Skip to main content

Advertisement

Log in

Acute hydrocephalus and delayed cerebral infarction after aneurysmal subarachnoid hemorrhage

  • Original Article - Vascular Neurosurgery - Aneurysm
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Background

Delayed cerebral infarction (DCIn) following aneurysmal subarachnoid hemorrhage (aSAH) is a major cause of morbi-mortality; yet, the causes for DCIn remain incompletely understood.

Objective

We tested the hypothesis that acute hydrocephalus could be related to the occurrence of DCIn, independently of the occurrence and severity of vasospasm.

Methods

Radiological and clinical data of patients treated at a single large volume academic center for aSAH between 2017 and 2019 were retrospectively analyzed. DCIn was defined as imaging stigma of cerebral infarction visible on 6-week imaging follow-up after aSAH. Hydrocephalus was defined on baseline imaging as a relative bicaudate index above 1. Cerebral vasospasm was defined by reduction of artery diameter in comparison with initial diameter. We used uni- and multivariable models to test the associations between these variables, hydrocephalus and DCIn.

Results

Of 164 included patients, vasospasm occurred in 58 patients (35.4%), and DCIn in 47 (28.7%). Acute hydrocephalus was present in 85 patients (51.8%) on baseline CT. No relation was found between acute hydrocephalus and delayed cerebral infarction in our multivariate analysis (adjusted OR: 1.20 95% CI [0.43–3.37]; p = 0.732). Only vasospasm occurrence was independently associated with DCIn (adjusted OR: 10.97 95% CI [4.60–26.01]).

Conclusion

Our study did not show an association between acute hydrocephalus and DCIn after aSAH, after adjustment for the presence and severity of cerebral vasospasm.

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

Abbreviations

SAH:

Subarachnoid hemorrhage

aSAH:

Aneurysmal subarachnoid hemorrhage

DCI:

Delayed cerebral ischemia

DCIn:

Delayed cerebral infarction

CT:

Computed tomography

MRI:

Magnetic resonance imaging

WFNS:

World federation of neurosurgical surgery

BCI:

Bicaudate index

rBCI:

Relative bicaudate index

EVD:

External ventricular drainage

References

  1. Bakker AM, Dorhout SM, Algra A, Rinkel GJ (2007) Extent of acute hydrocephalus after aneurysmal subarachnoid hemorrhage as a risk factor for delayed cerebral infarction. Stroke 38:2496–2499. https://doi.org/10.1161/STROKEAHA.107.484220

    Article  PubMed  Google Scholar 

  2. Balbi M, Koide M, Schwarzmaier SM, Wellman GC, Plesnila N (2017) Acute changes in neurovascular reactivity after subarachnoid hemorrhage in vivo. J Cereb Blood Flow Metab 37(1):178–187. https://doi.org/10.1177/0271678X15621253

    Article  CAS  PubMed  Google Scholar 

  3. Black PM (1986) Hydrocephalus and vasospasm after subarachnoid hemorrhage from ruptured intra-cranial aneurysms. Neurosurgery 18:12–16. https://doi.org/10.1227/00006123-198601000-00003

    Article  CAS  PubMed  Google Scholar 

  4. Bosche B, Graf R, Ernestus R-I, Dohmen C, Reithmeier T, Brinker G, Strong AJ, Dreier JP, Woitzik J (2010) Recurrent spreading depolarizations after subarachnoid hemorrhage decreases oxygen availability in human cerebral cortex. Ann Neurol 67(5):607–617. https://doi.org/10.1002/ana.21943

    Article  PubMed  PubMed Central  Google Scholar 

  5. Bosche B, Mergenthaler P, Doeppner TR, Hescheler J, Molcanyi M (2019) Complex clearance mechanisms after intraventricular hemorrhage and rt-PA treatment – a review on clinical trials. Transl Stroke Res. https://doi.org/10.1007/s12975-019-00735-6

    Article  PubMed  Google Scholar 

  6. Boulouis G, Labeyrie MA, Raymond J, Rodriguez-Régent C, Lukaszewicz AC, Bresson D, Ben Hassen W, Tristram D, Meder JF, Oppenheim C, Naggara O (2017) Treatment of cerebral vasospasm following aneurysmal subarachnoid haemorrhage: a systematic review and meta-analysis. Eur Radiol 27(8):3333–3342. https://doi.org/10.1007/s00330-016-4702-y

