Introduction
Cerebral revascularization by extracranial-to-intracranial (EC–IC) anastomosis between
the superficial temporal artery (STA) and the middle cerebral artery (MCA) is not
a commonly performed procedure in most neurosurgery training centers.
The initial enthusiasm for the new technique proposed by Yasargil[1] was dampened after the results of the first multicenter randomized controlled trial
on cerebral revascularization, which was funded by the National Institutes of Health
(NIH).[2]
However, the methodology of that study received much criticism and the validity of
its conclusions was called into question. In addition, the results of other multicenter
studies proving the benefits of another type of revascularization, endarterectomy
to treat carotid stenosis, reawakened interest in the EC–IC bypass technique.
The results of another multicenter study evaluating the indication of EC–IC bypass
surgery for carotid artery (CA) occlusion have been published recently.[3] Although EC–IC bypass was shown to increase cerebral blood flow, the procedure was
not superior to best medical treatment in stroke prevention.
In addition to the indication for atherosclerotic disease, EC–IC bypass is indicated
for the treatment of Moyamoya disease, arterial stenosis due to neoplasia, and in
the management of giant or complex brain aneurysms.
We present a case-series study of EC–IC bypass procedures performed in our service
and evaluate indications and results. We have included the cases of EC–IC bypass for
the posterior circulation.
Methods
We evaluated retrospectively the medical records of 30 patients undergoing 32 EC–IC
anastomosis procedures by the senior author in the period between January 1996 and
December 2013. Seventeen patients were male (56.6%). The age ranged from 26 to 85
years (mean: 58.2). The follow-up ranged from 1 to 211 months (mean: 54). We evaluated
the indications and complications of the surgical procedures. Late patency of the
anastomosis has been verified by imaging tests (angiography, angiotomography, or angio-MRI).
During the follow-up period we evaluated the incidence of stroke and death.
This study was approved by the Research Ethics Committee of the Biocor Institute.
All patients signed informed consent form.
Technique
Antiplatelet drugs were discontinued 7 days prior to the procedure. The patients received
bridge therapy with 40 mg subcutaneous enoxaparin, as done for endarterectomy.[4] Intraoperative monitoring, fluid loading, and choice of anesthetic agents were left
to the discretion of the anesthesiologist, with the recommendation of maintaining
normocapnia. All the patients were given antibiotics 1 hour before surgery through
the first postoperative (PO) day. Only one anastomosis was done in each patient. Either
the frontal or temporal branch of the STA was dissected; the connective tissue surrounding
the vessel adventitia was spared. The end centimeter of the arterial graft was prepared
in a “fish mouth” shape. Arterial blood flow was stopped with temporary clipping.
A circumferential frontotemporal craniotomy was done ([Fig. 1]). The dura mater was open and a cortical branch of the MCA was dissected to receive
the STA graft. This segment was isolated with the aid of small temporary clips. A
longitudinal arteriotomy was performed proportional to the luminal diameter of the
temporal artery graft. An end-to-side anastomosis was done using interrupted 9.0 Prolene
or nylon sutures. The patient was not heparinized during the anastomosis procedure.
After completion of the anastomosis, the temporary clips were removed. Any bleeding
on the suture line was controlled by gentle compression with Cottonoids and Surgicel.
The graft patency was tested by stopping the MCA flow upstream of the anastomosis
and assessing the arterial flow in the segment distal to the anastomosis. On the first
PO day, the patients were started on 325 mg oral aspirin or 75 mg clopidogrel daily.
Fig. 1 Craniotomy bypass. CT angiotomography showing circumferential craniotomy.
Results
The bypass procedures comprised 28 STA–MCA anastomoses (87.5%) and 4 posterior circulation
anastomoses. Of the latter, three procedures involved the occipital artery and the
vertebral artery, and one involved the occipital artery and a postmeatal segment of
the anterior inferior cerebellar artery (AICA). The indications were cervical internal
CA occlusion—unilateral (16 cases) and bilateral (3 cases), pseudo-aneurysm of the
cervical internal CA (1 case), severe stenosis or occlusion of the intracranial internal
CA from Moyamoya disease (3 cases), MCA stenosis (2 cases), cavernous internal CA
stenosis due to neoplasia (1 case), giant aneurysm in cavernous internal CA (2 cases),
vertebral–basilar insufficiency (3 cases), and giant aneurysm of the o basilar artery
(1 case). Immediate graft patency was ascertained in all the cases by observation,
as described. On follow-up, graft patency was confirmed in half of the cases by arterial
digital subtraction angiography in 10 cases, magnetic resonance angiography in 4 cases,
and CT angiography in 2 cases. The long-term graft patency rate based on those imaging
studies was 93.7%.
