- Email: [email protected]
Cerebral Revascularization: Which Patients Should Be Bypassed and Which Patients Should Be Passed by?
Accepted Manuscript Cerebral Revascularization: Which patients should be bypassed and which should be passed by? Brian M. Howard, MD, Daniel L. Barrow, MD PII:
S1878-8750(15)00004-2
DOI:
10.1016/j.wneu.2014.12.045
Reference:
WNEU 2654
To appear in:
World Neurosurgery
Received Date: 3 December 2014 Accepted Date: 20 December 2014
Please cite this article as: Howard BM, Barrow DL, Cerebral Revascularization: Which patients should be bypassed and which should be passed by?, World Neurosurgery (2015), doi: 10.1016/ j.wneu.2014.12.045. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
Cerebral Revascularization: Which patients should be bypassed and which should be passed by? Brian M. Howard, MD1 and Daniel L. Barrow, MD1 1
RI PT
Department of Neurological Surgery Emory University School of Medicine Atlanta, GA, USA
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Key Words Cerebral revascularization Bypass Stroke Intracranial Aneurysm Moyamoya Skull base tumor
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Daniel L. Barrow, MD MBNA-Bowman Professor and Chairman Department of Neurological Surgery Director, Emory MBNA Stroke Center Emory University School of Medicine 1365 Clifton Road, Ste. B6172 Atlanta, Georgia, USA 30322 Phone: 404.778.5374 Fax: 404.778.4472
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Corresponding Author
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Abbreviations CBF – Cerebral blood flow CVR – Cerebrovascular reactivity COSS - Carotid Occlusion Surgery Trial EC/IC - Extracranial/intracranial EDAS – encephaloduroarteriosynangiosis ICA – Internal carotid artery IC/IC – Intracranial/intracranial JET – Japanese EC/IC Bypass Trial MCA – Middle cerebral artery OEF – Oxygen extraction fraction PET – Positron emission tomography SPECT - Single-photon emission computed tomography STA – Superficial temporal artery
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On a warm and clear afternoon in late September 1934, at the opening ceremonies for McGill University’s newly formed Neurological Institute, Harvey Cushing said, “the technical details of intracranial procedures are so far from being fully perfected that scarcely a season goes by without some new and important element being introduced in the operative ritual which makes possible the exposure and treatment of lesions only yesterday thought to be forever out of reach”(4). In the following 80 years, advances in both surgical technique and technology in neurosurgery have been astounding. The advent of sub-specialization has accelerated the development and sophistication of individual fields. Within cerebrovascular disease specifically, the introduction of the operating microscope along with modern microsurgical technique, and the evolution of both endovascular procedures and stereotactic radiosurgery have not only expanded the vascular neurosurgeon’s armamentarium, but have transformed untreatable conditions into ailments for which various therapeutic options exist. The practice of neurosurgery will undoubtedly continue to evolve and improve. Unlike in eras past, when our forefathers would ask themselves, ‘can this patient be treated?’; today, we find ourselves asking, ‘by which modality may this patient be most safely and efficiently treated?’. In this volume of World Neurosurgery, Kalani and colleagues present their experience with cerebral revascularization to help define patients who remain appropriate candidates for surgical, intracranial bypass in the modern era. Yasargil (17) first described intracranial, arterial bypass over 40 years ago and indications for surgery quickly expanded to include treatment of complex aneurysms, moyamoya disease, extensive skull base neoplasms and occlusive vasculopathy. However, as Dr. Kalani points out, fewer bypasses are being completed now than in previous decades as innovations and increased experience in endovascular techniques have limited the number of complex aneurysms that require open surgical trapping and bypass. Similarly, a large proportion of skull base tumors, previously treated by resection and bypass, are often managed with less invasive surgery combined with newer, more effective chemotherapy and radiosurgery regimens. Microsurgical bypass, previously a mainstay in the treatment of symptomatic, cerebral ischemia related to carotid occlusive disease has been abandoned in most centers following publication of both the Extracranial/intracranial (EC/IC) bypass trial (1) in 1985 and the Carotid Occlusion Surgery Study (COSS - (13)) in 2011. While EC/IC bypass remains a viable treatment for moyamoya angiopathy, particularly