The History and Evolution of Internal Maxillary Artery Bypass

Literature Review

The History and Evolution of Internal Maxillary Artery Bypass Long Wang1,2, Li Cai3,4, Shuaibin Lu5, Hai Qian1, Michael T. Lawton2, Xiang’en Shi1,5

Key words Cephalic vein graft - High-flow EC-IC bypass - Internal maxillary artery bypass - Radial artery graft - Saphenous vein graft - Superficial temporal artery graft -

Abbreviations and Acronyms CTA: Computed tomography angiography CV: Cephalic vein DTA: Deep temporal arteries DUS: Doppler ultrasonography EC-IC: Extracranial-to-intracranial FR: Foramen rotundum FS: Foramen spinosum ICA: Internal carotid artery IMA: Internal maxillary artery ITF: Infratemporal fossa LPM: Lateral pterygoid muscle MCA: Middle cerebral artery MMA: Middle meningeal artery MRI: Magnetic resonance imaging RA: Radial artery RAG: Radial artery graft SC-IC: Subcranial-intracranial STA: Superficial temporal artery SV: Saphenous vein SVG: Saphenous vein graft From the 1Department of Neurosurgery, SanBo Brain Hospital, Capital Medical University, Beijing, China; 2 Department of Neurosurgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona, USA; 3Department of Neurosurgery, The First Affiliated Hospital of University of South China, Hengyang, China; 4 Arkansas Neuroscience Institute, CHI St. Vincent Infirmary, Little Rock, Arkansas, USA; and 5Department of Neurosurgery, Fu Xing Hospital, Capital Medical University, Beijing, China To whom correspondence should be addressed: Xiang’en Shi, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2018) 113:320-332. https://doi.org/10.1016/j.wneu.2018.02.158 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.

INTRODUCTION The internal maxillary artery (IMA) is a vital structure located within the infratemporal and pterygopalatine fossae that has been widely explored in head, neck, oral, and maxillofacial surgery. However, its use in

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Internal maxillary artery (IMA) bypass has gained momentum in the last 5 years for the treatment of complex cerebrovascular disorders and skull base tumors. However, some issues regarding this treatment modality have been proposed. As one of the most experienced neurosurgical teams to perform internal maxillary artery bypass in the world (>100 clinical cases), we reviewed the literature in aspects of basic anatomy of maxillary artery with its variations to the lateral pterygoid muscle, initial anastomosis modalities, and subsequent exposure techniques in cadaver studies, preoperative arterial evaluation methods, optimal interposed graft selections, and surgical outcome in the management of complex aneurysms, skull base tumors, and steno-occlusive disorders.

neurologic surgery remains sparse. During the past 5 years, the IMA has been proposed as an alternative donor vessel for connecting intracranial arteries via a short graft in both cadaveric studies and clinical practice of the treatment of intracranial complex aneurysms, skull base tumors, and stenoocclusive flow diseases.1-12 This new technique has various potential advantages over the standard extracranial-to-intracranial (ECIC) high-flow bypass technique.1,5,6,13,14 First, this technique is highly attractive because of its ability to achieve anastomosis via a single cranial incision and avoid attendant complications from the cervical incision. Furthermore, the deep tunneling of the interposition graft decreases the likelihood of graft compression. In addition, the closer proximity between the IMA and the cranial base allows for a shorter graft length and, thus, decreases the risk of graft torsion. The disadvantages of the IMA bypass technique are that the anastomosis is deep and not as easily achieved as the anastomosis on the surface, and mobilization of the IMA requires a zygomatic osteotomy or extensive subtemporal bone removal. Therefore, before attempting such a bypass, the surgeon must practice on cadavers. In this study, we retrospectively reviewed experiences with IMA bypass surgery reported in the available literature with a focus on the variations in IMA anatomy, an initial exploration of IMA bypass modalities, the current IMA exposure techniques used in both cadaveric studies and clinical microsurgical practice, and the surgical

outcomes of the IMA bypass procedure in clinical practice. To the best of our knowledge, this is the first literature review regarding the IMA bypass from a neurosurgical perspective.

IMA ANATOMY Knowledge regarding the anatomy of the human maxillary artery in the infratemporal fossa (ITF) is not only important to dentists, surgeons, or interventional radiologists but also to neurosurgeons. The IMA represents the larger of the 2 terminal branches of the external carotid artery, and anastomoses to branches arise from the main trunk of the internal carotid artery (ICA) and the ophthalmic artery.15 The IMA runs from a posterior-lateral to an anterior-medial course in the ITF, enters the pterygopalatine fossa,16 and distributes the blood flow to both hard and soft tissues and organs in the maxillofacial region, including the parotid gland, masseter muscles, rhinooral structures, cranial nerves, and meninges.15,17 The IMA originates at the mandibular level of the neck in the parenchyma of the parotid gland, turns anteriorly, and passes medially to the neck of the mandible condyle between the condylar process of the mandible and the sphenomandibular ligament and reaches the ITF.18 Then, the IMA may run superficially or deeply to the lower head of the lateral pterygoid muscle (LPM) toward the pterygopalatine fossa.18

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Figure 1. Anatomic segments of internal maxillary artery. Published with permission from Xiang’en Shi.

Anatomically, the IMA is divided into 3 portions based on its relationship with the LPM, and each section is named according to its trajectory (i.e., the mandibular, pterygoid, and pterygopalatine segments) (Figure 1).2,14,15,18-24 The mandibular/first segment runs horizontally and posteriorly to the neck of the mandible and passes anteriorly along the lower head of the LPM between the ascending ramus of the mandibular condyle (superficially) and sphenomandibular ligament (deeply). The branches from the first segment divide into the anterior tympanic, middle meningeal, accessory meningeal, and inferior alveolar arteries.18,24 The middle

meningeal artery (MMA) is usually the first branch of the mandibular IMA, but the MMA can arise together with the inferior alveolar artery at a common trunk. The accessory meningeal artery arises directly from the IMA or the MMA, passes through the foramen ovale, and enters the skull.24 The pterygoid/second segment of the IMA passes obliquely forward either laterally or medially to the lower head of the LPM in the ITF, reaches the pterygomaxillary fissure, and becomes embedded into the pterygoid venous plexus. The second segment gives off several branches that supply the temporal muscle via the anterior and posterior deep temporal arteries (DTAs)

