Skip to main content
Top
Published in: Journal of Neurology 11/2020

01-11-2020 | Subdural Hematoma | Original Communication

Features of intracranial hemorrhage in cerebral venous thrombosis

Authors: K. Afifi, G. Bellanger, P. J. Buyck, S. M. Zuurbier, C. G. Esperon, M. A. Barboza, P. Costa, I. Escudero, D. Renard, R. Lemmens, N. Hinteregger, F. Fazekas, J. Jimenez Conde, E. Giralt-Steinhauer, S. Hiltunen, A. Arauz, A. Pezzini, J. Montaner, J. Putaala, C. Weimar, Marc Schlamann, T. Gattringer, T. Tatlisumak, J. M. Coutinho, P. Demaerel, V. Thijs

Published in: Journal of Neurology | Issue 11/2020

Login to get access

Abstract

Background

Cerebral venous thrombosis (CVT) is associated with intracranial hemorrhage.

Aim

To identify clinical and imaging features of CVT-associated intracranial hemorrhage. We hypothesized that higher clot burden would be associated with a higher risk of intracranial hemorrhage.

Methods

We performed a retrospective analysis of an international, multicenter cohort of patients with confirmed cerebral venous thrombosis who underwent computed tomography within 2 weeks of symptom onset. Clinical and imaging features were compared between patients with and without intracranial hemorrhage. Clot burden was assessed by counting the number of thrombosed venous sinuses and veins on confirmatory imaging.

Results

We enrolled 260 patients from 10 institutions in Europe and Mexico. The mean age was 42 years and 74% were female. Intracranial hemorrhage was found in 102 (39%). Among them parenchymal hemorrhage occurred in 64 (63%), in addition, small juxta-cortical hemorrhage was found in 30 (29%), subarachnoid hemorrhage in 24 (24%) and subdural hemorrhage in 11 (11%). Multiple concomitant types of hemorrhage occurred in 23 (23%). Older age and superior sagittal thrombosis involvement were associated with presence of hemorrhage. The number of thrombosed venous sinuses was not associated with intracranial hemorrhage (median number IQRInterquartile ratio] of sinuses/veins involved with hemorrhage 2 (1–3) vs. 2 (1–3) without hemorrhage, p = 0.4).

