Aneurysms that are too complex for conventional

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1 J Neurosurg 20: , 204 AANS, 204 Anterior cerebral artery bypass for complex aneurysms: an experience with intracranial-intracranial reconstruction and review of bypass options Clinical article Adib A. Abla, M.D., and Michael T. Lawton, M.D. Department of Neurological Surgery, University of California, San Francisco, California Object. The authors describe their experience with intracranial-to-intracranial (IC-IC) bypasses for complex anterior cerebral artery (ACA) aneurysms with giant size, dolichoectatic morphology, or intraluminal thrombus; they determine how others have addressed the limitations of ACA bypass; and they discuss clinical indications and microsurgical technique. Methods. A consecutive, single-surgeon experience with ACA aneurysms and bypasses over a 6-year period was retrospectively reviewed. Bypasses for ACA aneurysms reported in the literature were also reviewed. Results. Ten patients had aneurysms that were treated with ACA bypass as part of their surgical intervention. Four patients presented with subarachnoid hemorrhage and 3 patients with mass effect symptoms from giant aneurysms; patient with bacterial endocarditis had a mycotic aneurysm, and patient s meningioma resection was complicated by an iatrogenic pseudoaneurysm. One patient had his aneurysm discovered incidentally. There were 2 precommunicating aneurysms (A segment of the ACA), 5 communicating aneurysms (ACoA), and 3 postcommunicating (A 2 A 3 segments of the ACA). In situ bypasses were used in 4 patients (A 3 -A 3 bypass), interposition bypasses in 4 patients, reimplantation in patient (pericallosal artery-to-callosomarginal artery), and reanastomosis in patient (pericallosal artery). Complete aneurysm obliteration was demonstrated in 8 patients, and bypass patency was demonstrated in 8 patients. One bypass thrombosed, but 4 years later. There were no operative deaths, and permanent neurological morbidity was observed in 2 patients. At last follow-up, 8 patients (80%) were improved or unchanged. In a review of the 29 relevant reports, the A 3 -A 3 in situ bypass was used most commonly, extracranial (EC) IC interpositional bypasses were the second most common, and reanastomosis and reimplantation were used the least. Conclusions. Anterior cerebral artery aneurysms requiring bypass are rare and can be revascularized in a variety of ways. Anterior cerebral artery aneurysms, more than any other aneurysms, require a thorough survey of patientspecific anatomy and microsurgical options before deciding on an individualized management strategy. The authors experience demonstrates a preference for IC-IC reconstruction, but EC-IC bypasses are reported frequently in the literature. The authors conclude that ACA bypass with indirect aneurysm occlusion is a good alternative to direct clip reconstruction for complex ACA aneurysms. ( Key Words aneurysm bypass anterior cerebral artery vascular disorders Aneurysms that are too complex for conventional clipping or endovascular coiling often require bypass as part of a strategy that first revascularizes territories distal to the aneurysm and then occludes the aneurysm without risk of ischemic complications. This approach is particularly relevant to giant, dolichoectatic, Abbreviations used in this paper: ACA = anterior cerebral ar tery; ACoA = anterior communicating artery; EC = extracranial; ELANA = excimer laser-assisted nonocclusive anastomosis; IC = intracranial; MCA = middle cerebral artery; mrs = modified Rankin Scale; PCA = posterior cerebral artery; RAG = radial artery graft; STA = superficial temporal artery; SVG = saphenous vein graft. and thrombotic aneurysms and has been applied with some success. Most aneurysms of the anterior cerebral artery (ACA) are amenable to conventional clipping or endovascular coiling, even when they are complex, and rarely require bypass surgery. In an experience with 82 patients with complex aneurysms, ACA bypasses were performed least of all. 30 Anterior cerebral artery bypasses are particularly challenging for several reasons. First, most ACA aneurysms requiring bypass are located around the anterior This article contains some figures that are displayed in color on line but in black-and-white in the print edition. 364 J Neurosurg / Volume 20 / June 204

2 Anterior cerebral artery bypasses for complex aneurysms communicating artery (ACoA) complex which has 2 afferent arteries (the A segments of the ACA bilaterally), 4 efferent arteries (the A 2 ACA segments and recurrent arteries of Heubner bilaterally), ACoA and its perforators, and nearby branch arteries (orbitofrontal and frontopolar arteries bilaterally). Furthermore, ACoA variability may increase the number of involved arteries with accessory A 2 branches or decrease the number with an atretic A segment or an azygos A 2 segment. This anatomical complexity and variability make ACA revascularization more difficult. Second, unlike most aneurysms whose surgical exposure accesses both the proximal afferent and distal efferent arteries for vascular control and anastomosis, these ACA aneurysms sit at the limit of transsylvian exposure, and access to both sides of the aneurysm requires 2 separate approaches. The pterional-transsylvian approach exposes the A segments and the aneurysm but provides only limited exposure of the proximal A 2 segments. The bifrontal-interhemispheric approach exposes the A 2 segments and the aneurysm but provides only limited exposure of the distal A segments. Therefore, these aneurysms lack one simple, encompassing surgical corridor in which to perform a bypass. Third, neurosurgeons who are proficient at bypass procedures mostly perform a traditional extracranial-to-intracranial (EC-IC) bypass that utilizes the superficial temporal artery (STA) as the donor artery, as with the STA-to middle cerebral artery (STA-MCA) bypass for complex MCA aneurysms, carotid occlusive disease, and moyamoya disease. The STA is less useful for ACA aneurysms because it is a lateral scalp artery that may not reach efferent arteries at the depths of the