Maxillary Artery to Middle Cerebral Artery Bypass: A Novel Technique for Exposure of the Maxillary Artery

Accepted Manuscript Maxillary artery to middle cerebral artery bypass: A novel technique for exposure of the maxillary artery Kaan Yagmurlu, MD, M. Yashar S. Kalani, MD, PhD, Nikolay L. Martirosyan, MD, Sam Safavi-Abbasi, MD, PhD, Evgenii Belykh, MD, Avra S. Laarakker, MSc, BEd, Peter Nakaji, MD, Joseph M. Zabramski, MD, Mark C. Preul, MD, Robert F. Spetzler, MD PII:

S1878-8750(17)30002-5

DOI:

10.1016/j.wneu.2016.12.130

Reference:

WNEU 5091

To appear in:

World Neurosurgery

Received Date: 11 October 2016 Revised Date:

28 December 2016

Accepted Date: 29 December 2016

Please cite this article as: Yagmurlu K, Kalani MYS, Martirosyan NL, Safavi-Abbasi S, Belykh E, Laarakker AS, Nakaji P, Zabramski JM, Preul MC, Spetzler RF, Maxillary artery to middle cerebral artery bypass: A novel technique for exposure of the maxillary artery, World Neurosurgery (2017), doi: 10.1016/j.wneu.2016.12.130. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT Yagmurlu K et al.1

Maxillary artery to middle cerebral artery bypass: A novel technique for exposure of the

Kaan Yagmurlu, MD* M. Yashar S. Kalani, MD, PhD*

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Nikolay L. Martirosyan, MD

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maxillary artery

Sam Safavi-Abbasi, MD, PhD

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Evgenii Belykh, MD

Avra S. Laarakker, MSc, BEd, Peter Nakaji, MD

Joseph M. Zabramski, MD

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Mark C. Preul, MD

Robert F. Spetzler, MD

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Department of Neurosurgery

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Barrow Neurological Institute

St. Joseph’s Hospital and Medical Center Phoenix, Arizona

*These authors contributed equally to this work

ACCEPTED MANUSCRIPT Yagmurlu K et al.2 Correspondence: Robert F. Spetzler, MD c/o Neuroscience Publications; Barrow Neurological Institute

350 W. Thomas Rd.; Phoenix, AZ 85013 Tel: 602.406.3593; Fax: 602.406.4104

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E-mail: [email protected]

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DISCLOSURES: None FINANCIAL SUPPORT: None

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St. Joseph’s Hospital and Medical Center

ACKNOWLEDGMENTS: The authors thank the Neuroscience Publications staff at Barrow Neurological Institute for assistance with manuscript preparation and Kristen Larson and Mark Schornak for illustrations. Kaan Yagmurlu, MD, performed and photographed all anatomical

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dissections at both the Dr. Albert L. Rhoton Neuro-Microanatomy Lab and the Barrow Neurological Institute Neuroanatomy Lab.

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SUBMISSION CATEGORY: Technical Note

ACCEPTED MANUSCRIPT Yagmurlu K et al.3 ABSTRACT Objectives: Define the maxillary artery (MaxA) anatomy and present a novel technique for exposing and preparing this vessel as a bypass donor.

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Methods: Cadaveric and radiological studies were used to define the MaxA anatomy and

illustrate a novel method for harvesting and preparing it for extracranial-to-intracranial bypass. Results: The MaxA runs parallel to the frontal branch of the superficial temporal artery (STA)

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and is located on average 24.8±3.8 mm inferior to the midpoint of the zygomatic arch. The pterygoid segment of the MaxA is most appropriate for bypass with a maximal diameter of

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2.5±0.4 mm. The pterygoid segment can be divided into a main trunk and terminal part based on anatomical features and usage in the bypass procedure. The main trunk of the pterygoid segment can be reached extracranially, either by following the deep temporal arteries downward toward their origin from the MaxA or by following the sphenoid groove downward to the terminal part

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of the pterygoid segment, which can be followed proximally to expose the entire MaxA. In comparison, the pre-bifurcation diameter of the STA is 1.9±0.5 mm. The average lengths of the mandibular and pterygoid MaxA segments are 6.3±2.4 and 6.7±3.3 mm, respectively.

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Conclusion: The MaxA can be exposed without zygomatic osteotomies or resection of the middle fossa floor. Anatomical landmarks for exposing the MaxA include the anterior and

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posterior deep temporal arteries and the pterygomaxillary fissure.

