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Double-Barrel Superficial Temporal Artery to Proximal Middle Cerebral Artery Bypass to Treat Complex Intracranial Aneurysms: A Reliable High Blood Flow Bypass
Original Article
Double-Barrel Superficial Temporal Artery to Proximal Middle Cerebral Artery Bypass to Treat Complex Intracranial Aneurysms: A Reliable High Blood Flow Bypass Peng Hu, Hong-Qi Zhang, Xiao-Yu Li, Xian-Zeng Tong
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BACKGROUND: The superficial temporal artery (STA) to proximal middle cerebral artery bypass has been reported before. However, the flow supply capacity of the doublebarrel STA to proximal MCA bypass in treating complex intracranial aneurysms has not been well documented.
bypass algorithm could be an alternative treatment for complex intracranial aneurysms.
METHODS: Consecutive cases using double-barrel STA to proximal MCA bypass to treat complex intracranial aneurysms during the past 5 years were collected. Somatosensory evoked potential monitoring and motor evoked potential monitoring were applied for each patient to identify any ischemic events during surgery. After bypass, the aneurysm was trapped, or the proximal parent artery was occluded. Digital subtraction angiography or computed tomography angiography was used to evaluate the patency of bypass postoperatively. Blood flow was measured by ultrasound before discharge.
INTRODUCTION
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RESULTS: Among 1561 patients treated for intracranial aneurysms in our institute, 6 were included for the current report. There were 2 dominant M2 fusiform aneurysms, 2 M1 fusiform aneurysms, 1 supraclinoid internal carotid artery fusiform aneurysm, and 1 M1 bifurcation giant aneurysm. All 6 cases were successfully treated using this technique. One patient had temporary numbness in the contralateral extremities, which was caused by perforator complications. The blood flow carried by the STA was 108e232 mL/minute.
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CONCLUSIONS: When anastomosed to proximal branches, a double-barrel STA to MCA bypass can reliably provide a high blood flow of >100 mL/minute. Combined with aneurysm trapping or parent artery occlusion, this
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Key words Bypass - Complex - Intracranial aneurysm - STA -
Abbreviations and Acronyms CT: Computed tomography DSA: Digital subtracted angiography ICA: Internal carotid artery MCA: Middle cerebral artery MEP: Motor evoked potential MRI: Magnetic resonance imaging
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T
he superficial temporal artery (STA) to cortical middle cerebral artery (MCA) bypass was pioneered by Yasargil in 1967 to treat MCA occlusion.1 Since then, STA to cortical MCA bypass has been widely applied to augment blood flow in cases with parent artery compromise during treatment of complex intracranial aneurysms.2-9 STA to cortical MCA bypass has been routinely performed as an adjuvant to treat complex aneurysms located at both anterior and posterior circulation.2,3,10 Most patients have reported a satisfactory outcome. However, some postoperative ischemic events have been observed, and these events are suspected to be due to insufficient blood flow supplied by the STA to cortical MCA bypass.5,11-15 Subsequently, graft interposition bypasses using radial artery or venous grafts have been developed to increase blood flow.16-19 Moreover, the concepts of a low-flow bypass (blood flow <50 mL/minute) and high-flow bypass (blood flow 50 mL/minute) have been established to classify the capacity of flow augmentation. Low-flow bypass includes pedicle grafts, such as STA and occipital artery pedicles. High-flow bypass includes a graft interposition bypass as a radial artery and autogenous vein grafts.19 However, it has been reported that pedicle grafts with STA may occasionally supply blood flow with a capacity of >100 mL/minute in clinical practice.7 Another type of STA to MCA bypass is used to target the recipient at the proximal MCA, such as segment M2 or M3; this type of bypass was first reported by Diaz et al. in 1985.20 The STA to proximal MCA bypass has been reported to be capable of providing more blood flow compared with a traditional STA to
SEP: Somatosensory evoked potential STA: Superficial temporal artery Department of Neurosurgery, Xuanwu Hospital, Capital Medical University, Beijing, China To whom correspondence should be addressed: Peng Hu, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.01.203 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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DOUBLE-BARREL STA TO PROXIMAL MCA BYPASS
cortical MCA bypass.4,20 However, its technical details and the capacity of blood flow supply have not been documented well yet. We report our initial experience in treating complex intracranial aneurysms with a double-barrel STA to proximal MCA bypass, which was qualitatively and quantitatively evaluated postoperatively.
scans were examined before discharge. Transcranial ultrasound was used to measure the blood flow of both donor vessels and recipients. DSA was performed to evaluate the patency of the bypass, which is the blood flow replacement for the target territory, and obliteration of the aneurysms. A scheduled follow-up by telephone or a clinic interview was proposed to each patient.
MATERIALS AND METHODS
RESULTS
This study was approved by the local university hospital ethics review board. Written consent was obtained from each patient. Patients with intracranial aneurysms were prospectively managed in our database. Electrophysiologic monitoring, including somatosensory evoked potential (SEP) monitoring and motor evoked potential (MEP) monitoring, was applied to detect ischemic events during intracranial aneurysm microsurgery over the past 5 years. Using this method, we could determine whether or not the bypass could supply enough blood flow after major vessel sacrifice in aneurysm surgery. We included consecutive intracranial aneurysms that were treated by the same senior physician (P.H.) using aneurysm trapping/proximal parent artery ligation and blood flow replacement with double-barrel STA to proximal MCA bypass in the anterior circulation. For terminal aneurysms that were considered unclippable, sacrifice of the parent artery in conjunction with blood flow replacement was anticipated. For internal carotid artery (ICA) aneurysms, a carotid compression test was performed during digital subtraction angiography (DSA). If the circle of Willis was present, a balloon test occlusion was subsequently performed. The size of STA for each patient was measured before operation.
Within the past 5 years, 1561 patients with intracranial aneurysms were treated microsurgically or endovascularly in our institute. Among 1561 patients, 6 had unruptured intracranial aneurysms and were included in the study. The selection process of these 6 patients is shown in Figure 1. Detailed information for these 6 patients is provided in Table 1. Specifically, 5 patients had a fusiform aneurysm, and 1 patient had a giant saccular aneurysm. Two of the fusiform aneurysms were located on the dominant M2 segment. Two of the fusiform aneurysms were located on the terminal M1 segment; 1 of these aneurysms was endovascularly coiled. Additionally, 1 fusiform aneurysm involved the whole supraclinoid ICA; this case has been reported elsewhere to illustrate our operative techniques.21 The last patient had a giant M1 aneurysm involving terminal bifurcation. One patient developed a small basal ganglion infarction on day 8 after the operation. The infarction resulted in numbness of the contralateral extremities with a modified Rankin Scale score of 1 that lasted for 1 week. Otherwise, the patients performed well with a modified Rankin Scale score of 0 up to their last follow-up. The blood flow carried by the STA was 108e232 mL/minute. MRI or CT perfusion was available for 5 patients. Two (patients 3 and 4) of these 5 patients showed slightly low perfusion and the other 3 patients (patient 1, 5, and 6) had roughly equal perfusion compared with the other side.
