- Email: [email protected]
Treatment of Ruptured Aneurysms: Earlier is Better
Perspectives Commentary on: Ultra-Early (within 24 Hours) Aneurysm Treatment After Subarachnoid Hemorrhage by Wong et al. pp. 311-315.
Ji-Zong Zhao, M.D. Professor and Chairman, Department of Neurosurgery Beijing Tiantan Hospital, Capital Medical University
Treatment of Ruptured Aneurysms: Earlier is Better Alexander G. Weil1,2 and Ji-Zong Zhao2
R
ebleeding is the primary cause of early morbidity and mortality after aneurysmal subarachnoid hemorrhage (SAH) (2, 5, 20). The efficacy of aneurysm obliteration at preventing rebleeding and improving outcome after SAH has been well established since the 1970s. However, the debate over optimal timing of aneurysm treatment after SAH has carried on for over 4 decades (1, 2, 4, 7-15, 17-21). Initially, the debate centered on the risks of rebleeding encountered while awaiting late surgery (⬎10 days) versus the morbidity incurred by operating early (⬍3 days) on an acutely injured and swollen brain or during the intermediate period of cerebral vasospasm (3 to 10 days). In the early 1980s, the International Cooperative Study, a large, multicenter, prospective, observational trial, addressed the issue of optimal timing for surgery. This study found that early surgery (⬍3 days) was at least equivalent to delayed surgery (⬎10 days) in terms of mortality and morbidity for good grade patients (7, 8). Over the next decade (1980s), improvements in the overall medical management of SAH, and in particular, the prevention and treatment of vasospasm and delayed cerebral ischemia, provided a further rationale for neurosurgeons to perform early aneurysm surgery (16, 18, 19). The vast majority of studies that ensued, including one randomized control trial and multiple observational studies, suggested that early and even intermediate surgery were associated with a better outcome and shorter hospitalization than later surgery in aneurysmal SAH patients, especially in good clinical grade patients, but also in poor-grade patients (4, 12, 13). Early aneurysm obliteration (⬍72 hours), either by neurosurgical clipping or endovascular coiling, has been widely adopted by neurovascular centers worldwide for over a decade.
third post-SAH day has been considered to be relatively late in terms of prevention of rebleeding (1, 5, 9, 10, 15, 20). For this reason, most experts now recommend repair of the aneurysm as early as possible, or so-called ultra-early (⬍24 hours) treatment (1, 9, 10, 14, 15). Contemporary observational studies provide direct evidence that ultra-early clipping (9, 10, 14, 15) and coiling (1, 15) are feasible and improve outcome, especially in poorgrade patients, who are at increased risk of rebleeding. Conversely, some authors have argued that ultra-early aneurysm repair may have the pitfall of increased surgical morbidity related to the technical difficulties associated with operating on an acutely edema/hyperemic brain and operating in suboptimal conditions at night with inexperienced staff (9, 11, 15). However, if operating on a swollen brain is a concern, then ultra-early surgery would not necessarily be disadvantageous compared with surgery on days 2 or 3 post-SAH because maximal cerebral edema often peaks in a delayed fashion 72 hours after the cerebral insult (3). This would evidently not be relevant for endovascular treatment, which should be offered as soon as possible (1). Also, if availability of ancillary personnel such as neurophysiologists and neuroanesthetists is a concern, then patients should be transferred as soon as possible to a specialized neurovascular center where such services would be readily available without an excessive delay. Perhaps the only reasonable exception to performing ultra-early aneurysm repair are poor-grade patients in whom a potential withdrawal of care is being considered (e.g., elderly, poor general condition, terminal illness) or those with hydrocephalus in which a 24-hour external ventricular drain trial would help determine the real extent of SAH-related brain injury.