in adults, patients are increasingly being treated with various, indirect revascularization procedures such as encephaloduroarteriosynangiosis (EDAS). Dr. Kalani and his co-authors report a retrospective series of 121 patients who underwent 131 direct cerebral bypass operations between 2006 and 2013 in one of the busiest cerebrovascular centers in North America. The majority of patients underwent direct bypass to treat moyamoya disease (36%) and complex aneurysms (43%); while 21% of the patients underwent revascularization for occlusive vascular disease. Patients who suffer from occlusive vascular disease represent perhaps the most interesting, if not most controversial, subset treated with bypass. The authors report on a relatively low number of patients (twenty-seven) who underwent bypass procedures for occlusive vascular disease. The majority (70%) of patients were treated for symptomatic internal carotid artery (ICA) or middle cerebral artery (MCA) occlusion, while the remaining patients suffered from various less common vasculitides. Fifty-six percent of
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patients benefitted from surgery with a low, overall, complication rate. While important, the external validity of these data is somewhat limited, as the inclusion criteria for patients who underwent bypass for cerebral ischemia in this cohort are not well elucidated. The first, published randomized control trial wherein patients who underwent EC/IC bypass via superficial temporal (STA) or occipital artery to MCA anastomosis failed to demonstrate reduction in mortality or stroke-related morbidity in the surgical arm over patients in the control (medical) arm (1). The study was highly criticized because the authors were unable to identify a subgroup of patients for whom EC/IC bypass may yield benefit (9, 13, 15). However, in light of the high bypass patency rate (96%), hope remained that if an appropriate cohort could be identified, patients with symptomatic, cerebral ischemia could still benefit from surgical revascularization. Subsequent trials of EC/IC bypass to prevent stroke from carotid occlusive disease were designed largely on the basis of the St. Louis Carotid Occlusion Study (5), which showed that patients with hemodynamic insufficiency demonstrated by increased oxygen extraction fraction (OEF) on PET were at the greatest risk of stroke following medical management for atherosclerotic carotid occlusion. Therefore, the major inclusion criteria for COSS was increased OEF on PET. However, STA-MCA bypass failed to afford those in the surgical arm any benefit over those in the medical group, primarily due to better than expected stroke reduction in the non-operative arm (6, 13). Conversely, the Japanese EC/IC Bypass Trial (JET) demonstrated 2-year stroke reduction benefit for patients who underwent STA-MCA bypass who demonstrated baseline hemodynamic insufficiency as defined by decreased cerebral blood flow (CBF) and cerebrovascular reactivity (CVR) on acetazolamide challenge as measured on SPECT. A recent study (9) may help to clarify these seemingly confounding results. Patients with known carotid occlusive disease were screened for hemodynamic insufficiency by measuring CBF and CVR on SPECT as well as OEF on PET. Forty-nine patients were prospectively enrolled and STA-MCA statistically reduced strokes as compared to medical therapy (0.7% vs 6.5%) for patients with reduced CBF and CVR and increased OEF. While many neurosurgeons have ceased to perform bypass procedures for occlusive disease because of the EC/IC bypass trial and COSS, the findings of JET and others raise the question of whether a large, multicenter prospective trial for highly selected patients with evidence of carotid occlusion and hemodynamic insufficiency as corroborated by multiple imaging modalities is warranted. Limitations to such a study are cost and the paucity of centers capable of performing such sophisticated imaging (15). The resurrection of a surgical, multicenter, randomized control trial for symptomatic carotid occlusion will likely be delayed until more readily available, cheaper imaging surrogates for the aforementioned studies can be validated. The number of cerebral revascularization procedures for giant, complex and thrombosed aneurysms has steadily dropped over the past decade as stent-coiling and flow diversion technology has increasingly improved (7, 8). However, certain aneurysms will continue to require bypass into the foreseeable future. Indeed, Dr. Kalani and coauthors report on 54 patients who underwent bypass for 55 aneurysms not amenable to clip reconstruction or endovascular management. While their results compare favorably with the established literature, seven (13%) patients died, all but one from post-operative stroke. These data serve to reinforce, that even in the most skilled and experienced hands,
