Skip Navigation LinksHome > May 2014 - Volume 74 - Issue 5 > Revascularization and Aneurysm Surgery: Techniques, Indicat...
doi: 10.1227/NEU.0000000000000312
Research-Human-Clinical Studies

Revascularization and Aneurysm Surgery: Techniques, Indications, and Outcomes in the Endovascular Era

Kalani, M. Yashar S. MD, PhD; Ramey, Wyatt MD; Albuquerque, Felipe C. MD; McDougall, Cameron G. MD; Nakaji, Peter MD; Zabramski, Joseph M. MD; Spetzler, Robert F. MD

Free Access
Article Outline
Collapse Box

Author Information

Division of Neurological Surgery, Barrow Neurological Institute, St. Joseph's Hospital 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:

Received September 06, 2013

Accepted January 28, 2014

Collapse Box


BACKGROUND: Given advances in endovascular technique, the indications for revascularization in aneurysm surgery have declined.

OBJECTIVE: We sought to define indications, outline technical strategies, and evaluate the outcomes of patients treated with bypass in the endovascular era.

METHODS: We retrospectively reviewed all aneurysms treated between September 2006 and February 2013.

RESULTS: We identified 54 consecutive patients (16 males and 39 females) with 56 aneurysms. 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 cerebral artery (MCA) (n = 13), posterior cerebral artery (PCA) (n = 3), posterior inferior cerebellar artery (n = 4), and vertebrobasilar arteries (n = 5). Revascularization was performed with superficial 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 posterior inferior cerebellar artery (n = 1), and in situ bypasses (n = 8). At a mean clinical follow-up of 18.5 months, 45 patients (81.8%) had a good outcome (Glasgow Outcome Scale 4 or 5). 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 revascularization remains an essential technique for aneurysm surgery.

ABBREVIATIONS: ACA, anterior cerebral artery

aSAH, aneurysmal subarachnoid hemorrhage

BTO, balloon test occlusion

GOS, Glasgow Outcome Scale

ICA, internal carotid artery

MCA, middle cerebral artery

OA, occipital artery

PCA, posterior cerebral artery

PComm, posterior communicating artery

PICA, posterior inferior cerebellar artery

SCA, superior cerebellar artery

STA, superficial temporal artery

When we last published the Barrow Neurological Institute experience with revascularization for aneurysm surgery in 1996,1 Guglielmi detachable coils had only recently been approved for use, and endovascular techniques were in their infancy.2-4 Over the past 2 decades, there has been rapid growth and advancements in the field of endovascular neurosurgery, and these techniques have become an alternative to microsurgery for the treatment of cerebral aneurysms.5,6 During the same period, the negative results of the Carotid Occlusion Surgery Study (COSS) trial7 and the introduction of flow-diverting stents8,9 have resulted in many practitioners rethinking the utility of cerebral revascularization for vascular pathologies.

Given the paradigm shift of the past 2 decades, we sought to reevaluate the role of revascularization in the treatment of complex cerebral aneurysms in the modern endovascular era, as well as review the indications and evaluate the outcomes of patients treated by using bypass surgery and either microsurgical, endovascular, or combined techniques.

Back to Top | Article Outline


Patient Population

Between September 2006 and February 2013, 55 patients with 56 complex cerebral aneurysms were treated with surgery, endovascular technique, 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 examinations, and radiographic studies were retrospectively reviewed. Pre- and postoperative neurological function was evaluated with the use of the Glasgow Outcome Scale (GOS) score.

Table 1
Table 1
Image Tools
Back to Top | Article Outline

The most 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 of mass effect. Seven patients had their aneurysms identified incidentally during a workup for nonrelated symptoms. Eleven patients presented owing to aneurysmal subarachnoid hemorrhage (aSAH). An additional 3 patients had a previous history of aSAH that led to the identification of their aneurysm. Of patients with aSAH, the Hunt and Hess grade10 was II in 3 patients, III in 5 patients, IV in 1 patient, and V in 1 patient. In 1 patient under the age of 1, a Hunt and Hess grade was not assigned. An additional patient presented owing to subarachnoid hemorrhage after an iatrogenic internal carotid artery (ICA) injury. Twelve cases were previously treated by the use of microsurgery (n = 6), endovascular (n = 5), or combined techniques (n = 1).

Back to Top | Article Outline
Aneurysm Location and Characteristics

There were 24 aneurysms on the right side and 27 aneurysms on the left side. Five aneurysms were located on the basilar artery. The average size of the aneurysms was 23 mm. There were 27 giant aneurysms and 18 large aneurysms. The majority of the aneurysms were saccular (n = 35, 62.5%), followed by fusiform (n = 16, 28.6%). Aneurysms were located along the cervical ICA (n = 1), petrous/cavernous ICA (n = 1), the cavernous ICA (n = 16), supraclinoid ICA (n = 7), posterior communicating artery (PComm) (n = 2), anterior cerebral artery (ACA) (n = 4), middle cerebral artery (MCA) (n = 13), posterior cerebral artery (PCA) (n = 3), posterior inferior cerebellar artery (PICA) (n = 4), and vertebrobasilar arteries (n = 5).

