(Stroke. 1995;26:214-217.)
© 1995 American Heart Association, Inc.
Articles |
From Clinica Neurologica (G.P.A., M.M.) and Cattedra di Radiologia (R.G., F.P.), University of Brescia (Italy).
Correspondence to Gian Paolo Anzola, MD, Clinica Neurologica, II Divisione di Neurologia, P le Spedali Civili 1 25125, Brescia, Italy.
| Abstract |
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Methods Twenty-five patients with unilateral ICA occlusion (n=20) or tight stenosis (n=5) demonstrated by duplex scanning or angiography were studied with both TCD and MRA. Three-dimensional time-of-flight MRA was used for the evaluation of extracranial-intracranial ICAs. Collateralization through the circle of Willis was investigated by means of selective two-dimensional MRA with presaturation of the carotid siphon, ophthalmic artery, or basilar artery. TCD was performed according to published standards: Anterior, middle, and posterior cerebral arteries were insonated through the temporal window, and carotid siphon and ophthalmic artery were assessed through a transorbital approach. Collateralization through the anterior circle of Willis was assumed if anterior cerebral artery flow was reversed, through the external carotid artery if ophthalmic artery flow was reversed, and through the basilar artery if the ratio of ipsilateral to contralateral posterior cerebral artery velocity was greater than 50%. TCD and MRA were performed by different investigators unaware of the results obtained with the other technique.
Results In every case time-of-flight MRA demonstrated the ICA
occlusion or stenosis. There was an excellent correlation (
=0.64)
between TCD and MRA in assessing the hemodynamic contribution of the
anterior part of the circle of Willis, whereas MRA was unable to detect
the anastomotic pathway of the ophthalmic artery (
=0.32). The
contribution of the posterior communicating artery was difficult to
assess with both techniques, but in three cases only MRA showed
unequivocal evidence of collateralization. In three cases of middle
cerebral artery stenosis TCD was superior to MRA in demonstrating the
patency of the vessel.
Conclusions TCD and MRA should be considered complementary techniques. Combining the findings of both examinations may help to better understand the changes in intracranial hemodynamics produced by extracranial carotid occlusion. The contribution of the ophthalmic pathway, although important for the intraorbital structures, is probably of limited functional significance to the hemispheric blood supply.
Key Words: angiography, magnetic resonance carotid artery diseases diagnostic imaging Doppler
| Introduction |
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Given these reciprocal limitations, we have tried to compare the respective efficacy of TCD and MRA in assessing the hemodynamics of intracranial vessels in patients with occlusion of the extracranial internal carotid artery (ICA).
| Subjects and Methods |
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In 9 cases intra-arterial digital subtraction angiography with selective injection of the common carotid and vertebral arteries (IADSA) was available for comparison. In 11 additional cases IADSA was incomplete in the intracranial study. There was complete agreement in the 20 patients in whom angiography could be compared with duplex scanning of the neck vessels.
All MRA studies were performed on a 1.5-T system (Magnetom SP 63, Siemens Medical Systems). Time-of-flight (TOF) MRA was performed to obtain a combined anatomic-functional study of cerebral circulation. A circularly polarized head coil was used for both extracranial and intracranial circulation. Three-dimensional (3D) Fourier transform FISP gradient-echo sequences were used for the evaluation of the ICA from the bifurcation through the siphon with the following scan parameters: repetition time, 60 milliseconds; echo time, 7 milliseconds; flip angle, 20°; field of view, 250 mm; 64-mm coronal slab with 64 partitions, including vertebral and basilar arteries. For the baseline study of the anatomy of intracerebral vessels, two-dimensional (2D) TOF MRA (fast low-angle shot sequences; repetition time, 30 milliseconds; echo time, 10 milliseconds; flip angle, 30°; sequential acquisition of 3-mm-thick slices with 40% overlap) was preferred to 3D TOF MRA, at the expense of spatial resolution, for two reasons: (1) it is less sensitive to saturation of slow flow, which can represent a potential source of error in the identification of major vessel occlusion, and (2) it permits a considerable reduction of the examination time.
