Anatomical Assessment of the Temporopolar Artery for Revascularization of Deep Recipients

Anatomical Assessment of the Temporopolar Artery for Revascularization of Deep Recipients Abstract BACKGROUND Intracranial–intracranial and extracranial–intracranial bypass options for revascularization of deep cerebral recipients are limited and technically demanding. OBJECTIVE To assess the anatomical feasibility of using the temporopolar artery (TPA) for revascularization of the anterior cerebral artery (ACA), posterior cerebral artery (PCA), and superior cerebellar arteries (SCA). METHODS Orbitozygomatic craniotomy was performed bilaterally on 8 cadaveric heads. The cisternal segment of the TPA was dissected. The TPA was cut at M3-M4 junction with its proximal and distal calibers and the length of the cisternal segment measured. Feasibility of the TPA-A1-ACA, TPA-A2-ACA, TPA-SCA, and TPA-PCA bypasses were assessed. RESULTS A total of 17 TPAs were identified in 16 specimens. The average distal TPA caliber was 1.0 ± 0.2 mm, and the average cisternal length was 37.5 ± 9.4 mm. TPA caliber was ≥ 1.0 mm in 12 specimens (70%). The TPA-A1-ACA bypass was feasible in all specimens, whereas the TPA reached the A2-ACA, SCA, and PCA in 94% of specimens (16/17). At the point of anastomosis, the average recipient caliber was 2.5 ± 0.5 mm for A1-ACA, and 2.3 ± 0.7 mm for A2-ACA. The calibers of the SCA and PCA at the anastomosis points were 2.0 ± 0.6 mm, and 2.7 ± 0.8 mm, respectively. CONCLUSION The TPA-ACA, TPA-PCA, and TPA-SCA bypasses are anatomically feasible and may be used when the distal caliber of the TPA stump is optimal to provide adequate blood flow. This study lays foundations for clinical use of the TPA for ACA revascularization in well-selected cases. Anterior cerebral artery, Complex aneurysm, Intracranial–intracranial bypass, Oculomotor-tentorial triangle, Orbitozygomatic approach, Posterior cerebral artery, Superior cerebellar artery ABBREVIATIONS ABBREVIATIONS ACA anterior cerebral artery ACoA anterior communicating artery ATA anterior temporal artery EC extracranial IC intracranial MCA middle cerebral artery PCA posterior cerebral artery SCA superior cerebellar arteries TPA temporopolar artery UPC upper posterior circulation STA superficial temporal artery Although rare, complex intracranial (IC) aneurysms are challenging because they may require a bypass procedure as part of the treatment strategy.1,2 The technical challenge of cerebral bypass is accentuated with deep recipients, such as those of the anterior cerebral artery (ACA) and the upper posterior circulation (UPC)—consisting of posterior cerebral artery (PCA) and superior cerebellar artery (SCA).2-12 This challenge is mainly due to the deep location of the recipient arteries surrounded by multiple eloquent neurovascular structures. The side-to-side A3-A3 bypass is probably the most common revascularization procedure for the ACA.4,6-11,13,14 The A3-A3 bypass is technically demanding both because of the deep location and the inherent challenge of a side-to-side anastomosis that requires completing an intraluminal suture line.2,15 Additionally, such a construct entails potential ischemia of the donor ACA territory. Other bypass options for revascularizing the ACA in cases of complex ACA aneurysms are limited, such as the use of interposition grafts between an IC or an extracranial (EC) donor and the ACA16,17, or the use of other adjacent IC donors, such as the frontopolar and orbitofrontal arteries.11,14 Similarly, few options are available for revascularization of the UPC. The superficial temporal artery (STA) has been used for this purpose.18-21 However, the STA may not have an optimal caliber or may be unavailable due to previous operative injury. The occipital artery can also be used, but when the anterior and lateral mesencephalic segments of the UPC vessels are targeted, problems may arise with rerouting the occipital artery to reach target vessels.22 An interposition graft between the external carotid artery and the UPC vessels is another EC-IC option. Apart from the need for remote incisions and vulnerability of the graft to external trauma, caliber mismatch and the increased risk of cerebral hyperperfusion syndrome or graft occlusion are important potential problems with EC-IC bypasses.2,4,12,23-27 As mentioned, IC-IC bypasses have an important limitation, which is the risk of ischemia to the donor artery territory. The IC vessels are end arteries that generally supply eloquent regions of the brain. However, IC-IC bypasses are attractive because of several advantages, such as: (1) sparing the patient additional incisions to expose the donor and/or graft vessels; (2) requiring fewer anastomoses; (3) protection by the calvarium; and (4) good caliber match between the donor and the recipient.2-4 Therefore, the identification of potential IC donors with good caliber and reach to recipient territories, while supplying a noneloquent area would provide valuable bypass options. The temporopolar artery (TPA) is the most proximal branch of the middle cerebral artery (MCA), feeding the pole and lateral aspect of the anterior temporal lobe,28-30 which are noneloquent areas.2,31-33 However, its use has not been studied as a donor to revascularize deep recipients. The purpose of the current study is to assess the potential of the TPA for revascularization of the ACA and UPC (Figure 1). FIGURE 1. View largeDownload slide Artist's Illustration showing the A, TPA-ACA and B, TPA-PCA bypass concepts. ACA = anterior cerebral artery; AChA = anterior choroidal artery; ACoA = anterior communicating artery; ATA = anterior temporal artery; BA = basilar artery; CN = cranial nerve; ICA = internal carotid artery; PCoA = posterior communicating artery; PCA = posterior cerebral artery. TPA = temporopolar artery. FIGURE 1. View largeDownload slide Artist's Illustration showing the A, TPA-ACA and B, TPA-PCA bypass concepts. ACA = anterior cerebral artery; AChA = anterior choroidal artery; ACoA = anterior communicating artery; ATA = anterior temporal artery; BA = basilar artery; CN = cranial nerve; ICA = internal carotid artery; PCoA = posterior communicating artery; PCA = posterior cerebral artery. TPA = temporopolar artery. METHODS The present study did not require IRB approval as it only involved cadaveric specimens and retrospective review of de-identified cerebral angiograms. Craniotomy and Preparation of the TPA Eight cadaveric heads (16 sides) were prepared for cadaveric dissection using our customized embalming formula.34 Using a head clamp (Mizuho America, Union City, California), each head was positioned classically for a pterional-orbitozygomatic approach. After completing a standard orbitozygomatic craniotomy, the dura was opened using a C-shaped incision (Figure 2A). Using a surgical microscope (Carl Zeiss AG, Oberkochen, Germany), the Sylvian fissure was widely split, and the branching pattern of the MCA was assessed to find the TPA. The origination patterns of TPA and anterior temporal artery (ATA) were recorded with regard to the MCA bifurcation (Figure 2B and 2C). Using a hand-held caliper, TPA caliber was recorded at origin and at M3-M4 junction. Next, the cisternal segment of the TPA (from origin to M3-M4 junction) was prepared by dividing small branches tethering it to the adjacent temporal lobe. However, any branches entering the anterior perforated substance were preserved. FIGURE 2. View largeDownload slide Cadaveric dissection showing the TPA-ACA bypass. A, a right pterional-orbitozygomatic craniotomy is performed and the sylvian fissure is split. B, the ATA and TPA are identified using the landmark of pars triangularis opposite to which ATA is most frequently found. C, the cisternal segment of the ATA and TPA are released to identify the origination pattern of these vessels from the MCA. White arrow points to the MCA bifurcation. The ATA and TPA originate from a common trunk which arises as an early branch proximal to the MCA bifurcation. D, the carotid and lamina terminalis cisterns are opened to expose the ipsilateral ACA. E, the TPA is mobilized towards the ACA after it is divided at the M3-M4 junction, and an end-to-side anastomosis is completed. F, overall view of the TPA-ACA bypass with the ATA (small white arrow) being untouched. ACA = anterior cerebral artery; ATA = anterior temporal artey; ICA = internal carotid artery; n. = nerve; Rt. = right; Orb. = orbitalis; Tri. = triangularis; TPA = temporopolar artery. FIGURE 2. View largeDownload slide Cadaveric dissection showing the TPA-ACA bypass. A, a right pterional-orbitozygomatic craniotomy is performed and the sylvian fissure is split. B, the ATA and TPA are identified using the landmark of pars