Visual Disturbance and Carotid Artery Disease
393
500 Symptomatic Patients Studied by Non-Invasive Carotid Artery
Testing Including B-Mode Ultrasonography
JAMES J. G A U L , M . D . ,
STEPHEN J. M A R K S , M . D . ,
AND JESSE WEINBERGER,
M.D.
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SUMMARY Non-invasive carotid artery testing was performed on 500 consecutive patients with visual
disturbances not related to local ophthalmic pathology to determine the extent of carotid artery disease,
particularly in patients with symptoms not typical of amaurosis fugax. Three hundred eighty six patients
(77.2%) had an abnormal study. However, the incidence of hemodynamkaHy significant lesions was only
16%. The patients could be divided into three groups: 1) Patients with symptoms that could be explained on
an ocular basis, including amaurosis fugax, had a 79% Incidence of ipsilateral carotid plaques. 2) Patients
with symptoms which could not be easily explained on an ocular basis, such as bilateral blurred vision,
bilateral visual loss (both transient and permanent), and homonymous hemianopsia had an incidence of
carotid artery plaques similar to patients with amaurosis fugax. 3) Patients with unilateral blurred vision
and bilateral scintillations had a lower Incidence (57%) of carotid plaques than the other groups. Younger
symptomatic patients had less carotid plaques than the overall series. Twenty-one percent of patients under
age 50 had the Doppler finding of early systolic flutter turbulence, which is usually of mitral valve origin.
Women predominated In the under 50 age group by about 2:1. In view of the prevalence of carotid plaques
In the population of patients with visual symptoms other than amaurosis fugax, evaluation of these patients
with non-invasive testing is indicated to determine which of these patients has hemodynamicaily significant
obstruction to flow at the carotid artery bifurcation.
Stroke Vol 17, No 3, 1986
THE CEREBRAL TRANSIENT ISCHEMIC ATTACK is the most frequently encountered manifestation of carotid artery disease,1 and is often considered a
warning sign that permanent strokes may follow.2
Amaurosis fugax is the ocular equivalent of the transient ischemic attack, and is often associated with emboli from the carotid artery bifurcation.2"7 While there
has been considerable interest in the relationship of
amaurosis fugax and atheromatous carotid disease, little attention has been focused on the association of
other visual symptoms with carotid disease. Various
investigators define amaurosis fugax differently, with
some including only patients who describe a classic
"curtain" or "veil,"8 while others include patients who
report episodic fogging or blurring.9 Grouping such
patients together may not be justified, as these symptoms may not be manifestations of the same disease. It
is also not clear if a correlation exists between carotid
disease and such non-specific visual symptoms as episodic blurred vision, scintillations, or permanent visual loss.
To investigate the relationship between visual disturbance and atherosclerotic plaque at the carotid bifurcation, wereviewedthe records of 500 consecutive
patientsreferredto the non-invasive vascular laboratory over a three year period who complained of visual
dysfunction with no apparent ophthalmologic disorder
to account for the symptoms. The incidence of plaque
From the Department of Neurology, Mount Sinai School of Medicine, The Mount Sinai Hospital, New York, New York.
Current address of Dr. Marks is Department of Neurology, Lincoln
Hospital Center and New York Medical Center. Current address of Dr.
Gaul is Saint Miry Hospital, Medical Office Building, LanghomeNewtown Road, Langborne, Pennsylvania 19047.
Address correspondence to: Jesse Weinberger, M.D., Department of
Neurology, The Mount Sinai School of Medicine, One Gustave L. Levy
Place, New York, New York 10029.
Received July 29, 1985; revision #1 accepted September 20, 1985.
at the carotid bifurcation and the incidence of hemodynamicaily significant obstruction to flow was correlated with the nature of the visual symptoms to determine which patients should be routinely evaluated for
the presence of carotid artery lesions.
Methods
Patients
The series included 500 consecutive patients studied
in the vascular laboratory over a three year period who
were referred for a visual/ocular disturbance without a
known ophthalmologic disorder to account for the
symptoms. There were 245 men and 255 women. The
age range was 27 to 95 years with the following distribution: under 50 years, 63 (13%); 50-65 years, 184
(37%); over 65 years, 253 (51%).