However, because most rebleeding occurs within the first 24 hours (especially the first 6 hours), when mortality can reach 80%, early intervention to secure the aneurysm on the second or
It is important to note that delays from late referral, time required for interinstitutional transfer, diagnostic delays, time required to organize the procedure, and medical reasons render ultra-early
Key words 䡲 Aneurysm 䡲 Clipping 䡲 Embolization 䡲 Subarachnoid hemorrhage 䡲 Timing
Abbreviations and Acronyms IMASH: Intravenous Magnesium Sulphate After Aneurysmal Subarachnoid Hemorrhage SAH: Subarachnoid hemorrhage SF-36: Short Form-36 WFNS: World Federation of Neurological Societies
WORLD NEUROSURGERY 77 [2]: 263-265, FEBRUARY 2012
From the 1Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China; and 2Neurosurgery Service, Department of Surgery, Notre Dame Hospital, University of Montreal Hospital Center (CHUM), Montreal, Quebec, Canada To whom correspondence should be addressed: Ji-Zong Zhao, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2012) 77, 2:263-265. DOI: 10.1016/j.wneu.2011.12.073
www.WORLDNEUROSURGERY.org
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PERSPECTIVES
intervention underperformed even in many centers that aim to treat aneurysms as early as possible (9, 10, 17, 21). In this setting, a short-course antifibrinolytic therapy may have a role, as it has been shown to reduce rebleeding and possibly improve outcome when discontinued immediately after early aneurysm repair (6); however, evidence is insufficient to support its systematic use (20). In this issue of WORLD NEUROSURGERY, Wong et al. report on a series of 268 patients retrieved from the Intravenous Magnesium Sulphate After Aneurysmal Subarachnoid Hemorrhage (IMASH) study who were evaluated for a relation between timing of aneurysm treatment and outcome. The authors found improved Short Form-36 (SF-36) mental score in patients who underwent ultra-early (⬍24 hours) compared with early (⬍ 72 hours) aneurysm treatment after SAH, especially poor-grade patients. Overall, ultra-early intervention was not associated with a statistically significant reduction in rebleeding, mortality, or clinical outcome. The reduced rate of rebleeding seen in poor-grade patients treated ultra-early did not reach statistical significance. The authors interpret their results to imply that ultra-early aneurysm treatment (⬍24 hours) with clipping or coiling reduces the incidence of rebleeding, which translates into improved clinical outcome at 6 months. Although these conclusions validate the widespread policy of most neurovascular centers to treat aneurysms as early as possible, there are a number of biases that preclude the ability to make firm conclusions based solely on this study. This is a post-hoc analysis of aneurysmal SAH patients randomized to receive either magnesium sulfate or placebo, and not randomized on timing of aneurysm repair. Furthermore, the management protocol is not specified, and it is not clear why some patients underwent ultra-early treatment and others later treatment. The timing of surgery was thus determined by unknown factors other than randomization, and these confounding factors bias the study. The difference (e.g., SF-36 mental score) or similarities (rebleeding rate, mortality, clinical outcome, SF-36 physical score) observed between both groups may be due to differences in the patient characteristics of both cohorts and not directly from the timing of surgery or rebleeding rate, as suggested by the authors. For example, patients in the ultra-early surgery group were younger and had a higher World Federation of Neurological Societies (WFNS) grade, which would inevitably
REFERENCES 1. Baltsavias GS, Byrne JV, Halsey J, Coley SC, Sohn MJ, Molyneux AJ: Effects of timing of coil embolization after aneurysmal subarachnoid hemorrhage on procedural morbidity and outcomes. Neurosurgery 47: 1320-1329, 2000. 2. Broderick J, Brott T, Duldner J, Tomsick T, Leach A: Initial and recurrent bleeding are the major causes of death following subarachnoid hemorrhage. Stroke 25:1342-1347, 1994. 3. Claassen J, Carhuapoma JR, Kreiter KT, Du EY, Connolly ES, Mayer SA: Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome. Stroke 33:1225-1232, 2002.
