J Neurosurg Pediatrics 11:533–542, 2013 ©AANS, 2013 Pediatric bypasses for aneurysms and skull base tumors: short- and long-term outcomes Clinical article Louis J. Kim, M.D., Farzana Tariq, M.D., and Laligam N. Sekhar, M.D. Department of Neurological Surgery, University of Washington, Seattle, Washington Object. Cerebral bypass is a useful microsurgical technique for the treatment of unclippable aneurysms and in­ vasive skull base tumors. The authors present the largest reported series of cerebrovascular bypasses in the pediatric population. They describe the short- and long-term clinical and radiographic outcomes of extracranial-intracranial and local bypasses performed for complex cerebral aneurysms and recurrent, invasive, and malignant skull base tumors in pediatric patients. Methods. A consecutive series of 17 pediatric patients who underwent revascularization were analyzed retro­ spectively for indications, graft patency, and neurological outcomes. Results. The mean age was 12 years (median 11 years, range 4–17 years), and there were 7 boys (41%) and 10 girls (59%). A total of 18 bypasses were performed in 17 patients and included 10 aneurysm cases (55.5%) and 8 tu­ mor cases (45%). Of these 18 bypasses, there were 11 (61.1%) extracranial-intracranial bypasses (10 saphenous vein grafts [90%] and 1 radial artery graft [10%]), 1 side-to-side anastomosis (5.5%), 2 intracranial reimplants (11.1%), and 4 interposition bypass grafts (22.2%; 2 radial artery grafts, 1 saphenous vein graft, and 1 lingual artery graft). The mean clinical follow-up was 40.5 months (median 24 months, range 3–197 months). The mean radiographic followup was 40 months (median 15 months, range 9–197 months). Eighty-two percent of patients (14 of 17) achieved a modified Rankin Scale score between 0 and 2; however, 2 patients died of disease progression during long-term follow-up. The short-term (0- to 3-month) graft patency rate was 100%. Two patients had graft stenosis (11.7%) and underwent graft revisions. Two patients (11.1%) with giant middle cerebral artery aneurysms (> 25 mm) had strokes postoperatively but recovered without a persistent neurological deficit. One patient observed for 197 months showed a stable dysplastic change at the end of the graft. The long-term graft patency was 100% with a mean follow-up of 40 months. There were 2 deaths in the cohort during follow-up; both patients died of malignant tumors (osteogenic sarcoma and chondrosarcoma). Conclusions. The authors conclude that in properly selected cases, bypasses can be safely performed in patients with aneurysms and skull base tumors. The bypasses remained patent over long periods of time despite the growth of the patients. (http://thejns.org/doi/abs/10.3171/2013.1.PEDS12444) Key Words • extracranial-intracranial cerebral bypass • pediatric neurosurgery • skull base tumor • outcome C erebral bypass is a useful microsurgical tech­ nique in the treatment of complex intracranial an­eu­r­­ysms2,4,5,13,19–21,23,27,29,31,33,38,40,41,43–46 and skull base tumors.1,24,26,27,34,39,42 In well-selected patients, this Abbreviations used in this paper: ACoA = anterior communicat­ ing artery; BA = basilar artery; CTA = CT angiography; DSA = digital subtraction angiography; EC-IC = extracranial-intracranial; ICA = internal carotid artery; MCA = middle cerebral artery; mRS = modified Rankin Scale; NF = neurofibromatosis; PCA = posterior cerebral artery; RAG = radial artery graft; STA = superficial tempo­ ral artery; SVG = saphenous vein graft. J Neurosurg: Pediatrics / Volume 11 / May 2013 • complex aneurysm • vascular disorders technique has been successfully used to provide alterna­ tive blood flow after carotid artery sacrifice,39 to preserve flow after small vessel sacrifice, and to provide collateral flow prior to arterial trapping.23 Various microsurgical series have shown good long-term outcomes and paten­ cy rates in adult patients.2,19,23,30,31,38,45 However, in pedi­ atric patients, there are limited data available to validate the use of high- and low-flow bypasses in complex aneu­ This article contains some figures that are displayed in color on­line but in black-and-white in the print edition. 