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bypass for complex aneurysms is a technically challenging procedure, often fraught with risk. Dolichoectactic and thrombosed aneurysms constitute particularly difficult lesions to treat, both by endovascular means and traditional surgical clip ligation. Since the introduction of the EC/IC bypass, several IC/IC bypass methods, which represent an elegant solution to otherwise untreatable aneurysms, have been described (10, 14, 16). The in situ bypass requires two parallel arteries, such as the anterior cerebral, posterior cerebral and superior cerebellar, and the distal posterior inferior cerebellar arteries, or branches of the MCA, which are anastomosed side-to-side (14). Reanastomosis of the parent artery or branches thereof proximal and distal to the aneurysm following complete resection of the diseased portion of the vessel is an attractive technique in places where the parent artery has sufficient redundancy to allow for end to end reconstruction (16). Short segment IC/IC bypass with a radial artery interposition graft is often a good alternative to EC/IC bypass. The radial artery is of similar diameter to the proximal intracranial vasculature, which makes reanastomosis technically simpler, and, with shorter grafts, the risk thrombosis is decreased (16). Finally, reimplantation of an important arterial branch that originates from the aneurysm itself is an essential tool for the vascular neurosurgeon when endovascular therapy would risk occluding the perforating branch or clip reconstruction would risk incomplete neck occlusion and aneurysm recurrence (16). While endovascular techniques have limited the number of complex aneurysms that require open surgery, bypass for difficult-to-treat aneurysms will continue to be a required skill that neurosurgeons must hone. Moyamoya disease, an idiopathic, occlusive vasculopathy of intracranial ICA is the most common indication for bypass (direct and indirect). Direct EC/IC bypass has traditionally been the treatment of choice to revascularize the affected hemisphere in symptomatic patients with moyamoya disease (12). Direct EC/IC bypass results in immediate flow augmentation to the hypoperfused hemisphere (11, 12). Kalani and colleagues report on their series of patients who underwent bypass for moyamoya. The overwhelming majority of the 40 patients who underwent 47 procedures had single implantation STA-MCA bypass. Two patients underwent double-barrel STA-MCA bypass while another underwent high-flow ICA-MCA bypass using a radial artery interposition graft. As expected, the graft patency rate was high (97%) for those patients with follow-up angiography. Indirect bypass via EDAS, is more commonly completed in the pediatric moyamoya population than in adults (2, 12). While restitution of flow is delayed in EDAS, the advantage lies in the ability of the oxygen-starved hemisphere to make pial anastamoses with the graft over time. Although not utilized in the patients about whom Kalani and collaborators reported, a direct STA-MCA bypass combined with EDAS is being increasingly advocated to maximize reperfusion both immediately and over time (3, 11). One glaring advantage of this approach over direct bypass alone is in cases of donor artery occlusion, wherein, the EDAS may still revascularize the underperfused territory. Overall, bypass techniques, whether direct EC or IC/IC bypass or indirect via EDAS, will clearly continue to have an important place in neurosurgery. While the field of neurosurgery has rapidly evolved, perhaps faster and farther than even Dr. Cushing had so insightfully predicted nearly a century ago, we continue to innovate and refine our techniques. Although advances in endovascular, medical and radiation therapies have
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limited the number of patients with complex aneurysms, ICA atherosclerotic occlusive disease and skull base tumors who undergo bypass procures, respectively, many such patients will require operative, intracranial revascularization in some form. Therefore, the onus remains, particularly on young neurosurgeons, to continue to sharpen microsurgical skills, such that when needed, we may continue to achieve the best possible results. Dr. Kalani and his colleagues should be commended for sharing their vast experience with bypass in the series published in this issue of World Neurosurgery; at minimum, this report is a yardstick for that which we can do, and we should strive to continue to achieve to improve outcomes for our patients with even the most difficult diseases to treat.
