Abstract
The utilization of the internal maxillary artery (IMAX) in subcranial-intracranial bypass for revascularization in complex aneurysms, tumors, or refractory ischemia shows promise. However, robust evidence concerning its outcomes is lacking. Hence, the authors embarked on a systematic review with pooled analysis to elucidate the efficacy of this approach. We systematically searched PubMed, Embase, and Web of Science databases following PRISMA guidelines. Included articles used the IMAX as a donor vessel for revascularizing an intracranial area and reported at least one of the following outcomes: patency, complications, or clinical data. Favorable outcomes were defined as the absence of neurologic deficits or improvement in the baseline condition. Complications were considered any adverse event directly related to the procedure. Out of 418 retrieved articles, 26 were included, involving 183 patients. Among them, 119 had aneurysms, 41 experienced ischemic strokes (transient or not), 2 had arterial occlusions, and 3 had neoplasia. Furthermore, 91.8% of bypasses used radial artery grafts, and 87.9% revascularized the middle cerebral artery territory. The median average follow-up period was 12 months (0.3–53.1). The post-operation patency rate was 99% (95% CI: 97–100%; I2=0%), while the patency rate at follow-up was 82% (95% CI: 68–96%; I2=77%). Complications occurred in 21% of cases (95% CI: 9–32%; I2=58%), with no significant procedure-related mortality in 0% (95% CI: 0–2%; I2=0%). Favorable outcomes were observed in 88% of patients (95% CI: 81–96%; I2=0%), and only 3% experienced ischemia (95% CI: 0–6%; I2=0%). The subcranial-intracranial bypass with the IMAX shows excellent postoperative patency and considerable favorable clinical outcomes. While complications exist, the procedure carries a minimal risk of mortality. However, long-term patency presents heterogeneous findings, warranting additional research.
Similar content being viewed by others
Data availability
Not applicable
Abbreviations
- IMAX:
-
Internal Maxillary Artery
- RAG:
-
Radial Artery Graft
- STA:
-
Superficial Temporal Artery
- SC-IC:
-
Subcranial-Intracranial
- MCA:
-
Middle Cerebral Artery
References
Reddy VP, Singh R, McLelland MD et al (2022) Bibliometric analysis of the extracranial-intracranial bypass literature. World Neurosurg 161:198–205.e5. https://doi.org/10.1016/j.wneu.2022.01.095
Lawton MT, Hamilton MG, Morcos JJ, Spetzler RF (1996) Revascularization and aneurysm surgery: current techniques, indications, and outcome. Neurosurgery 38(1):83–94. https://doi.org/10.1097/00006123-199601000-00020
Yaşargil MG (1999) A legacy of microneurosurgery: memoirs, lessons, and axioms. Neurosurgery 45(5):1025–1092. https://doi.org/10.1097/00006123-199911000-00014
Newell DW, Dailey AT, Skirboll SL (1998) Intracranial vascular anastomosis using the microanastomotic system. Technical note. J Neurosurg 89(4):676–681. https://doi.org/10.3171/jns.1998.89.4.0676
Dai K, Song Z, Gao Y, Zheng J, Liu Z (2019) Occipital artery to upper posterior circulation bypass through the presigmoid approach in revascularization of the posterior circulation: An anatomical study. J Clin Neurosci 63:209–212. https://doi.org/10.1016/j.jocn.2019.01.020
Hong JH, Jung SC, Ryu HS, Kim TS, Joo SP (2023) Occipital artery bypass importance in unsuitable superficial temporal artery: Two case reports. World J Clin Cases 11(9):2091–2097. https://doi.org/10.12998/wjcc.v11.i9.2091
Sun MZ, Wu EM, Starke RM, Morcos JJ (2023) Clipping of recurrent right middle cerebral artery trifurcation aneurysm with extracranial-intracranial and intracranial-intracranial bypass using a radial artery graft: 2-dimensional operative video [published online ahead of print, 2023 Oct 11]. Oper Neurosurg (Hagerstown). https://doi.org/10.1227/ons.0000000000000933
