- Email: [email protected]
Temporary Clipping for Unruptured Aneurysms
Perspectives Commentary on: The Impact of Temporary Artery Occlusion During Intracranial Aneurysm Surgery on Long-Term Clinical Outcome: Part II. The Patient Who Undergoes Elective Clipping by Griessenauer et al. World Neurosurg 2014 http://dx.doi.org/10.1016/j.wneu.2013.02.067
Gary K. Steinberg, M.D., Ph.D. Bernard and Ronni Lacroute-William Randolph Hearst Professor of Neurosurgery and the Neurosciences Chairman, Department of Neurosurgery Stanford University School of Medicine
Temporary Clipping for Unruptured Aneurysms Nitin Mukerji, Douglas J. Cook, Gary K. Steinberg
T
he stakes are often higher when operating on unruptured aneurysms compared with ruptured aneurysms because the patients are usually neurologically normal or minimally symptomatic. These are either incidental aneurysms discovered during screening for other symptoms or additional aneurysms in patients with subarachnoid hemorrhage. Unruptured aneurysms are being discovered and treated at an increasing rate, primarily as a result of the availability and improved quality of diagnostic imaging as well as a better understanding of the natural history. When operating on these aneurysms, the neurosurgeon generally has had adequate time to consider every possible scenario and plan ahead with the anesthesia team. Depending on the size, location, and morphology of the aneurysm and the surrounding vasculature, the neurosurgeon has the option of using temporary artery occlusion (TAO) or one of the cardiac standstill methods to facilitate dissection. The fundamental question to answer before discussing temporary clipping is whether an unruptured aneurysm requires any treatment. With agreement to proceed to treatment, the next question is whether treatment should be endovascular or surgical (13, 16, 18, 27, 29-31). Available natural history data do not allow us to answer these questions with absolute accuracy (19, 30). Although endovascular treatment is considered superior for certain types of ruptured aneurysms, no randomized evidence exists for unruptured aneurysms (13, 16, 17). The interpretation of current literature varies by center, country, and skill of the treating surgeon. Perhaps the only points on which most neurosurgeons agree are that aneurysms in patients with other prior ruptured aneurysms, giant aneurysms, and aneurysms in relation to the communicating arteries and posterior circulation are more likely to bleed and require treatment. Microsurgical
Key words Elective aneurysm clipping - Temporary artery occlusion -
Abbreviations and Acronyms TAO: Temporary artery occlusion
clipping is generally the best available option for middle cerebral artery aneurysms (9, 10, 17, 18, 22, 30). The patient’s age, comorbidities, and surgical risks also must be considered, balancing them against any modality of treatment. Epidemiologic evidence from multiple sources suggests that most incidentally discovered unruptured intracranial aneurysms do not rupture (9, 10, 17, 18, 22, 30-32). Identifying which unruptured intracranial aneurysms are at greatest risk of rupture is important when considering which ones to repair. It is also important to compare size, site, and group-specific natural history rates with size, site, and age-specific morbidity and mortality associated with repair of unruptured intracranial aneurysms because worse natural history risk is often associated with increased risk of aneurysm repair (9, 10, 17, 18, 22, 30-32). Patient age is crucial to decision making because of its major effect on operative morbidity and mortality; however, it does not substantially affect natural history. The effect of age is most notable in patients approximately 50 years old for open surgery and approximately 70 years old for endovascular procedures (14, 15). The authors in the current study found that aneurysm location (posterior vs. anterior circulation) was the most important prognostic predictor of poor outcome. Intraoperative rupture is less common in elective aneurysm clipping, and we employ Tao in selective cases at Stanford. The main use of temporary clips should be to facilitate aneurysm dissection and visualization (5), especially for larger aneurysms or aneurysms with major branches or perforators incorporated into the aneurysm base. Complete circumferential exposure of the aneurysm, branches, and perforators is required for safe and effective clipping of cerebral aneurysms. Better exposure and visualization prevent residual aneurysm necks or parent vessel or