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1. Failure of extracranial-intracranial arterial bypass to reduce the risk of ischemic stroke. Results of an international randomized trial. The EC/IC Bypass Study Group. The New England journal of medicine 313:1191-1200, 1985 2. Agarwalla PK, Stapleton CJ, Phillips MT, Walcott BP, Venteicher AS, Ogilvy CS: Surgical outcomes following encephaloduroarteriosynangiosis in North American adults with moyamoya. Journal of neurosurgery:1-7, 2014 3. Amin-Hanjani S, Singh A, Rifai H, Thulborn KR, Alaraj A, Aletich V, Charbel FT: Combined direct and indirect bypass for moyamoya: quantitative assessment of direct bypass flow over time. Neurosurgery 73:962-967; discussion 967-968, 2013 4. Cushing H: Psychiatrists, Neurologists and the Neurosurgeon. The Yale journal of biology and medicine 7:191-207, 1935 5. Grubb RL, Jr., Derdeyn CP, Fritsch SM, Carpenter DA, Yundt KD, Videen TO, Spitznagel EL, Powers WJ: Importance of hemodynamic factors in the prognosis of symptomatic carotid occlusion. Jama 280:1055-1060, 1998 6. Grubb RL, Jr., Powers WJ, Clarke WR, Videen TO, Adams HP, Jr., Derdeyn CP, Carotid Occlusion Surgery Study I: Surgical results of the Carotid Occlusion Surgery Study. Journal of neurosurgery 118:25-33, 2013 7. Kan P, Siddiqui AH, Veznedaroglu E, Liebman KM, Binning MJ, Dumont TM, Ogilvy CS, Gaughen JR, Jr., Mocco J, Velat GJ, Ringer AJ, Welch BG, Horowitz MB, Snyder KV, Hopkins LN, Levy EI: Early postmarket results after treatment of intracranial aneurysms with the pipeline embolization device: a U.S. multicenter experience. Neurosurgery 71:1080-1087; discussion 1087-1088, 2012 8. King B, Vaziri S, Singla A, Fargen KM, Mocco J: Clinical and angiographic outcomes after stent-assisted coiling of cerebral aneurysms with Enterprise and Neuroform stents: a comparative analysis of the literature. Journal of neurointerventional surgery2014 9. Kuroda S, Kawabori M, Hirata K, Shiga T, Kashiwazaki D, Houkin K, Tamaki N: Clinical significance of STA-MCA double anastomosis for hemodynamic compromise in post-JET/COSS era. Acta neurochirurgica 156:77-83, 2014 10. Lawton MT, Quinones-Hinojosa A, Chang EF, Yu T: Thrombotic intracranial aneurysms: classification scheme and management strategies in 68 patients. Neurosurgery 56:441-454; discussion 441-454, 2005 11. Nossek E, Langer DJ: How I do it: combined direct (STA-MCA) and indirect (EDAS) EC-IC bypass. Acta neurochirurgica 156:2079-2084, 2014 12. Pandey P, Steinberg GK: Neurosurgical advances in the treatment of moyamoya disease. Stroke; a journal of cerebral circulation 42:3304-3310, 2011 13. Powers WJ, Clarke WR, Grubb RL, Jr., Videen TO, Adams HP, Jr., Derdeyn CP, Investigators C: Extracranial-intracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: the Carotid Occlusion Surgery Study randomized trial. Jama 306:1983-1992, 2011 14. Quinones-Hinojosa A, Lawton MT: In situ bypass in the management of complex intracranial aneurysms: technique application in 13 patients. Neurosurgery 57:140-145; discussion 140-145, 2005 15. Rodriguez-Hernandez A, Josephson SA, Langer D, Lawton MT: Bypass for the prevention of ischemic stroke. World neurosurgery 76:S72-79, 2011
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16. Sanai N, Zador Z, Lawton MT: Bypass surgery for complex brain aneurysms: an assessment of intracranial-intracranial bypass. Neurosurgery 65:670-683; discussion 683, 2009 17. Yasargil MG, Krayenbuhl HA, Jacobson JH, 2nd: Microneurosurgical arterial reconstruction. Surgery 67:221-233, 1970
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The number of intracranial bypass procedures has been limited by the advent of endovascular therapy and less invasive skull base approaches. Intracranial bypass remains an important tool to treat complex aneurysms not amenable to endovascular therapy or traditional surgical clip ligation.