Back to Top | Article Outline
Diagnostic Evaluation and Criteria for Revascularization

Although recent advances in 3-D angiography have greatly facilitated the determination of whether an aneurysm can be clipped, intraoperative exploration remains the gold standard. If during intraoperative evaluation the surgeon concluded that the aneurysm could not be directly clipped or clip reconstructed, a decision to perform vessel sacrifice in the form of proximal 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 type of bypass performed (high-flow or low-flow) depends on the location of the aneurysm and available collateral circulation. Imaging assessment of patients included combinations of magnetic resonance imaging, magnetic resonance angiography, computed tomographic angiography, and digital subtraction angiography. Balloon test occlusion (BTO) is not a routine part 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 for endovascular management.

Back to Top | Article Outline
Perioperative Treatment Paradigm

Preoperatively, patients are placed on aspirin (325 mg/d) before intervention, and the dose is continued postoperatively. Some patients had a short postoperative course of heparin to prevent sudden thrombosis of their aneurysm. Electroencephalographic monitoring was conducted intraoperatively. We perform revascularization procedures under mild hypothermia and barbiturate protection. Table 2 outlines the treatment strategies used in treating these patients. Intraoperative evaluation of bypass patency and treatment were confirmed by using indocyanine green videoangiography or intraoperative angiography.

Table 2
Table 2
Image Tools
Back to Top | Article Outline


Bypass Procedures and Patency

We performed a total of 57 cerebral revascularization procedures in 55 patients. Revascularization was performed with superficial 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 artery and 1 using a saphenous vein graft), OA-MCA (n = 1), OA-PICA (n = 1), and in situ bypasses (n = 8). At a mean angiographic follow-up of 17.8 months (median, 11 months; range 1-72 months) graft occlusion was identified in 14 patients (Table 3). In 7 cases, bypass occlusion did not result in significant morbidity, and the patients were noted to be independent (GOS 4 or 5) at last follow-up. Bypass patency information was not available in 3 cases. The remaining bypasses (n = 42) remained patent.

Table 3
Table 3
Image Tools
Back to Top | Article Outline
Aneurysm Fate

In the surviving patients, we identified residual aneurysm in 6 patients (7 aneurysms) at last follow-up. Angiographic follow-up documenting aneurysm fate was available for all patients. The remaining 42 aneurysms were completely occluded. The aneurysms with residual filling included 4 cases of basilar trunk/tip aneurysms (one of whom died and was excluded from the analysis), 2 giant cavernous ICA aneurysms, 1 giant proximal MCA aneurysm, and 1 case of a small fusiform A2 segment aneurysm that did not exhibit evidence of growth after treatment but did not regress on angiographic follow-up.

Back to Top | Article Outline
Complications and Outcomes

At a mean clinical follow-up of 18.5 months (median, 9.5 months; range 1-72 months), 45 patients (81.8%) had a good outcome (GOS 4 or 5). Seven patients (12.5%) died (Table 4). Six deaths were related to postoperative stroke; in 5 of these 6 patients, stroke was associated with occlusion of the bypass, whereas, in 1 case, a giant basilar aneurysm, the patient experienced a massive brainstem infarct despite a patent bypass. There was 1 death secondary to medical complications. Six patients had asymptomatic strokes (10.5%). Additional morbidity occurred in 3 patients (5.4%), including 1 case of intracranial abscess, 1 extra-axial hematoma, and 1 case of postoperative blindness.

Table 4
Table 4
Image Tools
Back to Top | Article Outline


Bypass Surgery for Complex Aneurysms

With the expanding repertoire of endovascular tools, the indications for cerebral revascularization for aneurysm surgery have significantly decreased. Endovascular therapy has become a 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 allowed for 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 been a significant decrease in the use of bypass for treatment of complex ICA aneurysms, and the majority of these lesions are now referred for endovascular consideration (data not shown). Should these lesions be deemed inappropriate for endovascular treatment, they are then considered for surgical management. The data on the use of flow diverters in the posterior circulation are less convincing and too sparse to make definitive recommendations regarding the use of these devices in the posterior circulation.