interhemispheric fissure, or it may be too small in caliber if it does. Interposition grafts from the STA or cervical carotid artery intended to address this problem are often long and circuitous and require extensive surgical exposures. Therefore, ACA aneurysms call for other, less traditional bypasses like the intracranial-tointracranial (IC-IC) bypasses that are less familiar. In the report, we describe our experience with ACA bypass for complex aneurysms, which has been entirely IC-IC bypasses. We also review the literature to determine how others have addressed the limitations of ACA bypass. Finally, we discuss our clinical indications and microsurgical technique to help simplify the therapeutic decisions in these patients. We hypothesized that a simple algorithmic approach might be developed for managing patients who require ACA bypass. Methods Study Design This study was approved by the institutional review board and was conducted in compliance with Health Insurance Portability and Accountability Act regulations. Patients who underwent a bypass procedure involving the ACA were identified from the prospectively maintained database of the Vascular Neurosurgery Service at the University of California San Francisco. Patients with intracranial aneurysms were included in the study, whereas those with ischemia, moyamoya disease, tumor, or other J Neurosurg / Volume 20 / June 204 pathology were excluded. Medical records, preoperative radiographic images, operative reports, intraoperative photographs, hospital course, inpatient and outpatient charts, and follow-up radiographic images were reviewed. A clinician not directly involved in the care of these patients performed all outcome assessments. Neurological outcomes were assessed using the modified Rankin Scale (mrs). Patient Population During a 6-year period from September 997 to August 203, 3268 aneurysms were treated microsurgically by the senior author in 252 patients. During the same time, 323 bypasses were performed for the treatment of cerebrovascular diseases, of which 45 were for aneurysms. Ten bypasses were performed for ACA aneurysms in 0 patients, representing 0.3% of all aneurysms, 0.4% of all aneurysm patients, and 6.9% of bypasses for aneurysms. Nomenclature and Definitions Anterior cerebral artery segments as defined by Perlmutter and Rhoton 28 include: A, the precommunicating segment; A 2, the postcommunicating segment; A 3, the precallosal segment curving around the genu; A 4, the supracallosal segment on the anterior body of the corpus callosum; and A 5, the postcallosal segment on the posterior body to the splenium. Anterior cerebral artery aneurysms were categorized as precommunicating when they involved the A segment, communicating when located on the ACoA or at the A - A 2 junction, or postcommunicating when they involved distal ACA segments (A 2 A 5 segments) (Fig. ). Anterior cerebral artery bypasses are described by their involved segments (for example, A 2 -A 2, A 3 -A 3, and A 4 -A 4 bypass) and by their branch artery (pericallosal artery to pericallosal artery bypass). Segmental descriptions are usually more accurate than branch artery descriptions because of variability in the segment of origin of these branches. Bypasses are characterized by their donor blood flow as either EC-IC or IC-IC. Intracranial-to-intracranial bypasses are also characterized by one of 4 surgical techniques. An in situ bypass uses a parallel and proximate donor artery that is connected to the recipient artery with a side-to-side anastomosis. A reimplantation bypass reattaches the recipient artery to a parent or other donor artery with an end-to-side anastomosis. A reanastomosis bypass repairs the parent artery directly by reconnecting the afferent and efferent arteries with an end-to-end anastomosis. When the anatomy is unfavorable for one of the IC-IC reconstructions, an interpositional bypass uses a harvested graft (radial artery or saphenous vein) to connect donor and recipient arteries with 2 or more anastomoses. Anterior cerebral artery bypasses can be characterized by direction of flow. First, their interhemispheric location brings right and left arteries together in the midline to allow left-right flow. Second, their long course in the sagittal plane allows bypass flow from anterior to posterior, typically with interposition grafts. Third, the availability of donor flow from MCAs or from extracra- 365

3 A. A. Abla and M. T. Lawton Fig.. Management classifications in the treatment of complex ACA aneurysms with bypass. ECA = external carotid artery; ± = with or without. nial arteries (for example, STA) allows bypass flow from lateral to medial. Bypass Indications Bypass was performed when a normal parent or branch artery was deliberately occluded as part of aneurysm therapy and angiographic anatomy demonstrated inadequate collateral circulation. The ACoA often enabled safe occlusion of the A segment, making bypass for precommunicating aneurysms less common. However, an atretic or hypoplastic A segment on the contralateral side or a small ACoA indicated bypass. Distal ACA territories may be collateralized by leptomeningeal arteries from the MCA or posterior cerebral artery (PCA), but this is difficult to evaluate with preoperative balloon test occlusion or other radiographic imaging. Intraoperative test occlusion that elicits decreases in somatosensory or motor evoked potentials indicates a need for bypass, but this monitoring method is not specific enough to contraindicate bypass in patients who have no such neurophysiological changes. Surgical Technique Surgical exposure for bypass procedures was lateral (pterional craniotomy with or without orbitotomy and transsylvian approach), midline (bifrontal craniotomy and anterior interhemispheric approach), or combined (pterional plus bifrontal craniotomies, and transsylvian plus anterior interhemispheric approaches). Lateral approaches exposed precommunicating aneurysms and proximal afferent arteries to communicating aneurysms. Midline approaches exposed postcommunicating aneurysms and distal efferent arteries from communicating aneurysms. Combined approaches were used with communicating aneurysms when full exposure could not be gained with one craniotomy. The orbital-pterional craniotomy was the standard exposure used for aneurysms, without zygoma resection. The bifrontal approach was typically eccentric to the right side to avoid bridging veins on the dominant hemisphere and crossed the superior sagittal sinus to gain full access to the midline. If the bypass was at or distal to the genu of corpus callosum, the patient s head was turned laterally 90 (midline horizontal) with the head in slight extension and the neck angled upward 45 with respect to the floor. This position allows gravity to retract the dependent right hemisphere and widen the interhemispheric fissure. 