Surgical Techniques The surgical techniques have been previously reported in detail.21 In brief, after general anesthesia, SEP monitoring and MEP monitoring were begun. The main branches of the STA were dissected during craniotomy. In patients undergoing graft artery harvest, nimodipine saline (volume 1:5) irrigation was applied to prevent graft artery vasospasm. The craniotomy was performed based on a classic pterional approach.22 The sylvian fissure was extensively dissected. The inlet and outlet of the aneurysm were then determined. Next, the anticipated recipient arteries, such as M2 and M3, were sufficiently dissected. A tolerance test was performed under electrophysiologic monitoring.21 After validation of the recipient arteries, anastomosis was performed in an intermittent fashion. Indocyanine green angiography was employed to confirm the bypass patency. Subsequently, the aneurysm was trapped, or the proximal parent artery was clipped depending on whether there were side branches involved in the aneurysm or not. SEPs and MEPs were intermittently tested for 30 minutes before the wound closure. Postoperative Care Postoperatively, patients received intensive care. Fluid augmentation was given to each patient. A computed tomography (CT) scan was performed on the first day after the operation. If there was no intracranial hemorrhage, 100 mg aspirin was prescribed to patients daily. Patients were discharged 1 week after the operation if they had no complications. Magnetic resonance imaging (MRI)
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Illustrative Cases Case 1. A 53-year-old man presented with intermittent dizziness and a right dominant M2 fusiform aneurysm was diagnosed 1 week before admission (Figure 2). DSA demonstrated that the fusiform aneurysm had an irregular shape. Aneurysm wall enhancement was demonstrated on high-resolution MRI. The STA trunk was 2 mm, and the 2 branches of the STA were equally developed. These 2 branches were immediately anastomosed to the proximal MCAs after developing the aneurysm. The aneurysm was removed after confirmation of the patent anastomosis through indocyanine green angiography. MEPs and SEPs had no changes throughout the whole surgery. Postoperative DSA demonstrated the patency of the bypass and complete obliteration of the aneurysm. There was no evidence of ischemic lesions on MRI. Ultrasound showed blood flow was 232 mL/minute. Case 3. A 24-year-old man had a brain infarction 10 months before admission. He recovered well after conservative treatment. A fusiform aneurysm at the right M1 segment was found (Figure 3). Embolization of the aneurysm with stent placement was performed in another hospital. Angiography performed 6 months after the operation indicated regrowth of the aneurysm. Further intervention treatment failed owing to the difficulty of catheterization. He was then referred to our institute for further treatment. The right STA was measured 1.8 mm after his
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ORIGINAL ARTICLE PENG HU ET AL.
DOUBLE-BARREL STA TO PROXIMAL MCA BYPASS
Figure 1. Flow chart of patient selection. STA, superficial temporal artery; MCA, middle cerebral artery.
hospitalization. The equal-sized branches of the STA were anastomosed to the M3 branches of the right MCA. The stent was visible during the operation and was placed from M1 to the frontal M2 trunk. To prevent stent collapse and subsequent perforator occlusion, the aneurysm and parent artery were left intact. The second stage of endovascular M1 occlusion was planned before his
discharge. Postoperative CT and MRI showed neither intracranial hemorrhage nor a fresh ischemic lesion. Ultrasound demonstrated the patency of the bypass with a blood flow of 148 mL/minute. DSA was performed to occlude the parent artery. However, the parent artery occluded spontaneously on day 5 after operation (Figure 3). The patient was discharged on postoperative day 7. He
Table 1. Patient Characteristics AN
Result
Age Symptoms (years)/ (mRS Case Sex Location Morphology Score)
Treatment
Outcome (mRS Score)
AN
Flow Bypass (mL/minute)
Follow-Up (months)
Complications
1
53/M
M2
Fusiform
Dizziness (1) AN trapping þ bypass
Good (0)
Occluded Patent
232
18
No
2
60/F
M2
Fusiform
Headache (1) AN trapping þ bypass
Good (0)
Occluded Patent
—
17
No
3
26/F
M1
Fusiform
Headache (1) AN trapping þ bypass
Good (0)
Occluded Patent
108
12
No
4
60/F
M1
Giant saccular
Incidental (0) AN trapping þ bypass
Good (0)
Occluded Patent
210
10
No
5
24/M
M1
Fusiform
Ischemic (0)
Bypass
Symptomatic infarction, fully resolved (1)
Occluded Patent
148
15
No
6*
45/F
ICA C6y
Fusiform
Dizziness (1)
Proximal ICA occlusion þ bypass
Good (0)
Occluded Patent
146
10
No
AN, aneurysm; mRS, modified Rankin Scale; M, male; F, female; ICA, internal carotid artery. *This patient has been reported elsewhere to illustrate our microsurgical techniques. yC6 represents the supraclinoidal segment of ICA.
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Figure 2. Imaging studies of case 1. (A) Three-dimensional digital subtraction angiography shows a fusiform aneurysm on the dominant M2. (B) High-resolution magnetic resonance imaging demonstrates wall enhancement of the aneurysm (arrowhead). (C) Superficial temporal artery
experienced numbness in his left extremities on postoperative day 8. MRI demonstrated a small fresh infarction on the right internal capsule. The symptoms disappeared completely 1 week after conservative treatment.
is well developed. (D and E) Postoperative digital subtraction angiography shows full occlusion of the aneurysm and bypass patency. (F) Postoperative magnetic resonance imaging depicting no brain infarction.
demonstrated bypass patency. Ultrasound showed the bypass had a blood flow of 210 mL/minute.