    Article  PubMed  Google Scholar 

  7. Brami J, Chousterman B, Boulouis G, Le Dorze M, Majlath M, Saint-Maurice JP, Civelli V, Froelich S, Houdart E, Labeyrie MA (2020) Delayed cerebral infarction is systematically associated with a cerebral vasospasm of large intracranial arteries. Neurosurgery 86(2):E175–E183. https://doi.org/10.1093/neuros/nyz340

    Article  PubMed  Google Scholar 

  8. Bretz JS, Von Dincklage F, Woitzik J, Winkler MK, Major S, Dreier JP, Bohner G, School M (2017) The Hijdra scale has significant prognostic value for the functional outcome of Fisher grade 3 patients with subarachnoid hemorrhage. Clin Neuroradiol 27(3):361–369. https://doi.org/10.1007/s00062-016-0509-0

    Article  PubMed  Google Scholar 

  9. Brouwers PJ, Dippel DW, Vermeulen M, Lindsay KW, Hasan D, van Gijn J (1993) Amount of blood on computed tomography as an independent predictor after aneurysm rupture. Stroke 24:809–814. https://doi.org/10.1161/01.str.24.6.809

    Article  CAS  PubMed  Google Scholar 

  10. Budohoski KP, Guilfoyle M, Helmy A, Huuskonen T, Czosnyka M, Kirollos R, Menon DK, Pickard JD, Kirkpatrick P (2014) The pathophysiology and treatment of delayed cerebral ischaemia following subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry 85(12):1343–1353. https://doi.org/10.1136/jnnp-2014-307711

    Article  PubMed  Google Scholar 

  11. Chen S, Lou J, Reis C, Manaenko A, Zhang J (2017) Hydrocephalus after subarachnoid hemorrhage: pathophysiology, diagnosis, and treatment. Biomed Rest Int 2017:8584753. https://doi.org/10.1155/2017/8584753

    Article  CAS  Google Scholar 

  12. Dakson A, Kameda-Smith M, Staudt MD, Lavergne P, Makarenko S,Eagles ME, Ghayur H, Guo RC, Althagafi A, Chainey J, Touchette CJ, Elliott C, Iorio-Morin C, Tso MK, Green R Bargone L, Christie SD (2021) A nationwide prospective multicenter study of external ventricular drainage: accuracy, safety, and related complications. J Neurosurg: 1–9. https://doi.org/10.3171/2021.7.JNS21421.

  13. Ditz C, Leppert J, Neumann A, Krajewski KL, Gliemroth J, Tronnier VM, Küchler J (2020) Cerebral vasospasm following spontaneous subarachnoid hemorrhage: angiographic pattern and its impact on the clinical course. World Neurosurg 138:e913–e921. https://doi.org/10.1016/j.wneu.2020.03.146

    Article  PubMed  Google Scholar 

  14. Dong L, Zhou Y, Wang M, Yang C, Yuan Q, Fang X (2019) Whole-brain CT perfusion on admission predicts delayed cerebral ischemia following aneurysmal subarachnoid hemorrhage. Eur J Radiol 116:165–173. https://doi.org/10.1016/j.ejrad.2019.05.008

    Article  PubMed  Google Scholar 

  15. Dorsch NW, King MT (1994) A review of cerebral vasospasm in aneurysmal subarachnoid haemorrhage part I: incidence and effects. J Clin Neurosci 1(1):19–26. https://doi.org/10.1016/0967-5868(94)90005-1

    Article  CAS  PubMed  Google Scholar 

  16. Dupont SA, Wijdicks FM, Manno EM, Lanzino G, Rabinstein A (2009) Prediction of angiographic vasospasm after aneurysmal subarachnoid hemorrhage: value of the Hijdra sum scoring system. Neurocrit Care 11(2):172–176. https://doi.org/10.1007/s12028-009-9247-3

    Article  PubMed  Google Scholar 

  17. Etminan N, Beseoglu K, Heiroth HJ, Turowski B, Steiger HJ, Hanggi D (2013) Early perfusion computerized tomography imaging as a radiographic surrogate for delayed cerebral ischemia and functional outcome after subarachnoid hemorrhage. Stroke 44:1260–1266. https://doi.org/10.1161/STROKEAHA.111.675975

    Article  PubMed  Google Scholar 

  18. Fugate JE, Rabinstein AA, Wijdicks EF, Lanzoni G (2012) Aggressive CSF diversion reverses delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage: a case report. Neurocrit Care 17:112–116. https://doi.org/10.1007/s12028-012-9723-z