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Young neurosurgeons in particular must seek opportunities to develop bypass skills.
S1878-8750(15)00004-2
DOI:
10.1016/j.wneu.2014.12.045
Reference:
WNEU 2654
To appear in:
World Neurosurgery
Received Date: 3 December 2014 Accepted Date: 20 December 2014
Please cite this article as: Howard BM, Barrow DL, Cerebral Revascularization: Which patients should be bypassed and which should be passed by?, World Neurosurgery (2015), doi: 10.1016/ j.wneu.2014.12.045. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
Cerebral Revascularization: Which patients should be bypassed and which should be passed by? Brian M. Howard, MD1 and Daniel L. Barrow, MD1 1
RI PT
Department of Neurological Surgery Emory University School of Medicine Atlanta, GA, USA
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Key Words Cerebral revascularization Bypass Stroke Intracranial Aneurysm Moyamoya Skull base tumor
M AN U
Daniel L. Barrow, MD MBNA-Bowman Professor and Chairman Department of Neurological Surgery Director, Emory MBNA Stroke Center Emory University School of Medicine 1365 Clifton Road, Ste. B6172 Atlanta, Georgia, USA 30322 Phone: 404.778.5374 Fax: 404.778.4472
SC
Corresponding Author
AC C
Abbreviations CBF – Cerebral blood flow CVR – Cerebrovascular reactivity COSS - Carotid Occlusion Surgery Trial EC/IC - Extracranial/intracranial EDAS – encephaloduroarteriosynangiosis ICA – Internal carotid artery IC/IC – Intracranial/intracranial JET – Japanese EC/IC Bypass Trial MCA – Middle cerebral artery OEF – Oxygen extraction fraction PET – Positron emission tomography SPECT - Single-photon emission computed tomography STA – Superficial temporal artery
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On a warm and clear afternoon in late September 1934, at the opening ceremonies for McGill University’s newly formed Neurological Institute, Harvey Cushing said, “the technical details of intracranial procedures are so far from being fully perfected that scarcely a season goes by without some new and important element being introduced in the operative ritual which makes possible the exposure and treatment of lesions only yesterday thought to be forever out of reach”(4). In the following 80 years, advances in both surgical technique and technology in neurosurgery have been astounding. The advent of sub-specialization has accelerated the development and sophistication of individual fields. Within cerebrovascular disease specifically, the introduction of the operating microscope along with modern microsurgical technique, and the evolution of both endovascular procedures and stereotactic radiosurgery have not only expanded the vascular neurosurgeon’s armamentarium, but have transformed untreatable conditions into ailments for which various therapeutic options exist. The practice of neurosurgery will undoubtedly continue to evolve and improve. Unlike in eras past, when our forefathers would ask themselves, ‘can this patient be treated?’; today, we find ourselves asking, ‘by which modality may this patient be most safely and efficiently treated?’. In this volume of World Neurosurgery, Kalani and colleagues present their experience with cerebral revascularization to help define patients who remain appropriate candidates for surgical, intracranial bypass in the modern era. Yasargil (17) first described intracranial, arterial bypass over 40 years ago and indications for surgery quickly expanded to include treatment of complex aneurysms, moyamoya disease, extensive skull base neoplasms and occlusive vasculopathy. However, as Dr. Kalani points out, fewer bypasses are being completed now than in previous decades as innovations and increased experience in endovascular techniques have limited the number of complex aneurysms that require open surgical trapping and bypass. Similarly, a large proportion of skull base tumors, previously treated by resection and bypass, are often managed with less invasive surgery combined with newer, more effective chemotherapy and radiosurgery regimens. Microsurgical bypass, previously a mainstay in the treatment of symptomatic, cerebral ischemia related to carotid occlusive disease has been abandoned in most centers following publication of both the Extracranial/intracranial (EC/IC) bypass trial (1) in 1985 and the Carotid Occlusion Surgery Study (COSS - (13)) in 2011. While EC/IC bypass remains a viable treatment for moyamoya angiopathy, particularly in adults, patients are increasingly being treated with various, indirect revascularization procedures such as encephaloduroarteriosynangiosis (EDAS). Dr. Kalani and his co-authors report a