Double-Barrel Superficial Temporal Artery-Middle Cerebral Artery Bypass: Can It Be Considered “High-Flow?”

Double-Barrel Superficial Temporal Artery-Middle Cerebral Artery Bypass: Can It Be Considered... Abstract BACKGROUND Traditionally, superficial temporal artery-middle cerebral artery (STA-MCA) bypass uses one STA branch. Its augmentation of flow has classically been described as “low flow.” In a double-barrel STA-MCA bypass, however, both branches of the STA are utilized. Here we hypothesize that this should not be considered “low flow.” OBJECTIVE To review quantitative flow data from our cases and investigate the impact of double-barrel STA-MCA bypass on total flow augmentation, and to assess whether double-barrel STA-MCA bypass might be useful in situations that traditionally demand more complex bypass strategies. METHODS Intraoperative flow probe measurements from STA-MCA bypass cases were retrospectively tabulated and compared. Cut flow and bypass flow measurements were, respectively, taken before and after completion of anastomoses. The higher value was labeled best observed flow (BOF). RESULTS We identified 21 STA-MCA bypass cases with available intraoperative flow probe measurements, of which 17 utilized double-barrel technique. Only 1 STA branch was available in 4 cases. Significantly higher average BOF was seen when utilizing 2 STA branches (69 vs 39 cc/min, P < .001). A majority (9/17) of double-barrel bypasses provided BOF ≥ 65 cc/min (120 cc/min maximum). The single branch bypass maximum BOF was 40 cc/min. CONCLUSION Double-barrel bypass technique significantly enhances STA-MCA flow capacity and may be useful in situations in which a high-flow bypass is needed. The 2 efferent limbs allow flexibility in distributing flow across separate at-risk territories. The method compares favorably to other descriptions of high-flow bypass without the morbidity of graft harvest or an additional cervical incision. Cerebral bypass, Double-barrel, Flow rate, High-flow, STA-MCA ABBREVIATIONS ABBREVIATIONS BOF best observed flow EC-IC extracranial-intracranial IC-IC intracranial-to-intracranial ICG indocyanine green STA superficial temporal artery STA-MCA superficial temporal artery-middle cerebral artery In most patients, the superficial temporal artery (STA) has 2 major branches, the frontal and parietal. Superficial temporal artery-middle cerebral artery (STA-MCA) bypass is typically performed using only 1 of these terminal STA branches.1 Its augmentation of flow has often been described as “low flow.”2,3 Over the last 6 yr, we have adopted a “double-barrel” technique in which both branches of the STA are utilized as our default bypass option.4 Single-branch STA-MCA bypass was performed only in patients missing a suitable frontal or parietal STA branch. In this study, we investigate the impact of this method on total flow augmentation and assess whether double-barrel STA-MCA bypass might be useful in situations that traditionally demand more complex bypass strategies. To our knowledge, this is the largest series describing flow data for double-barrel STA-MCA bypass. METHODS An intraoperative flow probe (Transonic Systems, Ithaca, New York) was used to measure flow rates in our cases of STA-MCA bypass. These were retrospectively tabulated and compared. Cases of both traditional single-branch and double-barrel STA-MCA bypasses were included. Double-barrel STA-MCA bypass was performed, as previously described, using a linear incision combined with a satellite incision for harvesting of the frontal and parietal STA branches.4,5 Both frontal and parietal STA branches were anastomosed separately under individual clamp times to separate MCA territories. Bypasses were performed with inversion of the cut dural flaps to allow for complementary indirect revascularization. Measurements were obtained before and after completion of the bypass. Prior to anastomosis to the recipient territory, “cut flow” was measured in the main STA trunk with downstream branches open (Figure 1).6 After the anastomoses were completed, bypass flow was measured in each of the donor branches and a total postanastomosis bypass flow was determined (Figure 2). The higher of these 2 values was labeled best observed flow (BOF). BOF was then analyzed to understand the maximum potential supply capacity of the double-barrel STA-MCA bypass technique. FIGURE 1. View largeDownload slide Intraoperative photograph of the dissected STA frontal and parietal branches. Cut flow measurements using an ultrasonic flow probe were performed on the trunk (indicated by white star) with both downstream branches open. FIGURE 1. View largeDownload slide Intraoperative photograph of the dissected STA frontal and parietal branches. Cut flow measurements using an ultrasonic flow probe were performed on the trunk (indicated by white star) with both downstream branches open. FIGURE 2. View largeDownload slide Intraoperative photograph showing blood flow monitoring with an ultrasonic flow probe after double-barrel STA-MCA bypass. Bypass flow was measured in each donor branch (indicated by white stars) and summated to arrive at a total bypass flow measurement. FIGURE 2. View largeDownload slide Intraoperative photograph showing blood flow monitoring with an ultrasonic flow probe after double-barrel STA-MCA bypass. Bypass flow was measured in each donor branch (indicated by white stars) and summated to arrive at a total bypass flow measurement. Recipient branches for bypass were selected using our previously described technique of flow-directed revascularization.4 In combination with preoperative imaging, indocyanine green (ICG) videoangiography (Zeiss Pentero Flow 800 microscope; Zeiss Corporation, Oberkochen, Germany/IC-Green Indocyanine Green dye; Akorn, Buffalo Grove, Illinois) was used to select recipient vessels based on both vessel suitability for bypass and recipient territory need for blood flow. Relative areas of hypoperfusion were identified qualitatively by noting relative delays in ICG filling and decreased overall levels of opacification. The recorded ICG signal was further analyzed using the Zeiss Flow 800 color flow tool to produce objective color maps and quantified intensity graphs. Patient charts were reviewed to assess incision healing and clinical outcome. IRB approval and patient consent were not required for this retrospective review. Modified Rankin scale scores were determined retrospectively from follow-up clinic note documentation. Postoperative CT and digital subtraction angiography were reviewed for assessment of bypass patency. RESULTS Analysis of our cerebrovascular registry identified 51 cases of STA-MCA bypass performed by the senior author at a single institution over 6 yr (2009-2015). In 21 of these cases, intraoperative flow probe measurements were documented. The previously described double-barrel technique was used in 17 of these bypasses, with anastomosis of both STA branches to MCA territories. In the remaining 4 cases, only one STA branch was available for bypass. In 3 patients, bypass surgeries were performed on both hemispheres, in separate settings. In total, flow data were available for 38 individual bypasses performed on 21 hemispheres in 18 patients. The mean age at time of surgery was 51 yr (range 29-79). A majority of patients were female (61%, 11/18). Bypass was performed most commonly for treatment of Moyamoya disease (43%) followed by extracranial carotid occlusion (33%) and intracranial occlusion or stenosis (24%). CT-perfusion studies were performed in all but 1 case. Loss of cerebrovascular reserve was confirmed in all extracranial carotid occlusion cases. Perfusion studies were performed with acetazolamide challenge except in patients felt to have acutely tenuous perfusion, such as in the case of bilateral carotid occlusion. Use of both terminal STA branches provided significantly more flow for bypass compared to the