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Occlusion Due to Carotid Artery Dissection
A More Severe Disease Than Previously Suggested
Didier Milhaud, MD;
Gabriel R. de Freitas, MD;
Guy van Melle, PhD;
Julien Bogousslavsky, MD
Arch Neurol. 2002;59:557-561.
ABSTRACT
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Background Stroke due to internal carotid artery dissection is considered to have
a good prognosis.
Objective To determine whether the prognosis of internal carotid artery dissection
is worse than classically reported by comparing the characteristics of patients
who had an acute ischemic stroke admitted to a population-based primary care
center with internal carotid artery occlusion due to either dissection (DO)
or atherothrombosis (AO).
Patients and Methods Among 3502 patients admitted to our population-based primary care center,
DO (n = 73) was diagnosed by angiography or magnetic resonance imaging, while
AO (n = 81) was diagnosed by angiography. The characteristics of patients
with DO or AO were compared using univariate and multivariate analysis.
Results Patients with DO were younger (mean [SD] age, 44.6 [10] vs 60.1 [10]
years, P<.001), had fewer vascular risk factors,
and presented more frequently with global middle cerebral artery territory
involvement (42% vs 17%, P<.05) and less frequently
with watershed infarcts (3% vs 19%, P<.05) than
patients with AO. Unexpectedly, patients with DO were noted to have more severe
clinical impairment, with an increased frequency of decreased consciousness,
and a poorer outcome at 1 month. Multivariate analysis showed that the independent
factors associated with DO were age younger than 55 years, nonsmoker, no history
of hypertension, headache at presentation, and global aphasia.
Conclusions Patients with DO are younger and are initially seen with fewer risk
factors than patients with AO, but their clinical features and prognosis are
worse. Large infarcts involving the whole middle cerebral artery territory
that may be due to the lack of collateral circulation are responsible for
the bad prognosis of patients with DO.
INTRODUCTION
INTERNAL CAROTID artery dissection (ICAD) is a clearly identified cause
of stroke and accounts for about 20% of strokes in younger patients.1 The clinical picture of ICAD is variable, with either
pure local symptoms, such as Horner syndrome associated with headache or cervical
pain, or cerebral ischemia in up to 80% of patients with transient ischemic
attack or brain infarction.1-3
Internal carotid artery dissection can be diagnosed using conventional angiography,
which shows irregular, and often tapered, stenosis with the characteristic
"string sign," "flame-shaped" occlusion, or aneurysmal dilatation.4-8
More recently, ICAD has been diagnosed using magnetic resonance imaging, which
detects a crescent-shaped hyperintensity surrounding the narrowed lumen (T1-
and T2-weighted images of the neck), and usingmagnetic resonance angiography.8
Although certain authors consider ICAD to be a serious disease with
a potentially grave outcome,9 several studies
have shown excellent or good recovery in 70% to 90 % of these patients without
significant stroke sequelae.3-4,10-11
The rate of early death in ICAD is directly due to brain infarct and is estimated
at about 2% to 5%.3, 5, 10
However, in a previous study focusing on ICAD with occlusion, we reported
mortality as high as 23%,12 and Pozzati et
al13 reported that 37% of patients with occlusion
and ICAD have a bad outcome. To determine whether the prognosis of ICAD is
worse than classically reported, we compared the characteristics of patients
with acute ischemic stroke admitted to our population-based primary care center
with ICA occlusion due to either dissection (DO) or atherothrombosis (AO).
PATIENTS AND METHODS
From the Lausanne Stroke Registry, a prospective primary care center–based
registry,14 we selected all consecutive patients
initially seen with angiography-proven internal carotid artery occlusion related
to DO or AO and with first-ever ischemic stroke. Internal carotid artery dissection
with occlusion was diagnosed either using conventional angiography (64 cases),
which showed a tapered artery occlusion with wall artery irregularities, double
lumen, or outpouching, or, when available, using magnetic resonance angiography
and axial magnetic imaging (9 cases), showing wall artery hematoma or intra-arterial
thrombus. Traumatic and spontaneous dissections were grouped together because
of the difficulty in determining whether a dissection was spontaneous or secondary
to a minor trauma and because their presentation did not differ significantly.15 In all 81 cases, the internal carotid artery occlusion
type was diagnosed as AO using only conventional angiography. To further clarify
the mechanism of brain infarct and the outcome in patients with ICAD, we also
studied the infarct territory and outcome in patients with ICAD without occlusion
diagnosed using angiography or magnetic resonance imaging and compared the
results with those for patients with DO.
