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Erschienen in: Neurocritical Care 3/2016

20.09.2016 | Original Article

Functional Outcome After Poor-Grade Subarachnoid Hemorrhage: A Single-Center Study and Systematic Literature Review

verfasst von: Airton Leonardo de Oliveira Manoel, Ann Mansur, Gisele Sampaio Silva, Menno R. Germans, Blessing N. R. Jaja, Ekaterina Kouzmina, Thomas R. Marotta, Simon Abrahamson, Tom A. Schweizer, Julian Spears, R. Loch Macdonald

Erschienen in: Neurocritical Care | Ausgabe 3/2016

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Abstract

Background and Purpose

Poor-grade subarachnoid hemorrhage (SAH) (World Federation of Neurosurgical Societies grade 4 and 5) is associated with high mortality rates and unfavorable functional outcomes. We report a single-center cohort of poor-grade SAH patients, combined with a systematic review of studies reporting functional outcome in the poor-grade SAH population.

Methods

Data on a cohort of poor-grade SAH patients treated between 2009 and 2013 were retrospectively collected and combined with a systematic review (from inception to November 2015; PubMed, Embase). Two reviewers assessed the studies independently based on predefined inclusion criteria: consecutive poor-grade SAH, functional outcome measured at least 3 months after hemorrhage, and the report of patients who died before aneurysm treatment.

Results

The search yielded 329 publications, and 23 met our inclusion criteria with 2713 subjects enrolled from 1977 to 2014 in 10 countries (including 179 poor-grade patients from our cohort). Mortality rate was 60 % (1683 patients), of which 806 (29 %) died before and 877 (31 %) died after aneurysm treatment, respectively. Treatment was undertaken in 1775 patients (1775/2826—63 %): 1347 by surgical clipping (1347/1775—76 %) and 428 (428/1775—24 %) by endovascular methods. Outcome was favorable in 794 patients (28 %) and unfavorable in 1867 (66 %). When the studies were grouped into decades, favorable outcome increased from 13 % in the late 1970s to early 1980s to 35 % in the late 1980s to early 1990s, and remained unchanged thereafter.

Conclusion

Although mortality remains high in poor-grade SAH patients, a favorable functional outcome can be achieved in approximately one-third of patients. The development of new diagnostic methods and implementation of therapeutic approaches were probably responsible for the decrease in mortality and improvement in the functional outcome from 1970 to the 1990s. The plateau in functional outcome seen thereafter might be explained by the treatment of sicker and older patients and by the lack of new therapeutic interventions specific for SAH.
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Literatur
1.
Zurück zum Zitat Hunt WEW, Hess RMR. Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg. 1968;28:14–20.CrossRefPubMed Hunt WEW, Hess RMR. Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg. 1968;28:14–20.CrossRefPubMed
2.
Zurück zum Zitat Teasdale GM, Drake CG, Hunt W, et al. A universal subarachnoid hemorrhage scale: report of a committee of the World Federation of Neurosurgical Societies. J Neurol Neurosurg Psychiatry. 1988;51:1457.CrossRefPubMedPubMedCentral Teasdale GM, Drake CG, Hunt W, et al. A universal subarachnoid hemorrhage scale: report of a committee of the World Federation of Neurosurgical Societies. J Neurol Neurosurg Psychiatry. 1988;51:1457.CrossRefPubMedPubMedCentral
3.
Zurück zum Zitat Rosengart AJ, Schultheiss KE, Tolentino J, Macdonald RL. Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke. 2007;38:2315–21.CrossRefPubMed Rosengart AJ, Schultheiss KE, Tolentino J, Macdonald RL. Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke. 2007;38:2315–21.CrossRefPubMed
4.
Zurück zum Zitat Le Roux PD, Elliott JP, Newell DW, Grady MS, Winn HR. Predicting outcome in poor-grade patients with subarachnoid hemorrhage: a retrospective review of 159 aggressively managed cases. J Neurosurg. 1996;85:39–49.CrossRefPubMed Le Roux PD, Elliott JP, Newell DW, Grady MS, Winn HR. Predicting outcome in poor-grade patients with subarachnoid hemorrhage: a retrospective review of 159 aggressively managed cases. J Neurosurg. 1996;85:39–49.CrossRefPubMed
5.