Department of Neurosurgery, Stanford University School of Medicine, Stanford, California, USA To whom correspondence should be addressed: Gary K. Steinberg, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2013.07.094
WORLD NEUROSURGERY - (-): ---, MONTH 2014
www.WORLDNEUROSURGERY.org
1
PERSPECTIVES
perforator occlusion. Visualization is particularly important in areas deep and adjacent to the skull base, such as in the treatment of paraclinoid, basilar apex, and certain anterior communicating and posterior communicating artery aneurysms. Using temporary clips electively to facilitate dissection can help prevent an intraoperative rupture in most cases (4-6, 11, 20, 23). Elective TAO may be very helpful for aneurysms of the posterior circulation, including basilar aneurysms (5, 6, 11, 20, 23). In the event of an unforeseen intraoperative rupture, a TAO proceeding to permanent clipping is often necessary. The limitations of TAO and the alternatives require mention. A shortcoming of TAO is that it limits visibility and room for manipulation when operating in narrow surgical corridors close to the skull base, especially when operating on giant aneurysms (1, 8). TAO is also known to be associated with postoperative ischemic deficits, especially when the procedure is prolonged (6, 20). In such situations, it is reasonable to consider cardiac standstill techniques. When appropriately anticipated and planned, these techniques can be safely used. Drake et al. first reported the use of deep hypothermic circulatory arrest for the clipping of giant aneurysms approximately 40 years ago (2, 21), and the technique has been revived in recent years (3). Circulatory arrest decreases the inflow and pressure of the aneurysmal mass, and this allows the aneurysm to be collapsed, facilitating circumferential exposure. Deep hypothermic circulatory arrest also has the advantage of providing a bloodless surgical field; with adjuvant deep hypothermia, this is highly neuroprotective (21). However, circulatory arrest is cumbersome because a cardiopulmonary bypass is required, and the deep hypothermia required can be associated with development of coagulopathy and electrolyte abnormalities. Heparin is also required and increases the risk of intracranial bleeding (2). Groff et al. (7) first described transient adenosine-induced asystole during the open treatment of cerebral aneurysms in 1999 in posterior circulation aneurysms. The use of adenosine for cardiac standstill is now common, and its safety profile has been well reported (1, 8). It is important to be aware of this technique and to use it judiciously when required. Adenosine is an endogenous purine nucleoside whose mechanism of action involves reducing accumulation of intracellular cyclic adenosine monophosphate in cells. Adenosine inhibits adenylate cyclase and reduces intracellular calcium current in the myocardium. Adenosine affects both the sinoatrial and the atrioventricular nodes, making it the drug of choice for the treatment of paroxysmal supraventricular tachycardia. Other surgical uses for transient adenosine-induced asystole include endovascular aortic aneurysm repair and treatment of endovascular arteriovenous malformation (1, 8, 21).
REFERENCES 1. Bendok BR, Gupta DK, Rahme RJ, Eddleman CS, Adel JG, Sherma AK, Surdell DL, Bebawy JF, Koht A, Batjer HH: Adenosine for temporary flow arrest during intracranial aneurysm surgery: a single-center retrospective review. Neurosurgery 69:815-820, 2011 [discussion 820-821]. 2. Connolly ES Jr, Solomon RA: Hypothermic cardiac standstill for cerebral aneurysm surgery. Neurosurg Clin N Am 9:681-695, 1998.
