Revascularization and Aneurysm Surgery .4

Revascularization and Aneurysm Surgery:Techniques, Indications, and Outcomes in theEndovascular Era

BACKGROUND: Given advances in endovascular technique, the indications for revas-cularization in aneurysm surgery have declined.OBJECTIVE: We sought to define indications, outline technical strategies, and evaluatethe outcomes of patients treated with bypass in the endovascular era.METHODS: We retrospectively reviewed all aneurysms treated between September2006 and February 2013.RESULTS: We identified 54 consecutive patients (16 males and 39 females) with 56aneurysms. Aneurysms were located along the cervical internal carotid artery (ICA)(n = 1), petrous/cavernous ICA (n = 1), cavernous ICA (n = 16), supraclinoid ICA (n = 7),posterior communicating artery (n = 2), anterior cerebral artery (n = 4), middle cerebralartery (MCA) (n = 13), posterior cerebral artery (PCA) (n = 3), posterior inferior cerebellarartery (n = 4), and vertebrobasilar arteries (n = 5). Revascularization was performed withsuperficial temporal artery (STA) to MCA bypass (n = 25), STA to superior cerebellar artery(SCA) (n = 3), STA to PCA (n = 1), STA-SCA/STA-PCA (n = 1), occipital artery (OA) to PCA(n = 2), external carotid artery/ICA to MCA (n = 15), OA to MCA (n = 1), OA to posteriorinferior cerebellar artery (n = 1), and in situ bypasses (n = 8). At a mean clinical follow-upof 18.5 months, 45 patients (81.8%) had a good outcome (Glasgow Outcome Scale 4 or5). There were 7 cases of mortality (12.7%) and an additional 9 cases of morbidity (15.8%).At a mean angiographic follow-up of 17.8 months, 14 bypasses were occluded.Excluding the 7 cases of mortality, the majority of aneurysms (n = 42) were obliterated.We identified 7 cases of residual aneurysm and recurrence in 6 patients at follow-up.CONCLUSION: Given current limitations with existing treatments, cerebral revascular-ization remains an essential technique for aneurysm surgery.

KEY WORDS: Aneurysm, Bypass, Cerebral revascularization, Clipping, Endovascular, Extracranial-to-intracranial,

Intracranial-to-intracranial

Neurosurgery 74:482–498, 2014 DOI: 10.1227/NEU.0000000000000312 www.neurosurgery-online.com

When we last published the BarrowNeurological Institute experience withrevascularization for aneurysm surgery

in 1996,1 Guglielmi detachable coils had onlyrecently been approved for use, and endovascular

techniques were in their infancy.2-4 Over thepast 2 decades, there has been rapid growth andadvancements in the field of endovascular neu-rosurgery, and these techniques have become analternative to microsurgery for the treatment ofcerebral aneurysms.5,6 During the same period,the negative results of the Carotid OcclusionSurgery Study (COSS) trial7 and the introductionof flow-diverting stents8,9 have resulted in manypractitioners rethinking the utility of cerebralrevascularization for vascular pathologies.Given the paradigm shift of the past 2 decades,

we sought to reevaluate the role of revasculariza-tion in the treatment of complex cerebral aneur-ysms in the modern endovascular era, as well as

M. Yashar S. Kalani, MD, PhD

Wyatt Ramey, MD

Felipe C. Albuquerque, MD

Cameron G. McDougall, MD

Peter Nakaji, MD

Joseph M. Zabramski, MD

Robert F. Spetzler, MD

Division of Neurological Surgery, Barrow

Neurological Institute, St. Joseph’s Hospi-

tal and Medical Center, Phoenix, Arizona

Correspondence:

Joseph M. Zabramski, MD,

c/o Neuroscience Publications,

Barrow Neurological Institute,

St. Joseph’s Hospital and Medical Center,

350 W Thomas Rd, Phoenix, AZ 85013.

E-mail: [email protected]

Received, September 6, 2013.

Accepted, January 28, 2014.

Published Online, February 10, 2014.

Copyright © 2014 by the

Congress of Neurological Surgeons.

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ABBREVIATIONS: ACA, anterior cerebral artery;

aSAH, aneurysmal subarachnoid hemorrhage;

BTO, balloon test occlusion; GOS, Glasgow Out-

come Scale; ICA, internal carotid artery; MCA,

middle cerebral artery; OA, occipital artery; PCA,

posterior cerebral artery; PComm, posterior com-

municating artery; PICA, posterior inferior cerebel-

lar artery; SCA, superior cerebellar artery; STA,

superficial temporal artery

RESEARCH—HUMAN—CLINICAL STUDIESTOPIC RESEARCH—HUMAN—CLINICAL STUDIES

482 | VOLUME 74 | NUMBER 5 | MAY 2014 www.neurosurgery-online.com

Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited

review the indications and evaluate the outcomes of patientstreated by using bypass surgery and either microsurgical, endo-vascular, or combined techniques.

METHODS

Patient Population

Between September 2006 and February 2013, 55 patients with 56complex cerebral aneurysms were treated with surgery, endovasculartechnique, or a combination and cerebral revascularization (Table 1).There were 16 males and 39 females, with an average age of 46.1 years(median, 49; range, 1-77 years). Medical records, neurological exami-nations, and radiographic studies were retrospectively reviewed. Pre- andpostoperative neurological function was evaluated with the use of theGlasgow Outcome Scale (GOS) score.