Zurück zum Zitat The participants in the international multi-disciplinary consensus conference on the critical care management of subarachnoid hemorrhage, Vespa P, Diringer MN. High-Volume Centers. Neurocrit Care. 2011;15:369–372. The participants in the international multi-disciplinary consensus conference on the critical care management of subarachnoid hemorrhage, Vespa P, Diringer MN. High-Volume Centers. Neurocrit Care. 2011;15:369–372.
6.
Zurück zum Zitat Drake CG. Report of World Federation of Neurological Surgeons Committee on a Universal Subarachnoid Hemorrhage Grading Scale. J Neurosurg. 1988;68:985–6. Drake CG. Report of World Federation of Neurological Surgeons Committee on a Universal Subarachnoid Hemorrhage Grading Scale. J Neurosurg. 1988;68:985–6.
7.
Zurück zum Zitat Kothari RU, Brott T, Broderick JP, et al. The ABCs of measuring intracerebral hemorrhage volumes. Stroke. 1996;27:1304–5.CrossRefPubMed Kothari RU, Brott T, Broderick JP, et al. The ABCs of measuring intracerebral hemorrhage volumes. Stroke. 1996;27:1304–5.CrossRefPubMed
8.
Zurück zum Zitat Vergouwen MD, Vermeulen M, van Gijn J, et al. Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies: proposal of a multidisciplinary research group. Stroke. 2010;41:2391–5.CrossRefPubMed Vergouwen MD, Vermeulen M, van Gijn J, et al. Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies: proposal of a multidisciplinary research group. Stroke. 2010;41:2391–5.CrossRefPubMed
9.
Zurück zum Zitat de Oliveira Manoel AL, Turkel-Parrella D, Duggal A, Murphy A, McCredie V, et al. Managing aneurysmal subarachnoid hemorrhage: it takes a team. Clevel Clin J Med. 2015;82:177–92. de Oliveira Manoel AL, Turkel-Parrella D, Duggal A, Murphy A, McCredie V, et al. Managing aneurysmal subarachnoid hemorrhage: it takes a team. Clevel Clin J Med. 2015;82:177–92.
10.
Zurück zum Zitat Macdonald RL. Delayed neurological deterioration after subarachnoid haemorrhage. Nat Publ Group. 2013;10:44–58. Macdonald RL. Delayed neurological deterioration after subarachnoid haemorrhage. Nat Publ Group. 2013;10:44–58.
11.
Zurück zum Zitat de Oliveira Manoel AL, Goffi A, Marotta TR, Schweizer TA, Abrahamson S, Macdonald RL. The critical care management of poor-grade subarachnoid haemorrhage. Crit Care. 2016;20:21.CrossRefPubMedPubMedCentral de Oliveira Manoel AL, Goffi A, Marotta TR, Schweizer TA, Abrahamson S, Macdonald RL. The critical care management of poor-grade subarachnoid haemorrhage. Crit Care. 2016;20:21.CrossRefPubMedPubMedCentral
12.
Zurück zum Zitat Diringer MN, Bleck TP, Claude Hemphill J, et al. Critical care management of patients following aneurysmal subarachnoid hemorrhage: recommendations from the neurocritical care society’s multidisciplinary consensus conference. Neurocrit Care. 2011;15:211–40.CrossRefPubMed Diringer MN, Bleck TP, Claude Hemphill J, et al. Critical care management of patients following aneurysmal subarachnoid hemorrhage: recommendations from the neurocritical care society’s multidisciplinary consensus conference. Neurocrit Care. 2011;15:211–40.CrossRefPubMed
13.
Zurück zum Zitat Connolly ES Jr, Rabinstein AA, Carhuapoma JR, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2012;43:1711–37.CrossRefPubMed Connolly ES Jr, Rabinstein AA, Carhuapoma JR, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2012;43:1711–37.CrossRefPubMed
14.
Zurück zum Zitat Molyneux AJ, Kerr RS, Yu L-M, et al. 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. 2005;366:809–17.CrossRefPubMed Molyneux AJ, Kerr RS, Yu L-M, et al. 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. 2005;366:809–17.CrossRefPubMed
15.