Despite these advances, however, aneurysms remain that either fail, or are not appropriate candidates for, endovascular treatment. The results from several large series suggest that endovascular techniques are associated with a high recurrence rate, especially in patients with large and giant aneurysms.13-15 Flow-diverting stents have also been associated with perforator infarcts,16-18 and their use in the setting of aSAH remains a matter of continued debate.19,20 One of the most promising indications for flow-diverting stents, their application in the treatment of fusiform posterior circulation aneurysms, has been associated with high rates of morbidity and mortality.16,18 Finally, at least a subset of patients is not medically able to tolerate the dual-antiplatelet regimen necessary for the use of stents.21

Given the limitations of existing endovascular techniques and the inability to primarily clip a subset of complex cerebral aneurysms, there remains a clear indication for Hunterian ligation in the treatment of complex cerebral aneurysms. In historical series, surgical occlusion of the carotid artery for the management of intracranial aneurysms was associated with infarction in up to 40% of cases.22 BTO has been used by some groups in an attempt to determine whether it is safe to occlude a cerebral vessel; however, the BTO test itself is not without risks, and predictive results are less than perfect. Complications following BTO include dissections, embolic complications, and pseudoaneurysms in 0% to 8% of cases.23 Several studies of ICA occlusion following 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 major cerebral vessel increases the risk of flow-related aneurysms in collateral branches. De novo aneurysm formation in the collateral circulation of patients undergoing Hunterian ligation without revascularization has been estimated to be 10%.1

Several groups have combined BTO with measurements of cerebral blood flow to improve the predictive accuracy of this test.29-32 Others have used intraoperative blood flow measurements to determine the need for bypass and the extent of flow augmentation necessary with good results.33

Although each of these techniques has its proponents, our institutional preference has been to perform a bypass in all patients requiring acute vessel sacrifice for management of an aneurysm. In general, our strategy has been to assess the extent of collateral flow angiographically. When ample collaterals are present, or the flow demand is limited (eg, when only 1 M2 branch of the MCA needs to be sacrificed), we favor a low-flow (eg, STA-MCA) bypass. When collaterals are absent or diminutive (eg, the patient with a hypoplastic or absent A1 segment on the side of planned carotid occlusion), we favor a high-flow bypass. When ICA occlusion is being considering for the treatment of a complex aneurysm, simple manual compression of the carotid artery in the neck during angiography can provide a quick assessment of available collateral flow for determining whether to perform a low-flow or high-flow bypass.

Several series have documented favorable outcomes ranging from 50% to 93% in the treatment of complex cerebral aneurysms with microvascular bypass.1,34-43 In our current series, we noted a favorable outcome in 81.8% of patients. It is difficult to directly compare different series across different eras. In the present endovascular era, patients are referred for microsurgical treatment only when endovascular treatment of their aneurysm has failed, or when they have been deemed poor candidates for endovascular therapy.

Back to Top | Article Outline
Pathology-Specific Considerations

Our management strategy for aneurysms at specific sites is discussed below.

Back to Top | Article Outline
Aneurysms of the Precavernous ICA

Depending on the level, aneurysms of cervical ICA can be treated by direct excision and reconstruction or proximal occlusion and distal bypass (Figure 1).44 When acute carotid occlusion is necessary, revascularization often requires a high-flow bypass (saphenous vein or radial artery graft); however, in patients with a good collateral supply via the anterior communicating complex, and/or a large posterior communicating artery, an STA-MCA bypass can be considered for simple augmentation of flow.45

Figure 1
Figure 1
Image Tools
Back to Top | Article Outline
Aneurysms of the Cavernous ICA

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

Figure 2
Figure 2
Image Tools
Back to Top | Article Outline
Aneurysms of the Supraclinoid ICA

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

Back to Top | Article Outline
Aneurysms of the Posterior Communicating ICA

In this series, both aneurysms involving this segment of the ICA were treated by using a combination of trapping and high-flow bypass to the MCA with the use of a radial artery graft (Figure 3).52 A low-flow bypass may be permissible in such cases if adequate collaterals are available.

Figure 3
Figure 3
Image Tools
Back to Top | Article Outline
Aneurysms of the ACA

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

Figure 4
Figure 4
Image Tools
Back to Top | Article Outline
Aneurysms of the MCA

Proximal MCA aneurysms can be treated via proximal or distal vessel occlusion with a low-flow or high-flow bypass (Figure 5).34 Given the extensive network of lenticulostriate arteries arising from this segment, trapping is usually not feasible. The decision to perform a STA-MCA or a radial artery interposition graft from the ICA to MCA depends primarily on the caliber of the STA. Trapping or excision and direct vessel reconstruction are possible when the aneurysm arises distal to the lenticulostriate perforators. Various combinations of in situ and STA-MCA bypasses can also be used (Figure 5).58,59

Figure 5
Figure 5
Image Tools
Back to Top | Article Outline
Aneurysms of the PCA

Complex aneurysms involving the P2 and/or P3 segments of the PCA are most commonly treated by proximal or distal parent vessel occlusion (Figure 6). Visual impairments are a major risk in such cases, and, although distal bypass (OA-PCA) to augment flow is possible,60 an analysis of our experience revealed a higher than expected rate of complications associated with this procedure.61 In this subset of patients, we recommend BTO as part of the preoperative assessment and reserve revascularization for those for whom this test fails.