The patients were assigned to one of the following
12 groups according to their symptom. These groups
were: Amaurosis Fugax — These 171 patients complained of a unilateral, transient loss of vision or scotoma, most often described as a "curtain" or "veil"
coming over the eye. In the great majority of cases
symptomsresolvedin a few minutes, but in all cases in
less than 4 hours. Blurred Vision, Bilateral — The 70
patients in this group most often used the word
"blurred" in both eyes simultaneously to describe their
transient visual symptom, and on further questioning
better specificity regarding the phenomena could not
be obtained. Blurred Vision, Unilateral — These 58
patients complained of non-specific blurring that was
clearly unilateral, but the symptoms were not typical of
amaurosis fugax. Positive Symptoms, Bilateral —
These 50 patients complained of transient scintillations, "stars," fortification spectra, or "wavy lines"
occurring bilaterally. Eight of these patients reported
positive symptoms in homonymous bilateral fields.
Positive Symptoms, Unilateral — These 33 patients
394
STROKE
VOL 17, No 3, MAY-JUNE
1986
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had symptoms as described in the bilateral group,
above, but clearly unilateral. Gradual Visual Loss,
Unilateral — These 39 patients had progressive, unilateral visual failure. Gradual Visual Loss, Bilateral —
Ten patients had symptoms analogous to the unilateral
group. Homonymous Hemianopia — 33 patients with
transient or permanent bilateral homonymous visual
field disturbance, hemianopic or quadrantic, excluding
"positive" symptoms. Acute Permanent Visual Loss,
Unilateral — These 22 patients noted an acute onset of
visual loss similar to that described in the amaurosis
fugax group, but with permanent residua. Transient
Loss of Vision — These 18 patients had transient total
visual loss or "blackouts of vision," often with an onset
similar to that described in amaurosis fugax, but bilateral. Excluded were patients who reported faint or
impending faint, or any other disturbance of consciousness. Ischemic Optic Neuropathy — These 15
patients were referred by an ophthalmologist who had
noted bright plaques in the retinal arteries, ischemic
optic atrophy, or ocular neovascularization on a suspected ischemic basis during ophthalmological examination. Permanent Visual Loss, Bilateral — These 2
patients had sudden onset of bilateral visual disturbance with residua. Two Visual Symptoms — Twenty-one patients had two of the above listed symptoms
on different occasions, and have been included in both
appropriate groups, giving a total of 521. No patient
had more than two visual symptoms.
on Doppler flow analysis (with or without broadening
of spectral frequencies) and either a reduction in ophthalmic artery pressure or a reversal of supraorbital
Doppler flow ipsilaterally. High frequency turbulence
indicates a narrowing of the lumen of the carotid artery
severe enough to force a small stream of red blood cells
through the lumen at a high velocity, resulting in a
narrowed Doppler systolic wave form with a large
proportion of high frequency signals. A non-obstructive lesion was diagnosed when a plaque was noted on
B-scan in patients in whom normal ophthalmic artery
pressure, normal supraorbital flow and normal carotid
Doppler pulse wave form or low frequency turbulence
were found.
Early Systolic Flutter Turbulence on direct carotid
artery flow analysis was also noted in several patients.
This finding is not related to pathology at the carotid
bifurcation, and has been shown to correlate highly
with dysfunction of the mitral valve. It is most commonly observed in patients with mitral valve prolapse18
(p < 0.001). A biphasic systole can be found in both
mitral and aortic valve lesions, but we have noted the
ausculatative finding of Early Systolic Flutter Turbulence only with mitral valve lesions.
All patients were studied with the complete noninvasive test battery bilaterally, regardless of their
symptoms. Statistical analysis employed the ChiSquare method.
Non-Invasive Test Methodology
Ophthalmic artery pressure was measured by
pneumo-oculoplethysmography (Life Sciences PVR),
with a normal mean value taken to be 75% ± 5% SD
of the brachial artery pressure.10' " Supraorbital Doppler analysis was performed using a 9.0 MHz bidirectional Doppler (Parks 908), employing superficial
temporal artery compression to determine the extent of
collateral flow from the external to the internal carotid
circulation.12'13
Carotid pulse wave form analysis13'M was performed with the 9 mHz bidirectional Doppler device
(Parks 908) and a 4 mHz Duplex Doppler (Sonomed).
