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Hemorrhagic burden in poor-grade aneurysmal subarachnoid hemorrhage: a volumetric analysis of different bleeding distributions

  • Original Article - Vascular Neurosurgery - Aneurysm
  • Published:
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Abstract

Background

Volumetric assessment of aneurysmal bleeding has been evaluated in few studies and emerged as a promising outcome predictor. There is a lack of studies evaluating its impact in the poor-grade population.

Methods

Retrospective review of 63 consecutive poor-grade aneurysmal subarachnoid hemorrhage (aSAH) patients, defined as grade IV and V according to the World Federation of Neurological Surgeons (WFNS) classifications. Global intracranial bleeding volume was calculated with its subarachnoid, intracerebral (ICH), and intraventricular (IVH) portions by means of analytical software. Univariate and multivariate analyses were performed in order to identify independent predictors of outcome. Good outcome was defined as modified Rankin Scale (mRS) 0–2 and mortality as mRS 6. The cutoff values of bleeding volumes were derived by receiver operating curve (ROC) analysis.

Results

Mean follow-up was of 12.5 (± 1.5) months. Thirty (47.7%) patients achieved good outcome, whereas 19 (30.2) patients out of 63 died. Global intracranial bleeding resulted as an independent predictor of good outcome (cutoff 24 mL). Furthermore, ICH relative percentage of global volume (10% of total) and pure SAH (64% of total) emerged respectively as independent predictors of worsened and improved outcome. Global bleeding volume (cutoff 51 mL) along with global cerebral edema showed to independently predict mortality in the examined poor-grade aSAH population.

Conclusions

Volumetric assessment of aneurysmal bleeding has the potential for identifying cutoff values that independently predict outcome. Further insights into the relative importance of different bleeding volumes may be implicated in better tailoring the management of this dismal aSAH population.

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References

  1. Adams HP Jr, Kassell NF, Torner JC, Haley EC Jr (1987) Predicting cerebral ischemia after aneurysmal subarachnoid hemorrhage: influences of clinical condition, CT results, and antifibrinolytic therapy. A report of the cooperative aneurysm study. Neurology 37:1586–1591

    Article  PubMed  Google Scholar 

  2. Boers AM, Zijlstra IA, Gathier CS, van den Berg R, Slump CH, Marquering HA, Majoie CB (2014) Automatic quantification of subarachnoid hemorrhage on noncontrast CT. AJNR Am J Neuroradiol 35:2279–2286

    Article  CAS  PubMed  Google Scholar 

  3. Bruder M, Schuss P, Berkefeld J, Wagner M, Vatter H, Seifert V, Guresir E (2014) Subarachnoid hemorrhage and intracerebral hematoma caused by aneurysms of the anterior circulation: influence of hematoma localization on outcome. Neurosurg Rev 37:653–659

    Article  PubMed  Google Scholar 

  4. Claassen J, Bernardini GL, Kreiter K, Bates J, Du YE, Copeland D, Connolly ES, Mayer SA (2001) Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke 32:2012–2020

    Article  CAS  PubMed  Google Scholar 

  5. Claassen J, Carhuapoma JR, Kreiter KT, Du EY, Connolly ES, Mayer SA (2002) Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome. Stroke 33:1225–1232

    Article  PubMed  Google Scholar 

  6. Connolly ES Jr, Rabinstein AA, Carhuapoma JR, Derdeyn CP, Dion J, Higashida RT, Hoh BL, Kirkness CJ, Naidech AM, Ogilvy CS, Patel AB, Thompson BG, Vespa P, American Heart Association Stroke C, Council on Cardiovascular R, Intervention, Council on Cardiovascular N, Council on Cardiovascular S, Anesthesia, Council on Clinical C (2012) Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 43:1711–1737

    Article  Google Scholar 

  7. Darkwah Oppong M, Gembruch O, Herten A, Frantsev R, Chihi M, Dammann P, El Hindy N, Forsting M, Sure U, Jabbarli R (2018) Intraventricular hemorrhage caused by subarachnoid hemorrhage: does the severity matter? World Neurosurg 111:e693–e702

