Original Article

Brain Bypass Surgery for Complex Middle Cerebral Artery Aneurysms: Evolving
Techniques, Results, and Lessons Learned
Sabareesh K. Natarajan1, Qazi Zeeshan2, Basavaraj V. Ghodke3, Laligam N. Sekhar2

- OBJECTIVE: To analyze a consecutive series of patients months (0.4e124 months) and the mean radiological
with middle cerebral artery (MCA) aneurysms who needed follow-up was 37 months (0.4e134 months).
an adjunctive cerebral revascularization procedure to - CONCLUSIONS: Cerebral revascularization is an impor-
achieve aneurysm occlusion with preservation of flow
tant adjunct for treating MCA aneurysms and can be done
through all MCA branches.
safely. The article provides the insights we gained by ris-
- METHODS: A total of 42 patients with 43 MCA aneu- ing through the learning curve.
rysms underwent 52 bypass procedures over 13 years. The
location of the aneurysm were M1 trunk, M1 bifurcation,
M2 and beyond. The bypasses performed included intra-
cranial bypasses (resection with end to end anastomosis,
INTRODUCTION
end to side implantation, side to side anastomosis, and
short interposition graft), extraintracranial bypasses (su-
perficial temporal to middle cerebral artery anastomosis,
and radial artery bypass graft, or saphenous vein graft),
double bypasses, Y-grafts, and combined techniques.
M iddle cerebral artery (MCA) aneurysms are the most
common aneurysms managed by microsurgical clip
reconstruction. Some complex MCA aneurysms cannot
be safely occluded without risking the parent artery or the branch
vessels. These patients require adjunctive revascularization pro-
- RESULTS: Forty-two of 43 aneurysms (98%) had patent cedures. Common characteristics that make simple clip recon-
bypasses at long-term follow-up. All 43 aneurysms were struction difficult include: Branches arising from aneurysm neck or
completely occluded at last follow-up. Six patients (14%) dome, extensive atherosclerotic disease at the neck, previous
endovascular treatment, large or giant size (>15 mm diameter),
developed strokes related to the surgical treatment. At
fusiform aneurysms, and considerable intra-aneurysmal throm-
last follow-up, 36 patients had a modified Rankin score of
bosis. The majority of bypasses can be anticipated before surgery. In
0e2, 5 patients had modified Rankin score 3e5, and 1 a few patients, a significant branch stenosis may be found after
died. In this series, 31 (73.8%) patients improved, 8 (19%) clipping (after attempts to reposition the clip have been exhausted)
patients had same functional status, and 3 (7.2%) patients and may require a bypass procedure. The recurrence of a large or
deteriorated, including 1 patient who expired due to giant aneurysm after previous treatment often requires a bypass. In
sepsis. The mean clinical follow-up duration was 39.3 this consecutive series we examined the results and complications

Key words RAG: Radial artery graft

- Cerebral revascularization SAH: Subarachnoid hemorrhage
- Endovascular management SSEP: Somatosensory evoked potential
- Graft occlusion STA: Superficial temporal artery
- High flow bypass SVG: Saphenous vein graft
- Middle cerebral artery aneurysms
- Radial artery graft From the 1Department of Neurosurgery, University of Massachusetts Medical School,
- Saphenous vein graft Massachusetts; and Departments of 2Neurosurgery, and 3Radiology, University of
Washington, Seattle, Washington, USA
Abbreviations and Acronyms
To whom correspondence should be addressed: Laligam N. Sekhar, M.D.
ATA: Anterior temporal artery bifurcation [E-mail: lsekhar@uw.edu]
DSA: Digital subtraction angiography
Sabareesh K. Natarajan, and Qazi Zeeshan contributed equally to this work.
EC-IC: Extracranial-intracranial
EEG: Electroencephalogram Citation: World Neurosurg. (2019).
IC-IC: Intracranial-intracranial https://doi.org/10.1016/j.wneu.2019.06.059
ICA: Internal carotid artery Journal homepage: www.journals.elsevier.com/world-neurosurgery
MCA: Middle cerebral artery Available online: www.sciencedirect.com
MEP: Motor evoked potentials
1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
NCCT: Noncontrast computed tomography
PED: Pipeline Embolization Device

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 ORIGINAL ARTICLE
SABAREESH K. NATARAJAN ET AL. BRAIN BYPASS SURGERY FOR COMPLEX MCA ANEURYSMS

of 52 cerebral revascularization procedures for treatment of MCA radial artery or the saphenous vein was generally used for
aneurysms over 13 years. This includes a period of time before the US replacement of the M1 or large M2 vessels. For smaller arteries,
Food and Drug Administration approval of a flow diversion stent small interposition grafts, a side to side anastomosis, a reim-
(the Pipeline Endovascular Device [Medtronic, Minneapolis, Min- plantation, or a superficial temporal artery (STA) to MCA branch
nesota, USA]). Flow diversion stents (off-label) have been used for bypass was used. Aspirin 325 mg orally was given 1 week before
complex MCA aneurysms with varying results.1,2 planned surgery and the same dose was given per rectum in
emergent cases. Total intravenous anesthesia with propofol-
induced burst suppression and permissive hypertension during
METHODS temporary flow arrest was performed with neuromonitoring
All patients had been operated by the senior author (L.N.S.), and including somatosensory evoked potential, motor evoked poten-
the review was performed after the approval from the institutional tial, and electroencephalogram. Patients received 5000 U of hep-
review board. Individual patient consent was not sought. The re- arin intravenously before temporary low arrest and the actual
view included patient charts, radiographic studies, and, when bypass procedure. Most recent patients underwent an indocyanine
needed, telephonic follow-up. Operative drawings made by the green angiogram and micro Doppler studies postoperatively, and
senior author were redrawn by a medical illustrator. Statistical all patients underwent a digital subtraction angiography
analysis was done using SPSS software (IBM, Armonk, NY). In postoperatively.
many of these cases, an experienced neurointerventionist was also Bypass techniques evolved during the study period, with a
involved in the decision-making process. greater preference for radial artery grafts for major vessel
In addition to consultations between the 2 physicians, when replacement, as opposed to saphenous vein grafts and have been
there is equipoise, the patient is given the ability to make the described by the senior author in various papers before.3,4
choice of treatment. The final decision to proceed with the bypass The aneurysms were divided into: M1 segment, M1 bifurcation,
was made during the surgery after inspection of the aneurysms, M1 at anterior temporal artery bifurcation (ATA), and beyond M2.
except in patients where the postoperative angiogram showed
significant target vessel stenosis. The bypass conduit was generally
chosen on the basis of the artery being replaced; for instance, the RESULTS
Forty-two patients with 43 aneurysms underwent 52 bypass pro-
cedures from 2005 to 2018. There were 9 M1 aneurysm patients
Table 1. Demographics, Presentation and Location of who underwent 13 operations; 20 M1 bifurcation aneurysms pa-
Aneurysms tients underwent 24 operations (2 for recurrences, and 2 for graft-
Total patients 42 related problems); 3 M1 ATA aneurysm patients had 3 operations;
3 M2 aneurysms underwent 3 operations; and 8 patients with M3/
Total aneurysms 43
M4 aneurysms had 12 bypass operations (one patient has 2 an-
Total bypasses 52 eurysms on either side).
Ruptured 13
Hunt and Hess grade 1e3, n 9
Table 2. Complications and Graft Patency
Hunt and Hess grade 4e5, n 4
Unruptured, (n) 30 Complication n/N

