IC-IC Bypasses for Complex Brain Aneurysms

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13 IC-IC Bypasses for Complex Brain Aneurysms

Michael Lawton, Nader Sanai

Introduction

EC-IC bypass surgery has been essential in the management of brain aneurysms that are too complex for conventional clipping or endovascular coiling, despite its well-publicized failure to benefit patients with ischemic stroke in the EC-IC Bypass Trial.1,3,5,11,22,27 Revascularization of a territory distal to a giant, dolichoectatic, or thrombotic aneurysm enables the aneurysm to be occluded without risk of ischemic complications, or the parent artery’s blood flow to be reversed or reduced safely. The superficial temporal artery to middle cerebral artery (STA-MCA) bypass was the prototype, and subsequently an array of bypasses was developed with the same concept of redirecting extracranial blood flow from scalp arteries or cervical carotid arteries to the brain, either directly with one anastomosis or with interposition grafts and two anastomoses. In recent years, innovative bypasses have been introduced anecdotally that revascularize intracranial arteries with other intracranial arteries, without contribution from extracranial donor arteries.7–9,15,16,20 These intracranial to intracranial (IC-IC) bypasses are simple, elegant, and more anatomical than their EC-IC counterparts. IC-IC bypasses require no harvest of extracranial donors, spare patients a neck incision, shorten any interposition grafts, are protected within the cranium, and use caliber-matched donor and recipient arteries. These advantages of IC-IC bypasses appeal to experienced bypass surgeons, and their use has increased noticeably. For example, Sekhar and colleagues performed at least 11 IC-IC bypasses in an overall experience with 119 bypasses in 115 patients.26 Similarly, Spetzler and colleagues performed 28 IC-IC bypasses (44%) in an overall experience with 63 bypasses in 61 patients.15

The development of an array of IC-IC bypasses represents an important evolution of bypass surgery for brain aneurysms. We have embraced IC-IC bypasses in our aneurysm practice at the University of California, San Francisco, and categorize IC-IC bypasses into four types of intracranial arterial reconstruction: in situ bypass, reimplantation, reanastomosis, and intracranial bypass grafts.

Evolution of bypass surgery for brain aneurysms

Bypass surgery for brain aneurysms began with the introduction and popularization of the STA-MCA bypass by Yasargil.29 This simple bypass revascularized the MCA territory and protected patients from ischemic complications after deliberate arterial occlusion during the treatment of MCA and some ICA aneurysms. Bypass surgery for aneurysms evolved with the development of an array of EC-IC bypasses that used other extracranial donor arteries and interposition grafts connected to proximal donor sites in the neck.2,4,6,10,12–15,17–19,21,23,25,28,30 Even though these second-generation EC-IC bypasses yield excellent results, bypass surgery for aneurysms is evolving further with the development of an array of IC-IC bypasses that eliminates extracranial donor arteries and reconstructs the cerebral circulation in ways that resemble normal cerebrovascular anatomy. In this report, we analyzed this third generation of IC-IC bypasses in a large clinical series, categorized the techniques into four types, and demonstrated aneurysm and patient outcomes comparable to traditional EC-IC bypasses. Aneurysm obliteration rates, bypass patency rates, and neurological results (late GOS and change in GOS) were similar in EC-IC and IC-IC bypass patients, supporting this progression toward intracranial vascular reconstruction.

EC-IC bypasses are technically easier to perform than IC-IC bypasses. For example, an STA-MCA bypass requires one end-to-side anastomosis that is usually straightforward, particularly when the donor artery is large and mobilizes to visualize both suture lines. In contrast, an in situ bypass between two MCA branches requires a more challenging side-to-side anastomosis between arteries with limited mobility. Similarly, an ECA-MCA bypass requires a proximal anastomosis in the neck that can be performed in a superficial cervical site with no ischemia from cross-clamping an intracranial artery. In contrast, an A1 anterior cerebral artery (ACA)–MCA intracranial bypass graft requires a proximal anastomosis in a narrow surgical corridor that is even deeper than the distal anastomosis to the MCA. Although cross-clamping the A1 ACA does not produce ischemia in patients with a competent anterior communicating artery (ACoA), temporary clips on a major intracranial artery inevitably induce some time pressure. Therefore, IC-IC bypasses add a degree of difficulty.

Bypass demographics

Patients were divided into two groups according to the type of bypass: EC-IC versus IC-IC. EC-IC bypass involved donors arteries from external carotid artery branches (STA and occipital artery (OA)), cervical carotid arteries (common carotid artery (CCA), internal carotid artery (ICA), and external carotid artery (ECA)), or other extracranial arteries (e.g., subclavian artery). IC-IC bypass involved intracranial donor arteries, and were further categorized as in situ bypass (adjacent donor artery), reimplantation (aneurysm branch artery onto parent artery), reanastomosis (primary repair of parent artery), and intracranial bypass graft (graft interposed between donor and recipient arteries).

