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
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.
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.
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).
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).
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.
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.
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.
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.
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.
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.
Our management strategy for aneurysms at specific sites is discussed below.
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
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).
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
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.
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
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
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.
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.
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.
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.
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...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.
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.
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.
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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.
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
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.
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
1. What is the 30-day perioperative stoke risk after STA-MCA bypass for ipsilateral carotid occlusion?
2. What is the 5 year risk of rupture for a giant (>2.5 cm) aneurysm in the anterior circulation?
3. What is the documented incidence of delayed ischemia per year following carotid occlusion after BTO (balloon test occlusion)?