Figure 6
Figure 6
Image Tools
Back to Top | Article Outline
Aneurysms of the PICA

Unclippable aneurysms of PICA are usually fusiform. These aneurysms can be treated by trapping, or by proximal or distal vessel occlusion, with bypass. A variety of bypasses are available for revascularization of the PICA territory, including the OA-PICA bypass62,63 and the PICA-PICA (side-to-side) bypass procedures.58,62,64 Alternatively, the diseased segment of the blood vessel may be resected, and direct reconstruction can performed when there is sufficient redundancy.62 The PICA can also be reimplanted onto the vertebral artery after resection of the diseased segment of the vessel.

Back to Top | Article Outline
Aneurysms of the Vertebrobasilar Circulation

Giant and fusiform aneurysms involving the basilar artery remain treacherous lesions with a poor natural history.35,36 Recent experience with flow-diverting stents in these lesions has been disappointing,17 and the current treatment of choice remains vessel occlusion combined with bypass for flow reversal. For distal basilar artery aneurysms, we prefer clip occlusion of the basilar artery at the perforator-free zone below the SCAs combined with revascularization by using an STA-SCA or STA-PCA bypass or both (Figure 7).65,66 For aneurysms involving the more proximal portions of the basilar artery, reversal of flow can be achieved by clipping the vertebral arteries above the PICA takeoff on 1 side and distal to the PICA takeoff on the contralateral side.36 This strategy encourages retrograde (but reduced) flow in the basilar artery, reducing the risk of acute basilar artery thrombosis. In our experience, this treatment modality is best suited for individuals who already have significant thrombosis of their aneurysms and recruitment to the territories normally fed by brainstem perforators. In these cases, flow reduction is less likely to lead to infarction of the brainstem. Regardless of the treatment modality used, the outcome of patients with these aneurysms is generally poor.

Figure 7
Figure 7
Image Tools

Complex aneurysms involving the distal vertebral artery are typically amenable to treatment by proximal vessel occlusion. In cases where the contralateral vertebral artery is absent or hypoplastic, vertebral artery occlusion can be combined with STA-SCA and/or STA-PCA bypass, as described above to decrease the risk of brainstem stroke.

Back to Top | Article Outline
Outcomes of Cerebral Revascularization for Aneurysms

Overall, the outcomes of this series (Table 5) are comparable to older series of cerebral revascularization for aneurysm surgery.1,37-43 At a mean angiographic follow-up of 17.8 months (median, 11 months; range, 1-72 months), graft occlusion was identified in 14 bypass procedures.

TABLE 5-a Detailed P...
TABLE 5-a Detailed P...
Image Tools

Subgroup analysis of the aneurysms reaffirms previous reports of a more aggressive natural history of posterior circulation aneurysms.35,36 Of 7 cases of mortality, 3 belonged to aneurysms in the posterior circulation, including 2 basilar artery aneurysms and 1 PICA aneurysm. Two patients with basilar aneurysms had perforator infarcts after treatment that resulted in their eventual death. The patient with the PICA aneurysm presented with a poor-grade aSAH. The other 4 cases of mortality included a blister aneurysm of the supraclinoid ICA and a giant PComm aneurysm, both presenting with aSAH; a patient with a giant MCA aneurysm who had bypass thrombosis leading to death; and a patient with a giant cavernous ICA aneurysm who died secondary to other medical complications. Further, of 7 cases of residual aneurysms (in 6 patients) noted on angiographic follow-up among 56 aneurysms, 4 cases were aneurysms of the vertebrobasilar circulation.

TABLE 5-b Detailed P...
TABLE 5-b Detailed P...
Image Tools
TABLE 5-c Detailed P...
TABLE 5-c Detailed P...
Image Tools
Back to Top | Article Outline


Despite advances in endovascular technique, cerebral revascularization remains an essential skill necessary for the treatment of those aneurysms that fail endovascular management or are deemed inappropriate for endovascular or microsurgical technique. With more aneurysms being treated by the use of the endovascular technique, the aneurysms referred for this treatment strategy are naturally more challenging than those treated in historical series. Although stents and flow diverters have provided a less-invasive alternative to microsurgical technique, challenges associated with their use in the setting of aSAH, the occurrence of perforator strokes, and delayed complications such as in-stent stenosis have resulted in a more cautious approach to their use. As endovascular techniques improve, it is possible that cerebral revascularization will become obsolete, but, in the current state of affairs, bypass surgery remains an essential treatment strategy in the management of complex cerebral aneurysms.

