(Stroke. 1999;30:821-826.)
© 1999 American Heart Association, Inc.
Original Contributions |
Duplex Scanning Exploration of the Ophthalmic Artery for the Detection of the Hemodynamically Significant ICA Stenosis
From Angiology, Vascular Surgery (C.P., R.P., E.C.), and the Institute of Pathological Anatomy (F.G.), University of Florence, Florence, Italy.
Correspondence to Prof Giuseppe Nuzzaci, Via del Poggio alla Scaglia, 42, 50125–Firenze, Italy.
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Abstract |
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Background and Purpose—The North American and the European Carotid Endarterectomy Trials demonstrated a significant benefit of surgery in preventing stroke for patients with symptomatic hemodynamically significant internal carotid artery (ICA) stenosis. Because the 3 angiographic methods of measuring carotid stenosis provide discrepant results, the indication for surgery depends on the method used for the evaluation of the angiogram. The goal of this study was to verify whether color duplex scanning of the ophthalmic artery alone might be reliable for detection of the extracranial hemodynamically significant ICA stenosis.
Methods—Three groups of patients (351 total patients) with transient ischemic attack or minor stroke referred for possible carotid endarterectomy were examined by means of color duplex scanning of the ICA, transcranial Doppler, color duplex scanning of the ophthalmic artery, and angiography of the ICA.
Results—In the first group (n=31) the comparison of findings from each method and the direct measurement of the residual lumen of plaque removed "en bloc" showed that the findings of the ophthalmic artery color duplex scanning, subdivided into 5 categories—NP (normal positive), LP (low positive), NF (no flow), REV (reverse flow), PP (pathological positive)—were associated with the best overall agreement (96.7%). The accuracy of the various categories of the ophthalmic artery color duplex scanning signals was studied in the second group of patients (n=200). The results pointed out that all but low positive categories were associated with high diagnostic accuracy. Finally, the results obtained in the third group (n=120) showed that a significant increase in the specificity of the low positive signal could be obtained by processing this signal in terms of pulsatility index and of transmission of pulsatility index.
Conclusions—Our results suggest that the diagnostic capacity of color duplex scanning for the detection of ICA critical stenosis can be appropriately increased if it is performed also at the level of the ophthalmic artery and if the Doppler signals are processed on the basis of criteria we applied.
Key Words: Doppler, duplex • ophthalmic artery • stenosis • ultrasonography
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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The North American and the European Carotid Endarterectomy Trials1 2 have demonstrated a significant benefit of surgery in preventing stroke for patients with symptomatic hemodynamically significant internal carotid artery (ICA) stenosis. The detection of the hemodynamically significant ICA stenosis has become mandatory for all researchers in the diagnosis of ICA occlusive disease.
Arteriography provides an incomplete evaluation of the ICA stenosis because it images the lumen alone and does not give any information on the vessel wall. To accurately calculate the diameter stenosis, the residual lumen and the original diameter of the artery should both be measured.3 Furthermore, because the 3 angiographic methods of measuring carotid stenosis provide discrepant results, the indication for surgery depends on the method used for the evaluation of the angiogram.4 Finally, arteriography is not suitable for screening because of the ever-present risk of a disabling stroke and systemic complications5 6 7 8 9 10 and also because of its high cost.11 Ultrasound duplex scanning has become the leading routine method for the evaluation of ICA stenosis because not only is it noninvasive but it also appears capable of detecting the flow abnormalities associated with increasing degrees of narrowing.
Dawson et al12 have clearly shown that when skillful sonographers perform ultrasound studies it is possible to proceed to carotid endarterectomy without arteriography. Duplex scanning however, may be difficult when the bifurcation is very high, when the patient's neck is very thick, and when the carotid plaque is heavily calcified, preventing adequate insonation of the bulb.12 13 14
These limitations can be overcome if, as suggested by the pioneers of cerebrovascular ultrasound exploration,15 16 17 18 we perform additional studies of the collateral blood supply, which is automatically activated when the ICA narrowing becomes hemodynamically significant.19
The ophthalmic artery (OA) appears very suitable for study because of the following characteristics: (1) OA is the first branch of the ICA and therefore the nearest to the carotid bulb in which the stenosis is located; (2) according to its distribution, OA performs like a catheter that transfers straight away the values of the perfusion pressure gradient from downstream of the ICA stenosis toward the eyelids; (3) the easy insonation with color duplex scanning of the OA (OA CDS) allows us, without interference from the bony skull, to overcome the frequent limitations (5% to 19%)20 of transcranial Doppler ultrasonography (TCD) in the exploration of the middle cerebral artery and of the anterior cerebral artery because of the temporal bone thickness; and (4) finally, OA is placed at the watershed between the ICA and the external carotid artery (ECA) territories, therefore it is particularly liable to ischemias for hemodynamic reasons.
