Journal of Neurology, Neurosurgery, and Psychiatry, 1979, 42, 1133-1 140 Semiquantitative evaluation of ophthalmic collateral flow in carotid artery occlusion: ultrasonic doppler study HIRAO KANEDA, TADAYOSHI IRINO, MANABU WATANABE, EIJI KADOTA, AND MAMORU TANEDA From the Division of Cerebrovascular Diseases, Hanwa Hospital, Osaka, Japan SUM MARY The reliability of quantitative evaluation by doppler ultrasound with regard to the ophthalmic collateral blood flow in patients with carotid artery occlusion was estimated. The ultrasonic doppler flow signals of the ophthalmic collateral flow of 54 carotid occlusions were classified into four types and three degrees-high, moderate, and low reversed flow patterns- and were compared with the angiographic findings of the collateral flow classified into three grades-good, poor, and none. With the exception of three cases, the ultrasonic doppler flow patterns of the collateral flow correlated well with the angiographic findings in 54 occluded carotid arteries. The clinical symptoms of internal carotid occlusion are various, from no symptom to severe neuro- logical deficit. One of the reasons for the sympto- matic variation is the amount of collateral blood flow which flows into the distal territory of the occluded portion of the carotid artery through the ophthalmic artery, the circle of Willis, and/or other arteries. Therefore, it is clinically important to evaluate the collateral flow in patients with carotid artery occlusion. Although angiography is the best method for evaluating the collateral flow, its use is restricted because of its invasive nature and side effects. Much attention has been focused on the noninvasive evaluation of the collateral flow with the ultrasonic doppler technique. A patient with carotid occlusion frequently has a collateral flow through the ophthalmic artery which is often detectable as a "reversed" blood flow by the ultrasonic doppler flowmeter. Based on this pathological phenomenon, many authors (Muller, 1973; Hyman, 1974; Katz et al., 1976; Lye et al., 1976; von Reutern et al., 1976) re- ported that an occlusion or high grade stenosis of the carotid artery had been diagnosed non- invasively using doppler ultrasound. However, quantitative evaluation of the ophthalmic col- lateral flow by doppler ultrasound has not been Address for reprint requests: Dr Hirao Kaneda, Hanwa Memorial Hospital, 73-7, Karita-cho, Sumiyoshi-ku, Osaka 558, Japan. Accepted 21 April 1979 studied previously. The purpose of the present study was to evaluate by comparing the angiograms whether the quantitative findings of the doppler ultra- sound are reliable with regard to ophthalmic collateral flow. Patients and methods Fifty-four occluded internal or common carotid arteries of 51 patients (20 women, 31 men) were studied. Their mean age was 62.9 years. The clinical presentation ranged from acute to chronic stage within one year of the onset of the stroke. A directional ultrasonic doppler flowmeter was connected to a probe transmitting an ultrasound frequency of 5 MHz. The flowmeter had two filters to separate the signal into two signals corresponding to flow toward probe and flow away from probe. Each blood flow signal was recorded on a magnetic tape recorder and analysed by a sound spectrograph (Rion, SG-07, Tokyo) to pro- duce a sonogram in which we called the maximum blood flow velocity at systole as "S" and that at diastole as "d" (Fig. 1). In the sonogram of reversed ophthalmic blood flow caused by carotid occlusion, we defined the maximum systolic blood flow (S) as a reversed ophthalmic blood flow index for simplification, and we measured this in each patient. 1133 Protected by copyright. on March 15, 2020 by guest. http://jnnp.bmj.com/ J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.42.12.1133 on 1 December 1979. Downloaded from
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Journal ofNeurology, Neurosurgery, and Psychiatry, 1979, 42, 1133-1 140
Semiquantitative evaluation of ophthalmic collateralflow in carotid artery occlusion: ultrasonic dopplerstudyHIRAO KANEDA, TADAYOSHI IRINO, MANABU WATANABE,EIJI KADOTA, AND MAMORU TANEDAFrom the Division of Cerebrovascular Diseases, Hanwa Hospital, Osaka, Japan
SUM MARY The reliability of quantitative evaluation by doppler ultrasound with regard to theophthalmic collateral blood flow in patients with carotid artery occlusion was estimated. Theultrasonic doppler flow signals of the ophthalmic collateral flow of 54 carotid occlusions wereclassified into four types and three degrees-high, moderate, and low reversed flow patterns-and were compared with the angiographic findings of the collateral flow classified into threegrades-good, poor, and none. With the exception of three cases, the ultrasonic doppler flowpatterns of the collateral flow correlated well with the angiographic findings in 54 occludedcarotid arteries.