Zurück zum Zitat Campi A, Ramzi N, Molyneux AJ, et al. Retreatment of ruptured cerebral aneurysms in patients randomized by coiling or clipping in the international subarachnoid aneurysm trial (ISAT). Stroke. 2007;38:1538–44.CrossRefPubMed Campi A, Ramzi N, Molyneux AJ, et al. Retreatment of ruptured cerebral aneurysms in patients randomized by coiling or clipping in the international subarachnoid aneurysm trial (ISAT). Stroke. 2007;38:1538–44.CrossRefPubMed
16.
Zurück zum Zitat van Amerongen MJ, Boogaarts HD, de Vries J, et al. MRA versus DSA for follow-up of coiled intracranial aneurysms: a meta-analysis. AJNR. 2014;35:1655–61.CrossRefPubMed van Amerongen MJ, Boogaarts HD, de Vries J, et al. MRA versus DSA for follow-up of coiled intracranial aneurysms: a meta-analysis. AJNR. 2014;35:1655–61.CrossRefPubMed
17.
18.
Zurück zum Zitat Bruno A, Shah N, Lin C, et al. Improving modified Rankin Scale assessment with a simplified Questionnaire. Stroke. 2010;41:1048–50.CrossRefPubMed Bruno A, Shah N, Lin C, et al. Improving modified Rankin Scale assessment with a simplified Questionnaire. Stroke. 2010;41:1048–50.CrossRefPubMed
19.
Zurück zum Zitat Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg. 2010;8:336–41.CrossRefPubMed Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg. 2010;8:336–41.CrossRefPubMed
20.
Zurück zum Zitat Wilby MJ, Sharp M, Whitfield PC, Hutchinson PJ, Menon DK, Kirkpatrick PJ. Cost-effective outcome for treating poor-grade subarachnoid hemorrhage. Stroke. 2003;34:2508–11.CrossRefPubMed Wilby MJ, Sharp M, Whitfield PC, Hutchinson PJ, Menon DK, Kirkpatrick PJ. Cost-effective outcome for treating poor-grade subarachnoid hemorrhage. Stroke. 2003;34:2508–11.CrossRefPubMed
21.
Zurück zum Zitat Jennett B, Bond M. Assessment of outcome after severe brain damage: a practical scale. Lancet. 1975;305:480–4.CrossRef Jennett B, Bond M. Assessment of outcome after severe brain damage: a practical scale. Lancet. 1975;305:480–4.CrossRef
22.
Zurück zum Zitat Teasdale GM, Pettigrew L. Analyzing outcome of treatment of severe head injury: a review and update on advancing the use of the Glasgow Outcome Scale. J Neurotrauma. 1998;15:587–97.CrossRefPubMed Teasdale GM, Pettigrew L. Analyzing outcome of treatment of severe head injury: a review and update on advancing the use of the Glasgow Outcome Scale. J Neurotrauma. 1998;15:587–97.CrossRefPubMed
23.
Zurück zum Zitat Wilson JT, Hareendran A, Grant M, et al. Improving the assessment of outcomes in stroke: use of a structured interview to assign grades on the modified Rankin Scale. Stroke. 2002;33:2243–6.CrossRefPubMed Wilson JT, Hareendran A, Grant M, et al. Improving the assessment of outcomes in stroke: use of a structured interview to assign grades on the modified Rankin Scale. Stroke. 2002;33:2243–6.CrossRefPubMed
24.
Zurück zum Zitat van den Berg R, Foumani M, Schröder RD, et al. Predictors of outcome in World Federation of Neurologic Surgeons grade V aneurysmal subarachnoid hemorrhage patients. Crit Care Med. 2011;39:1–2727. van den Berg R, Foumani M, Schröder RD, et al. Predictors of outcome in World Federation of Neurologic Surgeons grade V aneurysmal subarachnoid hemorrhage patients. Crit Care Med. 2011;39:1–2727.
25.
Zurück zum Zitat Chyatte D, Fode NC, Sundt TM. Early versus late intracranial aneurysm surgery in subarachnoid hemorrhage. J Neurosurg. 1988;69:326–31.CrossRefPubMed Chyatte D, Fode NC, Sundt TM. Early versus late intracranial aneurysm surgery in subarachnoid hemorrhage. J Neurosurg. 1988;69:326–31.CrossRefPubMed
26.
Zurück zum Zitat Bailes JE, Spetzler RF, Hadley MN, Baldwin HZ. Management morbidity and mortality of poor-grade aneurysm patients. J Neurosurg. 1990;72:559–66.CrossRefPubMed Bailes JE, Spetzler RF, Hadley MN, Baldwin HZ. Management morbidity and mortality of poor-grade aneurysm patients. J Neurosurg. 1990;72:559–66.CrossRefPubMed
27.