264
www.SCIENCEDIRECT.com
introduce a bias in the results. The direction of this bias is hard to predict. One would normally think that more poor-grade patients would result in a worse outcome. However, there was a higher proportion of patients with intracranial hemorrhage–related coma who underwent emergent decompressive surgery in the ultraearly group, which could mean that more patients had reversible neurological dysfunction in contrast to patients with no surgically correctable findings on computed tomography scan, who are more likely to fare worse in the long run. Also, it is also not clear whether WFNS grading was performed before or after external ventricular drain placement. Furthermore, there is an inevitable selection bias favoring late surgery because patients in poor condition may have already died in the first 48 to 72 hours before treatment, and thus would have been excluded from the analysis. This would have been clearly different in a randomized trial with intention-to-treat analysis. Finally, the outcome data did not include important postoperative angiographic and neuroimaging results, such as aneurysm obliteration and postprocedural retraction injury/stroke, respectively. Only a randomized controlled trial could provide definite evidence for the indication for ultra-early aneurysm treatment. However, such a study would probably not be feasible due to a lack of clinical equipoise: given the welldocumented early and cumulative rate of rebleeding (2, 5, 7, 8), it would be unethical to delay aneurysm treatment for 48 to 72 hours when it could be performed earlier. The authors are to be commended for their effort in assessing whether ultra-early aneurysm repair actually affects outcome in aneurysmal SAH patients. Although this study does not present definite evidence for the benefits of ultra-early aneurysm treatment, there is enough direct and indirect scientific evidence for this approach to recommend it on a routine basis in neurovascular centers worldwide (1, 7-10, 14, 15). The exception being, as discussed earlier, poor-grade patients in whom withdrawal of care is being considered, particularly those presenting with significant hydrocephalus. It is the responsibility of specialized neurovascular centers to ensure the availability of sufficient ancillary personnel during weekend days to carry out safely these procedures and not delay aneurysm treatment. It is also the responsibility of centers without such capacity to transfer SAH patients as soon as possible to specialized neurovascular centers to avoid unjustifiable delays in patient care.
4. de Gans KMS, Nieuwkamp DJMS, Rinkel GJEMD, Algra AMD: Timing of aneurysm surgery in subarachnoid hemorrhage: a systematic review of the literature. Neurosurgery 50:336-342, 2002. 5. Fujii Y, Takeuchi S, Sasaki O, Minakawa T, Koike T, Tanaka R: Ultra-early rebleeding in spontaneous subarachnoid hemorrhage. J Neurosurg 84:35-42, 1996. 6. Hillman J, Fridriksson S, Nilsson O, Yu Z, Saveland H, Jakobsson KE: Immediate administration of tranexamic acid and reduced incidence of early rebleeding after aneurysmal subarachnoid hemorrhage: a prospective randomized study. J Neurosurg 97:771-778, 2002. 7. Kassell NF, Boarini DJ, Adams HP Jr, Sahs AL, Graf CJ, Torner JC, Gerk MK: Overall management of
ruptured aneurysm: comparison of early and late operation. Neurosurgery 9:120-128, 1981.
8. Kassell NF, Torner JC, Jane JA, Haley EC Jr, Adams HP: The international cooperative study on the timing of aneurysm surgery. Part 2: surgical results. J Neurosurg 73:37-47, 1990.
9. Laidlaw JD, Siu KH: Ultra-early surgery for aneurysmal subarachnoid hemorrhage: outcomes for a consecutive series of 391 patients not selected by grade or age: J Neurosurg 97:250-258, 2002.
10. Laidlaw JD, Siu KH: Poor-grade aneurysmal subarachnoid hemorrhage: outcome after treatment with urgent surgery. Neurosurgery 53:1275-1280, 2003.
WORLD NEUROSURGERY, DOI:10.1016/j.wneu.2011.12.073
PERSPECTIVES
11. Maurice-Williams RS, Wadley JP: Delayed surgery for ruptured intracranial aneurysms: a reappraisal. Br J Neurosurg 11:104-109, 1997. 12. McLaughlin N, Bojanowski MW: Aneurysmal surgery in the presence of angiographic vasospasm: an outcome assessment. Can J Neurol Sci 33:181-188, 2006. 13. Ohman J, Heiskanen O: Timing of operation for ruptured supratentorial aneurysms: a prospective randomized study. J Neurosurg 70:55-60, 1989. 14. Pan JW, Zhan RY, Wen L, Tong Y, Wan S, Zhou WY: Ultra-early surgery for poor-grade aneurysmal subarahnoid hemorrhage: a preliminary study. Yonsei Med J 50:521-524, 2009. 15. Phillips TJ, Dowling RJ, Yan B, Laidlaw JD, Mitchell PJ: Does treatment of ruptured intracranial aneurysms within 24 hours improve clinical outcome? Stroke 42:1936-1945, 2011.