use of a single branch (mean BOF = 69 cc/min vs 39 cc/min, P < .001). All but 1 (94%) of the double-barrel STA-MCA bypasses had BOF >40 cc/min, and 53% (9/17) provided BOF ≥65 cc/min. The maximum BOF observed with double-barrel bypass was 120 cc/min. The maximum flow observed with single-branch bypass was 40 cc/min. In 7 cases, only a postanastomosis bypass flow measurement was available, and in 3 cases, only a cut flow measurement taken before anastomosis was available. In these situations, the available measurement was labeled BOF. In the remaining 11 cases for which both sets of measurements were available, completed bypass flows generally exceeded pre-bypass cut flows with an average cut flow index of 1.31 for double-barrel cases (range 0.57-2.39) and 0.92 for single-branch cases (range 0.75-1.56). Flow data are highlighted in Figure 3 and Table 1. Double-barrel surgeries took longer to perform compared to single-barrel cases (mean of 383 vs 287 min). FIGURE 3. View largeDownload slide Box plot of best observed flow (BOF) measured for double-barrel and single-barrel bypasses. Double-barrel bypasses provided significantly more mean BOF (69 cc/min vs 39 cc/min, P < .001). FIGURE 3. View largeDownload slide Box plot of best observed flow (BOF) measured for double-barrel and single-barrel bypasses. Double-barrel bypasses provided significantly more mean BOF (69 cc/min vs 39 cc/min, P < .001). TABLE 1. Comparison of Best Observed Flow and Maximum Flow between Single- and Double-barrel Bypasses STA-MCA barrels  n  Mean best observed flow  Maximum  P-value  Single  4  38.5 cc/min  40 cc/min    Double  17  69.2 cc/min  120 cc/min  <.001*  STA-MCA barrels  n  Mean best observed flow  Maximum  P-value  Single  4  38.5 cc/min  40 cc/min    Double  17  69.2 cc/min  120 cc/min  <.001*  View Large At a median follow-up of 11 mo, 89% of patients had a modified Rankin Scale7 ≤3 and were able to walk unassisted. Wound healing was excellent, and there were no cases of scalp necrosis or wound dehiscence. Postoperative imaging was available for assessment of 36 of the 38 performed bypasses. In double-barrel bypass cases, there was 94% patency (32 of 34) of branch anastomoses (Figure 4). There was 100% patency for the 4 cases of single-vessel STA1MCA bypass. One case was complicated by kinking of one of the bypassing branches of the STA from a subdural hematoma. This was successfully addressed with subdural evacuation and widening of the extracranial to intracranial bony corridor. There were no cases of intracerebral hemorrhage in either group. There were 2 self-resolving episodes of transient ischemic declines occurring 2 and 6 wk after surgery in the double-barrel group. FIGURE 4. View largeDownload slide Selective left ECA preoperative lateral and AP angiograms A, B and postoperative AP angiogram from a patient who had undergone double-barrel STA-MCA bypass C. The 3D-3D fusion D comprises volumes from the left ICA (red) and left ECA (white) that were combined, allowing for easy evaluation of the perfused territories. Arrows demonstrate the frontal and parietal branches of the STA, comprising the “double-barrel” bypass. FIGURE 4. View largeDownload slide Selective left ECA preoperative lateral and AP angiograms A, B and postoperative AP angiogram from a patient who had undergone double-barrel STA-MCA bypass C. The 3D-3D fusion D comprises volumes from the left ICA (red) and left ECA (white) that were combined, allowing for easy evaluation of the perfused territories. Arrows demonstrate the frontal and parietal branches of the STA, comprising the “double-barrel” bypass. DISCUSSION Initially described by Woringer and Kunlin,8 and later refined by Yasargil with Donaghy,9 STA-MCA bypass remains an important technique in the treatment of complex aneurysms, cranial base tumors, Moyamoya disease, and occlusive cerebrovascular disease. However, historically, STA-MCA bypass has been described by many authors as a low-flow system1,10 unsuitable in many situations in which greater amounts of flow are thought to be needed. High-Flow Bypasses and Reported Flow Rates “High-flow” bypass is traditionally performed using an interposition graft, either a harvested radial artery or saphenous vein, between the extracranial carotid artery and a recipient intracranial vessel. There are numerous variations in this extracranial-intracranial (EC-IC) technique.10–13 Common challenges when compared to conventional STA-MCA bypass include longer operating room time, additional incisions, graft harvest site morbidity, and lower patency rates.3 Recently, local and intracranial-to-intracranial (IC-IC) bypasses have been developed and advocated.14,15 Advantages include a completely intracranial bypass with fewer incisions and often no need for an interposition graft. However, these bypasses can be technically demanding due to the need to work in a deep operative field or at challenging angles. There is an additional risk by involving 2 intracranial circulations. Late graft occlusion can also be an issue.10 Authors have reported a wide variety of flow rates for different types of bypasses. In general, saphenous vein graft bypasses provide the greatest flow; STA and occipital artery bypasses, the lowest. Radial artery graft bypasses provide flow rates somewhere between STA and occipital artery bypasses and saphenous vein grafts. For STA-MCA bypass, authors have specifically noted mean flow rates ranging anywhere from 15 to 25 cc/min,2 <50 cc/min,15 and 20 to 70 cc/min.3 For radial artery interposition grafts, this same set of authors reported flow rates of 40 to 70 cc/min,2 50 to 150 cc/min,15 and 60 to 100 cc/min,3 respectively. For comparison, double-barrel STA-MCA bypass in this series demonstrated a mean BOF rate of 69 cc/min, ranging from 27 to 120 cc/min. A majority provided at least 65 cc/min. Table 2 summarizes these reported flow rates in the literature. TABLE 2. Comparison of Reported Flow Rates for Different Types of Cerebral Bypass Authors, reference & year  Conventional STA-MCA  Double-barrel STA-MCA  EC-IC radial artery graft  EC-IC saphenous vein graft  Liu et al, Neurosurg Focus 20032  15-25  –  40-70  70-140  Sekhar et al, Neurosurgery 200815  <50  –  50-150  100-250  Vajkoczy et al, Curr Opin Neurol 20093  20-70  –  60-100  100-200  Present series  35-40  27-120  –  –  Authors, reference & year  Conventional STA-MCA  Double-barrel STA-MCA  EC-IC radial artery graft  EC-IC saphenous vein graft  Liu et al, Neurosurg Focus 20032  15-25  –  40-70  70-140  Sekhar et al, Neurosurgery 200815  <50  –  50-150  100-250  Vajkoczy et al, Curr Opin Neurol 20093  20-70  –  60-100  100-200  Present series  35-40  27-120  –  –  All measurements are in cc/min. EC-IC = extracranial to intracranial bypass; STA-MCA = superficial temporal artery to middle cerebral artery bypass. View Large Double-Barrel Bypass: More is More “Double-barrel,”2,4,16 “double-vessel,”17 “two-limb,”18 “double-anastomosis,”19 or simply “double”5,20 STA-MCA bypass was described as early as 1974 by Reichman et al.21 The method was proposed as both a means to increase flow and a redundancy to ensure a patent bypass should one of the branch anastomoses fail.17 It is perhaps for this second reason that the double-barrel technique might not have become widely adopted, as high rates of patency were and continue to be achieved with single-branch STA-MCA bypass.17,22–24 However, regarding increased flow, double-barrel technique increases the effective diameter of STA-MCA bypass by using both STA terminal branches as donors. In modeling laminar blood flow, Poiseuille's law relates flow rate as a function of donor vessel radius raised to the fourth power. The diameter of the STA trunk is larger than the diameters of the STA terminal branches.25 This suggests that STA trunk capacity is being underutilized when bypassing from a single terminal branch. Indeed, previous authors have demonstrated that