Safety and efficacy of the use of large bore intermediate suction catheters alone or in combination for the treatment of acute cerebral venous sinus thrombosis: A multicenter experience

Abstract

Background and purpose

Systemic anticoagulation is the standard treatment for cerebral venous sinus thrombosis (CVST). Several endovascular techniques have been described as salvage therapy for anticoagulation refractory CVST cases. We aim to evaluate the safety and feasibility of endovascular aspiration thrombectomy using the new generation, large bore suction catheters alone or in combination with stentriever devices for the treatment of CVST.

Methods

We collected data on 16 consecutive patients with CVST who received endovascular aspiration thrombectomy at three large academic centers. Second generation reperfusion catheters were used as a large bore suction catheter and advanced to the affected sinus using a coaxial technique. Suction was performed using pump suction. At times, a stentriever was used as an anchor to facilitate advancing the suction catheter and to increase thrombectomy capabilities.

Results

Median decade of age was the 50s and nine patients were women. Fifty percent of the patients had multiple sinuses involved. All patients received systemic anticoagulation prior to endovascular aspiration thrombectomy. The most common reason to pursue endovascular aspiration thrombectomy in CVST patients was deterioration of initial clinical status (10/16). The mean time from admission to endovascular aspiration thrombectomy was 1.5 days (range 0–6 days). Good recanalization was obtained in all patients. There were no major peri-procedural complications. Most patients were discharged to either home or a rehabilitation facility.

Conclusion

Endovascular aspiration treatment using large bore suction catheters for CVST is a safe and feasible approach for the treatment of anticoagulation refractory CVST. Heterogeneity of the clinical and radiological presentation requires further investigation to optimize patient selection before evaluating the efficacy of this technique in larger prospective studies.

Background

Cerebral venous sinus thrombosis (CVST) represents 0.5% of all strokes with a higher prevalence in the developing and under-developed world.^1–3 Systemic anticoagulation is the standard of care despite limited evidence to support its use.^4–6 Approximately 20% of patients with CVST experience neurological decline despite treatment with systemic anticoagulation after admission.^7,8

Endovascular therapy represents an adjunctive modality to systemic anticoagulation in refractory cases.⁹ Its primary goal is to reduce the clot burden, which might lead to better penetration of the anticoagulant and improved venous drainage.^10,11 Over the last decade, neurointerventionalists have employed a variety of endovascular techniques using peripheral and neurological devices to perform effective venous thrombectomy.¹⁰ In this study, we aim to describe a multicenter, initial experience of performing endovascular aspiration thrombectomy (EAT) using second-generation, large bore suction catheters alone or in combination with stentriever devices for the treatment of CVST patients. We report the technical aspects along with the safety profile and efficacy of radiographic recanalization of the technique.

Materials and methods

Study population and data collection

We performed a retrospective analysis of 16 consecutive patients with refractory CVST who received EAT using second-generation large bore suction catheters at three large comprehensive academic stroke centers from January 2017 to June 2018. Second-generation large bore catheters were defined as intermediate catheters with an inner diameter (ID) of 0.060 in. or larger. The diagnosis of CVST was confirmed using magnetic resonance imaging (MRI) plus magnetic resonance venogram (MRV). Refractory CVST was defined as the progression of neurological deficits or altered mental status despite adequate anticoagulation therapy. Catheter selection of the specific large bore catheter or the use of additional devices or intravenous thrombolysis was decided by the institutional neurointerventionalist. The study was approved by the institutional review board at each hospital.

Demographic and clinical data including age, gender, clinical presentation, and details of systemic anticoagulation therapy were collected from electronic medical records review. The reasons for pursuing EAT and time to treatment (time from arrival of the patient to the hospital to beginning of EAT) were also collected. The neurology stroke team at each institution performed daily neurological evaluations. When a neurological deterioration attributed to the CVST disease progression was observed, the neurointerventional team was consulted. Treatment was decided after consensus from both services. The stroke neurology team did not wait to achieve goal PTT in patients on heparin before involving the neurointerventional team to make a decision about EAT.