    Article  PubMed  Google Scholar 

  19. Hammer A, Erbguth F, Hohenhaus M, Hammer CM, Lücking H, Gesslein M, Killer-Oberpfalzer M, Steiner HH, Janssen H (2021) Neurocritical care complications and interventions influence the outcome in aneurysmal subarachnoid hemorrhage. BMC Neurol 21(1):27. https://doi.org/10.1186/s12883-021-02054-6

    Article  PubMed  PubMed Central  Google Scholar 

  20. Hammer A, Erbguth F, Hohenhaus M, Hammer CM, Lücking H, Gesslein M, Killer-Oberpfalzer M, Steiner HH, Janssen H (2021) Neurocritical care complications and interventions influence the outcome in aneurysmal subarachnoid hemorrhage. BMC Neurol 21:27. https://doi.org/10.1186/s12883-021-02054-6

    Article  PubMed  PubMed Central  Google Scholar 

  21. Hasan D, Tanghe HL (1992) Distribution of cisternal blood in patients with acute hydrocephalus after subarachnoid hemorrhage. 31(4):374-8. https://doi.org/10.1002/ana.410310405

  22. Hijdra A, van Gijn J, Nagelkerke NJ, Vermeulen M, van Crevel H (1988) Prediction of delayed cerebral ischemia, rebleeding, and outcome after aneurysmal subarachnoid hemorrhage. Stroke 19:1250–1256. https://doi.org/10.1161/01.str.19.10.1250

    Article  CAS  PubMed  Google Scholar 

  23. Hirashima Y, Hamada Y, Hamada H, Hayashi N, Kuwayama N, Origasa H, Endo S (2003) Independent predictors of late hydrocephalus in patients with aneurysmal subarachnoid hemorrhage – analysis by multivariate logistic regression model. Crebrovasc Dis 16(3):205–210. https://doi.org/10.1186/s13037-018-0160-6

    Article  Google Scholar 

  24. Hop JW, Rinkel GJ, Algra A, van Gijn J (1999) Initial loss of consciousness and risk of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Stroke 30:2268–2271. https://doi.org/10.1161/01.str.30.11.2268

    Article  CAS  PubMed  Google Scholar 

  25. Jingjing L, Nan J, Zhonghua Y, Xingquan Z (2012) Prognosis and treatment of acute hydrocephalus following aneurysmal subarachnoid haemorrhage. J Clin Neurosci 19(5):669–72. https://doi.org/10.1016/j.jocn.2011.06.032

    Article  Google Scholar 

  26. Lindvall P, Runnerstam M, Birgander R, Koskinen LO (2009) The Fisher grading correlated to outcome in patients with subarachnoid haemorrhage. Br J Neurosurg 23(2):188–192. https://doi.org/10.1080/02688690802710668.Sano

    Article  PubMed  Google Scholar 

  27. MacDonald RL (2014) Delayed neurological deterioration after subarachnoid haemorrhage. Nat Rev Neurol 10(1):44–58. https://doi.org/10.1038/nrneurol.2013.246

    Article  CAS  PubMed  Google Scholar 

  28. Nakagawa I, Hironaka Y, Nishimura F (2013) Early inhibition of natriuresis suppresses symptomatic cerebral vasospasm in patients with aneurysmal subarachnoid hemorrhage. Cerebrovasc Dis 35:131–137. https://doi.org/10.1159/000346586

    Article  PubMed  Google Scholar 

  29. Neifert SN, Chapman EK, Martini ML, Shuman WH, Schupper AJ, Oermann EK, Mocco J, Macdonald RL (2021) Aneurismal subarachnoid hemorrhage: the last decade. Trans Stroke Res 12(3):428–446. https://doi.org/10.10007/s12975-020-00867-0

    Article  Google Scholar 

  30. Roos YB, de Haan RJ, Beenen LF, Groen RJ, Albrecht KW, Vermeulen M (2000) Complications and outcome in patients with aneurysmal subarachnoid haemorrhage: a prospective hospital-based cohort study in The Netherlands. J Neurol Neurosurg Psychiatry 68(3):337–341. https://doi.org/10.1136/jnnp.68.3.337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Rowland MJ, Hadjipavlou G, Kelly M, Westbrook J, Pattinson KTS (2012) Delayed cerebral ischaemia after subarachnoid haemorrhage: looking beyond vasospasm. Br J Anaesth 109(3):315–329. https://doi.org/10.1093/bja/aes264

    Article  CAS  PubMed  Google Scholar 

  32. Sehba FA, Ryszard JH, Pluta M, Zhang JH (2012) The importance of early brain injury after subarachnoid hemorrhage. Prog Neurobiol 97(1):14–37. https://doi.org/10.1016/j.pneurobio.2012.02.003

