Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
BMC Neurology
Published in: BMC Neurology 1/2022

Open Access 01-12-2022 | Intracranial Aneurysm | Research

Early predictors of functional outcome in poor-grade aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis

Authors: Jordi de Winkel, Tim Y. Cras, Ruben Dammers, Pieter-Jan van Doormaal, Mathieu van der Jagt, Diederik W. J. Dippel, Hester F. Lingsma, Bob Roozenbeek

Published in: BMC Neurology | Issue 1/2022

Login to get access

Abstract

Background

Patients with poor-grade aneurysmal subarachnoid hemorrhage (aSAH) often receive delayed or no aneurysm treatment, although recent studies suggest that functional outcome following early aneurysm treatment has improved. We aimed to systematically review and meta-analyze early predictors of functional outcome in poor-grade aSAH patients. 

Methods

We included studies investigating the association of early predictors and functional outcome in adult patients with confirmed poor-grade aSAH, defined as World Federation of Neurological Surgeons (WFNS) grade or Hunt and Hess (H–H) grade IV-V. Studies had to use multivariable regression analysis to estimate independent predictor effects of favorable functional outcome measured with the Glasgow Outcome Scale or modified Rankin Scale. We calculated pooled adjusted odds ratios (aOR) and 95% confidence intervals (CI) with random effects models. 

Results

We included 27 studies with 3287 patients. The likelihood of favorable outcome increased with WFNS grade or H–H grade IV versus V (aOR 2.9, 95% CI 1.9–4.3), presence of clinical improvement before aneurysm treatment (aOR 3.3, 95% CI 2.0–5.3), and intact pupillary light reflex (aOR 2.9, 95% CI 1.6–5.1), and decreased with older age (aOR 0.7, 95% CI 0.5–1.0, per decade), increasing modified Fisher grade (aOR 0.4, 95% CI 0.3–0.5, per grade), and presence of intracerebral hematoma on admission imaging (aOR 0.4, 95% CI 0.2–0.8).

