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TECHNICAL CASE REPORT

OCCIPITAL ARTERY-TO-POSTERIOR INFERIOR


CEREBELLAR ARTERY BYPASS FOR TREATMENT OF
BILATERAL VERTEBRAL ARTERY OCCLUSION:
THE ROLE OF QUANTITATIVE MAGNETIC RESONANCE
ANGIOGRAPHY NONINVASIVE OPTIMAL VESSEL
Robert M. Starke, B.A.
ANALYSIS: TECHNICAL CASE REPORT
St. Luke’s Roosevelt Hospital Center,
New York, New York, and OBJECTIVE: Patients with partial or complete bilateral vertebral artery occlusion often
Albert Einstein College of Medicine,
Bronx, New York
present with signs and symptoms of transient ischemic attacks or infarction. Advances
in phase contrast magnetic resonance imaging have led to noninvasive assessment of
Mark Chwajol, M.D. volumetric blood flow rates and direction that help in the workup and management of
St. Luke’s Roosevelt Hospital Center, these patients.
New York, New York, and CLINICAL PRESENTATION: We present the case of a patient with symptoms of verte-
Albert Einstein College of Medicine,
Bronx, New York
brobasilar insufficiency without previous transient ischemic attacks or stroke. Quantitative
magnetic resonance angiography (QMRA) demonstrated bilateral vertebral artery occlu-
Daniel Lefton, M.D. sion with reversal of flow in the basilar and vertebral arteries to the level of the poste-
Department of Radiology, rior inferior cerebellar arteries bilaterally. A prominent right posterior communicating
St. Luke’s Roosevelt Hospital Center, and artery filled the basilar artery and proximal vertebral arteries.
Beth Israel Medical Center,
New York, New York INTERVENTION: The presence of reversal and diminished flow in the basilar and ver-
tebral arteries suggested that occipital artery-to-posterior inferior cerebellar artery bypass
Chandranath Sen, M.D. would improve posterior circulation, relieve symptoms, and reduce the risk of infarc-
St. Luke’s Roosevelt Hospital Center, tion. Postoperative QMRA and angiography confirmed revascularization, and QMRA con-
New York, New York, and firmed correction of blood flow direction.
Albert Einstein College of Medicine,
Bronx, New York CONCLUSION: This case illustrates the potential of QMRA as part of a comprehen-
sive cerebrovascular assessment, operative planning, and follow-up of patients with
Alejandro Berenstein, M.D. vertebrobasilar insufficiency.
St. Luke’s Roosevelt Hospital Center,
KEY WORDS: Blood flow, Bypass, Cerebral ischemia, Cerebrovascular disease, Revascularization, Vertebral
New York, New York, and
Albert Einstein College of Medicine,
artery occlusion, Vertebrobasilar insufficiency
Bronx, New York
Neurosurgery 64:E779–E781, 2009 DOI: 10.1227/01.NEU.0000339351.65061.D6 www.neurosurgery-online.com

David J. Langer, M.D.


St. Luke’s Roosevelt Hospital Center,

S
New York, New York, and tudies have found that patients with edge, in all but 1 reported case of bilateral ver-
Albert Einstein College of Medicine, intracranial vertebrobasilar stenosis experi- tebral occlusion, patients have presented with
Bronx, New York ence stroke rates of 4.5% to 15% (7, 13, 19). TIAs or infarction (4). The role of medical ther-
Reprint requests: Although there have been a limited number of apy in the treatment of symptomatic verte-
David J. Langer, M.D., patients with asymptomatic bilateral vertebral brobasilar stenosis remains controversial, and
1000 Tenth Avenue, artery occlusion, the rate of transient ischemic its effects in bilateral vertebral artery occlusion
Suite 5G-49,
attack (TIA) or stroke may approach 100% in remain even more unclear (9, 11, 19, 24, 25).
New York, NY 10019.
Email: DLanger@chpnet.org these patients (3–5, 11, 15, 17). To our knowl- Advances in bypass surgery (10, 23) and endo-

