Brain Bypass Surgery for Complex Middle Cerebral Artery Aneurysms: Evolving Techniques, Results, and Lessons Learned

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 with middle cerebral artery (MCA) aneurysms who needed an adjunctive cerebral revascularization procedure to achieve aneurysm occlusion with preservation of flow through all MCA branches.

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METHODS: A total of 42 patients with 43 MCA aneurysms underwent 52 bypass procedures over 13 years. The location of the aneurysm were M1 trunk, M1 bifurcation, M2 and beyond. The bypasses performed included intracranial bypasses (resection with end to end anastomosis, end to side implantation, side to side anastomosis, and short interposition graft), extraintracranial bypasses (superficial temporal to middle cerebral artery anastomosis, and radial artery bypass graft, or saphenous vein graft), double bypasses, Y-grafts, and combined techniques.

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RESULTS: Forty-two of 43 aneurysms (98%) had patent bypasses at long-term follow-up. All 43 aneurysms were completely occluded at last follow-up. Six patients (14%) developed strokes related to the surgical treatment. At last follow-up, 36 patients had a modified Rankin score of 0e2, 5 patients had modified Rankin score 3e5, and 1 died. In this series, 31 (73.8%) patients improved, 8 (19%) patients had same functional status, and 3 (7.2%) patients deteriorated, including 1 patient who expired due to sepsis. The mean clinical follow-up duration was 39.3

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Key words Cerebral revascularization - Endovascular management - Graft occlusion - High flow bypass - Middle cerebral artery aneurysms - Radial artery graft - Saphenous vein graft -

Abbreviations and Acronyms ATA: Anterior temporal artery bifurcation DSA: Digital subtraction angiography EC-IC: Extracranial-intracranial EEG: Electroencephalogram IC-IC: Intracranial-intracranial ICA: Internal carotid artery MCA: Middle cerebral artery MEP: Motor evoked potentials NCCT: Noncontrast computed tomography PED: Pipeline Embolization Device

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months (0.4e124 months) and the mean radiological follow-up was 37 months (0.4e134 months). CONCLUSIONS: Cerebral revascularization is an important adjunct for treating MCA aneurysms and can be done safely. The article provides the insights we gained by rising through the learning curve.

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INTRODUCTION

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 procedures. Common characteristics that make simple clip reconstruction difficult include: Branches arising from aneurysm neck or dome, extensive atherosclerotic disease at the neck, previous endovascular treatment, large or giant size (>15 mm diameter), fusiform aneurysms, and considerable intra-aneurysmal thrombosis. The majority of bypasses can be anticipated before surgery. In a few patients, a significant branch stenosis may be found after clipping (after attempts to reposition the clip have been exhausted) and may require a bypass procedure. The recurrence of a large or giant aneurysm after previous treatment often requires a bypass. In this consecutive series we examined the results and complications

RAG: Radial artery graft SAH: Subarachnoid hemorrhage SSEP: Somatosensory evoked potential STA: Superficial temporal artery SVG: Saphenous vein graft From the 1Department of Neurosurgery, University of Massachusetts Medical School, Massachusetts; and Departments of 2Neurosurgery, and 3Radiology, University of Washington, Seattle, Washington, USA To whom correspondence should be addressed: Laligam N. Sekhar, M.D. [E-mail: [email protected]] Sabareesh K. Natarajan, and Qazi Zeeshan contributed equally to this work. Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.06.059 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.

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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 aneurysms over 13 years. This includes a period of time before the US Food and Drug Administration approval of a flow diversion stent (the Pipeline Endovascular Device [Medtronic, Minneapolis, Minnesota, USA]). Flow diversion stents (off-label) have been used for complex MCA aneurysms with varying results.1,2

METHODS All patients had been operated by the senior author (L.N.S.), and the review was performed after the approval from the institutional review board. Individual patient consent was not sought. The review included patient charts, radiographic studies, and, when needed, telephonic follow-up. Operative drawings made by the senior author were redrawn by a medical illustrator. Statistical analysis was done using SPSS software (IBM, Armonk, NY). In many of these cases, an experienced neurointerventionist was also involved in the decision-making process. In addition to consultations between the 2 physicians, when there is equipoise, the patient is given the ability to make the choice of treatment. The final decision to proceed with the bypass was made during the surgery after inspection of the aneurysms, 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

Table 1. Demographics, Presentation and Location of Aneurysms Total patients

42

Total aneurysms

43

Total bypasses

52

Ruptured

13

Hunt and Hess grade 1e3, n

9

Hunt and Hess grade 4e5, n

4

Unruptured, (n)

30

Sex Male

26

Female

16

Location ATA

3

RESULTS Forty-two patients with 43 aneurysms underwent 52 bypass procedures from 2005 to 2018. There were 9 M1 aneurysm patients who underwent 13 operations; 20 M1 bifurcation aneurysms patients underwent 24 operations (2 for recurrences, and 2 for graftrelated problems); 3 M1 ATA aneurysm patients had 3 operations; 3 M2 aneurysms underwent 3 operations; and 8 patients with M3/ M4 aneurysms had 12 bypass operations (one patient has 2 aneurysms on either side).

