bypass surgery for complex brain aneurysms

14
CLINICAL STUDIES 670 | VOLUME 65 | NUMBER 4 | OCTOBER 2009 www.neurosurgery-online.com ABBREVIATIONS: ACA, anterior cerebral artery; ATA, anterior temporal artery; BTO, balloon test occlusion; EC-IC, extracranial-intracranial; GOS, Glasgow Outcome Scale; ICA, internal carotid artery; IC-IC, intracra- nial-intracranial; MCA, middle cerebral artery; OA, occipital artery; PCA, posterior cerebral artery; PICA, posteroinferior cerebellar artery; SCA, superior cerebellar artery; STA, superficial temporal artery; VA, verte- bral artery BYPASS SURGERY FOR COMPLEX BRAIN ANEURYSMS: AN ASSESSMENT OF INTRACRANIAL- INTRACRANIAL BYPASS OBJECTIVE: Bypass surgery for brain aneurysms is evolving from extracranial-intracra- nial (EC-IC) to intracranial-intracranial (IC-IC) bypasses that reanastomose parent arter- ies, revascularize efferent branches with in situ donor arteries or reimplantation, and recon- struct bifurcated anatomy with grafts that are entirely intracranial. We compared results with these newer IC-IC bypasses to conventional EC-IC bypasses. METHODS: During a 10-year period, 82 patients underwent bypass surgery as part of their aneurysm management. A quarter of the patients presented with ruptured aneurysms and two-thirds presented with compressive symptoms from unruptured aneurysms. Most aneurysms (82%) had non-saccular morphology and 56% were giant sized. Common locations included the cavernous internal carotid artery (23%), middle cere- bral artery (20%), and posteroinferior cerebellar artery (12%). RESULTS: Forty-seven patients (57%) received EC-IC bypasses and 35 patients (43%) received IC-IC bypasses, including 9 in situ bypasses, 6 reimplantations, 11 reanasto- moses, and 9 intracranial grafts. Aneurysm obliteration rates were comparable in EC- IC and IC-IC bypass groups (97.9% and 97.1%, respectively), as were bypass patency rates (94% and 89%, respectively). Three patients died (surgical mortality, 3.7%), and 4 patients were permanently worse as a result of bypass occlusions (neurological mor- bidity, 4.9%). At late follow-up (mean duration, 41 months), good outcomes (Glasgow Outcome Scale score 5 or 4) were measured in 68 patients (90%) overall, and were similar in EC-IC and IC-IC bypass groups (91% and 89%, respectively). Changes in Glasgow Outcome Scale score were slightly more favorable with IC-IC bypass (6% worse or dead after IC-IC bypass versus 14% with EC-IC bypass). CONCLUSION: IC-IC bypasses compare favorably to EC-IC bypasses in terms of aneurysm obliteration rates, bypass patency rates, and neurological outcomes. IC-IC bypasses can be more technically challenging to perform, but they do not require har- vest of extracranial donor arteries, spare patients a neck incision, shorten interposition grafts, are protected inside the cranium, use caliber-matched donor and recipient arter- ies, and are not associated with ischemic complications during temporary arterial occlu- sions. IC-IC bypass can replace conventional EC-IC bypass with more anatomic recon- structions for selected aneurysms involving the middle cerebral artery, posteroinferior cerebellar artery, anterior cerebral artery, and basilar apex. KEY WORDS: Aneurysm, Clipping, Extracranial-to-intracranial bypass, In situ bypass, Intracranial-to-intracra- nial bypass, Reanastomosis, Reimplantation, Revascularization Neurosurgery 65:670–683, 2009 DOI: 10.1227/01.NEU.0000348557.11968.F1 www.neurosurgery-online.com Nader Sanai, M.D. Department of Neurological Surgery, University of California at San Francisco, San Francisco, California Zsolt Zador, M.D. Department of Neurological Surgery, University of California at San Francisco, San Francisco, California Michael T. Lawton, M.D. Department of Neurological Surgery, University of California at San Francisco, San Francisco, California Reprint requests: Michael T. Lawton, M.D., Department of Neurological Surgery, University of California at San Francisco, 505 Parnassus Avenue, M779, Box 0520, San Francisco, CA 94143-0520. Email: [email protected] Received, September 21, 2008. Accepted, March 17, 2009. Copyright © 2009 by the Congress of Neurological Surgeons

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Page 1: Bypass Surgery for Complex Brain Aneurysms

CLINICAL STUDIES

670 | VOLUME 65 | NUMBER 4 | OCTOBER 2009 www.neurosurgery-online.com

ABBREVIATIONS: ACA, anterior cerebral artery; ATA, anterior temporal artery; BTO, balloon test occlusion;EC-IC, extracranial-intracranial; GOS, Glasgow Outcome Scale; ICA, internal carotid artery; IC-IC, intracra-nial-intracranial; MCA, middle cerebral artery; OA, occipital artery; PCA, posterior cerebral artery; PICA,posteroinferior cerebellar artery; SCA, superior cerebellar artery; STA, superficial temporal artery; VA, verte-bral artery

BYPASS SURGERY FOR COMPLEX BRAINANEURYSMS: AN ASSESSMENT OF INTRACRANIAL-INTRACRANIAL BYPASS

OBJECTIVE: Bypass surgery for brain aneurysms is evolving from extracranial-intracra-nial (EC-IC) to intracranial-intracranial (IC-IC) bypasses that reanastomose parent arter-ies, revascularize efferent branches with in situ donor arteries or reimplantation, and recon-struct bifurcated anatomy with grafts that are entirely intracranial. We compared resultswith these newer IC-IC bypasses to conventional EC-IC bypasses.METHODS: During a 10-year period, 82 patients underwent bypass surgery as part oftheir aneurysm management. A quarter of the patients presented with ruptured aneurysmsand two-thirds presented with compressive symptoms from unruptured aneurysms.Most aneurysms (82%) had non-saccular morphology and 56% were giant sized.Common locations included the cavernous internal carotid artery (23%), middle cere-bral artery (20%), and posteroinferior cerebellar artery (12%).RESULTS: Forty-seven patients (57%) received EC-IC bypasses and 35 patients (43%)received IC-IC bypasses, including 9 in situ bypasses, 6 reimplantations, 11 reanasto-moses, and 9 intracranial grafts. Aneurysm obliteration rates were comparable in EC-IC and IC-IC bypass groups (97.9% and 97.1%, respectively), as were bypass patencyrates (94% and 89%, respectively). Three patients died (surgical mortality, 3.7%), and4 patients were permanently worse as a result of bypass occlusions (neurological mor-bidity, 4.9%). At late follow-up (mean duration, 41 months), good outcomes (GlasgowOutcome Scale score 5 or 4) were measured in 68 patients (90%) overall, and weresimilar in EC-IC and IC-IC bypass groups (91% and 89%, respectively). Changes inGlasgow Outcome Scale score were slightly more favorable with IC-IC bypass (6%worse or dead after IC-IC bypass versus 14% with EC-IC bypass).CONCLUSION: IC-IC bypasses compare favorably to EC-IC bypasses in terms ofaneurysm obliteration rates, bypass patency rates, and neurological outcomes. IC-ICbypasses can be more technically challenging to perform, but they do not require har-vest of extracranial donor arteries, spare patients a neck incision, shorten interpositiongrafts, are protected inside the cranium, use caliber-matched donor and recipient arter-ies, and are not associated with ischemic complications during temporary arterial occlu-sions. IC-IC bypass can replace conventional EC-IC bypass with more anatomic recon-structions for selected aneurysms involving the middle cerebral artery, posteroinferiorcerebellar artery, anterior cerebral artery, and basilar apex.

KEY WORDS: Aneurysm, Clipping, Extracranial-to-intracranial bypass, In situ bypass, Intracranial-to-intracra-nial bypass, Reanastomosis, Reimplantation, Revascularization

Neurosurgery 65:670–683, 2009 DOI: 10.1227/01.NEU.0000348557.11968.F1 www.neurosurgery- online.com

Nader Sanai, M.D.Department of Neurological Surgery,University of Californiaat San Francisco,San Francisco, California

Zsolt Zador, M.D.Department of Neurological Surgery,University of Californiaat San Francisco,San Francisco, California

Michael T. Lawton, M.D.Department of Neurological Surgery,University of Californiaat San Francisco,San Francisco, California

Reprint requests:Michael T. Lawton, M.D.,Department of Neurological Surgery,University of Californiaat San Francisco,505 Parnassus Avenue,M779, Box 0520,San Francisco, CA 94143-0520.Email: [email protected]

Received, September 21, 2008.

Accepted, March 17, 2009.

