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• 2x higher chance for a mRS 0-2 and 7x more likely to recanalize* * Adjusted value odds ratio (95% CI) for “no intracranial occlusion on follow-up CT angiography” in the intervention group versus the control group was 6.88 (4.34 to 10.94). Values were adjusted for age, NIHSS at baseline, time from onset to randomization, status with respect to previous stroke, atrial fibrillation, diabetes mellitus and occlusion of the ICAT. Data for follow-up CT angiography were not available for 106 patients. 1

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Original article

Neurological recovery after coma related to diffuse cerebral venous sinus thrombosis. Interest in thrombi-aspiration with Penumbra system

Interventional Neuroradiology 2015, Vol. 21(2) 218–221 ! The Author(s) 2015 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/1591019915582000 ine.sagepub.com

Florent Gariel1, Jerome Berge2 and Vincent Dousset3

Abstract We report a young man with a history of deep coma secondary to an extensive superior sagittal sinus thrombosis despite full systemic anticoagulation. Endovascular treatment combining a 5 Max ACE reperfusion catheter (Penumbra) and Solitaire (Covidien) retrieval device permitted revascularization of the superior sagittal sinus with restoration of anterograde venous flow. This treatment led to the disappearance of cytotoxic edema on MRI and to a neurological improvement with a modified Rankin scale score of 2 after two months. Our experience shows that this technique provides a useful and safe tool after failure of anticoagulation in cerebral venous sinus thrombosis.

Keywords Cerebral venous sinus thrombosis, endovascular treatment, aspiration catheter, thrombi-aspiration

Introduction Cerebral venous sinus thrombosis is an uncommon and often unrecognized type of stroke that affects approximately five individuals per million annually and accounts for 0.5% to 1% of all strokes.1,2 First-line treatment is based on systemic full anticoagulation.2 Endovascular treatment is accepted as second-line treatment after failure of anticoagulation or in case of contraindication.3 New thrombectomy devices such as the Penumbra aspiration system and Solitaire retrieval device have shown efficacy and safety for arterial recanalization in acute ischemic stroke. We report in this case the benefits and efficacy of such devices for venous recanalization in cerebral venous sinus thrombosis.

Case presentation A 46-year-old man without medical history was admitted in emergency for coma and three left-sided lateralized seizures. Non-contrast head computed tomography (CT) showed multiple intra-axial hematomas associated with a high density of longitudinal superior sinus. Magnetic resonance imaging (MRI) confirmed thrombosis of the longitudinal superior sinus extended to cortical veins, right lateral and sigmoid sinuses. Moreover there was a bilateral frontoparietal cytotoxic edema with localized hemorrhages (Figure 1). There was no midline shift or signs of impending herniation.

The patient was admitted in intensive care under general anesthesia and best medical treatment with anticoagulation (continuous intravenous heparinization) and antiepileptics (clonazepam). There was no clinical improvement (persistent refractory seizures and no improvement of coma). Seventy-two hours later, sedation was stopped despite best medical treatment. After a multidisciplinary discussion among anesthesiologists, neurologists and interventional neuroradiologists, it was decided to attempt endovascular thrombectomy. Diagnosis angiography was performed by injection of both internal carotids (4 French diagnosis catheter). Complete occlusion of the longitudinal superior sinus was demonstrated, extending to the transverse sinus, sigmoid sinus and proximal part of the internal jugular vein. This thrombosis was not extended to the cortical veins. The venous drainage of both cerebral 1

Department of Diagnostic and Therapeutic Neuro-Imaging, CHU de Bordeaux, France 2 Department of Diagnostic and Therapeutic Neuro-Imaging, CHU de Bordeaux, France 3 Department of Diagnostic and Therapeutic Neuro-Imaging, CHU de Bordeaux, University of Bordeaux, France Corresponding author: Florent Gariel, Department of Diagnostic and Therapeutic Neuro-Imaging, CHU de Bordeaux, 16 Place Ame´lie Raba Le´on, 33000 Bordeaux, France. Email: [email protected]

Gariel et al.

219

Figure 1. Initial MR exam, axial FLAIR (a), diffusion (b) and ADC (c). Flair sequence showing bilateral hyperintensity, small petechial hemorrhages and subarachnoidal hemorrhage. Cytotoxic edema was affirmed by diffusion sequence (restricted diffusion). MR: magnetic resonance; FLAIR: fluid-attenuated inversion recovery; ADC: apparent diffusion coefficient.

