Download PDF
J Neurol Surg A Cent Eur Neurosurg
DOI: 10.1055/a-2568-4732
Original Article

Cerebral Hemorrhage Volume Threshold and Shunt-Dependent Acute Hydrocephalus in Aneurysmal Subarachnoid Hemorrhage: A Semiautomated Measurement Study

Gema Bravo-Garrido 
1   Department of Neurosurgery, Torrecardenas University Hospital, Almeria, Andalucía, Spain
,
Antonio José Vargas-Lopez
1   Department of Neurosurgery, Torrecardenas University Hospital, Almeria, Andalucía, Spain
,
Miriam Fernández-Gómez
2   Department of Interventional Neuroradiology, Torrecardenas University Hospital, Almeria, Andalucía, Spain
,
Mario Gomar-Alba
1   Department of Neurosurgery, Torrecardenas University Hospital, Almeria, Andalucía, Spain
,
Gaizka Urreta-Juárez
1   Department of Neurosurgery, Torrecardenas University Hospital, Almeria, Andalucía, Spain
,
Patricia Martínez-Sánchez
3   Department of Neurology, Torrecardenas University Hospital, Almeria, Andalucía, Spain
› Author Affiliations
Funding None.
› Further Information
Also available at
   Permissions and Reprints

Abstract

Background

Hydrocephalus is a common complication of aneurysmal subarachnoid hemorrhage (aSAH) that can adversely affect prognosis. This study investigates the association between semiautomatic measurement of cerebral hemorrhage volumes in aSAH patients and the onset of shunt-dependent acute hydrocephalus (SDAHC) within the first 72 hours. Furthermore, the study seeks to establish a bleeding volume threshold indicative of SDAHC.

Methods

A retrospective observational analysis was conducted on a cohort of aSAH patients admitted to a specialized referral hospital between 2016 and 2021. Volumes of SAH, intraventricular hemorrhage (IVH), intraparenchymal hemorrhage (IPH), and total hemorrhage (TH) were computed from brain computed tomography scans utilizing Advantage Workstation Server analytical software. Receiver operating characteristic (ROC) curves and multivariate analyses were employed to determine the association between hemorrhage volumes and SDAHC.

Results

The study included 170 patients, of whom 111 (65.3%) were women, with a mean age of 58.5 years (standard deviation: 14.6). Fifty-five patients (32.4%) presented SDAHC. IVH volumes had an area under the ROC curve of 0.757 (95% confidence interval [CI]: 0.674–0.839; p < 0.001). An IVH volume > 2.7 cm3 showed a sensitivity of 70.9% and a specificity of 77.2% for predicting SDAHC, whereas TH volumes > 29.5 cm3 demonstrated a sensitivity of 69.1% and a specificity of 61.4%. Multivariate analysis revealed that IVH volumes > 2.7 cm3 (odds ratio [OR]: 5.373; 95% CI: 2.477–11.657), TH volumes > 29.5 cm3 (OR: 2.232; 95% CI: 1.008–4.942), and a bicaudate index ≥ 0.2 were significantly associated with SDAHC, adjusting for confounders.

Conclusions

In aSAH patients, semiautomatic measurement of hemorrhage volumes using specialized software is independently associated with SDAHC. This method could facilitate early prediction and timely intervention.

Keywords

aneurysmal subarachnoid hemorrhage - semiautomated hemorrhage volumetric analysis - shunt-dependent acute hydrocephalus

Ethical Approval

The study protocol has been approved by the Clinical Research Ethics Committee. All personal data obtained in this study are confidential and have been used exclusively for the specific purposes of this study. This study has been conducted in accordance with the principles of good clinical practice and following international and national regulations governing biomedical research, especially the Declaration of Helsinki, Law 14/2007 of July 3 on Biomedical Research, as well as Regulation (EU) 2016/679 of the European Parliament and of the Council of April 27, 2016, and Law 3/2018 of December 5 on Personal Data Protection and guarantee of digital rights.


Availability of Data and Materials

The datasets generated and analyzed during the current study are available from the corresponding author upon reasonable request. All materials used in the study are fully accessible to ensure reproducibility of the results.




Publication History

Received: 02 November 2024

Accepted: 27 March 2025

Accepted Manuscript online:
28 March 2025

Article published online:
01 July 2025

© 2025. Thieme. All rights reserved.