triangularis opposite to which ATA is most frequently found. C, the cisternal segment of the ATA and TPA are released to identify the origination pattern of these vessels from the MCA. White arrow points to the MCA bifurcation. The ATA and TPA originate from a common trunk which arises as an early branch proximal to the MCA bifurcation. D, the carotid and lamina terminalis cisterns are opened to expose the ipsilateral ACA. E, the TPA is mobilized towards the ACA after it is divided at the M3-M4 junction, and an end-to-side anastomosis is completed. F, overall view of the TPA-ACA bypass with the ATA (small white arrow) being untouched. ACA = anterior cerebral artery; ATA = anterior temporal artey; ICA = internal carotid artery; n. = nerve; Rt. = right; Orb. = orbitalis; Tri. = triangularis; TPA = temporopolar artery. TPA-ACA and TPA-UPC Bypasses Using the surgical microscope, the carotid, chiasmatic, and lamina terminalis cisterns were opened to expose the ipsilateral A1-ACA, anterior communicating artery (ACoA), contralateral A1-ACA, and their adjacent branches. Also, the paired A2-ACAs were exposed after resecting a small portion of the ipsilateral gyrus rectus. Next, the TPA was divided at its opercular-cortical (M3-M4) junction and mobilized medially to reach the ACoA complex. The feasibility of completing an end-to-side TPA-ACA anastomosis without undue tension on the TPA stump was assessed at distal-most points on ipsilateral A1- and A2-ACA (Figure 2D-2F). When the anastomosis was deemed feasible, the caliber of the ACA was recorded at the point of anastomosis on A1 and A2 segments. The distance between the anastomosis point on A1-ACA was measured from the bifurcation of the internal carotid artery, and the distance between the anastomosis point on A2-ACA was measured from A1 to A2 junction. Distance measurements were accomplished using a stereotactic navigation system (Stryker, Kalamazoo, Michigan). Next, the feasibility of TPA-UPC bypass was assessed. To expose the UPC, the pretemporal corridor was developed by retracting the temporal lobe laterally and posteriorly. The carotid, chiasmatic, crural, and ambient cisterns were opened to expose the basilar apex, as well as the ipsilateral P1 and P2 segments of PCA, and the s1 and s2 segments of SCA. Next, the TPA was mobilized posteriorly to reach the SCA and PCA within a triangle formed between the oculomotor nerve medially, and the tentorial edge laterally (Figure 3). The feasibility of completing an end-to-side anastomosis without undue tension on the TPA was assessed for the most distal accessible point on the PCA and SCA inside the oculomotor-tentorial triangle. Care was taken not to manipulate the oculomotor nerve. The calibers of the PCA and SCA at anastomosis points were recorded. The lengths of the PCA and SCA segments between their origin on the basilar artery and the anastomosis points were also measured using the frameless stereotactic navigation system (Stryker). FIGURE 3. View largeDownload slide Cadaveric depiction of TPA-SCA bypass. A, exposure and release of cisternal segment of the TPA through a right transsylvian approach. B, TPA-SCA bypass completed. ATA = anterior temporal artery; CN = cranial nerve; ICA = internal carotid artery; MCA = middle cerebral artery; n. = nerve; TPA = temporopolar artery. FIGURE 3. View largeDownload slide Cadaveric depiction of TPA-SCA bypass. A, exposure and release of cisternal segment of the TPA through a right transsylvian approach. B, TPA-SCA bypass completed. ATA = anterior temporal artery; CN = cranial nerve; ICA = internal carotid artery; MCA = middle cerebral artery; n. = nerve; TPA = temporopolar artery. RESULTS Branching Pattern of TPA A total of 17 TPAs were found (1 specimen had duplicate TPAs). The average TPA caliber was 1.3 ± 0.3 mm at its origin and 1.0 ± 0.2 mm at M3-M4 junction. Twelve TPAs (70%) had a caliber ≥1.0 mm at the M3-M4 junction. The average cisternal length of the TPA was 37.5 ± 9.4 mm (range: 19-52.1 mm). Five different patterns of TPA origination with regards to MCA bifurcation and the origin of the ATA were noted (Table 1 and Figure 4). Using the 1-way analysis of variance statistical method, no statistically significant difference was found between the cisternal lengths of different TPA subtypes (P = .94). However, TPA type I had the shortest, and TPA type V had the longest average cisternal segment lengths (Table 1). FIGURE 4. View largeDownload slide Artist's illustration showing branching patterns of TPA relative to the middle cerebral artery bifurcation and origin of the ATA. A, Type I: ATA and TPA arise from a common stem distal to MCA bifurcation. B, Type II: ATA and TPA arise from a common stem proximal to MCA bifurcation. C, Type III: ATA and TPA arise separately distal to MCA bifurcation. D, Type IV: ATA and TPA arise separately proximal to MCA bifurcation. E, Type V: TPA arises proximal and ATA arises distal to MCA bifurcation. ATA = anterior temporal artery; TPA = temporopolar artery. FIGURE 4. View largeDownload slide Artist's illustration showing branching patterns of TPA relative to the middle cerebral artery bifurcation and origin of the ATA. A, Type I: ATA and TPA arise from a common stem distal to MCA bifurcation. B, Type II: ATA and TPA arise from a common stem proximal to MCA bifurcation. C, Type III: ATA and TPA arise separately distal to MCA bifurcation. D, Type IV: ATA and TPA arise separately proximal to MCA bifurcation. E, Type V: TPA arises proximal and ATA arises distal to MCA bifurcation. ATA = anterior temporal artery; TPA = temporopolar artery. TABLE 1. Origination Patterns of TPA With Regards to MCA Bifurcation and the Origin of the ATA in 17 TPAs. TPA origination type Definition Frequency (%) Average cisternal length (mm) I TPA originates distal to MCA bifurcation, with a common stem with ATA 4 (24%) 34.3 II The originates proximal to MCA bifurcation, with a common stem with ATA 4 (24%) 38.1 III TPA and ATA originate separately distal to MCA bifurcation 2 (11%) 34.8 IV TPA and ATA originate separately proximal to MCA bifurcation 3 (17%) 38.1 V TPA originates proximal and ATA originates distal to MCA bifurcation 4 (24%) 41.0 TPA origination type Definition Frequency (%) Average cisternal length (mm) I TPA originates distal to MCA bifurcation, with a common stem with ATA 4 (24%) 34.3 II The originates proximal to MCA bifurcation, with a common stem with ATA 4 (24%) 38.1 III TPA and ATA originate separately distal to MCA bifurcation 2 (11%) 34.8 IV TPA and ATA originate separately proximal to MCA bifurcation 3 (17%) 38.1 V TPA originates proximal and ATA originates distal to MCA bifurcation 4 (24%) 41.0 ATA = anterior temporal artery; MCA = middle cerebral artery; TPA = temporopolar artery. View Large TABLE 1. Origination Patterns of TPA With Regards to MCA Bifurcation and the Origin of the ATA in 17 TPAs. TPA origination type Definition Frequency (%) Average cisternal length (mm) I TPA originates distal to MCA bifurcation, with a common stem with ATA 4 (24%) 34.3 II The originates proximal to MCA bifurcation, with a common stem with ATA 4 (24%) 38.1 III TPA and ATA originate separately distal to MCA bifurcation 2 (11%) 34.8 IV TPA and ATA originate separately proximal to MCA bifurcation 3 (17%) 38.1 V TPA originates proximal and ATA originates distal to MCA bifurcation 4 (24%) 41.0 TPA origination type Definition Frequency (%) Average cisternal length (mm) I TPA originates distal to MCA bifurcation, with a common stem with ATA 4 (24%) 34.3 II The originates proximal to MCA bifurcation, with a common stem with ATA 4 (24%) 38.1 III TPA and ATA originate separately distal to MCA bifurcation 2 (11%) 34.8 IV TPA and ATA originate separately proximal to MCA bifurcation 3 (17%) 38.1 V TPA originates proximal and ATA originates distal to MCA bifurcation 4 (24%) 41.0 ATA = anterior temporal artery; MCA = middle cerebral artery; TPA = temporopolar artery. View Large Bypass Feasibility In all specimens, the TPA reached the distal-most point of A1-ACA (A1-A2 junction) to complete a bypass (average 15.8 ± 2.5 mm from the carotid bifurcation). The average caliber of the A1-ACA at the anastomosis point was 2.5 ± 0.5 mm. The TPA-A2 bypass was feasible with 16 TPAs (94%), and the anastomosis point on the A2-ACA had an average distance of 5.7 ± 1.9 mm from the A1-A2 junction. The average diameter of the recipient A2-ACA was 2.3 ± 0.7 mm at the point of anastomosis. In 1 specimen with a type I TPA (having the shortest cisternal length), the TPA did not reach the A2-ACA. The TPA-PCA and TPA-SCA bypasses were feasible in all specimens except in the specimen having a type I TPA with the shortest cisternal length (same specimen in which TPA-A2 bypass was not feasible). The