Received, April 6, 2008. ABBREVIATIONS: AICA, anteroinferior cerebellar artery; ICA, internal carotid artery; MRA, magnetic reso-
Accepted, October 10, 2008. nance angiography; NOVA, noninvasive optimal vessel analysis; OA, occipital artery; PCA, posterior cere-
bral artery; PComA, posterior communicating artery; PICA, posterior inferior cerebellar artery; QMRA,
Copyright © 2009 by the
quantitative magnetic resonance angiography; TIA, transient ischemic attack
Congress of Neurological Surgeons

NEUROSURGERY VOLUME 64 | NUMBER 4 | APRIL 2009 | E779


STARKE ET AL.

vascular treatment (12, 14) have provided more options for QMRA NOVA testing demonstrated significantly diminished
definitive treatment of patients with vertebrobasilar insuffi- and reversed blood flow in the basilar artery above (⫺22
ciency. However, options for screening, diagnosis, operative mL/min) and below (⫺17 mL/min) the anteroinferior cerebel-
planning, and follow-up of these patients have remained unclear. lar arteries (AICAs). Only 17 mL/min of flow was available for
We report the rare case of a patient with symptomatic bilat- perfusion of the lower brainstem and posterior inferior cerebel-
eral vertebral artery occlusion that presented before TIA or lar arteries (PICAs); some additional supply was likely pro-
infarction. We evaluate the role of quantitative magnetic reso- vided from the anterior spinal artery. Reversed and diminished
nance angiography (QMRA) (phase contrast magnetic reso- flow was also noted in the vertebral arteries distally to the
nance angiography [MRA] coupled with noninvasive optimal points of occlusion (left vertebral artery, ⫺15 mL/min; right
vessel analysis [NOVA]) in cerebrovascular assessment, opera- vertebral artery, ⫺16 mL/min) (Fig. 1). Additionally, flow
tive planning, and patient follow-up. through the right middle cerebral and anterior cerebral arteries
was at the low end of normal (110 and 82 mL/min, respec-
CASE REPORT tively) because of shunting of blood from the right internal
carotid artery (ICA) to the posterior circulation via the right
A 39-year-old man with no significant medical history presented posterior communicating artery (PComA) (flow of 54 mL/min).
with dizziness, particularly when moving from sitting to standing, and Flows in the right and left posterior cerebral arteries (PCAs)
vertigo. Originally mild symptoms progressed to severe dizziness and were below the normal range (45 and 26 mL/min, respectively)
later included imbalance and diplopia. Alternative causes for the (Fig. 1A).
patient’s symptoms were ruled out through appropriate cardiac, hema-
Selective angiography of the vertebral arteries confirmed
tological, metabolic, and migraine assessment. A diagnosis of bilateral
vertebral artery occlusion was made on MRA and then confirmed by
bilateral vertebral occlusion and revealed a diminutive anterior
QMRA NOVA and later by cerebral angiography. The patient received spinal artery contributing to the blood supply in the posterior
heparin and then warfarin. No evidence of stroke was found on the circulation (Fig. 2). Selective angiography of the right ICA
magnetic resonance imaging scan. demonstrated the right PComA artery filling the right PCA,
basilar artery, both PICAs, and vertebral arteries distal to the
RESULTS occlusion (Fig. 3, A and B). Selective angiography of the left
ICA showed the left PComA artery filling the left P1 segment
QMRA is performed in conjunction with standard MRA. and the remainder of the left PCA distribution. Stenosis of the
Information from phase contrast MRA is enhanced with com- left P1 segment was also noted (Fig. 3C).
mercially available software called NOVA, which has been A larger vessel to PCA bypass was considered. The presence
described previously (22). Normal blood flow ranges for indi- of an apparent left P1 stenosis made left PCA bypass less attrac-
vidual cerebral arteries as measured by NOVA are listed in tive because the stenosis would potentially lead to poor revas-
Table 1 (29). cularization in the left PCA territory. The reversed and dimin-
ished flow in the basilar and vertebral arteries and the
significantly decreased blood supply to the PICA territory (17
TABLE 1. Normal blood flow ranges for individual cerebral arter- mL/min) were indicative of high demand. We thought that, in
ies as measured by noninvasive optimal vessel analysisa this setting, a low-risk bypass to the PICA would remain patent
and provide sufficient blood supply, and that a higher-risk,
Vessel Range (mL/min)
higher-flow conduit bypass would not be required. Considering
L ICA 190–340 the presence of a robust left occipital artery (OA), a safer left
R ICA 180–310 OA-to-PICA bypass was selected.
L MCA 110–210 After a suboccipital craniotomy, the left PICA was gently
R MCA 100–200 dissected, and the flow was measured to be 8 mL/min. Cut
flow in the OA was 21 mL/min before the bypass (1). After
L ACA 60–170
suturing of the donor vessel to the recipient vessel, the donor
R ACA 60–160 vessel had a flow of 20 mL/min, and the recipient vessel now
L VA 80–170 had a bidirectional flow of 8 mL/min in the distal direction and
R VA 80–170 12 mL/min in the proximal direction. The calculated cut flow
BA 160–260 index was 1.0, indicating good bypass patency and a low risk
L PCA 50–100
of postoperative occlusion (1).
Postoperative QMRA NOVA demonstrated revascularization
R PCA 50–100
of the territory, with augmentation in the PICA and reversal of
a
L, left; R, right; ICA, internal carotid artery; MCA, middle cerebral artery; ACA, flow in the basilar artery and vertebral arteries bilaterally. Blood
anterior cerebral artery; VA, vertebral artery; BA, basilar artery; PCA, posterior cerebral flow was reversed (now antegrade) and increased to 62 and 58
artery. Standard flow values are based on research conducted at the Department of mL/min in the left and right vertebral arteries, respectively. In
Neurosurgery, University of Illinois at Chicago. Specific citations to authorities are the basilar artery, the flow appeared to be bidirectional with ⫺30
available upon request at VasSol, Inc., Chicago, IL.
mL/min in the upper portion (retrograde above the AICA) and

