Skip to main content
Erschienen in: Acta Neurochirurgica 4/2019

21.02.2019 | Original Article - Vascular Neurosurgery - Aneurysm

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

verfasst von: Pietro Panni, Elisa Colombo, Carmine Antonio Donofrio, Lina Raffaella Barzaghi, Luigi Albano, Claudio Righi, Francesco Scomazzoni, Franco Simionato, Pietro Mortini, Andrea Falini, Nicoletta Anzalone

Erschienen in: Acta Neurochirurgica | Ausgabe 4/2019

Einloggen, um Zugang zu erhalten

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.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat 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 37:1586–1591CrossRefPubMed 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 37:1586–1591CrossRefPubMed
2.
Zurück zum Zitat 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 35:2279–2286CrossRefPubMed 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 35:2279–2286CrossRefPubMed
3.
Zurück zum Zitat 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 37:653–659CrossRefPubMed 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 37:653–659CrossRefPubMed
4.
Zurück zum Zitat 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 32:2012–2020CrossRefPubMed 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 32:2012–2020CrossRefPubMed
5.
Zurück zum Zitat 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 33:1225–1232CrossRefPubMed 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 33:1225–1232CrossRefPubMed
6.
Zurück zum Zitat 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 43:1711–1737CrossRef 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 43:1711–1737CrossRef
7.
Zurück zum Zitat 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–e702CrossRefPubMed 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–e702CrossRefPubMed
8.
Zurück zum Zitat 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 25:338–350CrossRefPubMed 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 25:338–350CrossRefPubMed
9.
Zurück zum Zitat Fisher CM, Kistler JP, Davis JM (1980) Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6:1–9CrossRefPubMed Fisher CM, Kistler JP, Davis JM (1980) Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6:1–9CrossRefPubMed
10.
Zurück zum Zitat 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 97:401–407CrossRefPubMed 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 97:401–407CrossRefPubMed
11.
Zurück zum Zitat 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 21–27CrossRefPubMed 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 21–27CrossRefPubMed
12.
Zurück zum Zitat 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 1093–1084CrossRefPubMed 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 1093–1084CrossRefPubMed
13.
Zurück zum Zitat 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 90:81–83CrossRefPubMed 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 90:81–83CrossRefPubMed
14.
Zurück zum Zitat 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 42:1534–1539CrossRefPubMed 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 42:1534–1539CrossRefPubMed
15.
Zurück zum Zitat Hijdra A, Brouwers PJ, Vermeulen M, van Gijn J (1990) Grading the amount of blood on computed tomograms after subarachnoid hemorrhage. Stroke 21:1156–1161CrossRef Hijdra A, Brouwers PJ, Vermeulen M, van Gijn J (1990) Grading the amount of blood on computed tomograms after subarachnoid hemorrhage. Stroke 21:1156–1161CrossRef
16.
Zurück zum Zitat Ibrahim GM, Weidauer S, Macdonald RL (2011) Interobserver variability in the interpretation of computed tomography following aneurysmal subarachnoid hemorrhage. J Neurosurg 115:1191–1196CrossRefPubMed Ibrahim GM, Weidauer S, Macdonald RL (2011) Interobserver variability in the interpretation of computed tomography following aneurysmal subarachnoid hemorrhage. J Neurosurg 115:1191–1196CrossRefPubMed
17.
Zurück zum Zitat 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:E5CrossRefPubMed 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:E5CrossRefPubMed
18.
Zurück zum Zitat 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 42:669–674CrossRefPubMed 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 42:669–674CrossRefPubMed
19.
Zurück zum Zitat 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 128:100–110CrossRefPubMed 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 128:100–110CrossRefPubMed
20.
Zurück zum Zitat 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 138:2608–2618CrossRefPubMedPubMedCentral 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 138:2608–2618CrossRefPubMedPubMedCentral
21.
Zurück zum Zitat 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 907CrossRefPubMed 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 907CrossRefPubMed
22.
Zurück zum Zitat 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 266–257CrossRefPubMed 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 266–257CrossRefPubMed
23.
Zurück zum Zitat Rosengart AJ, Schultheiss KE, Tolentino J, Macdonald RL (2007) Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke 38:2315–2321CrossRefPubMed Rosengart AJ, Schultheiss KE, Tolentino J, Macdonald RL (2007) Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke 38:2315–2321CrossRefPubMed
24.
Zurück zum Zitat 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) 51:187–194CrossRef 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) 51:187–194CrossRef
25.
Zurück zum Zitat 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 85:125–129CrossRefPubMed 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 85:125–129CrossRefPubMed
26.
Zurück zum Zitat 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 73:28–35CrossRefPubMed 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 73:28–35CrossRefPubMed
27.
Zurück zum Zitat 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 155:579–586CrossRefPubMed 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 155:579–586CrossRefPubMed
28.
Zurück zum Zitat 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:e36CrossRefPubMed 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:e36CrossRefPubMed
29.
Zurück zum Zitat 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 61:403–415PubMed 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 61:403–415PubMed
30.
Zurück zum Zitat 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 126:1764–1771CrossRefPubMed 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 126:1764–1771CrossRefPubMed
Metadaten
Titel
Hemorrhagic burden in poor-grade aneurysmal subarachnoid hemorrhage: a volumetric analysis of different bleeding distributions
verfasst von
Pietro Panni
Elisa Colombo
Carmine Antonio Donofrio
Lina Raffaella Barzaghi
Luigi Albano
Claudio Righi
Francesco Scomazzoni
Franco Simionato
Pietro Mortini
Andrea Falini
Nicoletta Anzalone
Publikationsdatum
21.02.2019
Verlag
Springer Vienna
Erschienen in
Acta Neurochirurgica / Ausgabe 4/2019
Print ISSN: 0001-6268
Elektronische ISSN: 0942-0940
DOI
https://doi.org/10.1007/s00701-019-03846-z

Weitere Artikel der Ausgabe 4/2019

Acta Neurochirurgica 4/2019 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Neu im Fachgebiet Neurologie

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.