There was no surgical mortality. Three patients had PO complications (9.3%), including
one case of ischemia (3.1%). One patient had an acute subdural hematoma requiring
surgical drainage; late in the PO course, the same patient developed a pseudoaneurysm
at the site of the anastomosis, which was surgically treated. There was one case of
cerebrospinal fluid fistula with central nervous system infection, which responded
well to medical treatment. Fistula repair surgery was not necessary. One patient developed
mild crural paresis in the immediate PO period, which did not prevent ambulation.
No stroke or death was observed in the follow-up period.
Discussion
Since EC–IC bypass was proposed by Yasargil[1] in 1969, the reaction to this cerebral revascularization technique, also known as
low-flow bypass, has varied from heightened enthusiasm to total rejection.
In the 1970s, the EC–IC bypass procedure became mandatory in the training of residents
and was widely performed in neurosurgical services worldwide. Despite being a low-morbidity
procedure, the indications and results of EC–IC bypass were not well established.
The NIH funded an international, multicenter, randomized controlled trial to determine
whether cerebral revascularization by the EC–IC bypass technique would reduce the
risk of cerebrovascular events or death in patients with distal CA stenosis, CA occlusion,
or MCA stenosis.[2] The publication of that study results, in 1985, had a great impact on neurosurgical
practice, as it concluded that EC–IC bypass surgery offered no benefit over medical
treatment in the prevention of cerebrovascular events and death. Following that study,
EC–IC bypass procedures became an exception and were used in select cases and in few
centers of reference.
Nevertheless, several authors pointed to methodological flaws in that study.[5]
[6]
[7] The most common failure discussed was the analysis of the complications, which was
done on an intent-to-treat basis. Thus, 81 cases of stroke were counted in the group
of 663 surgical patients (12.2%). However, 16 of those patients had suffered a stroke
after randomization but before surgery. If only the cases of post-surgery strokes
were considered, stroke incidence rates would fall to 9.9% (65 cases of stroke in
652 operations).
The publication of the results of randomized studies on endarterectomy, another modality
of revascularization, was also used as criticism to the conclusions of the international
study and contributed to rekindle the interest in low-flow bypass surgery. The Asymptomatic
Carotid Atherosclerosis Study (ACAS),[8] North American Symptomatic Carotid Endarterectomy Trial (NASCET),[9] and European Carotid Surgery Trial (ECST)[10] are the most notable of those studies.
Indicated for moderate to severe cervical CA stenosis, even if asymptomatic, endarterectomy
proved to be more efficacious than the medical treatment alone. Similarly, cervical
CA angioplasty with stenting was shown to be efficacious for stroke prevention in
severe carotid stenosis.[11]
[12]
Carotid occlusion in patients with atherosclerosis is a risk factor for a stroke[13]: 27 to 38% of the patients with acute CA occlusion suffer a stroke, and the annual
risk ranges from 2 to 5.5%. The risk of death after a diagnosis of carotid occlusion
ranges from 30 to 40% in 5 years. In addition, the risk of endarterectomy or angioplasty
for treatment of carotid stenosis contralateral to the occlusion site increases significantly.
Because neither endarterectomy nor angioplasty is indicated for carotid occlusion,
bypass surgery began to be regarded as a potential therapeutic option.
To test the hypothesis that EC–IC bypass surgery would benefit patients with carotid
occlusion, the NIH funded the Carotid Occlusion Surgery Study (COSS).[3] This randomized study was conducted between 2002 and 2010, involving 49 centers
in the United States and Canada. All the cases of stroke and death within 30 PO days
were evaluated, as well as the incidence of ipsilateral stroke after 2-year randomization.
Despite the excellent graft patency rate and significant improvement in cerebral blood
flow as demonstrated by positron emission tomography (PET) scanning, the study data
did not demonstrate superiority of the surgical procedure compared with best medical
treatment.
Two-year rates for the primary end point were 21% in the surgical group and 22.7%
in the medical group. The incidence rate of ipsilateral stroke after 30 days was 14.3%
in the surgical group and 2% in the medical group.
In our series, CA occlusion ([Fig. 2]) was the principal indication for EC–IC bypass (19 cases, 59.3%). Because PET scanning
was not available, we used brain perfusion single-photon emission computed tomography
(SPECT) to confirm hypoperfusion in all cases. Only one patient suffered a stroke
in the 30-day PO period (3.1%). This patient had left-sided cervical CA occlusion
manifested as aphasia. During the immediate PO period, the patient developed crural
paresis. Magnetic resonance imaging (MRI) showed a small area of parietal ischemia.