bypasses from the STA trunk provide significantly more bypass flow than bypasses from a single terminal STA branch.26,27 Consistent with the law of mass conservation,28 use of both STA terminal branches captures the larger bypass capacity of the STA trunk. In this series, at least 40 cc/min of total flow was observed in all but one double-barrel case, with a majority exceeding 65 cc/min. In contrast, the maximum flow observed with single-branch STA-MCA bypass in this series was 40 cc/min. How Much Flow, Needed Where? Much of the prior literature has focused on qualitative labeling of flow ranges achieved by different bypass techniques into low, intermediate, and high categories.2,3 In truth, there is high variability of actual bypass flow rates reflective of multiple factors, including size of the donor and recipient vessels, length of bypass, surface area of anastomosis, choice of interposition graft, and need for bypass flow based on preexisting collaterals and metabolic demands in the territory to be revascularized. Comparing the flow rate numbers in this series to those cited in the literature for other types of bypasses, double-barrel STA-MCA bypasses have a capacity (27-120 cc/min) similar to the lower range of radial artery graft bypasses (40-150 cc/min).2,3,15 Double-barrel STA-MCA bypass is therefore a consideration in situations usually reserved for “high-flow” bypasses such as part of trapping strategies done for treatment of complex skull base tumors and giant MCA or ICA aneurysms. While not included in this series, we have performed double-barrel STA-MCA bypass to the M2 divisions with trapping of a fusiform prebifurcation MCA aneurysm. Despite the preceding emphasis on flow quantification, an equally important consideration, particularly in cases done for ischemia, is where exactly bypass flow is introduced. Flow can be directed either distally or more proximally in the vascular tree (see Figure 5). Flow introduced distally relies on retrograde bypass flow to revascularize adjacent territories and is constrained by the smaller size of the recipient vessels. Flow introduced more proximally allows for a larger surface area of anastomosis and is less reliant on retrograde flow, but requires a more technically challenging bypass (deeper in the fissure with an interposition graft). FIGURE 5. View largeDownload slide Schematic outlining differences in anterograde and retrograde bypass flow in 3 different bypass strategies: A, single-vessel STA-MCA bypass, B, EC-IC bypass with interposition graft, and C, double-barrel STA-MCA bypass. Blue block arrows represent points of anastomosis. Solid green and dashed orange line arrows represent anterograde and retrograde flows, respectively. FIGURE 5. View largeDownload slide Schematic outlining differences in anterograde and retrograde bypass flow in 3 different bypass strategies: A, single-vessel STA-MCA bypass, B, EC-IC bypass with interposition graft, and C, double-barrel STA-MCA bypass. Blue block arrows represent points of anastomosis. Solid green and dashed orange line arrows represent anterograde and retrograde flows, respectively. Double-barrel bypass STA-MCA bypass allows for a compromise of these competing relationships. Higher total flow can be introduced superficially across multiple at-risk regions in a distributed fashion. Though hyperperfusion with double-barrel STA-MCA bypass has been reported,20 there were no instances of postoperative intracerebral hemorrhage in our series. In most cases, terminal STA branches were anastomosed to M4 vessels arising from separate superior and inferior MCA divisions. This may have allowed “load sharing” of higher total bypassed flow across different individual territories (see Figure 5). More research is needed, but in light of the results of single-vessel STA-MCA bypass in the EC-IC Bypass Trial22 and Carotid Occlusion Surgery Study,23 double-barrel bypass may represent a relevant consideration to reduce the risk of recurrent ipsilateral stroke in appropriately selected patients.19 Multiple methods can be utilized to assess where and how much flow is needed, including ultrasonic flow probe measurement and intraoperative ICG videoangiography.4,6 In contrast to traditional descriptions of bypass surgery in which the recipient vessel is chosen for purely technical reasons,29–32 a flow-directed strategy of choosing recipient vessels intraoperatively based on functional factors provides immediate revascularization to the territories most in need.4 CONCLUSION Double-barrel STA-MCA bypass provides significantly more flow than traditional single-branch STA-MCA bypass and allows flexibility in distributing flow across different territories. The range of flow rates seen with double-barrel STA-MCA bypass resembles those previously reported for “high-flow” radial artery interposition grafts. Objective intraoperative flow assessment should be used to tailor flow delivery to case requirements. Disclosures There are no funding sources, financial support, or industry affiliations to disclose. The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article. The contents of this paper were presented as an oral presentation at the AANS/CNS Joint Cerebrovascular Section Annual Meeting, February 16, 2016, in Los Angeles, California. REFERENCES 1. Gross BA, Du R. STA-MCA bypass. Acta Neurochir (Wien) . 2012; 154( 8): 1463- 1467. Google Scholar CrossRef Search ADS PubMed  2. Liu JK, Kan P, Karwande SV, Couldwell WT. Conduits for cerebrovascular bypass and lessons learned from the cardiovascular experience. Neurosurg Focus . 2003; 14( 3): e3. Google Scholar PubMed  3. Vajkoczy P. Revival of extra-intracranial bypass surgery. Curr Opin Neurol . 2009; 22( 1): 90- 95. Google Scholar CrossRef Search ADS PubMed  4. Duckworth EAM, Rao VY, Patel AJ. Double-barrel bypass for cerebral ischemia: technique, rationale, and preliminary experience with 10 consecutive cases. Neurosurgery . 2013; 73: ons30- ons38. Google Scholar CrossRef Search ADS PubMed  5. Yoshimura S, Egashira Y, Enomoto Y, Yamada K, Yano H, Iwama T. Superficial temporal artery to middle cerebral artery double bypass via a small craniotomy. Neurol Med Chir (Tokyo) . 2010; 50( 10): 956- 959. Google Scholar CrossRef Search ADS PubMed  6. Amin-Hanjani S, Alaraj A, Charbel FT. Flow replacement bypass for aneurysms: decision-making using intraoperative blood flow measurements. Acta Neurochir (Wien) . 2010; 152( 6): 1021- 1032. Google Scholar CrossRef Search ADS PubMed  7. van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJ, van Gijn J. Interobserver agreement for the assessment of handicap in stroke patients. Stroke J Cereb Circ . 1988; 19( 5): 604- 607. Google Scholar CrossRef Search ADS   8. Woringer E, Kunlin J. Anastomosis between the common carotid and the intracranial carotid or the sylvian artery by a graft, using the suspended suture technic. Neurochirurgie . 1963; 9( 2): 181- 188. Google Scholar PubMed  9. Yasargil MG. Aneurysms, arteriovenous malformations and fistulae. In: Microsurgery Applied to Neurosurgery . Georg Thieme Verlag Stuttgart; 1969; 119- 150. 10. Ramanathan D, Temkin N, Kim LJ, Ghodke B, Sekhar LN. Cerebral bypasses for complex aneurysms and tumors: long-term results and graft management strategies. Neurosurgery . 2012; 70( 6): 1442- 1457. Google Scholar CrossRef Search ADS PubMed  11. Bulsara KR, Patel T, Fukushima T. Cerebral bypass surgery for skull base lesions: technical notes incorporating lessons learned over two decades. Neurosurg Focus . 2008; 24( 2): E11. Google Scholar CrossRef Search ADS PubMed  12. Couldwell WT, Taussky P, Sivakumar W. Submandibular high-flow bypass in the treatment of skull base lesions: an analysis of long-term outcome. Neurosurgery . 2012; 71( 3): 645- 651. Google Scholar CrossRef Search ADS PubMed  13. Nossek E, Costantino PD, Eisenberg M et al.   