During a 10-year period between November 1997 and November 2007, 1984 aneurysms were treated microsurgically in 1578 patients by the senior author (MTL). Of these patients, 82 (5%) underwent cerebral revascularization surgery as part of the management of an intracranial aneurysm. Overall, there were 50 women and 32 men, with a mean age of 53 years (range, 12–78 years) (Table 13–1). Twenty-one patients presented with subarachnoid hemorrhage (26%). Hunt-Hess Grade III was the most common clinical grade (48%), and four patients presented with poor Hunt-Hess grade. Fifty-six patients (68%) presented with unruptured aneurysms and neurological symptoms, with cranial neuropathy or hemiparesis from mass effect present in 38 patients (68%). Eight patients (14%) presented with transient ischemic attacks or stroke in association with thrombotic aneurysms. Five patients presented with incidental, unruptured aneurysms (6%).

Table 13–1 Study Demographics.

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Aneurysm characteristics for IC-IC bypass patients

Aneurysms were distributed throughout the intracranial circulation, with the most common locations being the cavernous ICA (19 aneurysms, 23%), MCA (16 aneurysms, 20%), and posterior inferior cerebellar artery (PICA) (10 aneurysms, 12%) (Table 13–2). The majority of aneurysms were giant in size (46 aneurysms, 56%). Only 15 aneurysms (18%) had saccular morphology, and the remaining 67 aneurysms (82%) had fusiform or dolichoectatic morphology. Thirty-one patients (38%) had thrombotic aneurysms. Eight aneurysms (10%) had been treated endovascularly with coils, of which three were incompletely treated and five were recurrent. Fifteen patients (19%) had multiple aneurysms, with 26 other aneurysms diagnosed.

Table 13–2 Aneurysm Demographics.

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Patient selection

Patient selection is one of the most important elements for successful aneurysm revascularization. Although balloon test occlusion is not always reliable for determining the necessity for revascularization, our reviewed experience employed balloon test occlusion (BTO) to a select 26 patients for aneurysm management with a bypass, all of them with cavernous or supraclinoid ICA aneurysms. Ten patients failed the test with balloon inflation alone, and 16 patients failed with additional hypotensive challenge (lowering mean arterial pressure with nitroprusside drip by 20 mm Hg, or 25% of mean arterial pressure, whichever was greater). Failed BTO can be used as an indication for bypass. High-flow bypass should be used in patients who fail BTO immediately, and low-flow bypass in patients who fail BTO after hypotensive challenge. The decision to perform a bypass with aneurysms in other locations should be based on patients’ angiographic anatomy, specifically the presence or absence of collateral circulation from the circle of Willis.

In situ bypass technique

In situ bypass requires donor and recipient arteries that lie parallel and in close proximity to one another. Four sites have this anatomy: bilateral ACAs as they course through the interhemispheric fissure over the corpus callosum’s genu and rostrum (A3 and A4 segments); MCA branches (M2 and M3 segments) and the anterior temporal artery (ATA) as they course through the Sylvian fissure; posterior cerebral artery (PCA, P2, and P3 segments) and superior cerebellar artery (SCA) as they course through the ambient cistern around the cerebral peduncle; and bilateral PICAs as they course through the cisterna magna to meet behind the medulla underneath the cerebellar tonsils. In situ bypasses require one side-to-side anastomosis.

Reimplantation technique

Complex aneurysms with branches that originate from the aneurysm base or side wall can often be reconstructed with tandem clipping techniques that preserve important branch arteries (a fenestrated clip encircling the branch origin and a stacked straight clip closing the fenestration). In cases where clip reconstruction fails, the neck can be clipped to exclude the aneurysm, preserve the parent artery, and sacrifice the branch artery. The occluded branch artery can then be reconstituted with reimplantation onto the parent artery (Figure 13–1). Alternatively, the branch artery can be reimplanted to an adjacent donor artery that is not the parent artery, as long as that donor artery lies in close proximity to the branch (Figure 13–2). Like in situ bypasses, this favorable anatomy occurs with MCA, ACA, and PICA aneurysms. Reimplantation requires one end-to-side anastomosis.