Conclusion

The high rate of intracranial hemorrhage in cerebral venous thrombosis is not explained by widespread involvement of the venous sinuses. Superior sagittal sinus involvement is associated with higher bleeding risk.
Literature
1.
go back to reference Ferro JM, Bousser MG, Canhao P et al (2017) European stroke o. european stroke organization guideline for the diagnosis and treatment of cerebral venous thrombosis - endorsed by the european academy of neurology. Eur J Neurol 24:1203–1213PubMedCrossRef Ferro JM, Bousser MG, Canhao P et al (2017) European stroke o. european stroke organization guideline for the diagnosis and treatment of cerebral venous thrombosis - endorsed by the european academy of neurology. Eur J Neurol 24:1203–1213PubMedCrossRef
2.
go back to reference Saposnik G, Barinagarrementeria F, Brown RD et al (2011) American heart association stroke c, the council on e, prevention diagnosis and management of cerebral venous thrombosis: a statement for healthcare professionals from the american heart association/american stroke association. Stroke 42:1158–1192PubMedCrossRef Saposnik G, Barinagarrementeria F, Brown RD et al (2011) American heart association stroke c, the council on e, prevention diagnosis and management of cerebral venous thrombosis: a statement for healthcare professionals from the american heart association/american stroke association. Stroke 42:1158–1192PubMedCrossRef
3.
go back to reference Silvis SM, De Sousa DA, Ferro JM et al (2017) Cerebral venous thrombosis. Nat Rev Neurol 13:555–565PubMedCrossRef Silvis SM, De Sousa DA, Ferro JM et al (2017) Cerebral venous thrombosis. Nat Rev Neurol 13:555–565PubMedCrossRef
4.
go back to reference Rother J, Waggie K, van Bruggen N et al (1996) Experimental cerebral venous thrombosis: evaluation using magnetic resonance imaging. J Cereb Blood Flow Metab 16:1353–1361PubMedCrossRef Rother J, Waggie K, van Bruggen N et al (1996) Experimental cerebral venous thrombosis: evaluation using magnetic resonance imaging. J Cereb Blood Flow Metab 16:1353–1361PubMedCrossRef
5.
go back to reference Sato S, Miyahara Y, Dohmoto Y, Kawase T, Toya S (1983) Cerebral Microcirculation in experimental sagittal sinus occlusion in dogs. In: Auer LM, Loew F (eds) The Cerebral Veins. Springer, Vienna Sato S, Miyahara Y, Dohmoto Y, Kawase T, Toya S (1983) Cerebral Microcirculation in experimental sagittal sinus occlusion in dogs. In: Auer LM, Loew F (eds) The Cerebral Veins. Springer, Vienna
6.
go back to reference Gotoh M, Ohmoto T, Kuyama H (1993) Experimental study of venous circulatory disturbance by dural sinus occlusion. Acta Neurochir (Wien) 124:120–126CrossRef Gotoh M, Ohmoto T, Kuyama H (1993) Experimental study of venous circulatory disturbance by dural sinus occlusion. Acta Neurochir (Wien) 124:120–126CrossRef
7.
go back to reference Schaller B, Graf R, Sanada Y et al (2003) Hemodynamic changes after occlusion of the posterior superior sagittal sinus: an experimental PET study in cats. AJNR Am J Neuroradiol 24:1876–1880PubMed Schaller B, Graf R, Sanada Y et al (2003) Hemodynamic changes after occlusion of the posterior superior sagittal sinus: an experimental PET study in cats. AJNR Am J Neuroradiol 24:1876–1880PubMed
8.
go back to reference Kurokawa Y, Hashi K, Okuyama T et al (1990) Regional ischemia in cerebral venous hypertension due to embolic occlusion of the superior sagittal sinus in the rat. Surg Neurol 34:390–395PubMedCrossRef Kurokawa Y, Hashi K, Okuyama T et al (1990) Regional ischemia in cerebral venous hypertension due to embolic occlusion of the superior sagittal sinus in the rat. Surg Neurol 34:390–395PubMedCrossRef
9.
go back to reference Oppenheim C, Domigo V, Gauvrit JY et al (2005) Subarachnoid hemorrhage as the initial presentation of dural sinus thrombosis. AJNR Am J Neuroradiol 26:614–617PubMed Oppenheim C, Domigo V, Gauvrit JY et al (2005) Subarachnoid hemorrhage as the initial presentation of dural sinus thrombosis. AJNR Am J Neuroradiol 26:614–617PubMed
10.
go back to reference Sztajzel R, Coeytaux A, Dehdashti A et al (2001) Subarachnoid hemorrhage: a rare presentation of cerebral venous thrombosis Headache. J Head Face Pain 41:889–892CrossRef Sztajzel R, Coeytaux A, Dehdashti A et al (2001) Subarachnoid hemorrhage: a rare presentation of cerebral venous thrombosis Headache. J Head Face Pain 41:889–892CrossRef
11.