calibers of the SCA and PCA at the anastomosis points were 2.0 ± 0.6 mm, and 2.7 ± 0.8 mm, respectively. The TPA could be successfully reimplanted onto the SCA 10.3 ± 3.7 mm from the SCA origin, and onto the PCA 13.9 ± 5.8 mm from the PCA origin. DISCUSSION We have shown the anatomical feasibility of the TPA-ACA and TPA-UPC bypasses. The TPA had enough length to reach the A1-A2 junction in all specimens. Also, in the majority (94%) of specimens, the TPA reached proximal A2-ACA, SCA and PCA. These findings, along with a caliber of ≥1.0 mm in more than 70% of specimens, show that the TPA may be a promising IC donor when revascularization of the ACA or UPC is considered. The SCA may be a better recipient as its caliber matches that of the TPA better than the PCA or ACA. Revascularization of Deep Recipients Various options exist for revascularization of ACA and UPC territories.3,8,17-22,35-44 Generally, the EC-IC bypasses have the advantages of no donor ischemia and relatively simple donor harvesting. On the other hand, they may require multiple anastomoses (eg, when an interposition graft is used) and are vulnerable to external compression or trauma. The IC-IC choices have the limitations of being more technically demanding and the risk of donor ischemia. However, they provide a better caliber match between the donor and recipient arteries and do not have the drawback of donor site complications.1,2 An IC-IC bypass with a minimum number of anastomoses (ie, 1), and with a donor supplying a noneloquent region combines the advantages of EC-IC and IC-IC bypasses and avoids their disadvantages. The TPA-UPC and TPA-ACA bypasses represent such an option and also have the advantage of relative proximity of the donor and recipient arteries. Additionally, as an IC-IC bypass, the TPA-ACA and TPA-UPC bypasses have the advantages of sparing a second incision, no graft harvesting time, and requiring a single anastomosis. Furthermore, the bypass components are entirely protected by skull. Infarct of the TPA territory should not result in neurological sequelae as the tip and anterior parts of the temporal lobe are resected in anterior lobectomy procedures without major complications.45-49 However, variability of the vascularization territory28 and transient visual, attentional, cognitive, speech, and memory complications have been reported after an anterior temporal lobectomy.48,50-52 Technical Feasibility of TPA-ACA and TPA-UPC Bypasses In our study, the TPA reached A1 in all specimens, and A2 and UPC vessels in 94% of specimens. The only TPA that failed to reach the A2 or UPC was a type I vessel (see Table 1), which originated from the postbifurcation MCA, and had a common stem with the ATA. This branching configuration may be less favorable because the origin of the TPA is both distal to MCA bifurcation (most distant from the ACoA complex), and common with ATA (providing a shorter cisternal length and less potential for mobilization). Although no statistically significant difference was observed when comparing the cisternal lengths of different TPA types, type I TPAs had the smallest average cisternal length compared to other types. Therefore, preoperative review of the TPA subtypes in angiograms is mandatory to rule out the unfavorable TPAs as candidates for transposition to deep recipients such as ACoA or UPC (Figure 5). FIGURE 5. View largeDownload slide Angiograms depicting different TPA types. A, Type I: ATA and TPA arise from a common stem distal to MCA bifurcation. B, Type II: ATA and TPA arise from a common stem proximal to MCA bifurcation. C, Type III: ATA and TPA arise separately distal to MCA bifurcation. D, Type IV: ATA and TPA arise separately proximal to MCA bifurcation. E, Type V: TPA arises proximal and ATA arises distal to MCA bifurcation. Please note: In all panels, red arrow points to the MCA bifurcation, yellow-shaded vessel segments designate the common stem for ATA and TPA, purple-shaded vessels are ATA (dashed arrow), and green-shaded vessels are TPA (black arrow). FIGURE 5. View largeDownload slide Angiograms depicting different TPA types. A, Type I: ATA and TPA arise from a common stem distal to MCA bifurcation. B, Type II: ATA and TPA arise from a common stem proximal to MCA bifurcation. C, Type III: ATA and TPA arise separately distal to MCA bifurcation. D, Type IV: ATA and TPA arise separately proximal to MCA bifurcation. E, Type V: TPA arises proximal and ATA arises distal to MCA bifurcation. Please note: In all panels, red arrow points to the MCA bifurcation, yellow-shaded vessel segments designate the common stem for ATA and TPA, purple-shaded vessels are ATA (dashed arrow), and green-shaded vessels are TPA (black arrow). It is important to note that performing an orbitozygomatic craniotomy may not always be necessary to complete the proposed bypasses. Less invasive craniotomies such as the pterional craniotomy may also be reasonable alternatives. In fact, the nature of the pathology (eg, location and size of the aneurysm) is the main factor determining the choice of approach. Despite the technical feasibility of the proposed bypasses, it is important to note that the proposed bypasses are still technically demanding, because the recipients are deep and embedded between multiple eloquent structures. There is no absolute way to compare the difficulty of the proposed bypasses to their former counterparts (eg, the A3-A3 in situ bypass). However, the present study tries to provide the anatomical foundations for a potential additional bypass option for these challenging cases. Does the TPA Provide Enough Flow? Despite the feasibility of the proposed bypasses in terms of reach, TPA caliber is an important consideration. Generally, equal donor and recipient calibers are the ideal for a bypass, yet not always possible. In our specimens, 12 out of 17 TPAs (70%) had a caliber ≥1 mm, making them eligible donors. However, the calibers of the recipients were usually >2 mm and there was an average caliber mismatch of 1 mm even when the TPA caliber was ≥1 mm. Fish-mouthing may address this problem to some extent. To the best of our knowledge, blood flow evaluation studies have never been performed on TPA. However, according to several studies, the completion of the bypass involving a small donor artery is followed by increased flow quantity delivered by the donor.53 This change is related to the flow demand of the territory vascularized by the recipient vessel, and it may be observed immediately or over time.53-56 However, specific evaluations should be performed to validate the clinical efficacy of the proposed bypass. Study Limitations This is a cadaveric study with the attempt to assess the anatomical feasibility of using the TPA as a donor vessel to revascularize deep recipients, but a clinical demonstration has not been reported so far. The main limitation of a cadaveric study is the lack of possibility to perform a blood flow evaluation or outcome assessment. Additionally, the proposed bypasses may have certain limitations when complex clinical scenarios are encountered. For example, with larger aneurysms, a longer TPA may be needed that might not be always available. Therefore, preoperative review of angiograms to assess the cisternal length of the TPA is mandatory (Figure 5). Additionally, with larger lesions, performing the anastomosis may be more difficult. Infarct of the temporal tip following the TPA occlusion has never been specifically discussed in the literature. Several studies in the literature report that the anterior temporal lobectomy may have transient cognitive, language, and memory sequelae.48,50-52,57,58 However, nonepileptic patients might have less tolerance to a temporal tip infarct, especially on the dominant side. Furthermore, not all patients could be radiologically evaluated for the diameter, dominance, and course of the TPA. Therefore, patient counseling regarding the possibility of permanent neurological sequelae after TPA use is of utmost importance. CONCLUSION To the best of our knowledge, the TPA has never been studied before as a donor artery for cerebral revascularization. We demonstrated that in most cases the TPA has a sufficient length and caliber to reach deep recipients of the anterior and posterior circulations. The proposed bypasses may be valid alternatives for revascularization of the ACA and UPC when simpler, more straightforward options are not available. This hypothesis awaits further validation by clinical application in well-selected cases. Disclosures This study was supported by Skull Base and Cerebrovascular Laboratory at UCSF, Barrow Neurological Foundation support to Dr Tayebi Meybodi, and from the Newsome Chair in Neurosurgery Research held by Dr Preul. The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article. Notes Portions of this study were presented as an e-poster at the Joint AANS/CNS Cerebrovascular Section Annual Meeting, in Houston, Texas, February 20-21, 2017. REFERENCES 1. Tayebi Meybodi A , Huang W , Benet A , Kola O , Lawton MT . 