533 L. J. Kim, F. Tariq, and L. N. Sekhar rysms and skull base tumors.3,7,9,11,12,15,16,18,22,25,28,32,33,36,37,47 In particular, the long-term durability of these pediat­ ric grafts as these patients mature into adolescence and adulthood is not well described in the literature beyond case reports and small case series. We analyzed a co­ hort of 17 children in whom different types of bypass procedures were performed. Perioperative, short-term, and long-term clinical and radiographic outcomes were analyzed. Study Design Methods All pediatric patients (defined as 0–17 years of age) who underwent bypass procedures for aneurysms and tu­ mors were identified from an institutional review board– approved retrospective cerebrovascular registry. Infor­ mation regarding clinical presentation and the patient’s neurological status was obtained from patient records or telephone interviews. All patients with unclippable an­ eurysms and invasive tumors with vascular encasement underwent DSA. When the lesion involved the ICA, ip­ silateral angiography with common carotid compression was performed and the collateral vessels were evalu­ ated by injecting the contralateral ICA and 1 vertebral artery.21,30,31,38 Preoperatively, graft caliber was measured using duplex ultrasonography.23,38 Postoperative graft patency was determined by CTA, catheter angiography, and duplex ultrasonography. Digital subtraction angiography or CTA was performed immedi­ ately postoperatively, at 6 months, and at 18 months. Pa­ tients with tumors underwent MRI follow-up at 6 months, 1 year, and then every 2 years to evaluate for recurrence. All patients underwent CTA at the 2-year postoperative period. Further angiographic follow-up after the 2-year point was less frequent and regular. Information gathered from angiograms included the caliber of the proximal and distal anastomosis, caliber of the graft (graft patency), ex­ tent of the collateral circulation, and any other abnormali­ ties such as formation of a new aneurysm. Information about surgical and endovascular repair and pathology re­ ports of the graft tissues were reviewed in cases in which graft repair was done. Any observed narrowing of ≥ 50% was considered stenosis. The mRS was used to evaluate the clinical outcomes, and scores were assigned to the physical examination reports or telephone interviews by the research fellow (F.T.). Indication for Bypass Indications for bypass for aneurysms included giant aneurysms (≥ 25 mm) with complex anatomy, presence of calcification or thrombosis or perforator or branch vessels arising from the neck or sac of the aneurysm, ruptured aneurysms with unfavorable geometric dimensions for simple coiling (broad neck, dome-to-neck ratio < 1.5) or clip reconstruction, fusiform morphology, or the presence of isolated circulation with planned parent vessel occlu­ sion. The main indications for performing bypass pro­ cedures for tumors were carotid encasement or invasion with recurrent, malignant tumor and/or poor collateral flow. 534 Preoperative Evaluation The first step after the decision to perform a bypass is to examine the donor as well as the recipient vessel. Do­ nor vessels, for example, eternal or internal carotid arter­ ies, were evaluated by angiography. Next was the choice of the graft material, which depends on the extent of col­ lateral flow, caliber of the recipient vessel, and availabil­ ity of the graft material. If the vessel sacrificed was of a small caliber, a local bypass (side-to-side anastomosis, in­ terposition grafts, and reimplantation) was the preferred choice. The donor grafts included the STA, the lingual artery, and the occipital artery in most cases. If a highflow bypass was deemed necessary, the graft chosen was an RAG or the SVG depending on the availability of the graft vessel. In children younger than 12 years, in whom the RAG was small in diameter, the SVG was the only alternative. Graft vessel diameters were evaluated using duplex ultrasonography; an RAG > 2 mm and an SVG ≥ 2.5 mm were the preferred choices.9,10 When an RAG was considered, an Allen test was performed using Doppler monitoring of the palmar arch to see if it could be safely removed. Age was not an absolute limiting factor consid­ ered for RAG extraction as long as the donor RAG was ≥ 2 mm. In 1 case, an RAG was extracted from a 4-year-old girl and successfully repaired by saphenous vein interpo­ sition bypass graft. Similarly, recipient vessels ≥ 2 mm were considered suitable for high-flow bypass. In cases of in situ or side-to-side anastomosis, we select vessels with diameters ≥ 1 mm as a suitable recipient.23,29,31 Graft Preparation The RAG was exposed from the wrist back to the brachial artery bifurcation, along with its accompanying veins. After extraction, the graft was flushed with hepa­ rinized saline, and terminal ends were devoided of the veins and adventitia. The graft was expanded using the pressure distension technique.23,38 