Skip to main content

Advertisement

Log in

What are the predictors of delayed cerebral ischaemia (DCI) after aneurysmal subarachnoid haemorrhage? An up-to-date systematic review

  • Review Article
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Purpose

Delayed Cerebral Ischaemia (DCI) remains an important preventable driver of poor outcome in aneurysmal subarachnoid haemorrhage (aSAH). Our ability to predict DCI is based on historical patient cohorts, which use inconsistent definitions for DCI. In 2010, a definition of DCI was agreed upon and published by a group of aSAH experts. The aim of this study was to identify predictors using this agreed definition of DCI.

Methods

We conducted a literature search of Medline (PubMed) to identify articles published since the publication of the 2010 consensus definition. Risk factors and prediction models for DCI were included if they: (1) adjusted for confounding factors or were derived from randomised trials, (2) were derived from prospectively collected data and (3) included adults with aSAH. The strength of studies was assessed based on quality, risk of bias and applicability of studies using PROBAST.

Results

Eight studies totalling 4,542 patients were included from 105 relevant articles from 4,982 records. The most common reason for not including studies was failure to use the consensus definition of DCI (75%). No prediction models were identified in the eligible studies. Significant risk factors for DCI included the presence of onsite neuro-interventional services, high Neuropeptide Y, admission leucocytosis, neutrophil:lymphocyte >5.9 and Fisher Grade > 2. All studies had a high or unclear risk of bias.

Conclusions

Only a few studies with high risk of bias have investigated the predictors using consensus-defined DCI. Further studies are warranted to clarify risk factors of DCI in the modern era.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

The data which supports the conclusions of this study is available from the corresponding author, HCP, upon reasonable request.

References

  1. Al-Mufti F, Amuluru K, Damodara N, Dodson V, Roh D, Agarwal S et al (2019) Admission neutrophil–lymphocyte ratio predicts delayed cerebral ischemia following aneurysmal subarachnoid hemorrhage. J Neurointerv Surg 11(11):1135–1140

    Article  PubMed  Google Scholar 

  2. Carlson AP, Hänggi D, Wong GK, Etminan N, Mayer SA, Aldrich F et al (2020) Single-dose intraventricular nimodipine microparticles versus oral nimodipine for aneurysmal subarachnoid hemorrhage. Stroke. 51(4):1142–1149

    Article  CAS  PubMed  Google Scholar 

  3. Chen J, Li M, Zhu X, Chen L, Yang S, Zhang C et al (2020) Atorvastatin reduces cerebral vasospasm and infarction after aneurysmal subarachnoid hemorrhage in elderly Chinese adults. Aging (Albany NY) 12(3):2939

    Article  CAS  PubMed  Google Scholar 

  4. de Rooij NK, Rinkel GJ, Dankbaar JW, Frijns CJ (2013) Delayed cerebral ischemia after subarachnoid hemorrhage: a systematic review of clinical, laboratory, and radiological predictors. Stroke. 44(1):43–54

    Article  PubMed  Google Scholar 

  5. Dorhout Mees SM, Kerr RS, Rinkel GJ, Algra A, Molyneux AJ (2012) Occurrence and impact of delayed cerebral ischemia after coiling and after clipping in the International Subarachnoid Aneurysm Trial (ISAT). J Neurol 259:679–683

    Article  PubMed  Google Scholar 

  6. Dorhout Mees SM, Molyneux AJ, Kerr RS, Algra A, Rinkel GJ (2012) Timing of aneurysm treatment after subarachnoid hemorrhage: relationship with delayed cerebral ischemia and poor outcome. Stroke. 43(8):2126–2129

    Article  PubMed  Google Scholar 

  7. Galea JP, Dulhanty L, Patel HC (2017) Predictors of outcome in aneurysmal subarachnoid hemorrhage patients: observations from a multicenter data set. Stroke. 48(11):2958–2963

    Article  PubMed  Google Scholar 

  8. Hollingworth M, Jamjoom A, Bulters D, Patel H (2019) How is vasospasm screening using transcranial Doppler associated with delayed cerebral ischemia and outcomes in aneurysmal subarachnoid hemorrhage? Acta Neurochir 161(2):385–392

    Article  CAS  PubMed  Google Scholar 

  9. Kirkpatrick PJ, Turner CL, Smith C, Hutchinson PJ, Murray GD (2014) Simvastatin in aneurysmal subarachnoid haemorrhage (STASH): a multicentre randomised phase 3 trial. Lancet Neurol 13(7):666–675