KEYWORDS: Aneurysm; bypass; ischemia; maxillary artery; revascularization RUNNING TITLE: Maxillary artery bypass surgery

ACCEPTED MANUSCRIPT Yagmurlu K et al.4 ABBREVIATIONS: EC-IC, extracranial to intracranial; MaxA, maxillary artery; MCA, middle

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cerebral artery; MMA, middle meningeal artery; STA, superficial temporal artery

ACCEPTED MANUSCRIPT Yagmurlu K et al.5 HIGHLIGHTS Anatomy and exposure of the maxillary artery for use as a bypass donor.

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Illustration of extracranial-intracranial (EC-IC) anastomosis.

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The maxillary artery may be used as an alternative donor to the STA in EC-IC bypass.

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ACCEPTED MANUSCRIPT Yagmurlu K et al.6 INTRODUCTION External carotid-to-internal carotid (EC–IC) artery bypass surgery has been used to treat complex aneurysms that require parent vessel occlusion,1-4 skull base tumors that involve the

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major vessels,5 moyamoya angiopathy,6, 7 iatrogenic injury to intracranial vessels, and ischemic disease refractory to maximal medical therapy.8 Bypass procedures for cerebral revascularization are divided into two categories depending on their flow volume: low-flow bypass (≤50 mL/min)

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and high-flow bypass (>50 mL/min).9 Cerebral revascularization techniques are also divided into two types depending on graft materials: pedicled arterial grafts (e.g., superficial temporal artery

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[STA], occipital artery, and middle meningeal artery [MMA]), which are generally used in lowflow bypass procedures, or free venous or arterial grafts (e.g., radial artery or saphenous vein), which are used in high-flow bypass procedures.9 The STA may, in some cases, be a robust conduit and provide more flow than a classic low-flow graft.

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The STA is a workhorse for EC–IC bypass surgery due to its ease of exposure and proximity to the circle of Willis. However, the size of the STA and previous surgery resulting in STA sacrifice may require an alternative bypass donor to be identified. The maxillary artery

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(MaxA) has been proposed as an alternative bypass donor for EC–IC bypass surgery.10, 11 Although neurosurgeons are familiar with the anatomy of the STA and techniques for harvesting

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this vessel, they are less familiar with the anatomy of the MaxA and the nuances of exposure and preparation of this vessel for bypass surgery, increased potential complications, and poor cosmetic outcomes associated with harvesting the vessel. The utility of the MaxA as a bypass donor has been examined in anatomical studies.10, 11 Vrionis et al.11 reported the first clinical case of the MaxA as a donor for bypass surgery using a saphenous vein graft to connect the MaxA and supraclinoid internal carotid artery in one patient

ACCEPTED MANUSCRIPT Yagmurlu K et al.7 with symptomatic fusiform petrous internal carotid artery aneurysm, and then Abdulrauf et al.12 reported on a bypass between the MaxA and middle cerebral artery (MCA) using a radial artery graft to treat a complex aneurysm. The bypass donor was brought intracranially using extradural

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drilling of the middle fossa for exposure of the MaxA. Since this initial report, another team13 has modified the technique, describing a lateral subtemporal craniectomy of the middle fossa floor to expose the MaxA and provide added room for the bypass.

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All current techniques used for the exposure of the MaxA require an osteotomy of the zygomatic arch or bony removal from the middle cranial fossa. Zygomatic osteotomies can be

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associated with severe postoperative pain and chewing difficulties, while middle cranial osteotomies can result in injury to adjacent neurovascular structures. We report a less invasive technique for exposure of the MaxA in the infratemporal fossa without additional drilling of the middle fossa floor or the need to perform a zygomatic osteotomy. Anatomical dissection and

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radiographic studies characterizing the anatomy of the MaxA are presented to familiarize neurosurgeons with the exposure of this vessel.

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METHODS Anatomical Dissections

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Radiographic anatomical measurements were compared with cadaveric dissections (Figure 1). The technical nuances of this dissection are described using a combination of intraoperative video (Video 1) and anatomical dissection performed on formalin-fixed cadaveric specimens. The details of cadaver preparation are described elsewhere.14

ACCEPTED MANUSCRIPT Yagmurlu K et al.8 Radiographic Anatomy of the MaxA The MaxA was bilaterally identified on computed tomography angiography studies in axial, coronal, and sagittal reconstructions in 25 patients (n=50 studies). Measurements at several

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points along the vessel as well as the relationship of the segments of the MaxA (Figure 2) to the zygomatic arch were used to define the anatomy of the MaxA. Measurements from the MaxA were compared to the pre-bifurcation STA to determine the difference in caliber between these

Surgical Technique

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vessels.

Figures 3 and 4 illustrate the surgical anatomy and step-by-step maneuvers to expose the MaxA and perform the bypass procedure.

