Materials and Methods
Twenty-three consecutive patients who underwent STA-MCA bypass surgery during 2 years
in Fujita Health University, Banbuntane Hotokukai Hospital (January 2018 to January
2020). All the data were provided by the senior author. Patients were evaluated preoperatively
using computed tomography (CT) perfusion scan to establish a better analysis of cerebral
blood flow (CBF) for patients who were candidates for bypass revascularization surgery.
Intraoperative monitoring for bypass patency was done using Doppler ultrasound and
DIVA (dual-image video angiography). Postoperative assessment of bypass patency was
made with CT cerebral angiogram.
Surgical technique of superficial temporal artery-middle cerebral artery bypass
Illustrative case
A 40-year-old female presented to hospital with multiple transient ischemic attacks
(TIA) due to left MCA stenosis. The preoperative radiological study showed severe
left MCA stenosis. Single-photon emission CT (SPECT) showed reduced CBF in the left
MCA territory.
The patient was operated in the supine position with the head turned to the right
with a slight extension. STA was located using a Doppler probe. Left frontotemporal
curvilinear incision was done. We use handheld Doppler to identify STA donor vessels
during subcutaneous dissection. It avoids inadvertent injury to the donor vessel [[Figure 1]].
Figure 1: Intraoperative Doppler localization of Donor left superficial temporal artery from
the beginning of subcutaneous dissection
Donor STA is mobilized from the root, long enough to reach MCA recipient branches
without avulsion [[Figure 2]].
Figure 2: Left superficial temporal artery dissection from surrounding soft tissue
The temporal muscle was divided under the STA [[Figure 3]], dissected and retracted inferiorly to expose the frontotemporal area, and a frontotemporal
bone flap was removed.
Figure 3: (a) Retraction of left temporalis muscle for craniotomy (b) mobilization of superficial
temporal artery
After performing the craniotomy, the duratomy was done. Cortical branches of the Left
MCA exiting from the Sylvian fissure were identified [[Figure 4]]. Left cortical M4 branches were mobilized and their arachnoid coverings were coagulated
and cut to allow mobilization. The left STA artery was clamped distally and cut for
mobilization toward MCA cortical branches [[Figure 5]]. Before performing the anastomosis, cortical M4 MCA branches are visualized with
intraoperative video indocyanine green (ICG) for luminal patency [[Figure 6]] and [[Figure 7]].
Figure 4: Mobilization of left M4 cortical branches
Figure 5: Clamping followed by mobilization of left superficial temporalartery
Figure 6: Preparation of left M4 middle cerebral artery for anastomosis
Figure 7: Intraoperative indocyanine green showing blood flow in recipient left M4 cortical
branch before anastomosis
The left STA was prepared as a donor vessel, an appropriate length was mobilized after
putting a temporary clip at the root of the STA and cut. The soft tissue was removed
from the temporal artery on its last 1 cm. The extremity was prepared as a fish mouth
and marked with methylene blue (to facilitate its identification in the operative
field). Heparin was injected into the STA. Gel foam was used in both working areas
(STA and MCA preparation). The recipient MCA cortical vessel was trapped with two
temporary clips, and the arteriotomy was marked with methylene blue [[Figure 8]].
Figure 8: Fish mouth arteriotomy of superficial temporal artery and application of ethylene
blue marker
Left M4 MCA cortical vessel arteriotomy was done, and edges were stained with blue
ink [[Figure 9]]. We used 10-0 sutures; first, we approximated donor and recipient vessels with
2 stitches. Then, an anterior wall [[Figure 10]] was closed with interrupted sutures. Then, the posterior wall was approximated
with interrupted sutures [[Figure 11]].
Figure 9: Arteriotomy of left M4 middle cerebral artery and application of ethylene blue marker
Figure 10: Closure of anterior wall anastomosis
Figure 11: Closure of the dorsal wall of the anastomosis
Then we proceed to the removal of temporary clips one by one:First, the proximal temporary
clip on the MCA was removed; second, we removed the distal clip-on MCA; finally, the
temporary clip on the STA was released allowing the verification of the patency of
the anastomosis. We confirmed the luminal patency of anastomosis with Doppler ultrasound
and DIVA. DIVA showed a good filling of blood through the anastomosis [[Figure 12]]. We verified the flow with a Doppler probe too [[Figure 13]].
Figure 12: DIVA showing good flow across the anastomosis
Figure 13: Doppler confirming luminal patency across superficial temporal artery middle cerebral
artery bypass
The dural closure is also an important step; usually, we use the temporal muscle to
ensure a good closure allowing a safe entrance of the STA without any compression.