Sex Stroke 6/44

Male 26 Complete recovery 4/6
Female 16 Hematoma (epidural, subdural, or intraparenchymal) 3
Location Infection 2
ATA 3 Deaths 1
M1 9 Bypass related 0
MCA bifurcation 20 Disease related 0
M2 and beyond 11 Other causes 1
Size of aneurysm (mm) Graft stenosis/thrombosis needing revision
0e9 17 Immediate postoperative 3/43 aneurysms
10e17 15 Long term 2/43 aneurysms
18e24 5 Graft patency
>24 6 Immediate (after revision) 42/43 (97.6%)
ATA, anterior temporal artery bifurcation. Long term 42/43 (97.6%)

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There were 20 (38.4%) extracranial-intracranial (EC-IC) high- Graft-Related Problems

flow bypass (radial artery graft [RAG]: 11, saphenous vein graft Saphenous vein conduit was used for 9 high-flow EC-IC bypasses.
[SVG]: 6, and RAGþSVG: 3), 8 (15.5%) EC-IC low bypass (direct Of these, 6 were pure SVG, and 3 were part of a Y-bypass. Four of
STA MCA: 5, RAG/SVG interposition graft from STA: 3) and 24 these (M1-C, MB-K1, MB-K2, MB-L MB-Q1, Figures 1e8) devel-
(46.1%) intracranial bypasses. Thirty-six of the aneurysms pre- oped some problem during or after the bypass requiring revision.
sented de novo, 3 were recurrent after previous surgery, and 4 were All were patent eventually, albeit with significant stenosis in one.
recurrent after prior coiling or flow diversion procedures. RAG was used in 15 EC-IC high flow bypasses-12 pure and 3
Table 1 summarizes the demographics, presentation, and procedure Y-bypasses and 1 patient (M1-A) developed asymptomatic graft
performed. Table 2 summarizes overall complications and graft occlusion 18 months later. Forty-two of 43 aneurysms (98%) had
patency. Tables 3e8 summarize the treatment, outcomes, and com- patent bypasses at long-term follow-up. Details of graft compli-
plications of M1 segment, M1 bifurcation, M1 at ATA, and beyond M2 cations are summarized in Tables 5 and 7 and Figures 1e8.
segment aneurysms, respectively. Figures 1e8 are a collage of the
preoperative imaging, technique illustration, and postoperative im- Early versus Late Cases
aging of all patients with salient comments for review. All the cases treated were divided in 2: 2005e2011(group A) and
2012e2018 (group B); results are summarized in Table 9.
Stroke The complications may have been reduced in the latter half
Based on magnetic resonance imaging scans, 6 (of 42, 14%) pa- thanks to improvements in bypass techniques, management of
tients (M1-B; M1-C; M1-E; MB-K1 and MB-K2; MB-L MB-Q1, perioperative anticoagulation, and better patient-graft matching.
Figures 1e8) suffered strokes during or after the operation. All
of them were either MCA-M1(M1-B; M1-C; M1-E) or bifurcation Table 4. Treatment and Outcome of M1 Trunk Aneurysms
aneurysms (MB-K1 and MB-K2, MB-L, MB-Q1). Four of these
strokes occurred in EC-IC bypass (n ¼ 4 of 28) and the 2 Treatment and Outcome n
remaining were encountered in intracranial-intracranial (IC-IC)
Total number of aneurysms (patients n ¼ 9) 9
bypasses (n ¼ 2 of 24). Residual deficits was noted in 1 patient at
the 3-month follow up (M1-E) and 1 patient (MB-L) died in the Type of aneurysms
hospital (Table 5 and 7, Figures 1e8). 1. Fusiform 7
2. Fusiform with some eccentric outpouching 2
Table 3. Treatment and Outcome of M1 Aneurysm at the
Total bypasses 13
Anterior Temporal Branch
SAH 2
Treatment/Outcome n
Treatment
Total number of aneurysms (patients n ¼ 3) 3 Clipping and EC-IC RAG 4
Total bypasses 3 Complete trapping and EC-IC SVG 1
SAH 1 Clip reconstruction and EC-IC SVG 1
Treatment Proximal partial occlusion and EC-IC SVG 2
Clipping and IC-IC reimplantation 1 Proximal partial occlusion and STA-MCA 1
Clip reconstruction and IC-IC side to side bypass 1 Resection and IC-IC 2
Excision and STA-MCA 1 Proximal partial occlusion and EC-IC RAG 1
Patency 3/3 (100%) Complete trapping and EC-IC RAG 1
Aneurysm occlusion 3/3 (100%) Bypass patency, long term (8/9) 89%
Complications None Aneurysm occlusion (9/9)100%
Outcome Outcome
mRS 0e2 3 mRS 0e2 8
mRS 3e5 0 mRS 3e5 1
mRS improved 3 mRS improved 8
mRS same 0 mRS same 1
mRS deteriorated 0 mRS deteriorated 0
Complications None Complications: see Table 5

EC-IC, extracranial-intracranial; IC-IC, intracranial-intracranial; MCA, middle cerebral ar- EC-IC, extracranial-intracranial; IC-IC, intracranial-intracranial; MCA, middle cerebral ar-
tery; mRS, modified Rankin Scale; SAH, subarachnoid hemorrhage; STA, superficial tery; mRS, modified Rankin Scale; RAG, radial artery graft; SAH, subarachnoid hem-
temporal artery. orrhage; STA, superficial temporal artery; SVG, saphenous vein graft.

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DISCUSSION bypass, which is much higher than any other series reported in
This is the largest series that has been reported to date of patients literature with comparable complication rates and complete
who underwent cerebral revascularization for MCA aneurysms. aneurysm obliteration rates. The follow-up on these patients is the
Our series is unique in that all modalities of bypass including longest reported when compared with any other series.
high-flow, STA-MCA, and IC-IC were used equally depending on The patient cohort in this series can be separated into 2 co-
the flow replacement needed in each case. A good number of the horts—patients who needed a high-flow replacement of M1 or
proximal aneurysms in M1, MCA bifurcation had a high-flow primary MCA branches (n ¼ 29) and patients who needed a
revascularization of the ATA (n ¼ 3) or distal revascularization
(n ¼ 12). The first group underwent 37 bypass procedures, which
Table 5. Complications of M1 Trunk Aneurysms included 19 EC-IC high-flow, 4 EC-IC low-flow, and 14 IC-IC
bypass predominantly with RAG/SVG conduits (RAG n ¼ 23,
M1- M1 stenosis and fusiform aneurysm Developed an asymptomatic graft SVG n ¼ 6). The second cohort had predominantly 11 IC-IC bypass
A underwent an RAG and clipping of a occlusion 18 months later. procedures with or without a conduit and 4 EC-IC bypass using
saccular portion of the aneurysm. Angiography revealed the STA as a donor.
enlargement of collaterals,
and good reconstitution of
Endovascular Management
all M2 branches.
Aneurysms around the MCA are technically challenging targets for
M1- Underwent an SVG and trapping of Required an anterior temporal endovascular treatment because of their distal location, multiple
B a partially calcified flask shaped lobectomy urgently. He recovered
aneurysm. During the surgery, an completely, and has completed
inferior and smaller M2 branch high school. Table 6. Treatment and Outcome of MCA Bifurcation
Which was arising from the Aneurysms
aneurysm was not revascularized
because there was very good Treatment and Outcome n
backflow from the distal stump.
This patient developed a temporal Total number of aneurysms (patients n ¼ 20) 20
lobe infarct. Total bypasses 24
M1- SVG and trapping an aneurysm,poor She was explored, and was found SAH 8
C flow postoperatively, with a small to have an abnormally oriented
stroke in the temporal area. valve, which was removed. She Treatment
recovered well, with patency of the Clip reconstruction and EC-IC SVG 1
graft. 11 months later, she
developed transient ischemic Clip reconstruction and EC-IC RAG 7
attacks and ischemia, and was Clip reconstruction and EC-IC STA-MCA 3
found to have developed a stenosis
Clip reconstruction and IC-IC, reimplantation 1
at the previous repair site. She was
explored, and had a segmental vein Clip reconstruction and IC-IC, jump graft 5
graft replacement; 23 months later,
Y-graft bypass 3
she had recurrent ischemic
symptoms, and was found to have Clip reconstruction and IC-IC, reimplantation and side to side 1
restenosis of the SVG. During a bypass
reoperation, an ATA was placed Bypass patency, long term (20/20)
from the proximal SVG to an M2 100%
branch bypassing the area of
stenosis, and then the stenotic area Aneurysm occlusion (20/20)
of the SVG was resected, and 100%
replaced with an ATA graft. She Outcome
remains free of symptoms, and both
grafts are patent on CTA, 96 months mRS 0e2 15
after this operation. mRS 3e5 4
M1- Ruptured fusiform MCA aneurysm Postoperatively, delayed filling of mRS 6 1
E underwent a double barrel bypass bypass, and evidence of cortical
with a large STA, followed by strokes. Radial artery graft was mRS improved 10
proximal occlusion. placed into the M2 branch proximal mRS same 7
to the STA bypass. Suffered
mRS deteriorated 3
hemispheric strokes, but recovered,
albeit with some dependency for Complications: see Table 7
daily activates (mRS 3).
EC-IC, extracranial-intracranial; IC-IC, intracranial-intracranial; MCA, middle cerebral ar-
ATA, anterior temporal artery bifurcation; CTA, computed tomography angiography; mRS, tery; mRS, modified Rankin Scale; RAG, radial artery graft; SAH, subarachnoid hem-
modified Rankin Scale; RAG, radial artery graft; SVG, saphenous vein graft. orrhage; STA, superficial temporal artery; SVG, saphenous vein graft.