retrospective series of 121 patients who underwent 131 direct cerebral bypass operations between 2006 and 2013 in one of the busiest cerebrovascular centers in North America. The majority of patients underwent direct bypass to treat moyamoya disease (36%) and complex aneurysms (43%); while 21% of the patients underwent revascularization for occlusive vascular disease. Patients who suffer from occlusive vascular disease represent perhaps the most interesting, if not most controversial, subset treated with bypass. The authors report on a relatively low number of patients (twenty-seven) who underwent bypass procedures for occlusive vascular disease. The majority (70%) of patients were treated for symptomatic internal carotid artery (ICA) or middle cerebral artery (MCA) occlusion, while the remaining patients suffered from various less common vasculitides. Fifty-six percent of
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patients benefitted from surgery with a low, overall, complication rate. While important, the external validity of these data is somewhat limited, as the inclusion criteria for patients who underwent bypass for cerebral ischemia in this cohort are not well elucidated. The first, published randomized control trial wherein patients who underwent EC/IC bypass via superficial temporal (STA) or occipital artery to MCA anastomosis failed to demonstrate reduction in mortality or stroke-related morbidity in the surgical arm over patients in the control (medical) arm (1). The study was highly criticized because the authors were unable to identify a subgroup of patients for whom EC/IC bypass may yield benefit (9, 13, 15). However, in light of the high bypass patency rate (96%), hope remained that if an appropriate cohort could be identified, patients with symptomatic, cerebral ischemia could still benefit from surgical revascularization. Subsequent trials of EC/IC bypass to prevent stroke from carotid occlusive disease were designed largely on the basis of the St. Louis Carotid Occlusion Study (5), which showed that patients with hemodynamic insufficiency demonstrated by increased oxygen extraction fraction (OEF) on PET were at the greatest risk of stroke following medical management for atherosclerotic carotid occlusion. Therefore, the major inclusion criteria for COSS was increased OEF on PET. However, STA-MCA bypass failed to afford those in the surgical arm any benefit over those in the medical group, primarily due to better than expected stroke reduction in the non-operative arm (6, 13). Conversely, the Japanese EC/IC Bypass Trial (JET) demonstrated 2-year stroke reduction benefit for patients who underwent STA-MCA bypass who demonstrated baseline hemodynamic insufficiency as defined by decreased cerebral blood flow (CBF) and cerebrovascular reactivity (CVR) on acetazolamide challenge as measured on SPECT. A recent study (9) may help to clarify these seemingly confounding results. Patients with known carotid occlusive disease were screened for hemodynamic insufficiency by measuring CBF and CVR on SPECT as well as OEF on PET. Forty-nine patients were prospectively enrolled and STA-MCA statistically reduced strokes as compared to medical therapy (0.7% vs 6.5%) for patients with reduced CBF and CVR and increased OEF. While many neurosurgeons have ceased to perform bypass procedures for occlusive disease because of the EC/IC bypass trial and COSS, the findings of JET and others raise the question of whether a large, multicenter prospective trial for highly selected patients with evidence of carotid occlusion and hemodynamic insufficiency as corroborated by multiple imaging modalities is warranted. Limitations to such a study are cost and the paucity of centers capable of performing such sophisticated imaging (15). The resurrection of a surgical, multicenter, randomized control trial for symptomatic carotid occlusion will likely be delayed until more readily available, cheaper imaging surrogates for the aforementioned studies can be validated. The number of cerebral revascularization procedures for giant, complex and thrombosed aneurysms has steadily dropped over the past decade as stent-coiling and flow diversion technology has increasingly improved (7, 8). However, certain aneurysms will continue to require bypass into the foreseeable future. Indeed, Dr. Kalani and coauthors report on 54 patients who underwent bypass for 55 aneurysms not amenable to clip reconstruction or endovascular management. While their results compare favorably with the established literature, seven (13%) patients died, all but one from post-operative stroke. These data serve to reinforce, that even in the most skilled and experienced hands,