Internal maxillary artery-middle cerebral artery bypass: infratemporal approach for subcranial-intracranial (SC-IC) bypass. Neurosurgery . 2014; 75( 1): 87- 95. Google Scholar CrossRef Search ADS PubMed  14. Davies JM, Lawton MT. Advances in open microsurgery for cerebral aneurysms. Neurosurgery . 2014; 74( 2): S7- S16. Google Scholar CrossRef Search ADS PubMed  15. Sekhar LN, Natarajan SK, Ellenbogen RG, Ghodke B. Cerebral revascularization for ischemia, aneurysms, and cranial base tumors. Neurosurgery . 2008; 62( 6): SHC1373- SHC1410. 16. Lawton MT, Hamilton MG, Morcos JJ, Spetzler RF. Revascularization and aneurysm surgery: current techniques, indications, and outcome. Neurosurgery . 1996; 38( 1): 83- 92; discussion 92-94. Google Scholar CrossRef Search ADS PubMed  17. Reichman OH, Anderson RE, Roberts TS, Heilbrun MP. The treatment of intracranial occlusive cerebrovascular disease by STA-cortical MCA anastomosis. Microneurosurg Handa H Ed . 1975: 31- 46. 18. Newell DW, Dailey AT, Skirboll SL. Intracranial vascular anastomosis using the microanastomotic system. J Neurosurg . 1998; 89( 4): 676- 681. Google Scholar CrossRef Search ADS PubMed  19. Kuroda S, Kawabori M, Hirata K et al.   Clinical significance of STA-MCA double anastomosis for hemodynamic compromise in post-JET/COSS era. Acta Neurochir (Wien) . 2013; 156( 1): 77- 83. Google Scholar CrossRef Search ADS PubMed  20. Matano F, Murai Y, Tanikawa R et al.   Intraoperative middle cerebral artery pressure measurements during superficial temporal artery to middle cerebral artery bypass procedures in patients with cerebral atherosclerotic disease. J Neurosurg . 2016; 125( 6): 1367- 1373. Google Scholar CrossRef Search ADS PubMed  21. Reichman OH, Davis DO, Roberts TS, Satovick RM. Anastomosis between STA and cortical branch of MCA for the treatment of occlusive cerebrovascular disease. Reconstr Surg Brain Arter Publ House Hung Acad Sci . 1974: 201- 218. 22. EC/IC Bypass Study group. Failure of extracranial—intracranial arterial bypass to reduce the risk of ischemic stroke. N Engl J Med . 1985; 313( 19): 1191- 1200. CrossRef Search ADS PubMed  23. Powers WJ, Clarke WR, Grubb RL et al.   Extracranial-intracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: the carotid occlusion surgery study randomized trial. JAMA . 2011; 306( 18): 1983- 1992. Google Scholar CrossRef Search ADS PubMed  24. Vilela MD, Newell DW. Superficial temporal artery to middle cerebral artery bypass: past, present, and future. Neurosurg Focus . 2008; 24( 2): E2. Google Scholar CrossRef Search ADS PubMed  25. Pinar YA, Govsa F. Anatomy of the superficial temporal artery and its branches: its importance for surgery. Surg Radiol Anat . 2006; 28( 3): 248- 253. Google Scholar CrossRef Search ADS PubMed  26. Alaraj A, Ashley WW, Charbel FT, Amin-Hanjani S. The superficial temporal artery trunk as a donor vessel in cerebral revascularization: benefits and pitfalls. Neurosurg Focus . 2008; 24( 2): E7. Google Scholar CrossRef Search ADS PubMed  27. Kaku Y, Funatsu N, Tsujimoto M, Yamashita K, Kokuzawa J. STA-MCA/STA-PCA bypass using short interposition vein graft. Acta Neurochir Suppl . 2014; 119: 79- 82. Google Scholar PubMed  28. Gabryś E, Rybaczuk M, Kędzia A. Blood flow simulation through fractal models of circulatory system. Chaos Solitons Fractals . 2006; 27( 1): 1- 7. Google Scholar CrossRef Search ADS   29. Wanebo JE, Zabramski JM, Spetzler RF. Superficial temporal artery-to-middle cerebral artery bypass grafting for cerebral revascularization. Neurosurgery . 2004; 55( 2): 395- 398; discussion 398-399. Google Scholar CrossRef Search ADS PubMed  30. Newell DW, Vilela MD. Superficial temporal artery to middle cerebral artery bypass. Neurosurgery . 2004; 54( 6): 1441-1448-1449. Google Scholar CrossRef Search ADS   31. Charbel FT, Meglio G, Amin-Hanjani S. Superficial temporal artery-to-middle cerebral artery bypass. Neurosurgery . 2005; 56( suppl 1): 186- 190; discussion 186-190. Google Scholar PubMed  32. Kadri PAS, Krisht AF, Gandhi GK. An anatomic mathematical measurement to find an adequate recipient M4 branch for superficial temporal artery to middle cerebral artery bypass surgery. Neurosurgery . 2007; 61( suppl 3): 74- 78; discussion 78. Google Scholar PubMed  COMMENTS Brain revascularization still represents a valuable option for flow augmentation in cases of Moyamoya disease and in selected cases of ICA occlusion with hemodynamic compromise, as well as for flow replacement. Traditionally, STA-MCA bypass has been considered a method to deliver only low flow in the brain territory, with a range of 15-70 cc/min, thus being a suitable option only for ischemic cases. However, nowadays there is the possibility to tailor the surgical revascularization options to both the brain demand and the real bypass flow capacity. This can be obtained by the use of new technologies like ICG video angiography with FLOW800 analysis and Transonic Probe measurements. In this way, the traditional equation ischemia=low flow bypass and replacement=high flow bypass should be modified and adapted to the real need of the brain and the actual flow possibilities of the bypass. The authors should be congratulated for their efforts in providing new insights into this matter. In particular, they showed in a large series of double-barrel STA-MCA bypass performed for ischemic cases (most of them being Moyamoya disease) that the flow possibilities are much higher than expected for a so-called “low-flow” bypass, with value as high as 120 cc/min and in the majority of cases above 65 cc/min. In some of their cases this was only a theoretical possibility as the flow measurements were performed only as “cut-flow”. However, this is a very important study because it confirms that the double-barrel technique in STA-MCA bypass can be used even with a high-flow demand. This maybe is not the case for all ischemic indication, like in Moyamoya disease (the use of ICG video angiography could be of great help to identify the patients in which multiple brain territories need to be revascularized and thus the double bypass could be of great help) but, more importantly, in cases of flow replacement, particularly for complex intracranial aneurysms. The use of a significantly simpler procedure, like the double-barrel STA-MCA bypass is compared to EC-IC bypasses with interposition grafts, should assure in selected cases a high rate of success with a significantly low percentage of complications. Francesco Acerbi Milan, Italy The authors demonstrate that double-barrel STA-MCA bypasses can achieve high flows. They report the results of intraoperative flow probe measurements in 21 cases, 17 of which were double-barrel bypasses and 4 of which were single-branch bypasses. Using a single branch, the average best observed flow (BOF) was 39 cc/min, and the maximum was 40 cc/min. By contrast, double-barrel bypasses resulted in an average BOF of 69 cc/min and a maximum of 120 cc/min. In the literature, radial artery interpositional grafts have been reported to have flow rates between 40 to 150 cc/min. Saphenous vein grafts are associated with the highest flow rates (70 to 250 cc/min). It is both interesting and surprising that the radial artery interpositional graft is not associated with flows dramatically higher than those of the STA double-barrel bypass. Certainly, the STA double barrel bypass is surgically easier than the radial artery interposition graft, which requires a cervical incision, tunneling of the artery, and an additional proximal anastomosis in the case of 2 distal MCA recipients vessels. This study is helpful in selecting a bypass donor compatible with the flow needs of individual patients. Rafael J. Tamargo Baltimore, Maryland Copyright © 2017 by the Congress of Neurological Surgeons http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Operative Neurosurgery Oxford University Press

Double-Barrel Superficial Temporal Artery-Middle Cerebral Artery Bypass: Can It Be Considered “High-Flow?”