16. Pickard JD, Murray GD, Illingworth R, Shaw MD, Teasdale GM, Foy PM, Humphrey PR, Lang DA, Nelson R, Richards P, Sinar J, Bailey S, Skene A: Effect of oral nimodipine on cerebral infarction and outcome after subarachnoid haemorrhage: British aneurysm nimodipine trial. BMJ 298:636-642, 1989. 17. Roos YBWEM, Beenen LFM, Groen RJM, Albrecht KW, Vermeulen M: Timing of surgery in patients with aneurysmal subarachnoid haemorrhage: rebleeding is still the major cause of poor outcome in neurosurgical units that aim at early surgery. J Neurol Neurosurg Psychiatry 63:490-493, 1997. 18. Ross N, Hutchinson P, Seeley H, Kirkpatrick P: Timing of surgery for supratentorial aneurysmal subarachnoid haemorrhage: report of a prospective study. J Neurol Neurosurg Psychiatry 72:480-484, 2002. 19. Solomon RA, Fink ME, Lennihan L: Early aneurysm surgery and prophylactic hypervolemic hypertensive therapy for the treatment of aneurysmal subarachnoid hemorrhage. Neurosurgery 23:699-704, 1988.
WORLD NEUROSURGERY 77 [2]: 263-265, FEBRUARY 2012
20. Starke RM, Connolly ES Jr, The Participants in the International Multi-Disciplinary Consensus Conference on the Critical Care Management of Subarachnoid Hemorrhage: Rebleeding after aneurysmal subarachnoid hemorrhage. Neurocrit Care 15: 241-246, 2011.
21. Whitfield PC, Moss H, Ohare D, Smielewski P, Pickard JD, Kirkpatrick PJ: An audit of aneurysmal subarachnoid haemorrhage: earlier resuscitation and surgery reduces inpatient stay and deaths from rebleeding. J Neurol Neurosurg Psychiatry 60:301306, 1996. Citation: World Neurosurg. (2012) 77, 2:263-265. DOI: 10.1016/j.wneu.2011.12.073 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter © 2012 Elsevier Inc. All rights reserved.
www.WORLDNEUROSURGERY.org
265
Ji-Zong Zhao, M.D. Professor and Chairman, Department of Neurosurgery Beijing Tiantan Hospital, Capital Medical University
Treatment of Ruptured Aneurysms: Earlier is Better Alexander G. Weil1,2 and Ji-Zong Zhao2
R
ebleeding is the primary cause of early morbidity and mortality after aneurysmal subarachnoid hemorrhage (SAH) (2, 5, 20). The efficacy of aneurysm obliteration at preventing rebleeding and improving outcome after SAH has been well established since the 1970s. However, the debate over optimal timing of aneurysm treatment after SAH has carried on for over 4 decades (1, 2, 4, 7-15, 17-21). Initially, the debate centered on the risks of rebleeding encountered while awaiting late surgery (⬎10 days) versus the morbidity incurred by operating early (⬍3 days) on an acutely injured and swollen brain or during the intermediate period of cerebral vasospasm (3 to 10 days). In the early 1980s, the International Cooperative Study, a large, multicenter, prospective, observational trial, addressed the issue of optimal timing for surgery. This study found that early surgery (⬍3 days) was at least equivalent to delayed surgery (⬎10 days) in terms of mortality and morbidity for good grade patients (7, 8). Over the next decade (1980s), improvements in the overall medical management of SAH, and in particular, the prevention and treatment of vasospasm and delayed cerebral ischemia, provided a further rationale for neurosurgeons to perform early aneurysm surgery (16, 18, 19). The vast majority of studies that ensued, including one randomized control trial and multiple observational studies, suggested that early and even intermediate surgery were associated with a better outcome and shorter hospitalization than later surgery in aneurysmal SAH patients, especially in good clinical grade patients, but also in poor-grade patients (4, 12, 13). Early aneurysm obliteration (⬍72 hours), either by neurosurgical clipping or endovascular coiling, has been widely adopted by neurovascular centers worldwide for over a decade.