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SABAREESH K. NATARAJAN ET AL. BRAIN BYPASS SURGERY FOR COMPLEX MCA ANEURYSMS

branches, ATA, or lenticulostriate branches. Flow diversion is an often require distal dual access for stent delivery and jailed micro-
option for M1 aneurysms when there is a good proximal (distal to catheter assisted coiling, and have a high complication rate.5 The
the internal carotid artery [ICA] terminus) and distal landing zone latest iteration of the Neuroform Atlas Stent (Stryker
(proximal to the MCA bifurcation). Neurovascular, Fremont, CA) makes this easier as they can be
Stent-assisted coil reconstruction of wide-neck MCA bifurcation delivered through a 0.16 micro catheter; and coiling can usually
aneurysms is often required for complex MCA bifurcation aneu- be done through the stent tines with the same micro catheter,
rysms but they are technically challenging procedures given that thereby reducing the necessity of multiple access and catheter
they need delivery of a stent through the tortuous MCA vessels, jailing.6 Distal flow diversion is being tested around the
bifurcation but often involves jailing of the smaller superior
trunk. The long-term safety and results of jailing the MCA
Table 7. Complications of M1 Bifurcation Aneurysm branch have not been studied.7 Intra-saccular flow diversion is
also being tested for MCA bifurcation aneurysm but this is not yet
MB-D Suffered a postoperative epidural This patient developed a delayed approved for use in the United States by the US Food and Drug
infection, requiring the removal of narrowing of a radial artery graft Administration.8
a bone flap and antibiotics. 4 months later. He was Ruptured aneurysms preclude a stent implantation (and dual
successfully managed by means antiplatelet therapy) in the acute stage and these patients are
of segmental graft resection and
preferentially treated by microsurgical techniques. In patients with
anastomosis.
poor grade subarachnoid hemorrhage or patients who are not
MB-K1 Ruptured MCA aneurysm had Was explored, and a good surgical candidates, partial coiling of the aneurysm in the
and severe narrowing of one M2 reimplantation and STA-MCA acute stage, followed by definitive treatment 2e3 weeks after
MB-K2 branch after clipping She was branch anastomosis was done in
subarachnoid hemorrhage may be performed. During the second
treated initially by a side to side an attempt to revascularize the
anastomosis between 2 M2s. clotted artery.
stage, parent vessel flow diversion with jailing of 1 MCA branch,
However, the narrowed branch The STA-MCA bypass was
and anastomosis clotted, with a partially successful, but the Table 8. Treatment and Outcome of M2 and Beyond Aneurysms
stroke. patient suffered a significant right
hemispheric stroke, with eventual Treatment and Outcome n
recovery to an mRS 3.
Total number of aneurysms (patients n¼10) 11
MB-L Patient with a giant MCA She had a postoperative capsular
aneurysm had multiple coiling stroke, with hemiparesis, but was Total bypasses 12
procedures previously, and recovering. Three days SAH 2
presented with an enlarging postoperatively, she sustained a
aneurysm, and headaches. She pneumonia related to COPD and Treatment
underwent a RAG to one M2 nosocomial infection in the Partial distal occlusion and IC-IC bypass (reimplantation) 1
branch, and a SVG to another intensive care unit. She
large M2 branch followed by progressed to systemic sepsis Resection and end-to-end anastomosis IC-IC bypass 1
proximal occlusion. During and died. Resection and interposition radial artery graft 1
surgery, and attempt was made to
extract the coils, and clip/or trap Resection and end-end anastomosis, IC-IC 2
the aneurysm. At this time, her Resection and STA-MCA bypass, EC-IC 3
MEPs and SSEPs deteriorated,
Resection and interposition RAG, IC-IC 3
and did not recover.
Reconstruction bypass with lingual artery 1
MB-Q1 Patient with a large MCA She did well initially, but
bifurcation aneurysm presented developed a subdural and Resection and IC-IC jump graft 1
with TIAs in the MCA distribution. subarachnoid hemorrhage due to
Bypass patency, long term 12/12 (100%)
The aneurysm was clipped. persistent oozing from her
However, since one M2 was anastomotic site, presumably due Aneurysm occlusion 12/12 (100%)
severely narrowed, and short SVG to a combination of aspirin, and Outcome
was placed between the two M2 subcutaneous heparin.She was
branches. explored, the clot was removed, mRS 0e2 10
but the graft was also found to be mRS 3e5 0
partially thrombosed. A
thrombectomy was done mRS improved 10
successfully. She suffered a mRS same 0
cortical infarct, but recovered at 6
mRS deteriorated 0
months to a mRS 1.
Complications None
COPD, chronic obstructive pulmonary disease; MCA, middle cerebral artery; MEP, motor
evoked potentials; mRS, modified Rankin Scale; RAG, radial artery graft; SSEP, so- EC-IC, extracranial-intracranial; IC-IC, intracranial-intracranial; MCA, middle cerebral ar-
matosensory evoked potential; STA, superficial temporal artery; SVG, saphenous vein tery; mRS, modified Rankin Scale; RAG, radial artery graft; SAH, subarachnoid hem-
graft; TIA, transient ischemic attack. orrhage; STA, superficial temporal artery; SVG, saphenous vein graft.