In this technique, an oblique arterial cut is fashioned along the distal end of the graft, and a fish mouth technique is used to slightly enlarge the graft tip.23,38 Preoperative duplex ultrasonography and marking are used to map the saphenous vein in the leg.23,38 After extraction, it is flushed through with heparinized saline and distended at slight pressure to release the spasm of the vessel. The flow direction in the vein is verified before anastomosis by flushing the graft with heparinized saline and confirming free flow of fluid from the other end.38 We do not perform valvotomies prior to use. Anesthesia and Neuromonitoring All patients were placed on an aspirin regimen (1–10 mg/kg/day). In 2 cases, clopidogrel was administered in dosage of 2–5 mg/kg/day immediately postoperatively due to mild or moderate graft stenosis identified angio­ graphically. During the anastomosis procedure, all pa­ tients were placed in burst suppression with propofol, and intraoperative monitoring (somatosensory evoked potentials, motor evoked potential, and electroencepha­ lography) was routinely performed. Intraoperative hepa­ rin was routinely administered as a bolus. Typical anti­ J Neurosurg: Pediatrics / Volume 11 / May 2013 Pediatric bypasses for aneurysms and skull base tumors coagulation regimens included a loading dose of 75–100 U/kg followed by a maintenance dose of 28 U/kg/hr for children younger than 1 year and 20 U/kg/hr for children older than 1 year (based on decreased normal infant anti­ thrombin levels. The dose in older children, 18 U/kg/hr, is similar to that in adults.23,29–31,33,38 High-Flow Bypass Technique There was no difference in the microsurgical tech­ nique of pediatric bypasses compared with the procedures in adults.23,29,31 In the anterior circulation the M2 segment and in the posterior circulation the P2 segment were the vessels of choice at the recipient end of the bypass as both are typically devoid of perforators. However, in the case of an SVG, a branch point is selected if possible to fa­ cilitate vessel size match. The superior cerebellar artery may be used as a recipient in case of a hypoplastic PCA. In all cases of high-flow bypass, the distal anastomosis was performed first followed by proximal anastomosis using 9-0 or 8-0 nylon for extracranial sutures. A small rubber dam measuring 0.5 × 1 cm was placed under the recipient vessel to isolate it, and the recipient vessel was covered with papaverine-soaked Gelfoam (Pfizer Inc.) to relax vasospasm of the vessel. Temporary clips were ap­ plied on the recipient artery, and Spetzler microsuction (NMT Medical, Inc.) was placed in the vicinity of the anastomosis to aspirate CSF on a continuous basis, and an end-to-side anastomosis was performed at the distal end. The proximal anastomosis was performed in an endto-side fashion when the external carotid artery was the donor vessel, or in an end-to-end fashion, when the ICA was the donor vessel. Low-Flow Bypass Technique Low-flow and local bypasses included the STA-MCA bypass, A3-A3 side-to-side anastomosis, M3 reimplanta­ tion, and an RAG or lingual artery interposition graft be­ tween 2 cerebral arteries; 10-0 or 9-0 nylon was used for the anastomosis. After the anastomosis was completed, the flow in the graft was checked using a Doppler flow probe (Mizuho micro Doppler, Mizuho America, Inc.) and indocyanine green angiography.23,30,31,38 Results A total of 18 bypasses were performed in 17 patients who ranged in age between 4 and 17 years (mean 12 years). Patient ages are shown in Table 1. There were 7 boys and 10 girls. There were 10 aneurysms (3 ruptured and 7 un­ ruptured) and 8 tumors (5 malignant [2 osteosarcomas, 2 chondrosarcomas, and 1 giant cell tumor] and 3 benign [1 recurrent meningioma and 2 recurrent chordomas]). The treated cohort included 6 MCA, 1 PCA, 1 ACoA, and 2 basilar artery aneurysms. There were 3 small aneurysms (3.7, 4, and 6.2 mm) and 7 large aneurysms (mean 24.2 mm, range 14–44 mm). A total of 10 bypasses were per­ formed in patients with aneurysms including 4 end-toside (4 SVGs), 1 side-to-side, 2 intracranial reimplants, and 3 interposition bypass grafts (2 RAGs and 1 lingual artery graft) (Table 1). J Neurosurg: Pediatrics / Volume 11 / May 2013 TABLE 1: Patient demographics and indications for bypass Parameter age mean/median/range spread (yrs)   4–6   7–9   10–12   13–15   16–17 no. of male/female patients no. of tumors osteosarcoma chondrosarcoma meningioma (NF2) chordoma giant cell no. of aneurysms ruptured   MCA   PCA unruptured    MCA (1 new aneurysm)   