DISCUSSION Case 5. In a 60-year-old woman, a left M1 terminal giant saccular aneurysm with a length of 3.7 cm was incidentally found on MRI (Figure 4). Preoperative angiography could not clearly show the position of the outlet owing to the significant stagnation. The STA was 2 mm with an underdeveloped frontal branch. The aneurysm was explored after craniotomy and extensive dissection of the sylvian fissure. The aneurysm had a broad base involving 2 branches of the M2. The parietal STA was anastomosed to the temporal M2 trunk, which was a dominant branch, whereas the smaller STA was anastomosed to the M3 branch of the frontal M2 trunk after its emergence from the operculum. The aneurysm was removed after confirmation of bypass patency and no changes in SEPs and MEPs during the operation. Postoperative MRI demonstrated there were no fresh brain infarctions 3 days after the operation. CT angiography
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An ideal treatment for intracranial aneurysms is to eliminate them from the cerebral circulation, which can usually be accomplished by direct neck clipping or endovascular coiling. However, both microsurgical clipping and endovascular coiling are challenging in complex aneurysms, including aneurysms that lack a neck, have significant neck calcification, are very large, were previously treated, or have special histology.23 Consequently, major vessels have to be sacrificed in such circumstances, and bypasses are needed to augment the blood flow, especially when the patients cannot tolerate the balloon test occlusion.9,10,18,24 The options for extracranial-intracranial artery anastomosis have been evolving since the first report by Yasagil et al.1 using Hunterian ligation and STA to cortical MCA bypass to treat 2 patients with intracranial aneurysms.1 In the decades since 1970, the most popular bypass involved 1 STA branch anastomosed to a cortical MCA
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Figure 3. Imaging studies of case 3. (A) A fusiform aneurysm on the M1 trunk is demonstrated on DSA image. (B) Thrombus (arrow) is shown on contrast-enhanced magnetic resonance imaging. (C) Embolization of the aneurysm is achieved with coils assisted by a stent. (D) Control angiography demonstrates aneurysm recurrence 7 months after
branch.2,3,5,6,12 Promising results have been reported by numerous centers.1-3,10 Thus, for unclippable aneurysms, clinicians initially preferred to perform a major vessel sacrifice and STA to cortical MCA bypass. However, there were also a few reports of patients who had ischemic complications after major vessel sacrifice even after STA to cortical MCA bypass was performed. Based on previous reports, most of which were successful treatments, Spetzler and Carter10 argued that the ischemic complications may have resulted from insufficient flow supplied by the anastomosis or due to clot propagation. The ischemic complications could be resolved by intravenous heparin administration and flow expansion. Subsequently, some clinicians switched to interposition graft bypasses, such as saphenous vein and radial artery bypasses.16,17,25 Initially, interposition grafts, such as radial artery and saphenous vein bypasses, had high operative morbidity and mortality owing to acute graft occlusion.16,17 After establishing a set of successful operative methods, the surgery results using interposition grafts have been significantly improved.17,25 It was reported that interposition anastomosis to M2 could supply a blood flow >100 mL/minute, which is known as a high-flow bypass.25 Therefore, the extracranial-intracranial bypasses have been divided into high-flow bypasses, such as an interposition graft bypass, and low-flow bypasses, such as a pedicle bypass using STA or occipital artery.18,25,26 The blood flow amounts used to define these 2 groups were controversial.7,18,19,25 Liu et al.18 reported that a low-flow bypass usually carries a flow of 15e25 mL/minute, whereas a high-flow bypass can provide a
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endovascular coiling. (E) Well-developed superficial temporal artery and its branches. (F and G) The aneurysm is fully occluded, and the bypass is patent. (H) Magnetic resonance imaging demonstrates a small fresh infarction at the right basal ganglion (arrowhead) on day 8 after surgery.
blood flow of 70e140 mL/minute.18 Ramanathan et al.19 divided low-flow bypass and high-flow bypass using blood flow supplied by an anastomosis of 50 mL/minute. Possibility of STA to MCA Bypass to Supply High Flow We reported our initial experience using a double-barrel STA to proximal MCA bypass and parent artery sacrifice to treat complex intracranial aneurysms. Among these 6 patients, only 1 patient had postoperative ischemic complications that were caused by clot formation and perforator occlusion. Postoperative ultrasound demonstrated that the blood flow using our method can be 108e 232 mL/minute, which was traditionally defined as a high-flow bypass. Amin-Hanjani et al.27 also reported their experience using STA to MCA bypass to treat intracranial aneurysms. They measured the bypass flow, which was 11e70 mL/minute, using intraoperative ultrasound. In their recent reports, they included 22 patients throughout a 10-year period in which they used STA to MCA bypass to treat intracranial complex aneurysms. Only 1 patient had symptoms related to flow insufficiency, which were confirmed to be due to bypass occlusion during the follow-up examinations. The bypass flow was measured at 42e170 mL/ minute, and the flow was kept steady during the follow-up examinations.7 However, the authors did not report the details of their technique, which could be STA to cortical MCA bypass or single STA to proximal MCA bypass. Our bypass flow was higher than previously reported results. This discrepancy could be due to 2 reasons. First, we used double-barrel anastomosis,
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Figure 4. Imaging studies of case 5. (A) Magnetic resonance imaging demonstrates a giant aneurysm. (B and C) Digital subtraction angiography shows a giant saccular aneurysm on the M1 bifurcation. The frontal superficial temporal artery branch is underdeveloped. (D and E)
and second, we chose M2 or M3 as the recipient. The artery blood flow is not markedly affected by the conduit lumen until lumen reduction is very pronounced.28 It was stressed that the flow that was produced was directly related to the cerebral perfusion pressure under such critical conditions.28 Moreover, it is well known that if an interposition graft, such as a radial artery or saphenous vein, was anastomosed with an STA trunk and M2 or M3, the bypass flow could be up to 100 mL/minute.29 It was reported that the whole MCA territory would be perfused if an M2 recipient was chosen. Although 60% of the MCA territory would be supplied by the bypass if a cortical artery was selected as a recipient, it would need several months to mature.4 Thus, it would be reasonable that our bypass flow was higher compared with the flow that was previously reported when we applied double-barrel anastomosis with an M2 or M3 segment. Additionally, our patient had no low flow-related ischemic events in the follow-up period. The flow was measured at 100e175 mL/minute in the ICA and 75e120 mL/minute in the MCA using ultrasound.28 Another study used MRI to quantify blood flow with an average of
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Postoperative computed tomography angiography shows the patency of the bypass. Arrows point to superficial temporal artery. (F) Postoperative magnetic resonance imaging demonstrates no brain infarction.
206 mL/minute in the ICA and 68e119 mL/minute in the MCA.30 Therefore, the rationale was that the bypass flow could be >100 mL/minute, which could reach the blood flow demand after a major vessel sacrifice. Although patients in this report were satisfied with the results, our study has some limitations. First, it was a small patient series with a selection bias. Second, the follow-up evaluation time was not long enough to evaluate the long-term prognosis. A larger number of patients and long-term follow-up are necessary to properly evaluate the effects of this treatment. CONCLUSIONS Our initial experience indicated that for the selected patients, double-barrel STA to MCA bypass could reliably provide blood flow of >100 mL/minute when anastomosed to M2 or M3 branches. When combined with aneurysm trapping or parent artery occlusion, this bypass algorithm could be an alternative treatment for complex intracranial aneurysms.