The principal investigator at each institution (SOG, VS, FS) reviewed MRI/MRV to confirm the CVST diagnosis. Imaging data, including number and extent of sinuses involved and additional imaging features associated with the CVST (presence and type of intracerebral hemorrhages, venous infarcts, venous edema, and mass effect), were collected. Procedural information including anesthesia type, type of venous access, guide and suction catheters, use of microcatheters and stentrievers, intra-sinus thrombolysis, and degree of recanalization were collected from review of the images and operative reports. Complete recanalization was defined as removal of 100% of the clot burden while partial recanalization was removal of 50–99% of the clot burden. Less than 50% removal of the clot burden was defined as incomplete recanalization. Good recanalization rate was either complete or partial recanalization as both achieved the goal of reducing clot burden and increasing the surface area for systemic anticoagulation to work.

Periprocedural complications were defined as stroke, worsening, or new intracranial hemorrhage in follow-up imaging, post-procedural anemia requiring blood transfusion, vascular injury to cervical or femoral vessels, and access site hematoma. All patients underwent a follow-up CT and/or MRI prior to discharge.

Clinical outcome was defined as combination of discharge modified Rankin scale (mRS) and discharge destination: home versus inpatient rehabilitation versus long-term acute care. Good clinical outcome was defined as mRS of ≤3 and discharge to home, as these patients were able to walk unassisted at time of discharge and would potentially improve significantly over time.

Interventional protocol

All patients were treated with intravenous heparin prior to EAT except one, who was treated with low molecular weight heparin. One patient was also on apixaban for chronic CVST. All procedures were performed under general anesthesia. Transfemoral arterial access was obtained in all patients to help perform diagnostic cerebral angiogram. Transfemoral venous access was obtained in 15 patients while 1 patient had transjugular access. A large bore, long sheath catheter was placed directly or through an 8-Fr short sheath for venous access as a guide catheter. Then, a large bore, intermediate, suction catheters with ID of 0.060 in. or greater were placed inside the guide catheter over a 0.035-in. wire and advanced to the proximal affected sinus until the tip was inside the thrombus. Suction was performed using the Penumbra Pump Max and Hi-Flow Aspiration tubing (Penumbra, Alameda, CA). To gain access to the distal affected sinus, a microcatheter over a microwire was introduced inside the intermediate catheter and used to navigate up to the affected sinus. In 8/16 patients, the microcatheter was used to deliver and deploy a stentriever to the distal sinus, which would then work as an anchor to move the large bore, intermediate catheter to and from within the affected sinus, while performing aspiration. Three patients received adjunctive intra-sinus alteplase with one of them continued on alteplase infusion for 24 h through microcatheter in the sinus after initial satisfactory recanalization. The endpoint of the procedure was to achieve at least partial recanalization of major venous sinus to re-establish the antegrade flow of major venous sinus.

Results

Clinical characteristics

Median decade of age of the cohort was 52.5 years and 43% were men. Four patients had thrombosis of just one sinus (two had transverse sinus involvement with contralateral hypoplastic sinus and two had occlusion of superior sagittal sinus), five patients had thrombosis of two sinuses, and the rest had multiple sinuses involved. Three patients exhibited extension of the thrombosis into the deep venous system. At least two sinuses were involved in 75% of the patients. Five patients had intraparenchymal hemorrhage (IPH), four patients had venous infarctions, three had global cerebral edema, one patient had associated subarachnoid hemorrhage (SAH), another had associated subdural hemorrhage, and one patient had both SAH and IPH. Out of these patients, one required decompressive hemicraniectomy and another two required use of hypertonic solutions for management of mass effect. Reasons to pursue EAT in CVST patients were worsening clinical exam in 10 patients, persistent severe symptoms after 24 h of anticoagulation in three patients, status epilepticus in two patients, and hemorrhagic lesion with mass effect in one patient. The median time to EAT was 1 day after admission (IQR 0–2 days). The mean time to EAT was 1.5 days after admission (range 0–6 days) (Table 1).

Table 1.

Clinical characteristics of the cohort.

