Successful presurgical endovascular management of venous sinus thrombosis associated with high-grade cerebral arteriovenous malformation: A case report

Abstract

We report a case of a 39-year-old man presenting with a high-grade left parieto-occipital arteriovenous malformation (AVM) complicated by superior sagittal sinus (SSS) stenosis, seven years after the first presentation. Magnetic resonance imaging revealed a newly developed perilesional edema. Venous sinus stenosis acutely progressed to occlusion and induced multiple intracerebral hemorrhages. An emergent balloon venoplasty of the SSS successfully recanalized the thrombosed sinus. Further, multistage transarterial nidus embolization was performed followed by surgical resection, resulting in a complete eradication of the large AVM. The emergence of perilesional edema is a key radiological feature for the early recognition of a newly developed venous drainage route disturbance, which would result in hemorrhagic events. Venous sinus thrombosis is a rare cause of drainage route disturbance in cerebral AVMs. For such cases, the recanalization of venous drainage concomitant with flow reduction by performing transarterial embolization is effective in preventing further hemorrhage, which enables a safe performance of subsequent radical surgery.

Introduction

The surgical indication of unruptured cerebral arteriovenous malformations (AVMs) has been controversial after the A Randomized Trial of Unruptured Brain Arteriovenous Malformations (ARUBA) trial.¹ Surgeons should know the natural history of unruptured cerebral AVMs, when considering surgical indication. A recent study has reported a 3.0% annual hemorrhage rate of unruptured AVMs.² One of the risk factors for further hemorrhages is the stenosis or occlusion of the venous drainage system, which can lead to perilesional brain edema.^3,4 The progression of brain edema is associated with symptoms such as headache, seizure, and neurological deficit. The aggravation of the venous drainage impairment may ultimately lead to ruptured AVMs.⁴ In this study, we report a case of high-grade cerebral AVMs with progressing perilesional edema and hemorrhage because of venous sinus thrombosis that was successfully eradicated using an emergent endovascular treatment followed by surgical resection.

Case report

History

A 32-year-old man originally presented with generalized seizures in 2008. Magnetic resonance imaging (MRI) and cerebral angiography revealed a large, unruptured left parieto-occipital AVM with multiple feeders (Figure 1(a)–(e)). The patient was conservatively managed with annual MRI examinations. Seven years after the first presentation, a routine MRI follow-up revealed a newly emerged T2-hyperintensity lesion adjacent to the nidus (Figure 1(f)). Cerebral angiography revealed a partial thrombosis of the nidus with severe stenosis in the parietal region of the superior sagittal sinus (SSS) and a retrograde flow to the anterior part of the SSS (Figure 1(g)–(k)). While the patient was considering future surgical interventions, he developed generalized seizures and was transferred to our hospital two months after the angiography.

Figure 1.

Axial T2-weighted image showing the large left parieto-occipital arteriovenous malformation (AVM) on the initial presentation (a), arterial phase of the left internal carotid angiography (b), left vertebral angiography (c), and left external carotid angiography (d), showing the nidus fed using multiple feeders. Venous phase of the left internal carotid angiography, showing an antegrade venous drainage to the superior sagittal sinus (SSS) (e). T2-weighted image obtained seven years after the initial presentation, revealing a brain edema adjacent to the nidus (f). Arterial phase of the left internal carotid angiography (g), left vertebral angiography (h), and left external carotid angiography (i), showing a partial thrombosis of the nidus. Venous phase of the left internal carotid angiography (j) and external carotid angiography (k), showing a severe SSS stenosis (arrow) and a retrograde flow to the anterior part of the SSS (arrowhead) (g). The SSS stenosis, located downstream of the entry point of the main draining vein (asterisk).

Examination and operation

On the second admission, the patient was drowsy with right hemiparesis and homonymous inferior quadrantanopia. Computed tomography revealed bilateral distant intracerebral hemorrhages in the right frontal and left parietal lobes (Figure 2(a) and (b)). Cerebral angiography revealed the SSS stenosis progressed to occlusion with a cortical venous reflux (Figure 2(c)). A venous sinus thrombosis was identified as the main cause of venous congestion and hemorrhage, and an emergency sinus venoplasty was performed to prevent further hemorrhage under systemic heparinization. The SSS was recanalized with a balloon percutaneous transluminal venoplasty (PTV) using a 6.0 mm × 30 mm angioplasty balloon (Figure 2(d)). An antegrade venous flow was confirmed at the posterior part of the SSS after performing PTV (Figure 2(e)). Concomitantly, the feeders from the left middle cerebral artery were embolized using an ethylene-vinyl alcohol copolymer liquid embolic system (Onyx; Medtronic, Minneapolis, MN, USA) and N-butyl-2-cyanoacrylate. The patient’s neurological deficits immediately improved after this emergency endovascular treatment. An anticoagulation therapy using heparin was continued for one week after PTV with conversion to warfarin to maintain the patency of the SSS. An additional transarterial embolization of the feeders from the left posterior cerebral artery and left external carotid artery was performed twice for flow reduction. Cerebral angiography after the third endovascular treatment revealed a marked reduction of the shunt flow (data not shown). The day after the third endovascular treatment (two months after the initial endovascular treatment), total removal of the nidus was successfully achieved without complications.

Figure 2.