4 If the bypass was proximal to the genu, the head was in the neutral position (nose up). Combined approaches were performed as 2 separate craniotomies with a thin strip of bone in between the two, rather than one large craniotomy. The side of the approach was determined by the side of dominant A supply, and the bifrontal craniotomy was eccentric to the ipsilateral side. The head was positioned with of contralateral rotation to access the sylvian fissure with additional contralateral table rotation, and the interhemispheric fissure with ipsilateral table rotation (nose up). The pterional scalp incision was extended past midline for this combined approach. Bypass was performed with end-to-side, side-to-side, or end-to-end anastomoses depending on the reconstructive technique (in situ, reimplantation, reanastomosis, or interpositional bypass). Heparin was not administered systemically and was used only as an irrigant locally during the anastomosis. The surgical field was evacuated with constant microsuction. Continuous suture technique was preferred because it required tying only 4 knots and 366 J Neurosurg / Volume 20 / June 204

4 Anterior cerebral artery bypasses for complex aneurysms saved time. Reanastomosis was ideal when there was only one efferent artery and the ends were sufficiently slack to reapproximate without undue tension. In situ bypass requires some ischemia time in the adjacent artery, some risk to an otherwise uninvolved artery, and a more challenging interluminal suture line, but the A 2 A 4 segments course in parallel naturally. Interpositional bypass requires harvesting a radial artery graft (RAG) and multiple anastomoses. After the bypass was completed, patency was confirmed with Doppler ultrasonography as well as with indocyanine green videoangiography. The patient was then placed in electroencephalography burst suppression with propofol or barbiturates during clamp time, and changes in neurophysiological monitoring were addressed with increases in systolic blood pressure until the changes reversed. After bypass, the aneurysm was occluded intraoperatively with distal clip occlusion, proximal clip occlusion, or both (complete trapping). Proximal clip occlusion resulted in flow reversal in the aneurysm. In some cases, trapping was deliberately incomplete to allow residual filling of branch arteries like the recurrent artery of Heubner. Aneurysms that were trapped completely were opened, thrombectomized, and debulked. In some cases, aneurysm occlusion was performed endovascularly as a second stage days later, either by direct coiling of the aneurysm or by parent artery sacrifice. In all cases, postoperative angiography was used to assess bypass patency and aneurysm occlusion. All bypass patients were started on a regimen of aspirin therapy postoperatively and continued indefinitely. Literature Search An extensive PubMed search identified 736 reports of ACA bypass. Review of these articles and their citations identified 29 relevant articles. This literature was reviewed to summarize the various bypass options for ACA aneurysms. Cases of bypass to the cortical surface or superficial ACA vessels were excluded. Results Experience With ACA Bypass Ten patients had aneurysms that were treated with ACA bypass as part of their surgical intervention (Table ). There were 7 women and 3 men, with a mean age of 56 years (range 8 86 years). Four patients presented with or had an earlier subarachnoid hemorrhage including patient with a dissecting proximal right A pseudoaneurysm (Fig. 2). Three patients with giant aneurysms presented with mass effect symptoms (hydrocephalus in 2 patients and seizures in patient). One patient s bacterial endocarditis was complicated by a mycotic aneurysm, and patient s large tuberculum sella meningioma resection was complicated by an arterial injury and iatrogenic pseudoaneurysm of the distal left A (Fig. 3). One patient had an incidentally discovered aneurysm. There were 2 precommunicating aneurysms (A ), 5 communicating aneurysms (ACoA), and 3 postcommunicating aneurysms (A 2 A 3 ). Three of these were saccular, J Neurosurg / Volume 20 / June were fusiform/dolichoectatic, and 3 were pseudoaneurysms (dissecting, infectious, and iatrogenic). In situ bypasses were used in 4 patients (A 3 -A 3 bypass), interposition bypasses in 4 patients, reimplantation in patient (pericallosal artery onto callosomarginal artery), and reanastomosis in patient (pericallosal artery) (Table 2). Interpositional bypasses included 2 with double reimplantations: one shunting flow from the right pericallosal to left pericallosal and callosomarginal arteries, and the other one shunting flow from proximal A 2 ACA to ipsilateral pericallosal and callosomarginal arteries. The other 2 interpositional bypasses shunted flow from the MCA (anterior temporal artery branch) to either the distal A segment or proximal A 2 segment (lateral to medial). Aneurysm occlusion was performed intraoperatively after bypass by proximal occlusion (with flow reversal) in patient, distal occlusion in 2 patients, and trapping in 5 patients. Trapping was complete in 3 patients with aneurysm excision in one of these patients. Aneurysm trapping was deliberately incomplete in 2 patients with giant aneurysms to preserve flow to the recurrent artery of Heubner, as seen in Case 7 and Case 0 (Fig. 4). Aneurysm occlusion was performed endovascularly in 2 patients (coiling in patient