    Article  PubMed  Google Scholar 

  8. de Oliveira Manoel AL, Mansur A, Silva GS, Germans MR, Jaja BN, Kouzmina E, Marotta TR, Abrahamson S, Schweizer TA, Spears J, Macdonald RL (2016) Functional outcome after poor-grade subarachnoid hemorrhage: a single-center study and systematic literature review. Neurocrit Care 25:338–350

    Article  PubMed  Google Scholar 

  9. Fisher CM, Kistler JP, Davis JM (1980) Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6:1–9

    Article  CAS  PubMed  Google Scholar 

  10. Friedman JA, Goerss SJ, Meyer FB, Piepgras DG, Pichelmann MA, McIver JI, Toussaint LG 3rd, McClelland RL, Nichols DA, Atkinson JL, Wijdicks EF (2002) Volumetric quantification of Fisher grade 3 aneurysmal subarachnoid hemorrhage: a novel method to predict symptomatic vasospasm on admission computerized tomography scans. J Neurosurg 97:401–407

    Article  PubMed  Google Scholar 

  11. Frontera JA, Claassen J, Schmidt JM, Wartenberg KE, Temes R, Connolly ES Jr, MacDonald RL, Mayer SA (2006) Prediction of symptomatic vasospasm after subarachnoid hemorrhage: the modified fisher scale. Neurosurgery 59:21–27 discussion 21–27

    Article  PubMed  Google Scholar 

  12. Guresir E, Beck J, Vatter H, Setzer M, Gerlach R, Seifert V, Raabe A (2008) Subarachnoid hemorrhage and intracerebral hematoma: incidence, prognostic factors, and outcome. Neurosurgery 63:1088–1093 discussion 1093–1084

    Article  PubMed  Google Scholar 

  13. Heiskanen O, Poranen A, Kuurne T, Valtonen S, Kaste M (1988) Acute surgery for intracerebral haematomas caused by rupture of an intracranial arterial aneurysm. A prospective randomized study. Acta Neurochir 90:81–83

    Article  CAS  PubMed  Google Scholar 

  14. Helbok R, Ko SB, Schmidt JM, Kurtz P, Fernandez L, Choi HA, Connolly ES, Lee K, Badjatia N, Mayer SA, Claassen J (2011) Global cerebral edema and brain metabolism after subarachnoid hemorrhage. Stroke 42:1534–1539

    Article  PubMed  Google Scholar 

  15. Hijdra A, Brouwers PJ, Vermeulen M, van Gijn J (1990) Grading the amount of blood on computed tomograms after subarachnoid hemorrhage. Stroke 21:1156–1161

    Article  CAS  Google Scholar 

  16. Ibrahim GM, Weidauer S, Macdonald RL (2011) Interobserver variability in the interpretation of computed tomography following aneurysmal subarachnoid hemorrhage. J Neurosurg 115:1191–1196

    Article  PubMed  Google Scholar 

  17. Klimo P Jr, Schmidt RH (2006) Computed tomography grading schemes used to predict cerebral vasospasm after aneurysmal subarachnoid hemorrhage: a historical review. Neurosurg Focus 21:E5

    Article  PubMed  Google Scholar 

  18. Ko SB, Choi HA, Carpenter AM, Helbok R, Schmidt JM, Badjatia N, Claassen J, Connolly ES, Mayer SA, Lee K (2011) Quantitative analysis of hemorrhage volume for predicting delayed cerebral ischemia after subarachnoid hemorrhage. Stroke 42:669–674

    Article  PubMed  Google Scholar 

  19. Konczalla J, Seifert V, Beck J, Guresir E, Vatter H, Raabe A, Marquardt G (2018) 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 128:100–110

    Article  PubMed  Google Scholar 

  20. Kummer TT, Magnoni S, MacDonald CL, Dikranian K, Milner E, Sorrell J, Conte V, Benetatos JJ, Zipfel GJ, Brody DL (2015) Experimental subarachnoid haemorrhage results in multifocal axonal injury. Brain 138:2608–2618