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Figure 13–1 Recipient reimplantation. This thrombotic ACA aneurysm, seen on axial T1-weighted magnetic resonance image (A), originated at the bifurcation of the pericallosal (PC) and callosomarginal (CM) arteries (B), right ICA angiogram, lateral view). C and D, The aneurysm (An) was exposed in the interhemispheric fissure through a bifrontal craniotomy, using gravity to retract the right hemisphere. Attempts to clip reconstruct the neck were unsuccessful; intraluminal thrombus caused the clips to occlude the pericallosal artery. The pericallosal artery was clip occluded, transected, and mobilized to the callosomarginal artery (E). An end-to-side PC-CM anastomosis was performed: back wall (F), front wall (G), and after completion (H). I, The CM artery supplied blood flow to the entire distal ACA territory.

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

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Figure 13–2 Donor reimplantation. This multilobulated left SCA aneurysm, seen on rotational angiogram with three-dimensional reconstruction (A), was incompletely coiled, leaving residual neck to preserve the SCA origin. After inspecting the anatomy intraoperatively, it seemed unlikely that the aneurysm could be clipped with occluding SCA and likely that a bypass would be needed to preserve it. B, A prominent ATA was found in the Sylvian fissure. C, This ATA had sufficient length to reach the SCA. D, The ATA was transected distally and reimplanted onto SCA with an end-to-side anastomosis. E, After bypass patency was confirmed, the aneurysm (An) was neck was dissected (F) and clipped (G) (arrows). H, Indocyanine green videography confirmed good flow in the ATA-SCA bypass, as did the postoperative angiogram (I) (left ICA injection, lateral view, with opacification of the left SCA [arrows]). Note the course of the SCA over the cerebellar vermis (asterisk). MCA, middle cerebral artery; ICA, internal carotid artery; PCA, posterior cerebral artery; CN3, oculomotor nerve.

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

Reanastomosis technique

Reanastomosis requires trapping the aneurysm, completely detaching afferent and efferent arteries, and reconnecting cut ends with an end-to-end anastomosis (Figure 13–3). This technique works well with fusiform aneurysms that are small or medium in size. Saccular aneurysms at bifurcations with more than two or more efferent arteries are difficult to reconstruct with primary reanastomosis because the second branch must either be reimplanted or bypassed with an extracranial donor artery. Large and giant aneurysms may be difficult to reanastomose because ends of the parent artery can be widely separated after excising an aneurysm. Mobilizing the ends of afferent and efferent arteries may enable the first stitch to pull them together with minimal tension. If the gap in the parent artery is too long and the tension too great, the suture will tear through the artery wall as it is tightened and ruin the repair. Some large aneurysms in PICA and MCA territories have an unusually redundant parent artery that will allow primary reanastomosis despite their size. Reanastomosis requires one end-to-end anastomosis.

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Figure 13–3 Reanastomosis. A, Digital subtraction angiogram (right internal carotid injection, lateral view) showed a distal middle cerebral artery aneurysm. After opening the distal Sylvian fissure (B), this large thrombotic aneurysm was exposed (C). The aneurysm was trapped between two permanent clips (D), and the afferent and efferent arteries were joined with an end-to-end anastomosis (E) to re-establish blood flow (F). G, Intraluminal thrombus prevented direct clipping. H, Postoperative angiography (right internal carotid injection, lateral view) confirmed exclusion of the aneurysm and preservation of angular branches.

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

Intracranial bypass technique with grafts

These bypasses use interposition grafts to connect donor and recipient arteries that are entirely intracranial, differentiating them from traditional EC-IC bypasses that utilize extracranial donor arteries (Figures 13-4 through 13-6). In contrast to EC-IC bypasses that use saphenous vein grafts to span from the neck to the Sylvian fissure, intracranial bypass grafts are shorter and radial artery grafts are sufficiently long. Radial artery grafts are preferred over saphenous vein grafts because they are composed of arterial tissue, have higher long-term patency rates, and match the caliber of intracranial arteries. Preoperatively, an Allen’s test with Doppler ultrasound is performed to ensure adequate perfusion of the hand with the ulnar artery and a competent palmar arch.

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Figure 13–4 Intracranial bypass graft with double reimplantation. A, This ruptured right MCA aneurysm was coiled, and recurred 6 months later (right ICA angiogram, anterior oblique view). B, Intraoperatively, the two M2 MCA trunks originated from the aneurysm (An) base and could not be kept open with direct clipping. Note the strand of coil in the lumen of the temporal M2 trunk (arrow). C, The A1 segment of the ACA was used as the donor for a radial artery graft (RAG) that was sutured with an end-to-side anastomosis (D and E). The frontal M2 trunk was reimplanted onto the RAG with a side-to-side anastomosis: (F) shown after suturing the deep suture line intraluminally and (G) after completing the superficial suture line. H, The end of the RAG was looped to the temporal M2 trunk and sewn with an end-to-side anastomosis. Postoperative angiography (right ICA injection, lateral [I] and anterior-posterior views [J]) confirmed patency of the bypass and filling of both MCA trunks (arrows indicate anastomoses).