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REFERENCES 1. Yasargil MG, Krayenbuhl HA, Jacobson JH 2nd. Microneurosurgical arterial reconstruction. Surgery. 1970;67:221-233. 2. Spetzler RF, Schuster H, Roski RA. Elective extracranial-intracranial arterial bypass in the treatment of inoperable giant aneurysms of the internal carotid artery. J Neurosurg. 1980;53:22-27. 3. Peerless SJ, Ferguson GG, Drake CG. Extracranialintracranial (EC/IC) bypass in the treatment of giant intracranial aneurysms. Neurosurg Rev. 1982; 5:77-81. 4. Collice M, Arena O, Fontana RA. Superficial temporal artery to proximal middle cerebral artery anastomosis: clinical and angiographic long term results. Neurosurgery. 1986;19:992-997. 5. Kodama N, Suzuki J. Bypass surgery in the treatment of aneurysms. Neurosurg Rev. 1982;5:87-90. 6. Silvani V, Rainoldi F, Gaetani P, Bonezzi C, Rodriguez y Baena R. Combined STA/MCA arterial bypass and gradual internal carotid artery occlusion for treatment of intracavernous and giant carotid artery aneurysms. Acta Neurochir (Wien). 1985;78:142-147. 7. Rustemi O, Amin-Hanjani S, Shakur SF, Du X, Charbel FT. Donor selection in flow replacement bypass surgery for cerebral aneurysms: quantitative analysis of long-term native donor flow sufficiency. Neurosurgery. 2016;78:332-341 [discussion: 341-342]. 8. Amin-Hanjani S, Alaraj A, Charbel FT. Flow replacement bypass for aneurysms: decisionmaking using intraoperative blood flow measurements. Acta Neurochir (Wien). 2010;152: 1021-1032 [discussion: 1032]. 9. Lawton MT, Hamilton MG, Morcos JJ, Spetzler RF. Revascularization and aneurysm surgery: current techniques, indications, and outcome. Neurosurgery. 1996;38:83-92 [discussion: 92-94]. 10. Spetzler RF, Carter LP. Revascularization and aneurysm surgery: current status. Neurosurgery. 1985;16:111-116. 11. Hopkins LN, Grand W. Extracranial-intracranial arterial bypass in the treatment of aneurysms of the carotid and middle cerebral arteries. Neurosurgery. 1979;5:21-31.
DOUBLE-BARREL STA TO PROXIMAL MCA BYPASS
12. Grote E, Schonmayr R. Extracranial-intracranial bypass in giant aneurysms. Neurosurg Rev. 1982;5: 83-85.
measure in managing complex MCA and PICA aneurysms. Acta Neurochir (Wien). 2016;158: 1523-1531.
13. Olteanu-Nerbe V, Marguth F. Extracranial-intracranial bypass operation in basal tumours. Neurosurg Rev. 1982;5:99-105.
24. Sekhar LN, Natarajan SK, Ellenbogen RG, Ghodke B. Cerebral revascularization for ischemia, aneurysms, and cranial base tumors. Neurosurgery. 2008;62:1373-1408 [discussion: 14081410].
14. Diaz FG, Ausman JI, Pearce JE. Ischemic complications after combined internal carotid artery occlusion and extracranial-intracranial anastomosis. Neurosurgery. 1982;10:563-570. 15. Fox AJ, Vinuela F, Pelz DM, et al. Use of detachable balloons for proximal artery occlusion in the treatment of unclippable cerebral aneurysms. J Neurosurg. 1987;66:40-46. 16. Diaz FG, Pearce J, Ausman JI. Complications of cerebral revascularization with autogenous vein grafts. Neurosurgery. 1985;17:271-276. 17. Sekhar LN, Duff JM, Kalavakonda C, Olding M. Cerebral revascularization using radial artery grafts for the treatment of complex intracranial aneurysms: techniques and outcomes for 17 patients. Neurosurgery. 2001;49:646-658 [discussion: 658-659]. 18. Liu JK, Kan P, Karwande SV, Couldwell WT. Conduits for cerebrovascular bypass and lessons learned from the cardiovascular experience. Neurosurg Focus. 2003;14:e3.
25. Sekhar LN, Kalavakonda C. Saphenous vein and radial artery grafts in the management of skull base tumors and aneurysms. Oper Tech Neurosurg. 1999;2:129-141. 26. Cenzato M, Bortolotti C. The role of extra- and intracranial bypass in the treatment of complex aneurysms. J Neurosurg Sci. 2016;60:70-82. 27. Amin-Hanjani S, Shin JH, Zhao M, Du X, Charbel FT. Evaluation of extracranial-intracranial bypass using quantitative magnetic resonance angiography. J Neurosurg. 2007;106:291-298. 28. Nornes H, Wikeby P. Cerebral arterial blood flow and aneurysm surgery. Part 1: local arterial flow dynamics. J Neurosurg. 1977;47:810-818. 29. Alaraj A, Ashley WW Jr, Charbel FT, AminHanjani S. The superficial temporal artery trunk as a donor vessel in cerebral revascularization: benefits and pitfalls. Neurosurg Focus. 2008;24:E7.
19. Ramanathan D, Temkin N, Kim LJ, Ghodke B, Sekhar LN. Cerebral bypasses for complex aneurysms and tumors: long-term results and graft management strategies. Neurosurgery. 2012;70: 1442-1457 [discussion: 1457].
30. Brockmann C, Gerigk L, Vajkoczy P, Groden C, Neumaier-Probst E. Magnetic resonance imaging flow quantification of non-occlusive excimer laserassisted EC-IC high-flow bypass in the treatment of complex intracranial aneurysms. Clin Neuroradiol. 2012;22:39-45.
20. Diaz FG, Umansky F, Mehta B, et al. Cerebral revascularization to a main limb of the middle cerebral artery in the Sylvian fissure. An alternative approach to conventional anastomosis. J Neurosurg. 1985;63:21-29.
Conflict of interest statement: This work was supported by the National Natural Science Foundation of China (Grant No. 81500988) and National Key R&D Program of China (Grant No. 2016YFC1300800).
21. Hu P, Zhang HQ, Li XJ. Double-barrel STA to proximal MCA bypass and proximal parent artery occlusion for a fusiform superior clinoidal ICA aneurysm. Acta Neurochir. 2018;160:1939-1943. 22. Hu P, Liang J, Bao Y, Li M, Ling F. The pterional transsylvian transtentorial approach to ventrolateral pontine cavernomas: indications and techniques. World Neurosurg. 2014;82:1276-1282.