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RESULTS

Microsurgical Anatomy of the Maxillary Artery The common carotid artery is divided into the internal carotid and external carotid

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arteries at the C3-C4 level (Figure 1). The external carotid artery ascends and gives rise to the STA and MaxA as its terminal branches. The MaxA turns anteriorly and passes medial to the

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neck of the mandibular condyle to reach the infratemporal fossa. The MaxA segments are named according to their trajectory location such as mandibular, pterygoid, and pterygopalatine segments.15 The mandibular segment of the MaxA is located just medial to the neck of the mandibular condyle and give rises to the middle meningeal artery (MMA), accessory meningeal artery, and inferior alveolar artery branches. The MMA usually is the first branch of the mandibular segment of the MaxA, but it can arise together with the inferior alveolar artery at a

ACCEPTED MANUSCRIPT Yagmurlu K et al.9 common trunk. The accessory meningeal artery can arise directly from the MaxA, or it can arise from the MMA, and passes through the foramen ovale to enter the skull. The pterygoid segment, the second segment of the MaxA, usually passes lateral to the lateral pterygoid muscle in the

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infratemporal fossa to reach the pterygomaxillary fissure and gives off several branches that supply the temporal muscle by anterior and posterior deep temporal arteries and muscles of mastication. The pterygoid segment of the vessel can be further divided into a main trunk, which

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is the largest part of the vessel in caliber, and a terminal part that makes a loop and gives rise to small branches. The main trunk of the pterygoid segment of the vessel is located between the

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level of the neck of the mandibular condyle and the level of the buccal nerve, over which a branch of the mandibular nerve crosses. The terminal part of the pterygoid segment of the vessel is located between the level where the buccal nerve crosses the vessel and pterygomaxillary fissure. After passing through the pterygomaxillary fissure, the MaxA enters the pterygopalatine

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fossa, becoming its third segment, called the pterygopalatine segment of the MaxA. The pterygopalatine segment of the MaxA gives rises to the sphenopalatine, infraorbital, and descending palatine arteries.16

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The relationship of the MaxA with the lateral pterygoid muscle is variable. The artery runs lateral to the lateral pterygoid muscle in 60% of cases.17 The right and left infratemporal

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fossae can also be asymmetrical, and differ among ethnic groups.17 In most cases, the pterygoid segment of the MaxA runs lateral to the lower head of the lateral pterygoid muscle, and the artery passes lateral to the inferior alveolar, lingual, and buccal nerves. In 16% of cases, only the buccal nerve crosses the MaxA laterally, and in 5% of cases the artery passes deeper than all the branches of the mandibular nerve.18

ACCEPTED MANUSCRIPT Yagmurlu K et al.10 Radiographic Anatomy of the MaxA Image guidance can be a useful adjunct for identifying the MaxA during surgical dissection (Figure 5). Alternatively, a thorough understanding of the anatomy of the MaxA and

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its relation to bony structures can be used to identify the MaxA with and without the need for neuronavigation. Based on the 50 radiography studies of the MaxA that we examined, the mean distance from the midpoint of the zygomatic arch to the main trunk of the pterygoid segment of

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the MaxA was 24.8±3.8 mm (range, 11.2-29.8 mm). The mean length of the mandibular segment was 6.3±2.4 mm (range, 2.2-11.7 mm). The mean length of the main trunk of the pterygoid

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segment of MaxA was 6.7±3.3 mm (range, 1-14 mm) and the terminal part of the pterygoid segment of MaxA was 27.7±4.7 mm (range, 15.9-36 mm). The maximal diameter of the main trunk of the pterygoid segment, the segment most likely used for anastomosis, was 2.5±0.4 mm (range, 1.9-3.8 mm). For comparison, the mean diameter of the pre-bifurcation STA was 1.9±0.5

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mm (range, 0.8-2.8 mm) (Figure 2).

DISCUSSION

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The pterygoid segment of the MaxA courses parallel to the STA frontal branch and, on average, is located 24.8±3.8 mm inferior to the midpoint of the zygomatic arch. Although

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neuronavigation can be readily used to identify the vessel intraoperatively, a detailed understanding of the anatomy of the infratemporal fossa must be applied to harvest and prepare this vessel for bypass.