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

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Figure 13–5 Intracranial bypass graft. A, This fusiform, giant basilar trunk aneurysm (left VA angiogram, anterior oblique view) was treated with a VA-SCA bypass. B, A combined far lateral-temporal craniotomy provided a subtemporal view of the basilar artery (BA) apex. C and D, A RAG was anastomosed to the right SCA. E, The proximal end of the graft was connected to the side of extradural VA at the foramen magnum. F, The course of the VA-SCA bypass is shown intraoperatively (arrows) and (G) angiographically (right VA injection, anterior-posterior view, with anastomoses indicated by the arrows). VA-SCA bypass and clip occlusion of the right VA resulted in thrombosis of the aneurysm lumen, shown preoperatively in blue and postoperatively in red on overlaid volumetric images generated from contrast-enhanced magnetic resonance angiography: lateral view (H) and anterior-posterior view (I).

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

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Figure 13–6 Intracranial bypass graft. An MCA-PCA bypass was used to treat this fusiform, giant basilar trunk aneurysm seen on coronal reformatted computed tomography angiogram (A) and three-dimensional reconstruction (B). Note the large amount of intraluminal thrombus and filling defect. C, The recipient PCA was accessed through a trans-Sylvian, pretemporal exposure. D and E, A radial artery graft (RAG) was connected with end-to-side anastomosis. F, The distal end of the RAG was connected to a donor M2 MCA branch, after which the basilar artery was clip occluded below the SCA, distal to the aneurysm. G, Postoperative CTA demonstrated patency of the bypass graft (white arrows). H, Thrombosis of the aneurysm below the clip. ICA, internal carotid artery; CN3, cranial nerve 3.

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

Intraoperatively, the forearm can be accessed to harvest the radial artery more easily than the thigh, particularly when the patient is positioned laterally or prone for posterior circulation aneurysms. Vasospasm in radial artery grafts has been described, but can be avoided by using pressure distension to dilate the graft before implantation, and by bathing the graft in a mixture of nitroprusside and heparin. Unlike the other IC-IC techniques, intracranial bypass grafts require at least two anastomoses and may require end-to-side, end-to-end, or side-to-side anastomoses. The anastomoses are planned to minimize brain ischemia during the time that intracranial arteries are temporarily occluded and sutured.

Selection of the Microsurgical Corridor

As can be expected, surgical approach depends on aneurysm location (see Table 13–2). ICA aneurysms are approached through a pterional craniotomy in most cases, with an orbitozygomatic craniotomy used for additional exposure with giant aneurysms. Similarly, a pterional craniotomy is adequate for most MCA aneurysms, with an orbitozygomatic craniotomy used with two giant aneurysms. ACA aneurysms are exposed through bifrontal craniotomies to access the interhemispheric fissure, with the midline of the head positioned parallel to the floor and angled up 45 degrees to allow gravity to retract the dependent hemisphere. All bypasses for basilar apex aneurysms are performed through orbitozygomatic craniotomies, capitalizing on its additional trans-Sylvian exposure for these deep bypasses. The VA-SCA bypass for basilar trunk aneurysms is performed through a combined far lateral-subtemporal craniotomy. PICA bypasses are performed through far lateral craniotomies, although the PICA-PICA bypass does not require extensive resection of the occipital condyle or much lateral exposure when performed without accessing the aneurysm, as with a staged endovascular occlusion (three patients).

Selection of the Bypass

Aneurysm location influenced bypass design. In our institutional experience, 31 of 33 patients with ICA aneurysms underwent EC-IC bypass. EC-IC bypasses are preferable and easier than IC-IC bypasses for these aneurysms at the skull base with limited proximal donor sites intracranially. The petrous-to-supraclinoid ICA bypass is the only IC-IC bypass used for ICA aneurysms. Similarly, nine of 14 aneurysms involving the basilar artery apex or trunk were managed with EC-IC bypass because of their deep location and limited proximal donor sites. IC-IC bypasses for basilar artery aneurysms include MCA-PCA bypass with radial artery grafts, VA-SCA bypass, and ATA-SCA reimplantation. In contrast to ICA and basilar artery aneurysms, ACA and PICA aneurysms are revascularized exclusively with IC-IC bypasses. The distal ACA territory is far removed from extracranial donor arteries in the neck, making IC-IC bypasses more appealing. IC-IC bypass options were numerous with PICA aneurysms and eliminated the tedious dissection required to harvest the occipital artery. Bypasses for MCA aneurysms are typically split between EC-IC and IC-IC bypasses.