and parent artery sacrifice in patient). Complete aneurysm obliteration was demonstrated in 8 patients, despite proximal occlusion, distal occlusion, or incomplete trapping in 5 patients, due to flow alterations and aneurysm thrombosis after bypass. Small residual aneurysm filling was observed in the 2 remaining patients, one with distal occlusion and one with endovascular coiling. Bypass patency was demonstrated postoperatively in 8 patients. One bypass thrombosed, but 4 years later. One patient with an occluded bypass had a pseudoaneurysm in the field of a gunshot wound. A significant amount of abnormal artery was resected to reach normal artery for reanastomosis, and, consequently, the ends of the arteries were under tension. An allograft saphenous vein rather than an autologous vein was used in the other patient with an occluded bypass, and these grafts have a lower associated patency rate. Another patient s bypass occluded 4 years later. The median preoperative mrs score was 2 (range 0 4). There were no operative deaths, and permanent neurological morbidity was observed in 2 patients. At last follow-up, good outcomes (mrs score 2) were observed in 6 patients, and 8 patients (80%) were improved or unchanged. Literature Review of ACA Bypasses Review of the 29 relevant reports describing bypasses to the ACA territory included a wide variety of EC-IC bypasses and IC-IC using one of the 4 reconstructive techniques (Table 3). 3,5 23,26,27,29 33 The A 3 -A 3 in situ bypass was used most commonly (Table 4). Reanastomosis and reimplantation were used the least, probably due to the difficulty in reapproximating arterial ends without tension or in mobilizing recipient arteries to adjacent donor arteries. Although we did not use extracranial donor arteries (STA and MCA) in our patients, EC-IC interpo- 367

5 A. A. Abla and M. T. Lawton TABLE : Patient and aneurysm treatment characteristics at the University of California, San Francisco* Case No. Age (yrs), Sex SAH Aneurysm Location Morphology, Size Bypass Bypass Flow Direction Cranial Approach IC-IC Bypass Technique Aneurysm Occlusion Presentation Preop mrs Score Last Outcome (Score) Angiography Outcome precommunicating 8 75, F yes A dissection,.3 mm ATA-SVG-A lat to medial 9 6, F no A pseudoaneurysm (iatrogenic during tumor resection), 2.5 mm orbitopte - rional interposition (SVG) trapping (complete) A 3 -A 3 rt to lt combined in situ trapping (complete) communicating 78, F no ACoA F/D, 25 mm A 3 -A 3 rt to lt BAIH in situ endovascular (proximal sacrifice) 2 48, F yes ACoA saccular, 0 mm A 3 -A 3 lt to rt BAIH in situ endovascular (coiling) 6 57, F yes ACoA saccular, 5 mm ATA-SVG-A 2 lat to medial 7 47, F no ACoA F/D, thrombotic, 43 mm 0 86, F no A -A 2 junction F/D & saccular, thrombotic, 52 mm A 2 -RAG-PcaA+ CmaA postcommunicating 3 24, M no A 2 -A 3 F/D, 27 mm A 2 -RAG-PcaA+ CmaA 4 8, M yes A 3 pseudoaneurysm, thrombotic, 2 mm 5 62, M no A 2 -A 3 saccular, thrombotic, 0 mm orbitopterional interposition (SVG) distal occlusion rt to lt combined interposition w/ double reimplantation (RAG) trapping (incomplete) A 3 -A 3 rt to lt combined in situ trapping (incomplete) A 3 segment excision & end-to-end reanastomosis ant to pst BAIH interposition w/ double reimplantation (RAG) proximal occlusion ant to pst BAIH reanastomosis trapping (complete) CmaA-PcaA ant to pst BAIH reimplantation distal occlusion SAH 4 same (4) patent bypass, obliteration of aneurysm lt visual deficit from tumor, iatrogenic pseudoaneurysm at tumor resection aphasia, headache, hydrocephalus SAH 7 yrs prior & recurrence after clipping/wrapping previous SAH/coiling w/ coil compaction on follow-up angiogram 2 same (2) patent bypass, obliteration of aneurysm 2 same (2) patent bypass, obliteration of aneurysm 0 same (0) occluded bypass (at 4 yrs), small neck remnant 0 worse (3) occluded by- pass, small residual seizures 2 same (2) patent bypass, obliteration of aneurysm hydrocephalus, mental status decline 2 same (2) patent bypass, obliteration of aneurysm endocarditis 0 same (0) patent bypass, obliteration of aneurysm SAH from traumatic aneurysm after gunshot wound yr prior incidental (hearing loss) 4 same (4) occluded bypass, obliteration of aneurysm worse (4) patent bypass, obliteration of aneurysm * ant = anterior; ATA = anterior temporal artery; BAIH = bifrontal anterior interhemispheric; CmaA = callosomarginal artery; F/D = fusiform/dolichoectactic; lt to rt = anastomosis between left and right hemispheres; PcaA = pericallosal artery; pst = posterior; rt to lt = anastomosis between right and left hemispheres; RAG = radial artery graft; SAH = subarachnoid hemorrhage; SVG = saphenous vein graft. Vessels on either side of the plus sign were both recipients. 368 J Neurosurg / Volume 20 / June 204

6 Anterior cerebral artery bypasses for complex aneurysms Fig. 2. Case 8. A 75-year-old woman presented with subarachnoid hemorrhage and a good neurological grade initially but declined precipitously to mrs Score 4 with concern for rerupture. Serial angiograms failed to show a source of the hemorrhage but the proximal ACA (A) showed evolving pathological findings suspicious for a pseudoaneurysm, thought to be the source of the hemorrhage (A, right carotid artery angiogram, anteroposterior view). Intraoperative inspection confirmed a dissecting pseudoaneurysm involving most of the A segment (B) with intraluminal dissection and thrombus. The pathological A segment was trapped, and a bypass was performed using an SVG from the MCA (anterior temporal artery) to the distal A segment. With temporary clips in place, the distal suture line is demonstrated between the saphenous vein and distal A in an end-to-end fashion (C). The distal end of the bypass can be seen just proximal to the anterior communicating artery complex with a clip on the proximal A segment (D). An RAG was not available due to severe peripheral vascular atherosclerosis. The patient s follow-up angiogram showed a patent graft that perfused her anterior communicating artery complex and her ACA territories bilaterally (E, right carotid angiogram, anteroposterior view). The patient s neurological status