2
www.SCIENCEDIRECT.com
The use of adenosine in aneurysm surgery is attractive for several reasons. Its action is characterized by rapid onset and rapid spontaneous reversal. This reversal is due to fast receptormediated uptake into erythrocytes and endothelial cells where the adenosine is inactivated. It can be administered repeatedly with predictable effects (1, 8, 21). There is no evidence of hematologic or biochemical toxicities associated with adenosine, and it has a favorable side-effect profile. Reported side effects include flushing, chest pain, and shortness of breath. Reported cardiac events in high-risk patients are infrequent and mild when they occur. A reduction in brain volume also occurs, giving the surgeon extra space and room for manipulation; this compares favorably with techniques such as TAO, which may reduce the window of access (1, 8, 21). The use of temporary clips remains the “gold standard.” Adenosine should be regarded as an additional and potentially synergistic tool with temporary clips, not a replacement for them. It is important to be reassured of the safety profile of this time-tested technique, and Griessenauer et al. should be commended for the meticulous presentation of their results. Many surgeons tend to use adjuncts such as neuromonitoring, mild hypothermia, neuroprotective drugs, and induced hypertension to decrease the risk of causing infarcts during TAO (12, 24-26, 28, 33, 34). TAO data may be of even greater relevance to unruptured aneurysms compared with ruptured aneurysms because these are increasingly the aneurysms that neurosurgeons clip in the wake of advancements in endovascular techniques and as more data on the long-term effectiveness of endovascular therapy emerge. Although the study by Griessenauer et al. was planned as a prospective study, it has a few limitations, and the authors have done a nice job of acknowledging and discussing these. The fact that total occlusion time was not significant in the binary logistic regression is most likely due to the authors’ policy of unoccluding and reperfusing each time the occlusion time was thought to be >15e20 minutes. This is a well-accepted technique, although criticisms exist. For a prospective study on TAO in unruptured aneurysms, the use of Glasgow Outcome Scale scores as an outcome measure instead of neuropsychologic testing and the lack of radiologic follow-up to detect new infarcts are potential weaknesses. The lack of controls also makes it difficult to draw conclusions regarding the benefit of temporary occlusion for unruptured aneurysms. In conclusion, despite the limitations, the authors should be congratulated on presenting the largest series available for TAO in patients with unruptured aneurysms. It is hoped that future studies in this field will extend this work.
3. Darsaut TE, Darsaut NM, Chang SD, Silverberg GD, Shuer LM, Tian L, Dodd RL, Do HM, Marks MP, Steinberg GK: Predictors of clinical and angiographic outcome after surgical or endovascular therapy of very large and giant intracranial aneurysms. Neurosurgery 68:903-915, 2011 [discussion 915]. 4. Dhandapani S, Pal SS, Gupta SK, Mohindra S, Chhabra R, Malhotra SK: Does the impact of elective temporary clipping on intraoperative rupture really influence neurological outcome after surgery for ruptured anterior circulation
aneurysms? A prospective multivariate study. Acta Neurochir 155:237-246, 2013. 5. Eftekhar B, Morgan MK: Indications for the use of temporary arterial occlusion during aneurysm repair: an institutional experience. J Clin Neurosci 18:905-909, 2011. 6. Giannotta SL, Oppenheimer JH, Levy ML, Zelman V: Management of intraoperative rupture of aneurysm without hypotension. Neurosurgery 28:531-535, 1991 [discussion 535-536].
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2013.07.094
PERSPECTIVES
7. Groff MW, Adams DC, Kahn RA, Kumbar UM, Yang BY, Bederson JB: Adenosine-induced transient asystole for management of a basilar artery aneurysm. Case report. J Neurosurg 91:687-690, 1999.
Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomized trial. J Stroke Cerebrovasc Dis 11:304-314, 2002.
8. Guinn NR, McDonagh DL, Borel CO, Wright DR, Zomorodi AR, Powers CJ, Warner DS, Lam AM, Britz GW: Adenosine-induced transient asystole for intracranial aneurysm surgery: a retrospective review. J Neurosurg Anesthesiol 23:35-40, 2011.
18. Molyneux AJ, Kerr RS, Yu LM, Clarke M, Sneade M, Yarnold JA, Sandercock P: International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet 366: 809-817, 2005.