Previously, Spencer and Whisler21 applied duplex scanning of the OA for the detection of intracranial ICA stenosis, and Schneider et al22 used duplex scanning for the assessment of OA as a source of collateral cerebral blood supply. Finally, Wilterdink et al23 found that to reliably ascertain the hemodynamically significant ICA stenosis, OA duplex scanning should be associated with TCD. The aim of this study was to verify whether the OA CDS examination alone may be a reliable approach for the detection of the extracranial hemodynamically significant ICA stenosis.
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Subjects and Methods |
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We studied 3 groups of patients (n=351) with transient ischemic attack or minor stroke referred for possible carotid endarterectomy, by means of ICA CDS, TCD, color duplex scanning of the OA, and arteriography. Patients with severe contralateral stenosis or intracranial artery stenosis were excluded from this study.
Our protocol included the following. Before carotid
endarterectomy all patients underwent ICA CDS with
an Acuson 128 XP ultrasound device with 7.0- and 5.0-MHz linear array
transducers. The peak systolic velocity and the
end-diastolic velocity at the stenotic area were
evaluated, and the findings were classified, according to the method of
Bluth et al,24 as critical ICA stenosis when the
peak systolic velocity was 
250 cm/s, and the
end-diastolic velocity was 100 cm/s.
TCD was performed with a hand-held system that used a 2-MHz Doppler probe (Multidop X4, DWL Elektronische Systeme GmbH) as described by Aaslid.25 The findings were classified as pathological when there was a reversal of flow in the ipsilateral anterior cerebral artery associated with appropriate effects of the ipsilateral and contralateral common carotid compression (CCC). This maneuver was always carried out at the farthest place from the carotid bulb only when, as shown by ICA CDS, any severe atherosclerotic changes were lacking.
The OA CDS signal was obtained by applying the 7.0-MHz Acuson probe on the closed eyelid with the patient in the supine position. The OA is easily located by aiming the Doppler beam near the optic nerve at a depth of 4 to 6 cm. Acuson 128 XP provides an ocular program that foresees <17 mW/cm2 of ultrasound emission at the transducer surface according to the FDA rules.21 The patient was invited to turn the eyes toward the contralateral side to avoid the refractive power of the ocular lenses.
Under normal conditions the perfusion pressure in the territory of the OA is higher than in the ipsilateral ECA territory. The direction of flow is toward the ECA territory and, therefore, the Doppler signal of the OA is anterograde.
Under pathological conditions, as long as the OA perfusion pressure decreases, the amplitude of the anterograde Doppler signal progressively decreases, reaching the basal line when the pressure gradient at the border between the 2 territories becomes equal to 0. When the perfusion pressure becomes higher in the ECA territory, the direction of the OA flow reverses. Finally, if the ICA stenosis is associated with stenosis or occlusion of the ipsilateral ECA, the perfusion pressure in the ECA territory may become very low. In that case the OA signal may still stand anterograde.
According to Figure 1
, the OA CDS
findings were classified as normal positive (NP) when the signal
obtained was anterograde. In that case the systolic
blood velocity of OA was 48.5±7.8 cm/s on both eyes. Moreover the
ipsilateral CCC was associated with a significant reduction of the
ipsilateral OA systolic velocity. The signal was classified low
positive (LP) when the amplitude of the Doppler signal on the
stenotic side was <25% of that found on the contralateral eye
and the ipsilateral CCC was associated with the disappearance of the OA
flow. This parameter was 12±4.6 cm/s. The signal was
classified no flow (NF) when no Doppler signal was detected on the
stenotic side and reverse (REV) when the signal on the
stenotic side was backward. Finally, it was classified
pathological positive (PP) when the signal disappeared during the
contralateral CCC and it did not change during the ipsilateral CCC. The
detection of the OA CDS signals was performed 3 times on each eye. NF,
REV, and PP signals were assessed qualitatively, whereas the NP and LP
signals were quantified according to the average of the 3 values of the
systolic velocity.