Copyright © 2009 by theCongress of Neurological Surgeons

Page 2: Bypass Surgery for Complex Brain Aneurysms

Despite its well-publicized failure to benefit patients withischemic stroke in the extracranial-intracranial (EC-IC)Bypass Trial, EC-IC bypass surgery has been essential in

the management of brain aneu rysms that are too complex forconventional clipping or endovascular coiling (2, 4, 8, 11, 22, 27).Revascularization of a territory distal to an unclippable, giant,dolichoectatic, or thrombotic aneurysm enables the aneurysm tobe occluded without risk of ischemic complications, or the par-ent artery’s blood flow to be reversed or reduced safely.Superficial temporal artery (STA)-to-middle cerebral artery(MCA) bypass was the prototype, and subsequently an array ofbypasses was developed with the same concept of redirectingextracranial blood flow from scalp arteries or cervical carotidarteries to the brain, either directly with 1 anastomosis or withinterposition grafts and 2 anastomoses. In recent years, innova-tive bypasses have been introduced anecdotally that revascular-ize intracranial arteries with other intracranial arteries, withoutextracranial donor arteries (6, 7, 9, 15, 16, 19). These intracranial-intracranial (IC-IC) bypasses are simple, elegant, and moreanatomic than their EC-IC counterparts. IC-IC bypasses requireno harvest of extracranial donors, spare patients a neck inci-sion, shorten any interposition grafts, are protected within thecranium, and use caliber-matched donor and recipient arteries.These advantages of IC-IC bypasses appeal to experiencedbypass surgeons, and the use of these bypasses has increasednoticeably. Sekhar et al. (26) performed at least 11 IC-ICbypasses in an overall experience with 119 bypasses in 115patients. Lawton et al. (15) performed 28 IC-IC bypasses (44%)in an overall experience with 63 bypasses in 61 patients.

The development of IC-IC bypasses represents an evolutionof bypass surgery for brain aneurysms. However, IC-IC bypassresults have not been compared with conventional EC-ICbypass results in a large clinical experience. We have embracedIC-IC bypasses in our aneurysm practice, and thereforereviewed our experience with bypass surgery for complexaneurysms in 82 patients. We hypothesized that IC-IC bypasseswould compare favorably to EC-IC bypasses in terms of effi-cacy, safety, and patient outcomes, and that these data wouldsupport the trend toward intracranial arterial reconstruction.

PATIENTS AND METHODS

Study DesignThe study was approved by the Institutional Review Board and con-

ducted in compliance with Health Insurance Portability and AccountabilityAct regulations. The prospectively maintained database for theCerebrovascular Service at the University of California–San Francisco wassearched for patients who had bypass surgery as part of their aneurysmtreatment. Patients were divided into 2 groups according to type of bypass.EC-IC bypass involved donor arteries from external carotid artery branches(STA and occipital artery [OA]), cervical carotid arteries (common carotidartery, internal carotid artery [ICA], and external carotid artery), or otherextracranial arteries (e.g., subclavian artery). IC-IC bypass involvedintracranial donor arteries, and were further categorized as in situ bypass(adjacent donor artery), reimplantation (aneurysm branch artery onto par-ent artery), reanastomosis (primary repair of parent artery), and intracranialbypass graft (graft interposed between donor and recipient arteries).

INTRACRANIAL-INTRACRANIAL BYPASS FOR COMPLEX ANEURYSMS

NEUROSURGERY VOLUME 65 | NUMBER 4 | OCTOBER 2009 | 671

Medical records, radiographic studies, operative reports, intraopera-tive photographs, neurological course, and clinical follow-up evalua-tions were reviewed retrospectively. Neurological outcomes wereassessed using the Glasgow Outcome Scale (GOS). A clinical nurse orclinician not directly involved in the care of these patients performed alloutcome assessments preoperatively, early postoperatively (6 weeks),and at late follow-up.

PatientsDuring a 10-year period between November 1997 and November

2007, 1984 aneurysms were treated microsurgically in 1578 patients bythe senior author (MTL). Of these patients, 82 (5%) underwent cerebralrevascularization as part of their aneurysm management; 50 patientswere women and 32 men, with a mean age of 53 years (age range,12–78 years) (Table 1). Twenty-one patients presented with subarach-noid hemorrhage (26%). Hunt and Hess grade III was the most com-mon clinical grade (48%), and 4 patients presented with poor Huntand Hess grade. Fifty-six patients (68%) presented with unrupturedaneurysms and neurological symptoms, with cranial neuropathy orhemiparesis from mass effect present in 38 patients (68%). Eightpatients (14%) presented with transient ischemic attacks or stroke inassociation with thrombotic aneurysms. Five patients presented withincidental, unruptured aneurysms (6%).

Aneurysm CharacteristicsThe most common locations were cavernous ICA (19 aneurysms,

23%), MCA (16 aneurysms, 20%), and posteroinferior cerebellar artery(PICA) (10 aneurysms, 12%) (Table 2). Forty-six aneurysms (56%) weregiant in size, and 67 (82%) had fusiform or dolichoectatic morphology.Thirty-one patients (38%) had thrombotic aneurysms. Eight aneurysms(10%) had been treated endovascularly with coils, of which 3 wereincompletely treated and 5 were recurrent. Fifteen patients (19%) hadmultiple aneurysms, with 26 other aneurysms diagnosed.

IndicationsBypasses were performed only when conventional clipping failed, as

a result of complex anatomy, large or giant size, dolichoectatic mor-phology, intraluminal thrombus, or atherosclerotic tissue at the neck.Balloon test occlusion (BTO) was used to select 26 patients, all of whomhad cavernous or supraclinoid ICA aneurysms, for aneurysm manage-ment with a bypass. Ten patients failed the test with balloon inflationalone, and 16 patients failed with additional hypotensive challenge(lowering mean arterial pressure with nitroprusside drip by 20 mm Hg,or 25% of mean arterial pressure, whichever was greater). Failed BTOwas used as an indication for bypass. High-flow bypass was used inpatients who failed BTO immediately, and low-flow bypass was usedin patients who failed BTO after hypotensive challenge. The decision toperform a bypass with aneurysms in other locations was based on theaneurysm’s unclippability and patients’ angiographic anatomy (pres-ence or absence of collateral circulation from the circle of Willis or lep-tomeningeal connections).

Surgical Technique

In Situ BypassIn situ bypass requires donor and recipient arteries that lie parallel

and in close proximity to one another. Four sites have this anatomy:MCA branches (M2 and M3 segments) and anterior temporal artery(ATA) as they course through the sylvian fissure (Fig. 1); bilateral ante-rior cerebral arteries (ACA) as they course through the interhemi-

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SANAI ET AL.

672 | VOLUME 65 | NUMBER 4 | OCTOBER 2009 www.neurosurgery-online.com

spheric fissure over the corpus callosum (A3 and A4 segments) (Fig. 2);posterior cerebral artery (PCA) (P2 and P3 segments) and superiorcerebellar artery (SCA) as they course through the ambient cisternaround the cerebral peduncle (Fig. 3); and bilateral PICAs as theycourse through the cisterna magna to meet behind the medulla under-neath the cerebellar tonsils (Fig. 4). In situ bypasses require 1 side-to-side anastomosis.

ReimplantationComplex aneurysms with branches that originate from the aneurysm

base can often be reconstructed with tandem clipping techniques thatpreserve branch arteries (a fenestrated clip encircling the branch origin

and a stacked straight clip closing the fenestration). In cases in whichclip reconstruction fails, the neck can be clipped to exclude theaneurysm, preserve the parent artery, and sacrifice the branch artery.The occluded branch artery can then be reconstituted with reimplanta-tion onto the parent artery. Alternatively, the branch artery can be reim-planted to an adjacent donor artery that is not the parent artery, as longas that donor artery lies near the branch. Similar to in situ bypasses,this favorable anatomy occurs with MCA, ACA, and PICA aneurysms.Reimplantation requires 1 end-to-side anastomosis.

ReanastomosisReanastomosis requires trapping the aneurysm, completely detaching

afferent and efferent arteries, and reconnecting cut ends with an end-to-end anastomosis. This technique works well with fusiform aneurysmsthat are small or medium in size. Saccular aneurysms at bifurcations aredifficult to reconstruct with primary reanastomosis because the secondefferent branch must either be reimplanted or bypassed with an extracra-nial donor artery. Large and giant aneurysms may be difficult to reanas-tomose because ends of parent artery are separated after excising ananeurysm. Mobilizing the ends of afferent and efferent arteries mayenable the first stitch to pull them together with minimal tension. If thegap in the parent artery is too long and the tension too great, the suturewill tear through the artery wall as it is tightened and ruin the repair.Some large aneurysms in PICA and MCA territories have a redundantparent artery that will allow primary reanastomosis despite their size.Reanastomosis requires 1 end-to-end anastomosis.