9. Hernesniemi J, Dashti R, Lehecka M, Niemelä M, Rinne J, Lehto H, Ronkainen A, Koivisto T, Jääskeläinen JE: Microneurosurgical management of anterior communicating artery aneurysms. Surg Neurol 70:8-28, 2008 [discussion 29]. 10. Lawton MT: Editorial: middle cerebral artery aneurysms. J Neurosurg 118:947-948, 2013 [discussion 948-949]. 11. Lawton MT, Quinones-Hinojosa A, Chang EF, Yu T: Thrombotic intracranial aneurysms: classification scheme and management strategies in 68 patients. Neurosurgery 56:441-454, 2005 [discussion 441-454]. 12. McDermott MW, Durity FA, Borozny M, Mountain MA: Temporary vessel occlusion and barbiturate protection in cerebral aneurysm surgery. Neurosurgery 25:54-61, 1989 [discussion 61-52]. 13. McDougall CG, Spetzler RF, Zabramski JM, Partovi S, Hills NK, Nakaji P, Albuquerque FC: The Barrow Ruptured Aneurysm Trial. J Neurosurg 116:135-144, 2012. 14. Mitchell P, Jakubowski J: Estimate of the maximum time interval between formation of cerebral aneurysm and rupture. J Neurol Neurosurg Psychiatry 69:760-767, 2000. 15. Mitchell P, Kerr R, Mendelow AD, Molyneux A: Could late rebleeding overturn the superiority of cranial aneurysm coil embolization over clip ligation seen in the International Subarachnoid Aneurysm Trial? J Neurosurg 108:437-442, 2008. 16. Molyneux A, Kerr R, Stratton I, Sandercock P, Clarke M, Shrimpton J, Holman R: International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet 360:1267-1274, 2002. 17. Molyneux A, Kerr R, Stratton I, Sandercock P, Clarke M, Shrimpton J, Holman R: International
19. Morita A, Kirino T, Hashi K, Aoki N, Fukuhara S, Hashimoto N, Nakayama T, Sakai M, Teramoto A, Tominari S, Yoshimoto T: The natural course of unruptured cerebral aneurysms in a Japanese cohort. N Engl J Med 366:2474-2482, 2012. 20. Ogilvy CS, Carter BS, Kaplan S, Rich C, Crowell RM: Temporary vessel occlusion for aneurysm surgery: risk factors for stroke in patients protected by induced hypothermia and hypertension and intravenous mannitol administration. J Neurosurg 84:785-791, 1996. 21. Powers CJ, Wright DR, McDonagh DL, Borel CO, Zomorodi AR, Britz GW: Transient adenosineinduced asystole during the surgical treatment of anterior circulation cerebral aneurysms: technical note. Neurosurgery 67:461-470, 2010. 22. Rodriguez-Hernandez A, Sughrue ME, Akhavan S, Habdank-Kolaczkowski J, Lawton MT: Current management of middle cerebral artery aneurysms: surgical results with a “clip first” policy. Neurosurgery 72:415-427, 2013. 23. Schramm J, Cedzich C: Outcome and management of intraoperative aneurysm rupture. Surg Neurol 40:26-30, 1993.
27. Thines L, Bourgeois P, Lejeune J-P: Surgery for unruptured intracranial aneurysms in the ISAT and ISUIA era. Can J Neurol Sci 39:174-179, 2012. 28. Wicks RT, Pradilla G, Raza SM, Hadelsberg U, Coon AL, Huang J, Tamargo RJ: Impact of changes in intraoperative somatosensory evoked potentials on stroke rates after clipping of intracranial aneurysms. Neurosurgery 70:1114-1124, 2012 [discussion 1124]. 29. Wiebers DO: Neuroepidemiology of unruptured intracranial aneurysms: implications for decision making regarding patient management. Neurosurg Clin N Am 16:309-312, 2005: ix. 30. Wiebers DO: Unruptured intracranial aneurysms: natural history and clinical management. Update on the International Study of Unruptured Intracranial Aneurysms. Neuroimaging Clin N Am 16: 383-390, 2006: vii. 31. Wiebers DO, Whisnant JP, Huston J 3rd, Meissner I, Brown RD Jr, Piepgras DG, Forbes GS, Thielen K, Nichols D, O’Fallon WM, Peacock J, Jaeger L, Kassell NF, Kongable-Beckman GL, Torner JC: Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet 362: 103-110, 2003. 32. Wiebers DO, Whisnant JP, O’Fallon WM: The natural history of unruptured intracranial aneurysms. N Engl J Med 304:696-698, 1981. 33. Woertgen C, Rothoerl RD, Albert R, Schebesch KM, Ullrich O-W: Effects of temporary clipping during aneurysm surgery. Neurol Res 30:542-546, 2008. 34. Wong JM, Ziewacz JE, Ho AL, Panchmatia JR, Kim AH, Bader AM, Thompson BG, Du R, Gawande AA: Patterns in neurosurgical adverse events: open cerebrovascular neurosurgery. Neurosurg Focus 33:E15, 2012.
