Correspondence to Marc I. Chimowitz MB, ChB, Department of Neurology, Emory University, 4th Floor Emory Clinic, 1365 Clifton Rd, Atlanta GA 30322. E-mail mchimo{at}neuro.emory.edu
Methods—We studied 68 patients with 50% to 99% stenosis
of one of the following arteries: intracranial vertebral (n=31),
basilar (n=28), posterior cerebral (PCA) (n=6), or posterior
inferior cerebellar (PICA) (n=3). All patients had previous
transient ischemic attack or stroke in the territory of the
stenotic artery and were treated with warfarin (n=42) or
aspirin (n=26). Follow-up was by chart review and personal or telephone
interview.
Results—During a median follow-up of 13.8 months, 15 patients
(22%) had an ischemic stroke (4 fatal), 3 patients (4.5%) had
a fatal myocardial infarction (MI) or sudden death, and 6 patients
(9%) had a nonfatal MI. Stroke rates in any vascular territory (per
100 patient-years of follow-up) were 15.0 in patients with basilar
artery stenosis, 13.7 in patients with vertebral artery
stenosis, and 6.0 in patients with PCA or PICA
stenosis. Stroke rates in the same territory as the
stenotic artery (per 100 patient-years of follow-up) were 10.7
in patients with basilar artery stenosis, 7.8 in patients with
vertebral artery stenosis, and 6.0 in patients with PCA or PICA
stenosis.
Conclusions—Patients with symptomatic intracranial
vertebral artery or basilar stenosis are at high risk of
stroke, MI, or sudden death. Further studies are needed to clarify
optimal therapy for these patients.
While there are numerous studies on the risk of stroke in patients with
carotid siphon or MCA stenosis, there are limited data on the
prognosis of patients with angiographically proved stenosis of
the intracranial vertebral arteries, basilar artery, or PCAs. Three
studies19 20 21 of small series of patients suggest
that the risk of stroke associated with intracranial vertebral artery,
basilar artery, or PCA stenosis is 2.5% to 5.5% per year,
which is substantially lower than the risk associated with carotid
siphon or MCA stenosis. In view of the limited data on the
prognosis of patients with symptomatic intracranial
posterior circulation stenosis, we undertook this study to
assess the risk of ischemic stroke, MI, and sudden death in
these patients. A secondary aim of this pilot study was to compare the
efficacy of warfarin versus aspirin for preventing ischemic
stroke, MI, or sudden death in patients with symptomatic
intracranial vertebral artery, basilar artery, or PCA
stenosis.
Potential candidates for WASID were identified by reviewing the reports
of consecutive angiograms performed at 7 participating centers between
1985 and 1991. An attempt was made to retrieve the angiograms of all
patients whose reports indicated a "moderate," "severe," or
"
Inclusion and Exclusion Criteria
Exclusion criteria were occlusion of an intracranial artery;
nonatherosclerotic intracranial vasculopathies, such as dissection,
moyamoya disease, or vasculitis; asymptomatic
stenosis of a major intracranial artery; distal branch
stenosis of an intracranial artery; coexistent
cardioembolic source (ie, atrial fibrillation, mitral stenosis,
prosthetic valve, MI within 6 weeks, intracardiac clot,
ventricular aneurysm, or bacterial endocarditis); a
severe neurological deficit from the qualifying stroke or from a stroke
occurring during cerebral angiography; stroke prevention treatment
other than aspirin or warfarin (eg, angioplasty, warfarin and aspirin
concurrently, ticloplidine, or dipyridamole alone); and
absence of follow-up data (ie, no notes on the chart after angiography
and no patient contact).