Conclusions

We present a summary of early predictors of functional outcome in poor-grade aSAH patients that can help to discriminate between patients with favorable and with unfavorable prognosis and may aid in selecting patients for early aneurysm treatment.
Appendix
Available only for authorised users
Literature
1.
Rinkel GJ, Algra A. Long-term outcomes of patients with aneurysmal subarachnoid haemorrhage. Lancet Neurol. 2011;10(4):349–56.PubMedCrossRef
2.
3.
Han Y, Ye F, Long X, Li A, Xu H, Zou L, et al. Ultra-Early Treatment for Poor-Grade Aneurysmal Subarachnoid Hemorrhage: A Systematic Review and Meta-Analysis. World Neurosurg. 2018;115:e160–71.PubMedCrossRef
4.
Connolly ES Jr, Rabinstein AA, Carhuapoma JR, Derdeyn CP, Dion J, Higashida RT, 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(6):1711–37.PubMedCrossRef
5.
Steiner T, Juvela S, Unterberg A, Jung C, Forsting M, Rinkel G, et al. European Stroke Organization guidelines for the management of intracranial aneurysms and subarachnoid haemorrhage. Cerebrovasc Dis. 2013;35(2):93–112.PubMedCrossRef
6.
de Winkel J, van der Jagt M, Lingsma HF, Roozenbeek B, Calvillo E, Chou SH, et al. International Practice Variability in Treatment of Aneurysmal Subarachnoid Hemorrhage. J Clin Med. 2021;10(4):762.PubMedPubMedCentralCrossRef
7.
Germans MR, Coert BA, Vandertop WP, Verbaan D. Time intervals from subarachnoid hemorrhage to rebleed. J Neurol. 2014;261(7):1425–31.PubMedCrossRef
8.
Park J, Woo H, Kang DH, Kim YS, Kim MY, Shin IH, et al. Formal protocol for emergency treatment of ruptured intracranial aneurysms to reduce in-hospital rebleeding and improve clinical outcomes. J Neurosurg. 2015;122(2):383–91.PubMedCrossRef
9.
Rawal S, Alcaide-Leon P, Macdonald RL, Rinkel GJ, Victor JC, Krings T, et al. Meta-analysis of timing of endovascular aneurysm treatment in subarachnoid haemorrhage: inconsistent results of early treatment within 1 day. J Neurol Neurosurg Psychiatry. 2017;88(3):241–8.PubMedCrossRef
10.
Oudshoorn SC, Rinkel GJ, Molyneux AJ, Kerr RS, Dorhout Mees SM, Backes D, et al. Aneurysm treatment <24 versus 24–72 h after subarachnoid hemorrhage. Neurocrit Care. 2014;21(1):4–13.PubMedCrossRef
11.
Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol. 2009;62(10):1006–12.PubMedCrossRef
12.
Hayden JA, van der Windt DA, Cartwright JL, Cote P, Bombardier C. Assessing bias in studies of prognostic factors. Ann Intern Med. 2013;158(4):280–6.PubMedCrossRef
13.
McGuinness LA, Higgins JPT. Risk-of-bias VISualization (robvis): An R package and Shiny web app for visualizing risk-of-bias assessments. Res Synth Methods. 2021;12(1):55–61.PubMedCrossRef
14.
Mocco J, Ransom ER, Komotar RJ, Schmidt JM, Sciacca RR, Mayer SA, et al. Preoperative prediction of long-term outcome in poor-grade aneurysmal subarachnoid hemorrhage. Neurosurgery. 2006;59(3):529–38 discussion -38.PubMedCrossRef
15.
Starke RM, Komotar RJ, Kim GH, Kellner CP, Otten ML, Hahn DK, et al. Evaluation of a revised Glasgow Coma Score scale in predicting long-term outcome of poor grade aneurysmal subarachnoid hemorrhage patients. J Clin Neurosci. 2009;16(7):894–9.PubMedCrossRef
16.
Zhao B, Tan X, Zhao Y, Cao Y, Wu J, Zhong M, et al. Variation in Patient Characteristics and Outcomes Between Early and Delayed Surgery in Poor-Grade Aneurysmal Subarachnoid Hemorrhage. Neurosurgery. 2016;78(2):224–31.PubMedCrossRef
17.
Zhao B, Yang H, Zheng K, Li Z, Xiong Y, Tan X, et al. Preoperative and postoperative predictors of long-Term outcome after endovascular treatment of poor-grade aneurysmal subarachnoid hemorrhage. J Neurosurg. 2017;126(6):1764–71.PubMedCrossRef
18.
Zhao B, Zhao Y, Tan X, Cao Y, Wu J, Zhong M, et al. Factors and outcomes associated with ultra-early surgery for poor-grade aneurysmal subarachnoid haemorrhage: A multicentre retrospective analysis. BMJ Open. 2015;5(4):e007410.PubMedPubMedCentralCrossRef
19.
Zheng K, Zhao B, Tan XX, Li ZQ, Xiong Y, Zhong M, et al. Comparison of Aggressive Surgical Treatment and Palliative Treatment in Elderly Patients with Poor-Grade Intracranial Aneurysmal Subarachnoid Hemorrhage. BioMed Res Int. 2018;2018:5818937.PubMedPubMedCentral
20.
Zheng K, Zhong M, Zhao B, Chen SY, Tan XX, Li ZQ, et al. Poor-grade aneurysmal subarachnoid hemorrhage: Risk factors affecting clinical outcomes in intracranial aneurysm patients in a multi-center study. Front Neurol. 2019;10:123.PubMedPubMedCentralCrossRef
21.
Duval S, Tweedie R. Trim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics. 2000;56(2):455–63.PubMedCrossRef