Back to Top | Article Outline

Drs Kalani, Nakaji, Zabramski, and Spetzler are supported by a grant from the National Institutes of Health (UH2TR000891-01). They have no personal, financial, or institutional interest in any of the materials or devices described in this article.

Back to Top | Article Outline


1. Lawton MT, Hamilton MG, Morcos JJ, Spetzler RF. Revascularization and aneurysm surgery: current techniques, indications, and outcome. Neurosurgery. 1996;38(1):83–92.

2. Guglielmi G, Viñuela F, Dion J, Duckwiler G. Electrothrombosis of saccular aneurysms via endovascular approach. Part 2: preliminary clinical experience. J Neurosurg. 1991;75(1):8–14.

3. Guglielmi G, Viñuela F, Briganti F, Duckwiler G. Carotid-cavernous fistula caused by a ruptured intracavernous aneurysm: endovascular treatment by electrothrombosis with detachable coils. Neurosurgery. 1992;31(3):591–596.

4. Guglielmi G, Viñuela F, Duckwiler G, et al.. Endovascular treatment of posterior circulation aneurysms by electrothrombosis using electrically detachable coils. J Neurosurg. 1992;77(4):515–524.

5. McDougall CG, Spetzler RF, Zabramski JM, et al.. The Barrow Ruptured Aneurysm Trial. J Neurosurg. 2012;116(1):135–144.

6. Molyneux A, Kerr R, Stratton I, et al.. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet. 2002;360(9342):1267–1274.

7. Powers WJ, Clarke WR, Grubb RL Jr, Videen TO, Adams HP Jr, Derdeyn CP. Extracranial-intracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: the Carotid Occlusion Surgery Study randomized trial. JAMA. 2011;306(18):1983–1992.

8. Kallmes DF, Ding YH, Dai D, Kadirvel R, Lewis DA, Cloft HJ. A new endoluminal, flow-disrupting device for treatment of saccular aneurysms. Stroke. 2007;38(8):2346–2352.

9. Fiorella D, Woo HH, Albuquerque FC, Nelson PK. Definitive reconstruction of circumferential, fusiform intracranial aneurysms with the pipeline embolization device. Neurosurgery. 2008;62(5):1115–1120.

10. Hunt WE, Hess RM. Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg. 1968;28(1):14–20.

11. Becske T, Kallmes DF, Saatci I, et al.. Pipeline for Uncoilable or Failed Aneurysms: results from a multicenter clinical trial. Radiology. 2013;267(3):858–868.

12. Nelson PK, Lylyk P, Szikora I, Wetzel SG, Wanke I, Fiorella D. The pipeline embolization device for the intracranial treatment of aneurysms trial. AJNR Am J Neuroradiol. 2011;32(1):34–40.

13. Parkinson RJ, Eddleman CS, Batjer HH, Bendok BR. Giant intracranial aneurysms: endovascular challenges. Neurosurgery. 2008;62(6 suppl 3):1336–1345.

14. Peluso JP, van Rooij WJ, Sluzewski M, Beute GN. Coiling of basilar tip aneurysms: results in 154 consecutive patients with emphasis on recurrent haemorrhage and re-treatment during mid- and long-term follow-up. J Neurol Neurosurg Psychiatry. 2008;79(6):706–711.

15. Jahromi BS, Mocco J, Bang JA, et al.. Clinical and angiographic outcome after endovascular management of giant intracranial aneurysms. Neurosurgery. 2008;63(4):662–674.

16. Siddiqui AH, Abla AA, Kan P, et al.. Panacea or problem: flow diverters in the treatment of symptomatic large or giant fusiform vertebrobasilar aneurysms. J Neurosurg. 2012;116(6):1258–1266.

17. Jabbour P, Chalouhi N, Tjoumakaris S, et al.. The pipeline embolization device: learning curve and predictors of complications and aneurysm obliteration. Neurosurgery. 2013;73(1):113–120.

18. Siddiqui AH, Kan P, Abla AA, Hopkins LN, Levy EI. Complications after treatment with pipeline embolization for giant distal intracranial aneurysms with or without coil embolization. Neurosurgery. 2012;71(2):E509–E513.

19. Cruz JP, O'Kelly C, Kelly M, et al.. Pipeline embolization device in aneurysmal subarachnoid hemorrhage. AJNR Am J Neuroradiol. 2013;34(2):271–276.

20. Narata AP, Yilmaz H, Schaller K, Lovblad KO, Pereira VM. Flow-diverting stent for ruptured intracranial dissecting aneurysm of vertebral artery. Neurosurgery. 2012;70(4):982–988.

21. Fiorella D, Thiabolt L, Albuquerque FC, Deshmukh VR, McDougall CG, Rasmussen PA. Antiplatelet therapy in neuroendovascular therapeutics. Neurosurg Clin N Am. 2005;16(3):517–540, vi.