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TREATMENT OF BILATERAL VERTEBRAL ARTERY OCCLUSION

A A B

FIGURE 2. A, selective preoperative angiogram showing that the right


vertebral artery (large arrow) is occluded intracranially, but a prominent
anterior spinal artery (small arrow), originating from the right vertebral
artery at the C4 level (not shown), opacifies the posterior circulation. B,
selective preoperative angiogram showing that the left vertebral artery
(large arrow) irregularly tapers off distal to the C1 level and occludes at the
level of the foramen magnum. Small collateral vessels (small arrow)
attempt to reconstitute the left vertebral artery, and a faint opacification of
the left posterior inferior cerebellar artery (PICA) is observed. A prominent
C1 branch from the vertebral artery forms an anastomosis with the left
B occipital artery (OA) (long arrow).

A B

FIGURE 3. Selective lateral (A) C


and anteroposterior (B) angio-
FIGURE 1. A, diagram of quantitative magnetic reso- grams of the right internal carotid
nance angiography (QMRA) noninvasive optimal ves- artery (ICA) demonstrating the
sel analysis (NOVA) before surgery, demonstrating right PComA (arrow) filling the
reversal and significantly diminished flow in the basi- right posterior cerebral, basilar,
lar artery (⫺22 mL/min) above the anteroinferior cere- and bilateral PICA and vertebral
bellar arteries (AICAs). Reversed and diminished flow arteries distal to the occlusion. C,
is also noted in the vertebral arteries (VAs) proximally selective lateral angiogram of the
to the points of occlusion (left VA, ⫺15 mL/min; right left ICA showing the left PComA
VA, ⫺16 mL/min). Note increased flow in the right (arrow) artery filling the left P1
posterior communicating artery (PComA) (54 mL/min) segment and the remainder of the
as it provides significant blood flow to the posterior cir- left PCA distribution.
culation. B, QMRA NOVA before surgery demonstrat-
ing diminished flow in the basilar artery below the
AICA (⫺17 mL/min). R, right; L, left; ACA, anterior the right and 45 mL/min on the left. Flow through the right
cerebral artery; MCA, middle cerebral artery; PCA, PComA artery was decreased from 54 to 26 mL/min (Fig. 4).
posterior cerebral artery; BA, basilar artery. Postoperative angiography was used to confirm QMRA find-
ings. Angiography demonstrated a patent left OA-to-PICA
bypass with increased retrograde flow down from the bypass
46 mL/min in the lower portion of the artery (antegrade below to the left vertebral artery. The bypass also provided flow to the
the AICA). Flow in the PCAs was augmented to 76 mL/min on contralateral vertebral artery and the basilar artery up to the