TABLE 1. Study demographicsa

EC-IC IC-ICTotal

bypass bypass

Total no. of patients 82 47 (57%) 35 (43%)

Median age (range), y 53 (12–78) 57 (12–77) 45 (15–78)

Female sex 50 (61%) 35 (74%) 15 (43%)

Patients with rupturedaneurysm

All 21 (26%) 8 (17%) 13 (37%)

Grade I 6 (29%) 2 (25%) 4 (31%)

Grade II 1 (5%) 1 (13%) 0 (0%)

Grade III 10 (48%) 3 (38%) 7 (54%)

Grade IV 4 (19%) 2 (25%) 2 (15%)

Grade V 0 (0%) 0 (0%) 0 (0%)

Patients with unrupturedaneurysm (symptomatic)

All 56 (68%) 37 (79%) 19 (54%)

Headache 22 (39%) 15 (41%) 7 (37%)

Cranial neuropathy 29 (52%) 22 (59%) 7 (37%)

Hemiparesis 9 (16%) 6 (16%) 3 (16%)

Seizure 3 (5%) 2 (5%) 1 (5%)

TIA (stroke) 8 (14%) 4 (11%) 4 (21%)

Hydrocephalus 4 (7%) 2 (5%) 2 (11%)

Incomplete coiling 7 (13%) 2 (5%) 5 (26%)or recurrence

Patients with unrupturedaneurysm (incidental)

All 5 (6%) 2 (4%) 3 (9%)

Aneurysm characteristics

Mean diameter (range), mm 23.8 (4–60) 28.5 (6–60) 17.2 (4–49)

Saccular 15 (18%) 10 (21%) 5 (14%)

Fusiform, dolichoectatic 67 (82%) 37 (79%) 30 (86%)

Giant 46 (56%) 34 (72%) 12 (34%)

Thrombotic 31 (38%) 18 (38% 13 (37%)

Outcome measure

Mean preoperative 4.5 4.7 4.4GOS score

a EC-IC, extracranial-intracranial; IC-IC, intracranial-intracranial; TIA, transient ischemic attack; GOS,Glasgow Outcome Scale.

TABLE 2. Aneurysm demographicsa

EC-IC IC-ICAneurysm location Total

bypass bypass

Internal carotid artery

Cavernous 19 (23%) 17 (36%) 2 (6%)

Supraclinoid 9 (11%) 9 (19%) 0 (0%)

Ophthalmic 3 (4%) 3 (6%) 0 (0%)

Terminus 2 (2%) 2 (4%) 0 (0%)

Middle cerebral artery

Total 16 (20%) 7 (15%) 9 (26%)

Anterior cerebral artery

Anterior communi- 3 (4%) 0 (0%) 3 (9%)cating artery

Pericallosal 2 (2%) 0 (0%) 2 (6%)

Distal ACA 1 (1%) 0 (0%) 1 (3%)

Basilar artery

Basilar bifurcation 2 (2%) 2 (4%) 0 (0%)

Posterior cerebral artery 2 (2%) 2 (4%) 0 (0%)

Superior cerebellar artery 2 (2%) 1 (2%) 1 (3%)

Basilar trunk 8 (10%) 4 (9%) 4 (11%)

Posterior inferior cere-bellar artery

PICA 10 (12%) 0 (0%) 10 (29%)

Vertebral artery 3 (4%) 0 (0%) 3 (9%)

Total 82 (100%) 47 (100%) 35 (100%)

a EC-IC, extracranial-intracranial; IC-IC, intracranial-intracranial; ACA, anterior cerebral artery;PICA, posteroinferior cerebellar artery.

Page 4: Bypass Surgery for Complex Brain Aneurysms

INTRACRANIAL-INTRACRANIAL BYPASS FOR COMPLEX ANEURYSMS

NEUROSURGERY VOLUME 65 | NUMBER 4 | OCTOBER 2009 | 673

FIGURE 2. IC-IC bypass techniques for anterior cerebral artery (ACA)aneurysms. A, overview of MCA anatomy. B, in situ bypass (A3-A3). C,reanastomosis (ACA). D, reimplantation (pericallosal-callosomarginal). E,intracranial bypass graft (ACA double implantation). ICA, internal carotidartery; MCA, middle cerebral artery; PcaA, pericallosal artery; CmaA, cal-losomarginal artery; L, left; and R, right; RAG, radial artery graft.

A

B C

D E

Intracranial Bypass With GraftsBypasses with interposition grafts connect donor and recipient arter-

ies that are entirely intracranial, differentiating them from EC-ICbypasses that use extracranial donors. In contrast to EC-IC bypasseswith saphenous vein grafts spanning from the neck to the sylvian fis-sure, intracranial bypass grafts are shorter and radial artery grafts aresufficiently long. Radial artery grafts are preferred over saphenousvein grafts because they are composed of arterial tissue, have higherlong-term patency rates, and match the caliber of intracranial arteries.A preoperative Allen test with Doppler ultrasound ensures adequateperfusion of the hand with ulnar artery and a competent palmar arch.Intraoperatively, the forearm is accessed for harvest more easily thanthe thigh, particularly when the patient is positioned laterally or pronefor posterior circulation aneurysms. Vasospasm in radial artery graftshas been described, but can be avoided by using pressure distension to

dilate the graft before implantation, and by bathing the graft in a mix-ture of nitroprusside and heparin. Unlike other IC-IC techniques,intracranial bypass grafts require at least 2 anastomoses, which can beend-to-side, end-to-end, or side-to-side. Anastomoses are planned tominimize brain ischemia during the time that intracranial arteries aretemporarily occluded and sutured.

RESULTS

Aneurysm TreatmentForty-seven patients (57%) received EC-IC bypasses and 35

patients (43%) received IC-IC bypasses. EC-IC bypassesincluded 16 low-flow bypasses with STA donors in 15 patientsand an OA donor in 1 patient (Table 3). High-flow EC-IC

FIGURE 1. Intracranial-intracranial (IC-IC) bypass techniques for middlecerebral artery (MCA) aneurysms. A, overview of MCA anatomy. B, in situbypass (anterior temporal artery [ATA]-MCA). C, reanastomosis (MCA).D, reimplantation (MCA-MCA). E, intracranial bypass graft (anterior cere-bral artery [ACA]-MCA double reimplantation). ICA, internal carotidartery; ST, superior trunk; IT, inferior trunk; RAG, radial artery graft.

A

B C

D E

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674 | VOLUME 65 | NUMBER 4 | OCTOBER 2009 www.neurosurgery-online.com

bypasses were performed in 31 patients using saphenous veingrafts in 27 patients and radial artery grafts in 4 patients. IC-ICbypasses consisted of in situ bypasses in 9 patients (26%), reim-plantation in 6 patients (17%), reanastomosis in 11 patients(31%), and intracranial bypass grafts in 9 patients (26%) (Table4). Unlike extracranial bypass grafts, intracranial bypass graftsused the radial artery more frequently than the saphenous vein(6 patients versus 3 patients, respectively). Seven patients hadcomplex bypass configurations (Table 5), of which 5 were cate-gorized as IC-IC bypass patients and 2 as EC-IC bypass patients.

Aneurysm location influenced bypass design. Overall, 31 of33 patients with ICA aneurysms underwent EC-IC bypass,which was easier than IC-IC bypass with the petrous-to-supra-clinoid ICA bypass. Similarly, 9 of 14 aneurysms involving thebasilar artery apex or trunk were managed with EC-IC bypass

because of their deep location and limited proximal donor sites.IC-IC bypasses for basilar artery aneurysms included MCA-PCA bypass with radial artery grafts (2 patients), vertebralartery (VA)-SCA bypass (1 radial artery graft and 1 saphenousvein graft), and ATA-SCA reimplantation (1 patient). In con-trast to ICA and basilar artery aneurysms, ACA and PICAaneurysms were revascularized exclusively with IC-ICbypasses. The distal ACA territory was far removed fromextracranial donor arteries, making IC-IC bypasses moreappealing. IC-IC bypass options were numerous with PICAaneurysms and eliminated the tedious dissection required toharvest the OA. Bypasses for MCA aneurysms were splitbetween EC-IC (7 patients) and IC-IC bypasses (9 patients).