go back to reference Ferro JM, Canhao P, Stam J et al (2004) Investigators I Prognosis of cerebral vein and dural sinus thrombosis: results of the International Study on Cerebral Vein and Dural Sinus Thrombosis (ISCVT). Stroke 35:664–670PubMedCrossRef Ferro JM, Canhao P, Stam J et al (2004) Investigators I Prognosis of cerebral vein and dural sinus thrombosis: results of the International Study on Cerebral Vein and Dural Sinus Thrombosis (ISCVT). Stroke 35:664–670PubMedCrossRef
12.
go back to reference Fink JN, McAuley DL (2001) Safety of anticoagulation for cerebral venous thrombosis associated with intracerebral hematoma. Neurology 57:1138–1139PubMedCrossRef Fink JN, McAuley DL (2001) Safety of anticoagulation for cerebral venous thrombosis associated with intracerebral hematoma. Neurology 57:1138–1139PubMedCrossRef
13.
go back to reference Pizzi MA, Alejos DA, Siegel JL et al (2016) Cerebral venous thrombosis associated with intracranial hemorrhage and timing of anticoagulation after hemicraniectomy. J Stroke Cerebrovasc Dis 25:2312–2316PubMedCrossRef Pizzi MA, Alejos DA, Siegel JL et al (2016) Cerebral venous thrombosis associated with intracranial hemorrhage and timing of anticoagulation after hemicraniectomy. J Stroke Cerebrovasc Dis 25:2312–2316PubMedCrossRef
14.
go back to reference Coutinho JM, van den Berg R, Zuurbier SM et al (2014) Small juxtacortical hemorrhages in cerebral venous thrombosis. Ann Neurol 75:908–916PubMedCrossRef Coutinho JM, van den Berg R, Zuurbier SM et al (2014) Small juxtacortical hemorrhages in cerebral venous thrombosis. Ann Neurol 75:908–916PubMedCrossRef
15.
go back to reference Takahashi S, Shinoda J, Hayashi T (2012) Cerebral venous sinus thrombosis in an adult patient presenting as headache and acute subdural hematoma. J Stroke Cerebrovasc Dis 21:338–340PubMedCrossRef Takahashi S, Shinoda J, Hayashi T (2012) Cerebral venous sinus thrombosis in an adult patient presenting as headache and acute subdural hematoma. J Stroke Cerebrovasc Dis 21:338–340PubMedCrossRef
16.
go back to reference Girot M, Ferro JM, Canhao P et al (2007) Investigators I Predictors of outcome in patients with cerebral venous thrombosis and intracerebral hemorrhage. Stroke 38:337–342PubMedCrossRef Girot M, Ferro JM, Canhao P et al (2007) Investigators I Predictors of outcome in patients with cerebral venous thrombosis and intracerebral hemorrhage. Stroke 38:337–342PubMedCrossRef
17.
go back to reference Buyck P (2019) Diagnostic accuracy of non-contrast ct imaging markers in cerebral venous thrombosis. Neurology 1:6 Buyck P (2019) Diagnostic accuracy of non-contrast ct imaging markers in cerebral venous thrombosis. Neurology 1:6
18.
go back to reference Dmytriw AA, Song JSA, Yu E et al (2018) Cerebral venous thrombosis: state of the art diagnosis and management. Neuroradiology 1:97 Dmytriw AA, Song JSA, Yu E et al (2018) Cerebral venous thrombosis: state of the art diagnosis and management. Neuroradiology 1:97
19.
go back to reference Barboza MA, Mejias C, Colin-Luna J et al (2015) Intracranial venous collaterals in cerebral venous thrombosis: clinical and imaging impact. J Neurol Neurosurg Psychiatry 86:1314–1318PubMedCrossRef Barboza MA, Mejias C, Colin-Luna J et al (2015) Intracranial venous collaterals in cerebral venous thrombosis: clinical and imaging impact. J Neurol Neurosurg Psychiatry 86:1314–1318PubMedCrossRef
20.
go back to reference Schuchardt F, Hennemuth A, Schroeder L et al (2017) Acute Cerebral venous thrombosis: three-dimensional visualization and quantification of hemodynamic alterations using 4-dimensional flow magnetic resonance imaging. Stroke 48:671–677PubMedCrossRef Schuchardt F, Hennemuth A, Schroeder L et al (2017) Acute Cerebral venous thrombosis: three-dimensional visualization and quantification of hemodynamic alterations using 4-dimensional flow magnetic resonance imaging. Stroke 48:671–677PubMedCrossRef
21.
go back to reference Zhang S, Zhao H, Li H et al (2017) Decompressive craniectomy in hemorrhagic cerebral venous thrombosis: clinicoradiological features and risk factors. J Neurosurg 127:709–715PubMedCrossRef Zhang S, Zhao H, Li H et al (2017) Decompressive craniectomy in hemorrhagic cerebral venous thrombosis: clinicoradiological features and risk factors. J Neurosurg 127:709–715PubMedCrossRef
22.
go back to reference Sahin N, Solak A, Genc B et al (2014) Cerebral venous thrombosis as a rare cause of subarachnoid hemorrhage: case report and literature review. Clin Imaging 38:373–379PubMedCrossRef Sahin N, Solak A, Genc B et al (2014) Cerebral venous thrombosis as a rare cause of subarachnoid hemorrhage: case report and literature review. Clin Imaging 38:373–379PubMedCrossRef