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Posterior circulation cerebral hyperperfusion syndrome after high flow external carotid artery to middle cerebral artery bypass . J Clin Neurosci . 2015 ; 22 ( 9 ): 1515 – 1518 . Google Scholar CrossRef Search ADS PubMed 28. De Long WB . Anatomy of the middle cerebral artery: the temporal branches . Stroke . 1973 ; 4 ( 3 ): 412 – 418 . Google Scholar CrossRef Search ADS PubMed 29. Meybodi AT , Griswold D , Tabani H et al. Topographic surgical anatomy of the parasylvian anterior temporal artery for intracranial-intracranial bypass . World Neurosurg . 2016 ; 93 : 67 – 72 . Google Scholar CrossRef Search ADS PubMed 30. Tanriover N , Kawashima M , Rhoton AL , Ulm AJ , Mericle RA . Microsurgical anatomy of the early branches of the middle cerebral artery: morphometric analysis and classification with angiographic correlation . J Neurosurg . 2003 ; 98 ( 6 ): 1277 – 1290 . Google Scholar CrossRef Search ADS PubMed 31. Ipekdal HI , Karadas O , Erdogan E , Gokcil Z . Spectrum of surgical complications of temporal lobe epilepsy surgery: a single—center study . Turk Neurosurg . 2011 ; 21 ( 2 ): 147 – 151 . Google Scholar PubMed 32. Jones JE , Blocher JB , Jackson DC . Life outcomes of anterior temporal lobectomy: serial long-term follow-up evaluations . Neurosurgery . 2013 ; 73 ( 6 ): 1018 – 1025 . Google Scholar CrossRef Search ADS PubMed 33. Sindou M , Guenot M , Isnard J , Ryvlin P , Fischer C , Mauguière F . Temporo-mesial epilepsy surgery: outcome and complications in 100 consecutive adult patients . Acta Neurochir (Wien) . 2006 ; 148 ( 1 ): 39 – 45 . Google Scholar CrossRef Search ADS PubMed 34. Benet A , Rincon-Torroella J , Lawton MT , González Sánchez JJ . Novel embalming solution for neurosurgical simulation in cadavers . J Neurosurg . 2014 ; 120 ( 5 ): 1229 – 1237 . Google Scholar CrossRef Search ADS PubMed 35. Davies JM , Lawton MT . “Picket Fence” clipping technique for large and complex aneurysms . Neurosurg Focus . 2015 ; 39 ( Video Supp l1 ): V17 . Google Scholar CrossRef Search ADS PubMed 36. Yang I , Lawton MT . Clipping of complex aneurysms with fenestration tubes: application and assessment of three types of clip techniques . Neurosurgery . 2008 ; 62 ( 5 suppl 2 ): ONS371 – 378 . Google Scholar PubMed 37. Nakahara I , Taha MM , Higashi T et al. Different modalities of treatment of intracranial mycotic aneurysms: Report of 4 cases . Surg Neurol . 2006 ; 66 ( 4 ): 405 – 409 . Google Scholar CrossRef Search ADS PubMed 38. Inoue T , Tsutsumi K , Ohno H , Shinozaki M . Revascularization of the anterior cerebral artery with an A3-A3 anastomosis and a superficial temporal artery bypass using an A3-radial artery graft to trap a giant anterior communicating artery aneurysm: technical case report . Neurosurgery . 2005 ; 57 ( 1 Suppl ): E207 . Google Scholar PubMed 39. Chang SW , Abla AA , Kakarla UK et al. Treatment of distal posterior cerebral artery aneurysms: a critical appraisal of the occipital artery-to-posterior cerebral artery bypass . Neurosurgery . 2010 ; 67 ( 1 ): 16 – 26 . Google Scholar CrossRef Search ADS PubMed 40. Touho H , Karasawa J , Ohnishi H , Kobitsu K . Anastomosis of occipital artery to posterior cerebral artery with interposition of superficial temporal artery using occipital interhemispheric transtentorial approach: case report . Surg Neurol . 1995 ; 44 ( 3 ): 245 – 250 . Google Scholar CrossRef Search ADS PubMed 41. Rodríguez-Hernández A , Huang C , Lawton MT . Superior cerebellar artery–posterior cerebral artery bypass: in situ bypass for posterior cerebral artery revascularization . J Neurosurg . 2013 ; 118 ( 5 ): 1053 – 1057 . Google Scholar CrossRef Search ADS PubMed 42. Saito H , Ogasawara K , Kubo Y , Tomitsuka N , Ogawa A . Treatment of ruptured fusiform aneurysm in the posterior cerebral artery with posterior cerebral artery-superior cerebellar artery anastomosis combined with parent artery occlusion: case report . Surg Neurol . 2006 ; 65 ( 6 ): 621 – 624 . Google Scholar CrossRef Search ADS PubMed 43. Lawton MT , Abla AA , Rutledge WC et al. Bypass surgery for the treatment of dolichoectatic basilar trunk aneurysms: A work in progress . Neurosurgery . 2016 ; 79 ( 1 ): 83 – 99 Google Scholar CrossRef Search ADS PubMed 44. Kalani MY , Spetzler RF . Internal carotid artery-to-posterior cerebral artery bypass for revascularization of the brainstem . J Clin Neurosci . 2016 ; 24 : 151 – 154 . Google Scholar CrossRef Search ADS PubMed 45. Behrens E , Schramm J , Zentner J , König R . Surgical and neurological complications in a series of 708 epilepsy surgery procedures . Neurosurgery . 1997 ; 41 ( 1 ): 1 – 10 . Google Scholar CrossRef Search ADS PubMed 46. Davies KG , Weeks RD . Temporal lobectomy for intractable epilepsy: experience with 58 cases over 21 years . Br J Neurosurg . 1993 ; 7 ( 1 ): 23 – 33 . Google Scholar CrossRef Search ADS PubMed 47. McClelland S , Guo H , Okuyemi KS . Population-based analysis of morbidity and mortality following surgery for intractable temporal lobe epilepsy in the United States . Arch Neurol . 2011 ; 68 ( 6 ): 725 – 729 . Google Scholar CrossRef Search ADS PubMed 48. Popovic EA , Fabinyi GC , Brazenor GA , Berkovic SF , Bladin PF . Temporal lobectomy for epilepsy—complications in 200 patients . J Clin Neurosci . 1995 ; 2 ( 3 ): 238 – 244 . Google Scholar CrossRef Search ADS PubMed 49. Wyler AR . Anterior temporal lobectomy . Surg Neurol . 2000 ; 54 ( 5 ): 341 – 345 . Google Scholar CrossRef Search ADS PubMed 50. Cohn M , St-Laurent M , Barnett A , McAndrews MP . Social inference deficits in temporal lobe epilepsy and lobectomy: risk factors and neural substrates . Soc Cogn Affect Neurosci . 2015 ; 10 ( 5 ): 636 – 644 . Google Scholar CrossRef Search ADS PubMed 51. Alpherts WC , Vermeulen J , van Rijen PC , da Silva FH , van Veelen CW , Program DCES . Verbal memory decline after temporal epilepsy surgery?: A 6-year multiple assessments follow-up study . Neurology . 2006 ; 67 ( 4 ): 626 – 631 . Google Scholar CrossRef Search ADS PubMed 52. Grivas A , Schramm J , Kral T et al. Surgical treatment for refractory temporal lobe epilepsy in the elderly: seizure outcome and neuropsychological sequels compared with a younger cohort . Epilepsia . 2006 ; 47 ( 8 ): 1364 – 1372 . Google Scholar CrossRef Search ADS PubMed 53. Amin-Hanjani S , Alaraj A , Charbel FT . Flow replacement bypass for aneurysms: decision-making using intraoperative blood flow measurements . Acta Neurochir . 2010 ; 152 ( 6 ): 1021 – 1032 . Google Scholar CrossRef Search ADS PubMed 54. Amin-Hanjani S , Du X , Mlinarevich N , Meglio G , Zhao M , Charbel FT . The cut flow index: an intraoperative predictor of the success of extracranial-intracranial bypass for occlusive cerebrovascular disease . Neurosurgery . 2005 ; 56 ( 1 suppl ): 75 – 85 . Google Scholar PubMed 55. Rustemi O , Amin-Hanjani S , Shakur SF , Du X , Charbel FT . Donor selection in flow replacement bypass surgery for cerebral aneurysms . Neurosurgery . 2016 ; 78 ( 3 ): 332 – 342 . Google Scholar CrossRef Search ADS PubMed 56. Guppy KH , Charbel FT , Corsten LA , Zhao M , Debrun G . Hemodynamic evaluation of basilar and vertebral artery angioplasty . Neurosurgery . 2002 ; 51 ( 2 ): 327 – 334 . Google Scholar CrossRef Search ADS PubMed 57. Hamberger MJ , Drake EB . Cognitive functioning following epilepsy surgery . Curr Neurol Neurosci Rep . 2006 ; 6 ( 4 ): 319 – 326 . Google Scholar CrossRef Search ADS PubMed 58. Rausch R , Kraemer S , Pietras CJ , Le M , Vickrey BG , Passaro EA . Early and late cognitive changes following temporal lobe surgery for epilepsy . Neurology . 