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and mastication muscles that contain the pterygoid, masseteric, and buccal arteries. The anterior DTA (ADTA) arises near the end of the pterygoid segment,18 and Yagmurlu et al.24 further divided this second segment into the main trunk, which is the largest portion of the vessel in caliber, and a terminal portion that creates a loop and gives rise to small branches. The main trunk of the pterygoid IMA is located between the 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 at which the buccal nerve crosses the vessel and the pterygomaxillary fissure. The first and second maxillary segments play an important role in the blood supply to the meninges, mastication muscles, and auditory organs of the inner ear.2 The pterygopalatine/third segment runs between the 2 heads of the LPM and enters the pterygopalatine fossa through the pterygomaxillary fissure, which supplies the mucosal and denticulate areas of the nasal and oral cavities.2 This segment gives rise to the posterior superior alveolar, infraorbital, recurrent meningeal, descending palatine (greater and lesser palatine), vidian, pharyngeal, and sphenopalatine arteries. The optimal selection of an IMA anastomosis site has been controversial. Initially, investigators were prone to use the third segment of the IMA for bypass surgery.1,13,22,25-29 Subsequently, several studies reported that the pterygopalatine IMA courses tortuously, forming a second S-shaped loop, which makes exposure difficult and time consuming.22,30 In addition, Feng et al.14 and Eller et al.13 described that the multiple branches and depth of the IMA in the pterygopalatine fossa could lead to a kinking of the vessel. Vrionis et al.22 reported that, on average, 8 blood vessels were required to be ligated and sacrificed in the pterygopalatine fossa. These features may increase the risk of damage to the IMA during exposure and complications related to a suboptimal bypass and potentially prevent adequate blood flow through the IMA, rendering the pedicle useless.13,14 Thus, most

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Table 1. Anatomic Variability in the Internal Maxillary Artery Reference

Number of Internal Maxillary Artery Dissections

1

Thomson, 189032

447

2

Lauber, 190133

200

3

Adachi, 192834

331

4

Fujita, 193235

119

5

Kijima, 193236

20

Number

6 7

37

Lurje, 1946

Lasker et al., 195138

39

Population

Race

Lateral Pattern (%)

Medial Pattern (%)

British

White

54.4

45.6

Austrian

White

8.5

91.5

Japanese

Asian

93.7

6.3

Japanese

Asian

89.9

10.1

Japanese

Asian

95.0

5.0

200

Soviet

White

67.5

32.5

67

American

White

54.4

45.6

147

African American

Black

68.7

31.3

8

Takarada, 1958

120

Japanese

Asian

90.8

9.2

9

Krizan, 196040

200

Yugoslavian

White

66.0

34.0

10

Ikakura, 196141

160

Japanese

Asian

90.6

9.4

11

Skopakoff, 196842

180

European

White

69.4

30.6

12

Czerwinski, 198143

240

Polish

White

65.8

34.2

158

Japanese

Asian

93.0

7.0

100

Japanese

Asian

93.0

7.0

278

Japanese

Asian

89.2

10.8

339

Japanese

Asian

93.5

6.5

204

European

White

55.4

44.6

89

South African

Black

53.9

46.1

194

Austrian

White

44.8

55.2

13 14 15 16 17 18

44

Iwamoto et al., 1981 Sashi, 198945

46

Suwa et al., 1990 Tsuda, 199147

48

Pretterklieber et al., 1991

49

Rischmuller and Meiring, 1991

19

Ortug and Moriggl, 199150

20

Vrionis et al., 199622

12

American

White

58.3

41.7

21

Harn and Durham, 200351

201

American

White

61.8

38.2

22

Orbay et al., 200752

16

Turkish

White

93.8

6.2

20

23

Hussain et al., 2008

44

Canadian

White

68.2

31.8

24

Dennison et al., 200953

53

New Zealander

White

56.6

43.4

25

Otake et al., 201154

28

Japanese

Asian

96.4

3.6

26

16

Uysal et al., 2011

14

Turkish

White

57.1

42.9

27

Gulses et al., 201219

572

Turkish

White

68.4

31.6

28

Maeda et al., 201255

208

Japanese

Asian

90.4

9.6

29

Hwang et al., 201421

200

Korean

Asian

82.0

18.0

30

Arimoto et al., 201517

38

Japanese

Asian

97.4

2.6

31

31

Alvernia et al., 2017

12

American

White

66.7

33.3

32

Akiyama et al., 201718

10

Japanese

Asian

60

40

practitioners assume that the pterygoid IMA is more appropriate than the pterygopalatine segment as a donor site for an IMA bypass because of its larger caliber size, ease of exposure within a wider working space, and good caliber

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match with the graft vessel.6,14,24,30 At our institution, we routinely use the second segment instead of the third segment as the anastomosis site of the IMA to a graft vessel because of the wider surgical field of dissection, fewer branches arising from

the pterygoid IMA, and closer distance to the skull base. The diameters of both the second and third segments of the IMA (2.4e3.46 mm vs. 2.3e3.2 mm) are well matched with the thickness of the recipient vessels, allowing the

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bypass to provide flow.3,16,18,22,24-29,31

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sufficient

blood

VARIOUS RELATIONSHIPS BETWEEN THE LPM AND IMA Understanding the course of the IMA in the ITF and its variations is of interest to many practitioners.20 The LPM is a short thick muscle that runs in the horizontal plane and occupies most of the ITF. The LPM has 2 distinct heads: a smaller upper infratemporal (superior) head and a lower pterygoid (inferior) head. The infratemporal/upper head originates at the infratemporal surface and crest of the greater sphenoid wing. This portion runs nearly parallel to the floor of the middle cranial fossa and merges posteriorly with the pterygoid head. The pterygoid/ inferior head arises on the lateral surface of the lateral pterygoid plate and runs laterally and superiorly. Both heads are inserted into a depression on the anterior aspect of the neck of the mandible.18,22 Because detailed knowledge regarding the positional relationship between the IMA and the lower head of the LPM is vitally important, the pterygoid IMA has been the subject of numerous anatomic studies that have shown anatomic variability (Table 1).16-22,24,31-53,55 The earliest report found by the authors appeared in 1890 and reported 447 observations from 13 medical schools in Great Britain and