The clinical symptoms of internal carotid occlusionare various, from no symptom to severe neuro-logical deficit. One of the reasons for the sympto-matic variation is the amount of collateral bloodflow which flows into the distal territory of theoccluded portion of the carotid artery throughthe ophthalmic artery, the circle of Willis, and/orother arteries. Therefore, it is clinically importantto evaluate the collateral flow in patients withcarotid artery occlusion. Although angiography isthe best method for evaluating the collateral flow,its use is restricted because of its invasive natureand side effects. Much attention has been focusedon the noninvasive evaluation of the collateralflow with the ultrasonic doppler technique.A patient with carotid occlusion frequently has
a collateral flow through the ophthalmic arterywhich is often detectable as a "reversed" bloodflow by the ultrasonic doppler flowmeter. Basedon this pathological phenomenon, many authors(Muller, 1973; Hyman, 1974; Katz et al., 1976;Lye et al., 1976; von Reutern et al., 1976) re-ported that an occlusion or high grade stenosis ofthe carotid artery had been diagnosed non-invasively using doppler ultrasound. However,quantitative evaluation of the ophthalmic col-lateral flow by doppler ultrasound has not beenAddress for reprint requests: Dr Hirao Kaneda, Hanwa MemorialHospital, 73-7, Karita-cho, Sumiyoshi-ku, Osaka 558, Japan.Accepted 21 April 1979
studied previously.The purpose of the present study was to
evaluate by comparing the angiograms whetherthe quantitative findings of the doppler ultra-sound are reliable with regard to ophthalmiccollateral flow.
Patients and methods
Fifty-four occluded internal or common carotidarteries of 51 patients (20 women, 31 men) werestudied. Their mean age was 62.9 years. Theclinical presentation ranged from acute to chronicstage within one year of the onset of the stroke.A directional ultrasonic doppler flowmeter was
connected to a probe transmitting an ultrasoundfrequency of 5 MHz. The flowmeter had twofilters to separate the signal into two signalscorresponding to flow toward probe and flow awayfrom probe. Each blood flow signal was recordedon a magnetic tape recorder and analysed by asound spectrograph (Rion, SG-07, Tokyo) to pro-duce a sonogram in which we called the maximumblood flow velocity at systole as "S" and that atdiastole as "d" (Fig. 1). In the sonogram ofreversed ophthalmic blood flow caused by carotidocclusion, we defined the maximum systolic bloodflow (S) as a reversed ophthalmic blood flow indexfor simplification, and we measured this in eachpatient.
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Fig. 1 Block diagram of a directionalultrason.c doppler flowmeter with dualfilter type (upper). Illustrativepresentation of a sonogram of bloodflow analysed by the sound spectrograph(lower).
Sonogram of blood flow
50
>, NU T
e-
0Time (270 mm/24 s)
Blood flow in the territory of the ophthalmicartery is detectable in two regions. One is on theskin of the upper eyelid about 10 mm above andlateral to the corneal midpoint where blood flowin the ophthalmic artery can be detected. Theother is on the inner canthus near the orbitalfissure where blood flow in the medial frontalartery, a branch of the ophthalmic artery, can bedetected. The former technique was adopted inthe present study because it is more informativethan the medial frontal artery blood flow detection(Kaneda et al., 1978).
Carotid angiograms were made in all subjects,using 7.5 ml of 60% amidotrizoate as contrastmedium, injected into the common carotid arteryat a speed of 7.5 ml/second. Serial angiogramswere obtained using an automatic injector and anautomatic cassette changer. Intracranial filling ofthe contrast medium through the ophthalmicartery was carefully observed to determine thequantity of this collateral blood flow.
If more than one angiogram or doppler ex-amination was performed in a patient, oneangiogram and one doppler study with theshortest time interval were chosen and compared.
Results
CAROTID ANGIOGRAPHY
Ophthalmic collateral flow associated with carotidartery occlusion was classified into three grades.When the contrast medium flowed into the middlecerebral artery and its branches through theophthalmic artery as shown in Fig. 2, the flowwas defined as "good collateral flow." If the con-trast medium only filled to the syphon of the in-ternal carotid artery or to the stem of the middlecerebral artery without filling its branches (Fig. 3),the flow was defined "poor ophthalmic collateralflow." When there was no collateral flow via theophthalmic artery (Fig. 4), the definition was "noophthalmic collateral flow."There were seven patients with good ophthalmic
collateral flow, 10 with poor collateral flow, and37 with no collateral flow.
DOPPLER ULTRASOUNDSonograms of the reversed ophthalmic blood flowof the 32 patients were arranged according to thevalue of "S" from high degree to low (Fig. 5).The results were then divided into three degrees.