The patients were studied using a standard protocol including at least
one computed tomographic scan within 7 days of the stroke. We also assessed
the risks factors of hypertension (blood pressure >160/90 mm Hg at least twice
before the stroke), known diabetes mellitus (2 or more fasting blood glucose
levels >117 mg/dL [>6.5 mmol/L] before the stroke), elevated venous hematocrit,
regular cigarette smoking, oral contraceptive use, hypercholesterolemia (fasting
cholesterol levels >232 mg/dL [>6 mmol/L]), and a history of ischemic heart
disease, atrial fibrillation, vascular claudication, or migraine. A history
of previous transient ischemic attack in the same territory as the infarct
was also recorded.
Infarct topography was classified according to vascular territory using
mapping templates developed in our center and elsewhere.16
The arterial territories considered were the anterior cerebral artery; middle
cerebral artery (MCA) pial territories, including the anterior and posterior
pial territories; the deep territory of the MCA, including perforating and
medullary branches; and the global MCA territory involving superficial and
deep territories. Multiple, superficial, and deep territories and watershed
infarcts (cortical or subcortical) were also considered. Neurological status
and type of stroke onset were evaluated on admission by a neurologist. Level
of consciousness was evaluated on admission, decreased consciousness being
defined as somnolence or coma. Functional status at 1 month was measured by
establishing a modified Rankin Scale score from the prospectively collected
Lausanne Stroke Registry data, with a poor outcome being considered a Rankin
Scale score of 3 or more.
The 2-sided t test was used to compare means.
To compare proportions, the Pearson  2 test was used unless
the number of cases was too small, in which case the Fisher exact test was
used. The Bonferroni-type correction attributed to Holmes was applied. To
further characterize ICAD, we performed a stepwise logistic regression (stepdown)
using all clinical factors identified in the univariate analysis as being
significantly different between patients with DO or AO. In all tests, P<.05 was considered statistically significant.
RESULTS
PATIENTS AND RISK FACTORS
Between January 1, 1979, and December 31, 1998, Lausanne Stroke Registry
recorded 3873 first-ever stroke patients and, in 3502 of these, the stroke
was diagnosed as ischemic in origin. Of this ischemic stroke group, 88 patients
had ICAD and, of these, 73 had occlusion. This last group consisted of 35
men and 38 women whose mean (SD) age was 44.6 (10) years. Two patients had
bilateral ICAD and occlusion. Fibromuscular dysplasia was diagnosed in 14
patients (19%) and dissection was clearly related to a history of trauma in
7 patients (9.6%). Eighty-one patients (65 men and 16 women; mean [SD] age,
60.1 [10] years) with ischemic stroke had AO proven by conventional angiography.
In this group, the contralateral carotid artery was normal in 18 cases and
showed atherosclerotic lesions with less than 70% stenosis in 42 cases or
with 70% or more stenosis in 16 cases, while internal carotid artery occlusion
was bilateral in 5 cases. In the acute phase, 36 (49%) of the patients with
DO received anticoagulant therapy using unfractionated heparin sulfate; all
other patients with DO (with contraindication for full-dose anticoagulant
therapy) and patients with AO were treated with a low dose of low-molecular-weight
heparin and aspirin. The DO group contained a significantly higher proportion
of women and patients were younger than in the AO group (Table 1).
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Table 1. Demographic and Vascular Risk Factors in Patients With Dissection
(DO) or Atherothrombotic Occlusion (AO)*
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Risk factors in patients with DO and AO are summarized in Table 1. In patients with DO, the prevalence of hypertension, diabetes
mellitus, smoking, hypercholesterolemia, and a history of vascular claudication
was significantly lower than in patients with AO.