Ireland.32 In 1928, Adachi.34 reported that a superficial/lateral course occurred in 93.7% of a Japanese sample. These investigators concluded that the superficial position of the pterygoid IMA occurred with the highest frequency in the Japanese population, which likely represented a “racial difference.” This observation is consistent with other large-scale studies (
100 cases) in Asia in which a lateral course of the pterygoid segment of the IMA was found to occur in approximately 82.0%e93.5% of cases.21,35,39,41,44,46,47,56 Thus, the course of the maxillary artery varies among different races and there is a tendency for the deep position to occur more frequently in white and African populations. Vrionis et al.22 reported that the pterygoid IMA was found laterally to the LPM in 58% of American whites, which is consistent with previous reports of an incidence of 8.5%e69.4% in >100 case studies involving whites.19,20,32,33,37,40,42,43,48,50,51 Similarly, the superficial/lateral position has been reported by Laskar et al.38 to occur in 68.7% of African Americans and this value was confirmed by Rischmullar et al.49 Some investigators have suggested that these anatomic variations may be associated with developmental processes.15 By combining the data from all these studies, the superficial pattern of the IMA was found in 58.1%, 90.9%, and 63.1% of 2856 white, 2109 Asian,

Figure 2. A superficial pattern of the internal maxillary artery was observed in 58.1%, 90.9%, and 63.1% of 2856 white, 2109 Asian, and 236 African subjects, respectively.

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and 236 African specimens, respectively (Figure 2). Thus, there is a need to summarize the influence of ethnicity on the position of the artery, particularly given the current ease of traveling. However, the mechanisms responsible for determining the relative position of the artery to the LPM remain unknown.20 INITIAL CADAVERIC STUDIES OF IMA BYPASS MODALITIES The notion of using the IMA as the donor artery for high-flow EC-IC bypass surgery was proposed by Vrionis et al. in 1996.22 These investigators described an in situ pterygopalatine IMA-to-supraclinoid ICA bypass. In this bypass, the IMA is transected before the origin of the greater palatine artery following the ligation and sacrifice of an average of 8 blood vessels. Meanwhile, the investigators found that in 25% (3/12) of cases, a tension-free IMA in situ bypass could not be achieved and suggested that a saphenous vein (SV) graft (SVG) could be used to bridge the pterygoid IMA with the supraclinoid ICA when the length of the IMA is inadequate. This technique was further explored by various practitioners at Selcuk University in cadaveric studies.25-30 The pterygoid IMAto-supraclinoid ICA bypass with SVG (mean length, 4.5  0.5 cm) procedure was initially described after a zygomatic osteotomy and extensive removal of the middle fossa floor.30 Subsequently, researchers from the same group reported several studies regarding pterygopalatine IMA-to-proximal posterior cerebral artery, pterygopalatine IMA-to-MCA, and pterygopalatine IMA-tosupraclinoid ICA bypass procedures using a radial artery (RA) graft (RAG), which was pulled through a drilled hole (2e3 cm) lateral to the foramen rotundum (FR) after the zygomatic osteotomy. The average lengths of the RAGs were 4.7  0.5 cm, 3.6  0.6 cm, and 4.0  0.5 cm.26,28,29 Arbag et al.25 then used a transantral approach to expose the IMA and used the superficial temporal artery (STA) (2.4  0.3) graft for the bypass of the pterygopalatine IMA-to-proximal MCA. The posterior wall of the maxillary sinus was removed, and a hole was drilled (5e6 mm) laterally to the posterior edge of the superior orbital fissure in the middle fossa floor to pass the IMA. The landmarks used

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Reference

Number of Cases

Donor Segment of IMA

IMA Identification

Proximal Graft Vessel Graft Length Anastomosis Fashion

Recipient Artery

Outline of Surgical Techniques

12

3rd (greater palatine artery)

NA

In situ IMA

NA

NA

Supraclinoid ICA

Single anastomosis; unsuccessful in 1/4 of the cases; massive branches had to be ligated

Karabulut et al., 200130

5

2nd (middle meningeal artery)

Medial to infratemporal crest

Saphenous vein graft

4.5  0.5 cm

End-to-end

Supraclinoid ICA

Drilling of anterior clinoid process; extensive subtemporal bone removal

Büyükmumcu et al., 200327

10

3rd (IOA)

1 cm medial to infratemporal crest

In situ IMA

3.8  1.7 cm

NA

Petrous ICA

Single anastomosis; zygomatic and infratemporal osteotomy

Ulku et al., 200428

10

3rd (IOA)

1e2 cm beneath the infratemporal crest

RAG

4.7  0.5 cm

End-to-end

Posterior cerebral artery

Zygomatic osteotomy and middle fossa hole drilling to pull RAG through

Üstün et al., 200429

10

3rd (IOA)

1e2 cm inferior to the infratemporal crest

RAG

3.6  0.6 cm

End-to-end

MCA

Zygomatic osteotomy and middle fossa hole drilling to pull RAG through

Arbag et al., 200525

5

3rd (posterior superior 1e2 cm inferior to the alveolar artery, IOA) infratemporal crest

RAG

4.0  0.5 cm

End-to-end

Supraclinoid ICA

Zygomatic osteotomy and middle fossa hole drilling to pull RAG through

Arbag et al., 200526

10

3rd (descending palatine artery)

Superomedial aspect of posterior wall of maxillary sinus

STA

2.4  0.3 cm

End-to-end

MCA

Frontotemporal craniotomy; a hole drilled lateral to superior orbital fissure to pull STA through; posterior wall removal of maxillary sinus

Abdulrauf et al., 20111

6

3rd

8.6 mm anterior to the lateral edge of the FR

RA

NA

Side-to-end

Opercular segment of the middle cerebral artery

Anteromedial extradural middle fossa approach

Eller et al., 201213,*

10

3rd

10 mm anterior and 5 mm lateral to the FR

NA

NA

NA

NA

Anterolateral extradural middle fossa approach

Nossek et al., 20146,y

NA

2nd

After DTA

NA

NA

NA

NA

Subcranial-intracranial middle fossa approach

Feng et al., 201614,*

10

2nd

Anterolateral to the foramen spinosum

NA

NA

NA

NA

Lateral triangle middle fossa approach

Yagmurlu et al., 201724

NA

2nd

DTA, pterygomaxillary fissure

RA

NA

End-to-end

Cortical segment of the Pterional approach middle cerebral artery

LITERATURE REVIEW

IMA, internal maxillary artery; NA, not available; ICA, internal carotid artery; IOA, infraorbital artery; RAG, radial artery graft; STA, superficial temporal artery; MCA, middle cerebral artery; FR, foramen rotundum; RA, radial artery; DTA, deep temporal artery. *IMA dissection studies only. yBrief cadaveric studies with detailed descriptions of clinical cases.

