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%).

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.

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.

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.

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.

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.

Figure 13–4 Intracranial bypass graft with double reimplantation. A,

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