Intraoperative Considerations

Brain relaxation is achieved with mannitol (1 g/kg) and cerebrospinal fluid drainage through a ventriculostomy, fenestration in the lamina terminalis, or dissection into a subarachnoid cistern. During the anastomosis, when parent arteries are temporarily occluded, mild hypothermia and barbiturate-induced electroencephalographic burst suppression can be used to increase tolerance to cerebral ischemia. In our experience, the average intracranial cross-clamp time for EC-IC bypass was 46 minutes (range, 32–63 minutes), and for IC-IC bypass was also 46 minutes (range, 26–76 minutes). Blood pressure was increased with pressor agents during this time if changes in somatosensory evoked potentials or the electroencephalogram were detected, but electrophysiological changes were rarely encountered. Heparin irrigation is used liberally in the surgical field during the anastomosis, but systemic heparin is not used.

The University of California, San Francisco Bypass Experience

In our institutional experience, of the 82 patients with aneurysms requiring a bypass, 47 patients (57%) received EC-IC bypasses and 35 patients (43%) received IC-IC bypasses.24 EC-IC bypasses included 16 low-flow bypasses with STA donors in 15 patients and OA donor in one patient (Table 13–3). High-flow EC-IC bypasses were performed in 31 patients using saphenous vein grafts in 27 patients and radial artery grafts in four patients. IC-IC bypasses consisted of in situ bypasses in nine patients (26%), reimplantation in six patients (17%), reanastomosis in 11 patients (31%), and intracranial bypass grafts in nine patients (26%) (Table 13–4). Unlike extracranial bypass grafts, intracranial bypass grafts used radial artery more frequently than saphenous vein (six patients vs. three patients, respectively). Seven patients had complex bypass configurations like double reimplantations or additional STA-MCA bypasses (Table 13–5), of which five were categorized as IC-IC bypass patients and two as EC-IC bypass patients.

Table 13–3 Distribution of Operative Approaches.

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Table 13–4 EC-IC Bypasses.

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Table 13–5 IC-IC Bypasses.

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Aneurysm occlusion was performed during the surgery in 54 patients and consisted of 27 aneurysm trappings (33%), 16 proximal aneurysm occlusions (20%), six distal aneurysm occlusions (7%), and five aneurysm clippings (6%) (Tables 13–6 and 13–7). The remaining 28 patients (34%) underwent staged endovascular occlusion of their aneurysms. Twenty-two of these endovascularly treated patients were in the EC-IC bypass group, reflecting the large number of ICA aneurysms. In contrast, half of the aneurysms in the IC-IC bypass group were trapped during surgery, reflecting the accessibility of these more distally located aneurysms. The small number of aneurysms clipped directly reflects the nonsaccular morphology of these aneurysms. Endovascular staging was typically performed 2 to 3 days after the bypass procedure. Patients were started on aspirin (350 mg qd) immediately after surgery.

Table 13–6 Complex Bypass Techniques.

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Table 13–7 Operative and Clinical Outcomes Following EC-IC and IC-IC Bypass.

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Angiography was performed after surgery in all patients to evaluate patency of the bypass and exclusion of the aneurysm. Overall, 80 of 82 aneurysms treated with a bypass were obliterated angiographically (97.6% obliteration rate). All four clipped and 26 trapped aneurysms were completely excluded. Of the 15 aneurysms that were proximally occluded, 14 were angiographically occluded postoperatively. Of the five aneurysms that were distally occluded, four were angiographically occluded postoperatively. Two fusiform aneurysms were filling angiographically after surgery, but had new intraluminal thrombosis, smaller angiographic size, and reduced flow. The 28 aneurysms that were treated with staged endovascular therapy were completely occluded, 16 of them with coils and 12 with proximal balloons. All six aneurysms with IC-IC bypasses were treated with direct coil occlusion, whereas only nine of 21 aneurysms with EC-IC bypasses were treated with direct coil occlusion. Aneurysm obliteration was comparable in the EC-IC and IC-IC bypass groups (97.9% and 97.1%, respectively).