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Copyright © 2017 by the Congress of Neurological Surgeons
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Abstract

Abstract BACKGROUND Traditionally, superficial temporal artery-middle cerebral artery (STA-MCA) bypass uses one STA branch. Its augmentation of flow has classically been described as “low flow.” In a double-barrel STA-MCA bypass, however, both branches of the STA are utilized. Here we hypothesize that this should not be considered “low flow.” OBJECTIVE To review quantitative flow data from our cases and investigate the impact of double-barrel STA-MCA bypass on total flow augmentation, and to assess whether double-barrel STA-MCA bypass might be useful in situations that traditionally demand more complex bypass strategies. METHODS Intraoperative flow probe measurements from STA-MCA bypass cases were retrospectively tabulated and compared. Cut flow and bypass flow measurements were, respectively, taken before and after completion of anastomoses. The higher value was labeled best observed flow (BOF). RESULTS We identified 21 STA-MCA bypass cases with available intraoperative flow probe measurements, of which 17 utilized double-barrel technique. Only 1 STA branch was available in 4 cases. Significantly higher average BOF was seen when utilizing 2 STA branches (69 vs 39 cc/min, P < .001). A majority (9/17) of double-barrel bypasses provided BOF ≥ 65 cc/min (120 cc/min maximum). The single branch bypass maximum BOF was 40 cc/min. CONCLUSION Double-barrel bypass technique significantly enhances STA-MCA flow capacity and may be useful in situations in which a high-flow bypass is needed. The 2 efferent limbs allow flexibility in distributing flow across separate at-risk territories. The method compares favorably to other descriptions of high-flow bypass without the morbidity of graft harvest or an additional cervical incision. Cerebral bypass, Double-barrel, Flow rate, High-flow, STA-MCA ABBREVIATIONS ABBREVIATIONS BOF best observed flow EC-IC extracranial-intracranial IC-IC intracranial-to-intracranial ICG indocyanine green STA superficial temporal artery STA-MCA superficial temporal artery-middle cerebral artery In most patients, the superficial temporal artery (STA) has 2 major branches, the frontal and parietal. Superficial temporal artery-middle cerebral artery (STA-MCA) bypass is typically performed using only 1 of these terminal STA branches.1 Its augmentation of flow has often been described as “low flow.”2,3 Over the last 6 yr, we have adopted a “double-barrel” technique in which both branches of the STA are utilized as our default bypass option.4 Single-branch STA-MCA bypass was performed only in patients missing a suitable frontal or parietal STA branch. In this study, we investigate the impact of this method on total flow augmentation and assess whether double-barrel STA-MCA bypass might be useful in situations that traditionally demand more complex bypass strategies. To our knowledge, this is the largest series describing flow data for double-barrel STA-MCA bypass. METHODS An intraoperative flow probe (Transonic Systems, Ithaca, New York) was used to measure flow rates in our cases of STA-MCA bypass. These were retrospectively tabulated and compared. Cases of both traditional single-branch and double-barrel STA-MCA bypasses were included. Double-barrel STA-MCA bypass was performed, as previously described, using a linear incision combined with a satellite incision for harvesting of the frontal and parietal STA branches.4,5 Both frontal and parietal STA branches were anastomosed separately under individual clamp times to separate MCA territories. Bypasses were performed with inversion of the cut dural flaps to allow for complementary indirect revascularization. Measurements were obtained before and after completion of the bypass. Prior to anastomosis to the recipient territory, “cut flow” was measured in the main STA trunk with downstream branches open (Figure 1).6 After the anastomoses were completed, bypass flow was measured in each of the donor branches and a total postanastomosis bypass flow was determined (Figure 2). The higher of these 2 values was labeled best observed flow (BOF). BOF was then analyzed to understand the maximum potential supply capacity of the double-barrel STA-MCA bypass technique. FIGURE 1. View largeDownload slide Intraoperative photograph of the dissected STA frontal and parietal branches. Cut flow measurements using an ultrasonic flow probe were performed on the trunk (indicated by white star) with both downstream branches open. FIGURE 1. View largeDownload slide Intraoperative photograph of the dissected STA frontal and parietal branches. Cut flow measurements using an ultrasonic flow probe were performed on the trunk (indicated by white star) with both downstream branches open. FIGURE 2. View largeDownload slide Intraoperative photograph showing blood flow monitoring with an ultrasonic flow probe after double-barrel STA-MCA bypass. Bypass flow was measured in each donor branch (indicated by white stars) and summated to arrive at a total bypass flow measurement. FIGURE 2. View largeDownload slide Intraoperative photograph showing blood flow monitoring with an ultrasonic flow probe after double-barrel STA-MCA bypass. Bypass flow was measured in each donor branch (indicated by white stars) and summated to arrive at a total bypass flow measurement. Recipient branches for bypass were selected using our previously described technique of flow-directed revascularization.4 In combination with preoperative imaging, indocyanine green (ICG) videoangiography (Zeiss Pentero Flow 800 microscope; Zeiss Corporation, Oberkochen, Germany/IC-Green Indocyanine Green dye; Akorn, Buffalo Grove, Illinois) was used to select recipient vessels based on both vessel suitability for bypass and recipient territory need for blood flow. Relative areas of hypoperfusion were identified qualitatively by noting relative delays in ICG filling and decreased overall levels of opacification. The recorded ICG signal was further analyzed using the Zeiss Flow 800 color flow tool to produce objective color maps and quantified intensity graphs. Patient charts were reviewed to assess incision healing and clinical outcome. IRB approval and patient consent were not required for this retrospective review. Modified Rankin scale scores were determined retrospectively from follow-up clinic note documentation. Postoperative CT and digital subtraction angiography were reviewed for assessment of bypass patency. RESULTS Analysis of our cerebrovascular registry identified 51 cases of STA-MCA bypass performed by the senior author at a single institution over 6 yr (2009-2015). In 21 of these cases, intraoperative flow probe measurements were documented. The previously described double-barrel technique was used in 17 of these bypasses, with anastomosis of both STA branches to MCA territories. In the remaining 4 cases, only one STA branch was available for bypass. In 3 patients, bypass surgeries were performed on both hemispheres, in separate settings. In total, flow data were available for 38 individual bypasses performed on 21 hemispheres in 18 patients. The mean age at time of surgery was 51 yr (range 29-79). A majority of patients were female (61%, 11/18). Bypass was performed most commonly for treatment of Moyamoya disease (43%) followed by extracranial carotid occlusion (33%) and intracranial occlusion or stenosis (24%). CT-perfusion studies were performed in all but 1 case. Loss of cerebrovascular reserve was confirmed in all extracranial carotid occlusion cases. Perfusion studies were performed with acetazolamide challenge except in patients felt to have acutely tenuous perfusion, such as in the case of bilateral carotid occlusion. Use of both terminal STA branches provided significantly more flow for bypass compared to the use