	Age	Sex	Sinuses	ADDL imaging features	Anticoag	Reason for EAT	Time to EAT from admission
Patient 1	29	F	TS	SAH	Heparin	Persistent symptom	1 day
Patient 2	65	M	SSS, TS, IJV, CV	Venous infarct	Heparin	Persistent AMS	Same day
Patient 3	28	F	SSS, TS	IPH	Heparin	Persistent symptom	Same day
Patient 4	56	M	SSS, STR-S, TS, SS	IPH	Heparin	HGIC lesion with mass effect	4 days
Patient 5	60	F	SSS, ISS, STR-S. TOR, B-TS, SS, IJV	Venous edema	LMWH	Worse AMS and blindness	2 days
Patient 6	57	M	SSS, TS, SS, IJV	IPH, mass effect	Heparin	Worse AMS	Same day
Patient 7	18	F	SSS, CV, TS, SS, IJV	Venous infarct	Heparin	Status epilepticus	1 day
Patient 8	34	M	SSS, TS, SS, IJV	Venous infarct	Heparin	Status epilepticus	6 days
Patient 9	27	F	SSS, CV	Venous edema, mass effect	Heparin	Worse AMS due to mass effect	1 day
Patient 10	77	F	SSS, STR-S, ICV, VoG	Venous infarct	Heparin	Worse AMS	Same day
Patient 11	53	M	SSS	SDH	Heparin	Worse exam	2 days
Patient 12	52	F	TS	None	Apixaban	Worse HA	N/A
Patient 13	12	M	SSS, TS	Subdural empyema	Heparin	Worse exam	1 day
Patient 14	75	F	TS, SS	Venous edema, IPH	Heparin	Worse exam	2 days
Patient 15	85	F	SSS, TS	IPH	Heparin	Worse exam	1 day
Patient 16	27	M	SSS	SAH, IPH	Heparin	Worse exam	1 day

TS: transverse sinus; SSS: superior sagittal sinus; IJV: internal jugular vein; CV: cortical vein; STR-S: straight sinus; SS: sigmoid sinus; TOR: torcula; ICV: internal cerebral vein; VoG: vein of Galen; SAH: subarachnoid hemorrhage; IPH: intraparenchymal hemorrhage; SDH: subdural hemorrhage; LMWH: low molecular weight heparin; ADDL: additional; EAT: endovascular aspiration thrombectomy.

Endovascular technique

Neuron Max 0.088 in (Penumbra, Alameda, CA) was used as the large bore, long sheath in the majority of the patients. The ACE 60–68 Reperfusion catheters (13/15) (Penumbra, Alameda, CA) were the most commonly used large bore, intermediate suction catheters. Other large bore suction catheters included Sofia (ID 0.071 in.) (MicroVention, Aliso Viejo, CA), Catalyst 6 (ID 0.060 in.) (Stryker, Fremont, CA) and ARC (ID 0.061 in.) (Medtronic, Irvine, CA). In patients in whom a stentriever was used as an anchor for the intermediate catheter (N = 7), a microcatheter and Solitaire 6 × 30 mm stentriever (Medtronic, Irvine, CA) were used in combination. A Penumbra 3D revascularization device (Penumbra, Alameda, CA) was used in one patient (Figure 1). One patient had continuous alteplase infusion for 24 h through microcatheter in the sinus after recanalization was achieved (Table 2).

Figure 1.

Penumbra 3D device (arrowheads) deployed in anterior sagittal sinus acting as anchor while the large bore Penumbra ACE 68 catheter (arrows) goes back and forth and acts as suction catheter to remove clot.

Table 2.

Technical considerations and outcomes.