TOPOGRAPHY OF INFARCTIONS
The global MCA territory was significantly more frequently involved
in the DO group than in the AO group (42% vs 17%, P<.05),
in which anterior pial MCA territory involvement predominated (Table 2). Patients with DO presented less frequently with watershed
infarcts than patients with AO (3% vs 19%, P<.05),
suggesting that DO most often caused stroke via embolism. Moreover, by studying
angiograms in patients with DO, we documented embolization in the M1- or M2-segments
of the MCA in 12 patients and distal embolization in 13 patients. The infarct
territories involved in patients with ICAD without occlusion were similar
to those in the DO group, with a low rate of watershed infarcts (7%); however,
these patients were seen less frequently with global MCA infarcts (20% vs
42%, P = .10).
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Table 2. Infarct Topography in Patients With Dissection Occlusion (DO),
With or Without Occlusion, or With Atherothrombotic Occlusion (AO)*
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CLINICAL PRESENTATION AND OUTCOME
Horner syndrome (complete or incomplete) was present in 18 of the patients
with DO (24%) and in 10 of the patients with AO (12%) (P = .12). Severe clinical
impairment, including motor and sensory deficits with lateral hemianopia,
was more frequent in patients with DO than in patients with AO (41% vs 14%, P<.01), as was global aphasia (32% vs 16%, P<.05) (Table 3). Motor
deficit involving the face, upper limb, and lower limb was more frequent in
patients with DO than in patients with AO (62% vs 36%, P<.01). Decreased consciousness was also more frequent in patients
with DO than in patients with AO (42% vs 16%, P<.05).
Finally, a bad outcome at 1 month was seen in 37% of the patients with DO
compared with 16% of the patients with AO (P<.05),
and mortality at 1 month was 14% in patients with DO compared with 1% in patients
with AO (P<.003). In comparison, at 1 month, 20%
of patients with ICAD without occlusion had a bad outcome and 7% died (P = .14 compared with patients with ICAD with occlusion).
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Table 3. Clinical Features and Outcome in Patients With Dissection
(DO) or Artherothrombotic Occlusion (AO)*
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MULTIVARIATE ANALYSIS
For the patients with DO, logistic regression (Table 4) showed that the independent factors characterizing occlusive
dissection were age younger than 55 years, nonsmoker, no history of hypertension,
headache at presentation, and global aphasia.
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Table 4. Multivariate Analysis Correlates Associated With Dissection
in Patients With Acute Ischemic Stroke Presenting With Carotid Artery Occlusion
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COMMENT
In this study, patients with DO fell into the same age range as those
reported in other series of patients with ICAD6
and were significantly younger than the patients with AO. There was no clear
male-female preponderance in the patients with DO, while the patients with
AO presented with male preponderance, as previously reported.17-18
Except for oral contraception, patients with DO had fewer vascular risk factors
(hypertension, diabetes mellitus, cigarette smoking, and vascular claudication)
than patients with AO. Finally, despite the patients with DO being younger
and having fewer vascular risk factors than the patients with AO, their clinical
features and outcomes were more severe.
In our study, infarct topography in patients with DO showed that almost
all infarcts (97%) were territorial, involving mainly the MCA territory, whereas
watershed infarcts were rare (only 2 cases). Cortical and subcortical infarcts
were more likely to be of embolic origin,16, 19
whereas junctional or watershed infarcts were more likely to be of hemodynamic
origin.20 As previously reported for ICAD with
stenosis or occlusion, in the present study, the presumed mechanism of cerebral
ischemia in the patients with DO was embolic. This point was confirmed by
studying the infarct territories involved in patients with ICAD without occlusion;
in these patients in whom strokes only occur via embolism, roughly the same
low frequency of watershed infarcts was found as in patients with DO. However,
in patients with ICAD without occlusion, there was a trend toward a better
prognosis than in the patients with DO; this may be due to the lower rate
of global MCA infarcts in this group, which may be related to a lower frequency
of intraluminal thrombus and smaller emboli.