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Figure 1. (ATA-A) 71-year-old man complaining of dizziness with 5 mm aneurysm. (A) 3D RA reconstruction of left ICA injection. (B) 3D illustration showing MCA
ATA aneurysm with ATA arising from the neck of aneurysm. (C). Postoperative 3D illustration showing reimplantation of ATA and clip reconstruction of the
aneurysm. (D) Digital subtraction angiography (DSA) showing filling of ATA and both MCA branches with complete obliteration of aneurysm. (ATA-B) 53-year-old
man with ruptured 16 mm aneurysm (A, B). DSA of left ICA injection showing MCA-ATA aneurysm and ATA arising from the neck of aneurysm (C). Preoperative
3D illustration showing anatomy at the level of aneurysm. (D) Postoperative 3D illustration showing clip reconstruction of aneurysm and revascularization of ATA
by side-side anastomosis. (E) Postoperative left ICA DSA showing filling of ATA. (ATA-C) 76-year-man with headache and 12-mm aneurysm. (A) 3D RA
reconstruction and (B). 3D illustration showing MCA ATA aneurysm with ATA arising from neck of aneurysm. (C) Postoperative 3D illustration showing clip
reconstruction of the aneurysm and STA-ATA anastomosis to revascularize ATA. (D) Postoperative DSA showing complete obliteration of the aneurysm and
filling of ATA from STA. (M1-A) 23-year-old woman with headache having 8.5 mm aneurysm (A). 3D RA reconstruction showing fusiform aneurysm of M1 with
pre-bifurcation stenosis. (B) Preoperative 3D illustration showing the aneurysm attached to frontal lobe. (C) Postoperative 3D illustration showing radial artery
bypass graft distal to aneurysm and clip reconstruction of the aneurysm. (D) Immediate postoperative DSA showing filling of the graft and MCA branches
postoperative DSA. (E) Capillary phase of left ICA injection showing delayed retrograde filling of the MCA through cortical collaterals, and occlusion of graft. (M1-
B) 13-year-old boy, incidentally diagnosed 30-mm aneurysm. (A) Preoperative DSA and (B). 3D illustration showing fusiform MCA M1 and bifurcation aneurysm
with involvement of all branches of MCA trunk. (C, D) Postoperative 3D illustration showing saphenous vein graft (SVG) to MCA M2 and excision of aneurysm.
(E) Postoperative DSA showing filling of MCA vessels from graft with no evidence of filling of ATA branches when compared to preoperative angiogram. (F)
Noncontrast CT (NCCT) showing left fronto- temporal stroke corresponding to vessels that is missing in postoperative angiogram. (M1-C1) 57-year-old woman
diagnosed with an asymptomatic 15 mm aneurysm. (A) 3D RA and (B). 3D illustration showing fusiform MCA aneurysm with atherosclerotic disease and
narrowing at level of neck. (C) Postoperative 3D illustration showing SVG to MCA M2 and clip reconstruction of the aneurysm. (D, E) Postoperative DSA showing
delayed filling through venous graft and antegrade filling through M1 into distal MCA vessels. (M1-C2) Patient presented with ischemic symptoms (A, B) and (C).
Preoperative 3D illustration showing a valve causing blockage of SVG that was repaired. (D) Noncontrast CT showing right frontotemporal stroke. (E, F)
Postoperative DSA after second surgery showing graft filling the distal MCA vessels.

intrasaccular flow diversion, or Pipeline flow diversion with the better kink resistance in the preauricular tunnel and at the
shield technology9 may be used as treatment options. intracranial turn, and remodels better into a small caliber graft
if the demand is lessthan what a native graft would supply. The
SVG was used in our cases only because RAG was not available,
EC-IC RAG/SVG versus EC-IC STA
or the desire to avoid extraction of the RAG in some young
In this series, the STA was used to revascularize the MCA territory
patients. We prefer to route our SVG behind the ear in a retro-
in 2 patients (M1-E1, and MB-P). In both patients, the STA was
mastoid bony tunnel to avoid kinking. We have reported using
selected because of its large size (>1 mm in diameter). In patient
the anterior tibial artery as conduit before8 and presently believe
M1-E1, a double-barrel bypass was performed. It proved to be
that the anterior tibial artery is a better conduit than the SVG in
inadequate, the patient developed a stroke in the MCA territory,
patients who do not have a RAG conduit. However, its
and this patient was salvaged by using a RAG. Traditionally, the
extraction takes more time, and requires the collaboration of a
STA grafts have shown to deliver less than 50 mL/minute and the
vascular surgeon.
RAG 50e150 mL/minute of blood and SVG 150e250 mL/minute.3
So we would like to call patients with donor as low-flow bypasses
and ECA/ICA donor with RAG/SVG conduits as high-flow by- IC-IC Bypass
passes. In the senior author’s experience, the STA does not reli- Local bypasses such as reimplantation and side to side anasto-
ably have adequate flow to replace the entire MCA territory or even mosis may be used to revascularize small MCA branches, resuture
the territory of the larger inferior trunk. STA can only be used as a of a vessel may be used when the vessels are redundant in length,
donor to replace a smaller MCA branch, the M3/M4 branches, or and a short interposition graft may also be used, when the gap
in patients who already have a large infarct in the MCA territory. between the 2 vessel ends is too long for the vessel to be sutured
The University of Illinois group has proposed measuring native without tension. Such bypasses are very useful for small arteries,
blood flow using magnetic resonance angiography NOVA and cut but also when the bypass is unplanned in the situation of a
flow index from the STA to make a treatment decision regarding ruptured aneurysm. However, as seen in our patient MB-K, when a
flow replacement bypass. They have stated that MCA flow local bypass (side to side in this patient) fails, it risks both vessels.
replacement needs only 50 mL/minute; and when a SVG graft is When technically well performed, the main reason for such failure
placed from the proximal STA in the zygomatic area it can provide may be the lack of antiplatelet activity, or a hypercoagulable state.
adequate flow replacement to the MCA territory.4,10
MCA ATA Aneurysm
RAG versus SVG Grafts for EC-IC High-Flow Bypass The need to revascularize the ATA is not proven. Moybedi et al.12
In this series of patients, we had more problems with SVGs than have reported a series where they used the ATA as a donor for IC-
our RAGs, particularly relating to valves and kinking. The main IC revascularization. Sacrifice of the anterior temporal artery al-
proposed reasons for the SVG problems are the presence of valves, ways leads to an anterior temporal lobe infarct, but the infarct may
low kink resistance, the size and volume mismatch, and their be small, or large and cause a functional deficit, particularly on the
inability to remodel to the desired flow in the recipient vessel.11 speech-dominant side. The senior author prefers to revascularize
The potential problems with choosing RAG as a conduit are the ATA when it is possible to avoid postoperative functional
graft spasm, size below 2.5 mm, prior use for radial artery lines, deficits. The different options for revascularizing ATA are reim-
and the absence of an adequate palmar arch in some patients. plantation, side to side anastomosis with another MCA branch, or
The problem of vasospasm has been eliminated by the senior STA-ATA bypass. The STA-ATA bypass is preferred in patients
author by the pressure distention technique.3 The RAG has with ruptured aneurysms because of the risk of thrombosis of local