Received 14 November 2018; accepted 30 January 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.01.203 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
23. Esposito G, Fierstra J, Regli L. Distal outflow occlusion with bypass revascularization: last resort
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Double-Barrel Superficial Temporal Artery to Proximal Middle Cerebral Artery Bypass to Treat Complex Intracranial Aneurysms: A Reliable High Blood Flow Bypass Peng Hu, Hong-Qi Zhang, Xiao-Yu Li, Xian-Zeng Tong
-
BACKGROUND: The superficial temporal artery (STA) to proximal middle cerebral artery bypass has been reported before. However, the flow supply capacity of the doublebarrel STA to proximal MCA bypass in treating complex intracranial aneurysms has not been well documented.
bypass algorithm could be an alternative treatment for complex intracranial aneurysms.
METHODS: Consecutive cases using double-barrel STA to proximal MCA bypass to treat complex intracranial aneurysms during the past 5 years were collected. Somatosensory evoked potential monitoring and motor evoked potential monitoring were applied for each patient to identify any ischemic events during surgery. After bypass, the aneurysm was trapped, or the proximal parent artery was occluded. Digital subtraction angiography or computed tomography angiography was used to evaluate the patency of bypass postoperatively. Blood flow was measured by ultrasound before discharge.
INTRODUCTION
-
RESULTS: Among 1561 patients treated for intracranial aneurysms in our institute, 6 were included for the current report. There were 2 dominant M2 fusiform aneurysms, 2 M1 fusiform aneurysms, 1 supraclinoid internal carotid artery fusiform aneurysm, and 1 M1 bifurcation giant aneurysm. All 6 cases were successfully treated using this technique. One patient had temporary numbness in the contralateral extremities, which was caused by perforator complications. The blood flow carried by the STA was 108e232 mL/minute.
-
CONCLUSIONS: When anastomosed to proximal branches, a double-barrel STA to MCA bypass can reliably provide a high blood flow of >100 mL/minute. Combined with aneurysm trapping or parent artery occlusion, this
-
Key words Bypass - Complex - Intracranial aneurysm - STA -
Abbreviations and Acronyms CT: Computed tomography DSA: Digital subtracted angiography ICA: Internal carotid artery MCA: Middle cerebral artery MEP: Motor evoked potential MRI: Magnetic resonance imaging
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T
he superficial temporal artery (STA) to cortical middle cerebral artery (MCA) bypass was pioneered by Yasargil in 1967 to treat MCA occlusion.1 Since then, STA to cortical MCA bypass has been widely applied to augment blood flow in cases with parent artery compromise during treatment of complex intracranial aneurysms.2-9 STA to cortical MCA bypass has been routinely performed as an adjuvant to treat complex aneurysms located at both anterior and posterior circulation.2,3,10 Most patients have reported a satisfactory outcome. However, some postoperative ischemic events have been observed, and these events are suspected to be due to insufficient blood flow supplied by the STA to cortical MCA bypass.5,11-15 Subsequently, graft interposition bypasses using radial artery or venous grafts have been developed to increase blood flow.16-19 Moreover, the concepts of a low-flow bypass (blood flow <50 mL/minute) and high-flow bypass (blood flow 50 mL/minute) have been established to classify the capacity of flow augmentation. Low-flow bypass includes pedicle grafts, such as STA and occipital artery pedicles. High-flow bypass includes a graft interposition bypass as a radial artery and autogenous vein grafts.19 However, it has been reported that pedicle grafts with STA may occasionally supply blood flow with a capacity of >100 mL/minute in clinical practice.7 Another type of STA to MCA bypass is used to target the recipient at the proximal MCA, such as segment M2 or M3; this type of bypass was first reported by Diaz et al. in 1985.20 The STA to proximal MCA bypass has been reported to be capable of providing more blood flow compared with a traditional STA to
SEP: Somatosensory evoked potential STA: Superficial temporal artery Department of Neurosurgery, Xuanwu Hospital, Capital Medical University, Beijing, China To whom correspondence should be addressed: Peng Hu, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.01.203 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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cortical MCA bypass.4,20 However, its technical details and the capacity of blood flow supply have not been documented well yet. We report our initial experience in treating complex intracranial aneurysms with a double-barrel STA to proximal MCA bypass, which was qualitatively and quantitatively evaluated postoperatively.
scans were examined before discharge. Transcranial ultrasound was used to measure the blood flow of both donor vessels and recipients. DSA was performed to evaluate the patency of the bypass, which is the blood flow replacement for the target territory, and obliteration of the aneurysms. A scheduled follow-up by telephone or a clinic interview was proposed to each patient.
MATERIALS AND METHODS
RESULTS
This study was approved by the local university hospital ethics review board. Written consent was obtained from each patient. Patients with intracranial aneurysms were prospectively managed in our database. Electrophysiologic monitoring, including somatosensory evoked potential (SEP) monitoring and motor evoked potential (MEP) monitoring, was applied to detect ischemic events during intracranial aneurysm microsurgery over the past 5 years. Using this method, we could determine whether or not the bypass could supply enough blood flow after major vessel sacrifice in aneurysm surgery. We included consecutive intracranial aneurysms that were treated by the same senior physician (P.H.) using aneurysm trapping/proximal parent artery ligation and blood flow replacement with double-barrel STA to proximal MCA bypass in the anterior circulation. For terminal aneurysms that were considered unclippable, sacrifice of the parent artery in conjunction with blood flow replacement was anticipated. For internal carotid artery (ICA) aneurysms, a carotid compression test was performed during digital subtraction angiography (DSA). If the circle of Willis was present, a balloon test occlusion was subsequently performed. The size of STA for each patient was measured before operation.
Within the past 5 years, 1561 patients with intracranial aneurysms were treated microsurgically or endovascularly in our institute. Among 1561 patients, 6 had unruptured intracranial aneurysms and were included in the study. The selection process of these 6 patients is shown in Figure 1. Detailed information for these 6 patients is provided in Table 1. Specifically, 5 patients had a fusiform aneurysm, and 1 patient had a giant saccular aneurysm. Two of the fusiform aneurysms were located on the dominant M2 segment. Two of the fusiform aneurysms were located on the terminal M1 segment; 1 of these aneurysms was endovascularly coiled. Additionally, 1 fusiform aneurysm involved the whole supraclinoid ICA; this case has been reported elsewhere to illustrate our operative techniques.21 The last patient had a giant M1 aneurysm involving terminal bifurcation. One patient developed a small basal ganglion infarction on day 8 after the operation. The infarction resulted in numbness of the contralateral extremities with a modified Rankin Scale score of 1 that lasted for 1 week. Otherwise, the patients performed well with a modified Rankin Scale score of 0 up to their last follow-up. The blood flow carried by the STA was 108e232 mL/minute. MRI or CT perfusion was available for 5 patients. Two (patients 3 and 4) of these 5 patients showed slightly low perfusion and the other 3 patients (patient 1, 5, and 6) had roughly equal perfusion compared with the other side.