ACoA (NF1)   BA no. of aneurysms treated (mm) small (0–6) medium (7–14) large (19–24) giant (>25) mean/median/range size of aneurysms no. of bypasses EC-IC local   interposition   side-to-side   reimplantation no. of grafts used SVG RAG lingual artery Value* 12/11/4–17 yrs 2 2 5 6 2 7/10 8 (47.1) 2 2 1 2 1 10 (52.9) 3 2 1 3 1 2 3 2 1 4 20.22/20/3.7–44 mm 18 11 (61.1) 7 (38.8) 5 1 1 11 3 1 * Values are the number of cases (%) unless noted otherwise. In the aneurysm group, there was complete occlusion of the aneurysm in 9 (90%) of 10 cases. One 6-year-old girl with a giant fusiform aneurysm involving the verte­ bral and basilar arteries (2 previous coiling procedures failed) underwent saphenous vein grafting from the V2 segment of the vertebral artery to the right PCA, followed by proximal occlusion of the aneurysm. The postoperative angiogram showed a residual aneurysm that was treated with endovascular coil embolization with complete oblit­ 535 L. J. Kim, F. Tariq, and L. N. Sekhar eration of the aneurysm. One patient (Case 3) had forma­ tion of a new aneurysm distal to the graft (RAG) at 6 months postoperatively that was treated by microsurgical resection of the aneurysm and revision using a lingual artery interposition graft.7,37 Another patient presented with regrowth of a residual aneurysm at 8 months and was treated by endovascular embolization.7,14 Subsequent 6-month follow-up angiography confirmed persistent ob­ literation. There were 8 skull base tumors, including 2 chondro­ sarcomas, 2 chordomas, 1 giant cell tumor, 2 osteogenic sarcomas, and 1 meningioma. Seven EC-IC bypasses (6 SVGs and 1 RAG) and 1 SVG interposition bypass were performed (Tables 1 and 2). Gross-total resection was achieved in 7 of 8 cases. The patient who underwent sub­ total resection demonstrated a small residual tumor in the cavernous sinus that required postoperative radiotherapy.32 Donor and Recipient Vessel Diameters Vessel diameters were measured via preoperative im­ aging studies (DSA, CTA, or vascular ultrasonography). The average high-flow bypass donor vessel diameter mea­ sured 5.4 mm (range 3.6–5.7 mm). High-flow bypass re­ cipient vessel diameters measured an average of 3.2 mm (range 2.6–4.0 mm). The average vessel diameter for in situ or side-to-side bypasses measured 1.5 mm (range 1.2–2.2 mm). Theses values reflect very similar donor and recipient artery diameters to those reported for cere­ bral bypasses in the adult population.23,29,31 Clinical and Radiographic Outcome and Complications Of the initial 17 bypasses performed, 16 patients (94.4%) achieved an mRS score less than 2 at short-term (0–3 months) follow-up. One patient with NF2 had a pre­ operative mRS score of 5, and this patient was discharged to a skilled nursing care facility. Two patients with giant MCA aneurysms suffered from postoperative ischemic strokes. One patient had a small MCA territory stroke, leading to mild dysarthria that resolved completely on follow-up. The other patient suffered from a frontopari­ etal stroke with left arm and leg weakness on discharge, which recovered completely without any residual deficit at the 6-week follow-up. There were 2 cases of mild graft stenosis, but no graft occlusions were encountered. The short-term graft patency was 100%. One of the graft ste­ noses was detected on intraoperative Doppler flow scan­ ning and was repaired by resection and reanastomosis, but mild stenosis was noted again on postoperative CTA as well as on follow-up CTA at 1 year. The second pa­ tient developed a focal stenosis in the RAG performed for MCA aneurysm; this patient developed a new aneurysm distal to the graft site involving the recipient artery at the 6-month follow-up. The graft was resected along with the aneurysm and was replaced by lingual artery graft. One patient suffered a vocal cord injury due to intubation, which subsequently recovered. On long-term clinical follow-up (mean 40.5 months, median 24 months, range 3–197 months), 12 (70.5%) of 17 patients had an outcome mRS score of 0–2. One patient with a WHO Grade I meningioma required lifetime de­ 536 pendent care (a patient with NF2). Two patients died of dis­ ease progression within 2 years postoperatively; one had chondrosarcoma and the other had osteogenic sarcoma. On long-term radiographic follow-up (mean 40 months, me­ dian 15 months, range 9–197 months), the graft patency rate was 100%. There was formation of one new aneurysm distal to the high-flow graft (RAG), and one residual an­ eurysm had a rapid recurrence (within 6 months) and was treated by endovascular