22. Polevaya NV, Kalani MY, Steinberg GK, Tse VC. The transition from Hunterian ligation to intracranial aneurysm clips: a historical perspective. Neurosurg Focus. 2006;20(6):E3.

23. Mathis JM, Barr JD, Jungreis CA, et al.. Temporary balloon test occlusion of the internal carotid artery: experience in 500 cases. AJNR Am J Neuroradiol. 1995;16(4):749–754.

24. Fox AJ, Vinuela F, Pelz DM, et al.. Use of detachable balloons for proximal artery occlusion in the treatment of unclippable cerebral aneurysms. J Neurosurg. 1987;66(1):40–46.

25. Swearingen B, Heros RC. Common carotid occlusion for unclippable carotid aneurysms: an old but still effective operation. Neurosurgery. 1987;21(3):288–295.

26. Larson JJ, Tew JM Jr, Tomsick TA, van Loveren HR. Treatment of aneurysms of the internal carotid artery by intravascular balloon occlusion: long-term follow-up of 58 patients. Neurosurgery. 1995;36(1):26–30.

27. Sudhakar KV, Sawlani V, Phadke RV, Kumar S, Ahmed S, Gujral RB. Temporary balloon occlusion of internal carotid artery: a simple and reliable clinical test. Neurol India. 2000;48(2):140–143.

28. Roski RA, Spetzler RF, Nulsen FE. Late complications of carotid ligation in the treatment of intracranial aneurysms. J Neurosurg. 1981;54(5):583–587.

29. Torigai T, Mase M, Ohno T, et al.. Usefulness of dual and fully automated measurements of cerebral blood flow during balloon occlusion test of the internal carotid artery. J Stroke Cerebrovasc Dis. 2013;22(3):197–204.

30. Kawai N, Kawanishi M, Shindou A, et al.. Cerebral blood flow and metabolism measurement using positron emission tomography before and during internal carotid artery test occlusions: feasibility of rapid quantitative measurement of CBF and OEF/CMRO(2). Interv Neuroradiol. 2012;18(3):264–274.

31. Kato K, Tomura N, Takahashi S, et al.. Balloon occlusion test of the internal carotid artery: correlation with stump pressure and 99mTc-HMPAO SPECT. Acta Radiol. 2006;47(10):1073–1078.

32. Erba SM, Horton JA, Latchaw RE, et al.. Balloon test occlusion of the internal carotid artery with stable xenon/CT cerebral blood flow imaging. AJNR Am J Neuroradiol. 1988;9(3):533–538.

33. Amin-Hanjani S, Alaraj A, Charbel FT. Flow replacement bypass for aneurysms: decision-making using intraoperative blood flow measurements. Acta Neurochir (Wien). 2010;152(6):1021–1032.

34. Kalani MY, Zabramski JM, Hu YC, Spetzler RF. Extracranial-intracranial bypass and vessel occlusion for the treatment of unclippable giant middle cerebral artery aneurysms. Neurosurgery. 2013;72(3):428–435.

35. Steinberg GK, Drake CG, Peerless SJ. Deliberate basilar or vertebral artery occlusion in the treatment of intracranial aneurysms. Immediate results and long-term outcome in 201 patients. J Neurosurg. 1993;79(2):161–173.

36. Kalani MY, Zabramski JM, Nakaji P, Spetzler RF. Bypass and flow reduction for complex basilar and vertebrobasilar junction aneurysms. Neurosurgery. 2013;72(5):763–775.

37. Drake CG. Giant intracranial aneurysms: experience with surgical treatment in 174 patients. Clin Neurosurg. 1979;26:12–95.

38. Yasargil MG. Giant intracranial aneurysms. In: Yasargil MG, eds. Microneurosurgery. Stuttgart, Germany: Georg Thieme; 1984:296–604.

39. Sundt TM Jr, Piepgras DG, Marsh WR, Fode NC. Saphenous vein bypass grafts for giant aneurysms and intracranial occlusive disease. J Neurosurg. 1986;65(4):439–450.

40. Ausman JI, Diaz FG, Sadasivan B, Gonzeles-Portillo M Jr, Malik GM, Deopujari CE. Giant intracranial aneurysm surgery: the role of microvascular reconstruction. Surg Neurol. 1990;34(1):8–15.

41. Drake CG, Peerless SJ, Ferguson GG. Hunterian proximal arterial occlusion for giant aneurysms of the carotid circulation. J Neurosurg. 1994;81(5):656–665.

42. Sughrue ME, Saloner D, Rayz VL, Lawton MT. Giant intracranial aneurysms: evolution of management in a contemporary surgical series. Neurosurgery. 2011;69(6):1261–1270.