In the study of Lucas et al,21 92% of
infarcts were large cortical and subcortical infarcts that were presumed to
be embolic, and, in the series of Steinke et al,22
70% of infarcts were territorial MCA infarcts or large striatocapsular infarcts
with a high probability of being due to embolism. However, in 1 study23 including only 11 patients, 5 presented with 1 or
more lesions in the rostral corona radiata ipsilateral to the ICAD and were
interpreted as low-flow–induced ischemic brain damage. In our series
of ICAD with occlusion, the presumed mechanism is the formation of a thrombus
in the dissected artery favored by blood stagnation after the level of occlusion,
with secondary distal embolism in the MCA territory in most cases. Moreover,
2 studies have shown that microembolic signals are detected by transcranial
Doppler in patients with brain infarct due to ICAD.24-25
In our patients with AO, the prevalence of watershed infarcts was higher (16%)
than in the patients with DO, the frequency being similar to that seen in
another of our studies.26 However, in these
patients, the predominant mechanism of ischemia was embolic. In the study
of Mounier-Vehier et al,18 of the 40 patients
with atherothrombotic internal carotid artery occlusion, only 5 presented
with border-zone infarcts.
In the present study, large cortical and subcortical infarcts due to
global MCA arterial territory involvement were significantly more frequent
in patients with DO than in patients with AO, whereas there was a trend to
a lower frequency of deep MCA infarcts in the DO group compared with the AO
group. Previous studies have emphasized the importance of the collateral circulation
in determining the size of infarcts.27-29
The extent of brain infarction in patients with DO may be due to poor functioning
and mobilization of the secondary collateral leptomeningeal pathways compared
with patients with AO. Indeed, in patients with AO, parenchymal chronic hypoperfusion
due to previous ipsilateral tight stenosis or contralateral stenosis greater
than 50% leads to mobilization of the secondary collateral pathways, which
was not the case in the patients with DO in the present study. In contrast
to the primary collateral system, which responds immediately to focal circulation
failure, the secondary collateral leptomeningeal pathways take longer to respond30-32 and do not develop
in patients with DO. Moreover, because dissection is a dynamic process, we
cannot exclude the possibility of an underlying hemodynamic mechanism prior
to thrombus formation and embolism in patients with DO, the combination of
which contributes to large lesions in the subcortical area.
In the present study, because of the profile of our registry, which
only includes patients with first-ever acute ischemic stroke, all patients
with DO presented with completed stroke compared with the 40% to 60% of reported
cases of ICAD in other series,9 emphasizing
limitations in the interpretation of registry-based studies because of the
use of data obtained from selected populations. However, the severity of stroke
related to ICAD is clearly due to the high prevalence of infarcts involving
the global MCA territory.
CONCLUSIONS
Although patients with DO are younger and are initially seen with fewer
risk factors than patients with AO, their clinical features and prognosis
are worse. Larger infarcts involving the global MCA territory, which may be
due to the lack of collateral circulation, are responsible for the bad prognosis
of patients with DO.
AUTHOR INFORMATION
Accepted for publication December 28, 2001.
Author contributions: Study concept and design (Drs Milhaud, de Freitas, and Bogousslavsky); acquisition
of data (Dr Bogousslavsky); analysis and interpretation
of data (Drs Milhaud, de Freitas, van Melle, and Bogousslavsky); drafting of the manuscript (Drs Milhaud and Bogousslavsky); critical revision of the manuscript for important intellectual content (Drs van Melle and Bogousslavsky); statistical expertise (Dr van Melle); obtained funding (Dr
Milhaud); administrative, technical, and material support (Drs Milhaud, de Freitas, and Bogousslavsky); study supervision (Drs Milhaud and Bogousslavsky).
Corresponding author and reprints: Julien Bogousslavsky, MD, Department
of Neurology, University Hospital Lausanne, rue du Bugnon 46, Lausanne 1011,
Switzerland.
From the Department of Neurology, Centre Hospitalier Universitaire
Vaudois Lausanne (Drs Milhaud, de Freitas, and Bogousslavsky) and the University
Institute of Social and Preventive Medicine (Dr van Melle), Lausanne, Switzerland;
and the Department of Neurology, Centre Hospitalier Universitaire Montpellier,
Montpellier, France (Dr Milhaud).
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