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STARKE ET AL.

A A

B
B

FIGURE 4. A, diagram of postoperative QMRA NOVA


demonstrating reversal of flow in the basilar artery and
vertebral arteries bilaterally. In the basilar artery, the
flow is bidirectional with ⫺30 mL/min in the upper
portion (retrograde above the AICA). Blood flow is
reversed (now antegrade) and increased to 62 and 58
mL/min in the left and right vertebral arteries, respec- FIGURE 5. Postoperative selective lateral (A) and anteroposterior (B)
tively. Flow through the right PComA is decreased from external carotid artery angiograms demonstrating a patent left OA-to-
54 to 26 mL/min. B, QMRA NOVA showing that flow PICA bypass (dashed arrow) with increased retrograde flow down the left
in the lower portion of the basilar artery is 46 mL/min vertebral artery (large arrow). The bypass also supplies flow to the con-
(antegrade below the AICA). tralateral vertebral artery and the basilar artery up to the level of the
AICA (small arrow).

level of the AICA (Fig. 5). Selective ICA injections revealed that
the right PComA filled the right PCA and superior cerebellar DISCUSSION
arteries bilaterally but no longer supplied blood flow to the
basilar artery below this level (Fig. 6). The left PComA contin- We report the rare case of a patient with symptomatic bilateral
ued to supply the left PCA territory. The patient’s symptoms vertebral artery occlusion that presented before TIA or infarction.
resolved, and he returned to work. He remained intact and QMRA was used to noninvasively diagnose the bilateral verte-
working at the time of the 6-month follow-up examination. bral occlusion and quantify the decrease and reversal of flow in

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TREATMENT OF BILATERAL VERTEBRAL ARTERY OCCLUSION

A TABLE 2. Outcomes of patients with bilateral intracranial verte-


bral artery occlusion treated with occipital artery-to-posterior
inferior cerebral artery bypass
No. of
Series (ref. no.) Outcome
cases
Ausman et al., 1990 (3) 11 4 improved and
asymptomatic
7 asymptomatic
Roski et al., 1982 (15) 6 3 improved
2 normal
1 same
Sundt et al., 1978 (18) 7 4 excellent
2 good
1 improved
Bogousslavsky 1 1 transient ischemic
et al., 1986 (4) attack