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Table 2. Summary of Cadaveric Studies of Internal Maxillary Artery Bypass

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Figure 3. Cadaveric illumination of internal maxillary arteryeradial arteryeinsular segment of the middle cerebral artery bypass technique. Published with permission from Xiang’en Shi.

to localize and expose the IMA were not described in any of the studies outlined earlier. ADDITIONAL CADAVERIC STUDIES OF IMA EXPOSURE TECHNIQUES Various investigators have criticized the IMA bypass technique because of the challenges it presents, including the difficulty of finding and isolating a suitable segment in the IMA within the ITF and the small space that is available in which to perform the anastomosis between the IMA and the graft vessel (either RAG or SVG). These factors have hindered the potential use of the IMA as an arterial donor for EC-IC bypass surgery.13,14,54 To address these issues, several IMA exposure techniques

have been published, including anteromedial approaches,1 anterolateral approaches,13 subcranial-intracranial (SCIC) approaches,5,6 a pterional approach with zygomatic osteotomy7-12 and, recently, a lateral triangle middle fossa approach3,14 (Table 2). In 2011, Abdulrauf et al.1 established a reliable method based on a bone landmark (i.e., the FR) to localize the IMA using an anteromedial extradural middle fossa approach with detailed measurements (8.6 mm anterior to the lateral edge of the FR). The anterolateral triangle was initially identified by locating the lateral edge of the FR, followed by anterolateral drilling of the middle fossa. Then, the anterior loop or pterygopalatine segment of the IMA can be reliably found. However, the

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small opening and narrow corridor into the pterygopalatine fossa make the precise localization and dissection of the IMA tedious and technically demanding.6,13,14 To address these shortcomings, the following year, the same group of investigators elucidated a simple modified anterolateral middle fossa approach that leads to a wider exposure of the pterygopalatine fossa.13 Using this technique, a larger expanded area of the anterolateral middle fossa from the greater wing of the sphenoid bone down to the infratemporal crest was created, which provided a larger area of exposure of the pterygopalatine fossa and allowed for the easy identification of a longer segment of the IMA. In addition, this approach ensured the preservation of the distal V2 branches and avoided the need to pull the IMA into the middle fossa, thus allowing for an efficient harvest of the IMA and preventing potential kinking of the vessel. However, several shortcomings remain.3,14 First, the surgical technique has been only briefly described, and detailed surgical landmarks for determining the exact location of the IMA in the ITF have not been discussed. Second, the boundaries of the drilled area in the middle fossa floor were not clearly defined. Third, these approaches did not provide a safe surgical trajectory for the protection of the branches of the third segment of trigeminal nerve (V3). In 2014, Nossek et al.6 described an SC-IC technique to open the communication between the middle fossa (intracranially) and ITF (extracranially). The investigators used a zygomatic osteotomy or orbitozygomatic osteotomy, followed by a lateral rectangular craniectomy, in the lateral aspect of the middle fossa to unroof the ITF. The corridor craniectomy reached a line 2 mm lateral to the virtual line between the FR and the foramen ovale. Then, the DTA on the medial aspect of the temporalis muscle were identified, and the IMA was dissected at its second segment (i.e., the pterygoid segment), as the proximal target of anastomosis.5 Similarly to the anterolateral middle fossa approach, a wider exposure of the IMA was facilitated by an extended lateral subtemporal craniectomy of the middle cranial fossa floor rather than a keyhole craniotomy, resulting in a less demanding proximal anastomosis for an SC-IC bypass. However, extensive skull

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Figure 4. Internal maxillary artery (Max. A)eradial arteryeinsular segment of the middle cerebral artery bypass (M2) for the management of giant M1 aneurysm. (Published with permission from Li Cai). Ant., anterior; ICA, internal carotid artery; Pcom, posterior communicating artery; Radial A, radial artery; Temp. A, temporal artery; Ant., anterior; ICA, internal carotid artery; Pcom, posterior communicating artery; Radial A, radial artery; Temp. A, temporal artery; O.N, optic nerve.

base drilling was needed, a definitive landmark for the localization of the IMA was not provided. In addition, the branches of V3 remained prone to compromise as a result of a blurry dissection. In 2016, Feng et al.3,14 described a new lateral triangle middle fossa approach based on its location lateral to both the anterolateral and posterolateral (Glasscock) triangles. The boundaries of the lateral triangle of the middle fossa were defined by the foramen spinosum (FS) as its vertex, posteriorly by a projected line from the FS to the anterior root of the zygomatic arch, medially by a line between the FS and FR, and laterally by the lateral edge of the middle fossa. This triangle is adjacent to, but does not include, the FS and FR. This dissection modality used a 2-step drilling technique after a pterional craniotomy. First, a triangular craniectomy was completed anterolateral to the FS. By following the MMA and dividing the LPM, the pterygoid IMA was consistently found inferolateral to the branches of V3. Second, a bone slot was drilled in a posterior-to-

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anterior direction from the anterior aspect of the first craniectomy. By tracing the proximal part, the main trunk of the IMA was obtained. When the IMA coursed laterally to the upper head of the LPM, the DTA was traced proximally, and then a partial resection or partial removal of the inferior border of the pterional craniotomy followed by medial retraction of LPM was potentially needed. The investigators stated that this 2-step drilling technique, which easily and safely facilitated the exposure of the IMA, differed from previously reported techniques.3,14 First, the V3 branches could be completely freed in a stepwise manner without inadvertent injury. Second, the multiple landmarks (i.e., MMA, DTA, FR, FS, and LPM) that were accessible and easily identified and guided the dissection toward the IMA during the middle fossa trajectory were well preserved. Third, the MMA was a reliable anatomic landmark that could be used to safely and efficiently expose the IMA in cases with an unfavorable anatomy or a tortuous trajectory of the IMA. Fourth, the whole second segment of

