Suction thrombectomy after balloon maceration for dural venous sinus thrombosis

Suction thrombectomy after balloon maceration for dural venous sinus thrombosis

Journal of the Neurological Sciences 365 (2016) 76–81 Contents lists available at ScienceDirect Journal of the Neurological Sciences journal homepag...

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Journal of the Neurological Sciences 365 (2016) 76–81

Contents lists available at ScienceDirect

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Suction thrombectomy after balloon maceration for dural venous sinus thrombosis Chung-Wei Lee a,b, Hon-Man Liu b,⁎, Ya-Fang Chen b, Yen-Heng Lin b, Jaw-Lin Wang a a b

Institute of Biomedical Engineering, National Taiwan University, Taiwan, ROC Department of Medical Imaging and Radiology, Hospital and Medical College, National Taiwan University, Taipei, Taiwan, ROC

a r t i c l e

i n f o

Article history: Received 20 January 2016 Received in revised form 17 March 2016 Accepted 31 March 2016 Available online 11 April 2016 Keywords: Dural venous sinus thrombosis Suction thrombectomy Balloon maceration

a b s t r a c t Purpose: To introduce the combination of suction thrombectomy (ST) and balloon maceration (BM) for the management of dural venous sinus thrombosis (DVST). Materials and methods: Ten consecutive patients (average age, 53 ± 15 years; range, 30 to 73 years) with DVST treated by ST after BM were evaluated including location of DVST, imaging presentation, procedural findings, and 3-month modified Rankin scale (mRS). Results: All 10 patients had evidence of venous infarct on MR or CT. In addition, seven patients had intracerebral hemorrhage (ICH), one had subarachnoid hemorrhage (SAH), and one had both ICH and SAH. More than one sinus was involved in nine patients. ST after BM was technically successful in all patients, and angiographic relief of venous congestion and good outcome (3-month mRS 0 or 1) was achieved in eight patients (80%). The average procedural time was 73.5 ± 24.7 min. Two patients who were in coma status had negative outcomes, and one had a known chronic thrombotic segment refractory to treatment. No recurrent thrombosis of recanalized sinus was found on follow-up MR venography in six patients and CT venography in two patients. Conclusion: BM followed by ST is a promising technique for the treatment of acute DVST. © 2016 Elsevier B.V. All rights reserved.

1. Introduction Dural venous sinus thrombosis (DVST) has an incidence of approximately 1.2–1.3 per 100,000 per year [1,2], and contributes to approximately 0.5% of all strokes [3]. The International Study on Cerebral Vein and Dural Sinus Thrombosis (ISCVT) meta-analysis showed a 15% overall death or dependency rate with 4% death rate in the acute phase [4]. The presentation of DVST varies from headaches to severe neurological deficits, and the majority of patients have good outcomes [5]. The mainstay therapy for DVST is heparin or low molecular weight heparin (LMWH) [5–10], even in cases with intracranial hemorrhage [7,11], as recommended by international guidelines [10]. Thrombolytic Abbreviations: APS, antiphospholipid syndrome; aPTT, activated partial thromboplastin time; BM, balloon maceration; CVC, central venous catheter; CVST, cerebral venous sinus thrombosis; DVST, Dural venous sinus thrombosis; ET, endovascular treatment; GC, guiding catheter; GCS, Glasgow coma scale; ICH, intracerebral hemorrhage; IICP, increased intracranial pressure; INR, international normalized ratio; ISCVT, International Study on Cerebral Vein and Dural Sinus Thrombosis; LMWH, low molecular weight heparin; LT, local thrombolysis; mRS, modified Rankin scale; MT, mechanical thrombectomy; OCP, oral contraceptive pill; PE, pulmonary embolism; SAH, subarachnoid hemorrhage; SS, sigmoid sinus; SSS, superior sagittal sinus; ST, suction thrombectomy; StS, straight sinus; TS, transverse sinus; VI, venous infarction. ⁎ Corresponding author at: Department of Medical Imaging, National Taiwan University Hospital, 7, Chung-Shan South Road, Taipei, 10016, Taiwan, ROC. E-mail address: [email protected] (H.-M. Liu). 0022-510X/© 2016 Elsevier B.V. All rights reserved.