third post-SAH day has been considered to be relatively late in terms of prevention of rebleeding (1, 5, 9, 10, 15, 20). For this reason, most experts now recommend repair of the aneurysm as early as possible, or so-called ultra-early (⬍24 hours) treatment (1, 9, 10, 14, 15). Contemporary observational studies provide direct evidence that ultra-early clipping (9, 10, 14, 15) and coiling (1, 15) are feasible and improve outcome, especially in poorgrade patients, who are at increased risk of rebleeding. Conversely, some authors have argued that ultra-early aneurysm repair may have the pitfall of increased surgical morbidity related to the technical difficulties associated with operating on an acutely edema/hyperemic brain and operating in suboptimal conditions at night with inexperienced staff (9, 11, 15). However, if operating on a swollen brain is a concern, then ultra-early surgery would not necessarily be disadvantageous compared with surgery on days 2 or 3 post-SAH because maximal cerebral edema often peaks in a delayed fashion 72 hours after the cerebral insult (3). This would evidently not be relevant for endovascular treatment, which should be offered as soon as possible (1). Also, if availability of ancillary personnel such as neurophysiologists and neuroanesthetists is a concern, then patients should be transferred as soon as possible to a specialized neurovascular center where such services would be readily available without an excessive delay. Perhaps the only reasonable exception to performing ultra-early aneurysm repair are poor-grade patients in whom a potential withdrawal of care is being considered (e.g., elderly, poor general condition, terminal illness) or those with hydrocephalus in which a 24-hour external ventricular drain trial would help determine the real extent of SAH-related brain injury.
However, because most rebleeding occurs within the first 24 hours (especially the first 6 hours), when mortality can reach 80%, early intervention to secure the aneurysm on the second or
It is important to note that delays from late referral, time required for interinstitutional transfer, diagnostic delays, time required to organize the procedure, and medical reasons render ultra-early
Key words 䡲 Aneurysm 䡲 Clipping 䡲 Embolization 䡲 Subarachnoid hemorrhage 䡲 Timing
Abbreviations and Acronyms IMASH: Intravenous Magnesium Sulphate After Aneurysmal Subarachnoid Hemorrhage SAH: Subarachnoid hemorrhage SF-36: Short Form-36 WFNS: World Federation of Neurological Societies
WORLD NEUROSURGERY 77 [2]: 263-265, FEBRUARY 2012
From the 1Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China; and 2Neurosurgery Service, Department of Surgery, Notre Dame Hospital, University of Montreal Hospital Center (CHUM), Montreal, Quebec, Canada To whom correspondence should be addressed: Ji-Zong Zhao, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2012) 77, 2:263-265. DOI: 10.1016/j.wneu.2011.12.073
www.WORLDNEUROSURGERY.org
263
PERSPECTIVES
intervention underperformed even in many centers that aim to treat aneurysms as early as possible (9, 10, 17, 21). In this setting, a short-course antifibrinolytic therapy may have a role, as it has been shown to reduce rebleeding and possibly improve outcome when discontinued immediately after early aneurysm repair (6); however, evidence is insufficient to support its systematic use (20). In this issue of WORLD NEUROSURGERY, Wong et al. report on a series of 268 patients retrieved from the Intravenous Magnesium Sulphate After Aneurysmal Subarachnoid Hemorrhage (IMASH) study who were evaluated for a relation between timing of aneurysm treatment and outcome. The authors found improved Short Form-36 (SF-36) mental score in patients who underwent ultra-early (⬍24 hours) compared with early (⬍ 72 hours) aneurysm treatment after SAH, especially poor-grade patients. Overall, ultra-early intervention was not associated with a statistically significant reduction in rebleeding, mortality, or clinical outcome. The reduced rate of rebleeding seen in poor-grade patients treated ultra-early did not reach statistical significance. The authors interpret their results to imply that ultra-early aneurysm treatment (⬍24 hours) with clipping or coiling reduces the incidence of rebleeding, which translates into improved clinical outcome at 6 months. Although these conclusions validate the widespread policy of most neurovascular centers to treat aneurysms as early as possible, there are a number of biases that preclude the ability to make firm conclusions based solely on this study. This is a post-hoc analysis of aneurysmal SAH patients randomized to receive either magnesium sulfate or placebo, and not randomized on timing of aneurysm