Surgical Techniques The surgical techniques have been previously reported in detail.21 In brief, after general anesthesia, SEP monitoring and MEP monitoring were begun. The main branches of the STA were dissected during craniotomy. In patients undergoing graft artery harvest, nimodipine saline (volume 1:5) irrigation was applied to prevent graft artery vasospasm. The craniotomy was performed based on a classic pterional approach.22 The sylvian fissure was extensively dissected. The inlet and outlet of the aneurysm were then determined. Next, the anticipated recipient arteries, such as M2 and M3, were sufficiently dissected. A tolerance test was performed under electrophysiologic monitoring.21 After validation of the recipient arteries, anastomosis was performed in an intermittent fashion. Indocyanine green angiography was employed to confirm the bypass patency. Subsequently, the aneurysm was trapped, or the proximal parent artery was clipped depending on whether there were side branches involved in the aneurysm or not. SEPs and MEPs were intermittently tested for 30 minutes before the wound closure. Postoperative Care Postoperatively, patients received intensive care. Fluid augmentation was given to each patient. A computed tomography (CT) scan was performed on the first day after the operation. If there was no intracranial hemorrhage, 100 mg aspirin was prescribed to patients daily. Patients were discharged 1 week after the operation if they had no complications. Magnetic resonance imaging (MRI)
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Illustrative Cases Case 1. A 53-year-old man presented with intermittent dizziness and a right dominant M2 fusiform aneurysm was diagnosed 1 week before admission (Figure 2). DSA demonstrated that the fusiform aneurysm had an irregular shape. Aneurysm wall enhancement was demonstrated on high-resolution MRI. The STA trunk was 2 mm, and the 2 branches of the STA were equally developed. These 2 branches were immediately anastomosed to the proximal MCAs after developing the aneurysm. The aneurysm was removed after confirmation of the patent anastomosis through indocyanine green angiography. MEPs and SEPs had no changes throughout the whole surgery. Postoperative DSA demonstrated the patency of the bypass and complete obliteration of the aneurysm. There was no evidence of ischemic lesions on MRI. Ultrasound showed blood flow was 232 mL/minute. Case 3. A 24-year-old man had a brain infarction 10 months before admission. He recovered well after conservative treatment. A fusiform aneurysm at the right M1 segment was found (Figure 3). Embolization of the aneurysm with stent placement was performed in another hospital. Angiography performed 6 months after the operation indicated regrowth of the aneurysm. Further intervention treatment failed owing to the difficulty of catheterization. He was then referred to our institute for further treatment. The right STA was measured 1.8 mm after his
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DOUBLE-BARREL STA TO PROXIMAL MCA BYPASS
Figure 1. Flow chart of patient selection. STA, superficial temporal artery; MCA, middle cerebral artery.
hospitalization. The equal-sized branches of the STA were anastomosed to the M3 branches of the right MCA. The stent was visible during the operation and was placed from M1 to the frontal M2 trunk. To prevent stent collapse and subsequent perforator occlusion, the aneurysm and parent artery were left intact. The second stage of endovascular M1 occlusion was planned before his
discharge. Postoperative CT and MRI showed neither intracranial hemorrhage nor a fresh ischemic lesion. Ultrasound demonstrated the patency of the bypass with a blood flow of 148 mL/minute. DSA was performed to occlude the parent artery. However, the parent artery occluded spontaneously on day 5 after operation (Figure 3). The patient was discharged on postoperative day 7. He
Table 1. Patient Characteristics AN
Result
Age Symptoms (years)/ (mRS Case Sex Location Morphology Score)
Treatment
Outcome (mRS Score)
AN
Flow Bypass (mL/minute)
Follow-Up (months)
Complications
1
53/M
M2
Fusiform
Dizziness (1) AN trapping þ bypass
Good (0)
Occluded Patent
232
18
No
2
60/F
M2
Fusiform
Headache (1) AN trapping þ bypass
Good (0)
Occluded Patent
—
17
No
3
26/F
M1
Fusiform
Headache (1) AN trapping þ bypass
Good (0)
Occluded Patent
108
12
No
4
60/F
M1
Giant saccular
Incidental (0) AN trapping þ bypass
Good (0)
Occluded Patent
210
10
No
5
24/M
M1
Fusiform
Ischemic (0)
Bypass
Symptomatic infarction, fully resolved (1)
Occluded Patent
148
15
No
6*
45/F
ICA C6y
Fusiform
Dizziness (1)
Proximal ICA occlusion þ bypass
Good (0)
Occluded Patent
146
10
No
AN, aneurysm; mRS, modified Rankin Scale; M, male; F, female; ICA, internal carotid artery. *This patient has been reported elsewhere to illustrate our microsurgical techniques. yC6 represents the supraclinoidal segment of ICA.
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DOUBLE-BARREL STA TO PROXIMAL MCA BYPASS
Figure 2. Imaging studies of case 1. (A) Three-dimensional digital subtraction angiography shows a fusiform aneurysm on the dominant M2. (B) High-resolution magnetic resonance imaging demonstrates wall enhancement of the aneurysm (arrowhead). (C) Superficial temporal artery
experienced numbness in his left extremities on postoperative day 8. MRI demonstrated a small fresh infarction on the right internal capsule. The symptoms disappeared completely 1 week after conservative treatment.
is well developed. (D and E) Postoperative digital subtraction angiography shows full occlusion of the aneurysm and bypass patency. (F) Postoperative magnetic resonance imaging depicting no brain infarction.
demonstrated bypass patency. Ultrasound showed the bypass had a blood flow of 210 mL/minute.
DISCUSSION Case 5. In a 60-year-old woman, a left M1 terminal giant saccular aneurysm with a length of 3.7 cm was incidentally found on MRI (Figure 4). Preoperative angiography could not clearly show the position of the outlet owing to the significant stagnation. The STA was 2 mm with an underdeveloped frontal branch. The aneurysm was explored after craniotomy and extensive dissection of the sylvian fissure. The aneurysm had a broad base involving 2 branches of the M2. The parietal STA was anastomosed to the temporal M2 trunk, which was a dominant branch, whereas the smaller STA was anastomosed to the M3 branch of the frontal M2 trunk after its emergence from the operculum. The aneurysm was removed after confirmation of bypass patency and no changes in SEPs and MEPs during the operation. Postoperative MRI demonstrated there were no fresh brain infarctions 3 days after the operation. CT angiography
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An ideal treatment for intracranial aneurysms is to eliminate them from the cerebral circulation, which can usually be accomplished by direct neck clipping or endovascular coiling. However, both microsurgical clipping and endovascular coiling are challenging in complex aneurysms, including aneurysms that lack a neck, have significant neck calcification, are very large, were previously treated, or have special histology.23 Consequently, major vessels have to be sacrificed in such circumstances, and bypasses are needed to augment the blood flow, especially when the patients cannot tolerate the balloon test occlusion.9,10,18,24 The options for extracranial-intracranial artery anastomosis have been evolving since the first report by Yasagil et al.1 using Hunterian ligation and STA to cortical MCA bypass to treat 2 patients with intracranial aneurysms.1 In the decades since 1970, the most popular bypass involved 1 STA branch anastomosed to a cortical MCA
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ORIGINAL ARTICLE PENG HU ET AL.