    Article  PubMed  PubMed Central  Google Scholar 

  33. Starnoni D, Maduri R, Hajdu SD, Pierzchala K, Giammattei L, Rocca A, Grosfilley SB, Saliou G, Messerer M, Roy (2019) Early perfusion computed tomography scan for prediction of vasospasm and delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. World Neurosurg 130:e743–e752. https://doi.org/10.1016/j.wneu.2019.06.213

    Article  PubMed  Google Scholar 

  34. van Asch CJ, van der Schaaf IC, Rinkel GJ (2010) Acute hydrocephalus and cerebral perfusion after aneurysmal subarachnoid hemorrhage. Am J Neuroradiol 31(1):67–70. https://doi.org/10.3174/ajnr.A1748

    Article  PubMed  PubMed Central  Google Scholar 

  35. van Gijn J, Hijdra A, Wijdicks FM, Vermeulen M, Van Crevel H (1985) Acute hydrocephalus after aneurysmal subarachnoid hemorrhage. J Neurosurg 63(3):355–362. https://doi.org/10.3171/jns.1985.63.3.0355

    Article  PubMed  Google Scholar 

  36. Van der Steen WE, Leemans EL, van den Berg R, Roos YB, Marquering HA, Verbaan D, Majoie C (2019) Radiological scales predicting delayed cerebral ischemia in subarachnoid hemorrhage: systematic review and meta-analysis. Neuroradiology 61(3):247–256. https://doi.org/10.1007/s00234-019-02161-9

    Article  PubMed  Google Scholar 

  37. Vergouwen MDI, Vermeulen M, van Gijn J, Rinkel GJE, Wijdicks EF, Muizelaar JP, Mendelow AD, Juvela S, Yonas H, Terbrugge KG, Macdonald RL, Diringer MN, Broderick JP, Dreier JP, Roos YBWEM (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 41:2391–2395. https://doi.org/10.1161/STROKEAHA.110.589275

    Article  PubMed  Google Scholar 

  38. Weidauer S, Lanfermann H, Raabe A, Zanella F, Seifert V, Beck J (2007) Impairment of cerebral perfusion and infarct patterns attributable to vasospasm after aneurysmal subarachnoid hemorrhage: a prospective MRI and DSA study. Stroke 38(6):1831–1836. https://doi.org/10.1161/STROKEAHA.106.477976

    Article  PubMed  Google Scholar 

  39. Yoshino M, Yoshimi Y, Taniguchi M, Nakamura S, Ikeda T (1999) Syndrome of inappropriate secretion of antidiuretic hormone associated with idiopathic normal pressure hydrocephalus. Intern Med 38(3):290–292. https://doi.org/10.2169/internalmedicine.38.290

    Article  CAS  PubMed  Google Scholar 

  40. Zhong Y, Xin H, Chao Y (2017) Endovascular therapy for vasospasm secondary to subarachnoid hemorrhage: a meta-analysis and systematic review. Clin Neurol Neurosurg 163:9–14. https://doi.org/10.1016/j.clineuro.2017.09.016

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Axel Masson or Héloïse Ifergan.

Ethics declarations

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This article does not contain any studies with animals performed by any of the authors.

Consent to participate

Informed consent was obtained from all individual participants included in the study.

Conflict of interest

Axel Masson declares that he has no conflict of interest.

Grégoire Boulouis declares that he has no conflict of interest.

Kévin Janot declares that he has no conflict of interest.

Denis Herbreteau declares that he has no conflict of interest.

Jean-Philippe Cottier declares that he has no conflict of interest.

Richard Bibi declares that he has no conflict of interest.

Clara Cohen declares that she has no conflict of interest.

Sandra Obry declares that she has no conflict of interest.

Stéphane Velut declares that he has no conflict of interest.

Aymeric Amelot declares that he has no conflict of interest.

Héloïse Ifergan declares that she has no conflict of interest.

Additional information

Publisher's note

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

This article is part of the Topical Collection on Vascular Neurosurgery - Aneurysm

Rights and permissions

Springer Nature or its licensor 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

Masson, A., Boulouis, G., Janot, K. et al. Acute hydrocephalus and delayed cerebral infarction after aneurysmal subarachnoid hemorrhage. Acta Neurochir 164, 2401–2408 (2022). https://doi.org/10.1007/s00701-022-05321-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-022-05321-8

Keywords

Navigation