Georg Thieme Verlag KG
Oswald-Hesse-Straße 50, 70469 Stuttgart, Germany

 

  • References

  • 1 Nornes H, Magnaes B. Intracranial pressure in patients with ruptured saccular aneurysm. J Neurosurg 1972; 36 (05) 537-547
    PubMedSearch in Google Scholar
  • 2 Suarez-Rivera O. Acute hydrocephalus after subarachnoid hemorrhage. Surg Neurol 1998; 49 (05) 563-565
    PubMedSearch in Google Scholar
  • 3 Muehlschlegel S. Subarachnoid hemorrhage. Continuum (Minneap Minn) 2018; 24 (06) 1623-1657
    PubMedSearch in Google Scholar
  • 4 Douglas MR, Daniel M, Lagord C. et al. High CSF transforming growth factor β levels after subarachnoid haemorrhage: association with chronic communicating hydrocephalus. J Neurol Neurosurg Psychiatry 2009; 80 (05) 545-550
    PubMedSearch in Google Scholar
  • 5 van Gijn J, Hijdra A, Wijdicks EF, Vermeulen M, van Crevel H. Acute hydrocephalus after aneurysmal subarachnoid hemorrhage. J Neurosurg 1985; 63 (03) 355-362
    PubMedSearch in Google Scholar
  • 6 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 (07) 635-642
    CrossrefPubMedSearch in Google Scholar
  • 7 Connolly Jr ES, Rabinstein AA, Carhuapoma JR. et al; American Heart Association Stroke Council, Council on Cardiovascular Radiology and Intervention, Council on Cardiovascular Nursing, Council on Cardiovascular Surgery and Anesthesia, Council on Clinical Cardiology. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2012; 43 (06) 1711-1737
    CrossrefPubMedSearch in Google Scholar
  • 8 Xie Z, Hu X, Zan X, Lin S, Li H, You C. Predictors of shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage? A systematic review and meta-analysis. World Neurosurg 2017; 106: 844-860.e6
    CrossrefPubMedSearch in Google Scholar
  • 9 Macdonald RL. Delayed neurological deterioration after subarachnoid haemorrhage. Nat Rev Neurol 2014; 10 (01) 44-58
    CrossrefPubMedSearch in Google Scholar
  • 10 Solár P, Zamani A, Lakatosová K, Joukal M. The blood-brain barrier and the neurovascular unit in subarachnoid hemorrhage: molecular events and potential treatments. Fluids Barriers CNS 2022; 19 (01) 29
    PubMedSearch in Google Scholar
  • 11 Tso MK, Ibrahim GM, Macdonald RL. Predictors of shunt-dependent hydrocephalus following aneurysmal subarachnoid hemorrhage. World Neurosurg 2016; 86: 226-232
    PubMedSearch in Google Scholar
  • 12 Rincon F, Gordon E, Starke RM. et al. Predictors of long-term shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage. Clinical article. J Neurosurg 2010; 113 (04) 774-780
    CrossrefPubMedSearch in Google Scholar
  • 13 Dorai Z, Hynan LS, Kopitnik TA, Samson D. Factors related to hydrocephalus after aneurysmal subarachnoid hemorrhage. Neurosurgery 2003; 52 (04) 763-769 , discussion 769–771
    CrossrefPubMedSearch in Google Scholar
  • 14 Lai L, Morgan MK. Predictors of in-hospital shunt-dependent hydrocephalus following rupture of cerebral aneurysms. J Clin Neurosci 2013; 20 (08) 1134-1138
    CrossrefPubMedSearch in Google Scholar
  • 15 de Oliveira JG, Beck J, Ulrich C, Rathert J, Raabe A, Seifert V. Comparison between clipping and coiling on the incidence of cerebral vasospasm after aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. Neurosurg Rev 2007; 30 (01) 22-30 , discussion 30–31
    PubMedSearch in Google Scholar
  • 16 Woernle CM, Winkler KM, Burkhardt JK. et al. Hydrocephalus in 389 patients with aneurysm-associated subarachnoid hemorrhage. J Clin Neurosci 2013; 20 (06) 824-826
    PubMedSearch in Google Scholar
  • 17 Wang YM, Lin YJ, Chuang MJ. et al. Predictors and outcomes of shunt-dependent hydrocephalus in patients with aneurysmal sub-arachnoid hemorrhage. BMC Surg 2012; 12: 12
    PubMedSearch in Google Scholar
  • 18 Germanwala AV, Huang J, Tamargo RJ. Hydrocephalus after aneurysmal subarachnoid hemorrhage. Neurosurg Clin N Am 2010; 21 (02) 263-270
    CrossrefPubMedSearch in Google Scholar
  • 19 Czorlich P, Ricklefs F, Reitz M. et al. Impact of intraventricular hemorrhage measured by Graeb and LeRoux score on case fatality risk and chronic hydrocephalus in aneurysmal subarachnoid hemorrhage. Acta Neurochir (Wien) 2015; 157 (03) 409-415
    PubMedSearch in Google Scholar
  • 20 Rubinos C, Kwon SB, Megjhani M. et al. Predicting shunt dependency from the effect of cerebrospinal fluid drainage on ventricular size. Neurocrit Care 2022; 37 (03) 670-677
    PubMedSearch in Google Scholar