2003 ; 60 ( 6 ): 951 – 959 . Google Scholar CrossRef Search ADS PubMed Operative Neurosurgery Speaks! Audio abstracts available for this article at www.operativeneurosurgery-online.com. COMMENTS Iwould like to congratulate the authors on a nice cadaveric study that brings new ideas into the field of bypass surgeries. The originality of this work comes from the fact that this seems to be the first study with focus on the TPA and its functionality as a donor for intracranial bypasses. It is unlikely that TPA would become a major donor for intracranial bypass surgeries but in a highly selected case it could prove useful. Martin Lehecka Helsinki, Finland The authors report the results of a study demonstrating the technical feasibility of using the TPA for IC-IC bypass to the A1 and A2 segments of the anterior cerebral artery, as well as to the superior cerebellar and posterior cerebral arteries. Anatomic dissections were performed bilaterally on 8 cadaveric heads, and the TPA was identified, mobilized, and divided at its M3-M4 junction. The distal caliper of the TPA at this junction was ≥1.0 mm in 70% of the specimens, which is roughly the lower limit necessary to provide adequate flow to the potential recipient artery territories. The authors found that the length of the TPA was sufficient to allow anastomosis to the A1-segment in 100% of the vessels, and to the A2-segment, SCA and PCA in 94% of cases. This is a well-written manuscript that includes remarkably clear illustrations and photographs of all key points. As pointed out by the authors, while use of the TPA is technically feasible, further studies are needed to define the clinical potential of this vessel for IC-IC bypass. Joseph M. Zabramski Phoenix, Arizona This is a nice paper showing not only innovative thinking but also dexterity, which is still needed to perform bypasses in selected cases in the era of endovascular therapy taking over. This is a good addition into the armamentarium of neurovascular surgeons who are still needed and patients should be centralized for better quality of care. The authors used orbitozygomatic approaches but often less is more for the benefit of time consumption and avoidance of complications, and a pterional or lateral supraorbital is all that is needed. Mika Niemelä Helsinki, Finland Operative Neurosurgery Speaks (Audio Abstracts) Listen to audio translations of this paper's abstract into select languages by choosing from one of the selections below. Chinese: Zuowei Wang, MD. Department of Neurosurgery Beijing Hospital Beijing, China Chinese: Zuowei Wang, MD. Department of Neurosurgery Beijing Hospital Beijing, China Close English: Oluwakemi Aderonke Badejo, MBBS, FWACS. Department of Surgery College of Medicine University of Ibadan Ibadan, Nigeria English: Oluwakemi Aderonke Badejo, MBBS, FWACS. Department of Surgery College of Medicine University of Ibadan Ibadan, Nigeria Close Italian: Alessandro Ducati, MD. Department of Neurosurgery University of Torino Torino, Italy Italian: Alessandro Ducati, MD. Department of Neurosurgery University of Torino Torino, Italy Close Spanish: Carlos E. Alvarez, MD. Department of Neurosurgery Instituto del Cerebro y la Columna Vertebral Lima, Peru Spanish: Carlos E. Alvarez, MD. Department of Neurosurgery Instituto del Cerebro y la Columna Vertebral Lima, Peru Close Japanese: Hidehito Kimura, MD, PhD. Department of Neurosurgery Kobe University Graduate School of Medicine Kobe, Japan Japanese: Hidehito Kimura, MD, PhD. Department of Neurosurgery Kobe University Graduate School of Medicine Kobe, Japan Close Korean: Hye Ran Park, MD. Department of Neurosurgery Soonchunhyang University Seoul Hospital Seoul, Republic of Korea Korean: Hye Ran Park, MD. Department of Neurosurgery Soonchunhyang University Seoul Hospital Seoul, Republic of Korea Close Russian: Roman Kovalenko, MD. Federal Almazov North-West Medical Research Centre St. Petersburg, Russian Federation Russian: Roman Kovalenko, MD. Federal Almazov North-West Medical Research Centre St. Petersburg, Russian Federation Close Greek: Marios Themistocleous, MD. Department of Neurosurgery Aghia Sophia Children's Hospital Athens, Greece Greek: Marios Themistocleous, MD. Department of Neurosurgery Aghia Sophia Children's Hospital Athens, Greece Close Copyright © 2018 by the Congress of Neurological Surgeons This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Operative Neurosurgery Oxford University Press

Anatomical Assessment of the Temporopolar Artery for Revascularization of Deep Recipients

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Congress of Neurological Surgeons
Copyright
Copyright © 2018 by the Congress of Neurological Surgeons
ISSN
2332-4252
eISSN
2332-4260
D.O.I.
10.1093/ons/opy115
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Abstract

Abstract BACKGROUND Intracranial–intracranial and extracranial–intracranial bypass options for revascularization of deep cerebral recipients are limited and technically demanding. OBJECTIVE To assess the anatomical feasibility of using the temporopolar artery (TPA) for revascularization of the anterior cerebral artery (ACA), posterior cerebral artery (PCA), and superior cerebellar arteries (SCA). METHODS Orbitozygomatic craniotomy was performed bilaterally on 8 cadaveric heads. The cisternal segment of the TPA was dissected. The TPA was cut at M3-M4 junction with its proximal and distal calibers and the length of the cisternal segment measured. Feasibility of the TPA-A1-ACA, TPA-A2-ACA, TPA-SCA, and TPA-PCA bypasses were assessed. RESULTS A total of 17 TPAs were identified in 16 specimens. The average distal TPA caliber was 1.0 ± 0.2 mm, and the average cisternal length was 37.5 ± 9.4 mm. TPA caliber was ≥ 1.0 mm in 12 specimens (70%). The TPA-A1-ACA bypass was feasible in all specimens, whereas the TPA reached the A2-ACA, SCA, and PCA in 94% of specimens (16/17). At the point of anastomosis, the average recipient caliber was 2.5 ± 0.5 mm for A1-ACA, and 2.3 ± 0.7 mm for A2-ACA. The calibers of the SCA and PCA at the anastomosis points were 2.0 ± 0.6 mm, and 2.7 ± 0.8 mm, respectively. CONCLUSION The TPA-ACA, TPA-PCA, and TPA-SCA bypasses are anatomically feasible and may be used when the distal caliber of the TPA stump is optimal to provide adequate blood flow. This study lays foundations for clinical use of the TPA for ACA revascularization in well-selected cases. Anterior cerebral artery, Complex aneurysm, Intracranial–intracranial bypass, Oculomotor-tentorial triangle, Orbitozygomatic approach, Posterior cerebral artery, Superior cerebellar artery ABBREVIATIONS ABBREVIATIONS ACA anterior cerebral artery ACoA anterior communicating artery ATA anterior temporal artery EC extracranial IC intracranial MCA middle cerebral artery PCA posterior cerebral artery SCA superior cerebellar arteries TPA temporopolar artery UPC upper posterior circulation STA superficial temporal artery Although rare, complex intracranial (IC) aneurysms are challenging because they may require a bypass procedure as part of the treatment strategy.1,2 The technical challenge of cerebral bypass is accentuated with deep recipients, such as those of the anterior cerebral artery (ACA) and the upper posterior circulation (UPC)—consisting of posterior cerebral artery (PCA) and superior cerebellar artery (SCA).2-12 This challenge is mainly due to the deep location of the recipient arteries surrounded by multiple eloquent neurovascular structures. The side-to-side A3-A3 bypass is probably the most common revascularization procedure for the ACA.4,6-11,13,14 The A3-A3 bypass is technically demanding both because of the deep location and the inherent challenge of a side-to-side anastomosis that requires completing an intraluminal suture line.2,15 Additionally, such a construct entails potential ischemia of the donor ACA territory. Other bypass options for revascularizing the ACA in cases of complex ACA aneurysms are limited, such as the use of interposition grafts between an IC or an extracranial (EC) donor and the ACA16,17, or the use of other adjacent IC donors, such as the frontopolar and orbitofrontal arteries.11,14 Similarly, few options are available for revascularization of the UPC. The superficial temporal artery (STA) has been used for this purpose.18-21 However, the STA may not have an optimal caliber or may be unavailable due to previous operative injury. The occipital artery can also be used, but when the anterior and lateral mesencephalic segments of the UPC vessels are targeted, problems may arise with rerouting the occipital artery to reach target vessels.22 An interposition graft between the external carotid artery and the UPC vessels is another EC-IC option. Apart from the need for remote incisions and vulnerability of the graft to external trauma, caliber mismatch and the increased risk of cerebral hyperperfusion syndrome or graft occlusion are important potential problems with EC-IC bypasses.2,4,12,23-27 As mentioned, IC-IC bypasses have an important limitation, which is the risk of ischemia to the donor artery territory. The IC vessels are end arteries that generally supply eloquent regions of the brain. However, IC-IC bypasses are attractive because of several advantages, such as: (1) sparing the patient additional incisions to expose the donor and/or graft vessels; (2) requiring fewer anastomoses; (3) protection by the calvarium; and (4) good caliber match between the donor and the recipient.2-4 Therefore, the identification of potential IC donors with good caliber and reach to recipient territories, while