Presentation

Themost common presentation was headache, observed in 23 patients.Other presenting symptoms included transient ischemic attacks, altered

mental status, cranial nerve palsies, and other symptoms suggestive ofmasseffect. Seven patients had their aneurysms identified incidentally duringa workup for nonrelated symptoms. Eleven patients presented owing toaneurysmal subarachnoid hemorrhage (aSAH). An additional 3 patientshad a previous history of aSAH that led to the identification of theiraneurysm.Of patients with aSAH, theHunt andHess grade10 was II in 3patients, III in 5 patients, IV in 1 patient, and V in 1 patient. In 1 patientunder the age of 1, a Hunt and Hess grade was not assigned. Anadditional patient presented owing to subarachnoid hemorrhage after aniatrogenic internal carotid artery (ICA) injury. Twelve cases werepreviously treated by the use of microsurgery (n = 6), endovascular(n = 5), or combined techniques (n = 1).

Aneurysm Location and Characteristics

There were 24 aneurysms on the right side and 27 aneurysms on the leftside. Five aneurysms were located on the basilar artery. The average size ofthe aneurysms was 23 mm. There were 27 giant aneurysms and 18 largeaneurysms. Themajority of the aneurysms were saccular (n = 35, 62.5%),followed by fusiform (n = 16, 28.6%). Aneurysms were located along thecervical ICA (n = 1), petrous/cavernous ICA (n = 1), the cavernous ICA

TABLE 1. Summary of Patient Characteristics in This Seriesa

Patient characteristics

Total patients 55

Total aneurysms 56

Sex

Male 16

Female 39

Age, y, mean 46.1

Age, y, range 1-77

Aneurysm characteristics, n (%)

Ruptured aneurysm 12 (21.4)

Unruptured aneurysm 44 (78.6)

Saccular aneurysm 35 (62.5)

Fusiform aneurysm 16 (28.6)

Dissecting aneurysm 1 (1.8)

Mycotic aneurysm 2 (3.6)

Blister aneurysm 1 (1.8)

Pseudoaneurysm 1 (1.8)

Aneurysm, mm, mean 23

Aneurysm, mm, range 3-43

Aneurysm location, n (%)

Cervical ICA 1 (1.8)

Petrous ICA 1 (1.8)

Cavernous ICA 16 (28.6)

Supraclinoid ICA 7 (12.5)

PComm 2 (3.6)

ACA 4 (7.1)

MCA 13 (23.2)

PCA 3 (5.3)

PICA 4 (7.1)

Vertebrobasilar 5 (8.9)

Total 56

aICA, internal carotid artery; ACA, anterior cerebral artery; MCA, middle cerebral

artery; PCA, posterior cerebral artery; PComm, posterior communicating artery;

PICA, posterior inferior cerebellar artery.

TABLE 2. Summary of Treatment Modalities and Revascularization

Techniques Used to Treat Complex Cerebral Aneurysmsa

n %

Bypass characteristics

STA-MCA 25 43.9

STA-SCA 3 5.3

STA-PCA 1 1.8

STA-PCA-SCA 1 1.8

PCA-OA 2 3.5

ECA/ICA-MCA 15 26.3

OA-MCA 1 1.8

OA-PICA 1 1.8

In situ 8 14

Total 57

Previous treatments

Microsurgical 6

Endovascular 5

Combined 1

Balloon test occlusion

Performed 18

Passed 12

Failed 6

Treatment strategies

Clip 2 3.5

Trapping 11 19.3

Proximal vessel occlusion 14 24.6

Distal vessel occlusion 9 15.8

Excision 6 10.5

Basilar occlusion 5 8.8

Bypass only 3 5.3

Other strategies 7 12.3

aSTA, superficial temporal artery; MCA, middle cerebral artery; SCA, superior

cerebellar artery; PCA, posterior cerebral artery; OA, occipital artery; ECA, external

carotid artery; ICA, internal carotid artery; PICA, posterior inferior cerebellar artery.

REVASCULARIZATION AND ANEURYSM SURGERY

NEUROSURGERY VOLUME 74 | NUMBER 5 | MAY 2014 | 483


(n = 16), supraclinoid ICA (n = 7), posterior communicating artery(PComm) (n = 2), anterior cerebral artery (ACA) (n = 4), middle cerebralartery (MCA) (n = 13), posterior cerebral artery (PCA) (n = 3), posteriorinferior cerebellar artery (PICA) (n = 4), and vertebrobasilar arteries (n = 5).

Diagnostic Evaluation and Criteriafor Revascularization

Although recent advances in 3-D angiography have greatly facilitatedthe determination of whether an aneurysm can be clipped, intraoperativeexploration remains the gold standard. If during intraoperative evaluationthe surgeon concluded that the aneurysm could not be directly clipped orclip reconstructed, a decision to perform vessel sacrifice in the form ofproximal or distal vessel occlusion, excision, or trapping was made.Our institutional preference is to perform a bypass in all patients

requiring acute vessel sacrifice for management of an aneurysm. The typeof bypass performed (high-flow or low-flow) depends on the location ofthe aneurysm and available collateral circulation. Imaging assessment ofpatients included combinations of magnetic resonance imaging, magneticresonance angiography, computed tomographic angiography, and digitalsubtraction angiography. Balloon test occlusion (BTO) is not a routinepart of our workup in these cases and was performed in only 18 of 55

patients in this series, some of whom were initially being considered forendovascular management.

Perioperative Treatment Paradigm

Preoperatively, patients are placed on aspirin (325 mg/d) beforeintervention, and the dose is continued postoperatively. Some patientshad a short postoperative course of heparin to prevent sudden thrombosisof their aneurysm. Electroencephalographic monitoring was conductedintraoperatively. We perform revascularization procedures under mildhypothermia and barbiturate protection. Table 2 outlines the treatmentstrategies used in treating these patients. Intraoperative evaluation ofbypass patency and treatment were confirmed by using indocyaninegreen videoangiography or intraoperative angiography.