The main trunk of the pterygoid segment of the MaxA has the largest caliber (mean, 2.5 mm; range, 1.9-3.8 mm) and is thus the best part of the MaxA for anastomosis. The border

ACCEPTED MANUSCRIPT Yagmurlu K et al.11 between the main trunk and the terminal part of the pterygoid segment, which usually makes a loop, corresponds to the location where the buccal nerve crosses the vessel medially or laterally. Using anatomical dissections depicting the surgical exposure, we demonstrate that the

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MaxA can be harvested without performing a zygomatic osteotomy or drilling the middle fossa. After reflecting the temporal muscle, the main trunk of the pterygoid segment can be reached extracranially in two ways. First, the vessel can be reached by following the deep temporal

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arteries downward toward their origin from the main trunk of the pterygoid segment of the MaxA. Second, the sphenoid groove, a groove on the greater wing of the sphenoid bone, can be

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followed downward to reach the terminal part of the pterygoid segment of the vessel. Then the main trunk of the pterygoid segment can be reached by following the vessel backward. The advantage of using the MaxA as a donor in EC-IC high-flow bypass instead of the extracranial carotid artery in the neck has been described by Abdulrauf et al.12 Additionally, the

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main trunk of the pterygoid segment of the MaxA (mean caliber of 2.6 mm in cadaveric specimens and 2.5 mm on radiographic studies) and the radial artery (2.5-mm mean caliber in cadaveric specimens) are similar in caliber, and the MaxA pterygoid segment is larger than the

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STA (mean caliber of 2.2 mm in cadaveric specimens and 1.9 mm on radiographic studies).19 The STA (pedicled artery graft)–MCA bypass is considered a low-flow bypass, whereas the

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MaxA may be considered comparatively as a higher-flow bypass technique. Currently, no study reports atrophy or fibrosis of the pterygoid muscle, with difficulty chewing and opening the jaw caused by harvesting and coagulating the distal part of the MaxA. Our patient did not experience that problem over the course of long-term follow-up. Abdulrauf et al.12 reported the exposure of the MaxA by performing an extensive extradural dissection and drilling the middle fossa for a MaxA–MCA M2 or M3 branch bypass.

ACCEPTED MANUSCRIPT Yagmurlu K et al.12 In that study, both anteromedial and anterolateral middle fossa craniectomies were described. In the anteromedial craniectomy, the MaxA is obtained via the infratemporal fossa and pulled up through a small craniectomy to perform an end-to-side anastomosis between the MaxA and

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radial artery. Due to the potential difficulty of finding the MaxA and creating an end-to-side anastomosis through a small anteromedial craniectomy, an anterolateral craniectomy in the middle fossa was described by same group.20 The anterolateral approach is aimed at obtaining

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the pterygopalatine segment of the MaxA, which is the terminal branch and smaller caliber than pterygoid segment to perform an end-to-end anastomosis. However, using the main trunk of the

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pterygoid segment as a donor vessel, which is the largest part of the MaxA, may provide higher blood flow and better long-term patency than that provided by the pterygopalatine segment. Moreover, the exposure of the pterygoid segment provides a larger working space for an anastomosis than the space provided by exposing the pterygopalatine segment. In a case report of

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bypass of the MaxA to MCA and to the PCA using a radial artery graft, the pterygoid segment of the MaxA as a donor vessel was obtained by removing the zygomatic arch.19 Similarly, in another study, a modification of the MaxA–MCA bypass was done by performing a zygomatic

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osteotomy and lateral subtemporal craniectomy in addition to the frontotemporal craniotomy in 4 patients.13 Our technique is less invasive compared to the others described in the literature and

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obviates the need for performing extensive bone work, which could cause cosmetic problems or difficulty with chewing.

The importance of appreciating anatomical variations cannot be overstated for the dissection and exposure of the MaxA. Although the proposed technique will assist with identification of this vessel without the need for zygomatic osteotomies in most cases, in cases where the vessel may be 20-30 mm below the zygomatic arch, a zygomatic osteotomy would be

ACCEPTED MANUSCRIPT Yagmurlu K et al.13 extremely helpful in finding the artery. Furthermore, performing a radial artery-to-M4 anastomosis may result in a significant size mismatch depending the size of the radial artery in some cases. Consideration should be given to performing the bypass to the M2 segment of the

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vessel if this more distal bypass is not possible.

CONCLUSION

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The MaxA is an alternative to the STA as a donor for EC–IC bypass surgery. The main trunk of the pterygoid segment of the artery can be exposed extracranially with a standard

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pterional incision without the need for middle fossa craniectomy or zygomatic osteotomy. Neuronavigation can be used to identify the MaxA. Alternatively, the relationship of the MaxA

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to the zygomatic arch can be used to expose the vessel in the infratemporal fossa.

