Introduction
The first vascular anastomosis in history was described by Eck in 1877 with his operation
on dogs to make a side-to-side anastomosis between the hepatic vein and the inferior
vena cava.[1]
[2]
[3] French surgeon Alexis Carrel published the first arterial end-to-end anastomosis
in 1902[1]
[4] and received the Nobel Prize in 1912. Kredel[5] attempted encephalomyosynangiosis in humans in 1942, but it was later abandoned
due to an increased prevalence of postoperative seizures. Then, in 1949, Beck et al.[6] published their revascularization technique of a carotidjugular fistula. Jacobson
et al. reported the first human microneurosurgical procedure in 1962: an middle cerebral
artery [MCA] endarterectomy.[1]
[2]
[7]
[8]
[9]
Pool et al.,[1]
[10]
[11] in 1961, first adventured into cerebral revascularization with a synthetic material
using a plastic tube to make a superficial temporal artery (STA) to anterior cerebral
artery bypass, but an angiogram showed that the tube was thrombosed, although the
patient recovered and survived. Woringer et al.[12] did the first extracranial to intracranial (EC-IC) bypass of the common carotid
artery (CCA) – intracranial (IC) internal carotid artery (ICA) using a saphenous vein
(SV) graft in 1963, but the patient died, although the graft was patent on autopsy.[1]
[2]
The first successful EC-IC bypass was performed by Prof. Yaşargil in 1967 in a patient
with occluded ICA and, since then, it has become an essential way for managing patients
with hemodynamic cerebral ischemia, complex intracranial aneurysms or skull base neoplasms.[13]
[14]
[15] The cases with cerebral hemodynamic ischemia have an annual stroke rate of 25%,
which increases by 2% per year.[13] They can have a fatal ischemic stroke. Moyamoya disease is also included in this
category.[13]
[16]
Yaşargil also did STA-middle cerebral artery (MCA) bypass for moyamoya disease in
1972. In 1971, Lougheed made the first EC-IC bypass using an SV graft. Ausman performed
an EC-IC bypass using a radial artery (RA) graft in 1978. In the 1970s, Sundt et al.[17] and others performed posterior circulation revascularization for the management
of steno-occlusive disease, vertebrobasilar insufficiency, and unclippable complex
aneurysms.[1]
In ischemic stroke, after the failure of an EC-IC bypass trial in 1985,[1]
[2] neurovascular surgeons were looking for cases in which an EC- IC bypass would help
the patients in neurological recovery and prevent future ischemic stroke. Moreover,
EC-IC bypass is also used for the treatment of moyamoya disease, complex aneurysm,
arterial dissection, and complex skullbase tumor. Here, we report our initial experiences
of the first 100 bypasses as experiences in ‘learning curve’ covering the preparation
and training of the surgeon, getting cases, patient selection, imaging, operative
skills and microtechniques, complications, follow-up, and outcome. Lessons learned
from the ‘learning curve experiences’ can be very useful for young vascular neurosurgeons
who are going to start EC-IC bypass or have already started it and are in the learning
curve.
Representative Cases
Fig. 1 (a): (A, B & C) CTA of the brain showing severe stenosis of the left MCA. (E, F & G) Cerebral DSA showing left MCA stenosis with delayed filling of the MCA territory.
(b) (A) Preoperative picture of STA-MCA bypass. (B) CTA of the brain on the 1st POD showing left STA-MCA bypass. (C & D) CTA of the brain 6 months after the operation showing patent STA-MCA bypass.
A 27-year-old male young doctor presented with right sided hemiplegia, aphasia, and
visual field defect. His hemiplegia improved from initial Medical Research Council
[MRC] grade 0/5 to 3 +/5 in the right lower limb and 2/5 in the right upper limb 1
day after admission. His perception and comprehension of speech were normal, but he
had motor aphasia and right homonymous hemianopia. Computed tomography (CT) scan and
magnetic resonance imaging (MRI) of the head showed left-sided patchy infarcts and
ischemic zones in left parieto-temporo-occipital zones. Digital subtraction angiography
(DSA) and CT angiography (CTA) of the brain showed left M1 stenosis with scarcity
of left MCA vessel ([Figure 1a] & [1b] [B, C and D). Perfusion weighted (PW) images showed perfusion mismatch.
On an urgent basis, the patient underwent left-sided STA-MCA bypass.
Operation
Under general anesthesia (GA), the patient was placed on the supine position with
the head turned > 60°. At this point, we used digital palpation technique and a handheld
Doppler probe to map out the course of both the frontal and parietal branches of the
STA.
The incision was started at the level of the zygoma and extended up to the near midline
behind the hairline. Both branches were procured up to the superior temporal line
very carefully (to avoid thermal damage or avulsion injury). Papaverine solution and
plain local anesthetic agent (2% lidocaine) was used to irrigate the STA for vasospasm
prevention. A mini pterional craniotomy was performed very carefully (so as to not
damage the procured STA). After durotomy, a small posterior Sylvian fissure split
was done to find out a suitable M3 as a recipient vessel for the bypass. Among the
frontal and parietal branches, the suitable and larger frontal branch was used to
make a STA-MCA anastomosis. After the bypass ([Figure 1B][A]), patency was checked clinically and with microdoppler. The dura was loosely
closed around the STA (not watertight). Along the temporal margin of the bone flap,
a portion was removed so that the STA would not be kinked or compressed by the bone.