Nossek E, Costantino PD, Eisenberg M et al (2014) Internal maxillary artery-middle cerebral artery bypass: infratemporal approach for subcranial-intracranial (SC-IC) bypass. Neurosurgery 75(1):87–95. https://doi.org/10.1227/NEU.0000000000000340
Shi X, Qian H, Fang T, Zhang Y, Sun Y, Liu F (2015) Management of complex intracranial aneurysms with bypass surgery: a technique application and experience in 93 patients. Neurosurg Rev 38(1):109–120. https://doi.org/10.1007/s10143-014-0571-5
Uysal II, Buyukmumcu M, Dogan NU, Seker M, Ziylan T (2011) Clinical significance of maxillary artery and its branches: a cadaver study and review of the literature. Int J Morphol 29(4):1274–1281. https://doi.org/10.4067/s0717-95022011000400034
Zaki Ghali MG, Srinivasan VM, Britz GW (2019) Maxillary artery to intracranial bypass. World Neurosurg 128:532–540. https://doi.org/10.1016/j.wneu.2019.03.015
Vrionis FD, Cano WG, Heilman CB (1996) Microsurgical anatomy of the infratemporal fossa as viewed laterally and superiorly. Neurosurgery 39(4):777–786. https://doi.org/10.1097/00006123-199610000-00027
Abdulrauf SI, Sweeney JM, Mohan YS, Palejwala SK (2011) Short segment internal maxillary artery to middle cerebral artery bypass: a novel technique for extracranial-to-intracranial bypass. Neurosurgery 68(3):804–809. https://doi.org/10.1227/NEU.0b013e3182093355
Shi XE, Qian H, KS KC, Zhang Y, Zhou Z, Sun Y (2011) Bypass of the maxillary to proximal middle cerebral artery or proximal posterior cerebral artery with radial artery graft. Acta Neurochir 153(8):1649–1655. https://doi.org/10.1007/s00701-011-1070-x
Ulku CH, Ustun ME, Buyukmumcu M, Cicekcibasi AE, Ziylan T (2004) Radial artery graft for bypass of the maxillary to proximal posterior cerebral artery: an anatomical and technical study. Acta Otolaryngol 124(7):858–862. https://doi.org/10.1080/00016480410017477
Karabulut AK, Ustün ME, Uysal II, Salbacak A (2001) Saphenous vein graft for bypass of the maxillary to supraclinoid internal carotid artery: an anatomical short study. Ann Vasc Surg 15(5):548–552. https://doi.org/10.1007/s10016-001-0027-6
Büyükmumcu M, Ustün ME, Seker M, Karabulut AK, Uysal YY (2003) Maxillary-to-petrous internal carotid artery bypass: an anatomical feasibility study. Surg Radiol Anat 25(5-6):368–371. https://doi.org/10.1007/s00276-003-0150-x
Wang L, Lu S, Cai L, Qian H, Tanikawa R, Shi X (2019) Internal maxillary artery bypass for the treatment of complex middle cerebral artery aneurysms. Neurosurg Focus 46(2):E10. https://doi.org/10.3171/2018.11.FOCUS18457
Page MJ, McKenzie JE, Bossuyt PM et al (2021) The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. J Clin Epidemiol 134:178–189. https://doi.org/10.1016/j.jclinepi.2021.03.001
Chiluwal AK, Nouri M, Knobel D, Dehdashti AR (2021) Surgical trapping of a large complex middle cerebral artery aneurysm with double-barrel bypass: 3-dimensional operative video. Oper Neurosurg (Hagerstown) 20(6):E444–E445. https://doi.org/10.1093/ons/opab028
Cho BR, Jang DK, Kim DS, Han YM (2023) Double-barreled IMA-M2 and STA-MCA bypass in severe stenosis of terminal internal carotid artery: three case reports. Acta Neurochir 165(3):631–636. https://doi.org/10.1007/s00701-023-05499-5
Doherty RJ, Moneley D, Brennan P, Javadpour M (2022) Internal maxillary artery to middle cerebral artery bypass for a complex recurrent middle cerebral artery aneurysm: case report and technical considerations. Br J Neurosurg 36(5):654–657. https://doi.org/10.1080/02688697.2020.1849545