22.
Anqi X, Ruiqi C, Yanming R, Chao Y. Elevated hemoglobin is associated with poor prognosis in Tibetans with poor-grade aneurysmal subarachnoid hemorrhage after clipping: A Retrospective Case-Control Study. Neurochirurgie. 2019;65(6):365–9.PubMedCrossRef
23.
Das KK, Singh S, Sharma P, Mehrotra A, Bhaisora K, Sardhara J, et al. Results of Proactive Surgical Clipping in Poor-Grade Aneurysmal Subarachnoid Hemorrhage: Pattern of Recovery and Predictors of Outcome. World Neurosurg. 2017;102:561–70.PubMedCrossRef
24.
Fukuda H, Hayashi K, Moriya T, Nakashita S, Lo BW, Yamagata S. Intrasylvian hematoma caused by ruptured middle cerebral artery aneurysms predicts recovery from poor-grade subarachnoid hemorrhage. J Neurosurg. 2015;123(3):686–92.PubMedCrossRef
25.
Hsieh PC, Wu YM, Wang AY, Chen CC, Chang CH, Chin SC, et al. The venous delay phenomenon in computed tomography angiography: a novel imaging outcome predictor for poor cerebral perfusion after severe aneurysmal subarachnoid hemorrhage. J Neurosurg. 2018;129(4):876–82.PubMedCrossRef
26.
Inamasu J, Nakae S, Ohmi T, Kogame H, Kawazoe Y, Kumai T, et al. The outcomes of early aneurysm repair in World Federation of Neurosurgical Societies grade V subarachnoid haemorrhage patients with emphasis on those presenting with a Glasgow Coma Scale score of 3. J Clin Neurosci. 2016;33:142–7.PubMedCrossRef
27.
Ironside N, Buell TJ, Chen CJ, Kumar JS, Paisan GM, Sokolowski JD, et al. High-Grade Aneurysmal Subarachnoid Hemorrhage: Predictors of Functional Outcome. World Neurosurg. 2019;125:e723–8.PubMedCrossRef
28.
Kaneko J, Tagami T, Unemoto K, Tanaka C, Kuwamoto K, Sato S, et al. Functional Outcome Following Ultra-Early Treatment for Ruptured Aneurysms in Patients with Poor-Grade Subarachnoid Hemorrhage. J Nippon Med Sch. 2019;86(2):81–90.PubMedCrossRef
29.
Konczalla J, Seifert V, Beck J, Guresir E, Vatter H, Raabe A, et al. Outcome after Hunt and Hess Grade V subarachnoid hemorrhage: a comparison of pre-coiling era (1980–1995) versus post-ISAT era (2005–2014). J Neurosurg. 2018;128(1):100–10.PubMedCrossRef
30.
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(1):39–49.PubMedCrossRef
31.
Liu J, Xiong Y, Zhong M, Yang Y, Guo X, Tan X, et al. Predicting Long-Term Outcomes After Poor-Grade Aneurysmal Subarachnoid Hemorrhage Using Decision Tree Modeling. Neurosurgery. 2020;87(3):523–9.PubMedCrossRef
32.
Panni P, Colombo E, Donofrio CA, Barzaghi LR, Albano L, Righi C, et al. Hemorrhagic burden in poor-grade aneurysmal subarachnoid hemorrhage: a volumetric analysis of different bleeding distributions. Acta Neurochir (Wien). 2019;161(4):791–7.CrossRef
33.
Ridwan S, Kristof R. Cardiac Arrest in Patients with Poor-Grade Aneurysmal Subarachnoid Hemorrhage: A Single-Center Experience. J Neurol Surg A Cent Eur Neurosurg. 2019;80(6):409–12.PubMedCrossRef
34.
Schuss P, Hadjiathanasiou A, Borger V, Wispel C. Poor-grade aneurysmal subarachnoid hemorrhage: factors influencing functional outcome—a single-center series. World neurosurgery. 2016;85:125–9.PubMedCrossRef
35.
Schwartz C, Pfefferkorn T, Ebrahimi C, Ottomeyer C, Fesl G, Bender A, et al. Long-term Neurological Outcome and Quality of Life after World Federation of Neurosurgical Societies Grades IV and V Aneurysmal Subarachnoid Hemorrhage in an Interdisciplinary Treatment Concept. Neurosurgery. 2017;80(6):967–74.PubMedCrossRef
36.
Shirao S, Yoneda H, Kunitsugu I, Ishihara H, Koizumi H, Suehiro E, et al. Preoperative prediction of outcome in 283 poor-grade patients with subarachnoid hemorrhage: a project of the Chugoku-Shikoku Division of the Japan Neurosurgical Society. Cerebrovasc Dis. 2010;30(2):105–13.PubMedCrossRef
37.
Szklener S, Melges A, Korchut A, Zaluska W, Trojanowski T, Rejdak R, et al. Predictive model for patients with poor-grade subarachnoid haemorrhage in 30-day observation: a 9-year cohort study. BMJ Open. 2015;5(6):e007795.PubMedPubMedCentralCrossRef
38.
Tsuang FY, Chen JY, Lee CW, Li CH, Lee JE, Lai DM, et al. Risk profile of patients with poor-grade aneurysmal subarachnoid hemorrhage using early perfusion computed tomography. World Neurosurg. 2012;78(5):455–61.PubMedCrossRef
39.
van den Berg R, Foumani M, Schroder RD, Peerdeman SM, Horn J, Bipat S, et al. Predictors of outcome in World Federation of Neurologic Surgeons grade V aneurysmal subarachnoid hemorrhage patients. Crit Care Med. 2011;39(12):2722–7.PubMedCrossRef
40.