Mini plates and screws were used to fix the bone flap. The rest of the wound was closed
accordingly without drain.
Postoperative Course
The patient recovered well from anesthesia. In the postoperative days, the patient
recovered quickly from hemiparesis and aphasia. By the end of the 7th postoperative day (POD), the patient became ambulant, but his visual field remained
as preoperatively. By the end of 4 weeks after the operation, he returned to his professional
work and muscle power on right side of the body was improved (MRC grade 4 +/5). A
postoperative CT scan showed no hematoma or new infarct. The CTA showed a patent STA-MCA
bypass on the left side.
Case 2 - High Flow Bypass (CCA-RA-MCA bypass) ([Figure 2a-2f])
Fig. 2 (a): (A, B, C & D) CTA of the brain showing a large fusiform aneurysm involving the left supraclinoidal
ICA. (b): (A & B) preoperative pictures of insurance STA-MCA bypass before performance of EC-IC high
flow bypass. (c): (A & B) preoperative pictures; sylvian dissection, identification and preparation of the
temporal M2 as recipient artery for anastomosis with radial artery (RA) graft. RA,
radial artery; M2 (MCA). (d): A & B-preoperative pictures of RA and M2 anastomosis. (e):
A & B preoperative pictures of RA and CCA anastomosis. (f): Postoperative CTA of the brain and neck vessel on the 2nd POD showing CCA-RA-M2 high flow EC-IC bypass and nonvisualization of the left supraclinoidal
ICA aneurysm.
A 55-year-old right-handed man presented with clinical features of recurrent subarachnoid
hemorrhage (SAH), that is, sudden severe headache and vomiting. His Hunt and Hess
grade was G-1. He was a smoker but nondiabetic and nonhypertensive. A CT scan showed
SAH in the carotid, the basal and both Sylvian fissures. A computed tomography angiography
of the brain showed a left-sided supraclinoidal large fusiform ICA aneurysm ([Figure 2a]). He was counselled for urgent operation. We decided to do a left sided CCA-RA-MCA
(M2) high flow bypass with occlusion of the left ICA at the neck. The Allen test was
done bilaterally and it showed that the ulnar arterial flow was adequate for hand
circulation in the absence of the radial artery.
Under general anesthesia with endotracheal intubation, the patient was placed in the
supine position. His head was fixed with a 3-pin head holder with neck extension and
head turning to the opposite (right) side (30°). The head end of the table was elevated (20°). Eyes, ears, pressure points, and nerve areas were protected. The left upper limb
was placed on a side ‘limb rest’ with extended elbow, 30° abducted from the trunk in supine for radial artery procurement. After preparation,
the front of the left forearm, the left side of the neck, and the left pterional areas
were draped properly.
With a longitudinal incision, the radial artery was harvested from the brachial bifurcation
at the elbow to the wrist (20 cm). The artery was distended with intraluminal injection
of heparin and papaverine mixed with normal saline. Then, the artery was kept in heparin
and papaverine mixed with normal saline. The forearm wound was closed with a drain.
A curved incision on the left side of the neck was made from the tip of the mastoid
process and extended downwards and medially 2 cm posterior to the angle of the mandible
to the midline. After cutting the platysma and investing deep fascia the sternocleidomastoid
muscle was retracted laterally. With further dissection of the posterior belly of
the digastric muscle, the hypoglossal nerve, the internal jugular vein, the common
carotid, the internal carotid, and the external carotid artery with its branches were
identified.
A left-sided precoronal posthairline curvilinear incision was made and the superficial
temporal artery (STA) with its parietal branch was procured and prepared for STA-MCA
protective bypass as donor artery. A temporally extended pterional craniotomy was
performed. The temporal bone was removed down to the middle fossa floor. In the cervical
wound, a blunt index finger dissection was made in between the digastric muscle and
the hypoglossal nerve upward and superiorly to the styloid process, and then the finger
dissection was continued upward, medially, and anteriorly to the lateral pterygoid
plate. A curved medium-sized artery forceps was passed from the middle fossa floor
to the fingertip, and, with finger guidance, the arterial tip was brought out into
the cervical wound, and then a 26Fr thoracostomy tube was passed from the cervical
wound to the middle fossa floor. The radial artery (RA) graft was passed from the
middle fossa floor to the cervical wound through the tube. With stabilization of both
ends of the RA graft, the thoracostomy tube was removed. The RA graft was made twist-free
by injecting heparinized solution into the lumen.
After durotomy, a STA–MCA (Temporal M4) ‘insurance bypass’ was done with 10/0 nylon
and checked for patency and function with micro Doppler ([Figure 2b]). After Sylvian dissection, the temporal M2 was identified and prepared for bypass
([Figure 2c]). The cranial end of the RA graft was also prepared for bypass, and the RA graft
and temporal M2 bypass was made ([Figure 2d]) after systemic heparinization with 3,000 units of heparin. The patency of anastomosis
was checked by retrograde flow of blood through the caudal end of the RA graft in
the cervical wound.
With the control of the common carotid artery (CCA), an anastomosis was made between
the caudal end of the RA graft and the CCA ([Figure 2e]). The patency and flow through the anastomoses and RA graft were checked with micro
Doppler. The left ICA was identified as well as dissected to ligate it at its origin
with 1-0 silk. The cervical wound and the craniotomy wound were closed with drains.