treatment in patients with poor response to anticoagulant therapy may help, but still carries a risk of hemorrhage [10,12–16], and may require continuous infusion [17]. Recent treatments have involved mechanical thrombectomy (MT) with or without (+/−) local thrombolysis (LT) [18]. A review in 2009 revealed that most of these reports have used a combination of MT and LT, with rheolytic catheters and balloon angioplasty used roughly equally [19]. In a more recent review of 185 patients, mechanical thrombectomy was suggested as reasonably safe and the rate of good outcomes was 84% [20]. A large proportion (71%) of the patients were treated with combination MT and LT [20]. Another report demonstrated higher procedural complication rates in MT ± LT group than in LT group [21]. However, the most commonly used device was the AngioJet (Boston Scientific Corporation, USA) which may be associated with a higher complication rate [20,21]. To date, there is no endovascular device specifically designed to treat DVST. Some reports of DVST cases treated with MT +/- LT used rheolytic catheters that were initially designed for treatment of peripheral or coronary thrombosis [19–22], and more recent reports used devices normally used for acute ischemic stroke [23–24]. The use of a combination of off-label devices has been frequently reported [20,21,24] and no comparison between new devices has been attempted. Although most case reports and small series have demonstrated a high percentage of positive outcomes, publication bias is a concern. Technical or clinical failures are often not reported and, thus, the results

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should be interpreted with caution [19]. There is currently no large series using MT alone as the main treatment protocol, since combined treatment was used in many cases and series [20]. The purpose of this study was to introduce a single-institute experience in treating DVST with suction thrombectomy (ST) after balloon maceration (BM).

2. Materials and methods This study was approved by our institute’s internal ethical review board. From January 2008 to April 2015, consecutive patients with DVST treated in the angiography suite were retrospectively reviewed. During this period, BM and ST with or without LT were performed. DVST was diagnosed by MR venography (MRV) or CT venography (CTV). The treatment policy deviated from international guidelines [10]. Medical treatment with anticoagulation is the first-line treatment. Endovascular treatment is indicated in patients with intracranial hemorrhage, deep venous involvement, coma, or failed medical treatment. The patient profiles, associated risks of DVST, lesion locations, imaging findings, pre-procedure conditions (major symptoms other than headache, Glasgow coma scale (GCS), type and result of treatment, complications, procedural times, and modified Rankin scale (mRS) at 3 months were recorded.


2.1. Suction thrombectomy The procedure was performed under general anesthesia. Both arterial and venous approaches were transfemoral. A 5 Fr angiographic catheter (H1, Cook, USA) was used for arteriography. Venous access included a combination of a long sheath (6 Fr or 7 Fr Shuttle sheath, Cook, USA), a 6 Fr guiding catheter (GC) (Envoy MPC, Cordis, Mexico; or Neuron 070, Penumbra, USA), a 5 Fr diagnostic catheter (H1, 125 cm, Cook, USA), and a microcatheter (Progreat, Terumo, Japan) in a tri-axial or tetra-axial pattern. Cerebral 3-vessel arteriography was initially performed to evaluate the cerebral venous drainage. After determining the location and extent of the occlusion and the existing collaterals, the venous long sheath was advanced to the upper portion of internal jugular vein on the lesion side (Fig. 1). With manipulation of the guidewire (Guidewire M, Terumo, Japan) or microcatheter plus micro guidewire, the complex of angiographic catheter and 6 Fr GC was navigated into the sigmoid sinus. The GCangiography catheter complex was then advanced into the superior sagittal sinus or straight sinus close to the thrombus, as needed. The microcatheter was advanced along the thrombotic sinus as much as possible. Contrast injection through the microcatheter was performed to confirm the location of the catheter and the presence of thrombi. An undersized balloon catheter (Sterling or Ultrasoft SV, Boston Scientific, Ireland), with a diameter that was approximately 80% of the estimated sinus size on MRV or CTV, traversed the thrombi along a

Fig. 1. Demonstration of the procedure. (a) Advancement of the guiding catheter into the superior sagittal sinus (SSS). Thrombosis (brown) inside the SSS and right transverse sinus (TS) is shown. Green indicates the 6F guiding catheter and blue indicates the 5F diagnostic catheter. (b) Balloon shattering. The balloon catheter is shown in green with the micro guidewire (yellow) inside. To-and-fro movement of the inflated balloon causes shattering of the thrombi. (c) Fragmentation of thrombus. (d) Segmental suction thrombectomy. (e) & (f) Further balloon shattering and suction thrombectomy within the lower segments (right transverse sinus in this case).