24. Snyder LA, Spetzler RF: Current indications for indocyanine green angiography. World Neurosurg 76:405-406, 2011. 25. Suzuki K, Kodama N, Sasaki T, Matsumoto M, Konno Y, Sakuma J, Oinuma M, Murakawa M: Intraoperative monitoring of blood flow insufficiency in the anterior choroidal artery during aneurysm surgery. J Neurosurg 98:507-514, 2003.
Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2013.07.094 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com
26. Taylor CL, Selman WR: Temporary vascular occlusion during cerebral aneurysm surgery. Neurosurg Clin N Am 9:673-679, 1998.
WORLD NEUROSURGERY - (-): ---, MONTH 2014
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Gary K. Steinberg, M.D., Ph.D. Bernard and Ronni Lacroute-William Randolph Hearst Professor of Neurosurgery and the Neurosciences Chairman, Department of Neurosurgery Stanford University School of Medicine
Temporary Clipping for Unruptured Aneurysms Nitin Mukerji, Douglas J. Cook, Gary K. Steinberg
T
he stakes are often higher when operating on unruptured aneurysms compared with ruptured aneurysms because the patients are usually neurologically normal or minimally symptomatic. These are either incidental aneurysms discovered during screening for other symptoms or additional aneurysms in patients with subarachnoid hemorrhage. Unruptured aneurysms are being discovered and treated at an increasing rate, primarily as a result of the availability and improved quality of diagnostic imaging as well as a better understanding of the natural history. When operating on these aneurysms, the neurosurgeon generally has had adequate time to consider every possible scenario and plan ahead with the anesthesia team. Depending on the size, location, and morphology of the aneurysm and the surrounding vasculature, the neurosurgeon has the option of using temporary artery occlusion (TAO) or one of the cardiac standstill methods to facilitate dissection. The fundamental question to answer before discussing temporary clipping is whether an unruptured aneurysm requires any treatment. With agreement to proceed to treatment, the next question is whether treatment should be endovascular or surgical (13, 16, 18, 27, 29-31). Available natural history data do not allow us to answer these questions with absolute accuracy (19, 30). Although endovascular treatment is considered superior for certain types of ruptured aneurysms, no randomized evidence exists for unruptured aneurysms (13, 16, 17). The interpretation of current literature varies by center, country, and skill of the treating surgeon. Perhaps the only points on which most neurosurgeons agree are that aneurysms in patients with other prior ruptured aneurysms, giant aneurysms, and aneurysms in relation to the communicating arteries and posterior circulation are more likely to bleed and require treatment. Microsurgical
Key words Elective aneurysm clipping - Temporary artery occlusion -
Abbreviations and Acronyms TAO: Temporary artery occlusion
clipping is generally the best available option for middle cerebral artery aneurysms (9, 10, 17, 18, 22, 30). The patient’s age, comorbidities, and surgical risks also must be considered, balancing them against any modality of treatment. Epidemiologic evidence from multiple sources suggests that most incidentally discovered unruptured intracranial aneurysms do not rupture (9, 10, 17, 18, 22, 30-32). Identifying which unruptured intracranial aneurysms are at greatest risk of rupture is important when considering which ones to repair. It is also important to compare size, site, and group-specific natural history rates with size, site, and age-specific morbidity and mortality associated with repair of unruptured intracranial aneurysms because worse natural history risk is often associated with increased risk of aneurysm repair (9, 10, 17, 18, 22, 30-32). Patient age is crucial to decision making because of its major effect on operative morbidity and mortality; however, it does not substantially affect natural history. The effect of age is most notable in patients