Zurück zum Zitat Lee KC, Huh SK, Park HS, Shin YS, Lee KS. Management of poor-grade patients with ruptured intracranial aneurysm. Keio J Med. 1997;46:69–73.CrossRefPubMed Lee KC, Huh SK, Park HS, Shin YS, Lee KS. Management of poor-grade patients with ruptured intracranial aneurysm. Keio J Med. 1997;46:69–73.CrossRefPubMed
28.
Zurück zum Zitat Rordorf GG, Ogilvy CSC, Gress DRD, Crowell RMR, Choi ISI. Patients in poor neurological condition after subarachnoid hemorrhage: early management and long-term outcome. Acta Neurochir. 1997;139:1143–51.CrossRefPubMed Rordorf GG, Ogilvy CSC, Gress DRD, Crowell RMR, Choi ISI. Patients in poor neurological condition after subarachnoid hemorrhage: early management and long-term outcome. Acta Neurochir. 1997;139:1143–51.CrossRefPubMed
29.
Zurück zum Zitat Starke RM, Komotar RJ, Otten ML, et al. Predicting long-term outcome in poor grade aneurysmal subarachnoid haemorrhage patients utilising the Glasgow Coma Scale. J Clin Neurosci. 2009;16:26–31.CrossRefPubMed Starke RM, Komotar RJ, Otten ML, et al. Predicting long-term outcome in poor grade aneurysmal subarachnoid haemorrhage patients utilising the Glasgow Coma Scale. J Clin Neurosci. 2009;16:26–31.CrossRefPubMed
30.
Zurück zum Zitat Schuss P, Hadjiathanasiou A, Borger V, Wispel C, Vatter H, Güresir E. Poor-grade aneurysmal subarachnoid hemorrhage: factors influencing functional outcome—a single-center series. World Neurosurg. 2016;85:125–9.CrossRefPubMed Schuss P, Hadjiathanasiou A, Borger V, Wispel C, Vatter H, Güresir E. Poor-grade aneurysmal subarachnoid hemorrhage: factors influencing functional outcome—a single-center series. World Neurosurg. 2016;85:125–9.CrossRefPubMed
31.
Zurück zum Zitat Ross J, O’Sullivan MG, Grant IS, Sellar R, Whittle IR. Impact of early endovascular aneurysmal occlusion on outcome of patients in poor grade after subarachnoid haemorrhage: a prospective, consecutive study. J Clin Neurosci. 2002;9:648–52.CrossRefPubMed Ross J, O’Sullivan MG, Grant IS, Sellar R, Whittle IR. Impact of early endovascular aneurysmal occlusion on outcome of patients in poor grade after subarachnoid haemorrhage: a prospective, consecutive study. J Clin Neurosci. 2002;9:648–52.CrossRefPubMed
32.
Zurück zum Zitat Vergouwen M, Jong-Tjien-Fa AV, Algra A. Time trends in causes of death after aneurysmal subarachnoid hemorrhage: a hospital-based study. Neurology. 2016;86:59–63.CrossRefPubMed Vergouwen M, Jong-Tjien-Fa AV, Algra A. Time trends in causes of death after aneurysmal subarachnoid hemorrhage: a hospital-based study. Neurology. 2016;86:59–63.CrossRefPubMed
33.
Zurück zum Zitat Ameen AA, Illingworth R. Anti-fibrinolytic treatment in the pre-operative management of subarachnoid haemorrhage caused by ruptured intracranial aneurysm. J Neurol Neurosurg Psychiatry. 1981;44:220–6.CrossRefPubMedPubMedCentral Ameen AA, Illingworth R. Anti-fibrinolytic treatment in the pre-operative management of subarachnoid haemorrhage caused by ruptured intracranial aneurysm. J Neurol Neurosurg Psychiatry. 1981;44:220–6.CrossRefPubMedPubMedCentral
34.
Zurück zum Zitat Mitra D, Gregson B, Jayakrishnan V, et al. Treatment of poor-grade subarachnoid hemorrhage trial. AJNR. 2015;36:116–20.CrossRefPubMed Mitra D, Gregson B, Jayakrishnan V, et al. Treatment of poor-grade subarachnoid hemorrhage trial. AJNR. 2015;36:116–20.CrossRefPubMed
35.