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Figure 2. (M1-C3) Patient presented with ischemic symptoms. (A) Preoperative 3D illustration of third surgery showing revision of stenotic SVG. (B) Preoperative
3D illustration of fourth surgery, a segment of ATA was used to bypass a stenotic SVG and this was followed by resection of stenotic area, and an additional ATA
interposition graft. (C) postoperative DSA showing filling of all MCA branches through the graft. (M1-D) 11-year-old girl with headache having 3.5 mm aneurysm.
(A, B) DSA showing M1 aneurysm with pre-aneurysmal stenosis. C. Preoperative 3D illustration showing anatomy at the level of aneurysm. (D) Postoperative 3D
illustration showing saphenous vein graft from MCA M2 and clip reconstruction of the aneurysm. (E) Postoperative 3D illustration showing segmental stenosis
of SVG for which resection and anastomosis was done. (F) Postoperative DSA showing complete obliteration of aneurysm and filling of all MCA branches by
graft. (M1-E1) 63-year-old man with ruptured 15 mm aneurysm. (A) DSA and (B). 3D illustration showing fusiform MCA M1 aneurysm. (C) Postoperative 3D
illustration showing proximal occlusion of aneurysm and double barrel STA-MCA bypass to revascularize the MCA branches. (D) 3D CT angiogram showing STA-
MCA bypass filling the MCA vessels. (E, F) Postoperative DSA with CCA injection showing delayed filling of MCA branches from STA and complete occlusion of
MCA and the aneurysm. (M1-E2) Postoperative stroke/ischemia. (A) Postoperative 3D illustration showing revision of previous STA-MCA bypass with radial
artery graft (RAG). (B) Postoperative DSA showing filling of MCA circulation by RAG. (C, D) Noncontrast CT showing a large frontotemporal stroke on left side
due to ischemia during attempted revascularization. (M1-F) 4-year-old girl complaining of headache with 25 mm aneurysm. (A) DSA and (B). 3D illustration
showing fusiform partially thrombosed MCA aneurysm involving ATA and bifurcation and no lenticulostriate perforators around aneurysm. (C) Resection and end-
to-end anastomosis of aneurysm with RAG. (D) Postoperative DSA showing complete obliteration of the aneurysm with filling of distal MCA branches with radial
artery jump graft. (M1-G) 37-year-old man with ruptured 37 mm aneurysm. (A) AP view of left ICA DSA showing MCA M1 aneurysm. (B) Postoperative 3D
illustration showing trapping of the aneurysm and revascularization of distal MCA branches with RAG. (C, D) Postoperative left ICA angiogram showing filling of
the MCA vessel with RAG and delayed antegrade filling of ophthalmic artery through ICA. (M1-H) 16-year-old boy presenting with headache and 20 mm
aneurysm. (A) left ICA DSA and (B). 3D RA showing fusiform MCA M1 aneurysm with pre-bifurcation atherosclerotic narrowing. (C) Preoperative 3D illustration
showing partially thrombosed aneurysm and relation of aneurysm around vessels. (D) Postoperative 3D illustration showing clip reconstruction of aneurysm and
distal occlusion of aneurysm and RAG to the MCA M2. (E) DSA showing the graft filling distal MCA vessels.

bypasses in the patient who has not been prepared with aspirin for M2-M4 MCA Aneurysms
antiplatelet effect. A relatively proximal origin of the ATA in the Distal MCA aneurysms lend themselves more easily to intracranial
vertical part of the fissure in the pre-bifurcation M1 segment gives revascularization procedures. There is sufficient redundancy and
significant length, mobility, and options for revascularization tortuosity of the M2 and proximal M3 MCA branches once we split
procedures in comparison with distal origin of ATA in the hori- the fissure and release the arachnoidal adhesions. This lends us to
zontal part of the fissure from the MCA bifurcation. the primary resection end to end anastomosis, resection and
interposition graft with RAG and SAG, resection followed by side
to side anastomosis, reimplantation to maintain blood supply to
MCA-M1 Trunk Aneurysms the distal MCA branch. Aneurysms situated around the circular
In fusiform aneurysms of the MCA it is difficult to treat all the sulcus are deep in the fissure and make direct revascularization
MCA branches that arise from this segment, and the lenticulos- procedures challenging for distal M3, or M4 aneurysms.
triate arteries may be end arteries, without collateral circulation. In
our series of patients, a high-flow bypass was used in the majority
Strokes Related to Bypass
of patients, a direct interposition graft in 1 very young patient, and
Six patients suffered strokes as a result of the bypass and aneu-
resection and end to end anastomosis in one with a distal M1
rysm treatment and 2 had a persistent deficit at 3 months post-
aneurysm. We had more difficulties involving SVGs (M1-B, M1-C)
operatively (1 was improving, but died in the hospital of sepsis).
than RAGs (M1-A). In this series of patients, and an STA-MCA
Three of these strokes occurred earlier in our experience in pa-
bypass (M1-E) was not adequate for flow replacement, requiring
tients with EC-IC high-flow bypasses (M1-B, M1-C, MB-L) with
salvage with a RAG. After a distal bypass, flow can be preserved
SVG grafts, indicating a possibility of a learning curve in perfor-
through the lenticulostriate arteriess by clip reconstruction,
mance and conduit choice in patients with high-flow EC-IC by-
proximal or distal occlusion (rather than trapping) of the MCA to
passes. The causes of the strokes have been discussed (Tables 5
preserve flow. For this group of aneurysms endovascular flow
and 7), and the senior author believes that most of them are
diversion is an alternative.
avoidable.

MCA-M1 Bifurcation Aneurysms Aneurysm Recurrence after Microsurgical or Endovascular

M1 bifurcation aneurysms have multiple branches arising from the Treatment
bifurcation. If the entire bifurcation is aneurysmal and involves the Three of 43 aneurysms had a recurrence after aneurysm treatment
origin of both the branches, the senior author’s current preference and bypass (6.8%). Two MCA bifurcation aneurysms recurred after
is to trap the bifurcation and perform a Y-graft EC-IC from revascularization—one after EC-IC jump graft and clip recon-
external carotid artery to both branches of the MCA or EC-IC RAG struction and another after RAG to the inferior trunk. In both
to the larger inferior trunk and a STA to smaller superior trunk. If these patients there likely was some abnormal artery wall that
one branch can be spared by clip reconstruction, then the other went on to develop into an aneurysm. The dissection of these
one can be revascularized with a RAG. A RAG from the proximal aneurysms is difficult, and the prior clips can be used to guide the
STA (in the preauricular area) can be used to revascularize a dissection. In light of our overall experience, the M1 bifurcation
smaller M2 branch. It is better to avoid a local bypass whenever site is most prone to recurrence. Although clip reconstruction
possible in order to avoid putting 2 vessels at risk (MB K and MB- without bypass could be attempted in a good number of MCA
Q). All MCA branches must be reconstituted, in order to avoid a aneurysms, in a majority of these patients diseases atherosclerotic
stroke. This is a very difficult group of aneurysms for endovascular or aneurysmal arterial walls would need to be left unsecured to
reconstruction, due to the MCA bifurcation, or trifurcation. preserve inflow from the parent vessel and outflow to the

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Figure 3. (M1-I) 32-year-old man, incidentally diagnosed with 13 mm aneurysm. (A) 3D RA Right ICA injection showing fusiform right M1 aneurysm on
dolichoectatic M1 MCA. (B) Preoperative 3D illustration showing atherosclerotic disease of fusiform MCA M1 aneurysm. (C) Postoperative 3D illustration
showing resection and end-end anastomosis of aneurysm. (D) 3D CT angiogram showing complete obliteration of aneurysm and preservation of flow through
MCA vessels. (MB-A) 62-year-old woman with headche, 10 mm aneurysm. (A) Preoperative 3D illustration showing fusiform aneurysm of MCA bifurcation with
involvement of the superior branch of MCA. (B) Postoperative 3D illustration showing clip reconstruction of the aneurysm and reimplantation of superior trunk
into inferior trunk. (C) Postoperative DSA showing filling of both MCA branches. (MB-B) 59-year-old man with headche, 13 mm aneurysm. (A) 3D left ICA
injection showing fusiform bifurcation aneurysm. (B) Preoperative 3D illustration showing atherosclerotic neck with superior trunk densely adhered to the dome
of aneurysm. (C) Postoperative 3D illustration showing clip reconstruction of the aneurysm neck with RAG bypass to superior trunk. (D) DSA showing graft
perfusing distal MCA vessels. (MB-C) 48-year-old man, stenosis after MCA clipping. (A) Preoperative 3D illustration showing fusiform MCA bifurcation aneurysm
with adherence of one of the branches to the dome of aneurysm and both branches arising from neck of aneurysm. (B) Postoperative 3D illustration showing clip
reconstruction of the aneurysm with preservation of all branches. (C) DSA and (D) postoperative 3D illustration showing stenosis at the level of clip
reconstruction. (E) Postoperative 3D illustration after second surgery showing radial artery graft to superior trunk and occlusion of one branch. (F) Postoperative
DSA showing filling of branches through graft. (MB-D1) 53-year-old man presenting with headache with 15 mm aneurysm (A). DSA showing MCA bifurcation
aneurysm, both branches arising from neck of aneurysm. (B) Preoperative 3d illustration showing anatomy of the aneurysm and surrounding vessels. (C) Clip
reconstruction of aneurysm neck with RAG to one of the branches of MCA. (D) Postoperative DSA showing RAG and ICA filling MCA vessels. (MB-D2)
Vasculopathy of the radial artery graft, secondary to infection. Preoperative (A). DSA and (B). 3D illustration showing the stenosis of RAG. (C) Revision surgery
with resection and reanastomosis of graft. (D) Postoperative 3 D RA showing good filling of MCA vessels through graft.

