(Stroke. 1999;30:814-820.)
© 1999 American Heart Association, Inc.
Original Contributions |
Frontal Bone Windows for Transcranial Color-Coded Duplex Sonography
From the Departments of Neurology (E.S., W.D.) and Neuroradiology (A.K.), Justus-Liebig University, Giessen, and Department of Neurology, Medical University at Luebeck (M.K.), Germany.
Correspondence to Dr Erwin Stolz, Department of Neurology, Justus-Liebig University, Am Steg 14, D-35385 Giessen, Germany. E-mail erwin.stolz{at}neuro.med.uni-giessen.de
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Abstract |
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Background and Purpose—The use of the conventional temporal bone window for transcranial color-coded duplex sonography (TCCS) often results in difficulties in obtaining angle-corrected flow velocity measurements of the A2 segment of the anterior cerebral artery, the posterior communicating artery, and the midline venous vasculature because of the unfavorable insonation angle. The same applies to B-mode imaging of the frontal parenchyma. However, transorbital TCCS raises problems with the insonation of the orbital lens. To overcome these drawbacks, we studied the feasibility of frontal bone windows for TCCS examinations.
Methods—In 75 healthy volunteers (mean age, 45.3±17.0 years; age range, 17 to 77 years), the circle of Willis and the venous midline vasculature were insonated through a lateral and paramedian frontal bone window. Insonation quality of parenchymal structures (B-mode) was graded on a 3-point scale depending on the visibility of typical parenchymal landmarks. In a similar manner, the quality of the color-/Doppler-mode imaging of the arteries of the circle of Willis and the internal cerebral veins was assessed. In 15 patients (mean age, 62.7±13.7 years; age range, 33 to 83 years), the color-/Doppler-mode imaging quality of the intracranial vessels before and after application of an ultrasound contrast-enhancing agent was compared.
Results—B-mode insonation quality was optimal to fair in 73.3% of cases using the lateral and in 52.0% of cases using the paramedian frontal bone window, with defined parenchymal structures used as reference. Insonation quality decreased in those older than 60 years. In those younger than 60 years, angle-corrected flow velocity measurements of the A2 segment of the anterior cerebral artery and the internal cerebral vein were possible in 73.6% and 60.0%, respectively. Contrast enhancement resulted in a highly significant improvement in the imaging quality of the intracranial vessels.
Conclusions—The transfrontal bone windows offer new possibilities for TCCS examinations, although the insonation quality is inferior to the conventional temporal bone window in terms of failure of an acoustic window. This can be compensated for by application of an ultrasound contrast-enhancing agent.
Key Words: cerebral arteries • cerebral veins • TCCS • ultrasonography
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Transcranial color-coded duplex sonography (TCCS) is an established tool for examination of the basal cerebral arteries.1 2 New aspects of TCCS are assessment of the brain parenchyma3 4 5 and intracranial veins and sinuses.6 7 8 The standard approach is insonation through a temporal bone window. With the use of the transforaminal insonation plane, the vertebrobasilar system can be identified.9 10 For examination of the straight sinus, a transoccipital approach has been described.11 12
However, the transtemporal approach poses problems in the imaging of the frontal parenchyma and in obtaining angle-corrected flow velocity measurements of the A2 segment of the anterior cerebral artery (ACA) and the posterior communicating artery (PCoA) because of the unfavorable insonation angle. A frontal insonation plane would facilitate the assessment of frontal tumors and aneurysms and could be helpful in solving the question of spasms of the ACA. Furthermore, cross-flow through the PCoA might be identified more easily. The ultrasonographic imaging of the internal cerebral veins (ICVs) that serve as important collateral channels in intracranial venous thrombosis13 is still only a partially solved problem. Identification rates reported thus far in the literature are <40% in the group aged 20 to 60 years when the transoccipital approach is used.12
Although TCCS allows the depiction of flow signals of the circle of Willis through the superior orbital fissure,14 partly avoiding the limitations of the transtemporal insonation plane, there are as yet no studies that have shown the feasibility of transorbital TCCS using Food and Drug Administration–approved power settings implemented for protection of the orbital lens.