Table 2. Complications and Graft Patency Complication

n/N

Stroke

6/44

Complete recovery

4/6

Hematoma (epidural, subdural, or intraparenchymal)

3

Infection

2

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

ATA, anterior temporal artery bifurcation.

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radial artery or the saphenous vein was generally used for replacement of the M1 or large M2 vessels. For smaller arteries, small interposition grafts, a side to side anastomosis, a reimplantation, or a superficial temporal artery (STA) to MCA branch bypass was used. Aspirin 325 mg orally was given 1 week before planned surgery and the same dose was given per rectum in emergent cases. Total intravenous anesthesia with propofolinduced burst suppression and permissive hypertension during temporary flow arrest was performed with neuromonitoring including somatosensory evoked potential, motor evoked potential, and electroencephalogram. Patients received 5000 U of heparin intravenously before temporary low arrest and the actual bypass procedure. Most recent patients underwent an indocyanine green angiogram and micro Doppler studies postoperatively, and all patients underwent a digital subtraction angiography postoperatively. Bypass techniques evolved during the study period, with a greater preference for radial artery grafts for major vessel replacement, as opposed to saphenous vein grafts and have been described by the senior author in various papers before.3,4 The aneurysms were divided into: M1 segment, M1 bifurcation, M1 at anterior temporal artery bifurcation (ATA), and beyond M2.

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Immediate (after revision)

42/43 (97.6%)

Long term

42/43 (97.6%)

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ORIGINAL ARTICLE SABAREESH K. NATARAJAN ET AL.

BRAIN BYPASS SURGERY FOR COMPLEX MCA ANEURYSMS

There were 20 (38.4%) extracranial-intracranial (EC-IC) highflow bypass (radial artery graft [RAG]: 11, saphenous vein graft [SVG]: 6, and RAGþSVG: 3), 8 (15.5%) EC-IC low bypass (direct STA MCA: 5, RAG/SVG interposition graft from STA: 3) and 24 (46.1%) intracranial bypasses. Thirty-six of the aneurysms presented de novo, 3 were recurrent after previous surgery, and 4 were recurrent after prior coiling or flow diversion procedures. Table 1 summarizes the demographics, presentation, and procedure performed. Table 2 summarizes overall complications and graft patency. Tables 3e8 summarize the treatment, outcomes, and complications of M1 segment, M1 bifurcation, M1 at ATA, and beyond M2 segment aneurysms, respectively. Figures 1e8 are a collage of the preoperative imaging, technique illustration, and postoperative imaging of all patients with salient comments for review. Stroke Based on magnetic resonance imaging scans, 6 (of 42, 14%) patients (M1-B; M1-C; M1-E; MB-K1 and MB-K2; MB-L MB-Q1, Figures 1e8) suffered strokes during or after the operation. All of them were either MCA-M1(M1-B; M1-C; M1-E) or bifurcation 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 remaining were encountered in intracranial-intracranial (IC-IC) 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 hospital (Table 5 and 7, Figures 1e8).

Graft-Related Problems Saphenous vein conduit was used for 9 high-flow EC-IC bypasses. Of these, 6 were pure SVG, and 3 were part of a Y-bypass. Four of these (M1-C, MB-K1, MB-K2, MB-L MB-Q1, Figures 1e8) developed some problem during or after the bypass requiring revision. All were patent eventually, albeit with significant stenosis in one. RAG was used in 15 EC-IC high flow bypasses-12 pure and 3 Y-bypasses and 1 patient (M1-A) developed asymptomatic graft occlusion 18 months later. Forty-two of 43 aneurysms (98%) had patent bypasses at long-term follow-up. Details of graft complications are summarized in Tables 5 and 7 and Figures 1e8. Early versus Late Cases All the cases treated were divided in 2: 2005e2011(group A) and 2012e2018 (group B); results are summarized in Table 9. The complications may have been reduced in the latter half thanks to improvements in bypass techniques, management of perioperative anticoagulation, and better patient-graft matching. Table 4. Treatment and Outcome of M1 Trunk Aneurysms Treatment and Outcome

n

Total number of aneurysms (patients n ¼ 9)