steadily improved to presenting baseline. sitional bypasses were the second most common type of bypass to the ACA. We favored intracranial donor arteries (MCA or ACA), which shortened the interposition graft length and kept much of the reconstruction within the interhemispheric fissure with ACA donor sites. Discussion An Algorithm for ACA Bypass? Our experience with 0 patients demonstrated that ACA aneurysms requiring bypass are rare and are performed in the minority of ACA aneurysm surgeries. One of our objectives was to develop an algorithm for managing patients who require ACA bypass, and instead we found no clear patterns or simplifications. Some aneurysms have one bypass that fits all aneurysms and makes the management strategy straightforward, like the cervical carotid artery to-mca bypass for cavernous internal carotid artery (ICA) aneurysms. Some aneurysms are so limited in their bypass options that management strategy is also straightforward, like the STA-PCA bypass for a J Neurosurg / Volume 20 / June 204 P2 PCA aneurysm. In contrast, ACA aneurysms can be revascularized in a variety of ways and the management strategy must be individualized. We examined aneurysm location (precommunicating, communicating, and postcommunicating), cranial approach (transsylvian, interhemispheric, and combined), bypass technique (EC-IC, in situ, reanastomosis, reimplantation, and interposition), bypass flow (lateral-to-medial, left-to-right, or anteriorto-posterior), and aneurysm occlusion (proximal, distal, trap, or endovascular), and none of these analyses yielded meaningful algorithms. This failure may reflect the small size of the patient series, which is an inherent limitation of this study. We conclude that ACA aneurysms, more than any others, require a thorough survey of patient-specific anatomy and microsurgical options before deciding on an overall strategy. At the present time, endovascular sacrifice is the mainstay of endovascular treatment for these complex aneurysms; in the future, flow diversion may be another viable adjunct, when devices of the appropriate diameter for the ACAs are available. Aneurysm location was perhaps the most helpful guiding feature. Precommunicating ACA aneurysms can 369

7 A. A. Abla and M. T. Lawton Fig. 3. Case 9. A 6-year-old woman with progressive visual loss in the left eye underwent elective surgery for resection of a large anterior cranial fossa meningioma (A, axial T-weighted MR image with gadolinium). The patient s resection at an outside institution was complicated by significant bleeding from a distal A injury. A cottonoid was placed over the bleeding site and the surgery was aborted. Cerebral angiography demonstrated a pseudoaneurysm of the distal A under the cottonoid, as well as an incidental anterior choroidal artery aneurysm (B, left carotid artery injection, anterior oblique view). The patient underwent a combined left orbitozygomatic and bifrontal interhemispheric approach, and the aneurysm was identified under the cottonoid (C). Through the interhemispheric fissure exposure, an A3-A3 side-to-side bypass was performed. After completion of the back wall of the anastomosis with continuous 0-0 suture (D), the front wall was sewn continuously to complete the bypass (E). The pseudoaneurysm of the distal A was trapped (F), and the bypass was patent on postoperative angiography (G, right carotid artery angiogram, anteroposterior view, arrow) with filling of both distal ACA vessels. There was no residual filling of the left A pseudoaneurysm. be exposed completely with an orbital-pterional craniotomy and transsylvian approach. Aneurysms located proximally on the A segment may provide more normal artery distally for the recipient anastomosis, but our precommunicating aneurysms were more distal. Both extended to the A-A2 junction, one requiring temporary clipping of the ACoA complex while suturing the distal anastomosis of an MCA-SVG-A ACA bypass and the other one re- quiring A3-A3 bypass. Precommunicating aneurysms are not as likely as other ACA aneurysms to require a bypass because the contralateral A segment and ACoA provide collateral blood flow across the midline to the ipsilateral A2 segment. Bypass is only indicated in the absence of these elements of the circle of Willis. Postcommunicating aneurysms can also be exposed completely in one surgical corridor. The interhemispheric TABLE 2: Bypass types performed in the University of California, San Francisco experience Bypass Type in situ IC-IC interposition IC bypass graft IC bypass graft graft w/ double reimplantation graft w/ double reimplantation reanastomosis reimplantation No. of Patients Bypass* Bypass Flow Direction Graft Flow Approach Anastomoses low BAIH or combined side-to-side end-to-side, end-to-end end-to-side, end-to-side end-to-side, end-to-side, end-to-side end-to-side, side-to-side, end-to-side end-to-end end-to-side 4 A3-A3 rt to lt MCA (ATA)-A MCA (ATA)-A 2 A3-PcaA+CmaA lat to medial lat to medial ant to pst SVG SVG RAG high high high orbito-pterional orbito-pterional BAIH A 2-PcaA+CmaA rt to lt RAG high combined 3 A3 CmaA-PcaA ant to pst ant to pst low low BAIH BAIH Technique * Recorded as donor-to-recipient. Vessels on either side of the plus sign were both recipients. 370 J Neurosurg / Volume 20 / June 204