This study was designed to test the abilities of frontal acoustic bone windows for TCCS examination with regard to the aforementioned problems.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Volunteers
Seventy-five healthy volunteers agreed to take part in this study. The age range was 17 to 77 years, with the mean age 45.3±17.0 years. Males (n=37; mean age, 49.7±16.9 years) and females (n=38; mean age, 41.1±16.2 years) were nearly equally represented. Thirty-five participants were aged <40 years, 20 were between 40 and 60 years, and 20 were aged >60 years. All volunteers were examined without ultrasound contrast enhancement.
Examination Technique
TCCS examinations were performed with a phased-array ultrasound
system (Hewlett Packard, Sonos 2000) equipped with a 2-MHz transducer.
For insonation, a lateral frontal bone window (LFBW) and paramedian
frontal bone window (PMFBW) were chosen (Figure 1
). The LFBW was located above the
lateral aspect of the eyebrow, and the PMFBW was slightly lateral of
the midline of the forehead.
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B-Mode (Parenchymal) Sonography
For depiction of the parenchymal anatomy, an insonation
depth of 16 cm was chosen so that the contralateral skull became
visible. The LFBW constantly allowed the imaging of the sylvian fissure
in a frontal-transverse insonation plane. In a high percentage of
subjects, the middle cerebral artery (MCA) was identified as an
anatomic structure from the outline of the vessel lumen as echogenic
double reflex (Figure 2). The hypophyseal
groove was visible in more than half of the volunteers. Similar to the
transtemporal approach, the mesencephalon was depicted as a
hypoechogenic structure, although the usual appearance was distorted by
the slightly oblique insonation plane.
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The most prominent parenchymal structure insonated through the PMFBW
was the hyperechogenic choroid plexus of the third ventricle; the
ventricle itself was depicted as a hypoechogenic structure, as was the
corpus callosum. The orbital roof appeared as a hyperechogenic
structure (Figure 3). A frontal-sagittal
insonation plane was used for insonation through the PMFBW.
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To quantify the parenchymal insonation quality, a 3-point scale was devised on the basis of the visibility of defined parenchymal landmarks. For the LFBW, the sylvian fissure and the mesencephalon were chosen as reference structures; for the PMFBW, the orbital roof, the choroid plexus of the third ventricle, and the corpus callosum were chosen. The following scale was used for both the LFBW and the PMFBW: 2, clearly visible parenchymal landmarks; 1, parenchyma visible but blurred; and 0, no parenchymal structures visible.
Color-/Doppler-Mode Sonography
To insonate the circle of Willis through the LFBW, the
insonation depth was lowered to 10 cm, and the pulse repetition
frequency (PRF) was adjusted to a medium range (20 cm/s). The most
prominent vascular structure when the LFBW was used was the A2 segment
of the ACA with a flow direction toward the probe. The ipsilateral A1
segment of the ACA was coded with a flow away from the probe, and the
M1 segment of the MCA was coded with a flow toward the probe, although
the insonation of the M1 segment was frequently difficult because of
the unfavorable insonation angle. The posterior cerebral artery (PCA)
was coded with flow away from the transducer in the lateral frontal
insonation plane. Frequently the PCoA was depicted (Figure 2
).
In some volunteers the basilar head was visible.
By further lowering the PRF, the ICVs could be insonated slightly above
the choroid plexus of the third ventricle at a depth of 9 to 10 cm with
the use of the PMFBW. Reduction of the insonation depth and a low PRF
enabled visualization of the pericallosal artery in its course around
the knee of the corpus callosum (Figure 4). In some of the volunteers, the
basilar head and the PCA could be depicted through the PMFBW.