the artery could be safely and simply exposed. Because of these factors, the lateral triangle approach was a straightforward suitable method for harvesting the IMA and avoiding confusion surrounding the exposure of the IMA in the ITF, which is performed blindly through a narrow craniectomy. However, the relative complexity of the technique and the variability of the course of the IMA in the ITF often prolonged the dissection time.3 In addition, the exposure of the IMA was limited by the lateral skull base, proximal zygoma, and the temporalis muscle.3 Although this technique of exposing the IMA seems to be simpler and easier than the previous approaches, this approach should be practiced with a cadaver dissection before it is applied clinically. In early 2017, Yagmurlu et al.24 proposed an easier method for exposing and harvesting the pterygoid IMA using a traditional pterional approach with a new landmark, the pterygomaxillary fissure. These investigators noted that all current IMA exposure techniques required an osteotomy of the zygomatic arch or bone removal from the middle cranial fossa. Zygomatic osteotomies can be associated with severe postoperative pain and chewing difficulties, and middle cranial osteotomies can result in injury to the adjacent neurovascular structures. However, the benefits of the zygomatic osteotomy exposure outweigh the cosmetic risks. Previous approaches have routinely removed the bony structures, allowing the temporalis muscle to be exposed further anteriorly and inferiorly, which enlarges the procedural field for IMA dissection, harvest, and proximal anastomosis. Even although good exposure of the pterygoid segment of the IMA in a cadaver study without zygomatic osteotomy has been shown in this technique, the composition and characteristics of the temporalis muscles in cadavers are completely different from their counterparts in vivo. Formalin can cause shrinkage of the soft tissue such that the measured volumes or distances in fresh cadavers are significantly greater than those in formalin-fixed cadavers.21 We are, therefore, concerned that the benefits associated with this technique may not translate into clinical application.57 Our team routinely uses frontotemporal craniotomy with zygomatic osteotomy

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Figure 5. Internal maxillary artery (Max. A)eradial arteryeinsular segment of the middle cerebral artery (M2) bypass for the management of distal internal carotid artery (ICA) aneurysm. (Published with permission from Li Cai). Ant., anterior; Radial A, radial artery; Temp. A, temporal artery; O.N, optic nerve.

without sacrificing the infratemporal crest to harvest the IMA (Figure 3).7-12 The infratemporal crest can be effectively used as a reference point to confirm the accurate position of the IMA. Because of the high percentage of Asians with a superficial IMA pattern, the pterygoid segment of the IMA can be easily exposed between the inferior neck of the mandible and the sphenomandibular ligament. Alternatively, the pterygoid IMA can be easily observed after blunt dissection between the lower head of the LPM and its superficial connective tissue (buccal fat pad). Even if the artery is beneath the LPM, it can still be located after separating the inferior border of the LPM through this wider exposure.23 Small bleeders inside the fat pad are well controlled by bipolar electrocauterization. However, there are a few drawbacks to this dissection modality. First, there are no measured data to localize the pterygoid IMA in the ITF because of its anatomic variations, making dissection empirical. Second, in the case of an IMA with a deep pattern, the LPM and its surrounding structures may be compromised in the vertical trajectory.

Third, the lateral middle fossa, which is the roof of the ITF, complicates proximal end-to-end anastomosis. The surgical trajectory and the extent of the first craniectomy depend on the type of IMA. We recommend obtaining preoperative images to distinguish the IMA pattern in relation to the LPM. Dissection of the medial-type IMA can be performed using the lateral triangle middle fossa approach from the superior view. Conversely, dissection of the lateral-type IMA can be performed using a pterional approach with a zygomatic osteotomy. PREOPERATIVE EVALUATION OF THE IMA The importance of anatomic variations in the dissection and exposure of the IMA cannot be overstated.24 Confirming the course of the IMA preoperatively is strongly recommended for planning the surgical approach and minimizing the risk of intraoperative or postoperative hemorrhage.20 Various imaging techniques, including Doppler ultrasonography (DUS), computed tomography angiography (CTA), and enhanced magnetic resonance imaging (MRI), can help identify the IMA course

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and increase the efficiency of the technique used for its exposure. DUS is a convenient, flexible, and less costly imaging modality with an acceptable diagnostic value and multislice scanning capacity. DUS also lacks a strong magnetic field and ionizing radiation.17 Arimoto et al.17 used DUS to determine the location of the IMA before orthognathic surgery with an acceptable accuracy of 92%. However, the degree of penetration with DUS can be influenced by air and the characteristics of the bone structures.56 In addition, it is difficult to obtain measurements of the long distance from the skin and visualize the medial pattern of the IMA using ultrasonography.58 CTA is another useful tool that provides a detailed overview of the vascular relationships.18 CTA allows for the visualization of tissues measuring 1 mm in diameter and can predict the location, length, and course of the vessels. CTA has been used in preoperative planning for treating maxillary artery lesions and orthognathic surgery.15,19 Similarly, neurosurgical investigators use CTA to show the basic IMA anatomy and the variations of its branches in the intracranial and extracranial areas19,21 and measure the diameter and course of the IMA before performing a bypass surgery.3,18,31 At SanBo Brain Hospital, we routinely use CTA to evaluate the diameter, length, and patterns of the pterygoid IMA before an IMA bypass. However, an obvious disadvantage of a CT scan is the higher dose of radiation exposure.17 MRI has the advantages of a high spatial resolution and direct multiplanar imaging. The maxillary vessels are usually visualized as flow voids on the medial side of the condyle and the inferior region of the LPM.17 The absence of ionizing radiation and the advantage of directly visualizing the soft tissue structures encourage the widespread use of MRI in dentistry and oral surgery.17 However, MRI applications may be limited because of its reduced availability, long examination time, and high cost, making it less suitable as a screening tool. CTA may the first choice for estimating the characteristics of the IMA, and DUS may be considered a rapid preliminary diagnostic tool that is used as an alternative modality to complement CTA.17,59 MRI should be used in cases in which the IMA cannot be detected by DUS.17

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Table 3. Published Cases of Internal Maxillary Artery Bypass Procedures Intracranial Disease

Reference

Proximal Anastomosis

IMA Exposure

Number Steno-Occlusive of Cases Aneurysm Disease Tumor

Approach

Vrionis et al., 199622

1

1

0

0

ZO and MF resection

Abdulrauf et al., 20111

1

1

0

0

Shi et al., 20117

3

2

1

Nossek et al., 20146

4

3

Nossek et al., 20165

4

Wang et al., 201610

Segment Landmark of IMA Graft Fashion NA

Recipient Artery

Graft Patency (%)

3rd

In situ IMA

NA

Supraclinoid internal carotid artery

NA

Anteromedial Anterior MF to FR

3rd

RA

S-E

M3

0

Pt with ZO

BFP and LPM

2nd

RA

E-E

M2, PCA

1

0

SC-IC

Between FR and FO

2nd

RA (1) S-E (1) MCA CV (3) E-E (3)

100

4

0

0

SC-IC

Between FR and FO

2nd

RA (2) S-E (1) MCA CV (4) E-E (3)