Postoperative Course
Postoperatively, the patient was on tab. Aspirin (75 mg daily). A CT scan on the 1st POD showed no infarct or any gross hematoma. A CT angiogram on the 2nd POD showed left external carotid artery (ECA)-radial artery graft (RAG)-M2 bypass
with regression of the ICA fusiform aneurysm, but the ICA was visualized completely
up to the ligation point at the neck. The patient made an uneventful recovery and
was discharged on the 8th POD. Thirteen months after the operation, he returned with clinical features of SAH.
A CTA showed a left ICA bifurcation aneurysm that had ruptured. But the bypass was
patent and the ICA was again visualized up to its ligation at neck ([Figure 2f]). We decided to reoperate the patient, but he did not agree with any kind of further
intervention. After the last SAH, he is under regular follow-up for the last 7 months,
without further bleeding.
Results
Dreaming Through: Brain Thought to Hand Skill ([Figure 3])
Fig. 3 Practices of microvascular anastomosis before clinical application. (A & B) Radial
artery graft anastomosis with M2 in Sylvian fissure of fresh cadaveric brain. (C)
Microvascular anastomosis practice on formalinized dry brain. (D) Microvascular anastomosis
practice on live hen.
When the main author was a 3rd year MBBS student, he became interested in neurosurgery after watching a video of
the removal of an intracranial meningioma in the college library (the operation was
done by late professor Rashid Uddin Ahmed). At that time, he was firmly motivated
to be a neurosurgeon. During his intern period, when he was placed in the neurosurgery
department, he presented on surgical management of intracranial hemorrhages on a clinical
meeting and, at that time, he first knew about the EC-IC bypass for the management
of various intracranial vascular lesions. Brain bypass!!! Is it really possible, who
used to do it? Is there anyone in Bangladesh who practices brain bypass? The answer
was no.
In 2001, in a neurosurgical meeting, a Japanese neurosurgeon showed a very brief video
on petrous to supraclinoidal ICA bypass. In the World Federation of Neurosurgical
Societies (WFNS) meeting in 2007 in Nagoya, Japan, a few lectures on vascular surgery
really inspired us on focusing on EC-IC bypass. We started to practice anastomosis
on fresh cadaveric brains [radial artery-MCA (M2)] in the forensic department, which
was very poorly equipped.
During a fellowship (2009) in the department of neurosurgery, KEM Hospital, Mumbai,
India, under professor Atul Goel, the main author took the opportunity to practice
microvascular anastomosis on formalinized brain surfaces in his microneurosurgery
lab under operating microscope. There, the main author practiced more than 50 times.
Some Italian fellow (who was also visiting at the same time) told the main author
to practice it on live rats or Guinea pigs. But that was not possible there. Then,
we practiced on live hen and rats several times in the microvascular lab of the department
of plastic surgery, Dhaka Medical College and Hospital, Dhaka ([Figure 3]).
Getting the Clinical Cases
After achieving adequate motor skills and background knowledge, we were looking for
cases that were appropriately indicated for EC-IC bypass, but we were not getting
any cases. Finally, we got a case of M1 giant aneurysm. We decided to do an EC-IC
bypass in this case, but when the relatives of the patient heard that it would be
our first case and no one had performed this operation before in this country, they
left the hospital to go outside the country. In this way, we failed to operate on
our first case for another 4 or 5 cases for which bypass was indicated. Ultimately,
we could convince our first case to undergo EC-IC bypass, a 14-year-old girl with
M2-M3 dissection.
It took one and a half year more to get the second case. After starting bypass, we
did only four cases in first 3 years and 7 cases in the next 2 years. Then, we got
cases more frequently.
Preoperative Assessment of the Patients
In ischemia
Patients in this case series with transient ischemic attack (TIA)/stroke/recurrent
stroke were evaluated clinically for history of TIA or recurrent/hemodynamic TIA (in
rest or during work) or progressive hemiparesis/aphasia/visual disturbances or sudden
hemiplegia/hemiparesis/aphasia with subsequent significant recovery (in days to in
a week). Permanent hemiplegia cases were not considered for EC-IC bypass. Then the
cases were evaluated radiologically for ischemia with or without infarcts and possible
revascularization by EC-IC bypass. Computed tomography scan of the brain was done
to exclude hemorrhage and other pathologies, such as tumors. Magnetic resonance imaging
of the brain was done in ischemic protocol (all images including diffusion weighted
[DW], afferent diffusion coefficient [ADC], PW, DTI and magnetic resonance angiography
[MRA] and MRV, including neck vessels) to see cerebral ischemic zones (DWand PW mismatch),
the corticospinal tract and other major tracts and intracranial or extracranial arterial
stenosis. To see the arterial pathology, dynamic CTA was also done in all cases. DSA
was done in 36 cases. When clinical features, cerebral ischemia on MRI and arterial
stenosis/occlusion on angiogram were concordant with each other, only then cerebral
revascularization by EC-IC bypass was done.
In other Indications
-
Moyamoya disease
-
As replacement: Intracranial giant fusiform ICA aneurysm or caroticocavernous fistula
(CCF) where ICA ligation at neck and EC-IC bypass was planned.
-
Protective bypass in skullbase tumor where ICA was encased by tumor and the chance
of injury or occlusion of ICA or ICA had to be removed with the tumor.