Treatment, Follow-up, and End Points
Follow-up of patients was by chart review and telephone or personal
interview. Patients were followed until occurrence of an end point,
death from a nonvascular cause, change in antithrombotic therapy, or
date of last contact. End points were stroke in any vascular territory,
MI, or sudden death. Sudden death was defined as death of sudden onset
that could not be explained by a known nonvascular process. Stroke in
the territory of the stenotic artery was defined as a new
infarct on CT or MRI in a region of the brain supplied by the
symptomatic stenotic artery or (in the absence of
an infarct on brain imaging) as the development of a new neurological
deficit that lasted at least 24 hours and was localized to an area of
the brain supplied by the symptomatic stenotic
artery. Safety of warfarin and aspirin was assessed by
recording hemorrhagic complications. Hemorrhages were
classified as major (fatal hemorrhage, any intracranial
hemorrhage, bleeding requiring hospitalization, or bleeding
requiring transfusion) or minor (any other bleeding complication).
Statistical Analysis
Outcome of Patients With Posterior Circulation Intracranial
Stenosis
Warfarin Versus Aspirin: Risk Factors, Location, and Severity
of Stenoses
End Points and Hemorrhagic Complications: Warfarin Group Versus
Aspirin Group
Hemorrhagic complications occurred in 7 patients on warfarin (5
minor, 2 major: 1 fatal intracerebral
hemorrhage and 1 fatal gastrointestinal hemorrhage).
The rates of both minor and major hemorrhagic complications were 11 per
100 patient-years of follow-up in the warfarin group compared with 0
per 100 patient-years of follow-up in the aspirin group
(P<0.01). The rate of major hemorrhagic complications in
the warfarin group was 3.2 per 100 patient-years of follow-up.
Stroke in Same Territory as Stenotic Artery: Warfarin
Versus Aspirin
Of 42 patients treated with warfarin for a median follow-up of 11
months, 4 (10%) had a stroke in the same territory as the
stenotic intracranial artery (2 of 19 [11%] with
stenosis involving the basilar artery, 2 of 5 [40%] with
bivertebral stenoses, 0 of 13 [0%] with unilateral vertebral
artery stenosis, and 0 of 5 [0%] with PCA or PICA
stenosis). The rate of stroke in the same territory as the
stenotic artery in patients on warfarin (per 100 patient-years)
was 6.3 (3.7 in patients with 50% to 79% stenosis versus
8.2% in patients with 80% to 99% stenosis).
Pessin et al20 followed 9 patients with
symptomatic stenosis (40% to 90%) of the middle
or distal segments of the basilar artery for 1 month to 13 years (8 of
9 patients were followed for
In the current study of 68 patients with
Despite the higher frequency of basilar artery or bilateral
vertebral artery stenoses in the warfarin group (57% of
patients) compared with the aspirin group (35% of patients), patients
treated with warfarin had a significantly lower rate of
ischemic stroke than patients treated with aspirin. However,
patients on warfarin had a significantly higher rate of hemorrhagic
complications, which partly offset the overall benefit of warfarin.
Although the warfarin group had a lower rate of major ischemic
events (stroke, MI, and sudden death combined) than the aspirin group,
this difference was not statistically significant. This may have been
due to the low power of the study.
Patients with severe stenosis (80% to 99%) had a
substantially higher rate of stroke in the same territory of the
stenotic artery than patients with moderate stenosis
(50% to 79%) in both treatment groups. This finding suggests that
symptomatic vertebrobasilar stenosis behaves
similarly to symptomatic extracranial carotid artery
stenosis, which is associated with a higher risk of ipsilateral
stroke for each decile increase in percent stenosis above
70%.23 The high rate of stroke in the territory
of a severely stenotic vertebral or basilar artery with either
antithrombotic agent suggests that adjunctive stroke-preventive
therapies (eg, intracranial angioplasty24–26)
may be needed for patients with symptomatic high-grade
vertebral or basilar artery stenosis.