Approach depended on aneurysm location. ICA aneurysmswere approached through a pterional craniotomy (29 patients),

FIGURE 3. IC-IC bypass techniques for basilar artery apex aneurysms. A,overview of basilar artery apex anatomy. B, in situ bypass (superior cere-bellar artery [SCA]–posterior cerebral artery [PCA]). C, reanastomosis(PCA). D, reimplantation (anterior temporal artery [ATA]-SCA). E,intracranial bypass graft (vertebral artery [VA]-SCA bypass). F, intracra-nial bypass (middle cerebral artery [MCA]-PCA bypass). ICA, internalcarotid artery; ACA, anterior cerebral artery; BA, basilar artery; CN III,oculomotor nerve.

A B

C D

E F

FIGURE 4. IC-IC bypass techniques for posterior inferior cerebellar artery(PICA) aneurysms. A, overview of PICA anatomy. B, in situ bypass(PICA-PICA). C, reanastomosis (PICA). D, reimplantation (PICA–vertebral artery [VA]). E, intracranial bypass graft (VA-PICA bypass).BA, basilar artery; L, left; R, right; RAG, radial artery graft.

A

B C

D E

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INTRACRANIAL-INTRACRANIAL BYPASS FOR COMPLEX ANEURYSMS

NEUROSURGERY VOLUME 65 | NUMBER 4 | OCTOBER 2009 | 675

and an orbitozygomatic craniotomy was used for additionalexposure with giant aneurysms (4 patients). Similarly, a pterionalcraniotomy was adequate for MCA aneurysms (14 patients), andan orbitozygomatic craniotomy was used for giant aneurysms (2patients). ACA aneurysms were exposed through bifrontal cran-iotomies, with the midline of the head positioned parallel to thefloor and angled up 45 degrees to allow gravity to retract thedependent hemisphere. All bypasses for basilar apex aneurysmswere performed through orbitozygomatic craniotomies. A VA-SCA bypass for 2 basilar trunk aneurysms was performedthrough a combined far lateral–subtemporal craniotomy. Onedistal OA-PCA bypass was performed through a torcular cran-iotomy. PICA bypasses were performed through far lateral cran-iotomies, although the PICA-PICA bypass did not require resec-tion of occipital condyle or much lateral exposure when theaneurysm was not accessed, as with a staged endovascularocclusion (3 patients).

Brain relaxation was achieved with mannitol (1 g/kg) andcerebrospinal fluid drainage through a ventriculostomy, fenes-tration in the lamina terminalis, or dissection into a subarach-noid cistern. During the anastomosis when parent arteries weretemporarily occluded, mild hypothermia and barbiturate-induced electroencephalographic burst suppression were usedto increase tolerance to ischemia. The average intracranialcross-clamp time was 46 minutes (range, 32–63 minutes) forEC-IC bypass and 46 minutes (range, 26–76 minutes) for IC-ICbypass. Changes in somatosensory evoked potentials or the

electroencephalogram were rare, and were managed byincreasing blood pressure with pressor agents. Heparin irriga-tion was used liberally in the surgical field during the anasto-mosis, but systemic heparin was not used.

Aneurysm occlusion was performed during surgery in 54patients and consisted of 27 aneurysm trappings (33%), 16proximal occlusions (20%), 6 distal occlusions (7%), and 5aneurysm clippings (6%) (Table 6). The remaining 28 patients(34%) underwent staged endovascular aneurysm occlusion.Twenty-two of these patients were in the EC-IC bypass group,reflecting the large number of ICA aneurysms. In contrast, halfof the aneurysms in the IC-IC bypass group were trapped dur-ing surgery, reflecting the accessibility of these more distallylocated aneurysms. The small number of aneurysms clippeddirectly reflects the nonsaccular morphology of theseaneurysms. Endovascular staging was typically performed 2 to3 days after the bypass procedure. Patients were started onaspirin (350 mg/d) immediately after surgery.

a STA, superficial temporal artery; MCA, middle cerebral artery; E-S, end-to-side;PCA, posterior cerebral artery; AICA, anterior inferior cerebellar artery; OA, occipitalartery; PICA, posterior inferior cerebellar artery; CCA, common carotid artery; ECA,external carotid artery; E-E, end-to-end; ICA, internal carotid artery; SCA, superiorcerebellar artery.

TABLE 3. Extracranial-intracranial bypassesa

No. of Anasto- Tech-Technique

patientsGraft Flow

mosis nique

Low-flow bypass

STA-MCA 9 No Low 1 E-S

STA-PCA 3 No Low 1 E-S

STA-SCA 3 No Low 1 E-S

STA-AICA 0 No Low 1 E-S

OA-PCA 1 No Low 1 E-S

OA-PICA 0 No Low 1 E-S

High-flow bypass

CCA-MCA 6 Yes High 2 E-S

ECA-MCA 16 Yes High 2 E-S, E-E

ICA-MCA 5 Yes High 2 E-S, E-E

Subclavian-MCA 3 Yes High 2 E-S

CCA-PCA/SCA 0 Yes High 2 E-S

ECA-PCA/SCA 1 Yes High 2 E-S, E-E

ICA-PCA/SCA 0 Yes High 2 E-S, E-E

TABLE 4. Intracranial-intracranial bypassesa

No. of Anasto- Tech-Technique

patientsGraft Flow

mosis nique

In situ bypass

ATA-MCA 1 No Low 1 S-S

MCA-MCA 1 No Low 1 S-S

ACA-ACA 2 No Low 1 S-S

PCA-SCA 0 No Low 1 S-S

PICA-PICA 5 No Low 1 S-S

Reimplantation

MCA-MCA 1 No Low 1 E-S

PC-CM 1 No Low 1 E-S

ATA-SCA 1 No Low 1 E-S

PICA-VA 3 No Low 1 E-S

Reanastomosis

MCA 5 No Low 1 E-E

ACA 1 No Low 1 E-E

PICA 5 No Low 1 E-E

IC bypass graft

Petrous–supra- 2 Yes High 2 E-Sclinoid ICA

ICA-MCA 0 Yes High 2 E-S

ACA-MCA 1 Yes High 2 E-S

MCA-ACA 1 Yes High 2 E-S

ACA-ACA 1 Yes High 2 E-S

MCA-PCA 2 Yes High 2 E-S

VA-SCA 2 Yes High 2 E-S

a ATA, anterior temporal artery; MCA, middle cerebral artery; S-S, side-to-side; ACA, anteriorcerebral artery; PCA, posterior cerebral artery; SCA, superior cerebellar artery; PICA, posteriorinferior cerebellar artery; E-S, end-to-side; PC, pericallosal artery; CM, callosomarginal artery;VA, vertebral artery; E-E, end-to-end; ICA, internal carotid artery.

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Aneurysm OutcomesAngiography was performed after surgery in all patients to

evaluate bypass patency and aneurysm exclusion. Overall, 80 of82 aneurysms were obliterated angiographically (97.6% obliter-ation rate). All 5 clipped and 27 trapped aneurysms were com-pletely excluded. Of the 16 aneurysms that were proximallyoccluded, 15 were angiographically occluded postoperatively.Of the 6 aneurysms that were distally occluded, 5 were angio-graphically occluded postoperatively. Two fusiform aneurysmswere filling angiographically after surgery, but had new intralu-minal thrombosis, smaller angiographic size, and reduced flow.The 28 aneurysms that were treated with staged endovasculartherapy were completely occluded, 16 of them with coils and 12with proximal balloons. All 6 aneurysms with IC-IC bypasseswere treated with direct coil occlusion, whereas only 9 of 21aneurysms with EC-IC bypasses were treated with direct coilocclusion. Aneurysm obliteration was comparable in the EC-ICand IC-IC bypass groups (97.9% and 97.1%, respectively).

Overall, 75 of 82 bypasses were patent on postoperative angiog-raphy (91%). Three EC-IC bypasses and 4 IC-IC bypassesoccluded, with comparable patency rates in the 2 groups (94% and89%, respectively). Intraoperative events predicted later occlusionin 4 cases. Two bypass grafts from the cervical carotid to MCAbecame limp at the end of the cases and both bypasses wererevised (1 proximally, 1 proximally and distally). One patient witha gunshot-related dissecting ACA aneurysm had damaged parentarteries that were reanastomosed after aneurysm excision. Theinitial repair occluded, the parent artery was excised back to morenormal tissue, and the anastomosis was revised with increasedtension. One MCA thrombosed after clipping of a large M1 seg-ment aneurysm; the aneurysm was excised, the M1 segment was

thrombectomized, and reanastomosis restored MCA flow. Despiteimmediate revisions in these 4 cases, the bypasses occluded post-operatively. The remaining 3 bypass occlusions were unexpected.One patient had a saphenous vein with significant varicosities; 1MCA reanastomosis required an STA interposition graft to bridgethe gap in the parent artery; and an allograft saphenous vein usedin the remaining patient occluded.