C.-W. Lee et al. / Journal of the Neurological Sciences 365 (2016) 76–81

micro guidewire. The balloon was advanced, inflated, withdrawn, and deflated in a step-by-step manner in the occlusion segment. The process was repeated as necessary. The balloon was inflated with a pressure less than 4 atm. Each time, the balloon catheter was withdrawn slowly for approximately 10 cm and then deflated. To prevent pushing the thrombi upward, the balloon was never advanced when it was inflated. After this process, the thrombi in the manipulated segment were fragmented. Before 2013, local infusion of urokinase (300,000 IU) was given prior to ST. Because of the limited additional effect of local thrombolysis, it was not routinely used after 2013, and its use is now reserved only for patients with failed ST. The GC was advanced into the BM segment, and manual ST was performed with a 25 cc syringe. When the thrombus occluded the GC or was engaged within the catheter tip, the GC was removed under negative pressure and then flushed for repeated suction thrombectomy. Intrasinus contrast injection was periodically performed to evaluate the status of any remaining thrombi. If most of the thrombi were cleared, the whole process was performed in another segment down to the internal jugular vein. If there was difficulty in these processes in the upper segments, management of the lower segments was performed first to relieve lower obstruction, and attempts in the upper segments were performed later. After each segmental ST, either an angiography from arterial injection or a venography was obtained to evaluate sinus patency and the flow pattern of the cortical veins. If antegrade flow through the sinus was restored and stasis within the cortical vein was decreased, the procedure was deemed successful. Repeat catheter angiography was performed 5 to 10 min after the procedure in order to detect early rethrombosis. 2.2. Medications used Before the endovascular procedure, heparin was used to maintain the activated partial thromboplastin time (aPTT) at approximately 50– 70 s. LMWH was administered after a successful procedure for 5 to 7 days, then changed to warfarin to maintain the international normalized ratio (INR) between 1.5 and 2.5 for at least 3 months. If the procedure failed, anticoagulation was continued unless surgery was considered. 3. Results Between January 2008 and April 2015, 10 consecutive patients (average age, 53 ± 15 years; range, 30 to 73 years) at our institute underwent

ET with ST after BM for DVST. Six of the patients were female. Among the 10 patients, five had limb weakness (quadriplegia, hemiplegia, and paraplegia), four were comatose, and one had persistent vomiting due to increased intracranial pressure (IICP). The patient profiles, associated risks of DVST, lesion locations, imaging findings, pre-procedural conditions, treatments, procedural times, and outcomes are outlined in Table 1. Venous infarct was found in all patients and intracranial hemorrhage was noted in nine patients. The intervention was performed 1 to 14 days (average 5.8 days) after development of headache or insult possibly resulting in DVST. From our initial experience (cases 1 and 2, before Jan 2013), the procedure was performed in combination with BM, LT, and ST. During the overall study period, partial recanalization was achieved in all patients, but venous congestion was not significantly relieved in two cases. In eight of the 10 cases, antegrade venous flow was restored and venous stasis was decreased (Fig. 2). The patients had no clinical deterioration after the procedure and showed minimal deficits (mRS ≤ 1) at 3-month follow-up. No major complication was observed including procedure-related venous injury. One patient had intracerebral hematoma progression after unsuccessful recanalization of one segment. One (case #6) of the clinically failed patients had a seizure and a DVST at SSS was detected by MRI 2 years ago. Chronic occlusion of the middle segment of SSS was noted on serial follow-up MRI in spite of anticoagulant used, but he was symptom-free for 2 years. He developed multiple venous infarcts and intracerebral hematomas after 3-week discontinuation of medication. After one-day re-institution of anticoagulation, he became comatose and the intracerebral hematomas enlarged, so endovascular treatment was attempted. Transverse sinus (TS), straight sinus (StS), and lower superior sagittal sinus (SSS) was successfully recanalized by BM and ST; however, there were multiple channels in middle SSS, and a route for balloon passage could not be found after serial attempts. Intra-sinus administration of urokinase (480000IU) over a 20 minute period was applied, but venous congestion in frontal lobes remained. Follow-up CT showed enlargement of bilateral frontal hematomas, and the patient was totally dependent (mRS = 5) at 3 month follow-up. The other clinically failed patient (case #8) had DVST resulting in intracerebral hemorrhage and coma 10 days after meningioma resection. After 12-hour of anticoagulation, ET was attempted. On control catheter angiography, arrested flow of bilateral internal carotid arteries was observed. After thrombectomy, no restoration of arterial flow was seen, and the patient underwent emergent craniectomy for decompression, but died 3 days later. One patient (case #2), with simultaneous deep vein thrombosis of the lower

Table 1 Clinical profiles, imaging presentations, treatments, and outcomes of 10 patients with dural venous sinus thrombosis treated by suction thrombectomy after balloon maceration. Patient no.