of a single branch (mean BOF = 69 cc/min vs 39 cc/min, P < .001). All but 1 (94%) of the double-barrel STA-MCA bypasses had BOF >40 cc/min, and 53% (9/17) provided BOF ≥65 cc/min. The maximum BOF observed with double-barrel bypass was 120 cc/min. The maximum flow observed with single-branch bypass was 40 cc/min. In 7 cases, only a postanastomosis bypass flow measurement was available, and in 3 cases, only a cut flow measurement taken before anastomosis was available. In these situations, the available measurement was labeled BOF. In the remaining 11 cases for which both sets of measurements were available, completed bypass flows generally exceeded pre-bypass cut flows with an average cut flow index of 1.31 for double-barrel cases (range 0.57-2.39) and 0.92 for single-branch cases (range 0.75-1.56). Flow data are highlighted in Figure 3 and Table 1. Double-barrel surgeries took longer to perform compared to single-barrel cases (mean of 383 vs 287 min). FIGURE 3. View largeDownload slide Box plot of best observed flow (BOF) measured for double-barrel and single-barrel bypasses. Double-barrel bypasses provided significantly more mean BOF (69 cc/min vs 39 cc/min, P < .001). FIGURE 3. View largeDownload slide Box plot of best observed flow (BOF) measured for double-barrel and single-barrel bypasses. Double-barrel bypasses provided significantly more mean BOF (69 cc/min vs 39 cc/min, P < .001). TABLE 1. Comparison of Best Observed Flow and Maximum Flow between Single- and Double-barrel Bypasses STA-MCA barrels  n  Mean best observed flow  Maximum  P-value  Single  4  38.5 cc/min  40 cc/min    Double  17  69.2 cc/min  120 cc/min  <.001*  STA-MCA barrels  n  Mean best observed flow  Maximum  P-value  Single  4  38.5 cc/min  40 cc/min    Double  17  69.2 cc/min  120 cc/min  <.001*  View Large At a median follow-up of 11 mo, 89% of patients had a modified Rankin Scale7 ≤3 and were able to walk unassisted. Wound healing was excellent, and there were no cases of scalp necrosis or wound dehiscence. Postoperative imaging was available for assessment of 36 of the 38 performed bypasses. In double-barrel bypass cases, there was 94% patency (32 of 34) of branch anastomoses (Figure 4). There was 100% patency for the 4 cases of single-vessel STA1MCA bypass. One case was complicated by kinking of one of the bypassing branches of the STA from a subdural hematoma. This was successfully addressed with subdural evacuation and widening of the extracranial to intracranial bony corridor. There were no cases of intracerebral hemorrhage in either group. There were 2 self-resolving episodes of transient ischemic declines occurring 2 and 6 wk after surgery in the double-barrel group. FIGURE 4. View largeDownload slide Selective left ECA preoperative lateral and AP angiograms A, B and postoperative AP angiogram from a patient who had undergone double-barrel STA-MCA bypass C. The 3D-3D fusion D comprises volumes from the left ICA (red) and left ECA (white) that were combined, allowing for easy evaluation of the perfused territories. Arrows demonstrate the frontal and parietal branches of the STA, comprising the “double-barrel” bypass. FIGURE 4. View largeDownload slide Selective left ECA preoperative lateral and AP angiograms A, B and postoperative AP angiogram from a patient who had undergone double-barrel STA-MCA bypass C. The 3D-3D fusion D comprises volumes from the left ICA (red) and left ECA (white) that were combined, allowing for easy evaluation of the perfused territories. Arrows demonstrate the frontal and parietal branches of the STA, comprising the “double-barrel” bypass. DISCUSSION Initially described by Woringer and Kunlin,8 and later refined by Yasargil with Donaghy,9 STA-MCA bypass remains an important technique in the treatment of complex aneurysms, cranial base tumors, Moyamoya disease, and occlusive cerebrovascular disease. However, historically, STA-MCA bypass has been described by many authors as a low-flow system1,10 unsuitable in many situations in which greater amounts of flow are thought to be needed. High-Flow Bypasses and Reported Flow Rates “High-flow” bypass is traditionally performed using an interposition graft, either a harvested radial artery or saphenous vein, between the extracranial carotid artery and a recipient intracranial vessel. There are numerous variations in this extracranial-intracranial (EC-IC) technique.10–13 Common challenges when compared to conventional STA-MCA bypass include longer operating room time, additional incisions, graft harvest site morbidity, and lower patency rates.3 Recently, local and intracranial-to-intracranial (IC-IC) bypasses have been developed and advocated.14,15 Advantages include a completely intracranial bypass with fewer incisions and often no need for an interposition graft. However, these bypasses can be technically demanding due to the need to work in a deep operative field or at challenging angles. There is an additional risk by involving 2 intracranial circulations. Late graft occlusion can also be an issue.10 Authors have reported a wide variety of flow rates for different types of bypasses. In general, saphenous vein graft bypasses provide the greatest flow; STA and occipital artery bypasses, the lowest. Radial artery graft bypasses provide flow rates somewhere between STA and occipital artery bypasses and saphenous vein grafts. For STA-MCA bypass, authors have specifically noted mean flow rates ranging anywhere from 15 to 25 cc/min,2 <50 cc/min,15 and 20 to 70 cc/min.3 For radial artery interposition grafts, this same set of authors reported flow rates of 40 to 70 cc/min,2 50 to 150 cc/min,15 and 60 to 100 cc/min,3 respectively. For comparison, double-barrel STA-MCA bypass in this series demonstrated a mean BOF rate of 69 cc/min, ranging from 27 to 120 cc/min. A majority provided at least 65 cc/min. Table 2 summarizes these reported flow rates in the literature. TABLE 2. Comparison of Reported Flow Rates for Different Types of Cerebral Bypass Authors, reference & year  Conventional STA-MCA  Double-barrel STA-MCA  EC-IC radial artery graft  EC-IC saphenous vein graft  Liu et al, Neurosurg Focus 20032  15-25  –  40-70  70-140  Sekhar et al, Neurosurgery 200815  <50  –  50-150  100-250  Vajkoczy et al, Curr Opin Neurol 20093  20-70  –  60-100  100-200  Present series  35-40  27-120  –  –  Authors, reference & year  Conventional STA-MCA  Double-barrel STA-MCA  EC-IC radial artery graft  EC-IC saphenous vein graft  Liu et al, Neurosurg Focus 20032  15-25  –  40-70  70-140  Sekhar et al, Neurosurgery 200815  <50  –  50-150  100-250  Vajkoczy et al, Curr Opin Neurol 20093  20-70  –  60-100  100-200  Present series  35-40  27-120  –  –  All measurements are in cc/min. EC-IC = extracranial to intracranial bypass; STA-MCA = superficial temporal artery to middle cerebral artery bypass. View Large Double-Barrel Bypass: More is More “Double-barrel,”2,4,16 “double-vessel,”17 “two-limb,”18 “double-anastomosis,”19 or simply “double”5,20 STA-MCA bypass was described as early as 1974 by Reichman et al.21 The method was proposed as both a means to increase flow and a redundancy to ensure a patent bypass should one of the branch anastomoses fail.17 It is perhaps for this second reason that the double-barrel technique might not have become widely adopted, as high rates of patency were and continue to be achieved with single-branch STA-MCA bypass.17,22–24 However, regarding increased flow, double-barrel technique increases the effective diameter of STA-MCA bypass by using both STA terminal branches as donors. In modeling laminar blood flow, Poiseuille's law relates flow rate as a function of donor vessel radius raised to the fourth power. The diameter of the STA trunk is larger than the diameters of the STA terminal branches.25 This suggests that STA trunk capacity is being underutilized when bypassing from a single terminal branch. Indeed, previous authors