Zurück zum Zitat Oudshoorn SC, Rinkel GJE, Molyneux AJ, et al. Aneurysm treatment <24 versus 24–72 h after subarachnoid hemorrhage. Neurocrit Care. 2014;21:4–13.CrossRefPubMed Oudshoorn SC, Rinkel GJE, Molyneux AJ, et al. Aneurysm treatment <24 versus 24–72 h after subarachnoid hemorrhage. Neurocrit Care. 2014;21:4–13.CrossRefPubMed
36.
Zurück zum Zitat Nieuwkamp DJ, Setz LE, Algra A, Linn FH, de Rooij NK, Rinkel GJ. Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. Lancet Neurol. 2009;8:635–42.CrossRefPubMed Nieuwkamp DJ, Setz LE, Algra A, Linn FH, de Rooij NK, Rinkel GJ. Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. Lancet Neurol. 2009;8:635–42.CrossRefPubMed
37.
Zurück zum Zitat Hop JW, Rinkel GJ, Algra A, van Gijn J. Case-fatality rates and functional outcome after subarachnoid hemorrhage: a systematic review. Stroke. 1997;28:660–4.CrossRefPubMed Hop JW, Rinkel GJ, Algra A, van Gijn J. Case-fatality rates and functional outcome after subarachnoid hemorrhage: a systematic review. Stroke. 1997;28:660–4.CrossRefPubMed
38.
Zurück zum Zitat Hijdra A, Braakman R, van Gijn J, Vermeulen M, van Crevel H. Aneurysmal subarachnoid hemorrhage. Complications and outcome in a hospital population. Stroke. 1987;18:1061–7.CrossRefPubMed Hijdra A, Braakman R, van Gijn J, Vermeulen M, van Crevel H. Aneurysmal subarachnoid hemorrhage. Complications and outcome in a hospital population. Stroke. 1987;18:1061–7.CrossRefPubMed
39.
Zurück zum Zitat Petruk KC, West M, Mohr G, et al. Nimodipine treatment in poor-grade aneurysm patients. Results of a multicenter double-blind placebo-controlled trial. J Neurosurg. 1988;68:505–17.CrossRefPubMed Petruk KC, West M, Mohr G, et al. Nimodipine treatment in poor-grade aneurysm patients. Results of a multicenter double-blind placebo-controlled trial. J Neurosurg. 1988;68:505–17.CrossRefPubMed
40.
Zurück zum Zitat Pickard JD, Murray GD, Illingworth R, et al. Effect of oral nimodipine on cerebral infarction and outcome after subarachnoid haemorrhage: British aneurysm nimodipine trial. BMJ. 1989;298:636–42.CrossRefPubMedPubMedCentral Pickard JD, Murray GD, Illingworth R, et al. Effect of oral nimodipine on cerebral infarction and outcome after subarachnoid haemorrhage: British aneurysm nimodipine trial. BMJ. 1989;298:636–42.CrossRefPubMedPubMedCentral
41.
Zurück zum Zitat Molyneux AA, Kerr RR, Stratton II, et al. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet. 2002;360:1267–74.CrossRefPubMed Molyneux AA, Kerr RR, Stratton II, et al. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet. 2002;360:1267–74.CrossRefPubMed
42.
Zurück zum Zitat Kramer AH, Zygun DA. Do neurocritical care units save lives? Measuring the impact of specialized ICUs. Neurocrit Care. 2011;14:329–33.CrossRefPubMed Kramer AH, Zygun DA. Do neurocritical care units save lives? Measuring the impact of specialized ICUs. Neurocrit Care. 2011;14:329–33.CrossRefPubMed
43.
Zurück zum Zitat Guglielmi G, Viñuela F, Dion J, Duckwiler G. Electrothrombosis of saccular aneurysms via endovascular approach. Part 2: preliminary clinical experience. J Neurosurg. 1991;75:8–14.CrossRefPubMed Guglielmi G, Viñuela F, Dion J, Duckwiler G. Electrothrombosis of saccular aneurysms via endovascular approach. Part 2: preliminary clinical experience. J Neurosurg. 1991;75:8–14.CrossRefPubMed
44.