  • 21 Aboul-Ela HM, Salah El-Din AM, Zaater AA, Shehab M, El Shahawy OA. Predictors of shunt-dependent hydrocephalus following aneurysmal subarachnoid hemorrhage: a pilot study in a single Egyptian institute. Egypt J Neurol Psychiatr Neurosurg 2018; 54 (01) 11
    PubMedSearch in Google Scholar
  • 22 Reginelli A, Belfiore MP, Monti R. et al. The texture analysis as a predictive method in the assessment of the cytological specimen of CT-guided FNAC of the lung cancer. Med Oncol 2020; 37 (06) 54
    PubMedSearch in Google Scholar
  • 23 Katsari K, Penna D, Arena V. et al. Artificial intelligence for reduced dose 18F-FDG PET examinations: a real-world deployment through a standardized framework and business case assessment. EJNMMI Phys 2021; 8 (01) 25
    PubMedSearch in Google Scholar
  • 24 García S, Torné R, Hoyos JA. et al. Quantitative versus qualitative blood amount assessment as a predictor for shunt-dependent hydrocephalus following aneurysmal subarachnoid hemorrhage. J Neurosurg 2018; 131 (06) 1743-1750
    PubMedSearch in Google Scholar
  • 25 Jiménez-Roldán L, Alén JF, Gómez PA. et al. Volumetric analysis of subarachnoid hemorrhage: assessment of the reliability of two computerized methods and their comparison with other radiographic scales. J Neurosurg 2013; 118 (01) 84-93
    PubMedSearch in Google Scholar
  • 26 Ko SB, Choi HA, Carpenter AM. et al. Quantitative analysis of hemorrhage volume for predicting delayed cerebral ischemia after subarachnoid hemorrhage. Stroke 2011; 42 (03) 669-674
    PubMedSearch in Google Scholar
  • 27 Kramer AH, Mikolaenko I, Deis N. et al. Intraventricular hemorrhage volume predicts poor outcomes but not delayed ischemic neurological deficits among patients with ruptured cerebral aneurysms. Neurosurgery 2010; 67 (04) 1044-1052 , discussion 1052–1053
    CrossrefPubMedSearch in Google Scholar
  • 28 Yuan JY, Chen Y, Jayaraman K. et al. Automated quantification of compartmental blood volumes enables prediction of delayed cerebral ischemia and outcomes after aneurysmal subarachnoid hemorrhage. World Neurosurg 2023; 170: e214-e222
    PubMedSearch in Google Scholar
  • 29 Meyer A, Forman E, Moody S. et al. Cisternal score: a radiographic score to predict ventriculoperitoneal shunt requirement in aneurysmal subarachnoid hemorrhage. Neurosurgery 2023; 93 (01) 75-83
    PubMedSearch in Google Scholar
  • 30 Lagares A, Jiménez-Roldán L, Gomez PA. et al. Prognostic value of the amount of bleeding after aneurysmal subarachnoid hemorrhage: a quantitative volumetric study. Neurosurgery 2015; 77 (06) 898-907 , discussion 907
    PubMedSearch in Google Scholar
  • 31 Bosche B, Mergenthaler P, Doeppner TR, Hescheler J, Molcanyi M. Complex clearance mechanisms after intraventricular hemorrhage and rt-PA treatment-a review on clinical trials. Transl Stroke Res 2020; 11 (03) 337-344
    PubMedSearch in Google Scholar
  • 32 Hanley DF, Lane K, McBee N. et al; CLEAR III Investigators. Thrombolytic removal of intraventricular haemorrhage in treatment of severe stroke: results of the randomised, multicentre, multiregion, placebo-controlled CLEAR III trial. Lancet 2017; 389 (10069): 603-611
    CrossrefPubMedSearch in Google Scholar
  • 33 Staykov D, Kuramatsu JB, Bardutzky J. et al. Efficacy and safety of combined intraventricular fibrinolysis with lumbar drainage for prevention of permanent shunt dependency after intracerebral hemorrhage with severe ventricular involvement: a randomized trial and individual patient data meta-analysis. Ann Neurol 2017; 81 (01) 93-103
    CrossrefPubMedSearch in Google Scholar
  • 34 Orešković D, Radoš M, Klarica M. Role of choroid plexus in cerebrospinal fluid hydrodynamics. Neuroscience 2017; 354: 69-87
    PubMedSearch in Google Scholar
  • 35 Sanz-Cuesta BE, Saver JL. Lipid-lowering therapy and hemorrhagic stroke risk: comparative meta-analysis of statins and PCSK9 inhibitors. Stroke 2021; 52 (10) 3142-3150
    CrossrefPubMedSearch in Google Scholar
  • 36 Pandit AK, Kumar P, Kumar A, Chakravarty K, Misra S, Prasad K. High-dose statin therapy and risk of intracerebral hemorrhage: a meta-analysis. Acta Neurol Scand 2016; 134 (01) 22-28
    PubMedSearch in Google Scholar
  • 37 Kuo LT, Lu HY, Tsai JC, Tu YK. Prediction of shunt dependency after intracerebral hemorrhage and intraventricular hemorrhage. Neurocrit Care 2018; 29 (02) 233-240
    PubMedSearch in Google Scholar
  • 38 Khalaveh F, Zeiser V, Cho A. et al. Predicting the need for cerebrospinal fluid shunt implantation after spontaneous intracerebral hemorrhage: a challenging task. Front Neurol 2023; 14: 1255477
    PubMedSearch in Google Scholar