embolization.5,19,31,44 Case 1 Illustrative Cases This 10-year-old boy with a history of acute lympho­ cytic leukemia and past cranial irradiation presented with an osteogenic sarcoma of the sphenoclival region. This extended into the right maxilla and skull base area and involved the right ICA in the petrocavernous segments (Fig. 1A). Surgery was performed to achieve a gross-total resection of the tumor in 3 steps. The first step was cere­ bral angiography, a right carotid cross-compression study (Fig. 1B and C), and embolization. Following this, a by­ pass was performed using an SVG from the right cervical ICA to the supraclinoid ICA (Fig. 1D). This was followed by bifrontal craniotomy and biorbital osteotomy, right optic nerve decompression, resection of the sphenoclival cavernous sinus tumor extradurally including the cavern­ ous ICA, and a transfacial degloving approach from be­ low to resect the tumor (Fig. 1E). At the 6-year follow-up the patient is doing well at school with an mRS of 0, and the bypass is widely patent (Fig. 1F). Case 2 This 13-year-old boy had an incidental discovery of a giant calcified, left MCA aneurysm, 3 cm in size, on MRI performed after a minor head injury (Fig. 2A). Cerebral angiography revealed a giant aneurysm that occupied the entire distal M1 segment and the M1-M2 junction, which arose just distal to the lenticulostriate branches (Fig. 2B). A small inferior M2 branch arose from the lower aspect of the aneurysm and came around it, and there were 3 perforating vessels arising from the upper aspect of the aneurysm. Because of the complex anatomy of the an­ eurysm neck, the surgical plan was trapping and bypass. The patient underwent a left frontotemporal craniotomy, orbital osteotomy, and SVG bypass from the cervical ICA to the intracranial M2 segment, trapping and excision of the aneurysm, and reconstruction of the trifurcation of the MCA by endarterectomy and suturing. Postoperative­ ly, the patient suffered from a left MCA territory stroke (Fig. 2C), with mild dysarthria that resolved completely on the follow-up images. The postoperative angiogram revealed occlusion of the aneurysm, a patent bypass graft (Fig. 2D), and filling of the MCA territory through the SVG (Fig. 2E). Follow-up CTA was performed at 4 years and showed a patent bypass graft (Fig. 2F). The patient had no neurological deficit, and he had an mRS score of 0. Case 3 This 13-year-old boy presented with a history of J Neurosurg: Pediatrics / Volume 11 / May 2013 Pediatric bypasses for aneurysms and skull base tumors Fig. 1. Case 1. A: Magnetic resonance image obtained in a 10-year-old boy with a history of acute lymphocytic leukemia and cranial radiation, who presented with sphenoclival osteogenic sarcoma with involvement of the right ICA. B: Preoperative angiogram with left ICA injection showing cross-filling after compressing the right common carotid artery, but poor flow. C: Angiogram showing slow venous filling. D: The patient underwent a right temporal craniotomy, biorbital osteotomy, and optic nerve decompression. The postoperative angiogram shows an SVG bypass from the cervical ICA to the supraclinoid ICA. E: Postoperative MR image obtained after the second-stage surgery, showing a complete tumor resection. The patient had an mRS score of 0 at the 3-month follow-up. F: Follow-up MR angiogram obtained at 6 years, showing a patent bypass graft. severe headaches for 1 month. Workup revealed a large fusiform aneurysm arising from the anterior parietal branch of the right MCA (Fig. 3A). The patient under­ went a frontotemporal craniotomy, resection of the aneu­ rysm, and placement of a radial artery M3-M3 interposi­ tion bypass graft (Fig. 3B). The postoperative angiogram showed complete exclusion of the aneurysm and a mild focal stenosis of the graft at the proximal anastomosis site (Fig. 3C). Postoperatively, the patient exhibited moderate left-sided weakness, facial droop, and dysarthria from a stroke in the MCA distribution (Fig. 3D). He was dis­ charged to inpatient rehabilitation and ultimately recov­ ered completely. At 4 months, the patient presented with headache recurrence. He underwent cerebral angiography that showed formation of a new aneurysm distal to the RAG (Fig. 3E).22 The patient underwent additional sur­ gery, and the aneurysm was resected along with the graft and was replaced by a lingual artery graft (Fig. 3F). The patient did well, and a follow-up angiogram at obtained at 32 months showed a patent bypass graft and no new aneurysm formation (Fig. 3G and H). Case 4 This 15-year-old