The evaluation of flow dynamics in the circle of Willis was obtained with 2D selective MRA, which consists of a combination of 2D techniques with radio frequency presaturation pulses.2 Ten-millimeter-thick presaturation bands are oriented along the course of the desired vessel to evaluate the dependent vascular territory. Presaturation causes a loss of flow signal intensity in the presaturated vessel and in its branches, including collateral flow, without affecting the vessels not coursing through the band.3 4 The middle cerebral artery (MCA) flow was visually assessed in the axial plane before and after presaturation of (1) the contralateral carotid siphon, for collateral flow through the anterior communicating artery (ACoA); (2) the ophthalmic arteries (OPHT), for collateral flow through the ipsilateral external carotid artery; and (3) the vertebral arteries, for collateral flow through the posterior communicating artery (PCoA). It was assumed that the presaturated vessel was carrying a significant portion of collateral flow if the signal of the MCA either disappeared or was significantly dimmed on visual inspection. Nineteen patients underwent a complete study, and in 16 of them it was possible to obtain a simultaneous presaturation of two or even all three putative collateral vessels. In the remaining 6 patients the study was incomplete and included the following: PCoA plus ACoA in 1 patient, OPHT plus ACoA in 2 patients, and ACoA alone in 3 patients. Therefore, the ACoA was assessed in all 25 patients, the OPHT in 21, and the PCoA in 20.
The imaging volumes were processed by a maximum intensity projection algorithm and reviewed together with the single slices to avoid loss of information due to artifacts in electronic reconstruction.
The Figure
is an example of the usefulness of MRA for
the noninvasive assessment of the anatomic variants of the circle of
Willis.
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As for TCD, the anterior cerebral artery (ACA), MCA, and posterior cerebral artery (PCA) were insonated through the temporal window, carotid siphon, and OPHT through the transorbital approach, according to published standards.5 6 Collateralization through the anterior part of the circle of Willis was assumed if ACA flow ipsilateral to the carotid occlusion was reversed (this usually occurred in conjunction with the acceleration of the contralateral ACA), through the external carotid artery if ophthalmic flow was reversed, and through the basilar artery if the ratio of ipsilateral to contralateral velocity in the PCA exceeded 50%.7 8 The criterion set for PCA was somewhat more conservative than others adopted in the literature and was based on our data for the normal population, which yield a PCA mean flow velocity of 42±11 cm/s and an average side-to-side asymmetry of 16±16% (G.P.A. et al, unpublished data, 1991). In 24 patients all three possible collateral sources were assessed; in 1 patient the ophthalmic flow could not be studied.
Carotid compression was performed on the asymptomatic side when deemed appropriate and safe. It was done in 3 patients in whom the asymptomatic ICA was undamaged and the collateral supply to the symptomatic hemisphere was carried by both the ACoA and the ipsilateral PCoA.
MRA and TCD were always done within 24 hours of each other and were performed an average of 18±7 days after the onset of symptoms. The results of one exam were unknown to the operator of the other exam.
| Results |
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Overall the results of selective MRA hemodynamic evaluation were
technically satisfactory for comparison with TCD in all 25 patients for
the ACoA, in 21 for the OPHT, and in 20 for the PCoA (see "Subjects
and Methods"). For the ACoA the two methods were concordant in 84%
of cases (Table 3
). In 3 cases the reversal of flow in
the ACA, as demonstrated by TCD, was apparently without functional
significance, as presaturation of the contralateral siphon on MRA did
not affect the signal in the MCA. In 1 patient TCD was unable to detect
the reversal of flow in the ACA. For the PCoA the agreement was
somewhat less satisfactory (80%) but still significant. Three of 4
discordant cases were due to the relative insensitivity of TCD in
demonstrating the contribution of the PCoA. In contrast, for the OPHT
the agreement in 62% of cases was counterbalanced by the disagreement
in 38% (Table 3
). In all cases of mismatch, MRA failed to confirm the
activation of the ophthalmic collateral pathway indicated by TCD.
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Among the 9 patients in whom IADSA was also performed, TCD and MRA were concordant in 5 cases: Arteriographic findings confirmed TCD and MRA in 4 of these cases, but IADSA failed to demonstrate the contribution of the contralateral internal carotid system through the ACoA in 1 patient with a 95% stenosis of the right ICA. In 4 patients TCD and MRA were discordant: In 2 TCD was unable to show the PCoA pathway, in 1 it failed to appreciate the inversion of the flow in the ACA, and in 1 MRA missed the ophthalmic contribution. The IADSA findings were in agreement with MRA in the first 3 cases, but in the last they confirmed the relative insensitivity of MRA in imaging the ophthalmic collateral pathway. Furthermore, in 2 patients IADSA showed additional collateral pathways through pial anastomoses.