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The quality of the color-/Doppler-mode sonography through the frontal bone windows was graded on a 3-point scale depending on the appearance of the frequency-based color-coded signal of a given vessel and the quality of its Doppler spectrum, as follows: 2, vessel visible to the full extent that can be expected in the given examination plane; Doppler spectrum sufficient for measurement; 1, vessel visible, but fragmented color coding or Doppler spectrum insufficient for measurement; and 0, no vessel visible and/or no Doppler spectrum obtainable.
The frontal bone windows appeared to be generally smaller than the temporal bone window, which allows the insonation in different transverse (mesencephalic, ventricular insonation) and coronal (anterior and posterior) planes. Therefore, generally no differentiation between insonation window and insonation plane was performed. Insonation through the LFBW had a transverse orientation, and that through the PMFBW had a sagittal orientation. From these positions, the vascular and parenchymal structures could be imaged by fanlike tilts of the transducer of approximately ±5°.
Patients
Fifteen patients (mean age, 62.7±13.7 years; age range, 33 to
83 years) were examined with echo contrast–enhanced TCCS (Levovist;
Schering AG; intravenous infusion of 17 mL at a
concentration of 300 mg/L by infusion pump, infusion rate 60 mL/h) for
the evaluation of the intracranial vasculature. Thirteen patients had
acute ischemic stroke, 1 a basilar head aneurysm,
and 1 cerebral venous thrombosis. Two of the stroke patients had an
occlusion, and 1 had a high-grade stenosis of the extracranial
internal carotid artery, diagnosed by duplex sonography.
In these patients, the imaging quality of the intracranial vasculature was assessed with the use of the frontal bone windows in terms of the number of the vessels imaged and the quality of insonation according to the 3-point scale for grading the color-/Doppler-mode imaging described above.
Data Evaluation
The software package Turbo Statistik 3.0 was used for
statistical data evaluation. A nonparametric ANOVA
(Mann-Whitney U test) was used for comparison of flow
velocities between different age and sex groups, and Fisher's exact
test was used for comparison of absolute frequencies of identification
rates of intracranial vessels. For comparison of precontrast and
postcontrast color-/Doppler-mode scores, Fisher's exact test was
also used. In this case, the number of insonated vessels rated with a
score of 2 on the color-/Doppler-mode scale (ie, those vessels with
clinically useful insonation conditions) before and after contrast
enhancement were compared.
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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B-Mode (Parenchymal) Sonography
Scores of 2 and 1 for parenchymal insonation quality through the LFBW were reached in 73.3% of volunteers; 26.7% showed lack of a sufficient acoustic bone window. The PMFBW allowed a fair insonation quality (scores of 2 and 1) in 52.0% of cases; no acoustic window was found in 48.0% of volunteers. A clear age dependence for both the LFBW and the PMFBW was observed. Insonation quality scores of 2 and 1 were found in 81.8% of cases for the LFBW and in 60.0% for the PMFBW for those aged
60 years; for those aged >60 years, insonation quality
declined to 50.0% (P<0.001) and 30.0%
(P<0.05), respectively. Best insonation conditions were
found in the volunteers aged <40 years. In this age group, scores of 2
and 1 were reached in 91.4% through the LFBW and in 68.6% through the
PMFBW. Men tended to have a better acoustic bone window than women for
both the LFBW and the PMFBW.
Color-/Doppler-Mode Sonography
The rates of sufficient vascular insonation conditions,
corresponding to a score of 2 on the scale grading the quality of
color-mode imaging and the Doppler spectrum, are summarized in
Table 1. The LFBW allowed angle-corrected
flow velocity measurements of the different segments of the circle of
Willis at insonation rates between 73.6% and 40.0% in those
volunteers aged 60 years. In the same age group, the PMFBW allowed a
sufficient insonation of the ICV in 60.0% (Table 1). In those
aged >60 years, insonation conditions declined markedly for both the
LFBW and the PMFBW. This finding was statistically significant for the
A2 ACA (P<0.0001), the A1 ACA (P<0.0001), the
M1 MCA (P<0.0001), the PCA (P=0.0003), the PCoA
(P=0.0027), and the ICV (P=0.02).