-
Protective bypass in giant MCA or ICA aneurysm where the trunk of the MCA or of the
ICA occlusion/compromise was a possibility.
-
Protective bypass in aneurysm with proximal stenosis.
-
Insurance bypass during high flow EC-EC bypass.
-
Treatment of CCF.
-
Arterial dissection.
Preoperative Patient Preparation
Counselling and other preoperative preparations were as usual except in cerebral ischemic
patients, in whom preoperative antiplatelet drugs were continued. In these cases,
platelet concentrates were made available preoperatively, but were not required in
any case.
Preoperative Assessment of Donor Artery
Preoperatively, the STA was assessed with digital palpation and Doppler in all cases
for its presence and rough estimation of caliber and flow. Preoperatively, the STA
was also assessed with angiogram (external carotid angiogram: DSA, CTA and MRA).
The Allen test was performed in cases where the RA was planned to procure as conduit
for high flow EC-IC bypass.
Procurement of Donor Artery; STA/RA
In initial cases, we did Donor arterty procurement without microscope, but later we
found that it is more comfortable with a microscope. Now, we routinely use a microscope
in the procurement of the donor vessel. We procure the STA and its frontal and parietal
branches up to the superior temporal line (length between 7 and 9 cm) ([Figure 4]). Initially, we used 2% plain lignocaine instillation on the STA to avoid vasospasm,
but in the later part of our experiences, we used papaverine solution along with lignocaine.
After application of a temporary clip on the STA, we routinely irrigated its lumen
with heparin solution several times.
Fig. 4 Preoperative picture of procurement of the right STA and its branches.
In two cases STA length was short up to suitable recipient artery on temporal surface
due to less available length of STA and also due to falling of brain in deep as a
result of cerebro spinal fluid (CSF) drainage. Extra dissection at the root of the
zygoma, flushing of the temporal bone and assistant ‘holding of donor artery’ near
the recipient artery helped to make anastomosis with some difficulty.
We procured both branches of the STA and the relatively larger branch was used as
donor artery where the other branch was ligated. Where needed, both branches were
used as donors in double barrel bypass. In moyamoya disease, we used the frontal branch
of the STA for direct STA-MCA bypass, where the parietal branch was used for indirect
revascularization (as in EDAS) and the distal end was kept in continuity with the
scalp.
Radial artery (RA) Procurement (in High Flow Bypass)
In all cases of high flow bypasses, the left RA was procured after performing the
Allen test with a radially placed longitudinal incision from wrist to elbow (20 to
22 cm). We used papaverine solution along with lignocaine solution on the artery during
procurement. After procurement, the RA graft was distended with heparin and papaverine
solution and then it was suspended in heparin and papaverine mixed solution.
Craniotomy
In most of the cases pterional craniotomy was used for EC-IC bypass. In two cases
of moyamoya disease, a suitable recipient artery was found near the bony margin and
was prepared for anastomosis, but there were a lot of difficulties (for example, in
instrumental movements during stitching) faced by the surgeons due to the bony margin.
In the later part of our experiences, when such situations occurred, we cut more bone
so that the bony margin did not interfere during instrumental movements
In high flow bypasses, pterional craniotomy was extended down until the root of the
pterygoid by removing bone with a rongeur or a drill, so that the RA graft could be
brought to the middle fossa through the infratemporal fossa from the cervical wound.
Recipient Selection
In most of the STA-MCA bypasses, the temporal M4 or M3 were used as recipient arteries,
which were easy to find and easy to prepare. Finding a suitable recipient artery in
moyamoya disease, especially in children, was very challenging. In some cases, deep
Sylvian dissection was needed to get a suitable artery. In children, the recipient
artery was very thin and fragile, which made anastomosis more difficult. With patience
and skill, anastomosis was successfully done in all cases (even in a 4-year-old boy)
([Figure 5]). In all cases, we had to make the anastomosis with 10/0 nylon with cutting body
needle, since there was no alternative suture. The unavailability of appropriate/alternative
suture material made anastomosis more complex and difficult.
Fig. 5 (A) preoperative MRA of the brain showing bilateral Moyamoya disease. (B & C) Preoperative
picture of direct STA-MCA bypass. (D) Postoperative CTA on the 1st POD showing patent STA-MCA anastomosis with increased vascularity.
In high flow bypasses, we did insurance bypass by STA-MCA bypass at first. Then, the
temporal M2 was dissected out for quite a distance up to its cortical branches with
deep Sylvian dissection. Then deep to the artery triangular background paper (prepared
from surgice a package covering) was passed. Both end of background paper was tied
with suture to bring the M2 superficially; so that anastomosis became easier. Spongostan
was put deep to the background to prevent blood collection in Sylvian fissure from
anastomotic leak after release of temporary clips.
The M3/M4 branches of the upper trunk of the MCA were used in 9 cases of double barrel
bypasses.
Why the temporal trunk of the MCA and its branches were preferable than the frontoparietal
trunk and its branches as recipient artery?
-
The upper trunk supplies more eloquent and important areas (Broca area, primary motor,
and primary sensory areas) than the temporal trunk (primary auditory areas and lower
part of the Wernicke area on the left side only, which has overlapping supply from
the upper trunk).
-
Occlusion of the upper M2 has more chances of infarction compared with the lower trunk.