approximately 50 years old for open surgery and approximately 70 years old for endovascular procedures (14, 15). The authors in the current study found that aneurysm location (posterior vs. anterior circulation) was the most important prognostic predictor of poor outcome. Intraoperative rupture is less common in elective aneurysm clipping, and we employ Tao in selective cases at Stanford. The main use of temporary clips should be to facilitate aneurysm dissection and visualization (5), especially for larger aneurysms or aneurysms with major branches or perforators incorporated into the aneurysm base. Complete circumferential exposure of the aneurysm, branches, and perforators is required for safe and effective clipping of cerebral aneurysms. Better exposure and visualization prevent residual aneurysm necks or parent vessel or
Department of Neurosurgery, Stanford University School of Medicine, Stanford, California, USA To whom correspondence should be addressed: Gary K. Steinberg, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2013.07.094
WORLD NEUROSURGERY - (-): ---, MONTH 2014
www.WORLDNEUROSURGERY.org
1
PERSPECTIVES
perforator occlusion. Visualization is particularly important in areas deep and adjacent to the skull base, such as in the treatment of paraclinoid, basilar apex, and certain anterior communicating and posterior communicating artery aneurysms. Using temporary clips electively to facilitate dissection can help prevent an intraoperative rupture in most cases (4-6, 11, 20, 23). Elective TAO may be very helpful for aneurysms of the posterior circulation, including basilar aneurysms (5, 6, 11, 20, 23). In the event of an unforeseen intraoperative rupture, a TAO proceeding to permanent clipping is often necessary. The limitations of TAO and the alternatives require mention. A shortcoming of TAO is that it limits visibility and room for manipulation when operating in narrow surgical corridors close to the skull base, especially when operating on giant aneurysms (1, 8). TAO is also known to be associated with postoperative ischemic deficits, especially when the procedure is prolonged (6, 20). In such situations, it is reasonable to consider cardiac standstill techniques. When appropriately anticipated and planned, these techniques can be safely used. Drake et al. first reported the use of deep hypothermic circulatory arrest for the clipping of giant aneurysms approximately 40 years ago (2, 21), and the technique has been revived in recent years (3). Circulatory arrest decreases the inflow and pressure of the aneurysmal mass, and this allows the aneurysm to be collapsed, facilitating circumferential exposure. Deep hypothermic circulatory arrest also has the advantage of providing a bloodless surgical field; with adjuvant deep hypothermia, this is highly neuroprotective (21). However, circulatory arrest is cumbersome because a cardiopulmonary bypass is required, and the deep hypothermia required can be associated with development of coagulopathy and electrolyte abnormalities. Heparin is also required and increases the risk of intracranial bleeding (2). Groff et al. (7) first described transient adenosine-induced asystole during the open treatment of cerebral aneurysms in 1999 in posterior circulation aneurysms. The use of adenosine for cardiac standstill is now common, and its safety profile has been well reported (1, 8). It is important to be aware of this technique and to use it judiciously when required. Adenosine is an endogenous purine nucleoside whose mechanism of action involves reducing accumulation of intracellular cyclic adenosine monophosphate in cells. Adenosine inhibits adenylate cyclase and reduces intracellular calcium current in the myocardium. Adenosine affects both the sinoatrial and the atrioventricular nodes, making it the drug of choice for the treatment of paroxysmal supraventricular tachycardia. Other surgical uses for transient adenosine-induced asystole include endovascular aortic aneurysm repair and treatment of endovascular arteriovenous malformation (1, 8, 21).