The results of this retrospective, nonrandomized pilot study suggest
that patients with symptomatic basilar artery or
intracranial vertebral artery stenosis are at high risk of
stroke and that warfarin may be more effective than aspirin for
preventing stroke in these patients. However, this retrospective study
has several limitations, including a nonrandomized study design; the
possibility that patients in this study may constitute a high-risk
subgroup of patients with posterior circulation stenosis who
were selected to undergo angiography; and the lack of standardized
therapy, such as a uniform dose of aspirin and international normalized
ratio target range. As such, a recommendation regarding the use of
warfarin for posterior circulation stenosis must await the
results of a prospective randomized study.
The following centers and personnel participated in this study.
University of Michigan Medical Center-Coordinating Center:
M.I. Chimowitz, J. Strong, M. B. Brown (statistician), A. Perkins
(statistician), W-M Liang (statistician), I. Yang (statistician).
Henry Ford Hospital: J. Kokkinos, S.R. Levine.
Tufts–New England Medical Center: S. Silliman, MS Pessin,
L.R.Caplan. Cleveland Clinic Foundation: E. Weichel, C.A.
Sila, A.J. Furlan, B. Dyko. Columbia–Presbyterian Medical
Center: D.E. Kargman, R.L. Sacco. Sinai Hospital of
Baltimore: R.J. Wityk, B. J. Stern, B. Agbogu, M. Jain.
Yale–New Haven Medical Center: G. Ford, P.B.
Fayad.
Received January 16, 1998;
revision received March 9, 1998;
accepted March 30, 1998.
© 1998 American Heart Association, Inc.
Original Contributions
Prognosis of Patients With Symptomatic Vertebral or Basilar Artery Stenosis
Abstract
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
Appendix 1
References
Background and Purpose—There are
limited data on the prognosis of patients with angiographically proved
symptomatic stenosis of the intracranial vertebral
artery or basilar artery.
Key Words: aspirin • atherosclerosis • cerebrovascular disorders • stroke • warfarin
Introduction
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
Appendix 1
References
Atherosclerotic
stenosis of the major intracranial arteries is an important
cause of ischemic stroke.1 2 3 4 5 6 7 8 In the
United States, intracranial arterial stenosis
causes approximately 10% of ischemic
strokes,1 6 8 9 10 ie, approximately 40 000
ischemic strokes annually. Several retrospective studies have
shown that the annual risk of stroke in patients with carotid siphon or
MCA stenosis is 4% to 12% per
year.11 12 13 14 15 16 The Extracranial-Intracranial (EC-IC)
Bypass Study17 18 provides prospective data on
the risk of stroke in patients with symptomatic carotid
siphon or MCA stenosis. In that trial, patients with carotid
siphon or MCA stenosis who were treated medically (ie,
management of risk factors and 1300 mg/d aspirin) had an annual stroke
rate of 8% to 10%.17 18
Subjects and Methods
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
Appendix 1
References
Study Design and Patient Identification
Patients enrolled in the WASID study22
were candidates for the current study. WASID was a retrospective,
multicenter, nonrandomized study that compared the efficacy of warfarin
versus aspirin for preventing stroke, MI, or sudden death in patients
with symptomatic stenosis (50% to 99%) of a major
intracranial artery (carotid siphon; anterior, middle, or posterior
cerebral artery; vertebral artery; basilar artery; or posterior
inferior cerebellar artery)
.22 
50%" intracranial stenosis. The exact degree of
stenosis was measured by the local investigator through
comparison of the diameter of the vessel at the site of
stenosis (D stenosis) with the normal diameter of the
vessel just distal to the stenosis (D distal) using the
following formula: % stenosis=(1-[D stenosis/D
distal])x100%.23 Patients whose angiogram
reports indicated a severe or 50% intracranial stenosis but
whose angiograms were not available for review (only 6% of patients)
were still considered potential candidates for the study. The medical
records of patients with a measured intracranial stenosis
of 50% or an angiogram report indicating a severe or 50%
stenosis were subsequently reviewed.
Inclusion criteria for the current study were (1) 50% to 99%
stenosis of one of the following arteries in the posterior
circulation: intracranial vertebral artery, basilar artery, PCA, or
PICA; (2) a transient ischemic attack or stroke in the
distribution of the stenotic artery; and (3) therapy with
aspirin or warfarin.