Fig. 2 Superficial temporal artery (STA) and middle cerebral artery (MCA). Remark to occlusion
of internal cervical carotid (big arrow) and swallow of MCA by anastomosis (small
arrow).
The bypass surgery for atherosclerotic disease was the object of two large randomized
trials and failed to show a significant benefit. It is speculated that a subgroup
of patients with refractory ischemic symptoms could benefit from the bypass provided
that perioperative complication rates are low.[14]
[15] However, given the results of the trials, there is no established recommendation
for revascularization in atherosclerotic disease. Despite its limited indication for
atherosclerotic disease, revascularization should not be abandoned. First, because
there is a group of patients who do benefit from this surgical technique, whose indications
must be individualized. Second, because the EC–IC bypass can be of great utility in
other pathologic conditions.
The EC–IC bypass procedure may be a valid alternative in intracranial arterial stenosis.
The findings of the SAMMPRIS trial support that aggressive medical management should
be used rather than angioplasty in patients with intracranial arterial stenosis.[16] The occurrence of any stroke and major hemorrhage was higher in the percutaneous
angioplasty group than in the medical group. Therefore, one may consider EC–IC bypass
to treat intracranial arterial stenosis. In our series, we performed EC–IC bypass
surgery on two patients with severe symptomatic stenosis in the MCA segment with good
outcome.
Moyamoya disease is also an indication for EC–IC bypass. It causes major hemodynamic
alterations in cerebral circulation involving the CA supraclinoid segments. The abundant
network of minute collateral vessels surrounding the arterial occlusion, which names
the disease because of its appearance of smoke (“Moyamoya” means “a puff of smoke”),
is not sufficient to ensure cerebral blood flow. Revascularization has proved useful
in these cases.[17]
[18] In our series, Three adult patients with Moyamoya disease underwent revascularization.
They had bilateral occlusion of the intracranial internal CA with the typical angiographic
pattern of the disease.
The EC–IC bypass procedure can also be used for revascularization when the sacrifice
of a major blood vessel is necessary, as in the treatment of some giant or complex
intracranial aneurysms. Following that indication, we performed the bypass in two
cases of giant aneurysm in the cavernous internal CA as part of the strategy of cervical
internal CA occlusion to manage the aneurysm. The same rationale supported the indication
of bypass for posterior circulation in the case of a giant aneurysm in the middle
one-third of the basilar artery. We did a bypass of the occipital artery to the AICA
at the cerebellopontine angle. In a second stage, the basilar artery upstream of the
anastomosis was occluded using endovascular technique.
The literature data are insufficient to support an evaluation of the indication and
efficacy of revascularization in the posterior fossa. We indicated posterior fossa
revascularization due to vertebral–basilar insufficiency in three cases in our series.
We performed anastomosis of the occipital artery with the horizontal segment of the
extracranial vertebral artery ([Fig. 3]). This technique was inspired by a case report by Hadley et al, who used it in a
case of blunt trauma to the vertebral artery.[19]
Fig. 3 Anastomosis of occipital artery with extracranial horizontal segment of vertebral
artery (arrow). Remark to swallow of system vertebral basilar by anastomosis.
Because the chief indication for revascularization is to prevent cerebral ischemia,
most reports of PO complications focus mainly on ischemic events. In the first trial,
regardless of the methodology adopted, the rate of ischemic complications was high:
based on the intent-to-treat analysis, the stroke rate was 12.2%. When the cases of
stroke prior to surgery were disregarded, still the ischemic complication rate was
9.9%. This complication was fatal in four cases (0.6%).[2] The COSS study found 14.3% of ipsilateral strokes in the group of surgically treated
patients.[3]
In our series, one patient had a minor stroke (3.1%). However, the evaluation of this
low incidence rate should take into consideration the limitations of our work: (1)
a retrospective study, (2) EC–IC bypass was not indicated only for atherosclerotic
disease, and (3) no control group was included.
The occurrence of non ischemic complications should also deserve attention. Samson
and Boone reported 13.6% of non ischemic complications in 376 operations.[20] Schick et al reported a 6% incidence rate of subdural hematoma in their series of
47 cases.[21] In our series, two patients developed non ischemic complications (6.45%).
Conclusion
The EC–IC bypass is a procedure with low morbidity and mortality. The indication of
EC–IC bypass surgery for cerebral atherosclerotic disease should not be generalized.
Some patients could benefit from cerebral revascularization and should be evaluated
on an individual basis.
The EC–IC bypass can be indicated for cerebral revascularization in Moyamoya disease,
intracranial stenosis, and in the management of complex aneurysms. This procedure
can be an alternative in the treatment of vertebral–basilar insufficiency.