Patient OutcomesThree patients died in the perioperative period (surgical mor-

tality, 3.7%), all with basilar trunk aneurysms. These patientsunderwent uncomplicated bypass procedures to revascularizethe basilar apex (STA-SCA, STA-PCA, and external carotidartery–SCA), but subsequent endovascular therapy resulted inaneurysm rerupture during coiling, basilar artery thrombosisafter bilateral VA occlusions, and intracerebral hemorrhagewhile taking heparin after bilateral VA occlusions.

Permanent neurological morbidity was observed in 4 patients(4.9%), all related to bypass occlusions. These patients had MCA

TABLE 5. Complex bypass techniquesa

EC-IC by- IC-IC by-pass group pass group

Double reimplantation

ECA-MCA-MCA 1 0

ACA-MCA-MCA 0 1

ACA-PC-CM 0 1

IC-IC � EC-IC

MCA-MCA reanastomosis 0 1+ STA-MCA

ATA-MCA + STA-MCA 0 1

Reanastomosis with inter-position STA

MCA-STA-MCA 0 1

Double EC-IC

STA-MCA, double barrel 1 0

a EC-IC, extracranial-intracranial; IC-IC, intracranial-intracranial; ECA, externalcarotid artery; MCA, middle cerebral artery; ACA, anterior cerebral artery; PC,pericallosal artery; CM, callosomarginal artery; STA, superficial temporal artery;ATA, anterior temporal artery.

a EC-IC, extracranial-intracranial; IC-IC, intracranial-intracranial; GOS, Glasgow Outcome Scale.

TABLE 6. Operative and clinical outcomes after extracranial-intracranial and intracranial-intracranial bypassesa

EC-IC IC-ICTotal

bypass bypass

Bypassed aneurysms 82 47 35

Aneurysm occlusion

Clipping 5 (6%) 2 (4%) 3 (9%)

Trapping 27 (33%) 10 (21%) 17 (49%)

Proximal occlusion 16 (20%) 11 (23%) 5 (14%)

Distal occlusion 6 (7%) 2 (4%) 4 (11%)

Endovascular occlusion 28 (34%) 22 (47%) 6 (17%)

Aneurysm obliteration 80 (98%) 46 (98%) 34 (97%)

Bypass patency 75 (91%) 44 (94%) 31 (89%)

No. of patients 82 47 35

Surgical mortality 3 (4%) 3 (6%) 0 (0%)

Transient neurological 4 (5%) 1 (2%) 3 (9%)morbidity

Late outcome

GOS score 5 59 (78%) 34 (81%) 25 (74%)

GOS score 4 9 (12%) 4 (10%) 5 (15%)

GOS score 3 4 (5%) 1 (2%) 3 (9%)

GOS score 2 0 (0%) 0 (0%) 0 (0%)

Dead 4 (5%) 3 (7%) 1 (3%)

Total 76 42 34

Lost 3 2 1

Change in GOS score atlate follow-up

Improved 15 (20%) 8 (19%) 7 (21%)

Unchanged 53 (70%) 28 (67%) 25 (74%)

Worse 4 (5%) 3 (7%) 1 (3%)

Dead 4 (5%) 3 (7%) 1 (3%)

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strokes after occlusion of high-flow EC-IC bypasses in 3 patientsand an MCA reanastomosis in 1 patient. Two other bypassocclusions (after aneurysm excision and reanastomosis) did notcause any permanent neurological deficits, and 1 bypass occlu-sion caused only transient neurological deficits. In addition tothis patient with transient neurological deficits related to bypassocclusion, 3 patients had postoperative epidural hematomaswith deficits that resolved completely (transient neurologicalmorbidity, 4.9%).

Excluding the 3 surgical mortalities and 3 additional patientslost to follow-up, final neurological outcomes were assessed in76 patients (93%). The mean duration of follow-up was 41months (range, 1–125 months) and did not differ significantlybetween EC-IC and IC-IC bypass groups (38.6 and 42.7 months,respectively). Four patients died after hospital discharge, 3from complications in rehabilitation and 1 from delayedgrowth of a basilar trunk aneurysm with resulting brainstemcompression. Three of the 4 late deaths were in the EC-ICbypass group. Good outcomes (GOS score 5 or 4) were meas-ured in 68 patients (90%) overall, and were similar in EC-ICand IC-IC bypass groups (91% and 89%, respectively) (Table 6).At late follow-up, 15 patients (20%) were improved and 53(70%) were un chang ed, relative to preoperative neurologicalcondition, ex clud ing lost patients. Chan ges in outcome by GOSscore were slightly more favorable in the IC-IC bypass groupthan the EC-IC bypass group (6% versus 14% worse or dead inIC-IC versus EC-IC bypass group, respectively). The mean finalGOS scores reflected a similar trend, with a mean GOS score of4.3 in the EC-IC bypass group and 4.6 in the IC-IC bypassgroup. Relative to preoperative neurological condition, meanGOS score decreased 0.30 in the EC-IC bypass group andincreased 0.21 in the IC-IC bypass group.

DISCUSSION

Evolution of Bypass Surgery for Brain AneurysmsBypass surgery for brain aneurysms began with the introduc-

tion and popularization of the STA-MCA bypass by Yasargil (29).This simple bypass protected patients from ischemic complica-tions after deliberate arterial occlusion during the treatment ofMCA and some ICA aneurysms. Bypass surgery evolved withEC-IC bypasses that used other extracranial donor arteries andinterposition grafts connected to proximal donor sites in the neck(1, 3, 5, 10, 12–15, 17, 18, 20, 21, 23, 25, 28, 30). Even though thesesecond-generation EC-IC bypasses yield excellent results, bypasssurgery for aneurysms is evolving further as IC-IC bypasses elim-inate extracranial donor arteries and reconstruct cerebral circula-tion in ways that resemble normal vascular anatomy. In our clin-ical experience, this third generation of IC-IC bypasses comparedfavorably to traditional EC-IC bypasses. Aneurysm obliterationrates, bypass patency rates, and neurological outcomes (late GOSscore and change in GOS score) were similar to EC-IC bypasspatients, supporting a progression toward vascular reconstruc-tion that is entirely intracranial.

EC-IC bypasses are technically easier to perform than IC-ICbypasses. For example, STA-MCA bypass requires 1 end-to-side

anastomosis that is usually straightforward because the donorartery is large and mobilizes to enable visualization of bothsuture lines. In contrast, in situ bypass be tween 2 MCA branchesrequires a more challenging side-to-side anastomosis betweenarteries with limited mobility. Similarly, an external carotidartery-MCA bypass requires a proximal anastomosis that can beperformed in a superficial cervical site with no cerebral ischemia,whereas an A1 ACA-MCA intracranial bypass graft re quires aproximal anastomosis in a narrow surgical corridor that is evendeeper than the distal anastomosis to MCA (Fig. 5). Althoughcross-clamping the A1 ACA does not produce ischemia inpatients with a com petent anterior communicating artery, tem-porary clips on a major intracranial artery induce some timepressure. Therefore, IC-IC bypasses add a degree of difficulty.

Based on our experience, we think the extra effort with IC-ICbypasses is justified. First, the caliber of scalp arteries is variableand sometimes too diminutive to revascularize an efferent artery.Although scalp arteries can dilate over time, they might not meetthe de mand immediately. Deep by passes to midline or parame-dian arteries can require 8 cm or more of scalp artery, and it maybe too small at the anastomotic depth to be safe. In contrast, insitu bypass, reana stomosis, and reimplantation techniques usedonor arteries that match or exceed the caliber of recipient arter-ies. Second, EC-IC bypasses that use cervical carotid arteryrequire long interposition grafts at the limit of the radial arterygraft. Con sequently, saphenous veins were used more frequentlythan radial arteries, introducing caliber mismatches between graftand intracranial artery. Longer grafts are also associated withlower long-term patency rates. In contrast, intracranial bypassgrafts are shorter, and enabled frequent use of radial artery grafts.Their smaller caliber closely resembles that of intracranial arter-ies and enhances the anastomosis. Although late patency rateswere not measured in this study, shorter grafts with arterial com-position are more likely to remain patent. Third, IC-IC bypasseseliminate neck incisions, reduce invasiveness, and improvecosmesis. Intracranial bypasses are less vulnerable than EC-ICbypasses to neck torsion, injury, and occlusion with external com-pression. Fourth, IC-IC bypasses eliminate the harvest of anextracranial donor artery, saving time and tedious effort. Intra -cranial donor arteries reside in the surgical field and requireminimal preparation. Finally, temporarily occluding an intracra-nial artery for bypass is well tolerated in the territories of mostIC-IC bypasses. In situ bypasses and reimplantations requiretemporary occlusion of 2 intracranial arteries to perform theanastomosis, instead of just 1 recipient artery with EC-IC bypass.However, neurophysiological changes were rarely encounteredduring these occlusions and always resolved with a boost in arte-rial pressure. We did not observe any neurological morbidity inthis patient series related to temporarily occluding an intracranialartery during anastomosis, or related to an intracranial donorartery that would not have been involved in an EC-IC bypass.