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Semiquantitative evaluation of ophthalmic collateral flow in carotid artery occlusion
A
Fig. 2 A ngiogram of a 65 year old man showing aninternal carotid occlusion (lower arrow) and a goodcollateral flow through the ophthalmic artery (upperarrow).
That higher than 38 mm (=3.17 kHz) was definedas a "high reversed flow"; from 19 mm(=1.58 kHz) to 38 mm (=3.17 kHz) was classifiedas a "moderate reversed flow"; and lower than19 mm (=1.58 kHz) was termed a "low reversedflow." Typical sonograms of the high, moderate,and low reversed ophthalmic collateral flow are
/
Fig. 3 The ophthalmic collateral flow extended tothe syphon of the internal carotid artery and the stemof the middle cerebral artery (upper arrow) but didnot fill its branches (72 year old woman).
represented in Fig. 6. There were eight patientswith high reversed flow, eight with moderatereversed flow, and 16 with low reversed flow. Theother 22 patients did not have a reversedophthalmic flow. Thirteen patients had no flowsignal type, two patients had a mixed type of flow,and seven patients had a physiological type offlow according to the ultrasonic doppler study(Fig. 7).
Fig. 4 A ngiogram showing collateralflow not through the ophthalmic arterybut, to a slight degree, through themiddle meningeal artery ( 52 year oldman).
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:;... 7..
-t
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Fig. 5 Quantitative evaluation bydoppler ultrasound of reversedophthalmic flow of the 32 carotidocclusions.
60(mm)
COMPARISON OF ULTRASONIC DOPPLER AND
ANGIOGRAPHIC FINDINGS
Ultrasonic doppler findings on ophthalmic col-lateral flow associated with 54 occluded carotidarteries were compared with the angiographicfindings (Fig. 8).
Eight patients with high reversed ophthalmicflow on doppler ultrasound all had a good angio-graphic collateral flow through the ophthalmicartery, except for one patient whose carotid angio-grams did not show any ophthalmic collateralflow. The reason for the absence of collateral flowon angiography in this case was that the highreversed ophthalmic flow was filled across the mid-line of the face, via the superficial arteries of theface from the contralateral external carotid artery.Digital compression of the contralateral commoncarotid artery stopped this reversed ophthalmicflow and compression of the contralateral facialartery decreased it.
Eight patients with moderate reversed flowaccording to the doppler study had a poor angio-graphic collateral flow without exception.Of 16 patients who had low reversed ophthalmic
flow on the doppler examination, 14 did not haveangiographic collateral flow. The other two hadpoor angiographic collateral flow which was notcorrelated with the findings of doppler ultrasound.One of them had suffered from cerebral oedemadue to simultaneous chronic subdural haematomaand internal carotid occlusion to the same cerebralhemisphere. The other patient had the main col-lateral flow through small arteries near theophthalmic artery but not through the ophthalmicartery itself.Of 22 patients with the no flow, mixed flow,
and physiological flow types, none had an angio-graphic collateral flow through the ophthalmicartery. Therefore, the findings of ultrasonicdoppler study correlated well with the angiographic
Semiquantitative evaluation of ophthalmic collateral flow in carotid artery occlusion
high reversed flow pattem
5=72-kd43mtK
moderate reversed flow patten
s 32=
d 1in
30~ ~ ~ ~ - VS
..<t *F 4
200..loomA
low reversed flow pattern
5= 2mm
d=
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Fig. 6 Typical sonograms of high, moderate, and low reversed ophthalmic bloodflow associated with carotid artery occlusion.
findings except for three patients when we
evaluated quantitatively the ophthalmic collateralflow in 54 cases of carotid occlusion.
Discussion
Since the ultrasonic doppler technique was intro-duced for measurement of blood flow by Satomuraand Kaneko in 1960, it has been widely used forthe evaluation of blood flow in various arteries. In
the field of cerebrovascular diseases, Maroon et
al. (1970) and Muller (1972) reported the diag-nostic possibility in internal carotid occlusiondetecting the direction of blood flow in theterritory of the ophthalmic artery. Thereaftermany authors have reported its diagnostic useful-ness in obstructive lesions of the internal carotid(Keller et al., 1976a; Shoumaker and Bloch, 1978;White and Curry, 1978; Wise et al., 1979) andvertebral artery (Kaneda et al., 1977).