RESULTS

Bypass Procedures and Patency

We performed a total of 57 cerebral revascularization proce-dures in 55 patients. Revascularization was performed withsuperficial temporal artery (STA)-MCA bypass (n = 25), STA-superior cerebellar artery (SCA) (n = 3), STA-PCA (n = 1), STA-SCA/STA-PCA (n = 1), occipital artery (OA)-PCA (n = 2),external carotid artery/ICA-MCA (n = 15; 14 using a radial arteryand 1 using a saphenous vein graft), OA-MCA (n = 1), OA-PICA(n = 1), and in situ bypasses (n = 8). At a mean angiographicfollow-up of 17.8 months (median, 11 months; range 1-72months) graft occlusion was identified in 14 patients (Table 3).In 7 cases, bypass occlusion did not result in significantmorbidity, and the patients were noted to be independent(GOS 4 or 5) at last follow-up. Bypass patency information wasnot available in 3 cases. The remaining bypasses (n = 42)remained patent.

Aneurysm Fate

In the surviving patients, we identified residual aneurysm in6 patients (7 aneurysms) at last follow-up. Angiographic follow-updocumenting aneurysm fate was available for all patients. Theremaining 42 aneurysms were completely occluded. The aneur-ysms with residual filling included 4 cases of basilar trunk/tipaneurysms (one of whomdied andwas excluded from the analysis),2 giant cavernous ICA aneurysms, 1 giant proximal MCAaneurysm, and 1 case of a small fusiform A2 segment aneurysmthat did not exhibit evidence of growth after treatment but did notregress on angiographic follow-up.

Complications and Outcomes

At a mean clinical follow-up of 18.5 months (median, 9.5months; range 1-72 months), 45 patients (81.8%) had a goodoutcome (GOS 4 or 5). Seven patients (12.5%) died (Table 4). Sixdeaths were related to postoperative stroke; in 5 of these 6 patients,stroke was associated with occlusion of the bypass, whereas, in 1case, a giant basilar aneurysm, the patient experienced a massivebrainstem infarct despite a patent bypass. There was 1 deathsecondary to medical complications. Six patients had asymptomatic

TABLE 3. Summary of Patient Outcomes, Including Bypass Patency

and Aneurysm Fatea

Patient outcomes

Mean clinical follow-up, mo 18.5

Median clinical follow-up, mo 9.5

GOS 4-5, n (%) 45 (81.8)

GOS ,4, n (%) 11 (18.2)

Aneurysm and bypass outcomes

Mean angiographic follow-up, mo 17.8

Median angiographic follow-up, mo 11 mos

Bypass patency, n (%) 42 (73.7)

Bypass occluded, n (%) 12 (21.1)

Bypass status unknown, n (%) 3 (5.2)

Obliterated aneurysm, n (%) 42 (85.7)b

Residual aneurysm, n (%) 7 (14.3)b

Aneurysm fate unknown, n (%) 1 (2)b

aGOS, Glasgow Outcome Scale.bExcluding 7 cases of mortality.

TABLE 4. Summary of Morbidity and Mortality Noted With

Revascularization as a Treatment Strategy

n %

Perioperative mortality 7 12.7

Perioperative morbiditya 9 15.8

Cerebrovascular accident 6 10.5

Infection 1 1.8

Extra-axial hemorrhage 1 1.8

Unilateral blindness 1 1.8

aCalculated based on 57 procedures.

KALANI ET AL



FIGURE 1. A 71-year-old woman presents with a pulsatile neck mass. Anteroposterior (A) and axial magneticresonance angiography (MRA) (B) reveal a 2.7-cm left cervical internal carotid artery (ICA) aneurysm. C, post-operative MRA reveals good distal flow in the ICA. Used with permission from Barrow Neurological Institute.




strokes (10.5%). Additional morbidity occurred in 3 patients(5.4%), including 1 case of intracranial abscess, 1 extra-axialhematoma, and 1 case of postoperative blindness.

DISCUSSION

Bypass Surgery for Complex Aneurysms

With the expanding repertoire of endovascular tools, theindications for cerebral revascularization for aneurysm surgeryhave significantly decreased. Endovascular therapy has becomea mainstay of treatment for most posterior circulation aneurysms,and the introduction of the pipeline embolization device (EV3,Inc, Irvine, California) and other flow-diverting stents has allowedfor a less-invasive alternative to bypass and vessel sacrifice for

proximal ICA aneurysms.5,6,8,11,12 Indeed, at our own institution,upon approval of the pipeline embolization device, there has beena significant decrease in the use of bypass for treatment of complexICA aneurysms, and the majority of these lesions are now referredfor endovascular consideration (data not shown). Should theselesions be deemed inappropriate for endovascular treatment, theyare then considered for surgical management. The data on the useof flow diverters in the posterior circulation are less convincing andtoo sparse to make definitive recommendations regarding the useof these devices in the posterior circulation.Despite these advances, however, aneurysms remain that

either fail, or are not appropriate candidates for, endovasculartreatment. The results from several large series suggest thatendovascular techniques are associated with a high recurrence

FIGURE 2. A 54-year-old woman presents with a several-month concern of diplopia. A, axial computed tomographic angiography (CTA) demonstrates a 3.2-cm left cavernousinternal carotid artery (ICA) aneurysm. Postoperative anteroposterior (B) and lateral ICA angiography (C) reveal stasis within the aneurysm after proximal clip occlusion and distalbypass.D, oblique external carotid artery angiography reveals a patent bypass. E, postoperative CTA demonstrates thrombosis of the aneurysm without evidence of flow. F, drawingdemonstrates the treatment strategy used for petrous ICA aneurysms where proximal occlusion with distal revascularization may be used as a treatment strategy. This same strategycould be applied for cavernous and supraclinoid ICA aneurysms. Figure 2F was modified from Lawton MT, Hamilton, MG, Morcos JJ, Spetzler, RF. Revascularization andaneurysm surgery: current techniques, indications, and outcome. Neurosurgery 1996;38(1):83-94. Used with permission from Barrow Neurological Institute.