supplying a noneloquent area would provide valuable bypass options. The temporopolar artery (TPA) is the most proximal branch of the middle cerebral artery (MCA), feeding the pole and lateral aspect of the anterior temporal lobe,28-30 which are noneloquent areas.2,31-33 However, its use has not been studied as a donor to revascularize deep recipients. The purpose of the current study is to assess the potential of the TPA for revascularization of the ACA and UPC (Figure 1). FIGURE 1. View largeDownload slide Artist's Illustration showing the A, TPA-ACA and B, TPA-PCA bypass concepts. ACA = anterior cerebral artery; AChA = anterior choroidal artery; ACoA = anterior communicating artery; ATA = anterior temporal artery; BA = basilar artery; CN = cranial nerve; ICA = internal carotid artery; PCoA = posterior communicating artery; PCA = posterior cerebral artery. TPA = temporopolar artery. FIGURE 1. View largeDownload slide Artist's Illustration showing the A, TPA-ACA and B, TPA-PCA bypass concepts. ACA = anterior cerebral artery; AChA = anterior choroidal artery; ACoA = anterior communicating artery; ATA = anterior temporal artery; BA = basilar artery; CN = cranial nerve; ICA = internal carotid artery; PCoA = posterior communicating artery; PCA = posterior cerebral artery. TPA = temporopolar artery. METHODS The present study did not require IRB approval as it only involved cadaveric specimens and retrospective review of de-identified cerebral angiograms. Craniotomy and Preparation of the TPA Eight cadaveric heads (16 sides) were prepared for cadaveric dissection using our customized embalming formula.34 Using a head clamp (Mizuho America, Union City, California), each head was positioned classically for a pterional-orbitozygomatic approach. After completing a standard orbitozygomatic craniotomy, the dura was opened using a C-shaped incision (Figure 2A). Using a surgical microscope (Carl Zeiss AG, Oberkochen, Germany), the Sylvian fissure was widely split, and the branching pattern of the MCA was assessed to find the TPA. The origination patterns of TPA and anterior temporal artery (ATA) were recorded with regard to the MCA bifurcation (Figure 2B and 2C). Using a hand-held caliper, TPA caliber was recorded at origin and at M3-M4 junction. Next, the cisternal segment of the TPA (from origin to M3-M4 junction) was prepared by dividing small branches tethering it to the adjacent temporal lobe. However, any branches entering the anterior perforated substance were preserved. FIGURE 2. View largeDownload slide Cadaveric dissection showing the TPA-ACA bypass. A, a right pterional-orbitozygomatic craniotomy is performed and the sylvian fissure is split. B, the ATA and TPA are identified using the landmark of pars triangularis opposite to which ATA is most frequently found. C, the cisternal segment of the ATA and TPA are released to identify the origination pattern of these vessels from the MCA. White arrow points to the MCA bifurcation. The ATA and TPA originate from a common trunk which arises as an early branch proximal to the MCA bifurcation. D, the carotid and lamina terminalis cisterns are opened to expose the ipsilateral ACA. E, the TPA is mobilized towards the ACA after it is divided at the M3-M4 junction, and an end-to-side anastomosis is completed. F, overall view of the TPA-ACA bypass with the ATA (small white arrow) being untouched. ACA = anterior cerebral artery; ATA = anterior temporal artey; ICA = internal carotid artery; n. = nerve; Rt. = right; Orb. = orbitalis; Tri. = triangularis; TPA = temporopolar artery. FIGURE 2. View largeDownload slide Cadaveric dissection showing the TPA-ACA bypass. A, a right pterional-orbitozygomatic craniotomy is performed and the sylvian fissure is split. B, the ATA and TPA are identified using the landmark of pars triangularis opposite to which ATA is most frequently found. C, the cisternal segment of the ATA and TPA are released to identify the origination pattern of these vessels from the MCA. White arrow points to the MCA bifurcation. The ATA and TPA originate from a common trunk which arises as an early branch proximal to the MCA bifurcation. D, the carotid and lamina terminalis cisterns are opened to expose the ipsilateral ACA. E, the TPA is mobilized towards the ACA after it is divided at the M3-M4 junction, and an end-to-side anastomosis is completed. F, overall view of the TPA-ACA bypass with the ATA (small white arrow) being untouched. ACA = anterior cerebral artery; ATA = anterior temporal artey; ICA = internal carotid artery; n. = nerve; Rt. = right; Orb. = orbitalis; Tri. = triangularis; TPA = temporopolar artery. TPA-ACA and TPA-UPC Bypasses Using the surgical microscope, the carotid, chiasmatic, and lamina terminalis cisterns were opened to expose the ipsilateral A1-ACA, anterior communicating artery (ACoA), contralateral A1-ACA, and their adjacent branches. Also, the paired A2-ACAs were exposed after resecting a small portion of the ipsilateral gyrus rectus. Next, the TPA was divided at its opercular-cortical (M3-M4) junction and mobilized medially to reach the ACoA complex. The feasibility of completing an end-to-side TPA-ACA anastomosis without undue tension on the TPA stump was assessed at distal-most points on ipsilateral A1- and A2-ACA (Figure 2D-2F). When the anastomosis was deemed feasible, the caliber of the ACA was recorded at the point of anastomosis on A1 and A2 segments. The distance between the anastomosis point on A1-ACA was measured from the bifurcation of the internal carotid artery, and the distance between the anastomosis point on A2-ACA was measured from A1 to A2 junction. Distance measurements were accomplished using a stereotactic navigation system (Stryker, Kalamazoo, Michigan). Next, the feasibility of TPA-UPC bypass was assessed. To expose the UPC, the pretemporal corridor was developed by retracting the temporal lobe laterally and posteriorly. The carotid, chiasmatic, crural, and ambient cisterns were opened to expose the basilar apex, as well as the ipsilateral P1 and P2 segments of PCA, and the s1 and s2 segments of SCA. Next, the TPA was mobilized posteriorly to reach the SCA and PCA within a triangle formed between the oculomotor nerve medially, and the tentorial edge laterally (Figure 3). The feasibility of completing an end-to-side anastomosis without undue tension on the TPA was assessed for the most distal accessible point on the PCA and SCA inside the oculomotor-tentorial triangle. Care was taken not to manipulate the oculomotor nerve. The calibers of the PCA and SCA at anastomosis points were recorded. The lengths of the PCA and SCA segments between their origin on the basilar artery and the anastomosis points were also measured using the frameless stereotactic navigation system (Stryker). FIGURE 3. View largeDownload slide Cadaveric depiction of TPA-SCA bypass. A, exposure and release of cisternal segment of the TPA through a right transsylvian approach. B, TPA-SCA bypass completed. ATA = anterior temporal artery; CN = cranial nerve; ICA = internal carotid artery; MCA = middle cerebral artery; n. = nerve; TPA = temporopolar artery. FIGURE 3. View largeDownload slide Cadaveric depiction of TPA-SCA bypass. A, exposure and release of cisternal segment of the TPA through a right transsylvian approach. B, TPA-SCA bypass completed. ATA = anterior temporal artery; CN = cranial nerve; ICA = internal carotid artery; MCA = middle cerebral artery; n. = nerve; TPA = temporopolar artery. RESULTS Branching Pattern of TPA A total of 17 TPAs were found (1 specimen had duplicate TPAs). The average TPA caliber was 1.3 ± 0.3 mm at its origin and 1.0 ± 0.2 mm at M3-M4 junction. Twelve TPAs (70%) had a caliber ≥1.0 mm at the M3-M4 junction. The average cisternal length of the TPA was 37.5 ± 9.4 mm (range: 19-52.1 mm). Five different patterns of TPA origination with regards to MCA bifurcation and the origin of the ATA were noted (Table 1 and Figure 4). Using the 1-way analysis of variance statistical method, no statistically significant difference was found between the cisternal lengths of different TPA subtypes (P = .94). However, TPA type I had the shortest, and TPA type V had the longest average cisternal segment lengths (Table 1). FIGURE 4. View largeDownload slide Artist's illustration showing branching patterns of TPA relative to the middle cerebral artery bifurcation and origin of the ATA. A, Type I: ATA and TPA arise from a common stem distal to MCA bifurcation. B, Type II: ATA and TPA arise from a common stem proximal to MCA bifurcation. C, Type III: ATA and TPA arise separately distal to MCA bifurcation. D, Type IV: ATA and TPA arise separately proximal to MCA bifurcation. E, Type V: TPA arises proximal and ATA arises distal to MCA bifurcation. ATA = anterior temporal artery; TPA = temporopolar artery. FIGURE 4. View largeDownload slide Artist's illustration showing branching patterns of TPA relative to the middle cerebral artery bifurcation and origin of the ATA. A, Type I: ATA and TPA arise from a common stem distal to MCA bifurcation. B, Type II: ATA and TPA arise from a common stem proximal to MCA bifurcation. C, Type III: ATA and TPA arise separately distal to MCA bifurcation. D, Type IV: ATA and TPA arise separately proximal to MCA bifurcation. E, Type V: TPA arises proximal and ATA arises distal to MCA bifurcation. ATA = anterior temporal artery; TPA = temporopolar artery. TABLE 1. Origination Patterns of TPA With Regards to MCA Bifurcation and the Origin of the ATA in 17 TPAs. TPA origination type Definition Frequency (%) Average cisternal length (mm) I TPA originates distal to MCA bifurcation, with a common stem with ATA 4 (24%) 34.3 II The originates proximal to MCA bifurcation, with a common stem with ATA 4 (24%) 38.1 III TPA and ATA originate separately distal to MCA bifurcation 2 (11%) 34.8 IV TPA and ATA originate separately proximal to MCA bifurcation 3 (17%) 38.1 V TPA originates proximal and ATA originates distal to MCA bifurcation 4 (24%) 41.0 TPA origination type Definition Frequency (%) Average cisternal length (mm) I TPA originates distal to MCA bifurcation, with a common stem with ATA 4 (24%) 34.3 II The originates proximal to MCA bifurcation, with a common stem with ATA 4 (24%) 38.1 III TPA and ATA originate separately distal to MCA bifurcation 2 (11%) 34.8 IV TPA and ATA originate separately proximal to MCA bifurcation 3 (17%) 38.1 V TPA originates proximal and ATA originates distal to MCA bifurcation 4 (24%) 41.0 ATA = anterior temporal artery; MCA = middle cerebral artery; TPA = temporopolar artery. View Large TABLE 1. Origination Patterns of TPA With Regards to MCA Bifurcation and the Origin of the ATA in 17 TPAs. TPA origination type Definition Frequency (%) Average cisternal length (mm) I TPA originates distal to MCA bifurcation, with a common stem with ATA 4 (24%) 34.3 II The originates proximal to MCA bifurcation, with a common stem with ATA 4 (24%) 38.1 III TPA and ATA originate separately distal to MCA bifurcation 2 (11%) 34.8 IV TPA and ATA originate separately proximal to MCA bifurcation 3 (17%) 38.1 V TPA originates proximal and ATA originates distal to MCA bifurcation 4 (24%) 41.0 TPA origination type Definition Frequency (%) Average cisternal length (mm) I TPA originates distal to MCA bifurcation, with a common stem with ATA 4 (24%) 34.3 II The originates proximal to MCA bifurcation, with a common stem with ATA 4 (24%) 38.1 III TPA and ATA originate separately distal to MCA bifurcation 2 (11%) 34.8 IV TPA and ATA originate separately proximal to MCA bifurcation 3 (17%) 38.1 V TPA originates proximal and ATA originates distal to MCA bifurcation 4 (24%) 41.0 ATA = anterior temporal artery; MCA = middle cerebral artery; TPA = temporopolar artery. View Large Bypass Feasibility In all specimens, the TPA reached the distal-most point of A1-ACA (A1-A2 junction) to complete a bypass (average 15.8 ± 2.5 mm from the carotid bifurcation). The average caliber of the A1-ACA at the anastomosis point was 2.5 ± 0.5 mm. The TPA-A2 bypass was feasible with 16 TPAs (94%), and the anastomosis point on the A2-ACA had an average distance of 5.7 ± 1.9 mm from the A1-A2 junction. The average diameter of the recipient A2-ACA was 2.3 ± 0.7 mm at the point of anastomosis. In 1 specimen with a type I TPA (having the shortest cisternal length), the TPA did not reach the A2-ACA. The TPA-PCA and TPA-SCA bypasses were feasible in all specimens except in the specimen having a type I TPA with the shortest cisternal length (same specimen in which TPA-A2 bypass was not feasible). The calibers of the SCA and PCA at the anastomosis points were 2.0 ± 0.6 mm, and 2.7 ± 0.8 mm, respectively. The TPA could be successfully reimplanted onto the SCA 10.3 ± 3.7 mm from the SCA origin, and onto the PCA 13.9 ± 5.8 mm from the PCA origin. DISCUSSION We have shown the anatomical feasibility of the TPA-ACA and TPA-UPC bypasses. The TPA had enough length to reach the A1-A2 junction in all specimens. Also, in the majority (94%) of specimens, the TPA reached proximal A2-ACA, SCA and PCA. These findings, along with a caliber of ≥1.0 mm in more than 70% of specimens, show that the TPA may be a promising IC donor when revascularization of the ACA or UPC is considered. The SCA may be a better recipient as its caliber matches that of the TPA better than the PCA or ACA. Revascularization of Deep Recipients Various options exist for revascularization of ACA and UPC territories.3,8,17-22,35-44 Generally, the EC-IC bypasses have the advantages of no donor ischemia and relatively simple donor harvesting. On the other hand, they may require multiple anastomoses (eg, when an interposition graft is used) and are vulnerable to external compression or trauma. The IC-IC choices have the limitations of being more technically demanding and the risk of donor ischemia. However, they provide a better caliber match between the donor and recipient arteries and do not have the drawback of donor site complications.1,2 An IC-IC bypass with a minimum number of anastomoses (ie, 1), and with a donor supplying a noneloquent region combines the advantages of EC-IC and IC-IC bypasses and avoids their disadvantages. The TPA-UPC and TPA-ACA bypasses represent such an option and also have the advantage of relative proximity of the donor and recipient arteries. Additionally, as an IC-IC bypass, the TPA-ACA and TPA-UPC bypasses have the advantages of sparing a second incision, no graft harvesting time, and requiring a single anastomosis. Furthermore, the bypass components are entirely protected by skull. Infarct of the TPA territory should not result in neurological sequelae as the tip and anterior parts of the temporal lobe are resected in anterior lobectomy procedures without major complications.45-49 However, variability of the vascularization territory28 and transient visual, attentional, cognitive, speech, and memory complications have been reported after an anterior temporal lobectomy.48,50-52 Technical Feasibility of TPA-ACA and TPA-UPC Bypasses In our study, the TPA reached A1 in all specimens, and A2 and UPC vessels in 94% of specimens. The only TPA that failed to reach the A2 or UPC was a type I vessel (see Table 1), which originated from the postbifurcation MCA, and had a common stem with the ATA. This branching configuration may be less favorable because the origin of the TPA is both distal to MCA bifurcation (most distant from the ACoA complex), and common with ATA (providing a shorter cisternal length and less potential for mobilization). Although no statistically significant difference was observed when comparing the cisternal lengths of different TPA types, type I TPAs had the smallest average cisternal length compared to other types. Therefore, preoperative review of the TPA subtypes in angiograms is mandatory to rule out the unfavorable TPAs as candidates for transposition to deep recipients such as ACoA or UPC (Figure 5). FIGURE 5. View largeDownload slide Angiograms depicting different TPA types. A, Type I: ATA and TPA arise from a common stem distal to MCA bifurcation. B, Type II: ATA and TPA arise from a common stem proximal to MCA bifurcation. C, Type III: ATA and TPA arise separately distal to MCA bifurcation. D, Type IV: ATA and TPA arise separately proximal to MCA bifurcation. E, Type V: TPA arises proximal and ATA arises distal to MCA bifurcation. Please note: In all panels, red arrow points to the MCA bifurcation, yellow-shaded vessel segments designate the common stem for ATA and TPA, purple-shaded vessels are ATA (dashed arrow), and green-shaded vessels are TPA (black arrow). FIGURE 5. View largeDownload slide Angiograms depicting different TPA types. A, Type I: ATA and TPA arise from a common stem distal to MCA bifurcation. B, Type II: ATA and TPA arise from a common stem proximal to MCA bifurcation. C, Type III: ATA and TPA arise separately distal to MCA bifurcation. D, Type IV: ATA and TPA arise separately proximal to MCA bifurcation. E, Type V: TPA arises proximal and ATA arises distal to MCA bifurcation. Please note: In all panels, red arrow points to the MCA bifurcation, yellow-shaded vessel segments designate the common stem for ATA and TPA, purple-shaded vessels are ATA (dashed arrow), and green-shaded vessels are TPA (black arrow). It is important to note that performing an orbitozygomatic craniotomy may not always be necessary to complete the proposed bypasses. Less invasive craniotomies such as the pterional craniotomy may also be reasonable alternatives. In