B
matic vertebrobasilar stenosis have annual stroke rates of 4.5%
to 15% (7, 13, 19). The exact prognosis in patients with bilateral
vertebral artery occlusion is unclear, but mortality in untreated
patients may approach 100%, with significant morbidity in sur-
vivors (3, 5, 20).
The role of medical therapy in patients with vertebrobasilar
insufficiency is unclear. A significant number of patients experi-
ence infarction despite treatment with heparin, warfarin, or
aspirin (9, 11, 19, 24, 25). The indications for surgical therapy in
patients with vertebrobasilar insufficiency remain incompletely
defined. In a recent study of patients with symptomatic verte-
brobasilar disease, all patients received QMRA NOVA as part of
the workup (2). Patients were classified as having either low or
normal distal flow in the vertebrobasilar circulation based on
the quantitative flow rates measured by QMRA NOVA. Patients
with normal distal flow were treated medically, resulting in 0%
stroke and 2.5% stroke/TIA rate per person-year at the 2-year
FIGURE 6. Postoperative selective anteroposterior (A) and lateral (B) right follow-up. Patients with low distal flow were offered surgical or
ICA angiograms revealing that the right PComA (arrow) fills the right endovascular treatment. Patients with low distal flow who
PCA and superior cerebellar artery but no longer fills the basilar artery. refused surgical or endovascular treatment (n ⫽ 4) experienced
18.9% stroke and 28.3% stroke/TIA rates per person-year, versus
the posterior circulation and increase of flow in the anterior cir- a 10.9% yearly ischemic event rate in the 12 patients who under-
culation. A noninvasive modality was used to diagnose a vessel went surgical or endovascular treatment.
occlusion, and preoperative angiography was used to corrobo- In studies of patients who underwent OA-to-PICA bypass
rate the findings found on QMRA. After left OA-to-PICA bypass, for vertebrobasilar insufficiency, success rates of 75% to 100%
the patient’s symptoms resolved, and we were able to demon- have been reported, with morality rates of 0% to 14% (3, 11, 15,
strate restoration and reversal of flow in the basilar and vertebral 17). Patients with bilateral vertebral artery occlusion may be at
arteries. This represents the first quantitative depiction of this increased risk of surgical infarction because of less collateral
phenomenon and provides further validation of QMRA NOVA blood flow, but they also seem to have a significantly more dis-
as a noninvasive technology capable of quantifying flow rate mal prognosis than patients with unilateral vertebral stenosis if
and direction in the intracranial circulation. left untreated. A review of 25 cases from various case reports
Bilateral vertebral artery occlusion is an exceedingly rare and case series of patients who presented with TIAs and/or
condition, occurring in approximately 0.5% of stroke patients infarction and underwent OA-to-PICA bypass for bilateral
(6). Almost all patients reported in the literature presented with intracranial vertebral artery occlusion showed that 14 patients
repeated TIAs and/or posterior circulation infarctions (3, 5, 11, had improved, excellent, or good results; 9 patients experi-
15, 17). Studies have demonstrated that patients with sympto- enced no further symptoms or remained asymptomatic; 1

NEUROSURGERY VOLUME 64 | NUMBER 4 | APRIL 2009 | E781


STARKE ET AL.