REFERENCES 1. Bendok BR, Gupta DK, Rahme RJ, Eddleman CS, Adel JG, Sherma AK, Surdell DL, Bebawy JF, Koht A, Batjer HH: Adenosine for temporary flow arrest during intracranial aneurysm surgery: a single-center retrospective review. Neurosurgery 69:815-820, 2011 [discussion 820-821]. 2. Connolly ES Jr, Solomon RA: Hypothermic cardiac standstill for cerebral aneurysm surgery. Neurosurg Clin N Am 9:681-695, 1998.
2
www.SCIENCEDIRECT.com
The use of adenosine in aneurysm surgery is attractive for several reasons. Its action is characterized by rapid onset and rapid spontaneous reversal. This reversal is due to fast receptormediated uptake into erythrocytes and endothelial cells where the adenosine is inactivated. It can be administered repeatedly with predictable effects (1, 8, 21). There is no evidence of hematologic or biochemical toxicities associated with adenosine, and it has a favorable side-effect profile. Reported side effects include flushing, chest pain, and shortness of breath. Reported cardiac events in high-risk patients are infrequent and mild when they occur. A reduction in brain volume also occurs, giving the surgeon extra space and room for manipulation; this compares favorably with techniques such as TAO, which may reduce the window of access (1, 8, 21). The use of temporary clips remains the “gold standard.” Adenosine should be regarded as an additional and potentially synergistic tool with temporary clips, not a replacement for them. It is important to be reassured of the safety profile of this time-tested technique, and Griessenauer et al. should be commended for the meticulous presentation of their results. Many surgeons tend to use adjuncts such as neuromonitoring, mild hypothermia, neuroprotective drugs, and induced hypertension to decrease the risk of causing infarcts during TAO (12, 24-26, 28, 33, 34). TAO data may be of even greater relevance to unruptured aneurysms compared with ruptured aneurysms because these are increasingly the aneurysms that neurosurgeons clip in the wake of advancements in endovascular techniques and as more data on the long-term effectiveness of endovascular therapy emerge. Although the study by Griessenauer et al. was planned as a prospective study, it has a few limitations, and the authors have done a nice job of acknowledging and discussing these. The fact that total occlusion time was not significant in the binary logistic regression is most likely due to the authors’ policy of unoccluding and reperfusing each time the occlusion time was thought to be >15e20 minutes. This is a well-accepted technique, although criticisms exist. For a prospective study on TAO in unruptured aneurysms, the use of Glasgow Outcome Scale scores as an outcome measure instead of neuropsychologic testing and the lack of radiologic follow-up to detect new infarcts are potential weaknesses. The lack of controls also makes it difficult to draw conclusions regarding the benefit of temporary occlusion for unruptured aneurysms. In conclusion, despite the limitations, the authors should be congratulated on presenting the largest series available for TAO in patients with unruptured aneurysms. It is hoped that future studies in this field will extend this work.
3. Darsaut TE, Darsaut NM, Chang SD, Silverberg GD, Shuer LM, Tian L, Dodd RL, Do HM, Marks MP, Steinberg GK: Predictors of clinical and angiographic outcome after surgical or endovascular therapy of very large and giant intracranial aneurysms. Neurosurgery 68:903-915, 2011 [discussion 915]. 4. Dhandapani S, Pal SS, Gupta SK, Mohindra S, Chhabra R, Malhotra SK: Does the impact of elective temporary clipping on intraoperative rupture really influence neurological outcome after surgery for ruptured anterior circulation
aneurysms? A prospective multivariate study. Acta Neurochir 155:237-246, 2013. 5. Eftekhar B, Morgan MK: Indications for the use of temporary arterial occlusion during aneurysm repair: an institutional experience. J Clin Neurosci 18:905-909, 2011. 6. Giannotta SL, Oppenheimer JH, Levy ML, Zelman V: Management of intraoperative rupture of aneurysm without hypotension. Neurosurgery 28:531-535, 1991 [discussion 535-536].
