% of the CE-TCCS examinations
were considered conclusive. Cross-flow through the anterior and
posterior communicating arteries due to extracranial occlusive disease
could be demonstrated in 3 and 2 patients, respectively. No
stenoses or occlusions of intracranial arteries could be
visualized.
We would like to add our CE-TCCS experiences in severely affected
stroke individuals with insufficient acoustic bone windows (IABW). 30
patients (17 women and 13 men; mean age, 75.2 [range, 59 to 86]
years) with IABW and severe cerebrovascular event (European Stroke
Scale score of <35 points) suggestive of middle cerebral artery (MCA)
trunk occlusion were examined after injection of 9 ml of 400mg/ml
echo-contrast agent (Levovist; Schering AG). The temporal bone window
was considered absent if no vascular structure could be detected in
unenhanced TCCS images. Occlusion of the MCA was diagnosed if the
following criteria were met: (1 ) discontinuous or missing color-coded
signal of the MCA main stem, (2 ) visualization of at least one other
ipsilateral artery (anterior cerebral artery or posterior cerebral
artery), and (3 ) identification of the MCA on the contralateral side.
For comparison with CE-TCCS scans, at least one angiographic study
(digital angiography, MR angiography, or spiral CT angiography) was
performed within 12 hours after the onset of clinical symptoms. The
ultrasonic examination was recorded on videotape and evaluated
off-line by two experienced ultrasound investigators who were blinded
to the results of angiographic studies. It was required that both
investigators confirm the diagnosis. In 15 patients, both angiographic
and CE-TCCS examinations demonstrated an occluded MCA main stem
(Figure
Temporal hyperostosis is known to be a major obstacle for successful
transtemporal insonation of the basal cerebral arteries.
Because of insufficient penetration of the ultrasound beam through the
temporal bone, up to 35% of stroke patients cannot be successfully
examined.2 It has been shown that CE-TCCS may overcome
this anatomic hindrance in the majority of healthy
individuals.3 4 Nevertheless, the clinical relevance of
these findings in stroke patients has not previously been established.
The study of Baumgartner et al1 shows for the first time
that CE-TCCS allows the assessment of intracranial cross-flow and
accurate depiction of most intracranial arteries in two thirds of the
stroke patients with inconclusive unenhanced examinations. In
accordance with Otis et al5 but in contrast to Baumgartner
et al, we found conclusive CE-TCCS results in more than 90% of stroke
patients with IABW. A likely reason for this disparity may be the
application mode of the echo contrast agent. Compared with the short
application period (10 to 15 seconds) in the study of Baumgartner et
al, we injected the echo contrast agent over a period of at least 3
minutes. In this way improved signal enhancement was achieved by
avoiding color artifacts ("blooming") that may totally obscure
ultrasound images during the first phase of echo contrast
enhancement.
In the study of Baumgartner et al, no intracranial stenosis or
occlusion was detected by CE-TCCS or angiography. This finding is most
likely attributed to the fact that the incidence of MCA occlusions is
low6 and that the disease may not be found in smaller
series of unselected stroke patients. Nevertheless, a rapid and
reliable diagnosis of MCA occlusion is of major importance, because
immediate therapeutic interventions such as
thrombolysis or decompressive surgery may improve the
prognosis of this vascular syndrome. In this respect, our experiences
in severely affected individuals show that CE-TCCS is an accurate and
time-saving tool for the diagnosis of MCA trunk occlusion in patients
with IABW. In conclusion, our findings clearly confirm the clinical
value of transpulmonary echo contrast agents for improved
diagnosis in stroke patients.
References
1.
Baumgartner RW, Arnold M, Gönner F, Staikow
I, Herrmann C, Rivoir A, Müri RM. Contrast-enhanced
transcranial color-coded duplex sonography in
ischemic cerebrovascular disease.
Stroke. 1997;28:24732478.
2.
Kaps M, Damian MS, Teschendorf U, Dorndorf W.
Transcranial Doppler ultrasound finding in
middle cerebral artery occlusion. Stroke. 1990;21:532537.
3.
Kaps M, Schaffer P, Beller KD, Seidel G, Bliesath H,
Wurst W. Phase I: transcranial echo contrast studies
in healthy volunteers. Stroke. 1995;26:20482052.
4.
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]
5.
Otis S, Rush M, Boyajian R. Contrast-enhanced
transcranial imaging: results of an American phase
two study. Stroke. 1995;26:203209.