Treatment with aspirin or warfarin was based on local physician
preference. The most common dose of aspirin prescribed for stroke
prophylaxis was 325 mg/d, and warfarin therapy was typically adjusted
to maintain prothrombin times in the range of 1.2 to 1.6 times control.
None of the centers were using the prothrombin time international
normalized ratio for measuring levels of anticoagulation during the
period 1985 to 1991.
Risk factor profiles and angiographic findings were compared in
patients treated with warfarin versus aspirin.
2 tests or Fisher exact tests were used to
compare rates and proportions of categorical variables;
t tests were used to compare the means of continuous
variables. Cumulative event-free rates for the time to a major
vascular event (stroke, MI, or sudden death) were estimated by the
Kaplan-Meier product limit method, and the 2 treatment groups were
compared with the log-rank statistic. Since there were relatively few
hemorrhagic complications, comparison of these rates in the 2 treatment
groups was performed by fitting a log-linear model, assuming a Poisson
distribution, and adjusting for duration of follow-up. All comparisons
of event rates in the 2 treatment groups were 2 tailed and based on an
intention-to-treat analysis.
Results
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
Appendix 1
References
Patient Enrollment and Angiographic Lesions
Sixty-eight patients with symptomatic stenosis
(50% to 99%) of a major intracranial artery in the posterior
circulation qualified for the current study. The intracranial
stenoses involved 1 vertebral artery in 26 patients (38%),
both vertebral arteries in 5 patients (7%), the basilar artery alone
in 20 patients (30%), tandem basilar and vertebral artery
stenoses in 6 patients (9%; 5 unilateral vertebral
stenosis and 1 bilateral vertebral stenoses), tandem
basilar and PCA stenoses in 2 patients (3%), unilateral PCA
stenosis in 6 patients (9%), and unilateral PICA
stenosis in 3 patients (4%). Forty-two patients (62%) were
treated with warfarin, and 26 (38%) were treated with aspirin. In the
aspirin group, 21 of 26 (81%) were treated with at least 325 mg/d
aspirin.
During a median follow-up of 13.8 months, 15 patients (22%)
had an ischemic stroke (4 were fatal; 10 were in the same
territory as the symptomatic stenotic artery), 3
patients (4.5%) had a fatal MI or sudden death, and 6 patients (9%)
had a nonfatal MI. The rates of primary end points (per 100
patient-years of follow-up) were 13.1 for ischemic stroke in
any vascular territory (8.7 in the same territory as the
stenotic artery, 4.4 in a different territory), 2.6 for fatal
MI or sudden death, and 5.2 for nonfatal MI. The artery-specific stroke
rates for the basilar artery, vertebral artery, and PCA/PICA are shown
in Table 1
.
View this table:
[in a new window]
Table 1. Stroke Rates Associated With Intracranial Vertebral
Artery, Basilar Artery, or PCA/PICA Stenosis
Risk factor profiles and angiographic findings of patients in the
2 treatment groups are shown in Table 2.
There were no significant differences between the 2 groups in the rates
of traditional vascular risk factors, previous stroke, or type of
qualifying event (ie, transient ischemic attack or stroke).
Additionally, the mean age of patients and mean percent
stenosis of the symptomatic intracranial artery in
both treatment groups were similar (Table 2). The percentage of
patients who had a measured intracranial stenosis of 80% to
99% or an angiogram report indicating a severe intracranial
stenosis was 55% (23 of 42) in the warfarin group and 50% (13
of 26) in the aspirin group. Of 33 patients with bivertebral or basilar
artery stenoses, 24 (73%) were treated with warfarin and 9
(27%) were treated with aspirin (P=0.09).