8 Anterior cerebral artery bypasses for complex aneurysms Fig. 4. Case 0. An 86-year-old woman presenting with progressive cognitive decline over 4 months was found to have hydrocephalus and a giant, partially thrombosed ACA aneurysm of the right A-A 2 junction with a calcified wall (A, CT angiogram, coronal view). The patient was otherwise healthy without comorbid medical conditions, was felt to have a life expectancy greater than 0 years based on demonstrated longevity in her family, and was active at her baseline functional status prior to her cognitive decline. Both observation and surgical treatment were presented to the family as appropriate courses of action, and they elected surgical treatment. Preoperative angiography demonstrated a robust jet of inflow from the right A and the outline of the aneurysm from the A 2 splayed over the dome (B, right carotid artery injection, anterior oblique view). There was no filling of the aneurysm from the left ICA injection. A combined right orbitozygomatic and bifrontal craniotomy were performed through one incision. An A3-A3 bypass was performed in case direct clip reconstruction was not possible (C). Intraluminally, the deep portion of the side-to-side anastomosis was sewn in continuous fashion, and the completed anastomosis was patent on the intraoperative indocyanine green angiogram (D). The fusiform morphology of the neck of the aneurysm was visualized at the termination of the A segment. A clip was placed proximal to the aneurysm on the distal A and distal to the aneurysm on the proximal A 2, allowing the ACoA to fill the recurrent artery of Heubner from the contralateral (left) side (E). The postoperative angiogram showed no filling of the aneurysm from the right, a trickle of flow to the aneurysm on late-phase angiography from the left (F, left carotid artery angiogram, anteroposterior view), and a patent bypass filling of the right A 2 segment anterograde and retrograde. approach exposes afferent and efferent arteries as well as aneurysms, which creates options for IC-IC reconstruction. Our 3 postcommunicating aneurysms were revascularized with reanastomosis, reimplantation, and double reimplantation techniques with anterior-to-posterior bypass flow. All 3 patients were positioned with the midline horizontally to allow gravity retraction to widen the interhemispheric fissure. More proximal postcommunicating aneurysms might not allow for gravity retraction, but the exposure still permits flexibility in designing IC-IC reconstructions. Communicating aneurysms are the most common and most difficult ACA aneurysms because they require a combined craniotomy that exposes both subfrontal and interhemispheric corridors. The interhemispheric exposure is needed for the bypass and distal aneurysm occlusion, and the subfrontal exposure is needed for aneurysm dissection and proximal occlusion. The A3-A3 bypass provides an elegant source of left-to-right bypass flow and is indicated when the aneurysm can be occluded while preserving antegrade flow in one of the A2 ACA efferj Neurosurg / Volume 20 / June 204 ents. Three of 5 patients with communicating aneurysms underwent revascularization with this reconstruction. Furthermore, staged endovascular aneurysm occlusion simplified the surgical exposure by reducing it to only a bifrontal-interhemispheric approach in 2 patients. A more complex bypass is needed when A2 segment outflow cannot be preserved or when 3 or more A2 segments originate from the aneurysm, as in one of our patients treated with the double reimplantation technique. The combined craniotomy is an invasive procedure with significant dissection, but we have found that 2 separate craniotomies reduce its impact. The Gamut of ACA Bypasses Most striking in our review of the literature, and different from our ACA bypass experience, was the frequency of EC-IC bypasses2,5,7, 6,8,9,27 (3 cases). The STA was long and large enough to directly revascularize the A segment6 or frontopolar artery,8 but its lateral location necessitated interposition grafts to reach the ACA in the midline. 37

9 A. A. Abla and M. T. Lawton TABLE 3: Listing of previous ACA bypasses from the literature review* Authors & Year Senior Author Aneurysm Location, Type Description of Bypasses (no. of cases) Bypass Technique Previously Reported Interposition Grafts Technique No. of Anastomoses per Bypass EC-IC or IC-IC Craniotomy precommunicating Kazumata et al., 20 Hauck & Samson, 2009 Kashimura et al., 2006 lt A, saccular M 2 -RAG-A STA-frontopolar (all in patient) in situ no, not STA to frontopolar Samson A, fusiform A -SVG-A () excision, interposition communicating Chen et al., 202 Spetzler ACoA or A 2 A 3 -A 3 (2) A 2 FP-A 2 () A, fusiform STA-A () EC-IC direct no, unique no end-to-end Dengler et al., 203 Vajkoczy ACoA STA-RAG [Y-shaped]- A 3 +A 3 () Park et al., 202 A -A 2, fusiform or saccular Jain et al., 202 ACoA-A 2, saccular Mirzadeh et al., 20 Lawton ACoA, fusiform & thrombotic Kim et al., 2006 ACoA, giant, thrombosed, saccular Quiñones-Hinojosa & Lawton, 2005 Lawton lt A -A 2 (ACoA), saccular ACoA, saccular Inoue et al., 2005 ACoA, giant thrombosed saccular in situ yes no, unique RAG end-to-side 3 mixed pterional no, unique SVG end-to-end 2 IC-IC pterional no side-to-side (A 3 -A 3 ) end-to-side (FP-A 2 ) IC-IC IC-IC interposition no, unique RAG end-to-side 4 EC-IC IC-IC STA-STA-ACA (2) interposition yes STA end-to-end, end-to-side ECA thoracodorsal axis forearm vein ACA territory () Azygos ACA bypass: A 2 -RAG-CmaA+PcaA () A 3 -A 3 +STA-RAG-A 3 () interposition no, unique thoracodorsal axis, forearm vein graft interposition w/ double reimplantation end-to-side, end-to-end, end-to-side (2) no, unique RAG end-to-side side-to-side end-to-side in situ + EC-IC yes RAG side-to-side end-to-side, end-toend 2 3 if double barrel EC-IC BAIH 4 EC-IC BAIH BAIH orbitopterional BAIH+ pterional 3 IC-IC BAIH+ orbitopterional 3 mixed BAIH (remote pterional approach) A 3 -A 3 (2) in situ yes no side-to-side IC-IC BAIH A 3 -A 3 +STA-RAG-A 3 () in situ + EC-IC no, unique RAG side-to-side end-to-side, end-toend 3 mixed BAIH Brilstra et al., 2002 ACoA (3) ECA-ACA (ELANA) (2) EC-IC direct no, unique SVG NR NR EC-IC NR (continued) 372 J Neurosurg / Volume 20 / June 204