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bypass for complex aneurysms is a technically challenging procedure, often fraught with risk. Dolichoectactic and thrombosed aneurysms constitute particularly difficult lesions to treat, both by endovascular means and traditional surgical clip ligation. Since the introduction of the EC/IC bypass, several IC/IC bypass methods, which represent an elegant solution to otherwise untreatable aneurysms, have been described (10, 14, 16). The in situ bypass requires two parallel arteries, such as the anterior cerebral, posterior cerebral and superior cerebellar, and the distal posterior inferior cerebellar arteries, or branches of the MCA, which are anastomosed side-to-side (14). Reanastomosis of the parent artery or branches thereof proximal and distal to the aneurysm following complete resection of the diseased portion of the vessel is an attractive technique in places where the parent artery has sufficient redundancy to allow for end to end reconstruction (16). Short segment IC/IC bypass with a radial artery interposition graft is often a good alternative to EC/IC bypass. The radial artery is of similar diameter to the proximal intracranial vasculature, which makes reanastomosis technically simpler, and, with shorter grafts, the risk thrombosis is decreased (16). Finally, reimplantation of an important arterial branch that originates from the aneurysm itself is an essential tool for the vascular neurosurgeon when endovascular therapy would risk occluding the perforating branch or clip reconstruction would risk incomplete neck occlusion and aneurysm recurrence (16). While endovascular techniques have limited the number of complex aneurysms that require open surgery, bypass for difficult-to-treat aneurysms will continue to be a required skill that neurosurgeons must hone. Moyamoya disease, an idiopathic, occlusive vasculopathy of intracranial ICA is the most common indication for bypass (direct and indirect). Direct EC/IC bypass has traditionally been the treatment of choice to revascularize the affected hemisphere in symptomatic patients with moyamoya disease (12). Direct EC/IC bypass results in immediate flow augmentation to the hypoperfused hemisphere (11, 12). Kalani and colleagues report on their series of patients who underwent bypass for moyamoya. The overwhelming majority of the 40 patients who underwent 47 procedures had single implantation STA-MCA bypass. Two patients underwent double-barrel STA-MCA bypass while another underwent high-flow ICA-MCA bypass using a radial artery interposition graft. As expected, the graft patency rate was high (97%) for those patients with follow-up angiography. Indirect bypass via EDAS, is more commonly completed in the pediatric moyamoya population than in adults (2, 12). While restitution of flow is delayed in EDAS, the advantage lies in the ability of the oxygen-starved hemisphere to make pial anastamoses with the graft over time. Although not utilized in the patients about whom Kalani and collaborators reported, a direct STA-MCA bypass combined with EDAS is being increasingly advocated to maximize reperfusion both immediately and over time (3, 11). One glaring advantage of this approach over direct bypass alone is in cases of donor artery occlusion, wherein, the EDAS may still revascularize the underperfused territory. Overall, bypass techniques, whether direct EC or IC/IC bypass or indirect via EDAS, will clearly continue to have an important place in neurosurgery. While the field of neurosurgery has rapidly evolved, perhaps faster and farther than even Dr. Cushing had so insightfully predicted nearly a century ago, we continue to innovate and refine our techniques. Although advances in endovascular, medical and radiation therapies have
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limited the number of patients with complex aneurysms, ICA atherosclerotic occlusive disease and skull base tumors who undergo bypass procures, respectively, many such patients will require operative, intracranial revascularization in some form. Therefore, the onus remains, particularly on young neurosurgeons, to continue to sharpen microsurgical skills, such that when needed, we may continue to achieve the best possible results. Dr. Kalani and his colleagues should be commended for sharing their vast experience with bypass in the series published in this issue of World Neurosurgery; at minimum, this report is a yardstick for that which we can do, and we should strive to continue to achieve to improve outcomes for our patients with even the most difficult diseases to treat.