43. Ramanathan D, Temkin N, Kim LJ, Ghodke B, Sekhar LN. Cerebral bypasses for complex aneurysms and tumors: long-term results and graft management strategies. Neurosurgery. 2012;70(6):1442–1457.

44. Fitzpatrick BC, Spetzler RF, Ballard JL, Zimmerman RS. Cervical-to-petrous internal carotid artery bypass procedure. Technical note. J Neurosurg. 1993;79(1):138–141.

45. Sekhar LN, Natarajan SK, Ellenbogen RG, Ghodke B. Cerebral revascularization for ischemia, aneurysms, and cranial base tumors. Neurosurgery. 2008;62(6 suppl 3):1373–1408.

46. Dolenc VV. Extradural approach to intracavernous ICA aneurysms. Acta Neurochir Suppl. 1999;72:99–106.

47. Dolenc VV. Surgery of vascular lesions of the cavernous sinus. Clin Neurosurg. 1990;36:240–255.

48. Ponce FA, Albuquerque FC, McDougall CG, Han PP, Zabramski JM, Spetzler RF. Combined endovascular and microsurgical management of giant and complex unruptured aneurysms. Neurosurg Focus. 2004;17(5):E11.

49. Abe H, Takemoto K, Higashi T, Inoue T. Surgical treatment for aneurysms in the cavernous-petrous portion of the internal carotid artery. Acta Neurochir Suppl. 2011;112:77–83.

50. Gelber BR, Sundt TM Jr. Treatment of intracavernous and giant carotid aneurysms by combined internal carotid ligation and extra- to intracranial bypass. J Neurosurg. 1980;52(1):1–10.

51. Serbinenko FA, Filatov JM, Spallone A, Tchurilov MV, Lazarev VA. Management of giant intracranial ICA aneurysms with combined extracranial-intracranial anastomosis and endovascular occlusion. J Neurosurg. 1990;73(1):57–63.

52. Velat GJ, Zabramski JM, Nakaji P, Spetzler RF. Surgical management of giant posterior communicating artery aneurysms. Neurosurgery. 2012;71(suppl operative 1):43–50.

53. Mura J, Riquelme F, Cuevas JL, Luna F, Vizhñay P. Simplified azygos anterior cerebral bypass: y-shaped superficial temporal artery interposition graft from A2 with double reimplantation of pericallosal arteries: technical case report. Neurosurgery. 2013;72:onsE235–onsE240.

54. Mirzadeh Z, Sanai N, Lawton MT. The azygos anterior cerebral artery bypass: double reimplantation technique for giant anterior communicating artery aneurysms. J Neurosurg. 2011;114(4):1154–1158.

55. Park ES, Ahn JS, Park JC, Kwon do H, Kwun BD, Kim CJ. STA-ACA bypass using the contralateral STA as an interposition graft for the treatment of complex ACA aneurysms: report of two cases and a review of the literature. Acta Neurochir (Wien). 2012;154(8):1447–1453.

56. Inoue T, Tsutsumi K, Ohno H, Shinozaki M. Revascularization of the anterior cerebral artery with an A3-A3 anastomosis and a superficial temporal artery bypass using an A3-radial artery graft to trap a giant anterior communicating artery aneurysm: technical case report. Neurosurgery. 2005;57:E207.

57. Kim LJ, Albuquerque FC, McDougall C, Spetzler RF. Combined surgical and endovascular treatment of a recurrent A3-A3 junction aneurysm unsuitable for stand-alone clip ligation or coil occlusion. Technical note. Neurosurg Focus. 2005;18(2):E6.

58. Sanai N, Zador Z, Lawton MT. Bypass surgery for complex brain aneurysms: an assessment of intracranial-intracranial bypass. Neurosurgery. 2009;65(4):670–683.

59. Bederson JB, Spetzler RF. Anastomosis of the anterior temporal artery to a secondary trunk of the middle cerebral artery for treatment of a giant M1 segment aneurysm. Case report. J Neurosurg. 1992;76(5):863–866.

60. Vishteh AG, Smith KA, McDougall CG, Spetzler RF. Distal posterior cerebral artery revascularization in multimodality management of complex peripheral posterior cerebral artery aneurysms: technical case report. Neurosurgery. 1998;43(1):166–170.

61. Chang SW, Abla AA, Kakarla UK, et al.. Treatment of distal posterior cerebral artery aneurysms: a critical appraisal of the occipital artery-to-posterior cerebral artery bypass. Neurosurgery. 2010;67(1):16–25.

62. Nussbaum ES, Mendez A, Camarata P, Sebring L. Surgical management of fusiform aneurysms of the peripheral posteroinferior cerebellar artery. Neurosurgery. 2003;53(4):831–834.

63. Sundt TM Jr, Piepgras DG. Occipital to posterior inferior cerebellar artery bypass surgery. J Neurosurg. 1978;48(6):916–928.