100

2

0

0

2

Pt with ZO

BFP and LPM

2nd

RA

E-E

M2

Yu et al., 201612

31

0

31

0

Pt with ZO

BFP and LPM

2nd

RA

E-E

MCA

Wang et al., 20178

7

7

0

0

Pt with ZO

BFP and LPM

2nd

RA

E-E

M2, cortical segment of the middle cerebral artery, ambient segment of the posterior cerebral artery, calcarine segment of the posterior cerebral artery

Liu et al., 20174

1

1

0

0

Pt with ZO

BFP and LPM

2nd

RA

E-E

M2

Patent

Feng et al., 20173

1

0

0

0

Lateral triangle MF

Between FR and FO

2nd

RA

E-E

M2

Patent

Wang et al., 20179

7

7

0

0

Pt with ZO

BFP and LPM

2nd

RA

E-E

M2, M3

100

Wang et al., 201711

32

32

0

0

Pt with ZO

BFP and LPM

2nd

RA

E-E

Posterior communicating segment of the internal carotid artery, MCA, PCA

90.6

Patent 100

100 96.80 100

ZO, zygomatic osteotomy; MF, middle fossa; NA, not applicable; FR, foramen rotundum; RA, radial artery; S-E, side-to-end; M3, opercular segment of the middle cerebral artery; Pt, pterional; BFP, buccal fat pad; LPM, lateral pterygoid muscle; E-E, end-to-end; M2, insular segment of the middle cerebral artery; PCA, posterior cerebral artery; SC-IC, subcranial-intracranial; FO, foramen ovale; CV, cephalic vein; MCA, middle cerebral artery.

OPTIMAL GRAFT SELECTION IN IMA BYPASS PROCEDURES The selection of the graft depends on the blood flow required through the bypass to adequately supply the territories of the occluded vessel and the status of the recipient and donor vessels related to the lesion.60 Grafts have been harvested from the RA, SV, cephalic vein (CV), and STA in IMA bypass surgery. Considering the RA as the conduit for bypass, patients must pass the Allen

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test to ensure that there are no ischemic events in the hand after harvesting the RAG.5 The potential advantages of the RA as a graft conduit include its ease of harvesting, good long-term patency, rare complications after harvesting, and well-matched thickness to the recipient artery (MCA, P2) in physiologic structure and size, which improves the ease of constructing the anastomosis.13,18,28,29,60-64 Such a bypass provides sufficient blood flow

when the mean diameters of these arteries are greater than 2 mm.28 The SVG is another commonly used graft in bypass surgery. The SV has a thicker wall than the intracranial vessels, and because of the high flow that runs through it, the SV is more prone to kinking at the distal anastomotic site. In addition, the anastomosis may be technically more difficult to perform with the SV.64 Shi et al.65 found that venous grafts undergo higher oxidative stress, have oxidized epitopes, and accumulate low-

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density lipoprotein. In addition, proatherogenic changes have been found in venous grafts early after revascularization, creating conditions for the development of graft thrombosis. These findings comprise the biological rationale for using arterial conduits for cerebral revascularization.64 Nonetheless, SVGs are used in certain circumstances, such as when the RA is either an unsuitable vessel or the RA has become occluded during the perioperative period.64 In addition, in children younger than 12 years, the SVG is the only alternative because the diameter of the RA graft is too small.64 Nossek et al.5,6 introduced a new graft conduit, the CV graft (CVG), for IMA bypass. This subcutaneous vein is easily manipulated in the volar forearm between the proximal cubital fossa, where the median cubital vein is confluent with the CV and the distal wrist.5 The CV has few valves, rare branches, and infrequent complications after upper extremity incision.6 In addition, this vessel is more easily harvested than the wider SVG and has an excellent diameter for communicating with the donor IMA and recipient M1/M2 segment of MCA.5,6,66 However, some investigators67 are concerned about the poor patency rate of this venous graft and prefer not to use it because the vein is thin walled and easily damaged. Purohit et al.67 reported that only 50% of the grafts remain patent after a cardiovascular bypass procedure at 3-year follow-up. However, Nossel et al.5 suggested that when CVGs are used as very short segments, such low rates can be avoided. The STA is the most commonly used donor vessel for bypass. The notion of using the STA as a graft in the IMA bypass procedure was proposed by Üstün et al.29 This technique obviates cervical and arm incisions, avoids potential technical and vascular complications, and decreases the length of the procedure.3 However, the main diameters of the STA trunk range from 1.9 to 2.3 mm, which, compared with that of the IMA (2.4e3.46 mm), provide less blood flow.3,16,24,25,27,30,31,48,68,69 Because the radius of the artery contributes exponentially to the flow rate, the flow rates for this bypass are likely to be closer to those of a standard STA-MCA bypass.3 Recently, Feng et al.3,68 showed the feasibility of using an STA interposition graft between the IMA and the MCA. These

INTERNAL MAXILLARY ARTERY BYPASS

investigators reported that a 7.5-cm STA graft can be obtained beginning 1.5 cm below the zygomatic arch. The average length of the STA graft required in a cadaveric study was 5.6 cm. However, this bypass modality seems questionable because of the varying STA lengths. The STA has been reported to average 31.7 mm from the zygoma to its bifurcation,69 with an additional length of 5e 10 mm gained below the zygoma.29 When more than 5 cm of the STA is harvested, the graft is likely to extend beyond the bifurcation of the STA into the frontal and parietal branches.3 The distance from the subtemporal fossa at the level of the pterygoid segment to the sylvian fissure is between 7 and 9 cm.5 However, even after harvesting a 7.5-cm STA graft, the artery seems to shorten during the virtual bypass procedure as a result of arterial vasospasm. Therefore, we are concerned that the benefits may not translate into clinical application, and a free-tension IMA bypass may be required. These findings support that the RA should be the first graft choice for an IMA bypass procedure. CVG and SVG may be valid options for patients who fail the Allen test in both hands or have a poor quality or inadequate RA. The STA trunk is not recommended as a graft vessel because of its poor diameter and short length, which could lead to a low-flow bypass. SURGICAL OUTCOME OF IMA BYPASS The IMA bypass was first considered a surgical intervention for managing a meningioma that involved the cavernous sinus and the ITF and had clivus chordomas and glomus tumors infiltrating the ICA.22 Wang et al.10 reported 2 cases of IMA bypass that were performed to manage a recurrent craniopharyngioma concurrent with symptomatic fusiform dilation of the ICA. Both cases occurred more than 5 years after the primary resection of the tumor. To resect the suprasellar lesion and the dilated artery in a single operation, the investigators performed an IMA bypass to better expose the tumor, after resection of the dilated artery. Postoperative neuroimaging confirmed the total resection of both lesions and the graft patency. The patients’ neurologic function was intact at the final follow-up.