Figure 3. Imaging studies of case 3. (A) A fusiform aneurysm on the M1 trunk is demonstrated on DSA image. (B) Thrombus (arrow) is shown on contrast-enhanced magnetic resonance imaging. (C) Embolization of the aneurysm is achieved with coils assisted by a stent. (D) Control angiography demonstrates aneurysm recurrence 7 months after
branch.2,3,5,6,12 Promising results have been reported by numerous centers.1-3,10 Thus, for unclippable aneurysms, clinicians initially preferred to perform a major vessel sacrifice and STA to cortical MCA bypass. However, there were also a few reports of patients who had ischemic complications after major vessel sacrifice even after STA to cortical MCA bypass was performed. Based on previous reports, most of which were successful treatments, Spetzler and Carter10 argued that the ischemic complications may have resulted from insufficient flow supplied by the anastomosis or due to clot propagation. The ischemic complications could be resolved by intravenous heparin administration and flow expansion. Subsequently, some clinicians switched to interposition graft bypasses, such as saphenous vein and radial artery bypasses.16,17,25 Initially, interposition grafts, such as radial artery and saphenous vein bypasses, had high operative morbidity and mortality owing to acute graft occlusion.16,17 After establishing a set of successful operative methods, the surgery results using interposition grafts have been significantly improved.17,25 It was reported that interposition anastomosis to M2 could supply a blood flow >100 mL/minute, which is known as a high-flow bypass.25 Therefore, the extracranial-intracranial bypasses have been divided into high-flow bypasses, such as an interposition graft bypass, and low-flow bypasses, such as a pedicle bypass using STA or occipital artery.18,25,26 The blood flow amounts used to define these 2 groups were controversial.7,18,19,25 Liu et al.18 reported that a low-flow bypass usually carries a flow of 15e25 mL/minute, whereas a high-flow bypass can provide a
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endovascular coiling. (E) Well-developed superficial temporal artery and its branches. (F and G) The aneurysm is fully occluded, and the bypass is patent. (H) Magnetic resonance imaging demonstrates a small fresh infarction at the right basal ganglion (arrowhead) on day 8 after surgery.
blood flow of 70e140 mL/minute.18 Ramanathan et al.19 divided low-flow bypass and high-flow bypass using blood flow supplied by an anastomosis of 50 mL/minute. Possibility of STA to MCA Bypass to Supply High Flow We reported our initial experience using a double-barrel STA to proximal MCA bypass and parent artery sacrifice to treat complex intracranial aneurysms. Among these 6 patients, only 1 patient had postoperative ischemic complications that were caused by clot formation and perforator occlusion. Postoperative ultrasound demonstrated that the blood flow using our method can be 108e 232 mL/minute, which was traditionally defined as a high-flow bypass. Amin-Hanjani et al.27 also reported their experience using STA to MCA bypass to treat intracranial aneurysms. They measured the bypass flow, which was 11e70 mL/minute, using intraoperative ultrasound. In their recent reports, they included 22 patients throughout a 10-year period in which they used STA to MCA bypass to treat intracranial complex aneurysms. Only 1 patient had symptoms related to flow insufficiency, which were confirmed to be due to bypass occlusion during the follow-up examinations. The bypass flow was measured at 42e170 mL/ minute, and the flow was kept steady during the follow-up examinations.7 However, the authors did not report the details of their technique, which could be STA to cortical MCA bypass or single STA to proximal MCA bypass. Our bypass flow was higher than previously reported results. This discrepancy could be due to 2 reasons. First, we used double-barrel anastomosis,
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Figure 4. Imaging studies of case 5. (A) Magnetic resonance imaging demonstrates a giant aneurysm. (B and C) Digital subtraction angiography shows a giant saccular aneurysm on the M1 bifurcation. The frontal superficial temporal artery branch is underdeveloped. (D and E)
and second, we chose M2 or M3 as the recipient. The artery blood flow is not markedly affected by the conduit lumen until lumen reduction is very pronounced.28 It was stressed that the flow that was produced was directly related to the cerebral perfusion pressure under such critical conditions.28 Moreover, it is well known that if an interposition graft, such as a radial artery or saphenous vein, was anastomosed with an STA trunk and M2 or M3, the bypass flow could be up to 100 mL/minute.29 It was reported that the whole MCA territory would be perfused if an M2 recipient was chosen. Although 60% of the MCA territory would be supplied by the bypass if a cortical artery was selected as a recipient, it would need several months to mature.4 Thus, it would be reasonable that our bypass flow was higher compared with the flow that was previously reported when we applied double-barrel anastomosis with an M2 or M3 segment. Additionally, our patient had no low flow-related ischemic events in the follow-up period. The flow was measured at 100e175 mL/minute in the ICA and 75e120 mL/minute in the MCA using ultrasound.28 Another study used MRI to quantify blood flow with an average of
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Postoperative computed tomography angiography shows the patency of the bypass. Arrows point to superficial temporal artery. (F) Postoperative magnetic resonance imaging demonstrates no brain infarction.
206 mL/minute in the ICA and 68e119 mL/minute in the MCA.30 Therefore, the rationale was that the bypass flow could be >100 mL/minute, which could reach the blood flow demand after a major vessel sacrifice. Although patients in this report were satisfied with the results, our study has some limitations. First, it was a small patient series with a selection bias. Second, the follow-up evaluation time was not long enough to evaluate the long-term prognosis. A larger number of patients and long-term follow-up are necessary to properly evaluate the effects of this treatment. CONCLUSIONS Our initial experience indicated that for the selected patients, double-barrel STA to MCA bypass could reliably provide blood flow of >100 mL/minute when anastomosed to M2 or M3 branches. When combined with aneurysm trapping or parent artery occlusion, this bypass algorithm could be an alternative treatment for complex intracranial aneurysms.