ACCEPTED MANUSCRIPT Yagmurlu K et al.14 REFERENCES 1. Kalani MY, Ramey W, Albuquerque FC, McDougall CG, Nakaji P, Zabramski JM, Spetzler RF. Revascularization and aneurysm surgery: techniques, indications, and outcomes in

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the endovascular era. Neurosurgery. May 2014;74(5):482-497; discussion 497-488. 2. Kalani MY, Zabramski JM, Nakaji P, Spetzler RF. Bypass and flow reduction for complex basilar and vertebrobasilar junction aneurysms. Neurosurgery. May 2013;72(5):763-775;

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discussion 775-766.

3. Kalani MY, Zabramski JM, Hu YC, Spetzler RF. Extracranial-intracranial bypass and vessel

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occlusion for the treatment of unclippable giant middle cerebral artery aneurysms. Neurosurgery. Mar 2013;72(3):428-435; discussion 435-426. 4. Kalani MY, Elhadi AM, Ramey W, Nakaji P, Albuquerque FC, McDougall CG, Zabramski JM, Spetzler RF. Revascularization and pediatric aneurysm surgery. J Neurosurg Pediatr.

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Jun 2014;13(6):641-646.

5. Kalani MY, Kalb S, Martirosyan NL, Lettieri SC, Spetzler RF, Porter RW, Feiz-Erfan I. Cerebral revascularization and carotid artery resection at the skull base for treatment of

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advanced head and neck malignancies. J Neurosurg. Mar 2013;118(3):637-642. 6. Abla AA, Gandhoke G, Clark JC, Oppenlander ME, Velat GJ, Zabramski JM, Albuquerque

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FC, Nakaji P, Spetzler RF, Wanebo JE. Surgical outcomes for moyamoya angiopathy at barrow neurological institute with comparison of adult indirect encephaloduroarteriosynangiosis bypass, adult direct superficial temporal artery-tomiddle cerebral artery bypass, and pediatric bypass: 154 revascularization surgeries in 140 affected hemispheres. Neurosurgery. Sep 2013;73(3):430-439.

ACCEPTED MANUSCRIPT Yagmurlu K et al.15 7. Guzman R, Lee M, Achrol A, Bell-Stephens T, Kelly M, Do HM, Marks MP, Steinberg GK. Clinical outcome after 450 revascularization procedures for moyamoya disease. Clinical article. J Neurosurg. Nov 2009;111(5):927-935.

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8. Kalani MY, Rangel-Castilla L, Ramey W, Nakaji P, Albuquerque FC, McDougall CG,

Spetzler RF, Zabramski JM. Indications and results of direct cerebral revascularization in the modern era. World Neurosurg. Mar 2015;83(3):345-350.

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9. Kawashima M, Rhoton AL, Jr., Tanriover N, Ulm AJ, Yasuda A, Fujii K. Microsurgical

2005;102(1):116-131.

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anatomy of cerebral revascularization. Part I: anterior circulation. J Neurosurg. Jan

10. Buyukmumcu M, Ustun ME, Seker M, Karabulut AK, Uysal YY. Maxillary-to-petrous internal carotid artery bypass: an anatomical feasibility study. Surg Radiol Anat. NovDec 2003;25(5-6):368-371.

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11. Vrionis FD, Cano WG, Heilman CB. Microsurgical anatomy of the infratemporal fossa as viewed laterally and superiorly. Neurosurgery. Oct 1996;39(4):777-785; discussion 785776.

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12. Abdulrauf SI, Sweeney JM, Mohan YS, Palejwala SK. Short segment internal maxillary artery to middle cerebral artery bypass: a novel technique for extracranial-to-intracranial

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bypass. Neurosurgery. Mar 2011;68(3):804-808; discussion 808-809. 13. Nossek E, Costantino PD, Eisenberg M, Dehdashti AR, Setton A, Chalif DJ, Ortiz RA, Langer DJ. Internal maxillary artery-middle cerebral artery bypass: infratemporal approach for subcranial-intracranial (SC-IC) bypass. Neurosurgery. Jul 2014;75(1):8795.

ACCEPTED MANUSCRIPT Yagmurlu K et al.16 14. Yagmurlu K, Rhoton AL, Jr., Tanriover N, Bennett JA. Three-dimensional microsurgical anatomy and the safe entry zones of the brainstem. Neurosurgery. Dec 2014;10 Suppl 4:602-619; discussion 619-620.

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15. Allen WE, 3rd, Kier EL, Rothman SL. The maxillary artery in craniofacial pathology. Am J Roentgenol Radium Ther Nucl Med. May 1974;121(1):124-138.

New York: Churchill Livingstone; 2005:519–526.

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16. Berkovitz BKB. Infratemporal region and pterygopalatine fossa. Gray’s Anatomy. 39th ed.

