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Stroke. 1998;29:1070-1073

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(Stroke. 1998;29:1070-1073.)
© 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

Thomas Postert, MD; Jens Federlein, MD; Bertram Braun, MD; Odo Köster, MD; Christian Börnke, MD; Horst Przuntek, MD; Thomas Büttner, MD

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 (FigureDown); 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).

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;28:2473–2478.[Abstract/Free Full Text]

2. Kaps M, Damian MS, Teschendorf U, Dorndorf W. Transcranial Doppler ultrasound finding in middle cerebral artery occlusion. Stroke. 1990;21:532–537.[Abstract/Free Full Text]

3. Kaps M, Schaffer P, Beller KD, Seidel G, Bliesath H, Wurst W. Phase I: transcranial echo contrast studies in healthy volunteers. Stroke. 1995;26:2048–2052.[Abstract/Free Full Text]

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;23:857–862.[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;26:203–209.[Abstract/Free Full Text]

6. Zanette EM, Fieschi C, Bozzao L. Comparison of cerebral angiography and transcranial Doppler sonography in acute stroke. Stroke. 1989;20:899–903.[Abstract/Free Full Text]

Response

Ralf W. Baumgartner, MD; Marcel Arnold, MD; Friedrich Gönner, MD; Iwan Staikow, MD; Cornelia Herrmann, MD

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;28:2473–2478.

2. Seidel G, Kaps M, Gerriets T. Potential and limitation of transcranial color-coded sonography in stroke patients. Stroke. 1995;26:2061–2066.[Abstract/Free Full Text]

3. Bogdahn U, Becker G, Winkler J, Greiner K, Perez J, Meurers B. Transcranial color-coded real-time sonography in adults. Stroke. 1990;21:1680–1688.[Abstract/Free Full Text]

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;26:2048–2052.

5. Otis S, Rush M, Boyajian R. Contrast-enhanced transcranial imaging: results of an American phase-two study. Stroke. 1995;26:203–209.

6. Kaps M, Damian MS, Teschendorf U, Dorndorf W. Transcranial Doppler ultrasound findings in middle cerebral artery occlusion. Stroke. 1990;21:532–537.

7. Mattle HP, Grolimund P, Huber P, Sturzenegger M, Zurbrügg H. Transcranial Doppler sonographic findings in middle cerebral artery disease. Arch Neurol. 1988;45:289–295.[Abstract/Free Full Text]

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;18:1018–1024.[Abstract/Free Full Text]

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;26:1024–1027.[Abstract/Free Full Text]

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;19:1328–1334.[Abstract/Free Full Text]

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;42:289–298.[Abstract/Free Full Text]

12. Eden A. Transcranial Doppler ultrasonography and hyperostosis of the skull. Stroke. 1988;19:1445–1446.[Medline] [Order article via Infotrieve]




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