View this table:
[in a new window]
Table 2. Risk Factor Profiles: Warfarin Group Versus
Aspirin Group
Patients treated with aspirin had a significantly higher
rate of ischemic stroke in any vascular territory compared with
patients treated with warfarin (stroke rates per 100 patient-years of
follow-up were 21.5 on aspirin versus 6.3 on warfarin;
P=0.02). There were no significant differences, however,
between the 2 groups in the rates of ischemic stroke, MI, and
sudden death combined (27.4/100 patient-years on aspirin versus
15.7/100 patient-years on warfarin; P=0.18) or in the rates
of MI and sudden death combined (5.9/100 patient-years on aspirin
versus 9.4/100 patient-years on warfarin; P=0.49).
Of 26 patients treated with aspirin for a median follow-up of 19.7
months, 6 (23%) had a stroke in the same territory as the
stenotic intracranial artery (2 of 13 patients [15%]
with unilateral vertebral artery stenosis, 3 of 9
patients [33%] with stenosis involving the basilar
artery, and 1 of 4 [25%] with PCA or PICA stenosis). The
rate of stroke in the same territory as the stenotic artery in
patients on aspirin (per 100 patient-years) was 11.7 (9.6 in patients
with 50% to 79% stenosis versus 15.1 in patients with 80% to
99% stenosis).
Discussion
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
Appendix 1
References
Previous studies19 20 21 suggest that
the risk of stroke associated with intracranial vertebral artery,
basilar artery, or PCA stenosis is approximately 2.5% to 5.5%
per year. Moufarrij et al19 studied 44 patients
(mean age, 57 years) with angiographically proved stenosis of
50% of the intracranial vertebral artery or basilar artery. Both
asymptomatic and symptomatic patients were
included. Treatment consisted of aspirin or
dipyridamole in 18 (41%), warfarin in 14 (32%), no
antithrombotic therapy in 7 (16%), and undetermined treatment in 5
(11%). During a mean follow-up of 6.1 years, 8 patients (18%) had a
stroke (3 fatal; 5 of the 8 strokes were in the territory of the
stenotic artery) and 5 patients (11%) died from causes
unrelated to stroke (2 cardiac). Six of 8 strokes occurred in patients
on a regimen of aspirin or dipyridamole, and 1 occurred
in a patient on no antithrombotic therapy; treatment was not determined
in the other patient who had a stroke. None of the patients taking
warfarin had a stroke. 
2 years). The mean age was 62 years; 5
were treated with warfarin and 2 with aspirin or
dipyridamole, and 2 were on no antithrombotic therapy.
During follow-up, 1 patient (11%) taking warfarin had a fatal brain
stem stroke and 2 patients died (1 of the original stroke and 1 of
alcohol abuse). In a study of 6 patients with PCA stenosis who
were treated with warfarin, 1 patient had a stroke (MCA territory) and
2 patients died (1 of traumatic brain hemorrhage and 1 of
sudden death) during follow-up of 4 months to 4
years.21 50% stenosis of the
intracranial vertebral artery, basilar artery, PCA or PICA, the rates
of stroke were substantially higher (Table 1
) than in previous studies
of patients with posterior circulation stenosis. Possible
explanations for the difference in stroke rates between these studies
are the higher frequency of vascular risk factors and severe
stenoses in the current study and inclusion of
asymptomatic patients and lower mean age of patients in
previous studies. Patients with basilar artery or vertebral artery
stenoses (particularly bilateral vertebral artery
stenosis) had the highest rate of stroke in this study (Table 1). Moreover, the stroke rates in patients with basilar artery or
vertebral artery stenosis were higher than the rates of stroke
reported in patients with symptomatic stenosis of
the carotid siphon or MCA11 12 13 14 15 16 17 18 and approached
the stroke rates of patients with symptomatic extracranial
carotid stenosis of 70%.23
Selected Abbreviations and Acronyms
MCA
=
middle cerebral artery
MI
=
myocardial infarction
PCA
=
posterior cerebral artery
PICA
=
posterior inferior cerebellar artery
WASID
=
Warfarin-Aspirin Symptomatic Intracranial Disease
Acknowledgments
This article is dedicated to the memory of Michael S. Pessin MD,
one of the original WASID investigators, an inspirational teacher, and
a close colleague of the Study Group.