17. Sashi R, Tomura N, Hashimoto M, Kobayashi M, Watarai J. Angiographic anatomy of the

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first and second segments of the maxillary artery. Radiat Med. May-Jun 1996;14(3):133138.

18. Pretterklieber ML, Skopakoff C, Mayr R. The human maxillary artery reinvestigated: I. Topographical relations in the infratemporal fossa. Acta Anat (Basel). 1991;142(4):281-

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287.

19. Shi X, Qian H, Singh K. C. KI, Zhang Y, Zhou Z, Sun Y. Bypass of the maxillary to proximal middle cerebral artery or proximal posterior cerebral artery with radial artery

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graft. Acta Neurochir (Wien). Aug 2011;153(8):1649-1655; discussion 1655. 20. Eller JL, Sasaki-Adams D, Sweeney JM, Abdulrauf SI. Localization of the Internal Maxillary

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Artery for Extracranial-to-Intracranial Bypass through the Middle Cranial Fossa: A Cadaveric Study. J Neurol Surg B Skull Base. Feb 2012;73(1):48-53.

ACCEPTED MANUSCRIPT Yagmurlu K et al.17 FIGURE LEGENDS Figure 1. Descriptive anatomy of the infratemporal fossa and maxillary artery. A, The removal of the parotid gland and masseter muscle exposes the mandible. A part of the mandibular ramus

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has also been removed, exposing the medial structures. The temporalis muscle arises from the superior temporal line and passes medial to the zygomatic arch to insert onto the coronoid

process of the mandible. The maxillary artery courses parallel to the trajectory of the frontal

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branch of the STA in nearly all specimens. B, Enlarged view shows the external carotid artery divided into the maxillary artery and superficial temporal artery. The maxillary artery runs

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forward medial to the mandible and mandibulosphenoidal ligament, called the mandibular segment of the maxillary artery, and usually runs lateral to the lateral pterygoid muscle. C, The temporalis muscle was removed while leaving the superior temporal line. The STA passes lateral to the zygomatic arch while the maxillary artery passes medial and inferior to the zygomatic

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arch. D, The mandibular condyle has been removed to expose the infratemporal fossa. The infratemporal fossa is bordered anteriorly by the maxillary bone, medially by the pterygoid process of the sphenoid bone, superiorly by the greater wing of the sphenoidal bone, posteriorly

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by the styloid process, which is located posteromedial to the styloid foramen, carotid sheath, and deep part of the parotid gland, and laterally by the mandibular ramus. E, The branches of the

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external carotid artery, which are the superior thyroidal artery, ascending pharyngeal artery, lingual artery, facial artery, occipital artery, superficial temporal artery, and maxillary artery, have been exposed in the neck. The vagal nerve travels together with the common and internal carotid arteries, while the hypoglossal nerve crosses the external carotid artery to reach the lingula. The upper and lower heads of the lateral pterygoid muscle have been removed to expose the mandibular nerve branches. F, The relationship of the branches of the mandibular nerve and

ACCEPTED MANUSCRIPT Yagmurlu K et al.18 the maxillary artery in the infratemporal fossa is shown. The mandibular nerve exits the skull by passing through the foramen ovale, and then it passes medial to the upper head of the lateral pterygoid muscle. After a short course, the nerve divides into a smaller anterior and a larger

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posterior trunk. The anterior trunk of the mandibular nerve is mainly a motor nerve, which innervates the muscle of mastication, and the posterior trunk is mainly a sensory nerve. The posterior trunk is composed of the auriculotemporal nerve, lingual nerve, and inferior alveolar

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nerve. The auriculotemporal nerve encircles the middle meningeal artery and turns backward by passing under the lateral pterygoid muscle to come superficially between the temporomandibular

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joint and external acoustic meatus. The auriculotemporal nerve joins the otic ganglion to innervate the parotid gland. The lingual nerve lies medial to the lateral pterygoid muscle, and then it passes downward in the pterygomandibular space located between the medial pterygoid muscle and mandible. In this space, the lingual nerve is situated anterior to the inferior alveolar

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nerve. The inferior alveolar nerve is the largest branch of the posterior trunk of the mandibular nerve. The inferior alveolar nerve descends deep to the lateral pterygoid muscle, posterior to the lingual nerve. It is also accompanied in its course by the inferior alveolar artery. The buccal

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nerve is the only sensory branch of the anterior trunk of the mandibular nerve. On emerging between the upper and lower heads of the lateral pterygoid muscle, it passes downward and