30
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Fig. 7 Ultrasonic doppler findings of theophthalmic blood flow with 22 carotidartery occlusions with no flow signal,mixed flow, and physiological flowtypes...;;;...;:: :.. ::....ZI47
48495051525354
0 0 20flow Reversed flow
(12mm=lkHz) (mm)
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00000 00000'0000oo_~~~~~~NFLOW_
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NO FLOWSIGNALTVDF
REVERSED FLOW TYPE,.,TH ERI
OPHTHALMIIC ARTERY DOPPLER
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MIXED or
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Fig. 8 Comparison of ultrasonic dopplerwith angiographic findings with regardto the ophthalmic collateral flow in54 carotid artery occlusions.
Quantitative evaluation of blood flow by dopplerultrasound is instructive in the physiology andpathophysiology of blood flow. Some efforts havebeen made to determine blood flow volume bydoppler ultrasound, but those seem to have beenlimited to experimental study or to biomedicalengineering, and there have been few clinicalstudies (Doriot et al., 1975; Keller et al., 1976b;Fish, 1978).From the results of the present study, it is
clear that there are four types of ophthalmicblood flow in carotid artery occlusions-reversed,
mixed, no flow, and physiological flow types.Moreover, the amount of reversed blood flow can
be graded as high, moderate, or low. This semi-quantitative evaluation by doppler ultrasoundproved very reliable. The noncorrelation betweenthe findings of angiogram and the doppler studyin three patients were all the result of particularpathological events and never of inaccuracy ofthe ultrasonic technique.We can demonstrate the clinical importance of
the semiquantitative evaluation of ophthalmiccollateral flow with three interesting examples. A
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s
GOOD
ANGIOGRAM POOR
NO
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Semiquantitative evaluation of ophthalmic collateral flow in carotid artery occlusion
reversed ophthalmic flow in a 72 year old manwith internal caiotid occlusion changed from lowreversed flow to high reversed flow in the courseof seven days of the acute stage according toultrasonic doppler examination. His angiogramsalso changed from "no collateral flow" to "goodcollateral flow." In this patient, canalisation ofthe ophthalmic collateral flow was diagnosed byultrasonic doppler study. A high reversed flow inthe ophthalmic artery of a 52 year old man withinternal carotid occlusion also changed to a lowreversed flow during the course of 10 monthsaccording to doppler study. His angiograms alsochanged from "good collateral flow" to "no col-lateral flow." This means that ultrasonic dopplerexamination can diagnose an occlusion of theophthalmic collateral flow. In the third case pre-viously reported by Kaneda et al. (1978), re-canalisation of the occluded carotid artery couldbe diagnosed noninvasively by the ultrasonicdoppler technique.The technique for detection of ophthalmic
artery blood flow was superior to that for medialfrontal artery blood flow for the purpose ofquantitative evaluation of the ophthalmic col-lateral flow as well as for a decision regarding thedirection of flow in the ophthalmic arterialterritory (Kaneda et al., 1978). When ophthalmicartery blood flow was measured as in the presentstudy, the findings of the angiograms and the
ar tery
doppler study disagreed in only three of 54 sub-jects. But when the blood flow of the medialfrontal artery was measured and compared withthe angiograms, there were as many as eightpatients with no correlation. The reason may bethat the diameter of the medial frontal arteryvaries more than that of the ophthalmic artery.From a theoretical standpoint, the value of the
maximum blood flow velocity at systole (S) is avery rough index of blood flow because it neglectsthe diameter of the ophthalmic artery, the anglebetween the artery and the ultrasonic beam, andthe mean blood flow velocity. For more precisedetermination of the volume of blood flow, sometheoretical considerations are necessary.The absolute quantity of the blood flow volume
in an artery (Q) is generally calculated by thefollowing equation:
Q=GcosoI V(t)dt
where V(t) is the mean blood flow velocity in theline of the sound beam, r is the radius of theartery, 0 is the angle between the axis ofthe artery and the sound beam, and C is a constant.
V(t), r and 0 are the important data necessaryfor calculation of the absolute quantity of bloodflow volume (Q): r and 0 can be measured withthe use of an ultrasonic duplex echo-dopplerscanner (Barber et al., 1974) (Fig. 9). Mean blood
I I Ulmr e
Fig. 9 Ultrasonic duplex echo-dopplerscan showing a longitudinal sectionalimage of common carotid artery. Thepath of the sound beam is indicated bythe oblique line (upper). Sound signal ofthe blood flow in the sample volume isdetected and analysed by the soundspectrograph, giving a sonogram (lower).
Sorogram o' the bi fod{tow
o - 2TC me ss i
F
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flow velocity in the line of the sound beam (V(t))or, at least an approximate value of it, may becalculated from the data obtained from the sono-gram of the blood flow. We hope, therefore, thatthe absolute quantity of the blood flow volume inan artery will be measured noninvasively in thenear future by such an ultrasonic dopplerinstrument.
References
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