9

Type of aneurysms 1. Fusiform

7

2. Fusiform with some eccentric outpouching

Table 3. Treatment and Outcome of M1 Aneurysm at the Anterior Temporal Branch

2

Total bypasses

13

SAH

2

Treatment/Outcome

n

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

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

1

Proximal partial occlusion and EC-IC RAG

1

Complete trapping and EC-IC RAG

1

Excision and STA-MCA Patency

3/3 (100%)

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

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

EC-IC, extracranial-intracranial; IC-IC, intracranial-intracranial; MCA, middle cerebral artery; mRS, modified Rankin Scale; SAH, subarachnoid hemorrhage; STA, superficial temporal artery.

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Complications: see Table 5 EC-IC, extracranial-intracranial; IC-IC, intracranial-intracranial; MCA, middle cerebral artery; mRS, modified Rankin Scale; RAG, radial artery graft; SAH, subarachnoid hemorrhage; STA, superficial temporal artery; SVG, saphenous vein graft.

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BRAIN BYPASS SURGERY FOR COMPLEX MCA ANEURYSMS

DISCUSSION This is the largest series that has been reported to date of patients who underwent cerebral revascularization for MCA aneurysms. Our series is unique in that all modalities of bypass including high-flow, STA-MCA, and IC-IC were used equally depending on the flow replacement needed in each case. A good number of the proximal aneurysms in M1, MCA bifurcation had a high-flow

Table 5. Complications of M1 Trunk Aneurysms M1- M1 stenosis and fusiform aneurysm Developed an asymptomatic graft A underwent an RAG and clipping of a occlusion 18 months later. saccular portion of the aneurysm. Angiography revealed the enlargement of collaterals, and good reconstitution of all M2 branches. M1- Underwent an SVG and trapping of B a partially calcified flask shaped aneurysm. During the surgery, an inferior and smaller M2 branch Which was arising from the aneurysm was not revascularized because there was very good backflow from the distal stump. This patient developed a temporal lobe infarct.

Required an anterior temporal lobectomy urgently. He recovered completely, and has completed high school.

M1- SVG and trapping an aneurysm,poor She was explored, and was found C flow postoperatively, with a small to have an abnormally oriented stroke in the temporal area. valve, which was removed. She recovered well, with patency of the graft. 11 months later, she developed transient ischemic attacks and ischemia, and was found to have developed a stenosis at the previous repair site. She was explored, and had a segmental vein graft replacement; 23 months later, she had recurrent ischemic symptoms, and was found to have restenosis of the SVG. During a reoperation, an ATA was placed from the proximal SVG to an M2 branch bypassing the area of stenosis, and then the stenotic area of the SVG was resected, and replaced with an ATA graft. She remains free of symptoms, and both grafts are patent on CTA, 96 months after this operation. M1- Ruptured fusiform MCA aneurysm E underwent a double barrel bypass with a large STA, followed by proximal occlusion.

Postoperatively, delayed filling of bypass, and evidence of cortical strokes. Radial artery graft was placed into the M2 branch proximal to the STA bypass. Suffered hemispheric strokes, but recovered, albeit with some dependency for daily activates (mRS 3).

ATA, anterior temporal artery bifurcation; CTA, computed tomography angiography; mRS, modified Rankin Scale; RAG, radial artery graft; SVG, saphenous vein graft.

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bypass, which is much higher than any other series reported in literature with comparable complication rates and complete aneurysm obliteration rates. The follow-up on these patients is the longest reported when compared with any other series. The patient cohort in this series can be separated into 2 cohorts—patients who needed a high-flow replacement of M1 or 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 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, SVG n ¼ 6). The second cohort had predominantly 11 IC-IC bypass procedures with or without a conduit and 4 EC-IC bypass using STA as a donor. Endovascular Management Aneurysms around the MCA are technically challenging targets for endovascular treatment because of their distal location, multiple Table 6. Treatment and Outcome of MCA Bifurcation Aneurysms Treatment and Outcome

n

Total number of aneurysms (patients n ¼ 20)

20

Total bypasses

24

SAH

8

Treatment Clip reconstruction and EC-IC SVG

1

Clip reconstruction and EC-IC RAG

7

Clip reconstruction and EC-IC STA-MCA

3

Clip reconstruction and IC-IC, reimplantation

1

Clip reconstruction and IC-IC, jump graft

5

Y-graft bypass

3

Clip reconstruction and IC-IC, reimplantation and side to side bypass

1

Bypass patency, long term

(20/20) 100%

Aneurysm occlusion

(20/20) 100%

Outcome mRS 0e2

15

mRS 3e5

4

mRS 6

1

mRS improved

10

mRS same

7

mRS deteriorated

3

Complications: see Table 7 EC-IC, extracranial-intracranial; IC-IC, intracranial-intracranial; MCA, middle cerebral artery; mRS, modified Rankin Scale; RAG, radial artery graft; SAH, subarachnoid hemorrhage; STA, superficial temporal artery; SVG, saphenous vein graft.