KALANI ET AL



rate, especially in patients with large and giant aneurysms.13-15

Flow-diverting stents have also been associated with perforatorinfarcts,16-18 and their use in the setting of aSAH remainsa matter of continued debate.19,20 One of the most promisingindications for flow-diverting stents, their application in the

treatment of fusiform posterior circulation aneurysms, has beenassociated with high rates of morbidity and mortality.16,18

Finally, at least a subset of patients is not medically able totolerate the dual-antiplatelet regimen necessary for the use ofstents.21

FIGURE 3. A 71-year-old woman with a known right posterior communicating artery aneurysm with multiple previousendovascular coil embolizations presents for surgical treatment. Anteroposterior (A) and lateral internal carotid artery (ICA)angiography (B) reveal a partially coiled 2.6-cm aneurysm. The patient was taken to the operative theater for trapping of theaneurysm with ICA to middle cerebral artery (MCA) bypass with a radial artery graft. C, postoperative oblique neck and headangiography reveals flow proximal and distal to the point of trapping. D, right common carotid artery angiography demonstratesa patent bypass with robust filling of the distal MCA territory. Used with permission from Barrow Neurological Institute.




Given the limitations of existing endovascular techniques andthe inability to primarily clip a subset of complex cerebralaneurysms, there remains a clear indication for Hunterian ligation

in the treatment of complex cerebral aneurysms. In historicalseries, surgical occlusion of the carotid artery for the managementof intracranial aneurysms was associated with infarction in up to

FIGURE 4. A 1-year-old girl was referred to our vascular service. A, computed tomography reveals aneurysmal subarachnoidhemorrhage. Sagittal computed tomographic angiography (CTA) (B) nd 3-D reconstruction of the CTA (C) demonstrate a 2-cmaneurysm involving the A2 segment of the anterior cerebral artery. The patient was taken to the operative theater for excision ofthe aneurysm with reimplantation of the right frontopolar branch to left A2.D, 3-D reconstruction of the CTA demonstrates thein situ bypass strategy used. E, anteroposterior internal carotid artery angiography reveals flow in the reimplanted vessel withoutevidence of residual aneurysm. Used with permission from Barrow Neurological Institute.

KALANI ET AL



40%of cases.22 BTO has been used by some groups in an attemptto determine whether it is safe to occlude a cerebral vessel;however, the BTO test itself is not without risks, and predictiveresults are less than perfect. Complications following BTOinclude dissections, embolic complications, and pseudoaneur-ysms in 0% to 8% of cases.23 Several studies of ICA occlusionfollowing BTO have documented stroke morbidity rates of 1.5%to 4.8% with ongoing ischemia in 10% to 12% of patients24-27

and delayed ischemia rates of 1.4% per year.28

In addition to ongoing ischemic risks, the sacrifice of a majorcerebral vessel increases the risk of flow-related aneurysms incollateral branches. De novo aneurysm formation in the collateralcirculation of patients undergoing Hunterian ligation withoutrevascularization has been estimated to be 10%.1

Several groups have combined BTO with measurements ofcerebral blood flow to improve the predictive accuracy of thistest.29-32 Others have used intraoperative blood flow measure-ments to determine the need for bypass and the extent of flowaugmentation necessary with good results.33

Although each of these techniques has its proponents, ourinstitutional preference has been to perform a bypass in all patientsrequiring acute vessel sacrifice for management of an aneurysm. Ingeneral, our strategy has been to assess the extent of collateral flowangiographically. When ample collaterals are present, or the flowdemand is limited (eg,when only 1M2branchof theMCAneeds tobe sacrificed), we favor a low-flow (eg, STA-MCA) bypass. Whencollaterals are absentordiminutive (eg, thepatientwithahypoplasticor absent A1 segment on the side of planned carotid occlusion), wefavor a high-flow bypass. When ICA occlusion is being consideringfor the treatment of a complex aneurysm, simple manual compres-sion of the carotid artery in the neck during angiography can providea quick assessment of available collateral flow for determiningwhether to perform a low-flow or high-flow bypass.

Several series have documented favorable outcomes ranging from50% to 93% in the treatment of complex cerebral aneurysms withmicrovascular bypass.1,34-43 In our current series, we noted a favor-able outcome in 81.8% of patients. It is difficult to directly comparedifferent series across different eras. In the present endovascular era,patients are referred for microsurgical treatment only whenendovascular treatment of their aneurysm has failed, or when theyhave been deemed poor candidates for endovascular therapy.

Pathology-Specific Considerations

Our management strategy for aneurysms at specific sites isdiscussed below.

Aneurysms of the Precavernous ICA

Depending on the level, aneurysms of cervical ICA can betreated by direct excision and reconstruction or proximalocclusion and distal bypass (Figure 1).44 When acute carotidocclusion is necessary, revascularization often requires a high-flow bypass (saphenous vein or radial artery graft); however, inpatients with a good collateral supply via the anteriorcommunicating complex, and/or a large posterior communi-cating artery, an STA-MCA bypass can be considered for simpleaugmentation of flow.45

Aneurysms of the Cavernous ICA

Aneurysms of the cavernous carotid artery are extradural andencompassed by an unforgiving maze of neurovascular structures.The practice of opening the cavernous sinus to directly clip theseaneurysms is now of historical value.46,47 In cases not amenable tothe use of flow-diverting stents, these aneurysms can be treatedvia proximal or distal ICA occlusion combined with distalbypass.48-50 When adequate collaterals are present, a low-flowbypass is sufficient (Figure 2).

Aneurysms of the Supraclinoid ICA

Aneurysms of the supraclinoid ICA present a risk of SAH thatmay be increased with changes in flow that do not result inthrombosis, and are preferentially treated via trapping. Othertreatment options include proximal or distal vessel occlusion andaugmentation with a bypass.45,51

Aneurysms of the Posterior Communicating ICA

In this series, both aneurysms involving this segment of the ICAwere treated by using a combination of trapping and high-flowbypass to theMCAwith the use of a radial artery graft (Figure 3).52

A low-flow bypass may be permissible in such cases if adequatecollaterals are available.