branches, especially in the bifurcation aneurysms with branches CONCLUSIONS

originating from the neck of the aneurysm. If there is doubt, such Cerebral revascularization is an important adjunct to preserve
aneurysms should be treated with occlusion (or excision) with a Y- blood flow in MCA branches and thus allow occlusion of complex
bypass. Another M3 aneurysm recurred at the distal anastomotic MCA aneurysms, and can be done safely. There is a learning curve
site after IC-IC interposition bypass, probably because there was in decision-making and technical performance of the bypass. This
still pathological tissue at the distal anastomotic site. The exten- report reviews this learning curve, presents our results, and re-
sion of the pre-existing disease process in the residual aneurysms ports our insights into patient/bypass selection. In our patients,
is sometimes hard to judge at during operation. STA was not an adequate donor for flow replacement of MCA-M1,
Four patients in this series had aneurysms that recurred after MCA bifurcation, or large MCA-M2 branch. The ideal surgery in
endovascular treatment: 2 after multiple coiling sessions, 1 after such cases is an EC-IC bypass graft from external carotid artery to
single coiling, and 1 after Pipeline Embolization Device treatment. one or both branches of MCA-M2/3. RAGs were easier to perform
The difficulty of surgical treatment of these lesions is related to the technically due to the size match and had less immediate and
size of the aneurysm, and its location, M1 trunk or M1 bifurcation long-term complications when compared with SVGs. IC-IC bypass
being the most difficult. techniques are reserved for distal aneurysms or ATA revasculari-
zation and they have excellent results. The long-term patency rates
Algorithm for the Surgical Treatment of Unclippable MCA after bypass techniques are excellent.
Aneurysms
Based on the experience from this series of patients, the senior
author has developed an algorithm, which is shown as a flow chart
(Figure 9). ACKNOWLEDGMENT
We acknowledge Dr Richard Ellenbogen, Department of Neuro-
Previous Studies of Bypasses for MCA Aneurysms logical Surgery, University of Washington Medicine Neuroscience
Table 10 summarizes the previous reports of MCA Institute, and Chair, American Board, for his continuous support
revascularization with at least 10 reported bypass procedures and for the study and Jennifer Pryll, medical illustrator, for her illus-
compares them to our study. trative diagrams.

4. Ramanathan D, Starnes B, Hatsukami T, Kim LJ, 8. Pierot L, Costalat V, Moret J, et al. Safety and ef-
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Figure 4. (MB-E) 73-year-old man with 9 mm asymptomatic aneurysm. (A) DSA showing MCA bifurcation aneurysm. (B) Preoperative 3D illustration showing
atherosclerosis with involvement of both branches of MCA. (C, D) Postoperative 3D illustration showing clip reconstruction of aneurysm with radial artery jump
graft between both branches. (E) Postoperative DSA showing filling of both branch of MCA and obliteration of aneurysm. (MB-F) 56-year-old woman with
ruptured 8 mm aneurysm. (A) 3D RA showing MCA bifurcation aneurysm. (B) Clip reconstruction of the aneurysm with RAG with perfusion of MCA vessels. (C)
Postoperative 3D RA showing complete obliteration of the aneurysm and filling of distal MCA vessels with RAG. (MB-G) 67-year-old woman with ischemic
symptoms, 8 mm aneurysm. (A) 3D RA and (B). 3D illustration showing MCA bifurcation aneurysm with atherosclerosis neck and partial thrombosis. (C)
Postoperative 3D illustration showing clip reconstruction of the aneurysm with saphenous vein jump graft from MCA superior trunk to inferior trunk. (D) 3D RA
showing complete obliteration of the aneurysm and filling of MCA vessels. (E, F) Noncontrast head CT showing large anterior temporal lobe infarct. (MB-H) 40-
year-old woman with ruptured 10 mm aneurysm. (A) DSA showing fusiform MCA bifurcation aneurysm. (B) Preoperative 3D illustration showing a proximal MCA
branch adhered to dome of the aneurysm and other two branches arising from neck of the aneurysm. (C) Postoperative 3D illustration showing clip
reconstruction of MCA aneurysm with revascularization of MCA branch by end-end and side-side anastomosis. (D) AP DSA showing filling of all branches and
complete obliteration of aneurysm. (MB-I) 67-year-old man, incidentally diagnosed with 20 mm aneurysm. (A, B) 3D RA showing MCA bifurcation aneurysm and
both branches arising from neck of aneurysm. (C) Preoperative 3D illustration showing atherosclerotic disease of neck with partial thrombosis of aneurysm. (D)
Postoperative 3D illustration showing clip reconstruction of aneurysm with RAG to MCA M2 and side-side anastomosis. (E) Postoperative DSA showing filling of
distal MCA vessels with graft and complete obliteration of aneurysm. (MB-J1) 47-year-old man with headache, 9.5 mm aneurysm. (A) 3D RA, (B) DSA, and (C).
preoperative 3D illustration showing MCA bifurcation aneurysm with atherosclerotic neck with involvement of both branches from aneurysm neck. (D)
Postoperative 3D illustration showing clip reconstruction of the aneurysm and RAG from MCA to M2. (E) Postoperative DSA showing complete obliteration of
the aneurysm and filling of distal branches through graft. (MB-J2) Recurrence of aneurysm measuring 12 mm. (A) 3D RA. (B) AP view DSA right ICA injection. (C)
Preoperative 3D illustration showing recurrence of MCA aneurysm with stenosis of MCA just proximal to graft. (D) Postoperative 3D illustration after second
surgery showing double barrel bypass to both branches of MCA. (E) Post second surgery DSA showing filling of both branches of MCA by graft.