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ORIGINAL ARTICLE SABAREESH K. NATARAJAN ET AL.

BRAIN BYPASS SURGERY FOR COMPLEX MCA ANEURYSMS

branches, ATA, or lenticulostriate branches. Flow diversion is an option for M1 aneurysms when there is a good proximal (distal to the internal carotid artery [ICA] terminus) and distal landing zone (proximal to the MCA bifurcation). Stent-assisted coil reconstruction of wide-neck MCA bifurcation aneurysms is often required for complex MCA bifurcation aneurysms but they are technically challenging procedures given that they need delivery of a stent through the tortuous MCA vessels,

Table 7. Complications of M1 Bifurcation Aneurysm MB-D

Suffered a postoperative epidural This patient developed a delayed infection, requiring the removal of narrowing of a radial artery graft a bone flap and antibiotics. 4 months later. He was successfully managed by means of segmental graft resection and anastomosis.

MB-K1 Ruptured MCA aneurysm had and severe narrowing of one M2 MB-K2 branch after clipping She was treated initially by a side to side anastomosis between 2 M2s. However, the narrowed branch and anastomosis clotted, with a stroke.

Was explored, and a reimplantation and STA-MCA branch anastomosis was done in an attempt to revascularize the clotted artery. The STA-MCA bypass was partially successful, but the patient suffered a significant right hemispheric stroke, with eventual recovery to an mRS 3.

Patient with a giant MCA aneurysm had multiple coiling procedures previously, and presented with an enlarging aneurysm, and headaches. She underwent a RAG to one M2 branch, and a SVG to another large M2 branch followed by proximal occlusion. During surgery, and attempt was made to extract the coils, and clip/or trap the aneurysm. At this time, her MEPs and SSEPs deteriorated, and did not recover.

She had a postoperative capsular stroke, with hemiparesis, but was recovering. Three days postoperatively, she sustained a pneumonia related to COPD and nosocomial infection in the intensive care unit. She progressed to systemic sepsis and died.

MB-Q1 Patient with a large MCA bifurcation aneurysm presented with TIAs in the MCA distribution. The aneurysm was clipped. However, since one M2 was severely narrowed, and short SVG was placed between the two M2 branches.

She did well initially, but developed a subdural and subarachnoid hemorrhage due to persistent oozing from her anastomotic site, presumably due to a combination of aspirin, and subcutaneous heparin.She was explored, the clot was removed, but the graft was also found to be partially thrombosed. A thrombectomy was done successfully. She suffered a cortical infarct, but recovered at 6 months to a mRS 1.

MB-L

often require distal dual access for stent delivery and jailed microcatheter assisted coiling, and have a high complication rate.5 The latest iteration of the Neuroform Atlas Stent (Stryker Neurovascular, Fremont, CA) makes this easier as they can be delivered through a 0.16 micro catheter; and coiling can usually be done through the stent tines with the same micro catheter, thereby reducing the necessity of multiple access and catheter 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 branch have not been studied.7 Intra-saccular flow diversion is also being tested for MCA bifurcation aneurysm but this is not yet approved for use in the United States by the US Food and Drug Administration.8 Ruptured aneurysms preclude a stent implantation (and dual antiplatelet therapy) in the acute stage and these patients are preferentially treated by microsurgical techniques. In patients with poor grade subarachnoid hemorrhage or patients who are not good surgical candidates, partial coiling of the aneurysm in the acute stage, followed by definitive treatment 2e3 weeks after subarachnoid hemorrhage may be performed. During the second stage, parent vessel flow diversion with jailing of 1 MCA branch, Table 8. Treatment and Outcome of M2 and Beyond Aneurysms Treatment and Outcome Total number of aneurysms (patients n¼10)

11

Total bypasses

12

SAH

2

Treatment Partial distal occlusion and IC-IC bypass (reimplantation)