FIGURE 5. A 41-year-old woman presents with headaches and dizziness. Anteroposterior (A) and lateral internal carotid artery angiography(B) reveal a 1-cm mycotic right distal middle cerebral artery (MCA) aneurysm.C, 3-D reconstruction of the angiographic images reveals multiplebranches arising from the diseased segment of the vessel. D & E, illustrations demonstrating 2 alternate treatment strategies used with MCAaneurysms. Given the rich network of perforators arising from the proximal MCA, it is not possible to trap the majority of unclippable aneurysmsarising from this segment of the vessel. In approaching MCA aneurysms, occlusion of the proximal inflow (D) or the distal outflow (E) of theaneurysm can be combined with distal revascularization. Although we prefer occlusion of the inflow to the aneurysm by placing a clip proximal tothe aneurysm, this may not always be possible. In this case, we placed a clip distal to the aneurysm and revascularized the distal territory of thevessel via a superficial temporal artery-MCA bypass. F, Alternatively, a branch of the MCA can be transposed from the diseased segment ontoa healthy branch. This is illustrated by the transposition of the anterior temporal artery from 1 branch of the MCA harboring an aneurysm ontoa healthy vessel in the vicinity. G, follow-up axial computed tomographic angiography demonstrates resolution of the aneurysm. Figure 5F wasmodified from Lawton MT, Hamilton, MG, Morcos JJ, Spetzler, RF. Revascularization and aneurysm surgery: current techniques, indications,and outcome. Neurosurgery 1996;38(1):83-94. Used with permission from Barrow Neurological Institute.

KALANI ET AL



Aneurysms of the ACA

Aneurysms of the ACA can be treated via excision of theaneurysm followed by direct end-to-end repair of the vessel or viaan in situ bypass to an adjacent vessels (Figure 4).53,54 The ACAdistribution can also be revascularized by using the STA.55,56 Incases where the aneurysm involves the A2 segment, proximalocclusion combined with a distal A3-A3 (side-to-side) bypass canbe used.57

Aneurysms of the MCA

Proximal MCA aneurysms can be treated via proximal or distalvessel occlusion with a low-flow or high-flow bypass (Figure 5).34

Given the extensive network of lenticulostriate arteries arisingfrom this segment, trapping is usually not feasible. The decisionto perform a STA-MCA or a radial artery interposition graft fromthe ICA to MCA depends primarily on the caliber of the STA.Trapping or excision and direct vessel reconstruction are possiblewhen the aneurysm arises distal to the lenticulostriate perforators.Various combinations of in situ and STA-MCA bypasses can alsobe used (Figure 5).58,59

Aneurysms of the PCA

Complex aneurysms involving the P2 and/or P3 segments of thePCA are most commonly treated by proximal or distal parentvessel occlusion (Figure 6). Visual impairments are a major risk in

FIGURE 6. A 7-year-old boy presents with headache and lethargy. A, axial T1-weighted magnetic resonance imaging (MRI) reveals a 1.5-cm left-sided lesion withcompression of the brainstem. Anteroposterior (B) and lateral vertebral artery (C) angiography reveals a fusiform giant posterior cerebral artery (PCA) aneurysm. Balloon testocclusion failed in this patient, and he was referred for surgical treatment. Revascularization of the distal PCA was performed via a superficial temporal artery-PCA bypass.Following the bypass, a clip was applied to the PCA distal to the aneurysm. D, postoperative axial computed tomographic angiography demonstrates the placement of theaneurysm clip distal to the aneurysm, with significant reduction in the mass of the aneurysm noted. Postoperatively, the patient had a cerebrovascular accident from which hemade a complete recovery. E, follow-up axial T1-weighted MRI reveals resolution of the mass effect. The patient remains asymptomatic. Used with permission from BarrowNeurological Institute.




such cases, and, although distal bypass (OA-PCA) to augmentflow is possible,60 an analysis of our experience revealed a higherthan expected rate of complications associated with this pro-cedure.61 In this subset of patients, we recommend BTO as partof the preoperative assessment and reserve revascularization forthose for whom this test fails.

Aneurysms of the PICA

Unclippable aneurysms of PICA are usually fusiform. Theseaneurysms can be treated by trapping, or by proximal or distalvessel occlusion, with bypass. A variety of bypasses are availablefor revascularization of the PICA territory, including the OA-PICA bypass62,63 and the PICA-PICA (side-to-side) bypass

FIGURE 7. A 53-year-old woman with a medical history significant for hypertension was referred to our neurovascular service forconsultation. Anteroposterior (A) and lateral vertebral artery angiography (B) demonstrate a large basilar apex aneurysm thatincorporates the bilateral posterior cerebral arteries (PCAs) and superior cerebellar arteries (SCAs). The patient had a previouslyattempted superficial temporal artery (STA)-SCA bypass and partial occlusion of the basilar artery. Despite this treatment paradigm,the aneurysm continued to enlarge and the bypass occluded. The patient was taken to the operative theater for revascularization of thebasilar apex and complete occlusion of the basilar artery. There are various options for revascularization of the basilar apex. One canperform a STA-PCA (C), STA-SCA (D), or a double-barrel STA-SCA-PCA (E) bypass. For flow reduction, the various optionsinclude placing a clip below the SCA on the perforator-free zone of the basilar artery or clipping the vertebral arteries. When clippingthe vertebral arteries, we prefer to clip 1 above and 1 below the takeoff of the posterior inferior cerebellar arteries. In this patient, weused the strategy depicted in E. Postoperatively, axial computed tomographic angiography demonstrated the patency of the bypass(white arrow) between the left parietal branch of the STA (black and white arrow) and the left SCA (arrowhead) (F) and the leftfrontal branch of the STA (arrow) and the left PCA (arrowhead) (G) Postoperatively, the patient’s bypass was occluded in a delayedfashion and the patient suffered brainstem infarction. Used with permission from Barrow Neurological Institute.