-
Infarction of lower trunk areas produce less severe deficits than upper trunk areas.
-
In some cases, the upper trunk supplies the corona radiata.
-
Use of the lower trunk and its branches as recipient arteries is technically easier.
Ischemic Time
From the beginning, we were afraid of infarction of the brain during performance of
anastomosis in clinical cases. When we talked to experts (including Prof. Atul Goel)
regarding ischemic time, all of them said ischemic time is not a major issue in bypass.
But it was our major concern even when we were practicing anastomosis on hen in < 20 minutes.
Realization regarding Ischemic Time
In the first 100 clinical bypasses, we faced no infarction related to temporary occlusion
of brain arteries. In the earlier cases, we did not take any protecting measures for
the brain parenchyma against ischemia or any talk with anesthesiologist regarding
ischemic time. Initially, we took 35 minutes to 40 minutes in STA-M4 anastomosis and
35 to 60 minutes in STA-M3 anastomosis, but, surprisingly, we found no infarct in
temporarily occluded arterial territory. In one case, we found infarct that was not
related to temporary clamping [[Figure 6]]. Now, we used to talk regularly with anesthesiologist to keep BP at upper normal
level and high dose inj. propofol in high dose. Now, we require 20 to 30 minutes to
performing STA-M4 or STA-M3 bypass.
Fig. 6 (A & B) Postoperative CT scan on the 1st POD showing a fronto-insulo-caudate infarct that was not related to cross clamping
of the temporal M3-M4 junction.
In the later part of our learning curve, we used to take heel and toe suture bites
on Donor arteriotomy before applying cross clamps on the recipient artery. This practice
decreases ischemic time to some extent.
Preoperative Use of Systemic Heparin
During high flow bypass inj. Heparin 3000 U i.v was used a single dose just before
putting a cross clamp 9 on M2. In STA-MCA bypass, no systemic heparin was used.
Hematoma in Sylvian Fissure
In the initial 3 to 4 cases in which STA-M3 bypass was performed, we found postoperatively
hematoma in the sylvian fissure, which was due to initial leaking through anastomotic
sites after removal of temporary clips. Later, to prevent this hematoma, we routinely
place Spongostan pieces deep to the anastomotic site so that leaking blood should
not spread into deep Sylvian spaces.
Common Leaking Sites ([Figure 7a-7c])
Fig. 7 (A) Schematic drawing showing “incorrect” techniques of 1st bites, needle direction, and suturing after the anchoring suture that results in
anastomotic leak after removal of cross clamps. (B) anastomotic leak through the anastomosis
(at the 1st suture site) after removal of cross clamps. (B) Schematic drawing showing “correct” techniques of 1st bites, needle direction, and suturing after the anchoring suture that prevents anastomotic
leak after removal of cross clamps. (C) Schematic drawing showing alternative two-step correct techniques of the 1st bites, needle direction, and suturing after the anchoring suture that also prevents
anastomotic leak after removal of cross clamps.
Leaking is near the heel or toe stitches. To prevent this, we use ‘right angle needle
pricking direction on recipient’ to the needle pricking direction on donor in first
stitch near the toe or heel stitch. Anastomotic leaking after removal of temporary
clips usually stops spontaneously within 5 minutes; if not, it should stop with round
Surgicel packing within the next 5 to 10 minutes. Even with Surgicel, if leaking persists,
a temporary clip should be applied on the donor artery for 3 to 5 minutes. If temporary
clipping of the donor artery fails to stop leaking, an additional microanastomotic
suture will be needed to stop leaking.
In these first 100 EC-IC bypasses, only 3 cases needed additional stiching after removal
of the temporary clips and their location was near to toe (anchoring) stich.
Patency Test after Anastomosis
After cessation of leaking through the anastomosis, the anastomotic patency and functionality
were checked by inspection, palpation, test occlusion of the donor artery by microforceps
or temporary clip and by micro-doppler. We found that the anastomosis was functioning
in all cases after completion, except in two cases in which the pathology was giant
supraclinoidal ICA aneurysm, and the anastomoses were found occluded after completion
of clip reconstruction of the aneurysm. Then, we opened the donor artery just proximal
to the anastomotic line with a small arteriotomy and found thrombus at the anastomotic
site. Then, we removed it and irrigated with heparinized solution along with systemic
heparinization. Blood flow was re-established through the anastomosis. In one case
in which the ICA lumen was compromised by aneurysm clips, the total MCA territory
was infarcted due to rethrombosis of the STA-MCA bypass ([Figure 8]). When we reviewed the operating videos, in this case we found that there was overstaining
of the endothelial surface of the donor artery at the anastomotic end with ‘gentian
violet’, and we think this might be the cause of thrombosis. Therefore, in subsequent
cases, the anastomotic margins of the donor artery were stained carefully after apposing
margins, so that the stain should not enter into the luminal surface, and staining
of the recipient artery was done before arteriotomy. In another case, we did not find
any definitive cause of thrombotic occlusion of the anastomotic site on reviewing
the operating video.
Fig. 8 (A) Preoperative CT scan showing suspected giant left ICA aneurysm. (B, C and D) CTA of the brain showing a giant partially thrombosed left ICA aneurysm. (E and F) Postoperative CT scan on the 1st POD showing massive left MCA infarct (clip reconstruction of the aneurysm was done
with protective STA-MCA bypass, but the bypass was thrombosed preoperatively and it
was rescued).