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The angle-corrected flow velocity measurements for the A2 segment of
the ACA and the ICV are summarized in Table 2. Systolic and
diastolic flow velocities of the A2 ACA decreased with
increasing age (P<0.05). This effect did not reach the
level of significance for the ICV. Women tended to have higher
systolic and diastolic flow velocities than men for
both the A2 ACA and the ICV, although this was without statistical
significance.
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Patients
Echo contrast enhancement resulted in a marked improvement of the
imaging quality of the intracranial vessels, whereas contrast
enhancement had no effect on B-mode (parenchymal) sonography. The
precontrast and postcontrast enhancement results are summarized in
Table 3. Concerning the quality of the
acoustic window assessed on the B-mode (parenchymal) scale, the patient
and normal collective groups were not distributed equally when similar
age groups were compared; in the patient group, only 6 of 15 (40%) had
a good to fair LFBW, and only 2 of 15 (13%) had a good to fair PMFBW.
Three patients had a total lack of any acoustic penetration. Even
contralateral and ipsilateral skull structures were not visible in
those patients.
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With the use of the LFBW, native TCCS was able to delineate
sufficiently (ie, score of 2 on the color-/Doppler-mode scale) the
different segments of the circle of Willis at success rates ranging
between 0% and 27%. Echo contrast enhancement resulted in a
significant improvement of vascular imaging conditions, with success
rates for the different segments of the circle of Willis ranging
between 53% for the M1 MCA and 70% to 80% for the remaining
arterial segments (Table 3). A
diagnostically sufficient color and Doppler signal of
the basilar head was found in 7% with native TCCS; echo contrast
enhancement increased the success rate to 40%. Contrast enhancement
resulted in a diagnostically useful color and Doppler
signal in up to 40% of cases with the use of the PMFBW. Those patients
without any acoustic penetration of the ultrasound beam did not show
any contrast-enhancing effect.
All patients with extracranial internal carotid artery occlusion or stenosis unambiguously displayed a flow direction of the PCoA directed from the PCA to the intracranial internal carotid artery on the affected side and from the internal carotid artery to the PCoA on the unaffected side, demonstrating a cross-flow condition. Furthermore, a retrograde flow direction in the A1 segment of the ACA was observed in these patients ipsilateral to the extracranial occlusion or stenosis, indicating a cross-flow from the contralateral ACA through the anterior communicating artery. Using a sagittal insonation plane through the PMFBW and a transverse temporal insonation plane, we observed a partial thrombosis of a basilar head aneurysm, and its size could be confirmed correctly in 1 patient compared with MR angiography. The status of the ICVs could be assessed correctly compared with the results of MR angiography in 1 patient with cerebral venous thrombosis. Normal venous flow velocity and direction indicated that the ICV did not serve as a collateral venous pathway in this patient.
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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As a standard approach for TCCS, the temporal bone window has been widely used for identification of the main segments of the circle of Willis and, as a new development, of intracranial veins and sinuses.1 2 6 7 8 Furthermore, the temporal bone window allows the identification of parenchymal abnormalities such as intracerebral hemorrhage, tumors, and pathology of the ventricular system.3 4 5 However, because of the unfavorable insonation angle, measurements of flow velocities of the A2 segment of the ACA, the PCoA, and the venous midline vasculature are often unreliable. The same difficulties apply to imaging of the frontal parenchyma.
Although the depiction of flow signals of the circle of Willis through the orbit by TCCS is possible,14 thus far no studies have shown the feasibility of this approach when Food and Drug Administration–approved ultrasound intensity settings implemented for the protection of the orbital lens are used. This study was designed to test the abilities of frontal acoustic bone windows for TCCS examination with regard to the aforementioned problems.