These advantages of IC-IC bypass justify their use. Althoughthey are more technically challenging to perform, they arewithin the expertise of experienced bypass neurosurgeons, andresult in elegant bypasses that we think represent the next gen-eration of bypass surgery for aneurysms.

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A1 ACA-MCA and MCA-PCAbypas ses has made them pre-ferred choices.

Selecting a bypass fromamong the 4 IC-IC techniquesdepends on aneurysm anat -omy, suitability of the donorartery, depth of the surgicalfield, and type of anastomosis.Fusiform aneurysms lendthemselves to reanastomosisbecause they are often distallylocated away from bifurca-tions, with 1 afferent and 1efferent artery. End-to-endrepair requires aneurysm exci-sion back to healthy arterialtissue on both ends, and join-ing ends without tension. Mo -bilizing the redundant arteryand resecting aneurysm canbring the arteries together.End-to-end anastomosis is theeasiest anastomosis: forcepstips in the lumen enable visu-alization of translucent arterialwalls and guidance of the nee-dle through its bites; the num-ber of bites needed to com-plete the anastomosis is less;and arteries rotate to visualizeboth suture lines.

In contrast to fusiform an eu -rysms, saccular aneu rysmswith multiple efferent arteriesrequire other reconstructivetechniques. In situ bypass andreimplantation revascularize 1efferent artery when the othercan be preserved with clip-ping. For example, the ACA-ACA bypass works when clip-ping or coiling an anteriorcommunicating artery aneu -rysm sacrifices 1 A2 ACA. Theother patent A2 ACA suppliesthe distal bypass and restoresflow to the opposite ACA.Side-to-side anastomosis isprobably the most difficult

anastomosis because the deep suture line is sewn inside thelumen. After approximating the 2 arteries with sutures at eachend of the arteriotomies, the first bite transitions the needle fromoutside the lumen where the knot is tied, to inside the lumenwhere running bites are taken. Bites are taken between 2 outerlayers of arterial wall, keeping track of 4 translucent layers. The

FIGURE 5. Intracranial bypass graft with double reimplantation. A, this ruptured right middle cerebral artery(MCA) aneurysm was coiled and recurred 6 months later (right internal carotid artery [ICA] angiogram, anterioroblique view). B, intraoperatively, the 2 M2 MCA trunks originated from the aneurysm (An) base and could not bekept open with direct clipping. Note the strand of coil in the lumen of the temporal M2 trunk (black arrow). C, theA1 segment of the anterior cerebral artery (ACA) was used as the donor for a radial artery graft (RAG) that wassutured with an end-to-side anastomosis (D and E). The frontal M2 trunk was reimplanted onto the RAG with a side-to-side anastomosis, (F) shown after suturing the deep suture line intraluminally and (G) after completing the super-ficial suture line. H, the end of the RAG was looped to the temporal M2 trunk and sewn with an end-to-side anas-tomosis. Postoperative angiography (right ICA injection, lateral [I] and anteroposterior [J] views) confirmed patencyof the bypass and filling of both MCA trunks (red arrows indicate anastomoses).

A B C

D E F

G H I J

Bypass SelectionMost current EC-IC bypasses convert to an IC-IC bypass pre-

sented in this clinical experience. ACA and PICA territorieswere particularly amenable to intracranial reconstruction, andeven though MCA and basilar apex territories were dividedbetween EC-IC and IC-IC techniques, growing experience with

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last bite transitions the needleagain from inside to outsidethe lumen to tie the knot. Thesecond suture line is per-formed from outside thelumen and is much easier. Thearteriotomy length should be3 times the diameter of thearteries in order to communi-cate generously between arter-ies. Conse quently, side-to-sideanastomoses require morebites than other anastomoses.This difficult anastomosisshould be avoided in deep,narrow surgical corridors, butcan be performed in the syl-vian fissure, cisterna magna,and interhemispheric fissure.

Reimplantation also sal-vages a branch artery compro-mised by aneurysm clippingwith an end-to-side anastomo-sis to the parent artery, theother efferent artery, or anuninvolved bystander. PICA-VA reimplantation was themost frequent location for thistechnique, but it works well inMCA and ACA territories(pericallosal-to-callosomar-ginal reimplantation) (Fig. 6).These recipient reimplanta-

FIGURE 6. Recipient reimplanta-tion. A, this thrombotic ACA aneu -rysm, seen on axial T1-weightedmagnetic resonance imaging scans,originated at the bifurcation of thepericallosal (PC) and callosomar-ginal (CM) arteries. B, right ICAangiogram, lateral view. C and D,the aneurysm (An) was exposed inthe interhemispheric fissure througha bifrontal craniotomy, using grav-ity to retract the right hemisphere(right hemisphere down; left hemi-sphere up; nose facing to the right).Attempts to clip reconstruct theneck were unsuccessful; intralumi-nal thrombus caused the clips toocclude the pericallosal artery. E,rather than opening the aneurysm,removing thrombus, and attempting

to reconstruct a neck, the pericallosal artery was clip occluded, transected, and mobilized to the callosomarginal artery. An end-to-side PC-CM anastomosis wasperformed: back wall (F), front wall (G), and after completion (H). I, the CM artery supplied blood flow to the entire distal ACA territory. Distal clip occlusionof the aneurysm resulted in its complete thrombosis.

A

D E

F G

H I

B C

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tions connect the proximal end of a branch to the side of donor,but donor reimplantations can also connect the distal end of abranch to a recipient artery to rededicate the branch artery tosupplying a new vascular territory. For example, ATA suppliesa silent vascular territory, and when reimplanted onto SCA, cansupply the SCA or basilar apex (Fig. 7). Reim planted arteries cantherefore donate or receive blood flow. The end-to-side anasto-mosis is identical to STA-MCA by pass, with a generous arteri-otomy in the donor (at least 2 times the diameter of the ar tery)

and a spatulated end of thereimplanted recipient to coverthe arteriotomy. Simple con-tinuous sutures are placedloosely and tightened after allbites have been taken. The siteof reimplantation is selected toslacken the reimplanted arteryand allow it to be shifted fromside to side to visualize bothsuture lines.

Complex reconstructionsare required when multipleefferent arteries are compro-mised by clipping. For exam-ple, the double reimplantationtechnique rebuilds a bifurca-tion with 3 anastomoses (Fig.5). A radial artery graft is firstconnected proximally to a do -nor artery to ready the bypassgraft. The first efferent arteryis reimplanted on the livegraft and blood flow is restor -ed immediately. The secondefferent artery is reimplanteddistally on the graft, allowingthe graft to supply the firstreimplanted artery during thissecond reimplantation. Place -ment of a temporary clip dis-tal to the first and proximal tothe second anastomosis redi-rects blood flow to the reim-planted trunk while keepingthe other surgical site dry. Thissuccessive reimplantation ofbranch arteries minimizes is -chemia, with temporary oc -clusion times for each of theefferent arteries equal to thetime needed to complete 1anastomosis. A double reim-plantation technique adapts totriple reimplantation for tri-furcated anatomy. Other intra -cranial bypass grafts replenish

cerebral blood flow with fewer anastomoses (Fig. 8). For exam-ple, the MCA-PCA bypass revascularizes quadrifurcatedanatomy of the basilar apex with a single deep anastomosis tothe P2 PCA and a superficial anastomosis to an MCA trunk thatis already exposed en route to the PCA site. Intracranial bypassgrafts such as the MCA-PCA bypass do not fully reconstructarterial anatomy and might not enable complete exclusion of theaneurysm, but might reverse flow or create more benign hemo-dynamics inside the aneurysm.