Zurück zum Zitat Kowalski RG, Claassen J, Kreiter KT, et al. Initial misdiagnosis and outcome after subarachnoid hemorrhage. JAMA. 2004;291:866–9.CrossRefPubMed Kowalski RG, Claassen J, Kreiter KT, et al. Initial misdiagnosis and outcome after subarachnoid hemorrhage. JAMA. 2004;291:866–9.CrossRefPubMed
45.
Zurück zum Zitat Perry JJ, Stiell IG, Sivilotti MLA, et al. Sensitivity of computed tomography performed within 6 h of onset of headache for diagnosis of subarachnoid haemorrhage: prospective cohort study. BMJ. 2011;343:d4277.CrossRefPubMedPubMedCentral Perry JJ, Stiell IG, Sivilotti MLA, et al. Sensitivity of computed tomography performed within 6 h of onset of headache for diagnosis of subarachnoid haemorrhage: prospective cohort study. BMJ. 2011;343:d4277.CrossRefPubMedPubMedCentral
46.
Zurück zum Zitat Kimball MM, Velat GJ, Hoh BL. Participants in the international multi-disciplinary consensus conference on the critical care management of subarachnoid hemorrhage. Critical care guidelines on the endovascular management of cerebral vasospasm. Neurocrit Care. 2011;15:336–41.CrossRefPubMed Kimball MM, Velat GJ, Hoh BL. Participants in the international multi-disciplinary consensus conference on the critical care management of subarachnoid hemorrhage. Critical care guidelines on the endovascular management of cerebral vasospasm. Neurocrit Care. 2011;15:336–41.CrossRefPubMed
47.
Zurück zum Zitat Yasargil MG, Fox JL. The microsurgical approach to intracranial aneurysms. Surg Neurol. 1975;3:7–14.PubMed Yasargil MG, Fox JL. The microsurgical approach to intracranial aneurysms. Surg Neurol. 1975;3:7–14.PubMed
48.
Zurück zum Zitat Molyneux AJ, Birks J, Clarke A, Sneade M, Kerr RSC. The durability of endovascular coiling versus neurosurgical clipping of ruptured cerebral aneurysms: 18 year follow-up of the UK cohort of the International subarachnoid aneurysm trial (ISAT). Lancet. 2015;385:691–7.CrossRefPubMedPubMedCentral Molyneux AJ, Birks J, Clarke A, Sneade M, Kerr RSC. The durability of endovascular coiling versus neurosurgical clipping of ruptured cerebral aneurysms: 18 year follow-up of the UK cohort of the International subarachnoid aneurysm trial (ISAT). Lancet. 2015;385:691–7.CrossRefPubMedPubMedCentral
49.
Zurück zum Zitat Ohman J, Heiskanen O. Timing of operation for ruptured supratentorial aneurysms: a prospective randomized study. J Neurosurg. 1989;70:55–60.CrossRefPubMed Ohman J, Heiskanen O. Timing of operation for ruptured supratentorial aneurysms: a prospective randomized study. J Neurosurg. 1989;70:55–60.CrossRefPubMed
50.
Zurück zum Zitat Steiner T, Juvela S, Unterberg A, Jung C, Forsting M, Rinkel G. European stroke organization guidelines for the management of intracranial aneurysms and subarachnoid haemorrhage. Cerebrovasc Dis. 2013;35:93–112.CrossRefPubMed Steiner T, Juvela S, Unterberg A, Jung C, Forsting M, Rinkel G. European stroke organization guidelines for the management of intracranial aneurysms and subarachnoid haemorrhage. Cerebrovasc Dis. 2013;35:93–112.CrossRefPubMed
51.
Zurück zum Zitat McNeill L, English SW, Borg N, Matta BF, Menon DK. Effects of institutional caseload of subarachnoid hemorrhage on mortality: a secondary analysis of administrative data. Stroke. 2013;44(3):647–52.CrossRefPubMed McNeill L, English SW, Borg N, Matta BF, Menon DK. Effects of institutional caseload of subarachnoid hemorrhage on mortality: a secondary analysis of administrative data. Stroke. 2013;44(3):647–52.CrossRefPubMed
52.
Zurück zum Zitat Cross DTD, Tirschwell DLD, Clark MAM, et al. Mortality rates after subarachnoid hemorrhage: variations according to hospital case volume in 18 states. J Neurosurg. 2003;99(5):810–7.CrossRefPubMed Cross DTD, Tirschwell DLD, Clark MAM, et al. Mortality rates after subarachnoid hemorrhage: variations according to hospital case volume in 18 states. J Neurosurg. 2003;99(5):810–7.CrossRefPubMed
53.