Results
From 2018 to 2020, we performed 23 STA-MCA bypass surgeries. The mean age was 52 years
with the youngest at 16 years and eldest at 84 years. There were 11 male and 12 female
patients.
Out of 23 patients, 10 patients had associated hypertension and 4 had diabetes mellitus.
In 16 patients, steno-occlusion was the indication for bypass. The goal of the bypass
was flow augmentation in these 16 patients. IC Carotid artery stenosis was seen in
7 patients and MCA stenosis was seen in 9 patients. Three patients had Moyamoya disease.
Low flow STA-MCA bypass was done in these 16 cases.
The most common symptom was frequent TIA presenting as hand numbness. Hemiparesis
was noted in 6 patients. The visual loss (50%) was noted in one patient. Headache
was noted in one patient. Handgrip weakness was seen in one patient. Facial weakness
was seen in one patient.
Nine patients were asymptomatic with incidentally detected severe IC internal carotid
artery (ICA) stenosis or MCA stenosis in magnetic resonance imaging (MRI) angiogram.
Three patients had a giant aneurysm of ICA (cavernous segment), and one had recurrent
anterior cerebral artery aneurysm (undergone coiling and clipping earlier).
SPECT analysis for baseline CBF was done in 6 patients. In 5 patients, baseline CBF
was reduced (Type 1 cerebral hemodynamic impairment).
In three patients, bypass was done to achieve the flow replacement. Two patients had
giant internal carotid aneurysms involving the cavernous segment. One patient had
undergone multiple clipping and endovascular procedures for giant A1 aneurysm.
One case of the bypass was done on an emergency basis. There was coil migration while
filling the left ICA (cavernous) aneurysm. Coil got migrated to distal MCA. An emergency
STA-MCA bypass was performed. The patient recovered without any neurological deficits.
A high flow bypass was done in all three cases explained above. Radial interposition
graft waft was used in the first two cases, and saphenous venous graft was used in
the latter case.
We used intraoperative Doppler before, during and after anastomosis in all patients
to assess luminal patency.
Method of prediction of postoperative cerebral hyperperfusion with use of flow 8oo
intraoperative indocyanine green
Four regions of interest are marked in the frontal and temporal lobe. CBF at the above
regions is measured with intraoperative ICG before anastomosis and after anastomosis.
An increase in CBF by 2.5 times is a predictor of cerebral hyper perfusion.
There are some limitations with intraoperative ICG used for the assessment of hyperperfusion.
-
ICG injection speed, dose, and systemic hemodynamic conditions might influence ICG
fluorescence configuration
-
Change in cardiac output and blood pressure would also affect maximal fluorescence
intensity.
We used intraoperative video ICG with flow 800 to assess the luminal patency of anastomosis
and compared with preanastomotic ICG angiogram. Intraoperative video ICG detected
decreased flow through the anastomotic site in 2 patients. It helped us to revise
anastomosis in the same setting, thus, decreasing perioperative morbidity and mortality.
We used to flow 800 to assess hypoperfusion and hyperperfusion after anastomosis.
None of our patients had hypoperfusion or hyperperfusion after anastomosis.
Discussion
Indication
There are many trials conducted to assess the benefit of the bypass in cerebrovascular
steno occlusive diseases. We will discuss the results of these trials and their limitations
International study on extracranial-intracranial bypass
Published in 1985, this prospective randomized trial investigated whether EC-IC arterial
bypass, in addition to best medical therapy, was superior to best medical therapy
alone in patients with ischemic cerebrovascular disease including EC ICA occlusion.[[1]] A total of 1377 patients were enrolled. The mean follow-up period of the study
was 55.8 months. The overall risk of TIA/stroke in the medical group was 29% and bypass
group was 31%. The incidence of perioperative stroke with surgery was12.2% and overall
mortality was 1.1%
There was no significant difference in outcome between the two groups. Hence, the
number of bypasses performed reduced drastically after this trial.
The main criticism of this trial was cerebral hemodynamic impairment was not analyzed
for case selection and randomization. Hence, carotid occlusion study (COSS) was performed
to assess cerebral hemodynamic impairment in bypass surgeries.
Cerebral hemodynamic impairment
To further understand the evolution of bypass surgery, the discussion about cerebral
hemodynamic impairment is necessary. It is divided into three stages.
Cerebral perfusion pressure is reduced in case of occlusion of ICA or MCA. Cerebral
autoregulation maintains the CBF by compensatory vasodilatation. This is assessed
by calculating baseline CBF and blood flow after acetazolamide challenge (using perfusion
CT, MRI, positron emission tomography [PET] or SPECT). This is termed as stage 1 hemodynamic
failure.