FIGURE 7. Donor reimplantation. A, a 55-year-old woman presented with subarachnoid hemorrhage from this mul-tilobulated left superior cerebellar artery (SCA) aneurysm, seen on rotational angiogram with 3-dimensional recon-struction. Only the superior lobule could be coiled, leaving residual neck to preserve the SCA origin. She wasreferred for surgery to protect her from rehemorrhage. After inspecting the anatomy intraoperatively, it seemedunlikely that the aneurysm could be clipped without occluding the SCA and likely that a bypass would be needed topreserve it. B, a prominent anterior temporal artery (ATA) was found in the sylvian fissure, and (C) it had sufficientlength to reach the SCA. D, ATA was transected distally and reimplanted onto the SCA with an end-to-side anasto-mosis. E, after bypass patency was confirmed, (F) the aneurysm (An) neck was dissected and clipped (G). H and I,indocyanine green videography confirmed good flow in the ATA-SCA bypass, as did the postoperative angiogram (leftICA injection, lateral view, with opacification of the left SCA [arrows]). Note the course of the SCA over the cerebel-lar vermis (red asterisk). The patient tolerated ATA sacrifice without neurological sequela. MCA, middle cerebralartery; ICA, internal carotid artery; PCA, posterior cerebral artery; CN3, oculomotor nerve.

A B C

D E F

G H I

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Bypass selection ultimately depends on an intraoperativeassessment of the aneurysm and surrounding anatomy. Wedevise a primary bypass strategy and several contingencystrategies, with preparations for each (such as prepping a graftsite). There might be several viable options (e.g., PICA-PICAbypass and PICA reimplantation), no options (e.g., P3 segment

PCA aneurysm), or serendipi-tous options (e.g., ATA-SCAbypass). We select the bypassthat facilitates an eu rysmocclusion, restores nor malblood flow, and is technicallymost feasible.

LimitationsOur conclusion that IC-IC

bypasses can replace manyEC-IC bypasses is based on acomparison between 2 groupsof patients that were differentand highly selected. This con-clusion applies to ACA, PICA,basilar apex, and many MCAaneurysms, but not to mostICA aneurysms. EC-IC by -passes will remain the pre-ferred choice for petrous, cav-ernous, and supraclinoid ICAaneurysms because they areeasier and less risky than thepetrous-to-supraclinoid ICAbypass. Therefore, the progres-sion from EC-IC to IC-ICbypass does not apply to allaneurysms. The STA-MCAbypass will remain a versatiletechnique, and we are not sug-gesting that it be abandoned.

Seventeen bypasses wereperformed in this clinical ex -perience, but several discus -sed here were not performed,such as the PCA-SCA andpetrous ICA-MCA bypasses.Indications for these bypassesare few and the technical de -mands are high. Other in -tracranial bypasses, such asSpetzler’s “figure 8 anastomo-sis,” (12a) were not a part ofour experience, but should beincluded in the menu of IC-ICbypasses. Innovation will addto this menu over time anddeepen our armamentariumof intracranial bypasses.

This study did not include patients in whom a plannedbypass was aborted. On several occasions, we found that P3PCA aneurysms were difficult to revascularize with intracra-nial reconstructive techniques because surgical corridors weredeep and narrow through all approaches (subtemporal, pos-terior interhemispheric, and supratentorial-infraoccipital).

FIGURE 8. Intracranial bypass graft. A, this fusiform, giant basilar trunk aneurysm (left vertebral artery [VA])angiogram, anterior oblique view) enlarged rapidly over a 2-year period, changing from a small, asymptomaticbump in the basilar trunk to a compressive mass with new hemiparesis, dysarthria, and gait instability. It was treatedwith a VA-to-superior cerebellar artery (SCA) bypass. B, a combined far lateral–temporal craniotomy provided a sub-temporal view of the basilar artery (BA) apex. C and D, a radial artery graft (RAG) was anastomosed to the rightSCA. E, the proximal end of the graft was connected to the side of extradural VA at the foramen magnum. F, thecourse of the VA-SCA bypass is shown intraoperatively (arrows) and (G) angiographically (right VA injection,anteroposterior view, with anastomoses indicated by the red arrows). VA-SCA bypass and clip occlusion of the rightVA resulted in thrombosis of the aneurysm lumen, shown preoperatively in blue and postoperatively in red on over-laid volumetric images generated from contrast-enhanced magnetic resonance angiography. H, lateral view. I, antero-posterior view. L, left; R, right; PCA, posterior cerebral artery.

A B C

D E F

G H I

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These aneurysms are increasingly treated with endovasculartechniques (24).

Bypass with aneurysm occlusion is a good strategy for giant,dolichoectatic, thrombotic, or previously coiled aneurysmsbecause it avoids the unpredictability of thrombectomy withclip reconstruction. It also avoids risky adjuncts such ashypothermic circulatory arrest. However, deliberate hemody-namic alteration with bypass and aneurysm occlusion can alsobe risky and unpredictable. Poor outcomes were encounteredwith flow reversal in basilar trunk aneurysms as a result ofbasilar artery thrombosis or occlusion of perforators. Othercomplications resulted from heparinization to decelerateaneurysm thrombosis, with subsequent intracranial hemor-rhage. Bypass with incomplete aneurysm occlusion relies onsome intraluminal aneurysm thrombosis, which has unavoid-able dangers. This management of basilar trunk aneurysmsmight not be the best strategy for this difficult disease. We arehopeful that stents or other endovascular devices will offerreconstructive options without open surgery, but these thera-pies are not available presently and will need to be evaluatedcritically before they replace surgical bypass strategies.

This experience demonstrates that old-fashioned microneu-rosurgery can be applied creatively to change the practice ofbypass surgery for complex aneurysms. Only suture and metic-ulous technique are needed to move from the current genera-tion of EC-IC bypasses to the next generation of IC-ICbypasses. New technology, such as ELANA (excimer laser-assisted nonocclusive anastomosis) (14) or automated staplers,will not facilitate most IC-IC bypasses. Instead, continued evo-lution will require mastering the simple craft of arterial anasto-mosis in all of its variations, and expending some extra effort tocreate more elegant and anatomic bypasses.

DisclosureThe authors have no personal financial or institutional interest in any of the

drugs, materials, or devices described in this article.

REFERENCES

1. Auguste KI, Quiñones-Hinojosa A, Lawton MT: The tandem bypass:Subclavian artery-to-middle cerebral artery bypass with dacron and saphe-nous vein grafts. Technical case report. Surg Neurol 56:164–169, 2001.

2. Ausman JI, Diaz FG: Critique of the extracranial-intracranial bypass study.Surg Neurol 26:218–221, 1986.

3. Barnett DW, Barrow DL, Joseph GJ: Combined extracranial-intracranialbypass and intraoperative balloon occlusion for the treatment of intracav-ernous and proximal carotid artery aneurysms. Neurosurgery 35:92–98, 1994.

4. Barnett HJ, Sackett D, Taylor DW, Haynes B, Peerless SJ, Meissner I,Hachinski V, Fox A: Are the results of the extracranial-intracranial bypasstrial generalizable? N Engl J Med 316:820–824, 1987.

5. Baskaya MK, Kiehn MW, Ahmed AS, Ates O, Niemann DB: Alternative vas-cular graft for extracranial-intracranial bypass surgery: Descending branchof the lateral circumflex femoral artery. Neurosurg Focus 24:E8, 2008.

6. Bederson JB, Spetzler RF: Anastomosis of the anterior temporal artery to asecondary trunk of the middle cerebral artery for treatment of a giant M1segment aneurysm. Case report. J Neurosurg 76:863–866, 1992.

7. Candon E, Marty-Ane C, Pieuchot P, Frerebeau P: Cervical-to-petrous inter-nal carotid artery saphenous vein in situ bypass for the treatment of a highcervical dissecting aneurysm: Technical case report. Neurosurgery 39:863–66, 1996.

SANAI ET AL.

682 | VOLUME 65 | NUMBER 4 | OCTOBER 2009 www.neurosurgery-online.com

8. EC/IC Bypass Study Group: Failure of extracranial-intracranial arterialbypass to reduce the risk of ischemic stroke. Results of an international ran-domized trial. The EC/IC Bypass Study Group. N Engl J Med 313:1191–1200, 1985.

9. Evans JJ, Sekhar LN, Rak R, Stimac D: Bypass grafting and revascularizationin the management of posterior circulation aneurysms. Neurosurgery55:1036–1049, 2004.

10. Friedman JA, Piepgras DG: Current neurosurgical indications for saphe-nous vein graft bypass. Neurosurg Focus 14:e1, 2003.

11. Goldring S, Zervas N, Langfitt T: The Extracranial-Intracranial Bypass Study.A report of the committee appointed by the American Association ofNeurological Surgeons to examine the study. N Engl J Med 316:817–820,1987.

12. Hadeishi H, Yasui N, Okamoto Y: Extracranial-intracranial high-flow bypassusing the radial artery between the vertebral and middle cerebral arteries.Technical note. J Neurosurg 85:976–979, 1996.