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forward across the lower head. G, In a different specimen, the temporal and infratemporal fossae have been exposed while the lateral pterygoid muscle was preserved. The lateral pterygoid muscle has upper and lower heads. The maxillary artery usually passes lateral to the lateral pterygoid muscle in the infratemporal fossa. Above the zygomatic arch, the layers of the temporal fascia and muscle have been exposed. The temporomandibular joint, between the mandibular condyle and temporal root of the zygomatic arch, is situated at the same axial level

ACCEPTED MANUSCRIPT Yagmurlu K et al.19 as the tragus. H, The maxillary artery is divided into three segments: mandibular, pterygoid, and pterygopalatine. The mandibular segment of the maxillary artery is located just medial to the neck of the mandibular condyle and gives rise to middle meningeal artery and inferior alveolar

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artery branches. The second segment of the maxillary artery, the pterygoid segment, is located between the mandibular segment of the vessel and the pterygomaxillary fissure. The pterygoid segment of the vessel can be further divided into a main trunk, which is located between the level

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of the neck of the mandibular condyle and the level where the buccal nerve crosses the vessel, and a terminal part of the pterygoid segment of the vessel, which is located between the level

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where the buccal nerve crosses the vessel and the pterygomaxillary fissure. After passing through the pterygomaxillary fissure, the third segment of the maxillary artery, called the pterygopalatine segment, enters the pterygopalatine fossa. I, the pterygopalatine fossa is exposed through the maxillary sinus. The pterygopalatine segment of the maxillary artery gives rise to the descending

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palatine artery, sphenopalatine artery, and infraorbital artery. Figures 1A-H are used with permission from Barrow Neurological Institute, Phoenix, Arizona. Figure 1I, dissections prepared by Kaan Yagmurlu, MD. Reproduced with permission from the Rhoton Collection.

sa/4.0).

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(http://rhoton.ineurodb.org), CC BY-NC-SA 4.0 (http://creativecommons.org/licenses/by-nc-

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Abbreviations: A., artery; Acc., accessory; Acus., acoustic; Ant., anterior; Asc., ascending; Aur., auricular; Br., branch; CCA, common carotid artery; CN, cranial nerve; Cor., coronoid; Desc., descending; ECA, external carotid artery; EJV, external jugular vein; Ext., external; For., foramen; Front., frontal; ICA, internal carotid artery; IJV, internal jugular vein; Inf., inferior; Infraorb, infraorbital; Interfasc., interfascial; Lat., lateral; M., muscle; Mand., mandibular; Max., maxillary; Med., medial; Men., meningeal; Mid., middle; MMA, middle meningeal artery;

ACCEPTED MANUSCRIPT Yagmurlu K et al.20 N., nerve; Occ., occipital; Pal., palatine; Par., parietal; Phar., pharyngeal; Post., posterior; Proc., process; Pteryg., pterygoid; SCM, sternocleidomastoid muscle; Segm., segment; Sphen., sphenoidal; Sphenopal., sphenopalatine; STA, superficial temporal artery; Stylomast.,

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stylomastoid; Sup., superior; Super., superficial; Temp., temporal; Term., terminal; Thyr., thyroidal; Zygo., zygomatic.

Figure 2. Schematic drawing illustrating the segments of the maxillary artery and their

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relationship to bony structures. The maxillary artery can be divided into three parts: the

mandibular segment (green), the pterygoid segment (light and dark blue), and the pterygopalatine

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segment (pink). The pterygoid segment can further be divided into a main trunk (light blue) and a terminal part (dark blue). 1) The distance from the midpoint of the zygomatic arch to the main trunk of the pterygoid segment of the MaxA. 2) The length of the terminal part of the pterygoid segment of the MaxA. 3) The length of the main trunk of the pterygoid segment of the MaxA. 4)

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The length of the mandibular segment of the MaxA. 5) The diameter of the main trunk of the pterygoid segment of the MaxA. 6) The diameter of the pre-bifurcation STA. Used with permission from Barrow Neurological Institute, Phoenix, Arizona.

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Figure 3. Surgical view of the maxillary artery in the infratemporal fossa. A, Through a pterional incision, the temporalis muscle is removed. If the deep temporal arteries are not well exposed, an

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alternative technique for obtaining the pterygoid segment of the maxillary artery is to follow the sphenoid groove downward. B, Enlarged view of Fig. 3A. The terminal part of the pterygoid segment of the artery, located just before the artery enters the pterygomaxillary fissure, is reached when following the sphenoid groove downward. The terminal part of the pterygoid segment usually makes a loop and gives rise to small branches between the pterygomaxillary fissure at the point where the buccal nerve crosses the artery. Thereafter, the artery is followed

ACCEPTED MANUSCRIPT Yagmurlu K et al.21 backward to reach the main trunk of the pterygoid segment, which is the largest part in caliber and most suited for use as a bypass donor. The buccal nerve usually runs medial to the vessel, but it sometimes runs laterally as this specimen. C, In another specimen, the trajectory of the

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pterygoid segment of the maxillary artery is exposed. Figures 3A and 3B are used with

permission from Barrow Neurological Institute, Phoenix, Arizona. Figure 3C, dissections

prepared by Kaan Yagmurlu, MD. Reproduced with permission from the Rhoton Collection.