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In contrast to its rare use in skull base neurosurgery, IMA bypass has been used for the management of both adult and pediatric complex intracranial aneurysms in multiple case series.1-4,6-9,11 Vrionis et al.22 initially reported a clinical case of a tension-free in situ IMA-supraclinoid ICA bypass surgery with an SVG to treat a fusiform petrous ICA aneurysm. However, no details were provided regarding the surgical approach, the patient characteristics, or the radiologic images of the aneurysm. More than a decade later, Abdulrauf et al.1 described a clinical case of a giant fusiform ICA aneurysm that was treated with a high-flow EC-IC bypass using the pterygopalatine IMA as the donor vessel. Bilateral end-to-side anastomosis connecting the IMA to the opercular segment of the middle cerebral artery (M3) using an RAG was performed, and a patent graft artery was confirmed intraoperatively. The patient achieved a favorable outcome at the 3-week follow-up without any new neurologic deficits. However, this bypass modality has some technical disadvantages. First, an end-toside anastomosis is needed below the level of the middle fossa floor, which is technically demanding.3 Second, the diameter of M3 is not appropriate for use in an anastomosis with RAG and IMA. Third, the IMA must be pulled out of the pterygopalatine fossa into the middle cranial fossa to perform an anastomosis between the IMA and RAG.13 In the same year, our senior author (X.S.)7 described another IMA bypass using RAG to treat a giant basilar trunk aneurysm after frontotemporal craniotomy with zygomatic osteotomy. The patient’s postoperative course was uneventful, and a favorable outcome was observed at the 6-year followup.11 In 2014, Nossek et al.6 further explored the IMA to MCA bypass using a CVG to treat giant MCA aneurysms in 3 patients. All grafts were patent postoperatively. One patient experienced postoperative brain swelling and underwent a decompressive craniotomy. His neurologic status recovered to the preoperative baseline. Two years later, investigators from the same group reported another 4 cases of IMA bypass for the management of complex MCA aneurysms.5 All venous grafts were patent postoperatively but 1 patient had a venous infarction on postoperative day 1 and subsequently died of a refractory increase of intracranial pressure. The remaining 3 patients recovered to their preoperative neurologic status. Recently, our team

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LITERATURE REVIEW LONG WANG ET AL.

reported 46 IMA bypasses using RAG for the treatment of complex cerebral aneurysms, including 7 cases of giant serpentine/ dolichoectatic aneurysms,9 32 cases of giant intracranial aneurysms,8 and 7 cases of complex pediatric aneurysms.11 The postoperative angiography reported good filling of the graft with a robust distal flow in 93.5% (43/46) of the cases, but 4 patients died by the final follow-up. One pediatric patient who was transferred to our institution for the management of a traumatic recurrent giant ICA aneurysm died of multiple-organ failure 6 months after the procedure. Another 3 adults died of diseases unrelated to the surgical procedure. Liu et al.4 reported a case of bilateral giant aneurysms that were treated with an initial high-flow external carotid artery-SVG-MCA and a novel IMA-RAMCA bypass spanning 8 years. The postoperative neurologic function was intact, with a patent RAG. Feng et al.3 reported another case of a standard pterygoid IMARA-M2 bypass for the management of a recurrent MCA aneurysm. The intraoperative and postoperative angiograms confirmed the graft patency. Despite the controversy surrounding the optimal treatment strategies for cerebral occlusive diseases, several reports have described use of the IMA bypass procedure to manage these disorders. The senior author (X.S.) initially described 2 cases of proximal MCA occlusive diseases that were treated with an IMA-RAG-M2 bypass.7 In addition, postoperative angiography showed the graft patency with refilling of the MCA territory. At final follow-up, both patients had returned to work with intact neurologic function. Nossek et al.6 described another case of ICA occlusion caused by resection of a cervical neurofibroma. An IMA bypass was performed for flow augmentation in the hypoperfused hemisphere. In 2016, our team reported a large-scale study of IMA bypass for the management of chronic arterial-sclerotic severe stenosis or occlusion of the ICA or MCA (Figures 4 and 5).12 Thirty-one patients were involved in the series, and the cerebral perfusion status was measured preoperatively and postoperatively. The postoperative graft patency and improved hemodynamic status were recorded in 96.8% of the patients. All patients, except for one, experienced stable or improved neurologic function (Table 3).

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CONCLUSIONS Because of the increasing momentum toward the use of neuroendovascular and endoscopic techniques, cerebral revascularization has faded during the past few years. However, in cases with complex cerebral lesions, bypass surgery, particularly this novel IMA bypass modality, remains a vital armamentarium for neurosurgery. ACKNOWLEDGMENTS Long Wang expresses his sincere gratitude to Xiang’en Shi for the constant encouragement and guidance at Sanbo Brain Hospital. He also thanks his beloved parents for their gracious consideration and great confidence during his entire 28 years of life. Finally, he appreciates the invaluable support received from his wife, Lujun Jing. REFERENCES 1. 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 bypass. Neurosurgery. 2011;68:804-808. 2. Assam JH, Quinn TH, Militsakh ON. The maxillary artery as a recipient vessel option for complex midface and anterior skull base microsurgical repair: a cadaveric study. Microsurgery. 2017;37: 611-617. 3. Feng X, Meybodi AT, Rincon-Torroella J, ElSayed IH, Lawton MT, Benet A. Surgical technique for high-flow internal maxillary artery to middle cerebral artery bypass using a superficial temporal artery interposition graft. Oper Neurosurg. 2017;13:246-257. 4. Liu Y, Shi X, Liu F, Sun Y, Qian H, Lei T. Bilateral cavernous carotid aneurysms treated by two-stage extracranial-intracranial bypass followed by parent artery occlusion: case report and literature review. Acta Neurochir (Wien). 2017;159:1693-1698. 5. Nossek E, Costantino PD, Chalif DJ, Ortiz RA, Dehdashti AR, Langer DJ. Forearm cephalic vein graft for short, “middle”-flow, internal maxillary artery to middle cerebral artery bypass. Oper Neurosurg. 2016;12:99-105.