1

Resection and end-to-end anastomosis IC-IC bypass

1

Resection and interposition radial artery graft

1

Resection and end-end anastomosis, IC-IC

2

Resection and STA-MCA bypass, EC-IC

3

Resection and interposition RAG, IC-IC

3

Reconstruction bypass with lingual artery

1

Resection and IC-IC jump graft

1

Bypass patency, long term

12/12 (100%)

Aneurysm occlusion

12/12 (100%)

Outcome mRS 0e2

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10

mRS 3e5

0

mRS improved

10

mRS same

0

mRS deteriorated

0

Complications COPD, chronic obstructive pulmonary disease; MCA, middle cerebral artery; MEP, motor evoked potentials; mRS, modified Rankin Scale; RAG, radial artery graft; SSEP, somatosensory evoked potential; STA, superficial temporal artery; SVG, saphenous vein graft; TIA, transient ischemic attack.

n

None

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

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BRAIN BYPASS SURGERY FOR COMPLEX MCA ANEURYSMS

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ORIGINAL ARTICLE SABAREESH K. NATARAJAN ET AL.

BRAIN BYPASS SURGERY FOR COMPLEX MCA ANEURYSMS

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. (M1B) 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 shield technology9 may be used as treatment options. EC-IC RAG/SVG versus EC-IC STA In this series, the STA was used to revascularize the MCA territory in 2 patients (M1-E1, and MB-P). In both patients, the STA was selected because of its large size (>1 mm in diameter). In patient M1-E1, a double-barrel bypass was performed. It proved to be inadequate, the patient developed a stroke in the MCA territory, and this patient was salvaged by using a RAG. Traditionally, the STA grafts have shown to deliver less than 50 mL/minute and the 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 bypasses. In the senior author’s experience, the STA does not reliably have adequate flow to replace the entire MCA territory or even the territory of the larger inferior trunk. STA can only be used as a donor to replace a smaller MCA branch, the M3/M4 branches, or in patients who already have a large infarct in the MCA territory. The University of Illinois group has proposed measuring native blood flow using magnetic resonance angiography NOVA and cut flow index from the STA to make a treatment decision regarding flow replacement bypass. They have stated that MCA flow replacement needs only 50 mL/minute; and when a SVG graft is placed from the proximal STA in the zygomatic area it can provide adequate flow replacement to the MCA territory.4,10 RAG versus SVG Grafts for EC-IC High-Flow Bypass In this series of patients, we had more problems with SVGs than our RAGs, particularly relating to valves and kinking. The main proposed reasons for the SVG problems are the presence of valves, low kink resistance, the size and volume mismatch, and their inability to remodel to the desired flow in the recipient vessel.11 The potential problems with choosing RAG as a conduit are graft spasm, size below 2.5 mm, prior use for radial artery lines, and the absence of an adequate palmar arch in some patients. The problem of vasospasm has been eliminated by the senior author by the pressure distention technique.3 The RAG has

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better kink resistance in the preauricular tunnel and at the 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, or the desire to avoid extraction of the RAG in some young patients. We prefer to route our SVG behind the ear in a retromastoid bony tunnel to avoid kinking. We have reported using the anterior tibial artery as conduit before8 and presently believe that the anterior tibial artery is a better conduit than the SVG in patients who do not have a RAG conduit. However, its extraction takes more time, and requires the collaboration of a vascular surgeon. IC-IC Bypass Local bypasses such as reimplantation and side to side anastomosis may be used to revascularize small MCA branches, resuture of a vessel may be used when the vessels are redundant in length, and a short interposition graft may also be used, when the gap between the 2 vessel ends is too long for the vessel to be sutured without tension. Such bypasses are very useful for small arteries, but also when the bypass is unplanned in the situation of a ruptured aneurysm. However, as seen in our patient MB-K, when a local bypass (side to side in this patient) fails, it risks both vessels. When technically well performed, the main reason for such failure may be the lack of antiplatelet activity, or a hypercoagulable state. MCA ATA Aneurysm The need to revascularize the ATA is not proven. Moybedi et al.12 have reported a series where they used the ATA as a donor for ICIC revascularization. Sacrifice of the anterior temporal artery always leads to an anterior temporal lobe infarct, but the infarct may be small, or large and cause a functional deficit, particularly on the speech-dominant side. The senior author prefers to revascularize the ATA when it is possible to avoid postoperative functional deficits. The different options for revascularizing ATA are reimplantation, side to side anastomosis with another MCA branch, or STA-ATA bypass. The STA-ATA bypass is preferred in patients with ruptured aneurysms because of the risk of thrombosis of local

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BRAIN BYPASS SURGERY FOR COMPLEX MCA ANEURYSMS

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ORIGINAL ARTICLE SABAREESH K. NATARAJAN ET AL.