have demonstrated that bypasses from the STA trunk provide significantly more bypass flow than bypasses from a single terminal STA branch.26,27 Consistent with the law of mass conservation,28 use of both STA terminal branches captures the larger bypass capacity of the STA trunk. In this series, at least 40 cc/min of total flow was observed in all but one double-barrel case, with a majority exceeding 65 cc/min. In contrast, the maximum flow observed with single-branch STA-MCA bypass in this series was 40 cc/min. How Much Flow, Needed Where? Much of the prior literature has focused on qualitative labeling of flow ranges achieved by different bypass techniques into low, intermediate, and high categories.2,3 In truth, there is high variability of actual bypass flow rates reflective of multiple factors, including size of the donor and recipient vessels, length of bypass, surface area of anastomosis, choice of interposition graft, and need for bypass flow based on preexisting collaterals and metabolic demands in the territory to be revascularized. Comparing the flow rate numbers in this series to those cited in the literature for other types of bypasses, double-barrel STA-MCA bypasses have a capacity (27-120 cc/min) similar to the lower range of radial artery graft bypasses (40-150 cc/min).2,3,15 Double-barrel STA-MCA bypass is therefore a consideration in situations usually reserved for “high-flow” bypasses such as part of trapping strategies done for treatment of complex skull base tumors and giant MCA or ICA aneurysms. While not included in this series, we have performed double-barrel STA-MCA bypass to the M2 divisions with trapping of a fusiform prebifurcation MCA aneurysm. Despite the preceding emphasis on flow quantification, an equally important consideration, particularly in cases done for ischemia, is where exactly bypass flow is introduced. Flow can be directed either distally or more proximally in the vascular tree (see Figure 5). Flow introduced distally relies on retrograde bypass flow to revascularize adjacent territories and is constrained by the smaller size of the recipient vessels. Flow introduced more proximally allows for a larger surface area of anastomosis and is less reliant on retrograde flow, but requires a more technically challenging bypass (deeper in the fissure with an interposition graft). FIGURE 5. View largeDownload slide Schematic outlining differences in anterograde and retrograde bypass flow in 3 different bypass strategies: A, single-vessel STA-MCA bypass, B, EC-IC bypass with interposition graft, and C, double-barrel STA-MCA bypass. Blue block arrows represent points of anastomosis. Solid green and dashed orange line arrows represent anterograde and retrograde flows, respectively. FIGURE 5. View largeDownload slide Schematic outlining differences in anterograde and retrograde bypass flow in 3 different bypass strategies: A, single-vessel STA-MCA bypass, B, EC-IC bypass with interposition graft, and C, double-barrel STA-MCA bypass. Blue block arrows represent points of anastomosis. Solid green and dashed orange line arrows represent anterograde and retrograde flows, respectively. Double-barrel bypass STA-MCA bypass allows for a compromise of these competing relationships. Higher total flow can be introduced superficially across multiple at-risk regions in a distributed fashion. Though hyperperfusion with double-barrel STA-MCA bypass has been reported,20 there were no instances of postoperative intracerebral hemorrhage in our series. In most cases, terminal STA branches were anastomosed to M4 vessels arising from separate superior and inferior MCA divisions. This may have allowed “load sharing” of higher total bypassed flow across different individual territories (see Figure 5). More research is needed, but in light of the results of single-vessel STA-MCA bypass in the EC-IC Bypass Trial22 and Carotid Occlusion Surgery Study,23 double-barrel bypass may represent a relevant consideration to reduce the risk of recurrent ipsilateral stroke in appropriately selected patients.19 Multiple methods can be utilized to assess where and how much flow is needed, including ultrasonic flow probe measurement and intraoperative ICG videoangiography.4,6 In contrast to traditional descriptions of bypass surgery in which the recipient vessel is chosen for purely technical reasons,29–32 a flow-directed strategy of choosing recipient vessels intraoperatively based on functional factors provides immediate revascularization to the territories most in need.4 CONCLUSION Double-barrel STA-MCA bypass provides significantly more flow than traditional single-branch STA-MCA bypass and allows flexibility in distributing flow across different territories. The range of flow rates seen with double-barrel STA-MCA bypass resembles those previously reported for “high-flow” radial artery interposition grafts. Objective intraoperative flow assessment should be used to tailor flow delivery to case requirements. Disclosures There are no funding sources, financial support, or industry affiliations to disclose. The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article. The contents of this paper were presented as an oral presentation at the AANS/CNS Joint Cerebrovascular Section Annual Meeting, February 16, 2016, in Los Angeles, California. REFERENCES 1. Gross BA, Du R. STA-MCA bypass. Acta Neurochir (Wien) . 2012; 154( 8): 1463- 1467. Google Scholar CrossRef Search ADS PubMed  2. Liu JK, Kan P, Karwande SV, Couldwell WT. Conduits for cerebrovascular bypass and lessons learned from the cardiovascular experience. Neurosurg Focus . 2003; 14( 3): e3. Google Scholar PubMed  3. Vajkoczy P. Revival of extra-intracranial bypass surgery. Curr Opin Neurol . 2009; 22( 1): 90- 95. Google Scholar CrossRef Search ADS PubMed  4. Duckworth EAM, Rao VY, Patel AJ. Double-barrel bypass for cerebral ischemia: technique, rationale, and preliminary experience with 10 consecutive cases. Neurosurgery . 2013; 73: ons30- ons38. Google Scholar CrossRef Search ADS PubMed  5. Yoshimura S, Egashira Y, Enomoto Y, Yamada K, Yano H, Iwama T. Superficial temporal artery to middle cerebral artery double bypass via a small craniotomy. Neurol Med Chir (Tokyo) . 2010; 50( 10): 956- 959. Google Scholar CrossRef Search ADS PubMed  6. Amin-Hanjani S, Alaraj A, Charbel FT. Flow replacement bypass for aneurysms: decision-making using intraoperative blood flow measurements. Acta Neurochir (Wien) . 2010; 152( 6): 1021- 1032. Google Scholar CrossRef Search ADS PubMed  7. van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJ, van Gijn J. Interobserver agreement for the assessment of handicap in stroke patients. Stroke J Cereb Circ . 1988; 19( 5): 604- 607. Google Scholar CrossRef Search ADS   8. Woringer E, Kunlin J. Anastomosis between the common carotid and the intracranial carotid or the sylvian artery by a graft, using the suspended suture technic. Neurochirurgie . 1963; 9( 2): 181- 188. Google Scholar PubMed  9. Yasargil MG. Aneurysms, arteriovenous malformations and fistulae. In: Microsurgery Applied to Neurosurgery . Georg Thieme Verlag Stuttgart; 1969; 119- 150. 10. Ramanathan D, Temkin N, Kim LJ, Ghodke B, Sekhar LN. Cerebral bypasses for complex aneurysms and tumors: long-term results and graft management strategies. Neurosurgery . 2012; 70( 6): 1442- 1457. Google Scholar CrossRef Search ADS PubMed  11. Bulsara KR, Patel T, Fukushima T. Cerebral bypass surgery for skull base lesions: technical notes incorporating lessons learned over two decades. Neurosurg Focus . 2008; 24( 2): E11. Google Scholar CrossRef Search ADS PubMed  12. Couldwell WT, Taussky P, Sivakumar W. Submandibular high-flow bypass in the treatment of skull base lesions: an analysis of long-term outcome. Neurosurgery . 2012; 71( 3): 645- 651. Google Scholar CrossRef Search ADS PubMed  13. Nossek E, Costantino PD, Eisenberg M et al.   