Figure 2. Subtracted lateral view of the left internal carotid artery angiogram confirming complete occlusion of superior sagittal sinus but residual slow opacification of cortical veins.

hemispheres was provided by both cavernous sinuses via cortical venous anastomosis. This veno-occlusive state was associated with a delayed venous transit time (Figure 2). The only last chance was to propose an endovascular approach to provide a mechanical reopening of the intracranial dural venous system. A 6 French NEURONMAX (Penumbra, Alameda, CA, USA) long sheath was introduced and positioned in the cervical common jugular vein. A coaxial 5 Max ACE reperfusion catheter (Penumbra) was carefully navigated up to the anterior third of the superior sagittal sinus (Figure 3) over a 0.35 guidewire (Terumo, Japan). This required slow progression to avoid any wall perforation or engagement of a cortical vein passage. Several retrieval passes were necessary under continuous aspiration within the 5 Max ACE to collect large amounts of black thrombus. We obtained a progressive recanalization of the superior sagittal sinus and of the right transverse sinus. A further attempt was performed with a clot retrieval device to optimize the clearance of the superior sagittal sinus. A Solitaire 6  30 mm stentriever (Covidien, Neurovascular, Irvine, CA, USA) was deployed in the anterior third

Figure 3. Unsubtracted anteroposterior and lateral view of the head showing transvenous access across the jugular bulb-sigmoid sinus with a coaxial system consisting of a 6F Neuronmax with telescoping 5 Max ACE reperfusion catheter (Penumbra) placed along the distal transverse sinus. The 5 Max ACE catheter was navigated over a 0.035 Terumo guidewire into the superior sagittal sinus.

of the superior sagittal sinus and pulled twice into the 5 Max ACE, each time retrieving large amounts of black clot. The final angiogram showed recanalization of the superior sagittal sinus and right transverse sinus on their entire length but with only partial opening of the sinuses lumen. On bilateral carotid opacification, venous drainage was normalized with an anterograde flow in the superior sagittal sinus in both transverse sinuses and jugular veins (Figure 4). Interestingly, reopening of the sinuses was immediately followed by recovery of anterograde flow in all the hemispheric cortical veins. The procedure was realized under full anticoagulation (heparin, anti-Xa activity between 0.3 and 0.6) and will be followed by six months of oral anticoagulation (Coumadine). Following further examination, no biologic etiology was identified to explain this prothrombotic state. The patient was extubated six days after intervention. There were no more seizures and he experienced

220 a rapid neurological recovery with only a residual left arm paresthesia at day 10. MRI at five days found a partial recanalization of the superior sagittal sinus, right transverse sinus and right internal jugular vein. Bilateral frontoparietal edema nearly completely disappeared except for a small right frontal lesion (Figure 5). Modified Rankin scale score at two months was 2 with minimal left arm weakness (3/5) left with ongoing rehabilitation.

Discussion We know from Coutinho et al.4 that cerebral venous thrombosis (CVT) may have a worse prognosis in men than women with, respectively, complete recovery in 71% instead of 81%. MRI is the most accurate exam for the purpose of CVT diagnosis and its complications. Indeed MRI diagnosis is required to differentiate vasogenic from cytotoxic edema. Management of cerebral venous sinus thrombosis includes anticoagulation

Figure 4. Subtracted lateral view of left internal carotid artery angiogram demonstrating superior sagittal sinus recanalization on its total length and recovery of anterograde flow in the cortical veins.