girl presented with progressive neu­rological decline, with stupor and quadriparesis. The workup revealed a giant fusiform aneurysm of the BA (Fig. 4A). She underwent aneurysm excision along with saphenous vein grafting from the cervical ICA to the J Neurosurg: Pediatrics / Volume 11 / May 2013 BA under deep hypothermic circulatory arrest. Postop­ eratively, her condition gradually improved to an mRS score of 1 at the 3-month follow-up. Her postoperative angiogram revealed complete exclusion of the aneurysm from the circulation and a patent bypass (Fig. 4B). Her last follow-up occurred after 16 years. She had completed a master’s degree and was working full time. She had an mRS socre of 1, reflecting unilateral hearing loss but no other deficits. Her MR angiography study showed no an­ eurysm and a patent SVG graft with mild dilation noted at the distal end that remains unchanged for the last several years (Fig. 4C). This patient was previously reported on in a case report with short-term follow-up.44 Discussion The use of cerebral bypass for treatment of unclippa­ ble intracranial aneurysms and complex skull base tumors is a well-known technique.1,2,4–21,23,41,42 While a tremen­ dous amount of data is available for moyamoya disease in children, the long-term viability of surgically created bypass grafts in the non-moyamoya pediatric population is only evident anecdotally. Bypass for flow preservation has not been well studied in the pediatric neurosurgery literature, except for in case reports and scattered cases embedded within larger adult patient series. Overall in the literature, a total of 33 cases of pedi­ atric bypasses have been reported.3,7,9,11,14–16,18,22,25,28,32,33,47 537 L. J. Kim, F. Tariq, and L. N. Sekhar Fig. 2. Case 2. A: Magnetic resonance image obtained in a 13-year-old boy, showing a giant, calcified thrombosed MCA aneurysm. B: Preoperative angiogram showing perforator branches arising from the aneurysm. C: Postoperative MR image showing a left MCA territory infarct. D: Postoperative angiogram showing an SVG bypass from the cervical ICA to the intracranial M2-MCA. E: Postoperative angiogram showing the MCA branches being filled up by the graft. F: Follow-up CT angiogram obtained at 4 years, showing a patent graft. Twenty-two cases3,7,14,15,22,33 had no clear reported radio­ graphic follow-up. Of the remaining 11 cases,7,14,28,32,33,47 the mean radiographic follow-up is 49 months, with a range of 5–155 months. In comparison, our series contrib­ utes 17 additional patients with follow-up ranging from 6 months to more than 16 years and a mean of 38.6 months. Hence, this single series represents the largest follow-up reported in the literature, permitting us to make some ob­ servations about long-term findings in this rare subgroup. We report these data in an attempt to analyze these long-term outcomes. The obvious concern in young pa­ tients is the durability of a bypass graft as the child ma­ tures into adulthood. Questions exist regarding procedur­ al complication rates, graft durability over many years, the fate of grafts (particularly EC-IC bypasses during pu­ bertal growth), and whether collateral flow develops over time that obviates the need for the bypass. Our data indicate that the durability of pediatric by­ pass grafts is excellent. The patency rate of pediatric by­ passes for aneurysm or tumor was high, with 100% of the grafts patent postoperatively (Table 2). During follow-up, 2 of 18 bypasses developed stenosis within 1 year of ini­ tial treatment. One of these required intraoperative revi­ sion but no further therapy, and the other was treated suc­ cessfully with antiplatelet therapy. However, no other case developed flow limitations or graft occlusions in a followup period averaging nearly 3.5 years and extending up to 16.4 years (Fig. 4). The delayed development of signifi­ cant collateral flow was not observed angiographically 538 during this extended follow-up in any case. In our series, 2 patients (11%) suffered a perioperative stroke, both of whom recovered completely in the follow-up period. A comparison of these results with other series in the adult bypass literature where perioperative stroke and graft oc­ clusion rates ranged from 4% to 14% and 5% to 13%, re­ spectively,17,31,33 indicates that the technical feasibility of pediatric bypasses is equal to or higher than adult coun­ terparts despite the smaller anatomical size of donor and recipient arteries. Because these bypasses preserve and maintain normal flow, they are vital to proper cerebral hemodynamics, and