Huang C, Qin S, Cao G, Huang W, Yu Y (2022) Internal maxillary artery-radial artery-middle cerebral artery bypass and STA-MCA bypass for the treatment of complex middle cerebral artery bifurcation aneurysm: a case report. Front Surg 8:773371. https://doi.org/10.3389/fsurg.2021.773371
Liu Y, Shi X, Liu F, Sun Y, Qian H, Lei T (2017) Bilateral cavernous carotid aneurysms treated by two-stage extracranial-intracranial bypass followed by parent artery occlusion: case report and literature review. Acta Neurochir 159(9):1693–1698. https://doi.org/10.1007/s00701-017-3101-8
Nossek E, Costantino PD, Chalif DJ, Ortiz RA, Dehdashti AR, Langer DJ (2016) Forearm cephalic vein graft for short, "Middle"-flow, internal maxillary artery to middle cerebral artery bypass. Oper Neurosurg (Hagerstown) 12(2):99–105. https://doi.org/10.1227/NEU.0000000000001027
Patel NV, Ligas B, Gandhi S et al (2020) Internal maxillary to middle cerebral artery bypass using an anterior tibial artery graft, performed using a 3-dimensional exoscope: 2-dimensional operative video. Oper Neurosurg (Hagerstown) 19(2):E187. https://doi.org/10.1093/ons/opz379
Sergeev AV, Савелло АВ, Cherebillo VU, Kiskaev AI, Chemurzieva F (2021) Sequential approach of internal maxillary-to-middle cerebral artery bypass and endovascular occlusion for giant middle cerebral artery aneurysm: a case report. Egypt J Neurol Psychiatr Neurosurg 57(1). https://doi.org/10.1186/s41983-021-00288-2
Wang L, Shi X, Liu F, Qian H (2016) Bypass surgery to treat symptomatic fusiform dilation of the internal carotid artery following craniopharyngioma resection: report of 2 cases. Neurosurg Focus 41(6):E17. https://doi.org/10.3171/2016.9.FOCUS16252
Wang L, Shi X, Qian H (2017) Flow reversal bypass surgery: a treatment option for giant serpentine and dolichoectatic aneurysms-internal maxillary artery bypass with an interposed radial artery graft followed by parent artery occlusion. Neurosurg Rev 40(2):319–328. https://doi.org/10.1007/s10143-016-0778-8
Wang L, Lu S, Qian H, Shi X (2017) Internal maxillary bypass for complex pediatric aneurysms. World Neurosurg 103:395–403. https://doi.org/10.1016/j.wneu.2017.04.055
Wang L, Lu S, Qian H, Shi X (2017) Internal maxillary artery bypass with radial artery graft treatment of giant intracranial aneurysms. World Neurosurg 105:568–584. https://doi.org/10.1016/j.wneu.2017.06.014
Wang L, Jing L, Liu F, Shi X (2023) How I do it: internal maxillary artery to middle cerebral artery bypass to manage giant thrombosed internal carotid artery aneurysm. Acta Neurochir 165(2):495–499. https://doi.org/10.1007/s00701-022-05463-9
White TG, Klironomos G, Langer DJ, Katz J, Dehdashti AR (2020) Combined internal maxillary artery to middle cerebral artery and in situ middle cerebral to middle cerebral artery bypass for complex middle cerebral artery aneurysm: 3-dimensional operative video. Oper Neurosurg (Hagerstown) 18(4):E121–E122. https://doi.org/10.1093/ons/opz166
Yağmurlu K, Kalani MYS, Martirosyan NL et al (2017) Maxillary artery to middle cerebral artery bypass: a novel technique for exposure of the maxillary artery. World Neurosurg 100:540–550. https://doi.org/10.1016/j.wneu.2016.12.130
Yu Z, Shi X, Qian H et al (2016) Internal maxillary artery to intracranial artery bypass: a case series of 31 patients with chronic internal carotid/middle cerebral arterial-sclerotic steno-occlusive disease. Neurol Res 38(5):420–428. https://doi.org/10.1080/01616412.2016.1177931
Yu Z, Shi X, Brohi SR, Qian H, Liu F, Yang Y (2017) Measurement of blood flow in an intracranial artery bypass from the internal maxillary artery by intraoperative duplex sonography. J Ultrasound Med 36(2):439–447. https://doi.org/10.7863/ultra.16.02011