Zurück zum Zitat Bardach NS, Olson SJ, Elkins JS, Smith WS, Lawton MT, Johnston SC. Regionalization of treatment for subarachnoid hemorrhage: a cost-utility analysis. Circulation. 2004;109:2207–12.CrossRefPubMed Bardach NS, Olson SJ, Elkins JS, Smith WS, Lawton MT, Johnston SC. Regionalization of treatment for subarachnoid hemorrhage: a cost-utility analysis. Circulation. 2004;109:2207–12.CrossRefPubMed
54.
Zurück zum Zitat Quigley MR, Salary M. Defining survivorship after high-grade aneurysmal subarachnoid hemorrhage. Surg Neurol. 2008;69:261–5.CrossRefPubMed Quigley MR, Salary M. Defining survivorship after high-grade aneurysmal subarachnoid hemorrhage. Surg Neurol. 2008;69:261–5.CrossRefPubMed
55.
Zurück zum Zitat Barcelos GK, Tholance Y, Grousson S, et al. Outcome of poor-grade subarachnoid hemorrhage as determined by biomarkers of glucose cerebral metabolism. Neurocrit Care. 2013;18:234–44.CrossRefPubMed Barcelos GK, Tholance Y, Grousson S, et al. Outcome of poor-grade subarachnoid hemorrhage as determined by biomarkers of glucose cerebral metabolism. Neurocrit Care. 2013;18:234–44.CrossRefPubMed
56.
Zurück zum Zitat Taylor B, Harries P, Bullock R. Factors affecting outcome after surgery for intracranial aneurysm in Glasgow. Br J Neurosurg. 1991;5:591–600.CrossRefPubMed Taylor B, Harries P, Bullock R. Factors affecting outcome after surgery for intracranial aneurysm in Glasgow. Br J Neurosurg. 1991;5:591–600.CrossRefPubMed
57.
Zurück zum Zitat Ransom ER, Mocco J, Komotar RJ, et al. External ventricular drainage response in poor grade aneurysmal subarachnoid hemorrhage: effect on preoperative grading and prognosis. Neurocrit Care. 2007;6:174–80.CrossRefPubMed Ransom ER, Mocco J, Komotar RJ, et al. External ventricular drainage response in poor grade aneurysmal subarachnoid hemorrhage: effect on preoperative grading and prognosis. Neurocrit Care. 2007;6:174–80.CrossRefPubMed
58.
Zurück zum Zitat Rosen DS, Macdonald RL. Subarachnoid hemorrhage grading scales: a systematic review. Neurocrit Care. 2005;2:110–8.CrossRefPubMed Rosen DS, Macdonald RL. Subarachnoid hemorrhage grading scales: a systematic review. Neurocrit Care. 2005;2:110–8.CrossRefPubMed
59.
Zurück zum Zitat Fung C, Inglin F, Murek M, et al. Reconsidering the logic of World Federation of Neurosurgical Societies grading in patients with severe subarachnoid hemorrhage. J Neurosurg. 2016;124:299–304.CrossRefPubMed Fung C, Inglin F, Murek M, et al. Reconsidering the logic of World Federation of Neurosurgical Societies grading in patients with severe subarachnoid hemorrhage. J Neurosurg. 2016;124:299–304.CrossRefPubMed
60.
Zurück zum Zitat Al-Khindi T, Macdonald RL, Schweizer TA. Cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Stroke. 2010;41:e519–36.CrossRefPubMed Al-Khindi T, Macdonald RL, Schweizer TA. Cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Stroke. 2010;41:e519–36.CrossRefPubMed
61.
Zurück zum Zitat Ohno K, Suzuki R, Masaoka H, Monma S, Matsushima Y, Inaba Y. A review of 102 consecutive patients with intracranial aneurysms in a community hospital in Japan. Acta Neurochir. 1988;94:23–7.CrossRefPubMed Ohno K, Suzuki R, Masaoka H, Monma S, Matsushima Y, Inaba Y. A review of 102 consecutive patients with intracranial aneurysms in a community hospital in Japan. Acta Neurochir. 1988;94:23–7.CrossRefPubMed
62.