collateral channel formation appears to be unnecessary. Unlike revascularization bypasses for moyamoya disease or ischemia, successful preservation of flow does not appear to trigger growth factors for col­ lateral flow development. Hence, these grafts do not pro­ gressively attenuate or occlude over time, a phenomenon that can be seen in adult bypasses that “temporize” isch­ emia until collaterals develop. This leads to several observations: 1) These conduits were imperative for not merely proper short-term but also long-term blood flow to the bypassed vascular terri­ tory. 2) The pediatric cerebral vasculature may be more adaptable to bypass grafts given the low rate of periop­ erative complications and the high rate of graft patency during follow-up compared with adult bypasses. 3) The high long-term patency in this pediatric cohort illustrates that graft stenosis from intimal hyperplasia or hemody­ namic shear stress appears to be an early (within 1 year J Neurosurg: Pediatrics / Volume 11 / May 2013 Pediatric bypasses for aneurysms and skull base tumors Fig. 3. Case 3. A: Three-dimensional angiogram showing a large saccular aneurysm arising from the anterior parietal branch of the MCA. B: Intraoperative drawing showing the RAG interposition graft. C: Postoperative angiogram showing occlusion of the aneurysm and RAG interposition bypass with proximal focal stenosis of the graft. D: Magnetic resonance FLAIR sequence showing an infarct. E: Follow-up angiogram obtained at 4 months, showing a new aneurysm distal to the anastomosis site. F: Intraoperative drawing showing resection of the aneurysm along with the graft and replacement by a lingual artery graft. G: Postoperative angiogram showing graft along with the aneurysm resected and replaced by lingual artery graft. H: Angiogram obtained at 32 months, showing a patent bypass and no aneurysm evidence. Panels B and F are printed with permission from Dr. Laligam N. Sekhar. postoperatively) phenomenon, and does not manifest in late follow-up. 4) Physical growth of pediatric patients with EC-IC bypasses occurs without long-term effect on the graft, which elongates proportionately. Although this is a small cohort, thereby making subgroup analy­ ses problematic, there do not appear to be any differences in bypass durability based on graft donor type or bypass technique, such as high flow, interposition, or other local types. These data are extremely reassuring given the lon­ gevity expected and required of these grafts. Of 14 EC-IC bypasses 8 were performed in children 13 years of age or younger, and the remainder were performed in patients older than 13 years. Zhang et al.47 reported 2 cases of pediatric EC-IC by­ passes for giant aneurysms; one of these patients was only 10 months old and the other was 23 months old. In their several-year follow-up, graft patency was angiographi­ cally documented in both cases. Our series provides ad­ ditional support to these authors’ astute observations that concerns about stretching or scarring down of the graft J Neurosurg: Pediatrics / Volume 11 / May 2013 during periods of childhood growth fortunately are un­ founded. Goedee et al.9 reported a single case of a gi­ ant MCA aneurysm treated with an STA-MCA bypass. Technical success was achieved; however, no long-term radiographic follow-up was reported. In our series, we did not use this technique because of to the diminutive size of STA in those patients who were considered. However, it is an identical technique to that used in moyamoya disease in children,10,35,36 which has a well-published record of du­ rability. In 6 cases, we performed an in situ bypass, con­ sisting of side-to-side, reimplantation, or intracranial-tointracranial interposition grafts. These types of bypasses have been reported primarily in adult patient series as be­ ing at lower risk for long-term occlusion.14 Based on our outcome data, we concur that pediatric patients tolerated these in situ–type bypasses quite well in the short and long term, with no technical complications or patency difficulties. Despite the dramatic differences in size compared with adults, these pediatric patients exhibited donor and 539 L. J. Kim, F. Tariq, and L. N. Sekhar TABLE 2: Outcome of bypasses* Parameter radiographic outcome overall short-term patency (0–3 mos) stenosis (non–flow limiting) mean/median/range long-term FU duration long-term graft patency aneurysm group complete occlusion new aneurysm formation aneurysm recurrence tumor group gross-total resection tumor recurrence clinical outcome overall