fact, the nature of the pathology (eg, location and size of the aneurysm) is the main factor determining the choice of approach. Despite the technical feasibility of the proposed bypasses, it is important to note that the proposed bypasses are still technically demanding, because the recipients are deep and embedded between multiple eloquent structures. There is no absolute way to compare the difficulty of the proposed bypasses to their former counterparts (eg, the A3-A3 in situ bypass). However, the present study tries to provide the anatomical foundations for a potential additional bypass option for these challenging cases. Does the TPA Provide Enough Flow? Despite the feasibility of the proposed bypasses in terms of reach, TPA caliber is an important consideration. Generally, equal donor and recipient calibers are the ideal for a bypass, yet not always possible. In our specimens, 12 out of 17 TPAs (70%) had a caliber ≥1 mm, making them eligible donors. However, the calibers of the recipients were usually >2 mm and there was an average caliber mismatch of 1 mm even when the TPA caliber was ≥1 mm. Fish-mouthing may address this problem to some extent. To the best of our knowledge, blood flow evaluation studies have never been performed on TPA. However, according to several studies, the completion of the bypass involving a small donor artery is followed by increased flow quantity delivered by the donor.53 This change is related to the flow demand of the territory vascularized by the recipient vessel, and it may be observed immediately or over time.53-56 However, specific evaluations should be performed to validate the clinical efficacy of the proposed bypass. Study Limitations This is a cadaveric study with the attempt to assess the anatomical feasibility of using the TPA as a donor vessel to revascularize deep recipients, but a clinical demonstration has not been reported so far. The main limitation of a cadaveric study is the lack of possibility to perform a blood flow evaluation or outcome assessment. Additionally, the proposed bypasses may have certain limitations when complex clinical scenarios are encountered. For example, with larger aneurysms, a longer TPA may be needed that might not be always available. Therefore, preoperative review of angiograms to assess the cisternal length of the TPA is mandatory (Figure 5). Additionally, with larger lesions, performing the anastomosis may be more difficult. Infarct of the temporal tip following the TPA occlusion has never been specifically discussed in the literature. Several studies in the literature report that the anterior temporal lobectomy may have transient cognitive, language, and memory sequelae.48,50-52,57,58 However, nonepileptic patients might have less tolerance to a temporal tip infarct, especially on the dominant side. Furthermore, not all patients could be radiologically evaluated for the diameter, dominance, and course of the TPA. Therefore, patient counseling regarding the possibility of permanent neurological sequelae after TPA use is of utmost importance. CONCLUSION To the best of our knowledge, the TPA has never been studied before as a donor artery for cerebral revascularization. We demonstrated that in most cases the TPA has a sufficient length and caliber to reach deep recipients of the anterior and posterior circulations. The proposed bypasses may be valid alternatives for revascularization of the ACA and UPC when simpler, more straightforward options are not available. This hypothesis awaits further validation by clinical application in well-selected cases. Disclosures This study was supported by Skull Base and Cerebrovascular Laboratory at UCSF, Barrow Neurological Foundation support to Dr Tayebi Meybodi, and from the Newsome Chair in Neurosurgery Research held by Dr Preul. The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article. Notes Portions of this study were presented as an e-poster at the Joint AANS/CNS Cerebrovascular Section Annual Meeting, in Houston, Texas, February 20-21, 2017. REFERENCES 1. Tayebi Meybodi A , Huang W , Benet A , Kola O , Lawton MT . 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Neurology . 2003 ; 60 ( 6 ): 951 – 959 . Google Scholar CrossRef Search ADS PubMed Operative Neurosurgery Speaks! Audio abstracts available for this article at www.operativeneurosurgery-online.com. COMMENTS Iwould like to congratulate the authors on a nice cadaveric study that brings new ideas into the field of bypass surgeries. The originality of this work comes from the fact that this seems to be the first study with focus on the TPA and its functionality as a donor for intracranial bypasses. It is unlikely that TPA would become a major donor for intracranial bypass surgeries but in a highly selected case it could prove useful. Martin Lehecka Helsinki, Finland The authors report the results of a study demonstrating the technical feasibility of using the TPA for IC-IC bypass to the A1 and A2 segments of the anterior cerebral artery, as well as to the superior cerebellar and posterior cerebral arteries. Anatomic dissections were performed bilaterally on 8 cadaveric heads, and the TPA was identified, mobilized, and divided at its M3-M4 junction. The distal caliper of the TPA at this junction was ≥1.0 mm in 70% of the specimens, which is roughly the lower limit necessary to provide adequate flow to the potential recipient artery territories. The authors found that the length of the TPA was sufficient to allow anastomosis to the A1-segment in 100% of the vessels, and to the A2-segment, SCA and PCA in 94% of cases. This is a well-written manuscript that includes remarkably clear illustrations and photographs of all key points. As pointed out by the authors, while use of the TPA is technically feasible, further studies are needed to define the clinical potential of this vessel for IC-IC bypass. Joseph M. Zabramski Phoenix, Arizona This is a nice paper showing not only innovative thinking but also dexterity, which is still needed to perform bypasses in selected cases in the era of endovascular therapy taking over. This is a good addition into the armamentarium of neurovascular surgeons who are still needed and patients should be centralized for better quality of care. The authors used orbitozygomatic approaches but often less is more for the benefit of time consumption and avoidance of complications, and a pterional or lateral supraorbital is all that is needed. Mika Niemelä Helsinki, Finland Operative Neurosurgery Speaks (Audio Abstracts) Listen to audio translations of this paper's abstract into select languages by choosing from one of the selections below. Chinese: Zuowei Wang, MD. Department of Neurosurgery Beijing Hospital Beijing, China Chinese: Zuowei Wang, MD. Department of Neurosurgery Beijing Hospital Beijing, China Close English: Oluwakemi Aderonke Badejo, MBBS, FWACS. Department of Surgery College of Medicine University of Ibadan Ibadan, Nigeria English: Oluwakemi Aderonke Badejo, MBBS, FWACS. Department of Surgery College of Medicine University of Ibadan Ibadan, Nigeria Close Italian: Alessandro Ducati, MD. Department of Neurosurgery University of Torino Torino, Italy Italian: Alessandro Ducati, MD. Department of Neurosurgery University of Torino Torino, Italy Close Spanish: Carlos E. Alvarez, MD. Department of Neurosurgery Instituto del Cerebro y la Columna Vertebral Lima, Peru Spanish: Carlos E. Alvarez, MD. Department of Neurosurgery Instituto del Cerebro y la Columna Vertebral Lima, Peru Close Japanese: Hidehito Kimura, MD, PhD. Department of Neurosurgery Kobe University Graduate School of Medicine Kobe, Japan Japanese: Hidehito Kimura, MD, PhD. Department of Neurosurgery Kobe University Graduate School of Medicine Kobe, Japan Close Korean: Hye Ran Park, MD. Department of Neurosurgery Soonchunhyang University Seoul Hospital Seoul, Republic of Korea Korean: Hye Ran Park, MD. Department of Neurosurgery Soonchunhyang University Seoul Hospital Seoul, Republic of Korea Close Russian: Roman Kovalenko, MD. Federal Almazov North-West Medical Research Centre St. Petersburg, Russian Federation Russian: Roman Kovalenko, MD. Federal Almazov North-West Medical Research Centre St. Petersburg, Russian Federation Close Greek: Marios Themistocleous, MD. Department of Neurosurgery Aghia Sophia Children's Hospital Athens, Greece Greek: Marios Themistocleous, MD. Department of Neurosurgery Aghia Sophia Children's Hospital Athens, Greece Close Copyright © 2018 by the Congress of Neurological Surgeons This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

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Operative NeurosurgeryOxford University Press

Published: May 30, 2018

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