10 Anterior cerebral artery bypasses for complex aneurysms TABLE 3: Listing of previous ACA bypasses from the literature review* (continued) Authors & Year Senior Author Aneurysm Location, Type Description of Bypasses (no. of cases) Bypass Technique Previously Reported Interposition Grafts Technique No. of Anastomoses per Bypass EC-IC or IC-IC Craniotomy communicating (continued) Mabuchi et al., 995 A -A 2 A 3 -A 3 (4) in situ no, unique no side-to-side IC-IC bicoronal incision frontal craniotomy Yokoh et al., 986 Ausman A -A 2, fusiform A -A 2 () A 2 -A 2 () orbitofrontal-a () postcommunicating Moon et al., 202 A 2 -A 3, fusiform giant Matsushima et al., 20 A 2 -A 3, giant fusiform thrombosed reimplantation no, unique no end-to-end end-to-side end-side IC-IC bifrontal bifrontal pterional A 3 -A 3 () in situ yes no end-to-side IC-IC BAIH proximal PcaA-CmaA w/o distal PcaA revascularization () in situ no no end-to-end IC-IC BAIH Dunn et al., 20 Ogilvy distal ACA, fusiform A 3 -A 3 (end-to-side) () in situ no, unique no end-to-side IC-IC BAIH no STA end-to-end 2 IC-IC BAIH Gelfenbeyn et al., 2009 Sekhar A 2 -A 3, fusiform thrombosed Ferroli et al., 2008 A 2, outflow vessel exits dome Lawton & Quiñones- Hinojosa, 2006 A 2 -PcaA+CmaA [common origin] () A 4 -A 4 w/ self-closing U-clips () Lawton A 2 -A 3 ACA (AIFA)-RAG-ACA (CmaA reimplant onto RAG) () excision, double barrel reanastomosis, interposition in situ no, unique no side-to-side IC-IC BAIH double reimplantation interposition no, unique RAG end-to-side 3 IC-IC BAIH Ewald et al., 2000 PcaA, fusiform giant CCA-SVG-PcaA () EC-IC direct no, unique SVG end-to-side 2 EC-IC BAIH Anson et al., 996 Spetzler lt A 2, F/D A 2 -A 2 () in situ yes no side-to-side IC-IC BAIH Lawton et al., 996 Spetzler ACA A 2 -A 2 (3) in situ yes no side-to-side IC-IC BAIH Smith & Parent, 982 A 3, fusiform A 3 -A 3 () reanastomosis no, unique no end-to-end IC-IC BAIH miscellaneous or mixed Mura et al., 203 Mura NA (for meningioma) A 2 -STA [Y-shaped]- PcaA+PcaA () Kawashima et al., 200 NA (moyamoya) STA-ACA (cortical) loose stitch method (7) interposition no, unique STA end-to-end 3 IC-IC BAIH+lt frontal EC-IC direct yes, by Iwama et al., 997/998 no end-to-side EC-IC dual craniotomy to expose ACA & MCA (continued) J Neurosurg / Volume 20 / June

11 A. A. Abla and M. T. Lawton TABLE 3: Listing of previous ACA bypasses from the literature review* (continued) EC-IC or IC-IC Craniotomy No. of Anastomoses per Bypass Interposition Grafts Technique Previously Reported Bypass Technique Description of Bypasses (no. of cases) Aneurysm Location, Type Senior Author Authors & Year IC-IC BAIH or orbitopterional 2 MCA-ACA for in situ 3 for double reimplantation SVG, RAG end-to-side (except ACA-ACA in situ) yes, previously by same group in situ interposition interposition double reimplant miscellaneous or mixed (continued) Sanai et al., 2009 Lawton various ACA-ACA (2) MCA (ATA)-ACA () ACA-ACA interposition double () Terasaka et al., 997 ischemic disease A 2 -STA-A 3 () IC interposition no, unique STA end-to-end 2 IC-IC BAIH Iwata et al., 988 ischemic disease STA-STA-ACA cortical EC-IC direct no, unique STA end-to-side 2 EC-IC NR vessel () * AIFA = anterior inferior frontal artery; CCA = common carotid artery; ECA = external CA; FP = frontopolar artery; NA = not applicable; NR = not reported. Vessels on either side of the plus sign were both recipients. A cervical carotid artery (external carotid artery or common carotid artery) also served as a donor artery. 2,7,5 Interposition grafts included the STA, 4,27 saphenous vein, 2,7 forearm vein, 5 radial artery,,9 and radial artery fashioned as a Y-shaped, dual efferent graft. 5 Saphenous vein grafts permit the use of the excimer laser-assisted nonocclusive anastomosis (ELANA) for ACA bypass. 2 Intracranial-to-intracranial reconstruction was reported in 24 cases in the literature, with the in situ bypass the most common (3 cases) (Table 4). The ACA joined to its contralateral ACA with a side-to-side anastomosis, whether at the rostrum, genu, or body, was the most widely used ACA bypass revascularizing the distal ACA territory with left-to-right flow. 3,6,8,20,22,25 Reanastomosis was the least common IC-IC reconstructive technique, 23,3 which may reflect the difficulty in bringing together ends of artery that have little redundancy and can be difficult to reapproximate after aneurysm excision. Reimplantation is a versatile technique, particularly when efferent arteries parallel uninvolved arteries on the contralateral side and might serve as donors (left-to-right bypass flow). 33 Pericallosal and callosomarginal arteries often run near each other, allowing one to be mobilized off an aneurysm and reimplanted on the other, as in our case of pericallosal artery onto callosomarginal artery reimplantion. Orbitofrontal and frontopolar arteries have both been reimplanted as bypass conduits to A and A 2 segments, respectively 3,33 (anterior-to-posterior bypass flow). The use of interpositional grafts in IC-IC reconstructions further expands the gamut of ACA bypasses. Simple jump grafts span gaps created by aneurysm excision 0,8,33 and double-barrel jump grafts reconstruct the bifurcation of A 2 segment into pericallosal and callosomarginal arteries (anterior-to-posterior bypass flow). 9 Bifurcation of the STA into frontal and parietal branches has been used as an interpositional graft in this location. 26 Jump grafts also donate flow from the MCA territory (M 2 segment or anterior temporal artery, lateral-to-medial bypass flow). 8 We reported the azygos bypass that uses a graft to build an azygos circulation from one A 2 segment in the interhemispheric fissure, with a RAG from one side donating flow to the pericallosal and callosomarginal arteries on the other side (left-to-right bypass flow). 24 For all the variety and creativity reported in these ACA bypasses, we envision others that have yet to be performed. The CmaA-CmaA bypass is analogous to the A 3 -A 3 bypass and joins the callosomarginal arteries together above the cingulate gyrus with a side-to-side anastomosis. Another possibility is a combined A 3 -A 3 bypass and CmaA-CmaA bypass as an alternative to the azygos bypass, sparing the patient the harvest of an interpositional RAG. Technical Considerations Our experience with ACA bypass demonstrates our strong preference for IC-IC reconstruction. Arterial reconstruction involves intracranial arteries that are already in the surgical field and do not require harvesting. When interposition grafts are needed, IC-IC grafts are shorter than EC-IC grafts and may have better patency in the long term. Radial artery grafts are always long enough for IC-IC bypass, and we resorted to SVG only when patients 374 J Neurosurg / Volume 20 / June 204