In Stage 2 failure, cerebral vasodilatation is insufficient to maintain CBF, and there
is a compensatory increase in oxygen extraction from arteries (evidenced by increased
oxygen deficit between artery and veins). This is called misery perfusion.
In Stage 3, there is complete failure to maintain adequate CBF even with vasodilatation
and increased oxygen extraction. The risk of subsequent TIA and stroke are highest
in Stage 2 and 3 failures. The subsequent trials were based on cerebral hemodynamic
failure as a deciding factor in the selection of cases for bypass.
ST Louis carotid occlusion study
It's a prospective blinded study evaluating raised oxygen extraction factor (OEF)
as a predictor of subsequent stroke. This study showed a relative risk of overall
stroke in patients with raised OEF (OEF >6.0).
The STLCOS conclusively demonstrated that symptomatic patients with EC ICA occlusion
were at increased risk of subsequent ischemic stroke. Importantly, previous studies
had established that EC-IC bypass surgery could improve hemispheric OEF ratios in
Stage II patients back toward normal levels.[[2]],[[3]] This study was followed by COSS.
Carotid occlusion study
COSS was a prospective, parallel-group, 1:1 randomized, open-label, blinded-adjudication
treatment trial designed to test the hypothesis that STA-MCA cortical branch anastomosis–added
to best medical therapy–would reduce the 2-year risk of subsequent ipsilateral ischemic
stroke by 40% in patients with carotid occlusion and recently symptomatic cerebral
ischemia.
Total 195 patients with angiographic-proven ICA occlusion causing an ischemic stroke
or TIA within 120 days and hemodynamic cerebral ischemia (indicated by an increased
OEF ratio on PET) were randomized to best medical therapy or best medical therapy
plus STA-MCA bypass. One hundred ninety-five patients were randomized. Ninety-seven
patients were randomized to the surgical group and 98 to the medical group.
The study was halted prematurely due to futility. In the intention-to-treat analysis,
the 2-year rates for ipsilateral stroke were 21% for the surgical group and 22.7%
for the medical group (P = 0.78). Perioperative (within 30 days of surgery) ipsilateral
stroke rates were 14.4% in the surgical group and 2.0% in the medical group, a significant
difference of 12.4% (95% confidence interval 4.9%–19.9%). The study concluded that
EC-IC bypass surgery in this patient population was not of clinical benefit.
This report was followed by a post hoc qualitative analysis of the mechanisms of perioperative
ischemic stroke in the COSS surgical cohort. In this investigation, Reynolds et al.[[4]] retrospectively identified patients from the COSS with an ipsilateral perioperative
ischemic stroke and categorized stroke mechanisms as bypass graft related (ischemic
infarct in the territory of the recipient artery, likely related to the technical
performance of the anastomosis) or nonbypass graft related (ischemic infarct attributable
to embolism, hypoperfusion, or other cause). The vast majority of perioperative ischemic
strokes (86% or 12 of 14) were found to be unrelated to the performance of bypass
grafting, while the minority (21.4% or 3 of 14) were found to be related to the performance
of bypass grafting.[[4]] One patient was considered to have dual stroke mechanisms. The authors concluded
that the majority of ischemic strokes were not attributable to technical problems
with the anastomosis but were most likely due to the hemodynamic fragility of the
patient population involved.
Thus, COSS has narrowed the indications for EC-IC bypass in the setting of ischemic
cerebrovascular disease.[[5]]
Hence, the relative indication for bypass in cerebral ischemia due to internal carotid
or MCA occlusion are:[[5]]
-
Recurrent TIA or stroke refractory to medical management
-
With impaired cerebral hemodynamic (Stage 1 or 2 failure) suggested by poor response
to acetazolamide challenge in SPECT or increased OEF in PET CT scan.
Types of bypass surgeries
Depending on flow rate across anastomosis, bypass can be classified as high flow or
low flow:[[6]],[[7]]
-
Standard flow-Flow rate of 20–70 ml/min
-
Intermediate flow-flow rate of 60–100 ml/min)
-
High flow-flow rate of 100–200 ml/min (uses a radial artery or saphenous vein interposition
graft between ECA and ICA).
Goals of extracranial-intracranial bypass surgeries
The goals of bypass either flow replacement or augmentation
-
Bypass for flow augmentation: It is performed for ischemic cerebrovascular disease
due to occlusive disease of ICA above level of c2 cervical spine and MCA disease.