KALANI ET AL



TABLE 5. Detailed Patient and Aneurysm Informationa

Patient

ID Age Sex Location Aneurysm Type Treatment Bypass Type Graft

Bypass

Patency Morbidity & Mortality

Aneurysm

Outcome

1 27 F A2 Fusiform Proximal ICA clip

occlusion

STA-MCA Y No evidence of

growth of

fusiform

segment

2 17 M M2-M3 Fusiform Excision ICA-MCA RAG N Obliterated

3 51 M M1 Saccular Trapping STA-MCA double

barrel

Y Obliterated

4 45 F M2 Fusiform Trapping STA-MCA Y Obliterated

5 17 M P2 Fusiform Distal coil occlusion OA-PCA Y Obliterated

6 71 F PComm Saccular Trapping ICA-MCA RAG Y Obliterated

7 53 F Cavernous ICA Saccular Distal ICA clip

occlusion

STA-MCA Y Obliterated

8 67 M Supraclinoid ICA Fusiform Excision ICA-MCA RAG Y Obliterated

9 17 F Cavernous ICA Saccular Coil decompression STA-MCA onlay N Obliterated

10 53 F Supraclinoid ICA Saccular — STA-MCA N —

53 F Supraclinoid ICA Saccular Distal ICA clip

occlusion

ICA-MCA RAG N/A Obliterated

11 49 M Supraclinoid ICA Fusiform Trapping ICA-MCA RAG Y Obliterated

12 78 F Cavernous ICA Saccular Distal subtotal ICA clip

occlusion


13 48 F Cavernous ICA Saccular Proximal ICA clip

occlusion

STA-MCA Y Residual

14 42 F Supraclinoid ICA Blister Trapping ICA-MCA RAG N Bypass thrombosis

postop, CVA, death

N/A

15 38 F PICA Dissecting Excision PICA end-to-end Y Obliterated

16 41 F M3 Mycotic Distal MCA clip

occlusion


17 51 M Petrous/cavernous

ICA

Fusiform Proximal ICA clip

occlusion


18 28 F M2 Fusiform Proximal MCA clip

occlusion

STA-MCA Y Residual treated

by clipping

19 35 F P2/P3 Junction Saccular Distal coil occlusion OA-PCA N Obliterated

20 29 M Cavernous ICA Fusiform — OA-MCA Y Abscess Residual

21 7 M P2 Fusiform Distal PCA clip

occlusion

STA-PCA Y CVA Obliterated

22 54 M Cavernous ICA Saccular Distal ICA clip

occlusion

STA-MCA N CVA Obliterated

23 75 F Cavernous ICA Fusiform — STA-MCA Y Obliterated

24 16 M A2 Fusiform Trapping A3-A3 Y Obliterated

25 38 F M3 Fusiform Proximal MCA clip

occlusion

STA-MCA Y CVA Obliterated

26 77 M M2 Saccular Clipping, excision STA-MCA N/A CVA Obliterated

27 31 F A2 Fusiform Trapping A3-A3 N/A Obliterated

28 54 F M2/M3 Mycotic Excision STA-MCA Y Obliterated

(Continues)

REV

ASC

ULA

RIZATIONANDANEU

RYSM

SURGERY

NEUROSU

RGERY

VOLU

ME74|NUMBER

5|MAY2014|493


TABLE 5. Continued

Patient

ID Age Sex Location Aneurysm Type Treatment Bypass Type Graft

Bypass

Patency Morbidity & Mortality

Aneurysm

Outcome

29 45 M Cavernous ICA Saccular ICA coil occlusion STA-MCA Y Obliterated

30 48 M Basilar Fusiform Occlusion of BA STA-SCA Y CVA, Death N/A

31 52 M Basilar trunk and tip Fusiform Partial basilar

occlusion

STA-SCA Y Residual

32 30 F M2 Saccular Clip-wrapping M2-Transposition Y Obliterated

33 60 M PICA Saccular Excision PICA-PICA

reanastomosis

N Obliterated

34 45 F Supraclinoid ICA Saccular Trapping ICA-MCA RAG Y Obliterated


occlusion

ICA-MCA RAG N Hypotensive event

necessitating

exploratory

laparotomy, Death

N/A

36 60 F PICA Saccular Coil OA-PICA Y Obliterated


occlusion


38 49 F Cavernous ICA Pseudoaneurysm Trapping ICA-MCA RAG Y Obliterated

39 39 F Supraclinoid ICA Saccular Proximal ICA clip

occlusion

ICA-MCA RAG Y Obliterated

40 51 F Supraclinoid ICA Saccular ICA coil occlusion STA-MCA Y Obliterated

41 16 F M1/M2 Saccular Proximal MCA clip

occlusion

CCA-MCA SVG Y CVA Obliterated


occlusion

STA-MCA Y Extra-axial Bleed Obliterated

43 74 F Cavernous ICA Saccular Primary clipping,

distal ICA clip

occlusion


44 55 F Basilar tip Saccular Partial basilar

occlusion

STA-SCA N Enlarged

55 F Basilar tip Saccular Basilar occlusion STA-SCA, STA-PCA

double-barrel

Nb Bypass thrombosis

postop, CVA, Death

N/A

45 61 F PICA Saccular Excision End-to-end

anastomosis

N Bypass thrombosis

postop, CVA, Death

N/A

46 ,1 F A2 Saccular Excision R Frontopolar branch

to Left A2

Y Obliterated

47 56 F PComm Saccular Trapping ICA-MCA RAG N Bypass thrombosis,

CVA, Death

N/A

48 58 F Basilar tip Saccular Basilar occlusion ICA-MCA RAG N CVA Residual

49 44 F Cavernous ICA Saccular Trapping STA-MCA Y Unilateral blindness Obliterated