BRAIN BYPASS SURGERY FOR COMPLEX MCA ANEURYSMS

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 STAMCA 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 endto-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 antiplatelet effect. A relatively proximal origin of the ATA in the vertical part of the fissure in the pre-bifurcation M1 segment gives significant length, mobility, and options for revascularization procedures in comparison with distal origin of ATA in the horizontal part of the fissure from the MCA bifurcation. MCA-M1 Trunk Aneurysms In fusiform aneurysms of the MCA it is difficult to treat all the MCA branches that arise from this segment, and the lenticulostriate arteries may be end arteries, without collateral circulation. In our series of patients, a high-flow bypass was used in the majority of patients, a direct interposition graft in 1 very young patient, and resection and end to end anastomosis in one with a distal M1 aneurysm. We had more difficulties involving SVGs (M1-B, M1-C) than RAGs (M1-A). In this series of patients, and an STA-MCA bypass (M1-E) was not adequate for flow replacement, requiring salvage with a RAG. After a distal bypass, flow can be preserved through the lenticulostriate arteriess by clip reconstruction, proximal or distal occlusion (rather than trapping) of the MCA to preserve flow. For this group of aneurysms endovascular flow diversion is an alternative. MCA-M1 Bifurcation Aneurysms M1 bifurcation aneurysms have multiple branches arising from the bifurcation. If the entire bifurcation is aneurysmal and involves the origin of both the branches, the senior author’s current preference is to trap the bifurcation and perform a Y-graft EC-IC from external carotid artery to both branches of the MCA or EC-IC RAG to the larger inferior trunk and a STA to smaller superior trunk. If one branch can be spared by clip reconstruction, then the other one can be revascularized with a RAG. A RAG from the proximal STA (in the preauricular area) can be used to revascularize a smaller M2 branch. It is better to avoid a local bypass whenever possible in order to avoid putting 2 vessels at risk (MB K and MBQ). All MCA branches must be reconstituted, in order to avoid a stroke. This is a very difficult group of aneurysms for endovascular reconstruction, due to the MCA bifurcation, or trifurcation.

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M2-M4 MCA Aneurysms Distal MCA aneurysms lend themselves more easily to intracranial revascularization procedures. There is sufficient redundancy and tortuosity of the M2 and proximal M3 MCA branches once we split the fissure and release the arachnoidal adhesions. This lends us to 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 the distal MCA branch. Aneurysms situated around the circular sulcus are deep in the fissure and make direct revascularization procedures challenging for distal M3, or M4 aneurysms. Strokes Related to Bypass Six patients suffered strokes as a result of the bypass and aneurysm treatment and 2 had a persistent deficit at 3 months postoperatively (1 was improving, but died in the hospital of sepsis). Three of these strokes occurred earlier in our experience in patients with EC-IC high-flow bypasses (M1-B, M1-C, MB-L) with SVG grafts, indicating a possibility of a learning curve in performance and conduit choice in patients with high-flow EC-IC bypasses. The causes of the strokes have been discussed (Tables 5 and 7), and the senior author believes that most of them are avoidable. Aneurysm Recurrence after Microsurgical or Endovascular Treatment Three of 43 aneurysms had a recurrence after aneurysm treatment and bypass (6.8%). Two MCA bifurcation aneurysms recurred after revascularization—one after EC-IC jump graft and clip reconstruction and another after RAG to the inferior trunk. In both these patients there likely was some abnormal artery wall that went on to develop into an aneurysm. The dissection of these aneurysms is difficult, and the prior clips can be used to guide the dissection. In light of our overall experience, the M1 bifurcation site is most prone to recurrence. Although clip reconstruction without bypass could be attempted in a good number of MCA aneurysms, in a majority of these patients diseases atherosclerotic or aneurysmal arterial walls would need to be left unsecured to preserve inflow from the parent vessel and outflow to the

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BRAIN BYPASS SURGERY FOR COMPLEX MCA ANEURYSMS

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 originating from the neck of the aneurysm. If there is doubt, such aneurysms should be treated with occlusion (or excision) with a Ybypass. Another M3 aneurysm recurred at the distal anastomotic site after IC-IC interposition bypass, probably because there was still pathological tissue at the distal anastomotic site. The extension of the pre-existing disease process in the residual aneurysms is sometimes hard to judge at during operation. Four patients in this series had aneurysms that recurred after endovascular treatment: 2 after multiple coiling sessions, 1 after single coiling, and 1 after Pipeline Embolization Device treatment. The difficulty of surgical treatment of these lesions is related to the size of the aneurysm, and its location, M1 trunk or M1 bifurcation being the most difficult. Algorithm for the Surgical Treatment of Unclippable MCA 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). Previous Studies of Bypasses for MCA Aneurysms Table 10 summarizes the previous reports of MCA revascularization with at least 10 reported bypass procedures and compares them to our study.