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(http://rhoton.ineurodb.org), CC BY-NC-SA 4.0 (http://creativecommons.org/licenses/by-ncsa/4.0).

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Abbreviations: A., artery; Ant., anterior; Front., frontal; Lat., lateral; M., muscle; Max., maxillary; N., nerve; Post., posterior; Pteryg., pterygoid; Segm., segment; STA, superficial temporal artery; Temp., temporal; Term., terminal; Zygo., zygomatic. Figure 4. Stepwise surgical technique for the maxillary artery-to-middle cerebral artery (MaxA–

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MCA) bypass. A, The head is rotated 60° to the contralateral side and extended 15° toward the floor to allow for gravity retraction. The head of the bed raises to re-align the patient into a more neutral position. A skin incision behind the hairline is made starting 1 cm anterosuperior to the

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tragus, extending almost parallel to the coronal suture, and ending at the level of the ipsilateral midpupillary line. B, The galeal flap is reflected toward the temporal fossa. C, The subfascial

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dissection is performed. D, The temporalis muscle is cut, leaving a cuff at the superior temporal line. E and F, After reflecting the temporalis muscle toward the temporal fossa, the anterior or posterior deep temporal arteries are found and followed caudally to the MaxA. If the deep temporal arteries are not exposed, the sphenoid groove is followed toward the infratemporal fossa to reach the terminal part of the pterygoid segment of the maxillary artery. Thereafter, the vessel is followed backward, and the loop of the terminal part of the pterygoid segment and the

ACCEPTED MANUSCRIPT Yagmurlu K et al.22 buccal nerve are encountered. G and H, The main trunk of the pterygoid segment, between the anterior and posterior deep arteries or behind the buccal nerve, is ligated by placing a permanent clip at the distal end and a temporary clip at the proximal side of the vessel. I, A recipient MCA

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cortical branch (M4) can be found 6 cm above the external auditory canal, perpendicular to a line that runs from the external auditory canal to the zygomatic prominence (blue dashed line). When a 3-cm opening is made at that point, an appropriate MCA branch can be identified and freed of

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its arachnoid adhesions. J and K, an end-to-end anastomosis is performed between the main trunk of the pterygoid segment of the maxillary artery and radial artery graft. L, an end-to-side

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anastomosis is performed between the radial artery graft and MCA cortical branch. M, enlarged view of Fig. 4L. N, after the bypass procedure is completed, the craniotomy flap is fixed using titanium plates. Used with permission from Barrow Neurological Institute, Phoenix, Arizona. Abbreviations: A., artery; Ant., anterior; M., muscle; Max., maxillary; N., nerve; Post.,

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posterior; Pteryg., pterygoid; Pterygomax., pterygomaxillary; RAG, radial artery graft; Segm., segment; STA, superficial temporal artery; Temp., temporal; Term., terminal. Figure 5. Case example of MaxA–MCA bypass. A 59-year-old female with a diagnosis of

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meningioma involving the left internal carotid artery (ICA), and with two prior resections, presented to our clinical service with transient ischemic attacks. A, Anteroposterior angiography

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revealed complete occlusion of the ICA, while axial magnetic resonance (MR) perfusion B, revealed decreased left hemispheric cerebral blood flow. C, The tumor was stable on coronal MR imaging. D, Intraoperative neuronavigation was used to identify the MaxA for harvesting as a bypass donor (top left, coronal; top right, axial; bottom left, axial; bottom right, coronal). The bypass was performed uneventfully and the patient was neurologically intact postoperatively without evidence of further transient ischemic attacks. E, Coronal postoperative computed

ACCEPTED MANUSCRIPT Yagmurlu K et al.23 tomography angiography reveals the patency of the bypass. Used with permission from Barrow Neurological Institute, Phoenix, Arizona.

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Abbreviations: L, left; R, right.

ACCEPTED MANUSCRIPT Yagmurlu K et al.24 VIDEO LEGEND Video 1. The video illustrates the case of a maxillary artery-to-middle cerebral artery bypass using a radial artery interposition graft. Used with permission from Barrow Neurological

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