In high flow bypasses, we did not face any preoperative or postoperative graft spasm
or occlusion.
Dural Closure
In all cases, watertight dural closure was not performed (actually, it was not possible).
The wound was closed with drain at the upper end of the wound. In most of the cases,
the drain was removed on the 3rd or 4th POD if drain collection was minimum. In only 9 cases in which CSF was coming through
the drain after the 4th POD, we continued the drain up to the 8th day and then removed the drain with stitching of the drain site. In four cases, there
was subcutaneous collection of CSF that was resolved within 3 weeks in 3 cases; in
1 case, repeated tapping failed to stop collection of CSF and the patient needed readmission
followed by lumbar CSF drainage to stop CSF collection at the end of 8 weeks postoperatively.
Patency of Anastomosis on Follow-up ([Figure 1b],[2f],[5] and [9f])
Fig. 9 (a) (A and B) MRI of the brain DW images showing the right MCA territory and left ACA ischemia
and patchy infarcts. (C and D) CTA of the brain showing right M1 stenosis (severe) and left A2 stenosis. (E and F) Cerebral DSA showing right M1 stenosis (severe) and left A2 stenosis. (b): (A, B, C, and D) Preoperative pictures of anastomosis for temporal STA-MCA bypass as a part of double
barrel bypass. (c) (A, B, C, and D) Preoperative pictures of anastomosis for frontal STA-MCA bypass as a part of double
barrel bypass. (d): (A, B, C, and D) Preoperative sequential picture of A3-A3 bypass in the frontal interhemispheric
fissure; (A and B) Durotomy and interhemispheric dissection. (C and D) Identification and preparation of left and right A3 after removal of a small part
of the falx. (e): (A, B, C, and D) Preoperative sequential pictures of A3-A3 side to side anastomosis. (f) (A and B) Postoperative CTA of the brain showing patent double barrel STA-MCA bypass and A3-A3
bypass (yellow circles indicate anastomosis). Privacy Policy | Disclaimer | Site Map.
Digital palpation of the STA, doppler checking, CT scan, and CTA of the brain including
neck vessels were performed in all cases on the 1st POD to check anastomotic patency. Computed tomography scan also detects hematomas
and infarcts. In one case, infarcts in the caudate nucleus head and in the anterior
insula were found, which were not due to cross clamping. Sylvian fissure hematoma
was found in two cases on CT scan. In two cases, there were no flows through the STA.
Subsequent follow-up was made by digital palpation and doppler routinely. Computed
tomography angiography/magnetic research angiography [MRA] were performed after 3
months, 9 months, and then at 12-month intervals. No DSA was done in the postoperative
follow-up.
At the end of 12 months (69 cases were available for follow-up), all anastomoses were
functioning on digital palpation and doppler examination. But CTA/MRA failed to show
the anastomosis in 11 cases. All high flow anastomosis were patent on CTA/MRA at the
end of 12 months after the operation.
A total of 100 bypasses were done in 83 patients, of which 43 were male and 40 were
female. The age range was from 04 to 72 years old (average 32 years old). Eleven patients
were lost to follow-up postoperatively after 3 months and they were not even available
for telephone follow-up. The follow-up period was from 03 to 120 months (average 18.4
months).
Total number of EC-IC bypasses:100
-
□ Cavernous ICA: 02
-
□ Supraclinoidal ICA: 04
-
Low flow STA-MCA bypass:
-
Single barrel:
-
□ Replacement:
-
Ischemia/infarct:17
-
MCA dissection: 04
-
CCF-04:
-
▪ Protective/Insurance:
♦ With proximal stenosis: 08
♦ Protective: 16
Indication of Bypass (83 Cases)
-
Arterial stenosis/occlusion/dissection causing cerebral ischemia:
-
Intracranial aneurysms: 30
-
Moyamoya disease: 21
-
Direct CCF- 04 ([Tables 1] and [2])
Table 1
Clinical Presentation of the patients (n = 83)
|
Features
|
Number
|
Percentage
|
|
Features of SAH
(Headache, vomiting, LOC)
|
33
|
39.8%
|
|
Hemiparesis
|
36
|
43.4%
|
|
Ophthalmoplegia
|
06
|
7.2%
|
|
Dysphasia
|
18
|
21.7%
|
|
Visual disturbance
|
06
|
7.2%
|
|
Seizure
|
02
|
2.4%
|
|
H/O TIA
|
31
|
37.3%
|
|
Red eye and proptosis
|
04
|
4.8%
|
Abbreviations: LOC, loss of consciousness, SAH, subarachnoid hemorrhage; H/O TIA,
history of transient ischemic attack.
Table 2
Review of death cases (03) in EC-IC bypass
|
No.
|
Age, gender, and diagnosis
|
Preoperative
|
Postoperative CT
|
Time of death
|
|
1
|
31, M, Moyamoya disease
|
Smoothly functioning bypass
|
Distant parenchymal hemorrhage
|
8th POD
|
|
2
|
36, M, giant supraclinoidal aneurysm with atherosclerosis
|
Preoperative thrombosis of STA-MCA bypass with occlusion of ICA lumen after multiple
clip reconstruction
|
LSA and total MCA infarct
|
1st POD
|
|
3
|
65, F, giant supraclinoidal aneurysm with atherosclerosis
|
Preoperative tear of aneurysm neck near bifurcation.
|
LSA and total MCA infarct
|
1st POD
|
Abbreviations: CT, computed tomography; F, female; LSA, lanticulo striate artery;
M, male; MCA, middle cerebral artery; STA-MCA, superficial temporal artery-middle
cerebral artery bypass; POD, postoperative day.