patient had no change; and 1 patient had new onset of TIAs (3, flow grafts in difficult locations more feasible (8, 16, 21, 23).
4, 5, 15, 18) (Table 2). Further studies with QMRA in bypass surgery of the posterior
In contrast to the prodrome of basilar artery occlusion, branch circulation could provide critical information about the flow in
disease, or embolic stroke, the prodromal symptoms of bilateral the recipient vessel and the quantity of flow that must be
vertebral artery occlusion can develop over many weeks before replaced to various ischemic regions.
infarction (5, 11). QMRA is a noninvasive imaging technique QMRA NOVA can identify the cross sectional area, quantity,
and does not require the administration of contrast medium. and direction of flow of a vessel. It is possible that the level and
The role of QMRA NOVA lies in the early diagnosis of verte- degree of stenosis, the quantity, direction, and reversal of flow
brobasilar insufficiency—during a TIA and before infarction. preoperatively, as well as the presence of reversal of flow direc-
When NOVA fails to detect occlusion, a nonvascular etiology of tion postoperatively, could predict clinical outcome (2, 19).
the patient’s symptoms should be considered, and a cerebral Analysis of flow data provided by QMRA NOVA may explain
angiogram might not be indicated. When early occlusion or
the great variance in the rates of bypass patency and morbid-
stenosis is diagnosed, cerebral angiography can be performed to
ity and mortality among patients with OA-to-PICA and other
assess the anatomy of large vessels and collaterals before poten-
kinds of bypass. Further studies with larger numbers of
tial revascularization surgery. An early diagnosis allows non-
patients need to be conducted to assess the utility of the infor-
emergent planning and surgery, and a better clinical outcome
mation supplied by the noninvasive modality, with emphasis
after definitive surgical treatment is more likely.
In a study of patients with vertebrobasilar insufficiency treated on identifying key prognostic factors for treatment outcome.
by extracranial-to-intracranial bypass, stable patients (with pre-
vious TIAs) had a better outcome than unstable patients (with CONCLUSION
crescendo TIAs or stroke in evolution). If stable patients are med-
ically managed for longer periods until they become unstable, This case illustrates the potential of QMRA as part of com-
the risk of surgery increases (3). prehensive pre- and postoperative management in patients
In our study, QMRA NOVA served as a valuable tool for pre- with posterior circulation steno-occlusive disease. QMRA has
operative quantification of the amount and direction of blood the ability to identify the cross sectional area, quantity, and
flow in the large vessels. Preoperative conventional angiogra- direction of flow of a vessel—parameters that can be valuable
phy was used to better assess the vessel anatomy and the in recipient vessel selection and graft patency monitoring.
degree and anatomy of collateral circulation. Postoperatively, QMRA allows for a noninvasive cerebrovascular assessment
QMRA NOVA was used to provide additional information and can be beneficial in diagnosis, treatment planning, and
about the amount and direction of flow; it was not intended to follow-up of patients with vertebrobasilar insufficiency.
replace an angiogram and its importance in the postoperative
assessment of vessel and bypass patency. We advocate the use DISCLOSURE
of QMRA NOVA as an important adjunct to conventional cere-
bral angiography, and not a replacement of it, because the 2 David J. Langer, M.D., is on the scientific advisory board of VasSol, Inc.,
modalities evaluate different aspects of the same cerebrovascu- Chicago, IL. David J. Langer, M.D., Daniel R. Lefton, M.D., and Alejandro
Berenstein, M.D., have served as advisors to VasSol, Inc. The other authors have
lar condition (vessel anatomy versus amount of blood flow).
no personal financial or institutional interest in any of the drugs, materials, or
The degree of flow decrease or reversal on preoperative devices described in this article.
QMRA NOVA implies an increased demand and, therefore, is
likely to indicate good patency and flow in the bypass. In
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24. Weksler BB, Lewin M: Anticoagulation in cerebral ischemia. Stroke 14:658– patients with difficult posterior circulation occlusive disease have a
663, 1983. mixture of flow-related and embolic problems, in addition to difficult
25. Whisnant JP, Cartlidge NE, Elveback LR: Carotid and vertebral-basilar tran- medical problems. They were not studied as part of the international
sient ischemic attacks: Effect of anticoagulants, hypertension, and cardiac bypass trial to evaluate superficial temporal artery-to-middle cerebral
disorders on survival and stroke occurrence—A population study. Ann artery bypass and are not part of the Carotid Occlusion Surgery Study
Neurol 3:107–115, 1978. trial. In some of these patients, an external carotid artery-to-vertebral
artery (V3 segment) bypass (with saphenous vein or radial artery) can
Acknowledgments be performed very safely, when the vertebral artery is occluded proxi-
We thank Rafael Ortiz, M.D., and Lauren Ostergren, B.S., for their help with mally. In others, an OA-to-PICA bypass, superficial temporal artery-to-
this project. superior cerebellar artery bypass, and external carotid artery-to-poste-

NEUROSURGERY VOLUME 64 | NUMBER 4 | APRIL 2009 | E781


STARKE ET AL.

rior communicating artery bypass are available surgical options. When ation, just putting them to sleep for any procedure carries some risk of
endovascular access to a stenotic vessel is possible, angioplasty and stroke and death, and this needs to be considered in making a treat-
stent placement of the vertebral artery and of the basilar artery are fea- ment decision.
sible; however, there has not been a careful evaluation of the risk ver-
sus benefit of the medical, surgical, and endovascular options in the Laligam N. Sekhar
various patients. Because these patients often have a very fragile situ- Seattle, Washington

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