11. Kim FY, Marhefka G, Ruggiero NJ, Adams S, of the exact location in the MCA tree. J Neurosurg. assisted nonocclusive anastomosis technique.
Whellan DJ. Saphenous vein graft disease: review 2014;120:398-408. Neurosurgery. 2008;63:12-20 [discussion 20-2].
of pathophysiology, prevention, and treatment.
Cardiol Rev. 2013;21:101-109. 15. Matano F, Murai Y, Tateyama K, et al. Periopera-
tive complications of superficial temporal artery to Conflict of interest statement: The authors declare that the
12. Meybodi AT, Griswold D, Tabani H, et al. Topo- middle cerebral artery bypass for the treatment of article content was composed in the absence of any
graphic surgical anatomy of the parasylvian ante- complex middle cerebral artery aneurysms. Clin commercial or financial relationships that could be construed
rior temporal artery for intracranial-intracranial Neurol Neurosurg. 2013;115:718-724. as a potential conflict of interest.
bypass. World Neurosurg. 2016;93:67-72.
16. Safavi-Abbasi S, Kalani MYS, Frock B, et al. Received 22 December 2018; accepted 7 June 2019
13. Tayebi Meybodi A, Huang W, Benet A, Kola O, Techniques and outcomes of microsurgical man- Citation: World Neurosurg. (2019).
Lawton MT. Bypass surgery for complex middle agement of ruptured and unruptured fusiform https://doi.org/10.1016/j.wneu.2019.06.059
cerebral artery aneurysms: an algorithmic cerebral aneurysms. J Neurosurg. 2017;127:
approach to revascularization. J Neurosurg. 2017; 1353-1360. Journal homepage: www.journals.elsevier.com/world-
127:463-479. neurosurgery
17. van Doormaal TP, van der Zwan A, Verweij BH, Available online: www.sciencedirect.com
14. Kivipelto L, Niemela M, Meling T, Lehecka M, Han KS, Langer DJ, Tulleken CA. Treatment of
Lehto H, Hernesniemi J. Bypass surgery for giant middle cerebral artery aneurysms with a flow 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All
complex middle cerebral artery aneurysms: impact replacement bypass using the excimer laser- rights reserved.

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Figure 5. (MB-K1) 50-year-old woman with headache, 5mm aneurysm. (A) 3D CT angiogram showing right MCA bifurcation aneurysm. (B) Preoperative 3D
illustration showing complex nature of aneurysm, and origin of both branches from neck and tear in neck during dissection. (C) Postoperative 3D illustration
showing clip reconstruction of the aneurysm. (D) Postoperative DSA showing that inferior M2 branch is not filling. (E) ADC map of diffusion MRI showing right
frontotemporal stroke. (MB-K2) Graft thrombosis postoperative day 1. (A, B) Preoperative 3D illustration showing revision of previous anastomosis with STA-
MCA bypass and reimplantation. (C) 3D RA showing complete obliteration of aneurysm and filling of superior M2 branches from ECA and ICA. (D) ECA injection
shows the filling of one superior M2 branch from the STA bypass. (E) NCCT shows large frontotemporal infarct. (MB-L) 67-year-old woman with headache, 26
mm aneurysm. (A, B) 3D rotational angiogram and (C). preoperative 3D illustration showing large partially thrombosed previously coiled MCA bifurcation
aneurysm with involvement of both branches by the aneurysm. (D) Postoperative 3D illustration showing trapping of aneurysm and double barrel bypass to the
MCA vessel. (E) Postoperative DSA showing filling of RAG and SVG not filling. (F) ADC map showing stroke in region of basal ganglia. (MB-M) 57-year-old
woman with headache, 8 mm aneurysm. (A) DSA and (B) 3D RA showing MCA bifurcation aneurysm and previously coiled aneurysm. (C) Preoperative 3D
illustration showing anatomy and point of rupture during dissection of atherosclerotic aneurysm. (D, E) Postoperative 3D illustration showing resection of dome
of aneurysm, clip reconstruction of neck, radial artery jump graft between MCA-M2 branches. (F) Postoperative DSA showing complete obliteration of aneurysm
and filling of both branches of MCA. (MB-N) 72-year-old man, incidentally diagnosed with 5 mm aneurysm. (A, B) 3D RA showing MCA bifurcation aneurysm and
one of the branches arising from neck. (C) Postoperative 3D illustration showing clip reconstruction of aneurysm and revascularization of one branch with SVG.
(D) Postoperative 3D RA showing complete obliteration of aneurysm and filling of both branches of MCA. (MB-O) 45-year-old woman with recurrence after
clipping, 11 mm aneurysm. (A) 3D RA right ICA injection showing MCA bifurcation aneurysm and involvement of branches. (B) Postoperative 3D illustration
showing resection of aneurysm and previous clipping at the region of neck. (C) 3D illustration showing reclipping of resected aneurysm and RAG to the inferior
trunk of MCA. (D, E) Postoperative DSA showing complete obliteration of aneurysm with filling of distal MCA vessels with RAG.

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Figure 6. (MB-P) 53-year-old man with intracerebral hemorrhage after flow diversion. (A) MRI brain with contrast coronal view showing large partially
thrombosed aneurysm. (B) Left ICA DSA showing giant MCA aneurysm with multiple lobes with MCA vessels originating from the aneurysm. (C) CTA
reconstruction of left MCA immediately after pipeline device in the aneurysm. (D) DSA showing filling of the aneurysm despite the pipeline device. (E) NCCT
showing massive leak from aneurysm with mass effect. (F) 3D RA at the time of aneurysmal leak showing persistence of aneurysm despite the PED. (G)
Preoperative 3D illustration showing the pipeline device freely floating in the aneurysm. (H) Postoperative 3D illustration showing reconstruction of aneurysm
with trapping of aneurysm and STA graft to revascularize the distal MCA branches. (I) Postoperative DSA showing STA filling MCA branches. (MB-Q1) 23-year-
old woman presenting with headache, 12 mm aneurysm. (A, B) 3D RA showing MCA bifurcation aneurysm. (C) Preoperative 3D illustration showing
atherosclerotic dome and neck and involvement of both branches from neck of aneurysm. (D) Clip reconstruction of the aneurysm with saphenous vein jump
graft between MCA and M2 vessels. (E) 3D RA showing remnant of aneurysm with filling of MCA branches distal to SVG. (MB-Q2) Recurrence of aneurysm. (A)
DSA showing recurrence of aneurysm proximal and distal to previous anastomotic site. (B) Preoperative 3D illustration showing distal occlusion of aneurysm
with double barrel bypass. (C) Postoperative DSA showing delayed filling of aneurysm with filling of distal MCA vessels with double barrel bypass. (MB-R) 49-
year-old woman with ruptured 9 mm aneurysm. (A) DSA and (B). 3D illustration showing partially thrombosed MCA bifurcation aneurysm. (C) Postoperative 3D
illustration showing clip reconstruction of the aneurysm with narrowing of inferior trunk with revascularization of inferior trunk with RAG. (D) Postoperative DSA
showing filling of MCA branch from RAG and complete obliteration of aneurysm. (MB-S1) 67-year-old man with ischemic symptoms (clipped previously) with 18
mm aneurysm. (A) 3D RA showing recurrent MCA bifurcation aneurysm after clipping. (B) CTA coronal view showing partially thrombosed aneurysm. (C) DSA
showing communication between thrombosed and unthrombosed part. (D) 3D illustration showing complex partially thrombosed MCA aneurysm with
surrounding branches. (E) Postoperative 3D illustration showing clip reconstruction of the aneurysm with excision and reconstruction of aneurysmof thrombosed
segment. (MB-S2) Ischemic symptoms after bypass. (A) DSA showing delayed filling of the MCA inferior trunk. (B, C) 3D illustration showing thrombosis of
inferior MCA trunk. (D) EC-IC bypass from CCA using RAG. (D) Postoperative DSA showing complete obliteration of the aneurysm and filling of all vessels. (MB-
T) 45-year-old man presenting with recurrence of aneurysm after clipping, 13 mm aneurysm. (A) DSA showing MCA bifurcation aneurysm. (B) 3D RA and (C).
preoperative 3D illustration showing recurrence of aneurysm and all the branches arising from the dome of aneurysm. (D) Postoperative 3D illustration showing
double barrel bypass and excision of the aneurysm. (E) Postoperative DSA showing filling of distal MCA vessels with double barrel bypass with complete
obliteration of the aneurysm.