12 Anterior cerebral artery bypasses for complex aneurysms TABLE 4: Summary of University of California, San Francisco and previously reported experiences* Bypass Type University of California, San Francisco No. of Cases Literature st Author (alternatively senior author) Year No. of Cases IC-IC in situ A 3 -A 3 4 A 3 -A 3 Mabuchi Ogilvy 6 Moon Spetzler A 2 -A 2 A 4 -A 4 Spetzler,20 Ferroli IC-IC reanastomosis PcaA (end to-end) A 3 (end-to-end) PcaA-CmaA Smith Matsushima IC-IC reimplantation PcaA-CmaA A -A 2 A 2 -A 2 OrbFrA-A FrPolA-A 2 IC-IC interposition graft ATA-A 2 ATA-A PcaA-PcaA/CmaA(azygos bypass) A 2 -STA-A 3 A -SVG-A A 2 -PcaA+CmaA double barrel Yokoh Yokoh Yokoh Spetzler 3 Teraska Samson 0 Sekhar ACA-PcaA/CmaA M 2 -RAG-A A 2 -STA [Y-shaped]-PcaA+PcaA EC-IC 0 STA-STA-ACA Kazumata Mura Iwata Park CCA-SVG-PcaA ECA-SVG-ACA (ELANA) STA-RAG-A 3 Ewald Brilstra Inoue Kim STA-A STA-FrPolA ECA-thoracodorsal-ACA STA-RAG [Y-shaped]-A 3 +A 3 Kashimura Kazumata Jain Vajkoczy total 0 37 * FrPolA = frontopolar artery; OrbFrA = orbitofrontal artery. Listed as donor-to-recipient. Vessels on either side of the plus sign were both recipients. J Neurosurg / Volume 20 / June 204 had an incompetent palmar arch that contraindicated radial artery harvest. Intracranial grafts are also less likely to be twisted, kinked, or compressed. The A 3 -A 3 bypass is an in situ bypass that requires sewing the deep suture line intraluminally between the two arterial walls of the superficial suture line. This is a more challenging anastomosis that requires a reversal stitch as the first and last bites, first passing the needle from the extraluminal side where the knot is tied to the intraluminal side where the suture is run, and then passing the needle from the intraluminal side to the extraluminal side to tie the next knot. In addition, one must minimize handling of the luminal surfaces and monitor the extraneous arterial walls. Interestingly, intraluminal suturing was used in 8 of 0 patients to reimplant arteries or sew the deep suture line of a distal A anastomosis. Therefore, ACA bypasses require a little extra technical expertise, but IC-IC reconstructions are an elegant technique for complex ACA aneurysms. The central question regarding ACA bypass is whether it is better to treat a complex ACA aneurysm indirectly with bypass and occlusion or directly with clip reconstruction. Complex ACA aneurysms can be especially challenging to clip for many reasons: a large or giant size can adhere the A 2 ACA efferents to the aneurysm wall; intraluminal thrombus might require opening the 375

13 A. A. Abla and M. T. Lawton aneurysm, removing organized thrombus, and endarterectomizing the neck; incomplete proximal and distal control might result in back bleeding into the surgical field; atherosclerosis and calcification may prevent the clips from closing the neck; ACoA perforators or recurrent arteries of Heubner may be difficult to protect in the reconstruction; patients may not tolerate prolonged temporary occlusion times; and thrombotic emboli or luminal narrowing after clip reconstruction may cause perioperative strokes. Committing to clip reconstruction by opening an aneurysm is hazardous, the decision is irrevocable, and the outcome is uncertain. One might end up with a gaping hole in the aneurysm, a failed reconstruction, ongoing cerebral ischemia with intraoperative neurophysiological changes, and no contingency plan. In contrast, a bypass strategy is more predictable, less stressful, and as effective. Ischemia times are limited to the time needed to perform the bypass, and typically just one efferent artery is temporarily occluded rather than all afferents and efferents around the aneurysm complex. Aneurysm occlusion can be accomplished with trapping or even just proximal or distal clipping, allowing the reduction or redirection of flow to thrombose the aneurysm lumen. Incomplete trapping is particularly important with communicating aneurysms because perfusion of ACoA perforators and the recurrent artery of Heubner must be maintained. Implementing a bypass strategy does not preclude an attempt at direct clipping. With a bypass in place, thrombectomy/clip reconstruction may be better tolerated, and if these maneuvers fail, the aneurysm can be trapped with the patient already protected against ischemic complications. Conclusions Anterior cerebral artery aneurysms requiring bypass are rare and can be revascularized in a variety of ways. These aneurysms, more than any other aneurysms, require a thorough survey of patient-specific anatomy and microsurgical options before deciding on an individualized management strategy. Our experience demonstrates a preference for the more technically demanding IC-IC reconstruction, but EC-IC bypasses are reported frequently in the literature. We conclude that ACA bypass with indirect aneurysm occlusion is a good alternative to direct clip reconstruction for complex ACA aneurysms. Bypass techniques to the ACA territory will continue to evolve and improve as long as we maintain our collective proficiency and creativity. Disclosure The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Author contributions to the study and manuscript preparation include the following. Conception and design: both authors. Acquisition of data: both authors. Analysis and interpretation of data: both authors. Drafting the article: both authors. Critically revising the article: both authors. Reviewed submitted version of manuscript: both authors. Approved the final version of the manuscript on behalf of both authors: Lawton. Statistical analysis: both authors. Administrative/technical/material support: both authors. Study supervision: both authors. References. Anson JA, Lawton MT, Spetzler RF: Characteristics and surgical treatment of dolichoectatic and fusiform aneurysms. J Neurosurg 84:85 93, Brilstra EH, Rinkel GJE, Klijn CJM, van der Zwan A, Algra A, Lo RTH, et al: Excimer laser-assisted bypass in aneurysm treatment: short-term outcomes. J Neurosurg 97: , Chen PR, Abla AA, McDougall CG, Spetzler RF, Albuquerque FC: Surgical techniques for unclippable fusiform A2-anterior cerebral artery aneurysms and description of a frontopolarto-a2 bypass. 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