Patterns of turbulence were identified either aurally13' l5 or by spectral analysis of Doppler frequencies.16
In combination, these three techniques (oculoplethysmography, supraorbital Doppler analysis and carotid
Doppler flow studies) have shown a 95% correlation
with angiographic demonstration of hemodynamically
obstructive lesions.13
To determine the presence of non-obstructive lesions at the carotid bifurcation, and to better define
obstructive ones, real-time B-Mode ultrasonography
was performed using a small-parts scanner at 7.5 MHz
(High Stoy). This technique has been shown to demonstrate lesions not seen by angiography, when the lesion
does not distort the origin of the internal or external
carotid artery.17
A hemodynamically significant lesion was diagnosed when an apparently obstructive plaque seen on
B-Scan was associated with high frequency turbulence
Overall Group
Table 1 lists the findings in the entire series of patients with respect to age and sex distribution. There
were nearly twice as many women as men in the youngest age group, with 22 of 245 men (8.9%) and 41 of
255 women (16.5%) below age 50 (p < 0.02). Normal
studies were found in 114 patients (22.8%), with a
significantly higher (p < 0.01) percentage in the youngest age group.
Bilateral carotid disease was present in 293 patients
(58.6%). Eighty patients (16%) had at least one hemodynamically significant lesion, with all but 6 of these
occurring in patients with bilateral disease.
Early Systolic Flutter Turbulence (suggesting mitral
valve disorders) occurred with approximately equal
frequency among men and women, with 28 of the 31
patients (90%) being age 65 or younger. Women again
dominated the youngest age group, with 10 of 41
women (24.4%) and 3 of 22 men (13.6%) below age
50 having Early Systolic Flutter Turbulence.
Table 2 correlates the symptoms of all the patients in
the series with the extent of atherosclerotic plaque at
the carotid artery bifurcation.
Results
1) Amaurosis Fugax
One hundred seventy one patients complained of
symptoms typical of amaurosis fugax. A carotid lesion
ipsilateral to the affected eye was present in 135
(79%). This is similar to the incidence of 76% reported
by Heyman et al." The lesion was hemodynamically
significant in 37 (21.6%). There was a significantly
VISUAL DISTURBANCE AND CAROTID ARTERY DISEASE/Gau/ et al
395
TABLE 1 Correlation of Age and Sex Distribution and Associated Conditions with Carotid Findings
Age
range
Unilateral
disease
Hemodynamic
lesions
Diabetes
Hypertension
ESFT
Total
Normal
Bilateral
disease
Males
50 yrs
50-65 yrs
65 yrs
All males
22
102
121
245
14
30
9
53
7
48
84
139
1
24
28
53
1
12
29
42
1
10
13
24
1
15
10
26
3
10
2
15
Females
50 yrs
50-65 yrs
65 yrs
All females
41
82
132
255
29
20
12
61
6
51
97
154
6
11
23
40
1
12
25
38
1
8
7
16
5
11
20
36
10
5
1
16
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80
93
293
500
144
Total
62
40
31
The extent of unilateral and bilateral carotid artery disease is demonstrated for each age group in patients presenting
with visual disturbances. The number of males and females in each group is indicated. The number of patients with
associated conditions which can also be responsible for ischemic symptoms (diabetes, hypertension and mitral valve
disease (ESFT) is shown.
increased incidence of carotid lesions on the side of the
symptoms as compared to a random distribution (p <
0.01). Among 23 patients with bilateral lesions in
which only one was hemodynamically obstructive, 19
(83%) had the symptom on the side of the hemodynamic lesion (p < 0.02), indicating that a hemodynamic lesion is more likely to give rise to ischemic symptoms than a non-obstructive lesion in a given patient
when all other factors are equal.