50 54 F Cavernous ICA Saccular Proximal ICA coil

occlusion


51 54 F M1 Saccular Proximal ICA clip

occlusion

ICA-MCA RAG N Bypass thrombosis,

CVA, Death

N/A

52 25 M M1/M2 Saccular Proximal MCA clip

occlusion

ECA-MCA RAG Y Obliterated

(Continues)

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procedures.58,62,64 Alternatively, the diseased segment of theblood vessel may be resected, and direct reconstruction canperformed when there is sufficient redundancy.62 The PICA canalso be reimplanted onto the vertebral artery after resection of thediseased segment of the vessel.

Aneurysms of the Vertebrobasilar Circulation

Giant and fusiform aneurysms involving the basilar arteryremain treacherous lesions with a poor natural history.35,36 Recentexperience with flow-diverting stents in these lesions has beendisappointing,17 and the current treatment of choice remainsvessel occlusion combined with bypass for flow reversal. For distalbasilar artery aneurysms, we prefer clip occlusion of the basilarartery at the perforator-free zone below the SCAs combined withrevascularization by using an STA-SCA or STA-PCA bypass orboth (Figure 7).65,66 For aneurysms involving the more proximalportions of the basilar artery, reversal of flow can be achieved byclipping the vertebral arteries above the PICA takeoff on 1 sideand distal to the PICA takeoff on the contralateral side.36 Thisstrategy encourages retrograde (but reduced) flow in the basilarartery, reducing the risk of acute basilar artery thrombosis. In ourexperience, this treatment modality is best suited for individualswho already have significant thrombosis of their aneurysms andrecruitment to the territories normally fed by brainstem perforators.In these cases, flow reduction is less likely to lead to infarction of thebrainstem. Regardless of the treatment modality used, the outcomeof patients with these aneurysms is generally poor.Complex aneurysms involving the distal vertebral artery are

typically amenable to treatment by proximal vessel occlusion. Incases where the contralateral vertebral artery is absent orhypoplastic, vertebral artery occlusion can be combined withSTA-SCA and/or STA-PCA bypass, as described above to decreasethe risk of brainstem stroke.

Outcomes of Cerebral Revascularization for Aneurysms

Overall, the outcomes of this series (Table 5) are comparableto older series of cerebral revascularization for aneurysmsurgery.1,37-43 At a mean angiographic follow-up of 17.8months (median, 11 months; range, 1-72 months), graftocclusion was identified in 14 bypass procedures.Subgroup analysis of the aneurysms reaffirms previous reports of a

more aggressivenatural history of posterior circulation aneurysms.35,36

Of 7 cases of mortality, 3 belonged to aneurysms in theposterior circulation, including 2 basilar artery aneurysms and1 PICA aneurysm. Two patients with basilar aneurysms hadperforator infarcts after treatment that resulted in their eventualdeath. The patient with the PICA aneurysm presented witha poor-grade aSAH. The other 4 cases of mortality includeda blister aneurysm of the supraclinoid ICA and a giant PCommaneurysm, both presenting with aSAH; a patient with a giantMCA aneurysm who had bypass thrombosis leading to death;and a patient with a giant cavernous ICA aneurysm who diedsecondary to other medical complications. Further, of 7 cases of

TABLE5.Continued

Patient

IDAge

Sex

Location

Aneurysm

Type

Treatm

ent

Bypass

Type

Graft

Bypass

Patency

Morbidity&

Mortality

Aneurysm

Outcome

53

43

FCavernousICA

Saccular

Proximal

ICAclip

occlusion

STA-M

CA

YObliterated

54

57

FM1/M

2Saccular

Clip

reconstruction

STA-M

CA

YObliterated

55

71

FCervical

ICA

Saccular

Excision

ECA-ICA

YObliterated

aBA,basilarartery;CCA,commoncarotidartery;CVA,cerebrovascularaccident;EC

A,externalcarotidartery;F,female;ICA,internal

carotidartery;M,male;MCA,middle

cerebralartery;N,no;N/A,not

applicab

le;O

A,o

ccipitalartery;PCA,p

osteriorcerebralartery;PComm,p

osteriorcommunicatingartery;PICA,p

osteriorinferiorcerebellarartery;R,right;RAG,rad

ialartery

graft;STA

,superficialtemporalartery;

SVG,saphenousvein

graft;Y,yes.

bInitially

openpostoperatively.




residual aneurysms (in 6 patients) noted on angiographicfollow-up among 56 aneurysms, 4 cases were aneurysms ofthe vertebrobasilar circulation.

CONCLUSION

Despite advances in endovascular technique, cerebral revascu-larization remains an essential skill necessary for the treatment ofthose aneurysms that fail endovascular management or are deemedinappropriate for endovascular or microsurgical technique. Withmore aneurysms being treated by the use of the endovasculartechnique, the aneurysms referred for this treatment strategy arenaturally more challenging than those treated in historical series.Although stents and flow diverters have provided a less-invasivealternative to microsurgical technique, challenges associated withtheir use in the setting of aSAH, the occurrence of perforatorstrokes, and delayed complications such as in-stent stenosis haveresulted in a more cautious approach to their use. As endovasculartechniques improve, it is possible that cerebral revascularizationwill become obsolete, but, in the current state of affairs, bypasssurgery remains an essential treatment strategy in the managementof complex cerebral aneurysms.

Disclosure

Drs Kalani, Nakaji, Zabramski, and Spetzler are supported by a grant from theNational Institutes ofHealth (UH2TR000891-01). They have nopersonal, financial,or institutional interest in any of the materials or devices described in this article.