B-Mode (Parenchymal) Sonography
For transcranial duplex sonography, the current
technological standard is the use of sector transducers. The best
spatial resolution is reached in the center beams of the sector. This
technical fact and the anatomic location of the temporal bone window
often result in difficulties in imaging the frontal regions of the
brain parenchyma. The frontal bone windows provide additional
transverse and sagittal frontal insonation windows with the use of the
LFBW and the PMFBW. With LFBW insonation, quality is sufficient in
>80% of cases aged 60 years with defined parenchymal structures
used as reference points. The most interesting feature of the LFBW is
the ability to insonate the MCA main stem as an anatomic structure,
visible as a hyperechogenic double reflex.
Although the imaging quality of the PMFBW is inferior to
the insonation through the LFBW, it offers adequate imaging conditions
in 60% of cases in those aged 60 years. In addition to the
transverse and coronal insonation planes through the temporal bone
window, the PMFBW enables the imaging of intracranial structures in a
sagittal plane, depicting the choroid plexus of the third ventricle,
the corpus callosum, and the hypophyseal groove. The frontal bone
windows in conjunction with the conventional temporal acoustic window
allow a more accurate size measurement of intracranial structures, as
could be demonstrated in our patient with a basilar head
aneurysm. In this study we observed a marked drop in imaging
conditions with increasing age. This effect was more pronounced in
women than in men. The most probable reason for this fact is increasing
frontal hyperostosis with increasing age. Overall, lack of a sufficient
acoustic window occurred more frequently compared with the conventional
temporal bone window, with an expected rate of up to 20% of
cases.1 The use of frontal bone windows for parenchymal
diagnostics in the group aged >60 years is limited by this
fact.
Color-/Doppler-Mode Sonography
The rate of depiction of the A2 segment of the ACA with the
use of the temporal bone window and frequency-coded TCCS is rather low,
with insonation rates between 40% and 65%.15 16 With the
use of the frontal bone windows, in >70% of cases flow velocity
measurements of the A2 segment of the ACA were possible in the group
aged 60 years. Our normal values of flow velocities are similar to
those found for the A1 segment of the ACA.1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 However,
the identification rate of the PCoA is low at 40% without echo
contrast enhancement and is not routinely possible. On the other hand,
the LFBW enables an angle-corrected flow velocity measurement of the
PCoA that is not possible in the temporal insonation plane. The drop in
the identification rates for the A1 ACA, M1 MCA, and PCA may be
explained by the unfavorable insonation angle in the frontal
examination plane.
In the frontal sagittal insonation plane, imaging of the A2
segment of the ACA, the pericallosal artery, and the ICVs is possible.
The identification rate of the ICVs by the paramedian frontal approach
is far higher than the results obtained by insonation through the
occipital bone when similar age groups are compared12
(60% versus 34% in those aged 60 years). Our reference values of
flow velocities in the ICV are in agreement with the results published
in the literature.12 Vascular imaging conditions
deteriorated with increasing age.
Effect of Echo Contrast Enhancement and Findings in
Patients
As expected by consideration of previous
studies,7 8 19 contrast enhancement resulted in a marked
improvement in the number and insonation length of the intracranial
vessels imaged. Contrast enhancement can compensate for the
deteriorating imaging conditions offered by the frontal bone windows in
the age group of the typical stroke patient. However, in those cases
without any acoustic penetration, no contrast-enhancing effect can be
expected.
Contrast-enhanced frontal TCCS enabled a more accurate determination of cross-flow conditions in those stroke patients with stenotic or occlusive disease of brain-supplying arteries because of an unambiguous assessment of the flow velocity and direction of the PCoA. In >40% of patients, the assessment of the basilar head region was possible through the frontal acoustic windows.
In summary, we have demonstrated the feasibility of frontal bone windows for TCCS examination. The frontal bone windows allow the insonation of vasculature and parenchyma in additional insonation planes not offered by the conventional temporal approach.
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Acknowledgments |
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The authors are indebted to Dr H.R. Duncker, Institute for Anatomy and Cellbiology, Justus-Liebig University, for his help in preparing the diaphanoscopies of the human skull.
Received October 22, 1998; revision received January 4, 1999; accepted January 15, 1999.
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