	Anesthesia	Access	Guide catheter	Suction catheter	Microcatheter/ stentriever	IST	Recan	Periproc complications	Discharge	Discharge MRS
Patient 1	Gen	Fem	Neuron max	Ace 64	None	None	Comp	None	Home	2
Patient 2	Gen	Jug	Neuron max	Ace 64	None	None	Comp	Anemia REQ BLD TX	Home	3
Patient 3	Gen	Fem	Cook shuttle	Ace 60	Renegade	None	Partial	None	Home	3
Patient 4	Gen	Fem	Cook shuttle	Ace 60	3MAX	None	Partial	None	Ac-Rehab	4
Patient 5	Gen	Fem	Neuron max	Ace 64	3MAX	None	Partial	None	Home	1
Patient 6	Gen	Fem	Neuron max	Ace 60	3MAX	Tpa (24 h)	Partial	None	Dead	6
Patient 7	Gen	Fem	Neuron max	Ace 60	3MAX	Tpa	Partial	None	Home	1
Patient 8	Gen	Fem	Neuron max	Ace 60	3MAX	Tpa	Partial	None	Home	0
Patient 9	Gen	Fem	Cook shuttle	Ace 60	Marksman/ solitaire	None	Partial	None	Ac-Rehab	1
Patient 10	Gen	Fem	Cook shuttle	Sofia	Marksman/ solitaire	None	Partial	None	LTAC	5
Patient 11	Gen	Fem	Cook shuttle	Arc	Marksman/ solitaire	None	Partial	None	Ac-Rehab	4
Patient 12	Gen	Fem	Asahi fubuki	Catalyst 6	Marksman/ solitaire	None	Partial	None	Home	2
Patient 13	Gen	Fem	Neuron max	Catalyst 6/ace 64	Marksman/ solitaire	None	Partial	None	Home	2
Patient 14	Gen	Fem	Cook shuttle	Ace 64	Marksman/ solitaire	None	Partial	Repeat RX	LTAC	5
Patient 15	Gen	Fem	Neuron max	Ace 64	Marksman/ solitaire	None	Partial	None	LTAC	4
Patient 16	Gen	Fem	Neuron max	Ace 68	Penumbra 3D 4.5 mm	None	Partial	None	AcRehab	4

IST: intrasinus thrombolysis; Recan: recanalization; GEN: general anesthesia; FEM: transfemoral access; JUG: transjugular access; TPA: Alteplase; RX: treatment; AcRehab: inpatient acute rehabilitation; LTAC: long-term acute care facility.

Radiological and clinical outcomes

Complete recanalization was obtained in two patients and partial recanalization in the remaining patients (Figure 2). There were no major peri-procedural complications. One patient required blood transfusion due to anemia the day after the procedure and another needed repeat EAT. The median amount of aspirated blood was 450 cc (IQR 150 cc). Eight patients were discharged to home, four patients to inpatient rehabilitation facilities, three patients to long-term acute care facilities, and one patient died after failing to improve from initial coma. Nine patients had good clinical outcome with mRS of 0–3 at discharge from hospital and discharge to home.

Figure 2.

Occluded superior sagittal and right transverse sinuses in Patient 15 seen on PA view (Panel A) and lateral view (Panel B) DSA. Post EAT, good recanalization of both sinuses visualized on PA view (Panel C) and lateral view (Panel D) DSA.

Discussion

CVST is a rare cause of stroke in the developed world, and thus the best management of the disease remains ill defined.^1–3 Based on the International Study on Cerebral Vein and Dural Sinus Thrombosis data, anticoagulation remains the mainstay treatment for most patients with CVST.⁸ A recent metanalysis by Siddiqui et al.¹⁰ demonstrated the safety of endovascular therapy for treatment of CVST, though the sheer variety of techniques and devices used demonstrate the lack of consensus over the approach. More importantly, early selection criteria of patients that might benefit for endovascular therapy remain unknown. Most commonly, patients undergo endovascular therapies when they are sick and/or have had a trial of being on systemic anticoagulation for some time, delaying time to treatment.¹⁰ In other instances, such as in patients with impending transtentorial herniation, achievement of good recanalization through endovascular therapy may not be the right answer to prevent death since those patients may benefit from emergent decompressive hemicraniectomy first.^12,13

Over the last decade, a variety of endovascular therapies have reported different rates of safety, efficacy, and procedure cost.^7,10 Balloon angioplasty was one of the first techniques to be described. It involves inflating intracranial or coronary balloons inside the sinus distally and dragging it back, thus breaking up the clot burden.⁹ The most worrisome adverse outcome is pulmonary embolism due to the lysed clot travelling down the internal jugular vein to the superior vena cava and onto the pulmonary circulation. Dowd et al.¹⁴ used AngioJet (Boston Scientific, Marlborough, MA) for the first time along with intra-sinus thrombolysis. Since then, it has been used separately or in combination with balloon angioplasty. AngioJet is a bulky, stiff device with only a 55% recanalization rate. Furthermore, the use of AngioJet has been associated with a lower chance of good functional outcome (odds ratio 0.5 {0.2–1.0}) and higher risk of complications (odds ratio 2.3 {1.2–4.6}). Other devices that have frequently been used include wire with microsnare or distal protection devices.