Computed tomography on the second admission, showing right frontal and left parietal intracerebral hemorrhages ((a) and (b)). Left vertebral angiography (venous phase), showing an occlusion (arrow) in the parietal region of the superior sagittal sinus (SSS) and a cortical venous reflux development (c). The SSS were recanalized by performing an emergency sinus venoplasty ((d) and (e)). Arrowhead indicates an antegrade venous flow to the posterior part of the SSS.

Postoperative course

The patient’s postoperative course was uneventful, and his right hemiparesis gradually improved to an independent status. A postoperative MRI revealed an improved brain edema (Figure 3(a)). A follow-up angiography, performed six months after the surgery, confirmed a complete AVM eradication and no SSS restenosis (Figure 3(b)–(d)). The patient maintained an independent daily life with lower right quadrantanopia and experienced no further hemorrhage during the 12-month follow-up.

Figure 3.

Postoperative T2-weighted image showing an improved edema (a). The follow-up angiography revealed the absence of the arteriovenous malformation ((b) and (c)) and no recurrence of the venous sinus stenosis (d).

Discussion

AVMs and surrounding brain edema

A few cases of brain edema with unruptured AVMs have been reported. A high-intensity brain edema is usually detected adjacent to the nidus in T2-weighted images.⁵ In the series reported by Kim et al., 3.9% of unruptured brain AVMs showed a surrounding brain edema.³ They have described that cerebral angiography revealed venous drainage impairment in 12 out of 13 (92%) AVM cases with brain edema and that the brain edema is caused by venous congestion because of the stenosis or occlusion of a high-flow draining vein.³ The present case showed that the progressive edema formation would be a useful predictor of hemorrhagic transformation. The pattern of hemorrhage in this case was different from that with a direct rupture of AVM. The SSS obstruction increased the venous pressure of the bilateral cerebral hemisphere, resulting in multiple intracerebral hemorrhages. This clinical course is common in a dural arteriovenous fistula;⁶ however, it is rarely reported in AVMs. Although there are few reports regarding the management of unruptured AVM cases with brain edema, surgical treatment may be justified in cases with progressive perilesional edema to prevent further hemorrhages.

Mechanisms of thrombosis

An impaired venous drainage route could be an indication of hemorrhage and spontaneous thrombotic AVM occlusion. The incidence of spontaneous AVM occlusion has been reported to be approximately 1%.^7,8 A single draining vein may play an important causative role in the spontaneous thrombosis phenomenon.⁷ In the present case, the thrombosis of the venous drainage route and nidus spontaneously progressed. Finally, the obstruction of the venous drainage system became dominant, resulting in intracerebral hemorrhage. However, the AVM was not completely occluded because of the presence of an escape drainage route to the anterior SSS. The present single case report cannot explain the exact mechanisms underlying the thrombosis of the nidus or the drainage route. The intimal damage caused by the mechanical action of pressure and shearing stress to the endothelial surface and change in the electrochemical characteristics of the endothelial membrane produced by the flow convective properties were considered to be the initial causes of the subsequent vessel wall hyperplasia, thrombosis, and luminal narrowing.^4,9

Role of endovascular treatment for venous sinus thrombosis

The standard medical treatment for venous sinus thrombosis is heparinization, which includes conversion to low-molecular-weight heparin or oral anticoagulant agents.¹⁰ However, endovascular treatment is considered for patients who are at a high risk of bleeding. Endovascular treatments involving thrombolytic agent infusion,¹¹ balloon angioplasty,¹² stenting,¹³ and, more recently, combined stent retriever and aspiration have been reported.¹⁴ The present case reported a venous sinus thrombosis at the drainage route of a high-flow draining vein in cerebral AVM. Thus, the degree of venous congestion was considered higher than that of spontaneous venous sinus thrombosis, facilitating the performance of an endovascular treatment. Song et al. have reported a similar case with a high-flow pial arteriovenous fistula that developed a high-grade SSS stenosis within a five-year period.⁹ The SSS stenosis was mechanically dilated using a balloon angioplasty and stent placement.⁹ Chen et al. have reported a successful endovascular treatment of an unruptured AVM with increased venous pressure because of a transverse-sigmoid sinus occlusion.¹⁵ They divided the endovascular treatment into two sessions: venous sinus recanalization in the initial session and AVM embolization in the second session.¹⁵ In our case, the SSS aggressively changed from stenosis to occlusion, causing an increased venous pressure followed by bleeding. On the day of hemorrhage, we decided to perform an emergent endovascular treatment. The occluded sinus was successfully recanalized by performing a balloon PTV only, without stent placement or thrombectomy. Emergent radical resection was considered unsuitable because of the large size and complicated structure of the AVM. Thus, flow reduction embolization was simultaneously performed. An additional transarterial embolization of multiple feeders was performed twice for flow reduction within a two-month period after the first endovascular treatment. This approach reduced the risk of further bleeding, which allowed the performance of a safe elective surgery.

Conclusions

The emergence of perilesional edema is a key radiological feature for the early recognition of impaired venous drainage of cerebral AVMs. Venous sinus thrombosis is a rare cause of venous drainage route disturbance in cerebral AVMs. In such cases, venous drainage recanalization concomitant with flow reduction by performing a transarterial embolization is effective in preventing further hemorrhage, which allows the performance of a safe subsequent radical surgery.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.