Footnotes
A complete list of the members of the WASID Study Group appears in the Appendix.
Appendix 1
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
Appendix 1
References
Financial support was received from the manufacturers of warfarin or aspirin by Dr Chimowitz, who gave grand rounds at the University of New Mexico in 1993, in the form of an honorarium provided by DuPont Pharma. DuPont Pharma supported two meetings of the WASID study group (both in 1996). DuPont Pharma and Bayer have agreed to provide study medications for a planned clinical trial for which WASID is applying for NIH funding. They are not providing financial support for the trial. Dr Sila has received honoraria for lectures supported by DuPont Pharma and the Aspirin Foundation. Dr Levine has received a research grant from DuPont Pharma.
References
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
Appendix 1
References
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W.-J. Jiang, Y.-J. Wang, B. Du, S.-X. Wang, G.-H. Wang, M. Jin, and J.-P. Dai Stenting of Symptomatic M1 Stenosis of Middle Cerebral Artery: An Initial Experience of 40 Patients Stroke, June 1, 2004; 35(6): 1375 - 1380. [Abstract] [Full Text] [PDF]
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V. Beletsky, Z. Nadareishvili, J. Lynch, A. Shuaib, A. Woolfenden, and J. W. Norris Cervical Arterial Dissection: Time for a Therapeutic Trial? Stroke, December 1, 2003; 34(12): 2856 - 2860. [Abstract] [Full Text] [PDF]
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J. F. Arenillas, J. Alvarez-Sabin, C. A. Molina, P. Chacon, J. Montaner, A. Rovira, B. Ibarra, and M. Quintana C-Reactive Protein Predicts Further Ischemic Events in First-Ever Transient Ischemic Attack or Stroke Patients With Intracranial Large-Artery Occlusive Disease Stroke, October 1, 2003; 34(10): 2463 - 2468. [Abstract] [Full Text] [PDF]
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 G.C. Cloud and H.S. Markus Diagnosis and management of vertebral artery stenosis QJM, January 1, 2003; 96(1): 27 - 54. [Full Text] [PDF]
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J.P. Mohr, J.L.P. Thompson, R.M. Lazar, B. Levin, R.L. Sacco, K.L. Furie, J.P. Kistler, G.W. Albers, L.C. Pettigrew, H.P. Adams Jr., et al. A Comparison of Warfarin and Aspirin for the Prevention of Recurrent Ischemic Stroke N. Engl. J. Med., November 15, 2001; 345(20): 1444 - 1451. [Abstract] [Full Text] [PDF]
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W. J. Powers Oral Anticoagulant Therapy for the Prevention of Stroke N. Engl. J. Med., November 15, 2001; 345(20): 1493 - 1495. [Full Text] [PDF]
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 C. R. Gomez and S. C. Orr Angioplasty and Stenting for Primary Treatment of Intracranial Arterial Stenoses Arch Neurol, October 1, 2001; 58(10): 1687 - 1690. [Full Text] [PDF]
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M. I. Chimowitz Angioplasty or Stenting Is Not Appropriate as First-Line Treatment of Intracranial Stenosis Arch Neurol, October 1, 2001; 58(10): 1690 - 1692. [Full Text] [PDF]
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 M. Piotin, R. Blanc, R. Kothimbakam, D. Martin, I. B. Ross, and J. Moret Primary Basilar Artery Stenting: Immediate and Long-Term Results in One Patient Am. J. Roentgenol., November 1, 2000; 175(5): 1367 - 1369. [Full Text] [PDF]
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C. C. Phatouros, J. E. Lefler, R. T. Higashida, P. M. Meyers, A. M. Malek, C. F. Dowd, and V. V. Halbach Primary Stenting for High-grade Basilar Artery Stenosis AJNR Am. J. Neuroradiol., |