The aim of surgery is to augment the blood flow to the brain from the external carotid
artery
-
Bypass for flow replacement: Here, bypass is performed for giant IC aneurysm, which
cannot be treated with clipping or by endovascular measures. In such instance, aneurysms
are trapped proximally and distally and EC-IC bypasses are performed.[[8]]
Thanapal et al.[[9]] mentioned the risk factors for subsequent stroke or TIA. These risk factors for
stroke include severe ICA or MCA stenosis (>70% stenosis), female gender, National
Institutes of Health Stroke Scale score >1, concurrent diabetes, borderline body mass
index values, hyperlipidemia, white ethnicity, and the presence of hemodynamic stenosis
increases the risk for stroke.
Since the beginning of bypass surgeries by Dr. Yasargil, the perioperative management
and intraoperative monitoring have evolved significantly. Here, the author will discuss
the use of transcranial Doppler and intraoperative ICG (ICG angiogram) to assess the
patency of anastomosis.
The introduction of intraoperative contact Doppler ultrasonography and flowmetry into
clinical practice made it possible to quantify the local blood circulation in the
territory of revascularization immediately after creating the bypass.
Morton et al.[[10]] explained in his article about intraoperative use of Doppler ultrasonography in
assessing luminal patency of anastomosis in the STA MCA bypass.
Balamurugan, et al.[[11]] reported intraoperative use of ICG-video angiogram (VA) before and after anastomosis.
Even though microvascular Doppler is being used for a long time in cerebrovascular
surgery, it has its own limitations. Although intraoperative DSA (digital subtraction
Angiogram) is the gold standard technique, it needs additional professional experience
and the table position needs to be changed. Moreover, it is time-consuming, expensive,
and has radiation exposure also in the operating suite. Hence, ICG VA is replacing
the above in many neurosurgical centers, because it is a simple, rapid, and reliable
method, and we can get real-time images with good quality and high spatial resolution,
and also, it is not an expensive one.
In EC-IC bypass, ICG VA gives exact information about the anastomotic site, so that
early bypass graft failure can be avoided.
Background Intraoperative ICG video angiography (ICG-VA) shows cerebral blood vessels
as white on a black background. However, other structures cannot be observed during
ICG-VA. Sato et al.[[12]] have developed a new, high-resolution intraoperative imaging system [DIVA] to simultaneously
visualize both light and near-infrared fluorescence images from ICG-VA, allowing observation
of blood vessels as well as other structures.
Feletti et al.[[13]] analyzed the role of ICG VA and DIVA in cerebrovascular procedures. They opined
that ICG VA provided better visual contrast between blood vessels (as white) and surrounding
structures (as black). However, DIVA makes it easier to understand anatomical relations
between IC structures. DIVA also gives a better vision of the depth of the field.
We revised anastomosis in two cases based on findings of DIVA (Dual Imaging Video
Angiogram) and Doppler intraoperatively. Both patients recovered without perioperative
morbidity or stroke. Hence, we recommend the use of intraoperative Doppler and DIVA
are must in bypass procedure.
The reported side effects are very low with this DIVA technique when compared to other
invasive methods. To avoid false positive findings, repeated injections of ICG within
short intervals should not be given.
Even though there are certain limitations, ICG VA is widely being used in many centers,
because it is simple, safe, and we can get faster results with high-resolution real-time
images. The use of intraoperative Doppler and DIVA allowed graft patency of 96%.
Thines et al.[[14]] discussed the role of perfect dural closure to prevent wound complications in the
perioperative period.
It is imperative to monitor patients after bypass surgery not only for patency of
anastomosis but also to predict and treat hypoperfusion or hyperperfusion. Among the
various hemodynamic modalities, MRI, CT perfusion, and transcranial Doppler sonography
are the most commonly used modalities. Post-stroke hypoperfusion is associated with
infarct expansion, while hyperperfusion, which once was considered the hallmark of
successful recanalization, is associated with hemorrhagic transformation. Either the
hypo- or the hyperperfusion may result in poor clinical outcomes. Individual blood
pressure target based on cerebral hemodynamic evaluation was crucial to improve the
prognosis.[[15]]
After revascularization surgery, a rapid and significant increase in ipsilateral CBF
beyond the metabolic demand of the brain tissue may occur. Excessive blood flow directed
into chronically ischemic brain through a bypass may induce a “luxury perfusion syndrome”
resulting in neurological deterioration.[[16]] Patients with poorer cerebrovascular reactivity are known to have a potentially
higher risk for hyperperfusion syndrome.[[17]]
Several methods have been proposed for the detection of cerebral hyper perfusion during
operation or early after surgery.[[18]] Gesang et al.[[19]] indicated that the laser Doppler flowmeter is useful for postoperative real-time
monitoring during the high-risk period. Intraoperative measurements such as thermography,
infrared brain surface monitoring, and ICG fluorescence angiography predict post anastomosis
cortical hemodynamic.[[18]]