Fifteen of 16 patients (94%) with hypertension had
an ipsilateral carotid lesion. Only seven of 12 diabetics
(58%) had ipsilateral carotid disease and 5 (42%) had
normal studies bilaterally. The diabetics with amaurosis fugax were younger than the rest of the group. Five
patients had both hypertension and diabetes. The difference between hypertensives and diabetics was statistically significant (p < 0.05). Thisfindingis similar
to previous reports implicating local small arterial
thrombosis as a greater source of ischemia in diabetics
than carotid artery disease.20
TABLE 2 Correlation of Visual Symptoms with Carotid Disease
Category
Total
patients
171
70
58
50
33
39
22
33
Total
ipsilateral (A)
lesions
Ipsilateral (B)
hemodynamic
lesion
Bilateral
lesion
64.3%
62.9%
48.3%
38.0%
72.7%
56.4%
77.3%
48.5%
61.1%
60.0%
60.0%
100.0%
57.1%
21.6%
78.9%
Amaurosis fugax
Blurred vision bilateral
81.4% (A)
12.9%
3.4%
Blurred vision unilateral
56.9%
58.0% (A)
4.0% (B)
Positive symptoms bilateral
0
Positive symptoms unilateral
75.8%
74.4%
10.3%
Gradual visual loss unilateral
22.7%
95.5%
Permanent visual loss unilateral
63.6%
0
Homonymous hemianopia
77.8% (A)
16.7% (B)
Transient visual loss bilateral
15
6.7%
66.7%
Ischemic retinopathy
10
90.0% (A)
20.0% (B)
Gradual visual loss bilateral
2
100.0% (A)
Permanent visual loss bilateral
0 (B)
21
Two visual symptoms
81.0% (A)
14.3% (B)
The category of visual symptoms is numbered corresponding to the text of the Result Section. The number of patients
with each visual symptom is tabulated in the second column Total Patients. The third column (ipsilateral disease)
indicates the percent of patients with a carotid lesion ipsilateral to the visual disturbance. The percentage of hemodynamically obstructive lesions is shown in the fourth column. The percentage of patients with bilateral carotid disease in each
symptom group follows (bilateral disease). Twenty-one patients complained of more than one visual symptom.
A) When patients complained of bilateral symptoms, the percentage of patients with a carotid lesion on either side is
shown in the ipsilateral lesion column.
B) When patients complained of bilateral symptoms, the percentage of patients with a hemodynamic lesion on either
side is shown in the hemodynamic lesion column.
1)
2a)
2b)
3a)
3b)
4a)
5a)
6)
7)
8)
4b)
5b)
396
STROKE
Four patients with amaurosis fugax had glaucoma
and all 4 had bilateral nonobstructive plaques. One
patient with associated temporal arteritis had a normal
carotid study.
All 16 patients with signs or symptoms of transient
or permanent cerebral ischemia from the hemisphere
ipsilateral to the eye with amaurosis fugax had disease
in the appropriate carotid distribution.
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2) Non-Specific Blurred Vision
a) Fifty-seven of 70 patients (81.4%) complaining
of bilateral blurred vision had carotid lesions, and 44
(63%) had bilateral disease. Nine carotid lesions were
hemodynamically significant. Ten patients with bilateral blurred vision had either hypertension, diabetes, or both. Five patients had glaucoma and two had
temporal arteritis.
b) Fifty eight patients complained of unilateral
blurred vision that was not clearly amaurosis fugax.
Thirty three (56.9%) had carotid lesions ipsilateral to
the symptoms, of which only 2 were hemodynamically
significant. Seven patients had diabetes or hypertension. Three patients had glaucoma. Patients with unilateral non-specific blurred vision had a lower incidence of ipsilateral carotid lesions than patients with
typical amaurosis fugax (p < 0.01).
3) Positive Visual Symptoms
a) Twenty-one of 50 patients (42%) complaining of
bilateral positive visual symptoms had normal studies.
There were only two hemodynamically significant lesions. Five of the 8 patients (62.5%) who reported
scintillations in homonymous bilateral fields had normal carotid studies.
b) Twenty-five of 33 (76%) of patients complaining
of unilateral positive visual symptoms had carotid lesions ipsilateral to the symptom, similar to the incidence in patients with typical amaurosis fugax.
4) Gradual Visual Loss
a) Twenty-nine of 39 patients (74%) complaining
of gradual unilateral visual loss had ipsilateral carotid
lesions of which 5 lesions were hemodynamic. There
were 6 hypertensives and 7 diabetics.
b) Ten patients complained of bilateral gradual visual loss. Only one had a normal carotid study. Six had
bilateral disease. Two lesions were hemodynamically
significant.
5) Acute Permanent Visual Loss
a) Twenty-one of 22 patients (95.5%) complaining
of acute permanent unilateral visual loss had ipsilateral
carotid lesions. Five of these lesions (22.7%) were
hemodynamic. This major symptom category had the
highest percentage of carotid atheroma in the entire
series of 500 patients. There were 2 diabetics and 6
hypertensives.
b) Two patients had acute onset of bilateral visual
loss. Both had bilateral nonobstructive carotid lesions.