Interventional Neuroradiology 21(2) therapy, epilepsy treatment and treatment of the underlying condition. There is no doubt that heparin therapy remains the first-line treatment.5 If clinical deterioration occurs despite systemic anticoagulation, interventional therapies may be considered according to American Heart Association (AHA) guidelines.6 Many invasive techniques have been described to treat CVT as a second-line treatment of cerebral venous sinus thrombosis after failed systemic anticoagulation. These cases suggest that invasive therapies such as a combined and successive use of the Penumbra aspiration system and Solitaire retrieval device should be considered during the same procedure to maximize the result. The goal of such invasive and potentially iatrogenic navigation is to retrieve large amounts of wall-adherent clots. Intracranial hemorrhage is not a contraindication for these techniques, whereas we would hesitate to use intra-sinus fibrinolytic drugs or anti-GP2B3A inhibitors like in the Coutinho series.7 This flow restoration may be prevented from worsening and the need for decompressive surgery.8 There are no results of randomized controlled trials to prove benefits of such techniques compared with anticoagulation or with each other. Results of the Thrombolysis or Anticoagulation for Cerebral Venous Thrombosis (TO-ACT) trial will have a major effect on the care of CVT.4 Neurologic deterioration despite systemic anticoagulation reflects vasogenic edema  cytotoxic edema related to venous obstruction. In that case, direct intravenous thrombo-aspiration can achieve complete venous recanalization and restore anterograde venous flow. These physiopathologic improvements can avoid vasogenic edema worsening and further venous stroke. In our experience, it was not necessary to catheterize cortical vein orifices to restore anterograde flow, limiting in this way potential injuries of the venous wall. Effective recanalization is made possible through new-generation devices. Easier venous distal access

Figure 5. MR exam five days after endovascular treatment (FLAIR (a), diffusion (b) and ADC (c)) showing resolutive cytotoxic edema and persistent hemorrhages (petechial and subarachnoidal). MR: magnetic resonance; FLAIR: fluid-attenuated inversion recovery; ADC: apparent diffusion coefficient.

Gariel et al. can be obtained with new-generation catheters such as the 5 Max ACE reperfusion catheter, which offers easy navigation and the possibility of high-flow aspiration. Flow restoration after endovascular procedure is the only way, in the absence of medical treatment efficiency, to provide an optimal diffusion of intravenous heparin within the clot and so on to permit permanent venous flow improvement. Unlike arterial stroke, initial normal, increased and decreased apparent diffusion coefficient (ADC) values have been describe in CVT. Pathophysiology of decreased ADC value is different according to arterial or venous stoke. Decreased ADC in abnormal brain areas associated with CVT might not have the same prognostic value as those associated with pure arterial stroke. Initial decreased ADC values can be reversible.9 We have found this procedure to be highly efficacious and without complications. This technique provides a useful tool after failure of anticoagulation in cerebral venous sinus thrombosis.

Conclusion Our experience shows that cerebral sinuses thrombectomy by using the Penumbra aspiration system combined with the Solitaire retrieval device offers an effective and safe complement for CVT in case of failed systemic anticoagulation. These techniques could even become the first-line treatment in cases of rapid clinical worsening with brain swelling on MRI. Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Conflict of interest JB (2nd author) is consultant for Penumbra (Alameda, California, USA).

221 References 1. Coutinho JM, Ferro JM, Canha˜o P, et al. Cerebral venous and sinus thrombosis in women. Stroke 2009; 40: 2356–2361. 2. Bousser MG and Crassard I. Cerebral venous thrombosis, pregnancy and oral contraceptives. Thromb Res 2012; 130(Suppl 1): S19–S22. 3. Raychev R, Tateshima S, Rastogi S, et al. Successful treatment of extensive cerebral venous sinus thrombosis using a combined approach with Penumbra aspiration system and Solitaire FR retrieval device. J Neurointerv Surg 2014; 6: e32. 4. Coutinho JM, Ferro JM, Zuurbier SM, et al. Thrombolysis or anticoagulation for cerebral venous thrombosis: Rationale and design of the TO-ACT trial. Int J Stroke 2013; 8: 135–140. 5. Ferro JM, Canha˜o P, Stam J, et al. Prognosis of cerebral vein and dural sinus thrombosis: Results of the International Study on Cerebral Vein and Dural Sinus Thrombosis (ISCVT). Stroke 2004; 35: 664–670. 6. Saposnik G, Barinagarrementeria F, Brown RD Jr, et al. Diagnosis and management of cerebral venous thrombosis: A statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2011; 42: 1158–1192. 7. Coutinho JM, Seelig R, Bousser MG, et al. Treatment variations in cerebral venous thrombosis: An international survey. Cerebrovasc Dis 2011; 32: 298–300. 8. Ferro JM, Crassard I, Coutinho JM, et al. Decompressive surgery in cerebrovenous thrombosis: A multicenter registry and a systematic review of individual patient data. Stroke 2011; 42: 2825–2831. 9. Ducreux D, Oppenheim C, Vandamme X, et al. Diffusionweighted imaging patterns of brain damage associated with cerebral venous thrombosis. Am J Neuroradiol 2001; 22: 261–268.

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