6.
Zanette EM, Fieschi C, Bozzao L. Comparison of
cerebral angiography and transcranial Doppler
sonography in acute stroke. Stroke. 1989;20:899903.
Department of Neurology,
University Hospital,
Bern, Switzerland
We have read with great interest the data and comments of
Postert et al. It is important to note that these authors assessed
intracranial hemodynamics with color Doppler
imaging without making use of spectral Doppler sonography, which is
different from our contrast-enhanced (CE) transcranial
color-coded duplex sonography (TCCS) investigation1 and
previous nonenhanced2 and CE3 4 5 TCCS
studies. Reducing TCCS to color Doppler imaging has several
limitations. (1 ) Especially in patients with inadequate temporal
windows, color Doppler imaging parameters are set to
obtain the best possible sensitivity for detecting signals by use of
the lowest emission frequency, the highest emission energy, and the
largest color Doppler gate. Together with the color-blooming
artifact induced by the echo contrast agent, these measures reduce the
spatial resolution of color Doppler imaging that is already
inferior to B-mode imaging. Thus, the reliable
identification of intracranial arteries without the additional use of
spectral Doppler may become impossible. (2 ) A deep middle cerebral
vein that drains toward the insula and the basal vein of Rosenthal
provides color Doppler signals showing the same flow directions as
the middle and posterior cerebral arteries, respectively. Consequently,
it is very difficult to distinguish venous flow from slow
arterial flow without the use of spectral Doppler
sonography. (3 ) In the case of color Doppler suspicion of a
nonoccluded cerebral artery, this technique is not adequate for
evaluating the presence of a stenosis. The presence of high
velocities or aliasing on the color Doppler scale may also
represent increased velocities due to increased flow that may
occur in collaterals and arteries feeding arteriovenous
malformations.6 7 8 9 10 Furthermore, color Doppler cannot
distinguish aliasing from reversed flow that may occur in the presence
of turbulence. (4 ) Intracranial stenoses may regress by
recanalization of thromboembolic
material,11 which may be detected by repetitive spectral
Doppler velocity measurements. In conclusion, the data of Postert
et al suggest that color Doppler ultrasound alone may reliably
detect the presence of MCA trunk occlusion. However, the
above-mentioned arguments and clinical experience indicate that the
additional use of spectral Doppler sonography is recommended for
CE-TCCS assessment of abnormal intracranial hemodynamics.
Postert et al reported conclusive CE-TCCS studies in 93% of their
patients compared with 66% in our series.1 These authors
assumed that the different detection rates were related to differences
in contrast medium administration: we injected within 10 to 15 seconds
one or more boluses of 2.0 g, whereas they infused 3.6 g over
a period of at least 3 minutes; identical concentrations of 400 mg/mL
Levovist were used in both studies. We agree with Postert et al that
the slower administration of the echo contrast agent may reduce color
artifacts and extend the duration of diagnostically useful
Doppler signals. However, we disagree with their assumption that
color artifacts shortened the duration of diagnostically
useful Doppler signals and were the reason for the higher rate of
inconclusive CE-TCCS investigations in our series. First, color
blooming can be avoided simply by reducing the color Doppler gain.
The echo contrast agent and its concentration and the ultrasonic
emission frequencies (2 MHz) and energies (the upper limit is given by
the Federal Drug Administration) were identical in both CE-TCCS
studies. Thus, we assume that both CE-TCCS studies differed in the
definitions of conclusive transtemporal CE-TCCS
investigations that were given by distinctive study goals and in
patient selection. We examined patients with ischemic strokes
located in the hemisphere underlying a temporal bone with an
insufficient acoustic window. Consequently, we appreciated the presence
of a conclusive study when CE color and spectral Doppler sonography
enabled evaluation of the presence or absence of stenoses and
occlusions in the middle, posterior, and anterior cerebral arteries and
of cross-flow through the circle of Willis. Conversely, Postert et al
insonated patients with acute ischemic stroke to investigate
whether the MCA was occluded. Accordingly, they used less severe
criteria for defining conclusive CE-TCCS investigations of the
ipsilateral hemisphere, because only color Doppler depiction (or
nondepiction, in case of occlusion) of the middle, anterior, or
posterior cerebral artery was needed. It is likely that differences in
selection of patients with insufficient temporal acoustic windows were
the other cause of the lower number of conclusive CE-TCCS studies in
our series. In our study, CE-TCCS detected the contralateral MCA in
25% of cases (8 of 32 patients), whereas Postert et al visualized by
definition the contralateral MCA in 93% of their cases. We have
reviewed our videotapes and found that by using the color Doppler
criterion of Postert et al, the contralateral MCA would have been
detected in 28% of cases, which suggests that our patients had more
CE-TCCS refractory temporal ultrasonic windows. The fact that the
patient populations were on average aged 70 to 75 years in both studies
but were 70% female gender in our series compared with 57% in that of
Postert et al underlines this assumption, because ultrasound
attenuation caused by the tem- poral bone increases with age and
is substantial in elderly women.12
References
1.