12a. Hanel RA, Spetzler RF: Surgical treatment of complex intracranialaneurysms. Neurosurgery SHC Suppl 3:SHC1289–SHC1299, 2008.

13. Kato Y, Sano H, Imizu S, Yoneda M, Viral M, Nagata J, Kanno T: Surgicalstrategies for treatment of giant or large intracranial aneurysms: Our expe-rience with 139 cases. Minim Invasive Neurosurg 46:339–343, 2003.

14. Langer DJ, Van Der Zwan A, Vajkoczy P, Kivipelto L, Van Doormaal TP,Tulleken CA: Excimer laser-assisted nonocclusive anastomosis. An emergingtechnology for use in the creation of intracranial-intracranial and extracra-nial-intracranial cerebral bypass. Neurosurg Focus 24:E6, 2008.

15. Lawton MT, Hamilton MG, Morcos JJ, Spetzler RF: Revascularization andaneurysm surgery: Current techniques, indications, and outcome. Neuro -surgery 38:83–94, 1996.

16. Lemole GM Jr, Henn J, Javedan S, Deshmukh V, Spetzler RF: Cerebral revas-cularization performed using posterior inferior cerebellar artery-posteriorinferior cerebellar artery bypass. Report of four cases and literature review.J Neurosurg 97:219–223, 2002.

17. Mohit AA, Sekhar LN, Natarajan SK, Britz GW, Ghodke B: High-flowbypass grafts in the management of complex intracranial aneurysms.Neurosurgery 60:ONS105–ONS123, 2007.

18. Morgan MK, Sekhon LH: Extracranial-intracranial saphenous vein bypassfor carotid or vertebral artery dissections: A report of six cases. J Neurosurg80:237–246, 1994.

19. Quiñones-Hinojosa A, Lawton MT: In situ bypass in the management ofcomplex intracranial aneurysms: Technique application in 13 patients.Neuro surgery 57:140–145, 2005.

20. Quiñones-Hinojosa A, Du R, Lawton MT: Revascularization with saphe-nous vein bypasses for complex intracranial aneurysms. Skull Base15:119–132, 2005.

21. Regli L, Piepgras DG, Hansen KK: Late patency of long saphenous veinbypass grafts to the anterior and posterior cerebral circulation. J Neurosurg83:806–811, 1995.

22. Relman AS: The extracranial-intracranial arterial bypass study: What havewe learned? N Engl J Med 316:809–810, 1987.

23. Rivet DJ, Wanebo JE, Roberts GA, Dacey RG Jr: Use of a side branch in asaph enous vein interposition graft for high-flow extracranial-intracranialbypass procedures. Technical note. J Neurosurg 103:186–187, 2005.

24. Sanai N, Tarapore P, Lee A, Lawton MT: The current role of microsurgery forposterior circulation aneurysms: A selective approach in the endovascularera. Neurosurgery 62:1236–1253, 2008.

25. Santoro A, Guidetti G, Dazzi M, Cantore G: Long saphenous-vein grafts forextracranial and intracranial internal carotid aneurysms amenable neither toclipping nor to endovascular treatment. J Neurosurg Sci 43:237–251, 1999.

26. Sekhar LN, Natarajan SK, Ellenbogen RG, Ghodke B: Cerebral revascular-ization for ischemia, aneurysms, and cranial base tumors. Neurosurgery 62[Suppl 3]:1373–1410, 2008.

27. Sundt TM Jr: Was the international randomized trial of extracranial-intracra-nial arterial bypass representative of the population at risk? N Engl J Med316:814–816, 1987.

28. Ustün ME, Büyükmumcu M, Ulku CH, Cicekcibasi AE, Arbag H: Radialartery graft for bypass of the maxillary to proximal middle cerebral artery:An anatomic and technical study. Neurosurgery 54:667–671, 2004.

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NEUROSURGERY VOLUME 65 | NUMBER 4 | OCTOBER 2009 | 683

morbidity and mortality. The comparison of these 2 groups is notentirely unbiased, as the aneurysm location and morphology will dic-tate the available options for revascularization. Nevertheless, the com-parison does demonstrate the utility of these innovative approachesand emphasizes the need to be versatile and creative in managing com-plex intracranial aneurysms. The use of IC-IC bypasses is particularlyuseful in cases where an unanticipated need for revascularizationoccurs during the course of an operation. IC-IC procedures do notrequire as much preoperative planning as EC-IC bypasses, owing to theneed for preparation of the extracranial donor vessel in the latter.

As the population of intracranial aneurysms presenting for surgicalmanagement becomes increasingly complex, the technical skills andinnovation of cerebrovascular surgeons will be increasingly challenged.This excellent article, which reviews these elegant vascularizationoptions, clearly indicates that this group is meeting the challenge.

Daniel L. BarrowAtlanta, Georgia

The authors report their experience with IC-IC bypass techniques forthe treatment of complex aneurysms that cannot be coiled or

clipped without revascularization. The data show that IC-IC bypassesperform comparably to EC-IC bypasses in terms of patient safety, out-come, and efficacy. However, both groups were highly selected, and thedata cannot be used to support “progression toward vascular recon-struction that is entirely intracranial” unless the indications and favor-able anatomic factors for IC-IC bypass are present. In some instances,the flow provided by an IC-IC bypass may be inadequate, as in thetreatment of basilar trunk aneurysms with flow reversal. Conversely,this technique appears particularly attractive for middle cerebral artery,anterior cerebral artery, and posteroinferior cerebellar artery-to-posteroinferior cerebellar artery bypasses.

In our experience, IC-IC bypasses have been similarly useful, espe-cially in challenging cases in which the patient’s anatomy is appropri-ate. However, with both donor and recipient territories at risk in the rareevent of bypass occlusion or with extended cross-clamping, our firstpreference is for clip reconstruction of the aneurysm versus suitableEC-IC bypass. Finally, the authors’ experience reinforces that a com-bined approach is often needed when an aneurysm cannot be treated byendovascular or standard microsurgical techniques alone. The authorshave presented a thorough, clear description of their impressive expe-rience with IC-IC bypass, including relevant technical notes, indica-tions, and rationales for the different challenging cases depicted.

Rasha GermainRobert F. SpetzlerPhoenix, Arizona

29. Yasargil MG: Anastomosis between the superficial temporal artery and abranch of the middle cerebral artery, in Yasargil MG (ed): MicrosurgeryApplied to Neurosurgery. Stuttgart: Georg Thieme-Verlag, 1969, pp 105–115.

30. Zhang YJ, Barrow DL, Day AL: Extracranial-intracranial vein graft bypassfor giant intracranial aneurysm surgery for pediatric patients: Two techni-cal case reports. Neurosurgery 50:663–668, 2002.

COMMENTS

anai et al. have made an excellent contribution to the literature.They report a number of creative microsurgical solutions to difficult

neurovascular pathologies. Clearly, the types of aneurysmal diseaseillustrated do not have acceptable endovascular options with existingtechnology. This type of creative approach represents a transition in theway microvascular surgeons conceptualize neurovascular anatomy. Inthe early days of microvascular surgery, the focus was on recreatingnormal anatomy by complex clip reconstructions even if prolongedtemporary arterial occlusion was required. It became obvious that per-fect reconstructions were not always possible or posed substantialischemic risks. The use of extracranial-intracranial (EC-IC) bypassgrafts with the superficial temporal artery, saphenous vein, or radialartery clearly advanced the field.

This contribution may eliminate the need for cervical dissections forproximal anastomoses in some cases and, in many circumstances, mayobviate the need for graft harvest. The tradeoff for using an intracranialinterposition graft is the requirement to put 2 different vascular terri-tories at risk during the creation of the bypass. Perhaps nontraditionalanastomoses, such as the excimer laser-assisted nonocclusive anasto-mosis technique, will reduce this risk in selected cases. This article willbe a valuable reference to cerebrovascular and cranial base surgeons asthey search for solutions in complex vascular cases.

Christopher S. EddlemanBernard R. BendokH. Hunt BatjerChicago, Illinois

This article represents yet another outstanding contribution from thecerebrovascular surgery group at the University of California, San

Francisco. The authors report a retrospective review of a decade ofexperience in managing patients with complex intracranial aneurysmsusing either EC-IC or intracranial-intracranial (IC-IC) bypasses. Indoing so, they report on a number of bypass techniques that were pre-viously undescribed, the subject of case reports, or reported in verysmall case series. In an interesting comparison of the outcome ofpatients undergoing EC-IC versus IC-IC bypass, it is clear that theresults are quite similar and associated with a low risk of operative

S