Internal maxillary artery-middle cerebral artery bypass: infratemporal approach for subcranial-intracranial (SC-IC) bypass. Neurosurgery . 2014; 75( 1): 87- 95. Google Scholar CrossRef Search ADS PubMed  14. Davies JM, Lawton MT. Advances in open microsurgery for cerebral aneurysms. Neurosurgery . 2014; 74( 2): S7- S16. Google Scholar CrossRef Search ADS PubMed  15. Sekhar LN, Natarajan SK, Ellenbogen RG, Ghodke B. Cerebral revascularization for ischemia, aneurysms, and cranial base tumors. Neurosurgery . 2008; 62( 6): SHC1373- SHC1410. 16. Lawton MT, Hamilton MG, Morcos JJ, Spetzler RF. Revascularization and aneurysm surgery: current techniques, indications, and outcome. Neurosurgery . 1996; 38( 1): 83- 92; discussion 92-94. Google Scholar CrossRef Search ADS PubMed  17. Reichman OH, Anderson RE, Roberts TS, Heilbrun MP. The treatment of intracranial occlusive cerebrovascular disease by STA-cortical MCA anastomosis. Microneurosurg Handa H Ed . 1975: 31- 46. 18. Newell DW, Dailey AT, Skirboll SL. Intracranial vascular anastomosis using the microanastomotic system. J Neurosurg . 1998; 89( 4): 676- 681. Google Scholar CrossRef Search ADS PubMed  19. Kuroda S, Kawabori M, Hirata K et al.   Clinical significance of STA-MCA double anastomosis for hemodynamic compromise in post-JET/COSS era. Acta Neurochir (Wien) . 2013; 156( 1): 77- 83. Google Scholar CrossRef Search ADS PubMed  20. Matano F, Murai Y, Tanikawa R et al.   Intraoperative middle cerebral artery pressure measurements during superficial temporal artery to middle cerebral artery bypass procedures in patients with cerebral atherosclerotic disease. J Neurosurg . 2016; 125( 6): 1367- 1373. Google Scholar CrossRef Search ADS PubMed  21. Reichman OH, Davis DO, Roberts TS, Satovick RM. Anastomosis between STA and cortical branch of MCA for the treatment of occlusive cerebrovascular disease. Reconstr Surg Brain Arter Publ House Hung Acad Sci . 1974: 201- 218. 22. EC/IC Bypass Study group. Failure of extracranial—intracranial arterial bypass to reduce the risk of ischemic stroke. N Engl J Med . 1985; 313( 19): 1191- 1200. CrossRef Search ADS PubMed  23. Powers WJ, Clarke WR, Grubb RL et al.   Extracranial-intracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: the carotid occlusion surgery study randomized trial. JAMA . 2011; 306( 18): 1983- 1992. Google Scholar CrossRef Search ADS PubMed  24. Vilela MD, Newell DW. Superficial temporal artery to middle cerebral artery bypass: past, present, and future. Neurosurg Focus . 2008; 24( 2): E2. Google Scholar CrossRef Search ADS PubMed  25. Pinar YA, Govsa F. Anatomy of the superficial temporal artery and its branches: its importance for surgery. Surg Radiol Anat . 2006; 28( 3): 248- 253. Google Scholar CrossRef Search ADS PubMed  26. Alaraj A, Ashley WW, Charbel FT, Amin-Hanjani S. The superficial temporal artery trunk as a donor vessel in cerebral revascularization: benefits and pitfalls. Neurosurg Focus . 2008; 24( 2): E7. Google Scholar CrossRef Search ADS PubMed  27. Kaku Y, Funatsu N, Tsujimoto M, Yamashita K, Kokuzawa J. STA-MCA/STA-PCA bypass using short interposition vein graft. Acta Neurochir Suppl . 2014; 119: 79- 82. Google Scholar PubMed  28. Gabryś E, Rybaczuk M, Kędzia A. Blood flow simulation through fractal models of circulatory system. Chaos Solitons Fractals . 2006; 27( 1): 1- 7. Google Scholar CrossRef Search ADS   29. Wanebo JE, Zabramski JM, Spetzler RF. Superficial temporal artery-to-middle cerebral artery bypass grafting for cerebral revascularization. Neurosurgery . 2004; 55( 2): 395- 398; discussion 398-399. Google Scholar CrossRef Search ADS PubMed  30. Newell DW, Vilela MD. Superficial temporal artery to middle cerebral artery bypass. Neurosurgery . 2004; 54( 6): 1441-1448-1449. Google Scholar CrossRef Search ADS   31. Charbel FT, Meglio G, Amin-Hanjani S. Superficial temporal artery-to-middle cerebral artery bypass. Neurosurgery . 2005; 56( suppl 1): 186- 190; discussion 186-190. Google Scholar PubMed  32. Kadri PAS, Krisht AF, Gandhi GK. An anatomic mathematical measurement to find an adequate recipient M4 branch for superficial temporal artery to middle cerebral artery bypass surgery. Neurosurgery . 2007; 61( suppl 3): 74- 78; discussion 78. Google Scholar PubMed  COMMENTS Brain revascularization still represents a valuable option for flow augmentation in cases of Moyamoya disease and in selected cases of ICA occlusion with hemodynamic compromise, as well as for flow replacement. Traditionally, STA-MCA bypass has been considered a method to deliver only low flow in the brain territory, with a range of 15-70 cc/min, thus being a suitable option only for ischemic cases. However, nowadays there is the possibility to tailor the surgical revascularization options to both the brain demand and the real bypass flow capacity. This can be obtained by the use of new technologies like ICG video angiography with FLOW800 analysis and Transonic Probe measurements. In this way, the traditional equation ischemia=low flow bypass and replacement=high flow bypass should be modified and adapted to the real need of the brain and the actual flow possibilities of the bypass. The authors should be congratulated for their efforts in providing new insights into this matter. In particular, they showed in a large series of double-barrel STA-MCA bypass performed for ischemic cases (most of them being Moyamoya disease) that the flow possibilities are much higher than expected for a so-called “low-flow” bypass, with value as high as 120 cc/min and in the majority of cases above 65 cc/min. In some of their cases this was only a theoretical possibility as the flow measurements were performed only as “cut-flow”. However, this is a very important study because it confirms that the double-barrel technique in STA-MCA bypass can be used even with a high-flow demand. This maybe is not the case for all ischemic indication, like in Moyamoya disease (the use of ICG video angiography could be of great help to identify the patients in which multiple brain territories need to be revascularized and thus the double bypass could be of great help) but, more importantly, in cases of flow replacement, particularly for complex intracranial aneurysms. The use of a significantly simpler procedure, like the double-barrel STA-MCA bypass is compared to EC-IC bypasses with interposition grafts, should assure in selected cases a high rate of success with a significantly low percentage of complications. Francesco Acerbi Milan, Italy The authors demonstrate that double-barrel STA-MCA bypasses can achieve high flows. They report the results of intraoperative flow probe measurements in 21 cases, 17 of which were double-barrel bypasses and 4 of which were single-branch bypasses. Using a single branch, the average best observed flow (BOF) was 39 cc/min, and the maximum was 40 cc/min. By contrast, double-barrel bypasses resulted in an average BOF of 69 cc/min and a maximum of 120 cc/min. In the literature, radial artery interpositional grafts have been reported to have flow rates between 40 to 150 cc/min. Saphenous vein grafts are associated with the highest flow rates (70 to 250 cc/min). It is both interesting and surprising that the radial artery interpositional graft is not associated with flows dramatically higher than those of the STA double-barrel bypass. Certainly, the STA double barrel bypass is surgically easier than the radial artery interposition graft, which requires a cervical incision, tunneling of the artery, and an additional proximal anastomosis in the case of 2 distal MCA recipients vessels. This study is helpful in selecting a bypass donor compatible with the flow needs of individual patients. Rafael J. Tamargo Baltimore, Maryland Copyright © 2017 by the Congress of Neurological Surgeons

Journal

Operative NeurosurgeryOxford University Press

Published: Mar 1, 2018

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