Overall, 75 of 82 bypasses were patent on postoperative angiography (91%). Three EC-IC bypasses and four IC-IC bypasses occluded, with comparable patency rates in the two groups (94% and 89%, respectively). Intraoperative events predicted later occlusion in four cases. Two bypass grafts from the cervical carotid to MCA became limp at the end of the cases and both bypasses were revised (one proximally, and one proximally and distally). One patient with a gunshot-related dissecting ACA aneurysm had damaged parent arteries that were reanastomosed after aneurysm excision. The initial repair occluded, the parent artery was excised back to more normal tissue, and the anastomosis was revised, albeit under increased tension. One MCA thrombosed after clipping of a large M1 segment aneurysm. The aneurysm was excised, the M1 segment was thrombectomized, and reanastomosis restored MCA flow. Despite intraoperative recognition of bypass occlusion and immediate revision in these four cases, the bypasses occluded postoperatively. The remaining three bypass occlusions were unexpected. One of these patients had a saphenous vein with significant varicosities, and one MCA reanastomosis required an STA interposition graft to bridge the gap in the parent artery.

Three patients died in the perioperative period (surgical mortality, 3.7%), all of them with basilar trunk aneurysms. These patients underwent uncomplicated bypass procedures to revascularize the upper basilar artery (STA-SCA, STA-PCA, and ECA-SCA), but subsequent endovascular therapy resulted in aneurysm re-rupture during coiling, basilar artery thrombosis after bilateral vertebral artery occlusions, and intracerebral hemorrhage while on heparin after bilateral vertebral artery occlusions.

Permanent neurological morbidity was observed in four patients (4.9%), all related to bypass occlusions. These patients suffered MCA strokes after occlusion of high-flow EC-IC bypasses in three patients and an MCA reanastomosis in one patient. Two other bypass occlusions (after aneurysm excision and reanastomosis) did not cause any permanent neurological deficits, and one bypass occlusion caused only transient neurological deficits. In addition to this patient with transient neurological deficits related to bypass occlusion, three patients had postoperative epidural hematomas with deficits that resolved completely (transient neurological morbidity, 4.9%).

Excluding the three surgical mortalities and three additional patients lost to follow-up, final neurological outcomes were assessed in 76 patients (93%). Mean duration of follow-up was 41 months (range, 1–125 months), and did not differ significantly between EC-IC and IC-IC bypass groups (38.6 months and 42.7 months, respectively). Four patients died after hospital discharge, three from complications in rehabilitation and one from delayed growth of a basilar trunk aneurysm with resulting brainstem compression. Three of the four late deaths were in the EC-IC bypass group. Good outcomes (GOS 5 or 4) were measured in 68 patients (90%) overall, and were similar in EC-IC and IC-IC bypass groups (91% and 89%, respectively) (Table 13–7). At late follow-up, 15 patients (20%) were improved and 53 (70%) were unchanged, relative to preoperative neurological condition, excluding lost patients. Changes in outcome by GOS were slightly more favorable in the IC-IC bypass group than the EC-IC bypass group (6% vs. 14% worse or dead in IC-IC vs. EC-IC bypass groups, respectively). Mean final GOS scores reflected a similar trend, with a mean GOS of 4.3 in the EC-IC bypass group and 4.6 in the IC-IC bypass group. Relative to preoperative neurological condition, mean GOS decreased 0.30 in the EC-IC bypass group and increased 0.21 in the IC-IC bypass group.

Conversion of EC-IC to IC-IC

Easy conversion from EC-IC to IC-IC bypass is needed to embrace this progression to intracranial vascular reconstruction. Every current EC-IC bypass can be translated to an IC-IC bypass presented in this clinical experience (Table 13–8). ACA and PICA territories were particularly amenable to intracranial reconstruction, and even though MCA and basilar apex territories were divided between EC-IC and IC-IC techniques, growing experience with A1 ACA-MCA and MCA-PCA bypasses have made them preferred choices for their respective territories.

Table 13–8 EC-IC to IC-IC Conversion Chart.

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Selecting a bypass from amongst the four IC-IC techniques depends on aneurysm anatomy, suitability of the donor artery, depth of the surgical field, and type of anastomosis. Fusiform aneurysms lend themselves to reanastomosis because frequently they are distally located away from bifurcations or origins of branch arteries, with one afferent and one efferent artery. The success of an end-to-end repair hinges on the excising aneurysm back to healthy arterial tissue on both ends, and on joining those ends without tension. Mobilizing redundant artery and resecting trapped aneurysm can help bring the arteries together. If the anatomy is favorable, end-to-end anastomosis is the easiest to do. Tips of the forceps can be held in the lumen to visualize translucent arterial walls and guide the needle through its bites; the number of bites needed to complete the anastomosis is small; and the arteries rotate freely to visualize the two suture lines.