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Figure 7. (M2-A) 58-year-old woman incidentally diagnosed with 7 mm aneurysm. (A) 3D RA showing MCA bifurcation aneurysm of superior trunk of MCA. (B)
3D illustration showing fusiform aneurysm of M2 with origin of perforators at proximal neck of aneurysm. (C) 3D illustration showing occlusion of aneurysm with
reimplantation of superior trunk on inferior trunk. (D) Postoperative 3D RA showing filling of the MCA branches with complete obliteration of aneurysm. (M2-B)
81-year-old woman with intracerebral hemorrhage, 9 mm aneurysm. (A) 3D RA showing fusiform distal M2 aneurysm. (B) 3D illustration showing fusiform
aneurysm of distal M2. (C) Postoperative 3D illustration showing resection and end to end anastomosis of aneurysm. (D) 3D RA complete obliteration of
aneurysm with persistent filling of distal branches. (M2-C) 48-year-old man complaining of headache, 11 mm aneurysm. (A, B) Preoperative angio showing
fusiform aneurysm of superior trunk of MCA. (C) 3D illustration showing fusiform aneurysm of superior trunk of MCA. (D) 3D illustration showing resection and
interposition radial artery graft in aneurysmal bearing segment. (E) Postoperative DSA showing complete obliteration of aneurysm and persistent filling of distal
MCA branches. (M3-A) 48-year-old man with headache, 10 mm aneurysm. (A, B) DSA and 3D RA showing M3 distal fusiform aneurysm. (C) Postoperative 3D
illustration showing STA bypass distal to aneurysm and 2 MCA branches going into the aneurysm. (D) Right ECA DSA with STA filling the superior trunk of MCA.
(E) Postoperative DSA showing complete obliteration of the aneurysm and antegrade filling of inferior trunk of MCA. (M3-B1) 14-year-old boy with headache, 16
mm aneurysm. (A) DSA, (B) 3D RA, and (C) preoperative 3D illustration showing distal fusiform M3 aneurysm with branches arising from the aneurysm. (D)
Postoperative 3D illustration showing radial artery interposition graft in aneurysm bearing segment. (E) Postoperative DSA showing complete obliteration of the
aneurysm and filling of all branches. (M3-B2) recurrence of aneurysm. (A) DSA showing recurrence of the aneurysm at distal anastomotic site. (B) Preoperative
3D illustration showing relation of the aneurysm with graft. (C) Postoperative 3D illustration showing lingual artery interposition graft. (D) Postoperative DSA
showing revascularized MCA branches with arrow. (M3-C) 38-year-old man with ruptured 7 mm aneurysm. (A, B) DSA and 3D RA showing M3 distal fusiform
aneurysm. (C) Postoperative 3D illustration showing STA-MCA bypass distal to aneurysm bearing segment. (D, E) Postoperative DSA showing STA filling the
vessel distal to aneurysm bearing segment and complete obliteration of the aneurysm.

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SABAREESH K. NATARAJAN ET AL. BRAIN BYPASS SURGERY FOR COMPLEX MCA ANEURYSMS

Figure 8. (M3-D) Recurrence of aneurysm after clipping. (A) NCCT showing showing complex nature of aneurysm and clot around aneurysm. (D)
hemorrhage in right sylvian fissure. (B) 3D RA showing distal MCA Postoperative 3D illustration showing excision of the aneurysm and STA
aneurysm. (C) 3D illustration showing previous clip and atherosclerosis at donor to revascularize distal MCA vessels. (E) Right ECA, and (F) right ICA
the origin of the MCA branches from neck. (D) Postoperative 3D illustration DSA showing filling of the branch distal to the aneurysm from STA and
showing resection of the aneurysm and radial artery graft to revascularize complete obliteration of the aneurysm. (M3-G) 28-year-old woman with
distal MCA vessels. (E) 3D RA showing complete obliteration of the ischemic symptoms, 36 mm aneurysm. (A, B) DSA/3D RA showing
aneurysm and filling of all MCA branches. (M3-E) 8-year-old boy with complex multilobed MCA aneurysm. (C) Preoperative 3D illustration
ruptured 7 mm aneurysm. (A, B) 3D RA showing M3 distal fusiform showing the fusiform aneurysm and surrounding branches. (D)
aneurysm. (C) 3D illustration showing fusiform nature of aneurysm, Postoperative 3D illustration showing excision of the aneurysm and
previous clip/adherence of branches to the dome of the aneurysm. (D) revascularization of distal vessels with radial artery jump graft. (E, F) Lateral
Postoperative 3D illustration showing excision of aneurysm, view DSA showing filling of distal MCA branches and complete obliteration
revascularization of distal branches with combination of radial artery of aneurysm. (M4) 55-year-old man with headache, 9 mm aneurysm. (A) 3D
interposition graft and reimplantation. (E) 3D RA showing complete RA showing left fusiform distal MCA aneurysm. (B) Preoperative 3D
obliteration of the aneurysm and filling of all MCA branches. (M3-F) illustration showing fusiform nature of the aneurysm and resection and
55-year-old woman with ischemic symptoms, 3 mm aneurysm. (A) Brain end-end anastomosis of the aneurysm followed by revision of anastomosis.
MRI T1 axial image without contrast showing ruptured MCA aneurysm. (B) (C) Postoperative 3D RA of left ICA showing complete obliteration of the
3D RA showing distal MCA aneurysm. (C) Preoperative 3D illustration aneurysm and filling of distal MCA vessels.

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SABAREESH K. NATARAJAN ET AL. BRAIN BYPASS SURGERY FOR COMPLEX MCA ANEURYSMS

Table 9. Early versus Late Cases

Group A (2005e2011) Group B (2012e2018)

Bypass procedures 31/52 (60%) Bypass procedures 21/52 (40%)

EC-IC high flow 13/31 (42%) EC-IC high flow 7/21 (33%)
EC-IC low flow 4/31 (13%) EC-IC low flow 4/21 (19%)
IC-IC 14/31(44%) IC-IC 10/21 (48%)
Grafts (RAG ¼ 16, SVG ¼ 8) Grafts (RAG ¼ 9, SVG ¼ 4)
Graft related problems 5 Graft related problems 1
Strokes 5/6 (84%) Stroke 1/6(16%)
Complete recovery 3 (50%) Complete recovery 1 (100%)

EC-IC, extracranial-intracranial; IC-IC, intracranial-intracranial; MCA, middle cerebral ar-

tery; RAG, radial artery graft; STA, superficial temporal artery; SVG, saphenous vein
graft.

Figure 9. Proposed algorithm for the treatment of complex MCA aneurysms.

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SABAREESH K. NATARAJAN ET AL. BRAIN BYPASS SURGERY FOR COMPLEX MCA ANEURYSMS

Table 10. Previously Published Studies with at Least 10 Bypass Procedures

No. of EC-IC High FU Duration Bypass Aneurysm Stroke
Author Year Bypasses Flow STA-MCA IC-IC months patency % obliteration % n/N (%)

Current series 2018 52 20 8 24 124 98 100 6/43 (14)

Meybodi13 2017 30 4 8 13 28 90 97 3/30 (10)
14
Kivipelto 2014 24 1 20 4 27 92 96 6/25 (25)
Matano15 2013 10 0 10 0 NA 80 NA 5/10 (50)
Kalani16 2013 16 3 13 0 58 94 75 3/16 (19)
17
Van Doormaal 2008 22 2 0 20 43 86 100 8/22 (36)

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