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Arteriography was performed using the intra-arterial
digital subtraction technique via the femoral artery with the injection
of contrast medium at the level of the first part of the aortic arch.
Biplanar images were obtained for each ICA. The measurements of ICA
diameter reduction were performed by the NASCET method and by visual
estimation by 2 independent angiographers. All measurements were
blindly assessed. Three experienced examiners (D.R., I.N., and F.B.)
performed ICA CDS, TCD, and OA CDS examinations without knowledge of
the degree and side of the stenosis or occlusion. Table 2 shows the criteria used for
discrimination between hemodynamically and
nonhemodynamically significant ICA
stenosis.
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Statistical analysis was performed with the Student's (2-tailed) t test, and the results are given as mean±SD. All subjects gave informed consent to participate in the study, which was approved by the Ethics Committee of the University of Florence.
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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In the first group of 31 patients (24 men and 7 women; mean age, 64 years; age range, 52 to 73 years) we compared the findings of ICA angiography, color duplex sonography of ICA, TCD, and (4) OA CDS versus the residual lumen of ICA obtained by the whole plaque removed en bloc at the time of carotid endarterectomy.
The 31 plaques consisted of short portions of the common carotid artery
and of the ECA with the diseased segment of the ICA, which always
included the point of maximum lumen encroachment. They were promptly
placed in 10% formalin and decalcified with EDTA for 3 hours. The
specimens were then sectioned horizontally at 0.2-cm intervals with a
razor blade and laid in series so that slides of each section could be
obtained. A slide scanner scanned the slide of the section with the
smallest residual lumen, and the images were stored on floppy
diskettes. The luminal area of each stored image was measured
digitally, and the minimal residual diameter was calculated from this
area measurement with a Corel computer program (Corel Corp, Ltd). The
residual lumen diameter measurements were rounded to the nearest
0.1 mm, ie, 0.15 mm was recorded as 0.2 mm. If the
vessel had 2 largely different diameters (ie, it was asymmetrical), the
value we chose was the mathematical mean of the 2 values. We considered
the ICA stenosis as hemodynamically significant
when the residual lumen was 
1.5 mm and
nonhemodynamically significant when the residual lumen
was >1.5 mm.
Thirteen plaques showed a residual lumen 1.5 mm and, therefore,
were considered hemodynamically significant
stenosis; 18 plaques showed a residual lumen >1.5 mm and
were considered as nonhemodynamically significant
stenosis.
In the first group of plaques (hemodynamic ICA stenosis) arteriography gave appropriate answers versus the gold standard in 11 and nonappropriate answers in 4 (false-positives), with specificity equal to 75.0%. In the second group of plaques (nonhemodynamic ICA stenosis), arteriography gave appropriate answers in 12 and nonappropriate answers in 1 (false-negative), with sensitivity equal to 91.6%. In 3 cases, the answers were considered nondiagnostic. The overall agreement between the gold standard and arteriography (accuracy) was equal to 74.2%.
ICA CDS in the first group of plaques gave appropriate answers versus the gold standard in 10 and nonappropriate answers in 0 (specificity=100%). In the second group of plaques, this method gave appropriate answers in 17 and nonappropriate answers in 0 (sensitivity, 100%). In 4 cases, the answers were nondiagnostic because of the presence of heavy calcification of the plaque. The overall agreement between the gold standard and color duplex scanning was 87.0%.
The TCD in the first group of plaques gave appropriate answers in 10 cases and nonappropriate answers in 0 (specificity, 100%), and in the second group of plaques this method gave appropriate answers in 17 cases and nonappropriate answers in 1 (sensitivity, 91.0%). In 3 cases the test was nondiagnostic because the temporal windows were closed. The overall agreement between the gold standard and TCD was 87.0%.
Finally, the OA CDS signals in the first group of plaques gave appropriate answers in 12 cases (in 6 the signal was REV, in 4 it was NF, in 1 it was PP, and in 1 it was LP) and nonappropriate answers in 0 (specificity, 100%), whereas in the second group of plaques the OA CDS gave appropriate answers in 18 (in these cases the signals were NP) and nonappropriate answers in 1 (LP signal; sensitivity, 92.3%). The overall agreement between this method and the gold standard was 96.7%.