64. Korja M, Sen C, Langer D. Operative nuances of side-to-side in situ posterior inferior cerebellar artery-posterior inferior cerebellar artery bypass procedure. Neurosurgery. 2010;67(suppl operative 2):471–477.

65. Lemole GM Jr, Henn J, Javedan S, Deshmukh V, Spetzler RF. Cerebral revascularization performed using posterior inferior cerebellar artery-posterior inferior cerebellar artery bypass. Report of four cases and literature review. J Neurosurg. 2002;97(1):219–223.

66. Kalani MY, Hu YC, Spetzler RF. A double-barrel superficial temporal artery-to-superior cerebellar artery (STA-SCA) and STA-to-posterior cerebral artery (STA-PCA) bypass for revascularization of the basilar apex. J Clin Neurosci. 2013;20(6):887–889.

Back to Top | Article Outline

The authors have presented their outcomes and indications for revascularization in the endovascular area. As the authors state, in my experience the indications have declined for a bypass with modern endovascular therapy, in particular, flow diversion. They retrospectively reviewed and identified 56 consecutive patients (16 males and 40 females) with 57 aneurysms. Revascularization was performed with a superficial 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 (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 cases of mortality (12.5%) and an additional 9 cases of morbidity (15.8%). At a mean angiographic follow-up of 17.8 months, 12 bypasses were occluded.

This, in the current times, is a large experience with cerebrovascular revascularization and the authors should be commended on the depth of bypasses. My personal practice has seen a significant decline in bypasses and my belief is that flow diversion will be the death of cerebral bypasses for the majority of the ICA aneurysms1 which used to represent a significant portion of the bypasses performed. Unfortunately this together with the results of the COSS trial, the art of revascularization will demise, particularly for the younger vascular surgeons who will be more adept at endovascular therapy. I agree however with the authors, that cerebral revascularization remains an essential technique for aneurysm surgery.

Gavin W. Britz

Houston, Texas

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

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

As endovascular technique, experience, materials improve, open surgical procedures for treatment of intracranial aneurysms continues to decline, with only the very challenging remaining for consideration. The authors retrospectively review the records of 56 patients with 57 aneurysms requiring flow augmentation in the form of an EC-IC or in situ bypass for treatment of large complex intracranial aneurysms. The decision for bypass was completed during intraoperative evaluation of the relationship of the vessels to the aneurysm and whether the exclusion of the aneurysm from the circulation would alter their patency. If this examination confirmed the need for vessel sacrifice, a bypass was performed. 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 Flow Diversion in the vertebrobasilar circulation. Those aneurysms not considered amenable for endovascular treatment are extremely challenging for an open surgical procedure. The authors are to be commended for their work, because this surgical review provides another standard for comparison with the results of endovascular treatment of this subset of aneurysms.

Frank Culicchia

Silvia Gesheva

New Orleans, Louisiana

This article contains important data from a large number of patients with large complex intracranial aneurysms in which an extracranial-intracranial (EC-IC) arterial bypass or an in situ arterial bypass was performed as part of the treatment to obliterate the aneurysm. Their results are comparable to or better than the results reported in the literature for EC-IC bypasses and/or in situ arterial bypasses used as part of the treatment of complex large intracranial aneurysms. Although there was a significant mortality rate (12.5%) and a significant morbidity rate (15.8%), including a 10.5% rate of cerebrovascular accidents, the results are quite good considering the complexity and difficulty of the treatment of this group of patients. While the Carotid Occlusion Surgery Study (COSS) did not show a benefit of superficial temporal artery-middle cerebral artery (STA-MCA) bypass in 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 situation from symptomatic atherosclerotic occlusive cerebrovascular disease, and EC-IC arterial bypass and in situ arterial bypasses are an important component of the treatment of many of these lesions. The introduction of endovascular flow-diversion stents (FDS) has significantly reduced the number of patients with complex intracranial aneurysms treated with direct clipping and some type of arterial bypass. However, significant complications have been reported with the use of these devices, and many complex intracranial aneurysms are not suitable for treatment with FDS. Thus, it is important for neurosurgery to retain the ability to perform intracranial arterial bypasses when indicated in the treatment of intracranial aneurysms and tumors.

Robert L. Grubb Jr

St. Louis, Missouri

Back to Top | Article Outline
CME Questions:

1. What is the 30-day perioperative stoke risk after STA-MCA bypass 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 year following 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%


Aneurysm; Bypass; Cerebral revascularization; Clipping; Endovascular; Extracranial-to-intracranial; Intracranial-to-intracranial

Copyright © by the Congress of Neurological Surgeons


Article Tools



Search for Similar Articles
You may search for similar articles that contain these same keywords or you may modify the keyword list to augment your search.