repair. Furthermore, the management protocol is not specified, and it is not clear why some patients underwent ultra-early treatment and others later treatment. The timing of surgery was thus determined by unknown factors other than randomization, and these confounding factors bias the study. The difference (e.g., SF-36 mental score) or similarities (rebleeding rate, mortality, clinical outcome, SF-36 physical score) observed between both groups may be due to differences in the patient characteristics of both cohorts and not directly from the timing of surgery or rebleeding rate, as suggested by the authors. For example, patients in the ultra-early surgery group were younger and had a higher World Federation of Neurological Societies (WFNS) grade, which would inevitably
REFERENCES 1. Baltsavias GS, Byrne JV, Halsey J, Coley SC, Sohn MJ, Molyneux AJ: Effects of timing of coil embolization after aneurysmal subarachnoid hemorrhage on procedural morbidity and outcomes. Neurosurgery 47: 1320-1329, 2000. 2. Broderick J, Brott T, Duldner J, Tomsick T, Leach A: Initial and recurrent bleeding are the major causes of death following subarachnoid hemorrhage. Stroke 25:1342-1347, 1994. 3. Claassen J, Carhuapoma JR, Kreiter KT, Du EY, Connolly ES, Mayer SA: Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome. Stroke 33:1225-1232, 2002.
264
www.SCIENCEDIRECT.com
introduce a bias in the results. The direction of this bias is hard to predict. One would normally think that more poor-grade patients would result in a worse outcome. However, there was a higher proportion of patients with intracranial hemorrhage–related coma who underwent emergent decompressive surgery in the ultraearly group, which could mean that more patients had reversible neurological dysfunction in contrast to patients with no surgically correctable findings on computed tomography scan, who are more likely to fare worse in the long run. Also, it is also not clear whether WFNS grading was performed before or after external ventricular drain placement. Furthermore, there is an inevitable selection bias favoring late surgery because patients in poor condition may have already died in the first 48 to 72 hours before treatment, and thus would have been excluded from the analysis. This would have been clearly different in a randomized trial with intention-to-treat analysis. Finally, the outcome data did not include important postoperative angiographic and neuroimaging results, such as aneurysm obliteration and postprocedural retraction injury/stroke, respectively. Only a randomized controlled trial could provide definite evidence for the indication for ultra-early aneurysm treatment. However, such a study would probably not be feasible due to a lack of clinical equipoise: given the welldocumented early and cumulative rate of rebleeding (2, 5, 7, 8), it would be unethical to delay aneurysm treatment for 48 to 72 hours when it could be performed earlier. The authors are to be commended for their effort in assessing whether ultra-early aneurysm repair actually affects outcome in aneurysmal SAH patients. Although this study does not present definite evidence for the benefits of ultra-early aneurysm treatment, there is enough direct and indirect scientific evidence for this approach to recommend it on a routine basis in neurovascular centers worldwide (1, 7-10, 14, 15). The exception being, as discussed earlier, poor-grade patients in whom withdrawal of care is being considered, particularly those presenting with significant hydrocephalus. It is the responsibility of specialized neurovascular centers to ensure the availability of sufficient ancillary personnel during weekend days to carry out safely these procedures and not delay aneurysm treatment. It is also the responsibility of centers without such capacity to transfer SAH patients as soon as possible to specialized neurovascular centers to avoid unjustifiable delays in patient care.
4. de Gans KMS, Nieuwkamp DJMS, Rinkel GJEMD, Algra AMD: Timing of aneurysm surgery in subarachnoid hemorrhage: a systematic review of the literature. Neurosurgery 50:336-342, 2002. 5. Fujii Y, Takeuchi S, Sasaki O, Minakawa T, Koike T, Tanaka R: Ultra-early rebleeding in spontaneous subarachnoid hemorrhage. J Neurosurg 84:35-42, 1996. 6. Hillman J, Fridriksson S, Nilsson O, Yu Z, Saveland H, Jakobsson KE: Immediate administration of tranexamic acid and reduced incidence of early rebleeding after aneurysmal subarachnoid hemorrhage: a prospective randomized study. J Neurosurg 97:771-778, 2002. 7. Kassell NF, Boarini DJ, Adams HP Jr, Sahs AL, Graf CJ, Torner JC, Gerk MK: Overall management of
ruptured aneurysm: comparison of early and late operation. Neurosurgery 9:120-128, 1981.