8. Wang L, Lu S, Qian H, Shi X. Internal maxillary artery bypass with radial artery graft treatment of giant intracranial aneurysms. World Neurosurg. 2017;105:568-584. 9. Wang L, Lu S, Qian H, Shi X. Internal maxillary bypass for complex pediatric aneurysms. World Neurosurg. 2017;103:395-403. 10. Wang L, Shi X, Liu F, Qian H. Bypass surgery to treat symptomatic fusiform dilation of the internal carotid artery following craniopharyngioma resection: report of 2 cases. Neurosurg Focus. 2016; 41:E17. 11. Wang L, Shi X, Qian H. 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. 2017;40:319-328. 12. Yu Z, Shi X, Qian H, Liu F, Zhou Z, Sun Y, et al. 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. 2016;38: 420-428. 13. Eller JL, Sasaki-Adams D, Sweeney JM, Abdulrauf SI. Localization of the internal maxillary artery for extracranial-to-intracranial bypass through the middle cranial fossa: a cadaveric study. J Neurol Surg B Skull Base. 2012;73:48-53. 14. Feng X, Lawton MT, Rincon-Torroella J, ElSayed IH, Meybodi AT, Benet A. The lateral triangle of the middle fossa: surgical anatomy and a novel technique for transcranial exposure of the internal maxillary artery. Oper Neurosurg. 2016;12: 106-111. 15. Tanoue S, Kiyosue H, Mori H, Hori Y, Okahara M, Sagara Y. Maxillary artery: functional and imaging anatomy for safe and effective transcatheter treatment. Radiographics. 2013;33:e209-224. 16. Uysal II, Buyukmumcu M, Dogan NU, Seker M, Ziylan T. Clinical significance of maxillary artery and its branches: a cadaver study and review of the literature. Int J Morphol. 2011;29:1274-1281. 17. Arimoto S, Hasegawa T, Okamoto N, Shioyasono A, Tateishi C, Akashi M, et al. Determining the location of the internal maxillary artery on ultrasonography and unenhanced magnetic resonance imaging before orthognathic surgery. Int J Oral Maxillofac Surg. 2015;44:977-983. 18. Akiyama O, Güngör A, Middlebrooks EH, Kondo A, Arai H. Microsurgical anatomy of the maxillary artery for extracranial-intracranial bypass in the pterygopalatine segment of the maxillary artery [e-pub ahead of print] Clin Anat. 2017. https://doi.org/10.1002/ca.22926.

6. Nossek E, Costantino PD, Eisenberg M, Dehdashti AR, Setton A, Chalif DJ, et al. Internal maxillary artery-middle cerebral artery bypass: infratemporal approach for subcranial-intracranial (SC-IC) bypass. Neurosurgery. 2014;75:87-95.

19. Gulses A, Oren C, Altug HA, Ilica T, Sencimen M. Radiologic assessment of the relationship between the maxillary artery and the lateral pterygoid muscle. J Craniofac Surg. 2012;23:1465-1467.

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20. Hussain A, Binahmed A, Karim A, Sandor GK. Relationship of the maxillary artery and lateral pterygoid muscle in a Caucasian sample. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2008;105: 32-36.

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21. Hwang SH, Joo YH, Seo JH, Kang JM. Proximity of the maxillary artery to the mandibular ramus: an anatomic study using three-dimensional reconstruction of computer tomography. Clin Anat. 2014;27:691-697.

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36. Kijima N. On distribution of the artery over the mandibular joint. Med J Kagoshima Univ. 1932;10: 71-83.

23. Wang CP, Yang TL, Ko JY, Lou PJ. Ligation of the internal maxillary artery to reduce intraoperative bleeding during total maxillectomy. Laryngoscope. 2007;117:1978-1981. 24. Yagmurlu K, Kalani MYS, Martirosyan NL, SafaviAbbasi S, Belykh E, Laarakker AS, et al. Maxillary artery to middle cerebral artery bypass: a novel technique for exposure of the maxillary artery. World Neurosurg. 2017;100:540-550. 25. Arbag H, Cicekcibasi AE, Uysal II, Ustun ME, Buyukmumcu M. Superficial temporal artery graft for bypass of the maxillary to proximal middle cerebral artery using a transantral approach: an anatomical and technical study. Acta Otolaryngol. 2005;125:999-1003. 26. Arbag H, Ustun ME, Buyukmumcu M, Cicekcibasi AE, Ulku CH. A modified technique to bypass the maxillary artery to supraclinoid internal carotid artery by using radial artery graft: an anatomical study. J Laryngol Otol. 2005;119:519-523. 27. Büyükmumcu M, Üstün ME, Seker M, Karabulut AK, Uysal YY. Maxillary-to-petrous internal carotid artery bypass: an anatomical feasibility study. Surg Radiol Anat. 2003;25:368-371. 28. Ulku CH, Ustun ME, Buyukmumcu M, Cicekcibasi AE, Ziylan T. Radial artery graft for bypass of the maxillary to proximal posterior cerebral artery: an anatomical and technical study. Acta Otolaryngol. 2004;124:858-862. 29. Üstün ME, Büyükmumcu M, Ulku CH, Cicekcibasi AE, Arbag H. Radial artery graft for bypass of the maxillary to proximal middle cerebral artery: an anatomic and technical study. Neurosurgery. 2004;54:667-671. 30. Karabulut AK, Üstün ME, Uysal II, Salbacak A. Saphenous vein graft for bypass of the maxillary to supraclinoid internal carotid artery: an anatomical short study. Ann Vasc Surg. 2001;15:548-552. 31. Alvernia JE, Hidalgo J, Sindou MP, Washington C, Luzardo G, Perkins E, et al. The maxillary artery and its variants: an anatomical study with neurosurgical applications. Acta Neurochir (Wien). 2017; 159:655-664. 32. Thomson A. Report of the committee of collective investigation of the anatomical society of great Britain and Ireland for the year 1889-90. J Anat Physiol. 1890;25:89-101. 33. Lauber H. Ueber einige Varietaten im Verlaufe der Arteria maxillaris interna. Anat Anz. 1901;19: 444-448 [in German]. 34. Adachi B. Das Arteriensystem der Japaner. Kyoto, Japan: Maruzen/Kaiserlich-Japanische Universität; 1928 [in German].

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Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Received 8 January 2018; accepted 26 February 2018 Citation: World Neurosurg. (2018) 113:320-332. https://doi.org/10.1016/j.wneu.2018.02.158 Journal homepage: www.WORLDNEUROSURGERY.org

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