    Article  CAS  PubMed  Google Scholar 

  10. Macdonald RL, Schweizer TA (2017) Spontaneous subarachnoid haemorrhage. Lancet 389(10069):655–666

    Article  PubMed  Google Scholar 

  11. Mijiti M, Mijiti P, Axier A, Amuti M, Guohua Z, Xiaojiang C et al (2016) Incidence and predictors of angiographic vasospasm, symptomatic vasospasm and cerebral infarction in Chinese patients with aneurysmal subarachnoid hemorrhage. PLoS One 11(12):e0168657

    Article  PubMed  PubMed Central  Google Scholar 

  12. Mogollon JP, Smoll NR, Panwar R (2018) Association Between Neurological Outcomes Related to Aneurysmal Subarachnoid Hemorrhage and Onsite Access to Neurointerventional Radiology. World Neurosurg 113:e29–e37

    Article  PubMed  Google Scholar 

  13. Pickard J, Murray G, Illingworth R, Shaw M, Teasdale G, Foy P et al (1989) Effect of oral nimodipine on cerebral infarction and outcome after subarachnoid haemorrhage: British aneurysm nimodipine trial. Br Med J 298(6674):636–642

    Article  CAS  Google Scholar 

  14. Rasmussen R, Bache S, Stavngaard T, Møller K (2019) Plasma levels of IL-6, IL-8, IL-10, ICAM-1, VCAM-1, IFNγ, and TNFα are not associated with delayed cerebral ischemia, cerebral vasospasm, or clinical outcome in patients with subarachnoid hemorrhage. World Neurosurg 128:e1131–e11e6

    Article  PubMed  Google Scholar 

  15. Rasmussen R, Stavngaard T, Jessing IR, Skjøth-Rasmussen J, Olsen NV, Ostrowski SR et al (2016) High plasma levels of neuropeptide y correlate with good clinical outcome but are not correlated to cerebral blood flow or vasospasm after subarachnoid hemorrhage. J Neurosurg Anesthesiol 28(1):65–70

    Article  PubMed  Google Scholar 

  16. Rowland M, Hadjipavlou G, Kelly M, Westbrook J, Pattinson K (2012) Delayed cerebral ischaemia after subarachnoid haemorrhage: looking beyond vasospasm. Br J Anaesth 109(3):315–329

    Article  CAS  PubMed  Google Scholar 

  17. Srinivasan A, Aggarwal A, Gaudihalli S, Mohanty M, Dhandapani M, Singh H et al (2016) Impact of early leukocytosis and elevated high-sensitivity C-reactive protein on delayed cerebral ischemia and neurologic outcome after subarachnoid hemorrhage. World Neurosurg 90:91–95

    Article  PubMed  Google Scholar 

  18. Vergouwen MD, Vermeulen M, van Gijn J, Rinkel GJ, Wijdicks EF, Muizelaar JP et al (2010) 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. 41(10):2391–2395

    Article  PubMed  Google Scholar 

  19. Wolf S, Mielke D, Barner C, Malinova V, Kerz T, Wostrack M, Czorlich P, Salih F, Engel DC, Ehlert A, Staykov D, Alturki AY, Sure U, Bardutzky J, Schroeder HWS, Schürer L, Beck J, Juratli TA, Fritsch M, Lemcke J, Pohrt A, Meyer B, Schwab S, Rohde V, Vajkoczy P, EARLYDRAIN Study Group (2023) Effectiveness of lumbar cerebrospinal fluid drain among patients with aneurysmal subarachnoid hemorrhage: a randomized clinical trial. JAMA Neurol 80(8):833–842. https://doi.org/10.1001/jamaneurol.2023.1792

  20. Wolff RF, Moons KG, Riley RD, Whiting PF, Westwood M, Collins GS et al (2019) PROBAST: a tool to assess the risk of bias and applicability of prediction model studies. Ann Intern Med 170(1):51–58

    Article  PubMed  Google Scholar 

Download references

Funding

HCP and LD are funded by the National Institute for Health Research Efficacy and Mechanism Evaluation Programme, Ref: 14/209/07. MH is supported by the Royal College of Surgeons England Research Fellowship and Brain Research UK.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. The literature search, data analysis and writing the first draft of the manuscript were performed by Caed Whittle and Milo Hollingworth. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Hiren C. Patel.

Ethics declarations

Ethics approval

This study is a meta-analysis that reuses data from prior publications.

Consent for publication

This study is a meta-analysis which reuses published data from prior publications.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

ESM 1

Supplementary Material 1. The Differing Definitions used by Excluded Studies in a Systematic Review of DCI Risk Factors (DOCX 30 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Whittle, C., Hollingworth, M.A., Dulhanty, L. et al. What are the predictors of delayed cerebral ischaemia (DCI) after aneurysmal subarachnoid haemorrhage? An up-to-date systematic review. Acta Neurochir 165, 3643–3650 (2023). https://doi.org/10.1007/s00701-023-05864-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-023-05864-4

Keywords

Navigation