In contrast to fusiform aneurysms, saccular aneurysms occur at bifurcations with two or more efferent arteries and other reconstructive techniques are required. In situ bypass and reimplantation are effective when a saccular aneurysm is obliterated while preserving one of the efferent arteries. For example, the ACA-ACA in situ bypass works when clipping or coiling an ACoA aneurysm sacrifices one A2 ACA. The other patent A2 ACA supplies the distal bypass and restores flow to the opposite ACA. In situ bypasses require a side-to-side anastomosis, which is probably the most difficult anastomosis because the deep suture line is sewn inside the lumen. After approximating the two arteries with sutures at each end of the arteriotomies, the first bite must transition the needle from outside the lumen where the knot is tied, to inside the lumen where the running bites are taken. The neurosurgeon must work between two outer layers of arterial wall, keeping track of four translucent layers. The last bite must transition the needle again from inside to outside the lumen to tie the knot. The arteriotomy length with side-to-side anastomosis should be three times the diameter of the arteries in order to create generous communication between arteries. Therefore, side-to-side anastomoses require more bites than other anastomoses. Tracking all four walls and long suture lines make this a more difficult anastomosis that should be avoided in deep, narrow surgical fields. Side-to-side anastomosis can be performed comfortably in the Sylvian fissure, cisterna magna, and interhemispheric fissure, but it has not been attempted at the depths of the basilar apex. The superficial suture line is performed from outside the lumen and is much easier.

Reimplantation is the other basic reconstructive technique that salvages a branch artery compromised by aneurysm occlusion. An end-to-side anastomosis to the parent artery, the other efferent artery, or an uninvolved bystander will rescue this branch. PICA-VA reimplantation was the most frequent location for this technique, but it also works well in the MCA and ACA territories (pericallosal to callosomarginal reimplantation). These recipient reimplantations connect the proximal end of a branch to the side of the donor, but donor reimplantations can also connect the distal end of a branch to a recipient artery to rededicate the branch artery to supplying a new vascular territory. For example, the ATA supplies a silent vascular territory, and when reimplanted onto the SCA, it can assume the supply of the SCA or even the basilar apex. The ATA-SCA bypass therefore demonstrates another facet of the reimplantation technique. Technically, end-to-side anastomosis is identical to that used with STA-MCA bypass. A generous arteriotomy is made in the donor (at least two times the diameter of the artery), and the end of the reimplanted recipient is spatulated to cover the arteriotomy. Simple continuous sutures are loosely placed and tightened after all bites have been taken. The site of reimplantation should be selected to make the reimplanted artery as slack as possible because a mobile artery can be shifted from one direction to another to better visualize the two suture lines.

Complex reconstructions are required when multiple efferent arteries are compromised. For example, the double reimplantation technique completely rebuilds a bifurcation with three anastomoses. A radial artery graft is first connected proximally to a donor artery to ready the bypass graft. The first efferent artery is reimplanted on the live graft and blood flow is restored immediately. The second efferent artery is reimplanted distally on the graft, allowing the graft to supply the first reimplanted artery during this second reimplantation. Placement of a temporary clip distal to the first and proximal to the second anastomosis redirects blood flow to the reimplanted trunk while keeping the other surgical site dry. This successive reimplantation of branch artery minimizes ischemia, with temporary occlusion times for each of the efferent arteries equal to the time needed to complete one anastomosis. This double reimplantation technique adapts to triple reimplantation for trifurcated anatomy. Other intracranial bypass grafts replenish cerebral blood flow with fewer anastomoses. For example, the MCA-PCA bypass revascularizes the quadrifurcated anatomy of the basilar apex with a single deep anastomosis. The superficial anastomosis site is already accessible after the exposure of the recipient P2 PCA site. Intracranial bypass grafts like the MCA-PCA bypass do not fully reconstruct the arterial anatomy and may not enable complete exclusion of the aneurysm, but may reverse flow or create more benign hemodynamics inside the aneurysm.

Bypass selection ultimately depends on an intraoperative assessment of the aneurysm and surrounding anatomy. We typically devise a primary bypass strategy, several contingency strategies (Table 13–8), and make preparations for each (like prepping a graft site). At surgery, there may be several viable options (e.g., PICA-PICA bypass and PICA reimplantation), no options (e.g., P3 segment PCA aneurysm), or serendipitous anatomy presenting unexpected options (e.g., ATA-SCA bypass). We select the bypass that facilitates aneurysm occlusion, restores normal blood flow, and is technically most feasible.