23.
go back to reference Mohri H (1987) Acquired von Willebrand disease in patients with polycythemia rubra vera. Am J Hematol 26:135–146PubMedCrossRef Mohri H (1987) Acquired von Willebrand disease in patients with polycythemia rubra vera. Am J Hematol 26:135–146PubMedCrossRef
24.
go back to reference Murakawa M, Okamura T, Tsutsumi K et al (1992) Acquired von Willebrand's disease in association with essential thrombocythemia: regression following treatment. Acta Haematol 87:83–87PubMedCrossRef Murakawa M, Okamura T, Tsutsumi K et al (1992) Acquired von Willebrand's disease in association with essential thrombocythemia: regression following treatment. Acta Haematol 87:83–87PubMedCrossRef
25.
go back to reference Ferro JM, Lopes MG, Rosas MJ et al (2002) Cerebral venous thrombosis portugese collaborative study G. Long-term prognosis of cerebral vein and dural sinus thrombosis results of the VENOPORT study. Cerebrovasc Dis 13:272–278PubMedCrossRef Ferro JM, Lopes MG, Rosas MJ et al (2002) Cerebral venous thrombosis portugese collaborative study G. Long-term prognosis of cerebral vein and dural sinus thrombosis results of the VENOPORT study. Cerebrovasc Dis 13:272–278PubMedCrossRef
26.
go back to reference Damak M, Crassard I, Wolff V et al (2009) Isolated lateral sinus thrombosis: a series of 62 patients. Stroke 40:476–481PubMedCrossRef Damak M, Crassard I, Wolff V et al (2009) Isolated lateral sinus thrombosis: a series of 62 patients. Stroke 40:476–481PubMedCrossRef
27.
go back to reference Kumral E, Polat F, Uzunkopru C et al (2012) The clinical spectrum of intracerebral hematoma, hemorrhagic infarct, non-hemorrhagic infarct, and non-lesional venous stroke in patients with cerebral sinus-venous thrombosis. Eur J Neurol 19:537–543PubMedCrossRef Kumral E, Polat F, Uzunkopru C et al (2012) The clinical spectrum of intracerebral hematoma, hemorrhagic infarct, non-hemorrhagic infarct, and non-lesional venous stroke in patients with cerebral sinus-venous thrombosis. Eur J Neurol 19:537–543PubMedCrossRef
28.
go back to reference Bansal H, Chaudhary A, Mahajan A et al (2016) Acute subdural hematoma secondary to cerebral venous sinus thrombosis: case report and review of literature. Asian J Neurosurg 11:177PubMedPubMedCentralCrossRef Bansal H, Chaudhary A, Mahajan A et al (2016) Acute subdural hematoma secondary to cerebral venous sinus thrombosis: case report and review of literature. Asian J Neurosurg 11:177PubMedPubMedCentralCrossRef
29.
go back to reference Azeemuddin M, Awais M, Mubarak F et al (2018) Prevalence of subarachnoid haemorrhage among patients with cranial venous sinus thrombosis in the presence and absence of venous infarcts. Neuroradiol J 31:496–503PubMedPubMedCentralCrossRef Azeemuddin M, Awais M, Mubarak F et al (2018) Prevalence of subarachnoid haemorrhage among patients with cranial venous sinus thrombosis in the presence and absence of venous infarcts. Neuroradiol J 31:496–503PubMedPubMedCentralCrossRef
30.
go back to reference Arnoux A, Triquenot-Bagan A, Andriuta D et al (2017) Imaging characteristics of venous parenchymal abnormalities. Stroke 48:3258–3265PubMedCrossRef Arnoux A, Triquenot-Bagan A, Andriuta D et al (2017) Imaging characteristics of venous parenchymal abnormalities. Stroke 48:3258–3265PubMedCrossRef
31.
go back to reference Zhou G, Li M, Zhu Y et al (2016) Cerebral venous sinus thrombosis involving the straight sinus may result in infarction and/or hemorrhage. Eur Neurol 75:257–262PubMedCrossRef Zhou G, Li M, Zhu Y et al (2016) Cerebral venous sinus thrombosis involving the straight sinus may result in infarction and/or hemorrhage. Eur Neurol 75:257–262PubMedCrossRef
Metadata
Title
Features of intracranial hemorrhage in cerebral venous thrombosis
Authors
K. Afifi
G. Bellanger
P. J. Buyck
S. M. Zuurbier
C. G. Esperon
M. A. Barboza
P. Costa
I. Escudero
D. Renard
R. Lemmens
N. Hinteregger
F. Fazekas
J. Jimenez Conde
E. Giralt-Steinhauer
S. Hiltunen
A. Arauz
A. Pezzini
J. Montaner
J. Putaala
C. Weimar
Marc Schlamann
T. Gattringer
T. Tatlisumak
J. M. Coutinho
P. Demaerel
V. Thijs
Publication date
01-11-2020
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 11/2020
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-020-10008-0

Other articles of this Issue 11/2020

Journal of Neurology 11/2020 Go to the issue