VOL 17, No
3, MAY-JUNE
1986
6) Homonymous Hemianopia
Twenty-one of 33 patients (64%) presenting with
signs of homonymous hemianopia had carotid lesions
ipsilateral to the appropriate cerebral hemisphere (contralateral to symptoms). None of these lesions were
hemodynamically significant. Eleven of 17 patients
(65%) with associated hemimotor/sensory syndromes
ipsilateral to the homonymous field disturbance had a
lesion in the appropriate carotid.
7) Transient Bilateral Loss of Vision
Eighteen patients complained of bilateral simultaneous transient loss of vision. Four (22%) had normal
carotid studies. Eleven (61%) had bilateral carotid lesions, of which three were hemodynamically significant.
8) Ischemic Optic Neuropathy
Ten of 15 patients (67%)referredby an ophthalmologist with a diagnosis of ischemicretinopathyhad ipsilateral carotid lesions. The subgroup of 7 patients without associated conditions related to cerebrovascular
disease had a much lower percentage (2 of 7, 29%) of
ipsilateral carotid lesions. Age does not appear to account for this difference, which is statistically significant (p < 0.01).
Early Systolic Flutter Turbulence
Early systolicflutterturbulence occurred in 31 cases
(6% of the entire series), consistent with a reported
incidence of mitral valve prolapse in the general population of 5-6%, 2I ' u but was found in 21.6% of patients
with visual disturbance below age 50. While 9 patients
of the 171 with amaurosis fugax had early systolic
flutter turbulence (5%), 8 of the 50 patients with positive bilateral symptoms had early systolic flutter turbulence (16%) (p < 0.02). Five of 58 patients (9%) with
unilateral blurred vision had early systolic flutter turbulence. These latter five patients were all in the under
50 year age group, and all 5 had normal carotid
studies.
Discussion
There is a strikingly high incidence of carotid artery
disease in this population of 500 patients with visual
disturbance and no known ophthahnologic disorder to
account for their symptoms. 386 patients (77.2%) had
evidence of atherosclerotic plaque at the carotid bifurcation. This should be compared with the unselected
autopsy series of Fisher et al,23 whoreportedan overall
incidence of disease at the carotid bifurcation to be
39.3% in cases with an age range quite similar to this
series (under 50 years, 12%; 59-69 years, 36%; over
70 years, 52%). Kollarits, et al24 reviewed a series of
100 consecutive carotid arteriograms performed in
hospital patients at least 60 years old and found an
incidence of carotid atheromatous disease of only
24%. Embolism of atheroma from the carotid bifurca-
VISUAL DISTURBANCE AND CAROTID ARTERY DISEASE/Gau/ et al
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tion to the retinal circulation probably accounts for a
large proportion of monocular visual symptoms, including amaurosis fugax, monocular scintillating scotomas and unilateral acute permanent visual loss. In
Fisher's series,23 only 17 patients (9.5%) with carotid
lesions had evidence of cerebral infarction due to probable embolism in spite of the much greater prevalence
of plaque. Amaurosis fugax was associated with hemispheric symptoms in 16 of 171 patients (9.4%) and all
16 had ipsilateral carotid disease. Transient ischemic
attacks, particularly ocular, appear to be a much more
frequent occurrence with carotid artery lesions than
cerebral infarction. Pessin has suggested that an embolus of sufficient size to temporarily obstruct the central
retinal artery may be too small to cause clinically evident cerebral dysfunction.9
Several studies13' "• "• "• ** have indicated that hemodynamically significant carotid stenosis poses an increased risk for cerebral hemispheric symptoms and
stroke. This is not the case for ocular stroke. In this
series, 22 patients had permanent visual loss, while
171 patients had amaurosis fugax. Thus, 22 of 193
patients (11.4%) with a definite retinal ischemic event
had an ocular stroke, similar to the incidence of 11.8%
reported by Marshall and Meadows.5 Permanent visual
loss occurred in 5 of 42 patients (11.9%) with an ocular
ischemic event ipsilateral to a hemodynamic carotid
lesion, the same percentage as patients with amaurosis
fugax. There was an increased incidence of permanent
visual loss in hypertensives (6/22, 27.2%) (p < 0.02),
but not in diabetics.