    Article  PubMed  PubMed Central  Google Scholar 

  21. Lagares A, Jimenez-Roldan L, Gomez PA, Munarriz PM, Castano-Leon AM, Cepeda S, Alen JF (2015) Prognostic value of the amount of bleeding after aneurysmal subarachnoid hemorrhage: a quantitative volumetric study. Neurosurgery 77:898–907 discussion 907

    Article  PubMed  Google Scholar 

  22. Rosen DS, Amidei C, Tolentino J, Reilly C, Macdonald RL (2007) Subarachnoid clot volume correlates with age, neurological grade, and blood pressure. Neurosurgery 60:259–266 discussion 266–257

    Article  PubMed  Google Scholar 

  23. Rosengart AJ, Schultheiss KE, Tolentino J, Macdonald RL (2007) Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke 38:2315–2321

    Article  PubMed  Google Scholar 

  24. Sato T, Sasaki T, Sakuma J, Watanabe T, Ichikawa M, Ito E, Matsumoto Y, Ando H, Saito K, Kikori K, Yusa T, Suzuki K, Watanabe Y, Taira S, Sato M (2011) Quantification of subarachnoid hemorrhage by three-dimensional computed tomography: correlation between hematoma volume and symptomatic vasospasm. Neurol Med Chir (Tokyo) 51:187–194

    Article  Google Scholar 

  25. Schuss P, Hadjiathanasiou A, Borger V, Wispel C, Vatter H, Guresir E (2016) Poor-grade aneurysmal subarachnoid hemorrhage: factors influencing functional outcome—a single-center series. World Neurosurg 85:125–129

    Article  PubMed  Google Scholar 

  26. Suwatcharangkoon S, Meyers E, Falo C, Schmidt JM, Agarwal S, Claassen J, Mayer SA (2016) Loss of consciousness at onset of subarachnoid hemorrhage as an important marker of early brain injury. JAMA Neurol 73:28–35

    Article  PubMed  Google Scholar 

  27. Wostrack M, Sandow N, Vajkoczy P, Schatlo B, Bijlenga P, Schaller K, Kehl V, Harmening K, Ringel F, Ryang YM, Friedrich B, Stoffel M, Meyer B (2013) Subarachnoid haemorrhage WFNS grade V: is maximal treatment worthwhile? Acta Neurochir 155:579–586

    Article  PubMed  Google Scholar 

  28. Wu Y, Peng J, Pang J, Sun X, Jiang Y (2017) Potential mechanisms of white matter injury in the acute phase of experimental subarachnoid haemorrhage. Brain 140:e36

    Article  PubMed  Google Scholar 

  29. Zhao B, Rabinstein A, Murad MH, Lanzino G, Panni P, Brinjikji W (2017) Surgical and endovascular treatment of poor-grade aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. J Neurosurg Sci 61:403–415

    PubMed  Google Scholar 

  30. Zhao B, Yang H, Zheng K, Li Z, Xiong Y, Tan X, Zhong M, Group AS (2017) Preoperative and postoperative predictors of long-term outcome after endovascular treatment of poor-grade aneurysmal subarachnoid hemorrhage. J Neurosurg 126:1764–1771

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Neurosurgery and Gamma Knife Radiosurgery, IRCCS San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Via Olgettina 60, 20132, Milan, Italy

    Pietro Panni, Carmine Antonio Donofrio, Lina Raffaella Barzaghi, Luigi Albano & Pietro Mortini

  2. Department of Neuroradiology, Interventional Neuroradiology Division, IRCCS San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Via Olgettina 60, 20132, Milan, Italy

    Pietro Panni, Elisa Colombo, Claudio Righi, Francesco Scomazzoni, Franco Simionato, Andrea Falini & Nicoletta Anzalone

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  1. Pietro Panni
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  2. Elisa Colombo
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Correspondence to Pietro Panni.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee (name of institute/committee) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. For this type of study, formal consent is not required.

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Panni, P., Colombo, E., Donofrio, C.A. et al. Hemorrhagic burden in poor-grade aneurysmal subarachnoid hemorrhage: a volumetric analysis of different bleeding distributions. Acta Neurochir 161, 791–797 (2019). https://doi.org/10.1007/s00701-019-03846-z

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  • DOI: https://doi.org/10.1007/s00701-019-03846-z

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