In a second group of 200 patients (148 men and 52 women; mean age, 68.4
years; 397 ICAs), we verified, on the basis of the results obtained in
the first group, the accuracy of each of the 5 categories of the OA
signals versus its screening capacity between the
hemodynamically and nonhemodynamically
significant ICA stenoses. The results obtained in this second
group of patients are shown in Figure 2.
In this group, 285 ICAs showed a nonhemodynamically
significant stenosis, 51 a hemodynamically
significant stenosis, and 61 an ICA occlusion.
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The NP signal was in any case associated with a nonhemodynamically significant ICA stenosis. The NF signal was constantly associated with hemodynamically significant ICA occlusive disease: 13 ICAs with 80% to 99% luminal narrowing and 16 ICAs with occlusion of the lumen. The REV signal was constantly associated with hemodynamically significant ICA occlusive disease: 18 ICAs with 80% to 99% stenosis of the lumen and 19 ICAs with occlusion of the lumen. The PP signal was constantly associated with hemodynamically significant ICA occlusive disease: 10 ICAs with 80% to 99% stenosis and 10 ICAs with occlusion of the lumen.
The LP Doppler signal was associated with 90 ICAs with <60% nonhemodynamically significant stenosis, 30 ICAs with 60% to 79% nonhemodynamically significant ICA stenosis, 10 ICAs with 80% to 99% hemodynamically significant ICA stenosis, and 16 ICAs with occlusion of the lumen.
Finally we examined a third group of 120 patients (63 men, 57 women; mean age, 69.1 years; age range, 56 to 80 years; 240 ICAs), who showed LP signal at 1 eye. Toward the aim of increasing the specificity of LP signal, we processed this parameter in terms of the pulsatility index (PI)26 : (PI=systolic velocity-diastolic velocity/mean velocity). We also calculated the transmission of the PI (TPI)27 : (TPI=PI of the stenotic side/PI of nonstenotic side x100) between the 2 OAs. Because the reproducibility of PI, as automatically provided by our device, was low, we measured straight away on the display the value of the systolic and diastolic velocities. Then we traced the envelope of each OA CDS signal and received automatically the values of PI. In 5 patients without ICA occlusive disease, we tested the maximum and the mean reproducibilities of PI (5.9% and 4.7%, respectively) and of TPI (6.1% and 4.2%, respectively). We classified the signal as NP if the TPI value was >90% and LP if this value was <80%, whereas the TPI values ranged between 80% and 90% and were classified "uncertain values." On the basis of arteriography, ICA CDS, and TCD, the ICAs were classified into 3 subgroups: (1) patients with nonhemodynamically significant stenosis (n=55 with <60% stenosis and n=25 with 60% to 79% ICA stenosis); (2) n=15 patients with 80% to 99% ICA stenosis; and (3) n=25 patients with occlusion.
The OA PI value was 1.29±0.54 ipsilateral to an ICA with hemodynamically significant occlusive disease, whereas it was 1.62±0.37 in the presence of noncritical ICA stenosis (P<0.01). The average length for a complete measurement of TPI in each patient was 8.1±2.5 minutes.
In the first subgroup, the values of TPI ranged between 89% and 107%,
mean±SD 96.9%±5.1 (<60% ICA stenosis), and between 87%
and 106%, mean±SD 96.1%±5.9 (60% to 79% ICA stenosis). In
the second subgroup, the value of TPI ranged from 48% to 84%,
mean±SD 68.2±9.8 (80% to 99% ICA stenosis), and in the
third subgroup 43% to 88%, mean±SD 69.8%±12.9 (occlusion of ICA).
The difference between the mean value of TPI of the ICAs of the first 2
subgroups (96.6±5.3) and that of the other 2 subgroups (69.2%±11.7)
was statistically significant (P<0.01). Figure 3 also shows that in 7 cases the TPI
values dropped in the "uncertain area": 2 cases of the first
subgroup, 2 of the second, and 3 of the third subgroup; therefore there
were 2 cases of false-positive results and 5 cases of false-negative
results.
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Our results point out that the duplex scanning approach of the OA appears very suitable for the assessment of hemodynamically significant ICA occlusive disease. The comparison of the gold standard and the findings obtained by the other methods of ICA examination has shown that the ones delivered by OA CDS were associated with the overall best agreement: OA CDS, 96.7%; ICA CDS, 87.0%; TCD, 87.0%; and arteriography, 74.2% (Table 1
).