In the younger age group 14 of 22 men (63.6%) and
29 of 41 women (70.7%) had normal carotid studies.
In our series, early systolic flutter turbulence originating from the mitral valve was present in 21.6% of the
patients with visual disturbance who were under age
50. The frequency was twice as high in women as in
men (p < 0.01). There is arelationshipbetwen mitral
valve prolapse and cerebral ischemia, particularly in
younger patients and in those without other risk factors
for stroke.27"29 This suggests that dysfunction at the
mitral valve, with possible embolic phenomena, is related to the increased incidence of visual disturbances
in these younger patients, particularly women.
Patients with unilateral positive symptomatology
have an incidence of ipsilateral carotid disease almost
exactly that of the amaurosis fugax group. Dyll et al
have reported symptoms of "bright lights" proceeding
episodes of amaurosis fugax6 suggesting a common
etiology for these symptoms.
The highest percentage of normal carotid studies
and lowest incidence of bilateral carotid disease occurred in patients with bilateral positive symptoms
(significant p < 0.01 compared to amaurosis fugax).
Only 10 of the 50 patients in this group had headaches.
Patients with the clearcut clinical syndrome of migraine were probably less likely to be referred for their
visual syndromes. The patients with bilateral positive
symptoms had the highest incidence of early systolic
flutter turbulence (16%), significantly (p < 0.02) more
frequent than in the amaurosis fugax group (5%). The
397
incidence of carotid disease and hemodynamic lesions
in the group of patients with non-specific unilateral
blurred vision was also lower than patients with amaurosis fugax (p < 0.01). Migraine may account for
many of the symptoms in these patients.
Patients with bilateral blurred vision had an incidence of carotid artery disease much like the amaurosis
fugax group, though they had significantly fewer
hemodynamic lesions than patients with amaurosis fugax (p < 0.02). Troost3132 has noted that "blurred
vision" and "transient loss of vision" are frequently
accompanied by complaints of dizziness and vertigo,
and that they can occur in the situation of transient
brainstem ischemia. Atherosclerotic disease in the carotid bifurcation may indicate there is disease in the
vertebrobasilar system as well and reduced flow in the
carotid circulation may also influence vertebrobasilar
disease.33 This may account for the high incidence of
carotid disease in patients whose visual symptoms cannot be easily explained on an ocular basis.
There are clinical differences between diabetics and
hypertensives with visual complaints. The diabetics
are younger, with 68% being under age 65, as compared to 45% in the hypertensives (p < 0.05). Diabetics also have a higher proportion of normal carotid
studies, 33%, compared to 13% in hypertensives (p <
0.02). This may be accounted for by the age difference, but diabetics may be more prone to pathology
other than carotid disease, such as small vessel disease, platelet dysfunction or biochemical abnormalities.20
Since 114 patients (22.8%) in the series had completely normal non-invasive carotid studies, there remains a significant proportion of people whose visual
disturbances are not due to disease at the carotid bifurcation, especially in the younger age groups. These
patients probably have their symptoms on the basis of
local vascular disease or emboli of cardiac origin. One
case of amaurosis fugax with ophthalmic artery stenosis and a normal carotid bifurcation has been documented.34 Mitral valve prolapse may play a role, especially in younger patients.
There is a dramatic prevalence of carotid disease in
the population of patients with visual complaints. It is
not possible to predict, on the basis of clinical presentation, which patient with visual disturbance will have
a hemodynamically significant carotid lesion, and thus
a higher risk of stroke. However, the incidence of
hemodynamic stenosis in these patients is only 16%. In
view of the small but significant proportion of complications associated with carotid angiography,35 non-invasive carotid testing with B-mode imaging in conjunction with spectral analysis of the Doppler shift
signal and ocular plethysmography provides an appropriate method for evaluating the carotid artery bifurcation in these patients.
Acknowledgments
The authors wish to thank Mrs. Dianne Davis for her efforts in
preparing the manuscript. Supported in part by a contribution to stroke
research in honor of Mr. and Mrs. Morris Renvin.
398
STROKE
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Stroke. 1986;17:393-398
doi: 10.1161/01.STR.17.3.393
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