Choulakian et al.¹⁵ reported the earliest experience using first-generation, large bore suction catheters for lysing cerebral venous thrombosis in four patients. All cases were treated with the Penumbra 0.41 catheters. Simultaneous use of matching separator wires to prevent clogging and balloon angioplasty was required in three cases to augment thrombolysis. Siddiqui et al.¹⁶ reported their experience with the use of Penumbra 0.54 catheters for the treatment of CVST. Since then, larger size second-generation suction catheters with better trackability, support, and suction properties have been developed. The larger internal diameter of these catheters also allows for stronger thrombo-aspiration, potentially effecting more rapid sinus recanalization. The same catheter can be used for local tPA infusion and thrombo-aspiration, minimizing the need for re-catheterization and use of adjunctive devices like separator wires and balloon angioplasty. In our usage of all the available second-generation, large bore catheters at the time of the study, we have demonstrated 100% good recanalization rate with minimal safety concerns. One patient developed periprocedural acute anemia without hemodynamic compromise requiring blood transfusion and another required repeat EAT due to re-accumulation of significant clot burden. In addition, we observed that the addition of a stentriever as an anchor for delivery of the intermediate catheters might enhance the thrombectomy efficacy by decreasing the blood loss and duration of the procedure.

Anticoagulation was continued in all patients as we believe that EAT is an adjunctive therapy to help reduce clot burden, improve drainage, and prevent venous outflow obstruction in large sinuses. However, anticoagulation is probably still needed to prevent further clot expansion and treat endovascular inaccessible territories such as the cortical thrombosed veins or deep venous system. If performed early enough in the disease process, it may even avoid the need for decompressive hemicraniectomy, which usually leads to interruption of systemic anticoagulation.

Limitations

Since this is a retrospective study, there are inherent biases and limitations with data collection and analysis of our study. The data regarding risk factors for CVT in the individual patients was not available for analysis. Since the stroke neurology team did not wait for PTT to be therapeutic in all cases before consulting for endovascular intervention but based this decision on their clinical judgment, this could be source of bias for patient selection. Although our cohort did not encounter previously described complications such as access site hematoma, soft tissue infections, iatrogenic arteriovenous fistula formation, and peripheral nerve injuries, we did not objectively evaluate for others such as the incidence of pulmonary embolism. The lack of pre-CVT and 30-day follow-up mRS data does limit the interpretation of clinical outcome analysis of our study. Also, the interpretation of efficacy of the technique is limited by the lack of data on radiation exposure, which have traditionally had longer procedure times compared to arterial thrombectomy. The fluoroscopic times and dose were not collected as the procedures were performed across multiple institutions on many different machines, thus making comparison difficult. Our small sample size and heterogeneity of endovascular techniques limit our ability to objectively evaluate the efficacy of this therapy. More importantly, the efficacy might be confounded by the lack of standardized selection criteria and timing of the therapy.

Conclusion

CVST is a disease with potential for high morbidity and mortality in a subgroup of young patients. Anticoagulation is the current standard of care, but more aggressive therapies, such as EAT, may be of benefit in select cases. Our study suggests that EAT using second-generation suction catheters in combination with stentrievers is reasonably safe in the majority of cases. Controlled prospective studies are required to provide consistent data on the safety and efficacy of EAT in patients with CVST. However, it is imperative to better stratify high risk CVST patients requiring EAT and define the therapeutic window of EAT before testing this therapy in a randomized clinical trial.

Authors’ contribution

Conception and design: SD, SOG. Acquisition, Analysis and Interpretation of data: SD, UK, BZ, VS. Statistical analysis and data interpretation: SD, FS, SOG. Drafting of the article: SD. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Administrative/technical/material support: SOG. Study supervision: SOG.

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 disclosed receipt of the following financial support for the research authorship, and/or publication of this article: This work was supported by 2018 Society of Vascular and Interventional Neurology Pilot Research Grant.