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COMMENTS

T he authors have presented their outcomes and indications for revas-cularization in the endovascular area. As the authors state, in my

experience the indications have declined for a bypass with modernendovascular therapy, in particular, flow diversion. They retrospectivelyreviewed and identified 56 consecutive patients (16males and 40 females)with 57 aneurysms. Revascularization was performed with a superficialtemporal artery (STA) to MCA bypass (n = 25), STA to superior cere-bellar artery (SCA) (n = 3), STA to PCA (n = 1), STA-SCA/STA-PCA(n = 1), occipital artery (OA) to PCA (n = 2), external carotid artery(ECA)/ICA to MCA (n = 15), OA to MCA (n = 1), OA to PICA (n = 1),and in situ bypasses (n = 8). At a mean clinical follow-up of 18.5 months,46 patients (82%) had a good outcome (GOS 4 or 5). There were 7 casesof mortality (12.5%) and an additional 9 cases of morbidity (15.8%).At a mean angiographic follow-up of 17.8 months, 12 bypasses wereoccluded.This, in the current times, is a large experience with cerebrovascular

revascularization and the authors should be commended on the depth ofbypasses. My personal practice has seen a significant decline in bypasses andmy belief is that flow diversion will be the death of cerebral bypasses for themajority of the ICAaneurysms1 which used to represent a significant portionof the bypasses performed. Unfortunately this together with the results of theCOSS trial, the art of revascularization will demise, particularly for theyounger vascular surgeons who will be more adept at endovascular therapy. Iagree however with the authors, that cerebral revascularization remains anessential technique for aneurysm surgery.

Gavin W. BritzHouston, Texas

1. Mattei TA, Ferrell AS, Britz GW. Is flow diversion the death of cerebral bypass andcoiling/stent-assisted coiling for giant cavernous aneurysms? A critical review oncomparative outcomes and ongoing clinical trials. Neurosurg Rev. 2013;36(4):505-511; discussion 511-512.




2. Grubb RL Jr, Powers WJ, Clarke WR, Videen TO, Adams HP Jr, Derdeyn CP;Carotid Occlusion Surgery Study Investigators. Surgical results of the carotidocclusion surgery study. J Neurosurg. 2013;118(1):25-33.

A s endovascular technique, experience, materials improve, open sur-gical procedures for treatment of intracranial aneurysms continues to

decline, with only the very challenging remaining for consideration. Theauthors retrospectively review the records of 56 patients with 57 aneur-ysms requiring flow augmentation in the form of an EC-IC or in situbypass for treatment of large complex intracranial aneurysms. The deci-sion for bypass was completed during intraoperative evaluation of therelationship of the vessels to the aneurysm and whether the exclusion ofthe aneurysm from the circulation would alter their patency. If thisexamination confirmed the need for vessel sacrifice, a bypass was per-formed. Their overall results were quite good; mortality was 12.5%,morbidity 15.8% in this very high risk group of patients.As pointed out in this article, with the introduction of the Pipeline

Exclusion Device, even fewer aneurysms require open surgical treatment,yet Meckel et al reported a 40%mortality associated with the use of FlowDiversion in the vertebrobasilar circulation. Those aneurysms not con-sidered amenable for endovascular treatment are extremely challenging foran open surgical procedure. The authors are to be commended for theirwork, because this surgical review provides another standard for com-parison with the results of endovascular treatment of this subset ofaneurysms.

Frank CulicchiaSilvia Gesheva

New Orleans, Louisiana

T his article contains important data from a large number of patientswith large complex intracranial aneurysms in which an extracra-

nial-intracranial (EC-IC) arterial bypass or an in situ arterial bypasswas performed as part of the treatment to obliterate the aneurysm.Their results are comparable to or better than the results reported inthe literature for EC-IC bypasses and/or in situ arterial bypasses used aspart of the treatment of complex large intracranial aneurysms.Although there was a significant mortality rate (12.5%) and a signifi-cant morbidity rate (15.8%), including a 10.5% rate of cerebrovas-cular accidents, the results are quite good considering the complexityand difficulty of the treatment of this group of patients. While theCarotid Occlusion Surgery Study (COSS) did not show a benefit ofsuperficial temporal artery-middle cerebral artery (STA-MCA) bypassin patients with symptomatic occlusion of the internal carotid artery,planned sacrifice of a large intracranial artery in the treatment of

complex intracranial aneurysms and tumors is a different situationfrom symptomatic atherosclerotic occlusive cerebrovascular disease,and EC-IC arterial bypass and in situ arterial bypasses are an importantcomponent of the treatment of many of these lesions. The introduc-tion of endovascular flow-diversion stents (FDS) has significantlyreduced the number of patients with complex intracranial aneurysmstreated with direct clipping and some type of arterial bypass. However,significant complications have been reported with the use of thesedevices, and many complex intracranial aneurysms are not suitable fortreatment with FDS. Thus, it is important for neurosurgery to retainthe ability to perform intracranial arterial bypasses when indicated inthe treatment of intracranial aneurysms and tumors.

Robert L. Grubb JrSt. Louis, Missouri

CME Questions:

1. What is the 30-day perioperative stoke risk after STA-MCAbypass for ipsilateral carotid occlusion?A. 0-5%B. 5-10%C. 10-15%D. 15-20%E. 20-25%

2. What is the 5 year risk of rupture for a giant (.2.5 cm)aneurysm in the anterior circulation?A. 10%B. 20%C. 30%D. 40%E. 50%

3. What is the documented incidence of delayed ischemia per yearfollowing carotid occlusion after BTO (balloon test occlusion)?A. 1-1.5%B. 1.5-3%C. 3-4.5%D. 4.5-6%E. 6-7.5%

KALANI ET AL



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