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Figure 2
shows that not all of the 5 categories of the OA CDS
signals have shown the same degree of reliability. NP, NF, REV, and PP
parameters showed a very high degree of specificity
(100%). The NP parameter was constantly associated with
nonhemodynamically significant ICA stenosis,
whereas NF and REV signals were, in any case, associated with
hemodynamically significant ICA occlusive disease.
However, these 2 parameters were not able to discriminate
between hemodynamically significant stenosis
and occlusion of the ICA: NF and REV signals were found in 13 and 18
patients, respectively, with hemodynamically
significant ICA stenosis and in 16 and 19 patients with ICA
occlusion. These results are in keeping with those obtained by
others.20
The PP OA CDS signal, for which the incidence rate has been equal to
5% of all ICAs studied and which can be easily discriminated by NP and
LP signals on the basis of the ipsilateral and contralateral CCCs, was
found in 10 patients with hemodynamically significant
ICA stenosis and in 10 patients with ICA occlusion. Therefore,
this signal also appeared very reliable for the screening of
hemodynamically ICA occlusive disease, but it did not
discriminate between ICA stenosis and ICA occlusion. LP signal,
on the other hand, has shown a very low specificity (18%). This
parameter was associated with
hemodynamically nonsignificant ICA stenosis in
90 patients and with hemodynamically significant ICA
stenosis or occlusion in 26 patients. The very low accuracy of
the LP OA CDS signal may be related to the following: (1) the
abnormal origin of OA from the middle meningeal artery (branch of ECA)
whose frequency ranges between 2% and 5%28 ; (2) the
tortuous pathway of the OA, associated with eye movement, makes the
angle between the ultrasound beam and the artery lumen variable;
(3) the absolute value of the velocity measurement is more liable to be
wrong primarily when its value is low. These limitations may be
reliably overcome if we process the LP signal in terms of PI, which, as
the result of a ratio, is less dependent on the ultrasound beam angle
of insonation. The results shown in Figure 3 point out that the
LP OA CDS signal when processed in terms of PI and TPI can properly
discriminate between hemodynamically nonsignificant and
significant ICA stenosis. The >90% TPI value (the value with
the highest sensitivity) was in all cases associated with
hemodynamically nonsignificant ICA stenosis,
and the <80% TPI value (the value with the highest specificity) was
associated with hemodynamically significant ICA
stenosis or occlusion. Finally, the TPI values ranged between
80% and 90% and appeared as "uncertain values."
Because the ICA occlusion cannot be subjected to carotid
endarterectomy, the most clinically relevant
diagnostic problem concerns the discrimination between
hemodynamically and nonhemodynamically
significant ICA stenosis. The results shown in Figure 3
point out that if we set the cutoff point at the TPI value of 90% all
the hemodynamically significant ICA stenoses
are discriminated, and a few (only 2 ICAs in our group of patients)
hemodynamically nonsignificant ICA stenoses may
be diagnosed as "false-positives." However, because for the
subgroup of transient ischemic attack patients with severe ICA
stenosis the average annual risk of stroke in nonoperated
patients was 14% per year and the perioperative risk
of any stroke or death was 5.8% (and functional deficit persisting
beyond 90 days and death was 2.1%),1 we believe it is
better to use a cutoff point that provides the best sensitivity rather
then the best specificity.
In conclusion, our results confirm the statement that the exploration of the collateral blood supply in an arterial territory can be a reliable way to ascertain the hemodynamic meaning of the artery stenosis present in that territory. Also, if the advent of duplex ultrasound modality has unfortunately made the periorbital Doppler sonography a procedure that is not routinely performed at present for the extracranial ICA exploration, that approach still is the most cost-effective Doppler approach for the detection of the extracranial critical stenosis of this artery.29 Our results suggest that according to the periorbital Doppler principle if the Duplex ICA examination is performed also at the level of the OA, and if the obtained signals are assessed on the basis of the criteria we applied, its diagnostic capacity in the detection of the critical stenosis and its cost-effectiveness both can be appropriately increased.
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Acknowledgments |
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We thank Dr G. M. Von Reutern for reviewing our manuscript.
Received May 28, 1998; revision received October 15, 1998; accepted October 15, 1998.
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