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1. Failure of extracranial-intracranial arterial bypass to reduce the risk of ischemic stroke. Results of an international randomized trial. The EC/IC Bypass Study Group. The New England journal of medicine 313:1191-1200, 1985 2. Agarwalla PK, Stapleton CJ, Phillips MT, Walcott BP, Venteicher AS, Ogilvy CS: Surgical outcomes following encephaloduroarteriosynangiosis in North American adults with moyamoya. Journal of neurosurgery:1-7, 2014 3. Amin-Hanjani S, Singh A, Rifai H, Thulborn KR, Alaraj A, Aletich V, Charbel FT: Combined direct and indirect bypass for moyamoya: quantitative assessment of direct bypass flow over time. Neurosurgery 73:962-967; discussion 967-968, 2013 4. Cushing H: Psychiatrists, Neurologists and the Neurosurgeon. The Yale journal of biology and medicine 7:191-207, 1935 5. Grubb RL, Jr., Derdeyn CP, Fritsch SM, Carpenter DA, Yundt KD, Videen TO, Spitznagel EL, Powers WJ: Importance of hemodynamic factors in the prognosis of symptomatic carotid occlusion. Jama 280:1055-1060, 1998 6. Grubb RL, Jr., Powers WJ, Clarke WR, Videen TO, Adams HP, Jr., Derdeyn CP, Carotid Occlusion Surgery Study I: Surgical results of the Carotid Occlusion Surgery Study. Journal of neurosurgery 118:25-33, 2013 7. Kan P, Siddiqui AH, Veznedaroglu E, Liebman KM, Binning MJ, Dumont TM, Ogilvy CS, Gaughen JR, Jr., Mocco J, Velat GJ, Ringer AJ, Welch BG, Horowitz MB, Snyder KV, Hopkins LN, Levy EI: Early postmarket results after treatment of intracranial aneurysms with the pipeline embolization device: a U.S. multicenter experience. Neurosurgery 71:1080-1087; discussion 1087-1088, 2012 8. King B, Vaziri S, Singla A, Fargen KM, Mocco J: Clinical and angiographic outcomes after stent-assisted coiling of cerebral aneurysms with Enterprise and Neuroform stents: a comparative analysis of the literature. Journal of neurointerventional surgery2014 9. Kuroda S, Kawabori M, Hirata K, Shiga T, Kashiwazaki D, Houkin K, Tamaki N: Clinical significance of STA-MCA double anastomosis for hemodynamic compromise in post-JET/COSS era. Acta neurochirurgica 156:77-83, 2014 10. Lawton MT, Quinones-Hinojosa A, Chang EF, Yu T: Thrombotic intracranial aneurysms: classification scheme and management strategies in 68 patients. Neurosurgery 56:441-454; discussion 441-454, 2005 11. Nossek E, Langer DJ: How I do it: combined direct (STA-MCA) and indirect (EDAS) EC-IC bypass. Acta neurochirurgica 156:2079-2084, 2014 12. Pandey P, Steinberg GK: Neurosurgical advances in the treatment of moyamoya disease. Stroke; a journal of cerebral circulation 42:3304-3310, 2011 13. Powers WJ, Clarke WR, Grubb RL, Jr., Videen TO, Adams HP, Jr., Derdeyn CP, Investigators C: Extracranial-intracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: the Carotid Occlusion Surgery Study randomized trial. Jama 306:1983-1992, 2011 14. Quinones-Hinojosa A, Lawton MT: In situ bypass in the management of complex intracranial aneurysms: technique application in 13 patients. Neurosurgery 57:140-145; discussion 140-145, 2005 15. Rodriguez-Hernandez A, Josephson SA, Langer D, Lawton MT: Bypass for the prevention of ischemic stroke. World neurosurgery 76:S72-79, 2011
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16. Sanai N, Zador Z, Lawton MT: Bypass surgery for complex brain aneurysms: an assessment of intracranial-intracranial bypass. Neurosurgery 65:670-683; discussion 683, 2009 17. Yasargil MG, Krayenbuhl HA, Jacobson JH, 2nd: Microneurosurgical arterial reconstruction. Surgery 67:221-233, 1970
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The number of intracranial bypass procedures has been limited by the advent of endovascular therapy and less invasive skull base approaches. Intracranial bypass remains an important tool to treat complex aneurysms not amenable to endovascular therapy or traditional surgical clip ligation.
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Young neurosurgeons in particular must seek opportunities to develop bypass skills.