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REFERENCES 1. Yasargil MG, Krayenbuhl HA, Jacobson JH 2nd. Microneurosurgical arterial reconstruction. Surgery. 1970;67:221-233. 2. Spetzler RF, Schuster H, Roski RA. Elective extracranial-intracranial arterial bypass in the treatment of inoperable giant aneurysms of the internal carotid artery. J Neurosurg. 1980;53:22-27. 3. Peerless SJ, Ferguson GG, Drake CG. Extracranialintracranial (EC/IC) bypass in the treatment of giant intracranial aneurysms. Neurosurg Rev. 1982; 5:77-81. 4. Collice M, Arena O, Fontana RA. Superficial temporal artery to proximal middle cerebral artery anastomosis: clinical and angiographic long term results. Neurosurgery. 1986;19:992-997. 5. Kodama N, Suzuki J. Bypass surgery in the treatment of aneurysms. Neurosurg Rev. 1982;5:87-90. 6. Silvani V, Rainoldi F, Gaetani P, Bonezzi C, Rodriguez y Baena R. Combined STA/MCA arterial bypass and gradual internal carotid artery occlusion for treatment of intracavernous and giant carotid artery aneurysms. Acta Neurochir (Wien). 1985;78:142-147. 7. Rustemi O, Amin-Hanjani S, Shakur SF, Du X, Charbel FT. Donor selection in flow replacement bypass surgery for cerebral aneurysms: quantitative analysis of long-term native donor flow sufficiency. Neurosurgery. 2016;78:332-341 [discussion: 341-342]. 8. Amin-Hanjani S, Alaraj A, Charbel FT. Flow replacement bypass for aneurysms: decisionmaking using intraoperative blood flow measurements. Acta Neurochir (Wien). 2010;152: 1021-1032 [discussion: 1032]. 9. Lawton MT, Hamilton MG, Morcos JJ, Spetzler RF. Revascularization and aneurysm surgery: current techniques, indications, and outcome. Neurosurgery. 1996;38:83-92 [discussion: 92-94]. 10. Spetzler RF, Carter LP. Revascularization and aneurysm surgery: current status. Neurosurgery. 1985;16:111-116. 11. Hopkins LN, Grand W. Extracranial-intracranial arterial bypass in the treatment of aneurysms of the carotid and middle cerebral arteries. Neurosurgery. 1979;5:21-31.
DOUBLE-BARREL STA TO PROXIMAL MCA BYPASS
12. Grote E, Schonmayr R. Extracranial-intracranial bypass in giant aneurysms. Neurosurg Rev. 1982;5: 83-85.
measure in managing complex MCA and PICA aneurysms. Acta Neurochir (Wien). 2016;158: 1523-1531.
13. Olteanu-Nerbe V, Marguth F. Extracranial-intracranial bypass operation in basal tumours. Neurosurg Rev. 1982;5:99-105.
24. Sekhar LN, Natarajan SK, Ellenbogen RG, Ghodke B. Cerebral revascularization for ischemia, aneurysms, and cranial base tumors. Neurosurgery. 2008;62:1373-1408 [discussion: 14081410].
14. Diaz FG, Ausman JI, Pearce JE. Ischemic complications after combined internal carotid artery occlusion and extracranial-intracranial anastomosis. Neurosurgery. 1982;10:563-570. 15. Fox AJ, Vinuela F, Pelz DM, et al. Use of detachable balloons for proximal artery occlusion in the treatment of unclippable cerebral aneurysms. J Neurosurg. 1987;66:40-46. 16. Diaz FG, Pearce J, Ausman JI. Complications of cerebral revascularization with autogenous vein grafts. Neurosurgery. 1985;17:271-276. 17. Sekhar LN, Duff JM, Kalavakonda C, Olding M. Cerebral revascularization using radial artery grafts for the treatment of complex intracranial aneurysms: techniques and outcomes for 17 patients. Neurosurgery. 2001;49:646-658 [discussion: 658-659]. 18. Liu JK, Kan P, Karwande SV, Couldwell WT. Conduits for cerebrovascular bypass and lessons learned from the cardiovascular experience. Neurosurg Focus. 2003;14:e3.
25. Sekhar LN, Kalavakonda C. Saphenous vein and radial artery grafts in the management of skull base tumors and aneurysms. Oper Tech Neurosurg. 1999;2:129-141. 26. Cenzato M, Bortolotti C. The role of extra- and intracranial bypass in the treatment of complex aneurysms. J Neurosurg Sci. 2016;60:70-82. 27. Amin-Hanjani S, Shin JH, Zhao M, Du X, Charbel FT. Evaluation of extracranial-intracranial bypass using quantitative magnetic resonance angiography. J Neurosurg. 2007;106:291-298. 28. Nornes H, Wikeby P. Cerebral arterial blood flow and aneurysm surgery. Part 1: local arterial flow dynamics. J Neurosurg. 1977;47:810-818. 29. Alaraj A, Ashley WW Jr, Charbel FT, AminHanjani S. The superficial temporal artery trunk as a donor vessel in cerebral revascularization: benefits and pitfalls. Neurosurg Focus. 2008;24:E7.
19. Ramanathan D, Temkin N, Kim LJ, Ghodke B, Sekhar LN. Cerebral bypasses for complex aneurysms and tumors: long-term results and graft management strategies. Neurosurgery. 2012;70: 1442-1457 [discussion: 1457].
30. Brockmann C, Gerigk L, Vajkoczy P, Groden C, Neumaier-Probst E. Magnetic resonance imaging flow quantification of non-occlusive excimer laserassisted EC-IC high-flow bypass in the treatment of complex intracranial aneurysms. Clin Neuroradiol. 2012;22:39-45.
20. Diaz FG, Umansky F, Mehta B, et al. Cerebral revascularization to a main limb of the middle cerebral artery in the Sylvian fissure. An alternative approach to conventional anastomosis. J Neurosurg. 1985;63:21-29.
Conflict of interest statement: This work was supported by the National Natural Science Foundation of China (Grant No. 81500988) and National Key R&D Program of China (Grant No. 2016YFC1300800).
21. Hu P, Zhang HQ, Li XJ. Double-barrel STA to proximal MCA bypass and proximal parent artery occlusion for a fusiform superior clinoidal ICA aneurysm. Acta Neurochir. 2018;160:1939-1943. 22. Hu P, Liang J, Bao Y, Li M, Ling F. The pterional transsylvian transtentorial approach to ventrolateral pontine cavernomas: indications and techniques. World Neurosurg. 2014;82:1276-1282.
Received 14 November 2018; accepted 30 January 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.01.203 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
23. Esposito G, Fierstra J, Regli L. Distal outflow occlusion with bypass revascularization: last resort
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