The most common presentation was hemiparesis and dysphasia in the ischemic group with
history of transient ischemic attack (H/O TIA). Features of SAH (that is, headache,
vomiting and loss of consciousness [LOC]) were the presenting symptoms of the intracranial
aneurysm group. Eight cases of intracranial aneurysm had stenosis just proximal to
the aneurysm. Middle cerebral stenosis cases presented with TIA and ischemic stroke.
In MCA dissection, both ischemic clinical picture and SAH picture were present. All
CCF cases were direct and had H/O head injury. Most cases of moyamoya disease presented
with symptoms of ischemia. Infection was the etiology of thrombosis in cavernous ICA,
in two cases. In one case, orbital cellulitis spread in the CS and caused thrombosis
of the ICA (with aneurysm). In the other cases, panrhinosinusitis (by MRSA) spread
to both cavernous sinuses (CSs) and both ICAs were occluded. In one interesting case,
a giant partially thrombosed ICA bifurcation aneurysm thrombosed totally with distal
ICA, A1 and M1. Acute thrombosis of the ICA with aneurysm in CS occurred in 4 cases,
one of whom was a 3-month pregnant woman. In one case, there was intractable TIA with
impending major stroke in which the whole brain was supplied only by the right-sided
ICA, and the patient developed posterior inferior cerebellar artery (PICA) infarct
12 hours before the ‘scheduled urgent’ revascularization operation; high flow EC-IC
bypass was done in this case. Postoperatively, the patient developed ‘behavioural,
intellectual, and psychogenic’ symptoms that recovered slowly. The average ischemic
time was 28 minutes (range: 20–60 minutes). There was no clamp-related infarction.
In one case, the patient developed postoperative insulofrontal infarct unrelated to
temporary clamping. One preoperative ambulant patient deteriorated neurologically
in the postoperative period and developed hemiplegia. Six months after the operation,
she was ambulant with support. In this case, the cause seemed to be hyperperfusion.
Headache resolved in all cases. Transient ischemic attack and seizures were also gone
postoperatively. Ophthalmoplegia recovered in all cases in which it was present, except
in one case, in which abducent nerve palsy persisted. In one girl, mono-ocular complete
blindness developed postoperatively due to ophthalmic artery occlusion, in which high
flow bypass with ICA occlusion were performed. Red eye and proptosis were cured in
CCF cases. Motor and sensory dysphasia improved in all cases in which it was present,
except for one case in which preoperative global aphasia converted to sensory aphasia
in the postoperative period.
Three patients died in the postoperative period. The rest of the patients improved
postoperatively. All patients were ambulant with static neurostatus without new stroke/TIA
until the last follow-up. All bypasses were patent until the last follow-up (clinical,
doppler/imaging).
Discussion
As microneurosurgery advanced tremendously, indications for cerebral revascularization
expanded to include multi-infarct dementia, acute ischemic stroke, MCA stenosis, MCA
dissection, and ischemic retinopathy. To recommend the indications and results of
EC-IC bypass, the International Cooperative Study of Extracranial/Intracranial Arterial
Anastomosis (EC/IC bypass study) was performed from 1977 to 1985.[18] However, the data of the study showed that EC-IC anastomosis was not superior in
preventing stroke in patients with atherosclerotic arteriopathy of the ICA and MCA
compared with best medical therapy.[18] The study identified two important subgroups that seemed to do particularly poorly:
cases with severe MCA stenosis and those with persistence of TIA or of ischemic symptoms
in known ICA occlusion.[19] The subgroups subsequently identified to potentially benefit from surgical cerebral
revascularization were those in which hemodynamic changes play a primary role in the
precipitation of ischemic stroke. Since then, recent technological advances that were
not available at the time of the EC/IC bypass study have made it possible to better
identify this potential subgroup of patients.[20]
[21]
[22]
[23] One of these parameters (the oxygen extraction fraction [OEF] as determined by positron
emission tomography [PET]) identifies cases with hemodynamic susceptibility, which
may then benefit from an EC-IC bypass procedure.[24]
[25]
[26]
[27]
Currently, EC-IC bypass is either done for cerebral blood flow (CBF) augmentation
or replacement. Examples of the first one would be symptomatic cases with ICA occlusion
and proven hemodynamic vulnerability or moyamoya disease. Extracranial to intracranial
bypass surgery for CBF replacement is most commonly done in complex aneurysm management,
such as when an aneurysm is trapped, or in skull base neoplasm surgery associated
with arterial sacrifice or injury.[1]
[2]
[22]
[28]
In the following conditions, EC-IC bypass is usually considered:
-
an aneurysm or atherosclerotic plaque that is not treatable endovascularly or by other
means
-
failure of medication to control TIA symptoms or stroke
-
imaging tests (angiogram, CTA, MRA) that show arterial stenosis or occlusion
-
cerebral blood flow (CBF) studies (CT perfusion, PET, single photon emission computed
tomography [SPECT]) that show arterial stenosis is causing insufficient blood flow
to the brain
Cerebral bypass may be helpful in restoring blood flow and reducing the risk of stroke
in conditions such as:
-
Moyamoya disease: a narrowing of the internal carotid arteries at the base of the
brain that can cause multiple strokes or hemorrhages. To compensate for the narrowing
arteries, the brain creates collateral blood vessels in an attempt to deliver oxygen-rich
blood to deprived areas of the brain. A bypass can restore blood flow to the brain
and prevent future strokes.