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2013.07.094
PERSPECTIVES
7. Groff MW, Adams DC, Kahn RA, Kumbar UM, Yang BY, Bederson JB: Adenosine-induced transient asystole for management of a basilar artery aneurysm. Case report. J Neurosurg 91:687-690, 1999.
Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomized trial. J Stroke Cerebrovasc Dis 11:304-314, 2002.
8. Guinn NR, McDonagh DL, Borel CO, Wright DR, Zomorodi AR, Powers CJ, Warner DS, Lam AM, Britz GW: Adenosine-induced transient asystole for intracranial aneurysm surgery: a retrospective review. J Neurosurg Anesthesiol 23:35-40, 2011.
18. Molyneux AJ, Kerr RS, Yu LM, Clarke M, Sneade M, Yarnold JA, Sandercock P: International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet 366: 809-817, 2005.
9. Hernesniemi J, Dashti R, Lehecka M, Niemelä M, Rinne J, Lehto H, Ronkainen A, Koivisto T, Jääskeläinen JE: Microneurosurgical management of anterior communicating artery aneurysms. Surg Neurol 70:8-28, 2008 [discussion 29]. 10. Lawton MT: Editorial: middle cerebral artery aneurysms. J Neurosurg 118:947-948, 2013 [discussion 948-949]. 11. Lawton MT, Quinones-Hinojosa A, Chang EF, Yu T: Thrombotic intracranial aneurysms: classification scheme and management strategies in 68 patients. Neurosurgery 56:441-454, 2005 [discussion 441-454]. 12. McDermott MW, Durity FA, Borozny M, Mountain MA: Temporary vessel occlusion and barbiturate protection in cerebral aneurysm surgery. Neurosurgery 25:54-61, 1989 [discussion 61-52]. 13. McDougall CG, Spetzler RF, Zabramski JM, Partovi S, Hills NK, Nakaji P, Albuquerque FC: The Barrow Ruptured Aneurysm Trial. J Neurosurg 116:135-144, 2012. 14. Mitchell P, Jakubowski J: Estimate of the maximum time interval between formation of cerebral aneurysm and rupture. J Neurol Neurosurg Psychiatry 69:760-767, 2000. 15. Mitchell P, Kerr R, Mendelow AD, Molyneux A: Could late rebleeding overturn the superiority of cranial aneurysm coil embolization over clip ligation seen in the International Subarachnoid Aneurysm Trial? J Neurosurg 108:437-442, 2008. 16. Molyneux A, Kerr R, Stratton I, Sandercock P, Clarke M, Shrimpton J, Holman R: International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet 360:1267-1274, 2002. 17. Molyneux A, Kerr R, Stratton I, Sandercock P, Clarke M, Shrimpton J, Holman R: International
19. Morita A, Kirino T, Hashi K, Aoki N, Fukuhara S, Hashimoto N, Nakayama T, Sakai M, Teramoto A, Tominari S, Yoshimoto T: The natural course of unruptured cerebral aneurysms in a Japanese cohort. N Engl J Med 366:2474-2482, 2012. 20. Ogilvy CS, Carter BS, Kaplan S, Rich C, Crowell RM: Temporary vessel occlusion for aneurysm surgery: risk factors for stroke in patients protected by induced hypothermia and hypertension and intravenous mannitol administration. J Neurosurg 84:785-791, 1996. 21. Powers CJ, Wright DR, McDonagh DL, Borel CO, Zomorodi AR, Britz GW: Transient adenosineinduced asystole during the surgical treatment of anterior circulation cerebral aneurysms: technical note. Neurosurgery 67:461-470, 2010. 22. Rodriguez-Hernandez A, Sughrue ME, Akhavan S, Habdank-Kolaczkowski J, Lawton MT: Current management of middle cerebral artery aneurysms: surgical results with a “clip first” policy. Neurosurgery 72:415-427, 2013. 23. Schramm J, Cedzich C: Outcome and management of intraoperative aneurysm rupture. Surg Neurol 40:26-30, 1993.
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Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2013.07.094 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com
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