mean/median/range FU duration mRS score‡ aneurysm group   0–2   3–4   5–6 tumor group   0–2   3–4   5–6 complications infection major stroke surgical morbidity graft stenosis Value† Comment 18 of 18 (100) 2 of 18 (11.1) 40/15/9–197 mos 16 of 16 (100) 1 graft was replaced; 1 patient did not undergo FU imaging 9 of 10 (90) 2 of 10 (20) 0 of 9 (0) 7 of 8 (87) 2 of 7 (28.5) 1 osteogenic sarcoma; 1 chondrosarcoma; 1 patient did not undergo FU imaging 40.5/24/3–197 mos 9 of 9 0 0 5 0 3 0 1 of 18 (5.5) 1 of 18 (5.5) 2 1 osteosarcoma; 1 chondrosarcoma; 1 giant cell tumor; 2 chordomas 1 osteosarcoma; 1 chondrosarcoma; 1 patient w/ NF2 discharged to skilled nursing facility anterior parietal branch of the MCA vocal chord injury requiring op 1 detected intraop; 1 detected postop * FU = follow-up. † Values are the number of cases (%) unless noted otherwise. ‡ Values represent the number of patients. recipient vessel diameters quite similar to those reported for bypass in adults.23,29,31 Because the scale of size was similar to adults, the microsurgical technique remained familiar to surgeons accustomed to adult anatomy. Given the reasonable long-term results in this series, we rec­ ommend careful preoperative donor/recipient vessel and anastomosis site selection that maintains a minimum diameter vessel size as discussed in Results. Based on our experience, as a guideline we recommend minimum RAG diameter ≥ 2 mm, SVG ≥ 2.5 mm, and in situ or side-to-side bypass vessels ≥ 1.0 mm. Certainly smaller vessels can be used, as has been reported by others;47 this is merely a guide. Hence, we prefer size-based selection of vessels for bypass suitability rather than using the age of patient. At our institution, we approach all complex vascular 540 and skull base lesions with a multimodality team approach. Hence, in addition to microsurgery, complex aneurysms are evaluated for possible endovascular therapy, and complex skull base tumors are considered for endoscopic and radio­ surgical treatment. The vascular cases presented in this se­ ries either predate modern neuroendovascular techniques or represent cases in which stent-assisted coiling or flow di­ version was not considered suitable by the treatment team. Undoubtedly, endovascular therapies have revolutionized the treatment of complex vascular disease. However, we believe that there exists a highly selected population of le­ sions that require cerebral bypass for definitive treatment. Although these technical skills are still widely present in neurosurgical centers worldwide, the diminishing indica­ tions for cerebrovascular bypass will make training future surgeons problematic. J Neurosurg: Pediatrics / Volume 11 / May 2013 Pediatric bypasses for aneurysms and skull base tumors Approved the final version of the manuscript on behalf of all authors: Kim. Administrative/technical/material support: Kim, Sekhar. Study supervision: Kim, Sekhar. References Fig. 4. Case 4. A: Preoperative angiograms obtained in a 15-yearold girl with a giant basilar artery aneurysm. B: Postoperative angiograms showing complete exclusion of the aneurysm from the circulation and a patent bypass graft. C: Magnetic resonance angiogram obtained at the 16.4-year follow-up, showing complete obliteration of the aneurysm and a patent bypass graft with a mild dilation before the anastomotic site in the SVG that has been unchanged for the last several years. Images in Panels A and B are reprinted with permission from Sekhar LN, Chandler JP, Alyono D: Saphenous vein graft reconstruction of an unclippable giant basilar artery aneurysm performed with the patient under deep hypothermic circulatory arrest: technical case report. Neurosurgery 42(3):667–673, 1998. Conclusions While our pediatric bypass experience was garnered over a long treatment period, it has provided us long-term follow-up that confirms extended bypass patency in pe­ diatric patients in complex aneurysms and tumors. 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Zhang YJ, Barrow DL, Day AL: Extracranial-intracranial vein graft bypass for giant intracranial aneurysm surgery for pedi­ atric patients: two technical case reports. Neurosurgery 50: 663–668, 2002 Manuscript submitted August 31, 2012. Accepted January 23, 2013. Please include this information when citing this paper: pub­ lished online March 1, 2013; DOI: 10.3171/2013.1.PEDS12444. Address correspondence to: Louis J. Kim, M.D., University of Washington, Box 359924, 325 Ninth Avenue, Seattle, Washington 98104. email: ljkim1@u.washington.edu. J Neurosurg: Pediatrics / Volume 11 / May 2013