Finally, Table 4
shows the distribution of the different
patterns of collateralization as shown by TCD and MRA. In approximately
50% of cases two collateral pathways were simultaneously at work, as
shown by both TCD and MRA. TCD indicated as equally frequent the
activation of one or three collateral pathways (25% each), whereas
according to MRA the single collateral pathway accounted for 31% of
all patients compared with 11% for the three concomitant pathways. No
collateralization was found in 1 patient by TCD and in 2 patients by
MRA. The single most frequent collateral pathway was the ACoA,
demonstrated in 71% of patients by TCD and in 73% by MRA.
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| Discussion |
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TCD and MRA showed excellent correlation in assessing the contribution
of the anterior circle of Willis and the high prevalence of the ACoA
(>70%) as a collateral pathway (Tables 3
and 4
). The three cases in
which MRA failed to appreciate the contribution of ACoA were those in
which the ICAs were bilaterally occluded (two cases of bilateral
thrombosis, one of unilateral thrombosis with contralateral >90%
stenosis) and the blood supply to the brain was actually carried by the
basilar or the external carotid artery. This explains the apparent
discrepancy of the findings: The blood flow in the A1 tract of the ACA
was actually reversed on one side, but this was without hemodynamic
consequences because the main blood supply came from alternative
sources.
The correlation between TCD and MRA in the appreciation of the contribution of posterior-to-anterior anastomoses was slightly less promising than for the anterior circle of Willis (84% versus 80%, respectively). This we could attribute to the relatively arbitrary criterion that we had adopted to assume the posterior contribution (>50% increase in ipsilateral PCA velocity compared with contralateral). Given the variability of diameter of the posterior vessels, this criterion is likely to have reduced the sensitivity of TCD with respect to MRA, as TCD failed to recognize the contribution of PCoA in three cases, which was confirmed by angiography in two patients. In summary, TCD actually underestimated the anastomoses between carotid and basilar arteries. The adoption of a more refined criterion, such as the addition of the systematic compression of vertebral arteries, might improve the accuracy of TCD in the future.
Finally, it is apparent from Table 3
that the assessment of collateral
flow through the OPHT represents the major mismatch between the
two techniques. In all discordant cases TCD showed flow reversal in the
OPHT, suggesting the activation of the physiological external-internal
carotid artery bypass, whereas MRA presaturation of the OPHT failed to
affect the signal in the MCA. Therefore, it is clear that either TCD
overestimates or MRA underestimates the contribution of the ipsilateral
compensatory pathway. One intrinsic limitation of TCD is that the
reversal of flow in the OPHT actually represents the reversal
of the pressure gradient between external and internal carotid artery
territories, but is no proof by itself that the external carotid artery
provides an effective collateralization to the ipsilateral hemisphere.
It is thus likely that at least in some patients, ophthalmic reversal,
although necessary for the blood supply to the intraorbital structures,
especially the eye, may have little functional significance for the
hemispheric blood flow. It is perhaps worth noting that in all but one
of the eight cases in which TCD indicated the activation of
external-internal carotid artery bypass and MRA was negative, at least
one other collateral pathway was at work (ACoA four times and PCoA
twice, both in one case). Moreover, as shown in Table 4
, the MCA was
recanalized by the OPHT alone in only 2 of 18 cases of ophthalmic
reversal. This agrees with those studies that have reported on the
activation of ophthalmic collaterals in patients with reduced cerebral
perfusion pressure but not in those with normal cerebrovascular
reserve.9 10 On the other hand, the disappearance of the
MRA signal in the MCA after presaturation of the putative collateral
vessel does not completely rule out the possibility that other sources
carry a small fraction of flow, as MRA technology is still insufficient
in imaging very slow flow. If, for instance, both the ACoA and
OPHT contribute to the blood supply of one MCA, but the former is
quantitatively preponderant, MRA may fail to appreciate the ipsilateral
contribution simply because it is unable to image the residual slow
flow that remains after presaturation of the contralateral siphon. A
very recent study on intracranial collateral blood flow in patients
with ICA occlusion, the design of which is similar to the present
report, came essentially to the same conclusion as to the inadequacy of
MRA in imaging of ophthalmic collaterals.11
In conclusion, our findings suggest that TCD and MRA are complementary techniques. The former is probably more sensitive in depicting all the potential sources of collateralization, and the latter is more specific in delineating which source, among multiple possible pathways, has the greatest functional importance.
Received July 7, 1994; revision received November 7, 1994; accepted November 8, 1994.
| References |
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