Zurück zum Zitat Inagawa T, Takahashi M, Aoki H, Ishikawa S, Yoshimoto H. Aneurysmal subarachnoid hemorrhage in Izumo City and Shimane Prefecture of Japan. Outcome Stroke. 1988;19:176–80.CrossRefPubMed Inagawa T, Takahashi M, Aoki H, Ishikawa S, Yoshimoto H. Aneurysmal subarachnoid hemorrhage in Izumo City and Shimane Prefecture of Japan. Outcome Stroke. 1988;19:176–80.CrossRefPubMed
63.
Zurück zum Zitat Seifert V, Trost HA, Stolke D. Management morbidity and mortality in grade IV and V patients with aneurysmal subarachnoid haemorrhage. Acta Neurochir. 1990;103:5–10.CrossRefPubMed Seifert V, Trost HA, Stolke D. Management morbidity and mortality in grade IV and V patients with aneurysmal subarachnoid haemorrhage. Acta Neurochir. 1990;103:5–10.CrossRefPubMed
64.
Zurück zum Zitat Nowak G, Schwachenwald R, Arnold H. Early management in poor grade aneurysm patients. Acta Neurochir. 1994;126:33–7.CrossRefPubMed Nowak G, Schwachenwald R, Arnold H. Early management in poor grade aneurysm patients. Acta Neurochir. 1994;126:33–7.CrossRefPubMed
65.
Zurück zum Zitat Alberti O, Becker R, Benes L, Wallenfang T, Bertalanffy H. Initial hyperglycemia as an indicator of severity of the ictus in poor-grade patients with spontaneous subarachnoid hemorrhage. Clin Neurol Neurosurg. 2000;102:78–83.CrossRefPubMed Alberti O, Becker R, Benes L, Wallenfang T, Bertalanffy H. Initial hyperglycemia as an indicator of severity of the ictus in poor-grade patients with spontaneous subarachnoid hemorrhage. Clin Neurol Neurosurg. 2000;102:78–83.CrossRefPubMed
66.
Zurück zum Zitat Inamasu J, Nakamura Y, Saito R, Kuroshima Y, Mayanagi K, Ichikizaki K. Endovascular treatment for poorest-grade subarachnoid hemorrhage in the acute stage: Has the outcome been improved? Neurosurgery. 2002;50:1199–1205 (discussion 205–6). Inamasu J, Nakamura Y, Saito R, Kuroshima Y, Mayanagi K, Ichikizaki K. Endovascular treatment for poorest-grade subarachnoid hemorrhage in the acute stage: Has the outcome been improved? Neurosurgery. 2002;50:1199–1205 (discussion 205–6).
67.
Zurück zum Zitat Ritz R, Schwerdtfeger K, Strowitzki M, Donauer E, Koenig J, Steudel W-I. Prognostic value of SSEP in early aneurysm surgery after SAH in poor-grade patients. Neurol Res. 2002;24:756–64.CrossRefPubMed Ritz R, Schwerdtfeger K, Strowitzki M, Donauer E, Koenig J, Steudel W-I. Prognostic value of SSEP in early aneurysm surgery after SAH in poor-grade patients. Neurol Res. 2002;24:756–64.CrossRefPubMed
68.
Zurück zum Zitat Laidlaw JD, Siu KH. Poor-grade aneurysmal subarachnoid hemorrhage: outcome after treatment with urgent surgery. Neurosurgery. 2003;53:1275–1280 (discussion 1280–2). Laidlaw JD, Siu KH. Poor-grade aneurysmal subarachnoid hemorrhage: outcome after treatment with urgent surgery. Neurosurgery. 2003;53:1275–1280 (discussion 1280–2).
Metadaten
Titel
Functional Outcome After Poor-Grade Subarachnoid Hemorrhage: A Single-Center Study and Systematic Literature Review
verfasst von
Airton Leonardo de Oliveira Manoel
Ann Mansur
Gisele Sampaio Silva
Menno R. Germans
Blessing N. R. Jaja
Ekaterina Kouzmina
Thomas R. Marotta
Simon Abrahamson
Tom A. Schweizer
Julian Spears
R. Loch Macdonald
Publikationsdatum
20.09.2016
Verlag
Springer US
Erschienen in
Neurocritical Care / Ausgabe 3/2016
Print ISSN: 1541-6933
Elektronische ISSN: 1556-0961
DOI
https://doi.org/10.1007/s12028-016-0305-3

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