Yu Z, Shi X, Zhou Z, Yang Y, Li P, Zhang Y (2020) Cerebral glucose metabolism changes in chronic ischemia patients following subcranial-intracranial bypass. Neurosurg Rev 43(5):1383–1389. https://doi.org/10.1007/s10143-019-01177-2
Zhang J, Shi X, Liu F, Sun Y, Qian H, Zhou Z (2019) Serpentine aneurysm of the posterior cerebral artery treated by internal maxillary artery bypass followed by parent artery occlusion: a case report and literature review. Acta Neurochir 161(6):1183–1189. https://doi.org/10.1007/s00701-019-03902-8
Wang X, Han G, Wang H et al (2023) Cerebral revascularization for complex middle cerebral artery aneurysms: surgical strategies and outcomes in a single center. Neurosurg Rev 46(1):68. https://doi.org/10.1007/s10143-023-01977-7
Shi X, Qian H, Singh KC et al (2013) Surgical management of vertebral and basilar artery aneurysms: a single center experience in 41 patients. Acta Neurochir 155(6):1087–1093. https://doi.org/10.1007/s00701-013-1656-6
Nouri M, Schneider JR, Shah K, White TG, Katz JM, Dehdashti AR (2021) Cerebral Bypass for Aneurysms in the Era of Flow Diversion: Single-Surgeon Case Series. Oper Neurosurg (Hagerstown) 21(5):303–311. https://doi.org/10.1093/ons/opab215
Chen Y, Chen P, Duan G, Li R, Li Z, Guo G (2023) Extracranial-intracranial bypass surgery for intracranial aneurysm of the anterior cerebral circulation: A systematic review and meta-analysis. Front Neurol 14:1174088. https://doi.org/10.3389/fneur.2023.1174088
Lawton MT, Spetzler RF (1999) Surgical strategies for giant intracranial aneurysms. Acta Neurochir Suppl 72:141–156. https://doi.org/10.1007/978-3-7091-6377-1_12
Drake CG (1979) Giant intracranial aneurysms: experience with surgical treatment in 174 patients. Clin Neurosurg 26:12–95. https://doi.org/10.1093/neurosurgery/26.cn_suppl_1.12
Britz GW (2014) Flow diversion is not yet the complete package. World Neurosurg 82(6):1005–1006. https://doi.org/10.1016/j.wneu.2014.02.017
Krishna C, Hopkins LN (2014) Flow diversion: exciting new technology in its infancy. World Neurosurg 82(6):1003–1004. https://doi.org/10.1016/j.wneu.2013.11.005
Siddiqui AH, Abla AA, Kan P et al (2012) Panacea or problem: flow diverters in the treatment of symptomatic large or giant fusiform vertebrobasilar aneurysms. J Neurosurg 116(6):1258–1266. https://doi.org/10.3171/2012.2.JNS111942
Szikora I, Turányi E, Marosfoi M (2015) Evolution of flow-diverter endothelialization and thrombus organization in giant fusiform aneurysms after flow diversion: a histopathologic study. AJNR Am J Neuroradiol 36(9):1716–1720. https://doi.org/10.3174/ajnr.A4336
Ma Y, Wang T, Wang H et al (2023) Extracranial-Intracranial bypass and risk of stroke and death in patients with symptomatic artery occlusion: the CMOSS Randomized Clinical Trial. JAMA 330(8):704–714. https://doi.org/10.1001/jama.2023.13390
Powers WJ, Clarke WR, Grubb RL Jr et al (2011) Extracranial-intracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: the Carotid Occlusion Surgery Study randomized trial [published correction appears in JAMA. 2011 Dec 28;306(24):2672. Obviagele, Bruce [corrected to Ovbiagele, Bruce]]. JAMA 306(18):1983–1992. https://doi.org/10.1001/jama.2011.1610
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical approval
Not applicable
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Oliveira, L.d.B., Cieslak, P.H., Marques, G.N. et al. Maxillary artery utilization in subcranial-intracranial bypass procedures: a comprehensive systematic review and pooled analysis. Neurosurg Rev 47, 41 (2024). https://doi.org/10.1007/s10143-023-02265-0
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10143-023-02265-0