8. Kassell NF, Torner JC, Jane JA, Haley EC Jr, Adams HP: The international cooperative study on the timing of aneurysm surgery. Part 2: surgical results. J Neurosurg 73:37-47, 1990.
9. Laidlaw JD, Siu KH: Ultra-early surgery for aneurysmal subarachnoid hemorrhage: outcomes for a consecutive series of 391 patients not selected by grade or age: J Neurosurg 97:250-258, 2002.
10. Laidlaw JD, Siu KH: Poor-grade aneurysmal subarachnoid hemorrhage: outcome after treatment with urgent surgery. Neurosurgery 53:1275-1280, 2003.
WORLD NEUROSURGERY, DOI:10.1016/j.wneu.2011.12.073
PERSPECTIVES
11. Maurice-Williams RS, Wadley JP: Delayed surgery for ruptured intracranial aneurysms: a reappraisal. Br J Neurosurg 11:104-109, 1997. 12. McLaughlin N, Bojanowski MW: Aneurysmal surgery in the presence of angiographic vasospasm: an outcome assessment. Can J Neurol Sci 33:181-188, 2006. 13. Ohman J, Heiskanen O: Timing of operation for ruptured supratentorial aneurysms: a prospective randomized study. J Neurosurg 70:55-60, 1989. 14. Pan JW, Zhan RY, Wen L, Tong Y, Wan S, Zhou WY: Ultra-early surgery for poor-grade aneurysmal subarahnoid hemorrhage: a preliminary study. Yonsei Med J 50:521-524, 2009. 15. Phillips TJ, Dowling RJ, Yan B, Laidlaw JD, Mitchell PJ: Does treatment of ruptured intracranial aneurysms within 24 hours improve clinical outcome? Stroke 42:1936-1945, 2011.
16. Pickard JD, Murray GD, Illingworth R, Shaw MD, Teasdale GM, Foy PM, Humphrey PR, Lang DA, Nelson R, Richards P, Sinar J, Bailey S, Skene A: Effect of oral nimodipine on cerebral infarction and outcome after subarachnoid haemorrhage: British aneurysm nimodipine trial. BMJ 298:636-642, 1989. 17. Roos YBWEM, Beenen LFM, Groen RJM, Albrecht KW, Vermeulen M: Timing of surgery in patients with aneurysmal subarachnoid haemorrhage: rebleeding is still the major cause of poor outcome in neurosurgical units that aim at early surgery. J Neurol Neurosurg Psychiatry 63:490-493, 1997. 18. Ross N, Hutchinson P, Seeley H, Kirkpatrick P: Timing of surgery for supratentorial aneurysmal subarachnoid haemorrhage: report of a prospective study. J Neurol Neurosurg Psychiatry 72:480-484, 2002. 19. Solomon RA, Fink ME, Lennihan L: Early aneurysm surgery and prophylactic hypervolemic hypertensive therapy for the treatment of aneurysmal subarachnoid hemorrhage. Neurosurgery 23:699-704, 1988.
WORLD NEUROSURGERY 77 [2]: 263-265, FEBRUARY 2012
20. Starke RM, Connolly ES Jr, The Participants in the International Multi-Disciplinary Consensus Conference on the Critical Care Management of Subarachnoid Hemorrhage: Rebleeding after aneurysmal subarachnoid hemorrhage. Neurocrit Care 15: 241-246, 2011.
21. Whitfield PC, Moss H, Ohare D, Smielewski P, Pickard JD, Kirkpatrick PJ: An audit of aneurysmal subarachnoid haemorrhage: earlier resuscitation and surgery reduces inpatient stay and deaths from rebleeding. J Neurol Neurosurg Psychiatry 60:301306, 1996. Citation: World Neurosurg. (2012) 77, 2:263-265. DOI: 10.1016/j.wneu.2011.12.073 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter © 2012 Elsevier Inc. All rights reserved.
www.WORLDNEUROSURGERY.org
265