REFERENCES 1. Iosif C, Mounayer C, Yavuz K, et al. Middle cerebral artery bifurcation aneurysms treated by extrasaccular flow diverters: midterm angiographic evolution and clinical outcome. AJNR Am J Neuroradiol. 2017;38:310-316. 2. Machi P, Lobotesis K, Vendrell JF, et al. Endovascular therapeutic strategies in ruptured intracranial aneurysms. Eur J Radiol. 2013;82:1646-1652. 3. Sekhar LN, Natarajan SK, Ellenbogen RG, Ghodke B. Cerebral revascularization for ischemia, aneurysms, and cranial base tumors. Neurosurgery. 2008;62(6 Suppl 3):1373-1408 [discussion 1408-1310].

CONCLUSIONS Cerebral revascularization is an important adjunct to preserve blood flow in MCA branches and thus allow occlusion of complex MCA aneurysms, and can be done safely. There is a learning curve in decision-making and technical performance of the bypass. This report reviews this learning curve, presents our results, and reports our insights into patient/bypass selection. In our patients, STA was not an adequate donor for flow replacement of MCA-M1, MCA bifurcation, or large MCA-M2 branch. The ideal surgery in such cases is an EC-IC bypass graft from external carotid artery to one or both branches of MCA-M2/3. RAGs were easier to perform technically due to the size match and had less immediate and long-term complications when compared with SVGs. IC-IC bypass techniques are reserved for distal aneurysms or ATA revascularization and they have excellent results. The long-term patency rates after bypass techniques are excellent.

ACKNOWLEDGMENT We acknowledge Dr Richard Ellenbogen, Department of Neurological Surgery, University of Washington Medicine Neuroscience Institute, and Chair, American Board, for his continuous support for the study and Jennifer Pryll, medical illustrator, for her illustrative diagrams.

4. Ramanathan D, Starnes B, Hatsukami T, Kim LJ, Di Maio S, Sekhar L. Tibial artery autografts: alternative conduits for high flow cerebral revascularizations. World Neurosurg. 2013;80:322-327. 5. Gory B, Rouchaud A, Saleme S, et al. Endovascular treatment of middle cerebral artery aneurysms for 120 nonselected patients: a prospective cohort study. AJNR Am J Neuroradiol. 2014;35: 715-720. 6. Cay F, Peker A, Arat A. Stent-assisted coiling of cerebral aneurysms with the Neuroform Atlas stent. Interv Neuroradiol. 2018;24:263-269. 7. Pierot L, Biondi A. Endovascular techniques for the management of wide-neck intracranial bifurcation aneurysms: a critical review of the literature. J Neuroradiol. 2016;43:167-175.

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8. Pierot L, Costalat V, Moret J, et al. Safety and efficacy of aneurysm treatment with WEB: results of the WEBCAST study. J Neurosurg. 2016;124: 1250-1256. 9. Martinez-Galdamez M, Lamin SM, Lagios KG, et al. Periprocedural outcomes and early safety with the use of the Pipeline Flex Embolization Device with Shield Technology for unruptured intracranial aneurysms: preliminary results from a prospective clinical study. J Neurointerv Surg. 2017; 9:772-776. 10. Alaraj A, Ashley WW Jr, Charbel FT, AminHanjani S. The superficial temporal artery trunk as a donor vessel in cerebral revascularization: benefits and pitfalls. Neurosurg Focus. 2008;24:E7.

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BRAIN BYPASS SURGERY FOR COMPLEX MCA ANEURYSMS

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) 40year-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, Whellan DJ. Saphenous vein graft disease: review of pathophysiology, prevention, and treatment. Cardiol Rev. 2013;21:101-109. 12. Meybodi AT, Griswold D, Tabani H, et al. Topographic surgical anatomy of the parasylvian anterior temporal artery for intracranial-intracranial bypass. World Neurosurg. 2016;93:67-72. 13. Tayebi Meybodi A, Huang W, Benet A, Kola O, Lawton MT. Bypass surgery for complex middle cerebral artery aneurysms: an algorithmic approach to revascularization. J Neurosurg. 2017; 127:463-479. 14. Kivipelto L, Niemela M, Meling T, Lehecka M, Lehto H, Hernesniemi J. Bypass surgery for complex middle cerebral artery aneurysms: impact

of the exact location in the MCA tree. J Neurosurg. 2014;120:398-408.

assisted nonocclusive anastomosis technique. Neurosurgery. 2008;63:12-20 [discussion 20-2].