-
Aneurysm: a bulge or ballooning of an artery wall. Some giant, fusiform, or dissecting
aneurysms cannot be treated with surgical clipping or endovascular coiling. In such
cases, the parent artery must be sacrificed, and the blood flow bypassed for the aneurysm
to be effectively treated.
-
Skull base tumor: a tumor can grow where the major vessels enter the skull and surround
or invade the artery. Removing the tumor may require sacrificing the encased artery
and bypassing the blood flow.
-
Carotid artery stenosis: a narrowing or blockage of the carotid artery in the neck
caused by atherosclerotic plaque deposits in the vessel wall.
-
Intracranial arterial stenosis: a narrowing or blockage of an artery inside the skull
that supplies blood to specific areas within the brain.[1]
[2]
[22]
[28]
Several techniques for the creation of artificial CBF conduits are available in addition
to the arterial graft of the STA-MCA anastomosis. A STA-MCA bypass has a luminal flow
patency rate > 95%.[29] Since the first STA-MCA procedure was described by Yasargil,[11]
[16] many variations have been published, but STA-MCA bypass remains the main workhorse
of a neurovascular surgeon. Many of these variations have been developed in dealing
with complex intracranial aneurysms and skull base neoplasms. These variations include
anastomoses between the bilateral anterior cerebral arteries, the occipital artery
to the posterior inferior cerebellar artery (PICA), and the anterior inferior cerebellar
artery (AICA). Others include PICA to PICA, vertebral artery (VA) to PICA, STA to
SCA or to the posterior cerebral artery (PCA), subclavian artery to PCA, PCA to SCA,
and even a tandem occipital artery to AICA and PICA anastomoses.[10]
Other common EC-IC bypasses for cerebral revascularization methods include venous
interposition grafts, such as the great saphenous vein, free arterial conduits including
the radial artery, and artificial grafts (with polytetrafluoroethylene ePTFE tubes).[30]
[31]
The great saphenous vein graft has been used in bypasses for giant intracranial aneurysms,
skull base neoplasms requiring ICA sacrifice or involving the ICA, or VA occlusive
disease.[32]
[33] Internal carotid artery bypasses include the cervical-supraclinoid ICA, the petrous-supraclinoid
ICA, and the cervical–petrous ICA.[34] The radial artery bypass graft has been shown to have long-term patency when used
for the management of giant aneurysms of the ICA.[35]
Intracranial-intracranial (IC-IC) bypasses are occasionally necessary ([Figure 9d] and [9e]). A short interposition graft such as the the saphenous vein of the patient can
be used in IC-IC bypasses. Donor vessels in IC-IC bypasses are usually from the ICA,
M1 or A1 arteries, and the recipients may include the ICA, M1–3, A1–2, P1–2, the basilar artery,
and the superior cerebellar artery (SCA).[1]
Very useful and important advancements in monitoring intraoperative blood flow have
also been developed. The use of micro-Doppler, and of transit time flowmetry, such
as the Charbel microflow probes (Transonic), and indocyanine green (ICG) video angiography
have all had a positive impact on cerebral revascularization by EC-IC bypass surgery
by ensuring anastomotic and graft patency.[1]
Complications in STA-MCA bypass are limited and include early postoperative TIA, delayed
stroke, development of a pseudoaneurysm, and wound dehiscence. High-flow bypass grafts
are more prone to develop complications than low-flow STA-MCA bypass. Radial artery
grafts may suffer vasospasm or intimal hyperplasia and, eventually, occlude. Proatherogenic
changes can occur in SV grafts, which eventually leads to occlusion. After parent
vessel occlusion, thromboembolic complications are common in high flow bypass, mainly
due to the change in intracranial hemodynamics. Preoperative antiplatelet medications,
as well as intraoperative anticoagulation, can prevent these thromboembolic events.
In patients without vascular reserve, prolonged temporary occlusion times can lead
to territory infarcts without changes in the neuromonitoring. So, it is important
to minimize occlusion times in these patients. In longstanding perfusion deficiency,
reperfusion hemorrhage may be problematic after revascularization, although its incidence
is low. Other complications involve the site of graft harvests, such as infection,
ischemic hand, or hematoma.[10]
Cerebral revascularization by EC-IC bypass has evolved from the culmination of several
technologies, from the early dawn of vascular surgical techniques in animals to the
development and utilization of the surgical microscope, of bipolar coagulation, and
of suitable suture material. Major asking regarding the indications and benefits of
cerebral revascularization are being addressed. Fascination in further development
of this matter to make it safer for the patients remains strong and high. Advanced
research into perioperative blood flow assessment will play a key role in determining
the positive result of cerebral revascularization. It is logical to hope that, with
better understanding of the pathophysiology of cerebral ischemia and better patient
selection, cerebral revascularization by EC-IC bypass will remain an indispensable
tool in microneurosurgery.[1]