Baumgartner RW, Arnold M, Gönner F, Staikov
Y, Herrmann C, Rivoir A, Müri RM. Contrast-enhanced
transcranial color-coded duplex sonography in
ischemic cerebrovascular disease.
Stroke. 1997;28:24732478.
2.
Seidel G, Kaps M, Gerriets T. Potential and
limitation of transcranial color-coded sonography in stroke
patients. Stroke. 1995;26:20612066.
3.
Bogdahn U, Becker G, Winkler J, Greiner K, Perez J,
Meurers B. Transcranial color-coded real-time
sonography in adults. Stroke. 1990;21:16801688.
4.
Kaps M, Schaffer P, Beller K-D, Seidel G, Bliesath H,
Wurst W. Phase I: transcranial echo contrast studies
in healthy volunteers. Stroke. 1995;26:20482052.
5.
Otis S, Rush M, Boyajian R. Contrast-enhanced
transcranial imaging: results of an American
phase-two study. Stroke. 1995;26:203209.
6.
Kaps M, Damian MS, Teschendorf U, Dorndorf W.
Transcranial Doppler ultrasound findings in
middle cerebral artery occlusion. Stroke. 1990;21:532537.
7.
Mattle HP, Grolimund P, Huber P, Sturzenegger M,
Zurbrügg H. Transcranial Doppler
sonographic findings in middle cerebral artery disease.
Arch Neurol. 1988;45:289295.
8.
Grolimund P, Seiler RW, Aaslid R, Huber P,
Zurbrügg H. Evaluation of cerebrovascular disease by
combined extracranial and transcranial Doppler
sonography: experience in 1039 patients.
Stroke. 1987;18:10181024.
9.
Mast H, Mohr JP, Thompson JLP, Osipov A, Trocio SH,
Mayer S, Young WL. Transcranial Doppler
ultrasonography in cerebral arteriovenous malformations:
diagnostic sensitivity and association of flow velocity
with spontaneous hemorrhage and focal neurological deficit.
Stroke. 1995;26:10241027.
10.
Schneider PA, Ringelstein EB, Rossmann ME, Dilley RB,
Sobel DF, Otis SM, Bernstein EF. Importance of cerebral
collateral pathways during carotid
endarterectomy. Stroke. 1988;19:13281334.
11.
Ringelstein EB, Biniek R, Weiller C, Ammeling B, Nolte
PN, Thron A. Type and extent of hemispheric brain infarctions
and clinical outcome in early and delayed middle cerebral artery
recanalization. Neurology. 1992;42:289298.
12.
Eden A. Transcranial Doppler
ultrasonography and hyperostosis of the skull.
Stroke. 1988;19:14451446.[Medline]
[Order article via Infotrieve]
© 1998 American Heart Association, Inc.
Letters to the Editor
Contrast-Enhanced Transcranial Color-Coded Real-Time Sonography: A Reliable Tool for the Diagnosis of Middle Cerebral Artery Trunk Occlusion in Patients With Insufficient Temporal Bone Window
);
in 13 individuals both diagnostic methods showed a patent
vessel. In 2 cases (1 with and 1 without occlusion of the MCA main stem
in angiography) it was not possible to make a definite diagnosis.

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Figure 1. A, Axial unenhanced TCCS image demonstrating an
insufficient acoustic temporal bone window without
visualization of any intracranial vessel, (B indicates weak depiction
of the brain stem); B, after application of echo contrast agent, the
missing color-coded signal of the symptomatic middle (1),
anterior (2), and posterior (3) cerebral arteries are clearly
detectable; C, visualization of the contralateral MCA (4); and D,
spiral CT angiography showing MCA trunk occlusion (arrow).
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