Limitations of IC-IC Bypasses

IC-IC bypasses can potentially replace EC-IC bypasses, as intracranial reconstructive techniques represent an evolution of bypass surgery for aneurysms. However, these conclusions are based on our comparative analysis between two groups of patients that are different and highly selected. While IC-IC bypasses can be applied to ACA, PICA, basilar apex aneurysms, and many MCA aneurysms, EC-IC bypasses will remain the preferred choice for petrous, cavernous, and supraclinoid ICA aneurysms because intracranial carotid reconstruction is technically difficult and associated with risks from exposing the petrous ICA (hearing loss, facial weakness, etc.). Therefore, the progression from EC-IC to IC-IC bypass does not encompass all aneurysms. The STA-MCA bypass will forever be a versatile technique and we are not suggesting that it be abandoned.

Seventeen different bypasses have been performed in the course of our clinical experience, indicating that a wide variety of reconstructions can be created. Some bypasses discussed here were not performed, like the PCA-SCA bypass and the petrous ICA-MCA bypass graft. Indications for these bypasses are few and technical demands are high. Other intracranial bypasses, like Spetzler’s “figure-8 anastomosis,” were not a part of our experience but should be included in menu of IC-IC bypasses. Innovative neurosurgeons will add to this menu over time and we will have a deepening armamentarium of intracranial bypasses for most aneurysms.

Bypass with aneurysm occlusion is a good strategy for managing giant, dolichoectatic, thrombotic, or previously coiled aneurysms because it avoids the unpredictable strategy of thrombectomy with clip reconstruction. It also avoids risky adjuncts like hypothermic circulatory arrest. However, deliberate hemodynamic alteration with bypass and aneurysm occlusion can also be risky and unpredictable. Poor outcomes can be encountered with flow reversal in basilar trunk aneurysms due to basilar artery thrombosis or occlusion of perforators. Other complications come from heparinization to decelerate aneurysm thrombosis, with subsequent intracranial hemorrhage. Bypass with incomplete aneurysm occlusion relies on some degree of intraluminal aneurysm thrombosis, with unavoidable dangers. This management of basilar trunk aneurysms may not be the best strategy for this difficult disease. We are hopeful that stents or other endovascular devices will offer reconstructive options without open surgery. However, such endovascular therapies are not available presently and will need to be evaluated critically before they replace surgical bypass strategies.

Conclusions

Despite the added complexity of IC-IC bypasses, the extra effort is justified for several reasons. First, the caliber of extracranial scalp arteries is highly variable and sometimes too diminutive to revascularize an occluded efferent artery. Although scalp arteries can dilate over time to meet demand, they may not be able to restore blood flow immediately. Deep bypasses to midline or paramedian arteries can require 8 cm or more of scalp artery and are often too small at the anastomotic depth to be safe. In contrast, in situ bypass, reanastomosis, and reimplantation techniques use donor arteries that match or exceed the caliber of recipient arteries. Second, EC-IC bypasses that use the cervical carotid artery as a donor require long interposition grafts at the limit of the radial artery graft. Therefore, saphenous veins were used more frequently than radial arteries with our EC-IC bypasses, introducing significant caliber mismatches between the graft and intracranial artery. Longer grafts are also associated with lower patency rates long-term. In contrast, intracranial bypass grafts are shorter and enabled us to use radial artery grafts more frequently. Their smaller caliber closely resembles that of intracranial arteries and enhances the anastomosis. Although late patency rates were not measured in this study, shorter grafts with arterial composition are more likely to remain patent. Third, IC-IC bypasses eliminate cervical incisions, minimizing invasiveness and improving cosmesis. Intracranial bypasses are less vulnerable than EC-IC bypasses to neck torsion, injury, and inadvertent occlusion with external compression. Fourth, IC-IC bypasses eliminate the need to harvest an extracranial donor artery, saving time and tedious effort. Intracranial donor arteries reside in the surgical field that is already dissected, and typically require minimal preparation for the bypass. Finally and importantly, temporarily occluding an intracranial artery for bypass is well tolerated in the territories of most IC-IC bypasses. In situ bypasses and reimplantations require temporary occlusion of two intracranial arteries to perform the anastomosis, instead of just temporarily occluding one recipient artery with a traditional EC-IC bypass. However, neurophysiological changes are rarely encountered during these occlusion times and always resolved with a boost in arterial pressure. In our experience, we have not observed any neurological morbidity related to temporarily occluding an intracranial artery during anastomosis, or related to an intracranial donor artery that would not have been involved in an EC-IC bypass.

In our opinion, these advantages of IC-IC bypass justify their use. They are more technically challenging to perform, but well within the expertise of experienced bypass neurosurgeons. The end result is an array of elegant and more anatomical bypasses that we think represents the next generation of bypass surgery for aneurysms.

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