15. Matano F, Murai Y, Tateyama K, et al. Perioperative complications of superficial temporal artery to middle cerebral artery bypass for the treatment of complex middle cerebral artery aneurysms. Clin Neurol Neurosurg. 2013;115:718-724.

Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

16. Safavi-Abbasi S, Kalani MYS, Frock B, et al. Techniques and outcomes of microsurgical management of ruptured and unruptured fusiform cerebral aneurysms. J Neurosurg. 2017;127: 1353-1360.

Received 22 December 2018; accepted 7 June 2019

17. van Doormaal TP, van der Zwan A, Verweij BH, Han KS, Langer DJ, Tulleken CA. Treatment of giant middle cerebral artery aneurysms with a flow replacement bypass using the excimer laser-

Available online: www.sciencedirect.com

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Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.06.059 Journal homepage: www.journals.elsevier.com/worldneurosurgery 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.

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BRAIN BYPASS SURGERY FOR COMPLEX MCA ANEURYSMS

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 STAMCA 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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BRAIN BYPASS SURGERY FOR COMPLEX MCA ANEURYSMS

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-yearold 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) 49year-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. (MBT) 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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Figure 8. (M3-D) Recurrence of aneurysm after clipping. (A) NCCT showing hemorrhage in right sylvian fissure. (B) 3D RA showing distal MCA aneurysm. (C) 3D illustration showing previous clip and atherosclerosis at the origin of the MCA branches from neck. (D) Postoperative 3D illustration showing resection of the aneurysm and radial artery graft to revascularize distal MCA vessels. (E) 3D RA showing complete obliteration of the aneurysm and filling of all MCA branches. (M3-E) 8-year-old boy with ruptured 7 mm aneurysm. (A, B) 3D RA showing M3 distal fusiform aneurysm. (C) 3D illustration showing fusiform nature of aneurysm, previous clip/adherence of branches to the dome of the aneurysm. (D) Postoperative 3D illustration showing excision of aneurysm, revascularization of distal branches with combination of radial artery interposition graft and reimplantation. (E) 3D RA showing complete obliteration of the aneurysm and filling of all MCA branches. (M3-F) 55-year-old woman with ischemic symptoms, 3 mm aneurysm. (A) Brain MRI T1 axial image without contrast showing ruptured MCA aneurysm. (B) 3D RA showing distal MCA aneurysm. (C) Preoperative 3D illustration

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showing complex nature of aneurysm and clot around aneurysm. (D) Postoperative 3D illustration showing excision of the aneurysm and STA donor to revascularize distal MCA vessels. (E) Right ECA, and (F) right ICA DSA showing filling of the branch distal to the aneurysm from STA and complete obliteration of the aneurysm. (M3-G) 28-year-old woman with ischemic symptoms, 36 mm aneurysm. (A, B) DSA/3D RA showing complex multilobed MCA aneurysm. (C) Preoperative 3D illustration showing the fusiform aneurysm and surrounding branches. (D) Postoperative 3D illustration showing excision of the aneurysm and revascularization of distal vessels with radial artery jump graft. (E, F) Lateral view DSA showing filling of distal MCA branches and complete obliteration of aneurysm. (M4) 55-year-old man with headache, 9 mm aneurysm. (A) 3D RA showing left fusiform distal MCA aneurysm. (B) Preoperative 3D illustration showing fusiform nature of the aneurysm and resection and end-end anastomosis of the aneurysm followed by revision of anastomosis. (C) Postoperative 3D RA of left ICA showing complete obliteration of the aneurysm and filling of distal MCA vessels.

WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.06.059

ORIGINAL ARTICLE SABAREESH K. NATARAJAN ET AL.

BRAIN BYPASS SURGERY FOR COMPLEX MCA ANEURYSMS

Table 9. Early versus Late Cases Group A (2005e2011) Bypass procedures 31/52 (60%)

Group B (2012e2018) 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 artery; 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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BRAIN BYPASS SURGERY FOR COMPLEX MCA ANEURYSMS

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

Year

No. of Bypasses

EC-IC High Flow

STA-MCA

IC-IC

FU Duration months

Bypass patency %

Aneurysm obliteration %

Stroke 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)

2013

16

3

13

0

58

94

75

3/16 (19)

2008

22

2

0

20

43

86

100

8/22 (36)

Kalani16 17

Van Doormaal

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WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.06.059