Wang X, Han C, Xing D, Wang C, Ding X. Early management of poor-grade aneurysmal subarachnoid hemorrhage: A prognostic analysis of 104 patients. Clin Neurol Neurosurg. 2019;179:4–8.PubMedCrossRef
41.
Wostrack M, Sandow N, Vajkoczy P, Schatlo B, Bijlenga P, Schaller K, et al. Subarachnoid haemorrhage WFNS grade V: is maximal treatment worthwhile? Acta Neurochir (Wien). 2013;155(4):579–86.CrossRef
42.
Jaja BN, Cusimano MD, Etminan N, Hanggi D, Hasan D, Ilodigwe D, et al. Clinical prediction models for aneurysmal subarachnoid hemorrhage: a systematic review. Neurocrit Care. 2013;18(1):143–53.PubMedCrossRef
43.
Jaja BNR, Saposnik G, Lingsma HF, Macdonald E, Thorpe KE, Mamdani M, et al. Development and validation of outcome prediction models for aneurysmal subarachnoid haemorrhage: the SAHIT multinational cohort study. BMJ. 2018;360:j5745.PubMedCrossRef
44.
Lo BW, Fukuda H, Nishimura Y, Farrokhyar F, Thabane L, Levine MA. Systematic review of clinical prediction tools and prognostic factors in aneurysmal subarachnoid hemorrhage. Surg Neurol Int. 2015;6:135.PubMedPubMedCentralCrossRef
45.
Risselada R, Lingsma HF, Bauer-Mehren A, Friedrich CM, Molyneux AJ, Kerr RS, et al. Prediction of 60 day case-fatality after aneurysmal subarachnoid haemorrhage: results from the International Subarachnoid Aneurysm Trial (ISAT). Eur J Epidemiol. 2010;25(4):261–6.PubMedPubMedCentralCrossRef
46.
Risselada R, Lingsma HF, Molyneux AJ, Kerr RS, Yarnold J, Sneade M, et al. Prediction of two month modified Rankin Scale with an ordinal prediction model in patients with aneurysmal subarachnoid haemorrhage. BMC Med Res Methodol. 2010;10:86.PubMedPubMedCentralCrossRef
47.
Rosengart AJ, Schultheiss KE, Tolentino J, Macdonald RL. Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke. 2007;38(8):2315–21.PubMedCrossRef
48.
Stienen MN, Germans M, Burkhardt JK, Neidert MC, Fung C, Bervini D, et al. Predictors of In-Hospital Death After Aneurysmal Subarachnoid Hemorrhage: Analysis of a Nationwide Database (Swiss SOS [Swiss Study on Aneurysmal Subarachnoid Hemorrhage]). Stroke. 2018;49(2):333–40.PubMedCrossRef
49.
Giraldo EA, Mandrekar JN, Rubin MN, Dupont SA, Zhang Y, Lanzino G, et al. Timing of clinical grade assessment and poor outcome in patients with aneurysmal subarachnoid hemorrhage. J Neurosurg. 2012;117(1):15–9.PubMedCrossRef
50.
51.
Bijlenga P, Morita A, Ko NU, Mocco J, Morel S, Murayama Y, et al. Common Data Elements for Subarachnoid Hemorrhage and Unruptured Intracranial Aneurysms: Recommendations from the Working Group on Subject Characteristics. Neurocrit Care. 2019;30(Suppl 1):20–7.PubMedCrossRef
52.
Guresir E, Beck J, Vatter H, Setzer M, Gerlach R, Seifert V, et al. Subarachnoid hemorrhage and intracerebral hematoma: incidence, prognostic factors, and outcome. Neurosurgery. 2008;63(6):1088–93 discussion 93–4.PubMedCrossRef
53.
Kent DM, van Klaveren D, Paulus JK, D’Agostino R, Goodman S, Hayward R, et al. The Predictive Approaches to Treatment effect Heterogeneity (PATH) Statement: Explanation and Elaboration. Ann Intern Med. 2020;172(1):W1–25.PubMedCrossRef
Metadata
Title
Early predictors of functional outcome in poor-grade aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis
Authors
Jordi de Winkel
Tim Y. Cras
Ruben Dammers
Pieter-Jan van Doormaal
Mathieu van der Jagt
Diederik W. J. Dippel
Hester F. Lingsma
Bob Roozenbeek
Publication date
01-12-2022
Publisher
BioMed Central
Published in
BMC Neurology / Issue 1/2022
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/s12883-022-02734-x

Other articles of this Issue 1/2022

BMC Neurology 1/2022 Go to the issue

Research

3D slicer-based calculation of hematoma irregularity index for predicting hematoma expansion in intracerebral hemorrhage

Research

Impact of COVID-19 infection among myasthenia gravis patients- a Cerner Real-World DataTM study

Research

Results of a Web-based survey of 2105 Greek migraine patients in 2020: demographics, clinical characteristics, burden and the effects of the COVID-19 pandemic on the course of migraine

Case report

A novel TTR mutation (p.Ala65Val) underlying late-onset hereditary transthyretin (ATTRv) amyloidosis with mixed cardiac and neuropathic phenotype: a case report

Research

Does the 5–2-1 criteria identify patients with advanced Parkinson's disease? Real-world screening accuracy and burden of 5–2-1-positive patients in 7 countries

Case report

Autonomic dysfunction detected by skin sympathetic response in Lambert-Eaton myasthenic syndrome: a case report