Risk factors

Days after initial symptom

Location of DVST

Imaging presentation




Endovascular treatment

#1 #2 #3

35F 30M 49F

4 1 4



Quadriplegia Coma Left hemiplegia

E3M6V4 E1M4Vt E3M6V4

5 5 4


90 90 60

1 1 0

#4 #5 #6

50M 41F 71M

Graves' disease APS Protein S deficiency OCP Trauma OCP Polycythemia

4 5 14



E2M4Vt E4M6V5 E2M4V2

5 1 5


90 45 95

1 0 5



Protein S deficiency



















#9 #10

73M 66F

Meningioma operated Dehydration + CVC Protein S deficiency Graves’ disease

Coma Persistent vomiting Status epilepticus Coma Dysphasia Right hemiplegia Coma

4 3



E4M6V5 E3M5Va

4 4


110 35

0 1

Leg paraplegia Aphasia Right hemiplegia

Procedural time (min)

3-month mRS

Abbreviations: Pre-GCS, pre-procedure Glasgow coma scale; Pre-mRS, pre-procedure modified Rankin scale; APS, antiphospholipid syndrome; OCP, oral contraceptive pill; CVC, central venous catheter; TS, transverse sinus; SS, sigmoid sinus; SSS, superior sagittal sinus; StS, straight sinus; ICH, intracerebral hemorrhage; SAH, subarachnoid hemorrhage; VI, venous infarction; BM, balloon maceration; ST, suction thrombectomy; LT, local thrombolysis; mRS, modified Rankin scale, M, male; F, female.

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Fig. 2. A 52-year-old woman (case #7) with headache for 10 days and speech difficulty for one day. (a) Initial CT shows venous infarction and hematoma within the left parietal lobe as well as a hyperdensity within the superior sagittal sinus (SSS). (b) CT venography confirms thrombosis within the SSS and right transverse-sigmoid sinus (TS-SS, not shown). Anticoagulation was administered, but signs of increased intracranial pressure developed on the next day. Endovascular treatment is performed. (c) & (d) Venous phase of left ICA angiography shows thrombosis of the SSS and right TS and SS. (e) Advancement of the guiding catheter in the SSS and a balloon for shattering the thrombus. (f) After balloon shattering and suction thrombectomy within the SSS, the venous phase of the left ICA angiogram shows recanalization of the SSS, but the right TS and SS are still occluded. (g) After further balloon shattering and suction thrombectomy of the right TS and SS, antegrade sinus flow is restored. (h) Thrombi are aspirated. Further examination reveals protein S deficiency. Patient had mild agraphia and acalculia during the 3 months of clinical follow-up.

extremities, developed pulmonary embolism (PE) 25 days after the procedure which was successfully treated by anticoagulation alone without recurrent PE. Eight patients (except for cases #8 and #9) had follow-up MRV (n = 6) or CTV (n = 2) which showed that all endovascular recanalized segments remained patent. In patient #6, the SSS, which had not been successfully recanalized, was still occluded one month later despite anticoagulation, although the TS and StS were patent on follow-up CTV. None of our successful cases had recurrence or required another session of treatment.

4. Discussion ST after BM was introduced for the management of DVST. Technically, at least partial recanalization could be achieved in all 10 cases, while a clinically successful rate with good outcome (mRS ≤ 1) was achieved in eight of 10 cases (80%). ST has been successful in the treatment of acute ischemic stroke [25]. According to recent reports, large-bore suction catheters have successfully recanalized thrombotic dural sinuses alone, or in combination with multiple devices [20–21,24]. Our method was similar to a large-


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bore suction catheter, but we used an even larger 6 Fr GC for suction and passage of balloon catheters, and performed BM before ST. Modern distal access GC’s (such as Neuron 070 we used) are flexible and easy to be inserted into dural sinuses, and the maximal size of these GC’s is 6 Fr. They can be applied in our technique. The inner lumen is large enough for most balloon catheters and even some peripheral vascular stents. This may provide more options during ET, and GC's are usually less expansive. GC’s larger than 6 Fr are much stiffer and not easy to advance into the dural sinuses. Although the inner diameter of a 6 Fr GC is larger than that of large-bore suction catheter, the thrombi in DVST are usually much larger than the catheter lumen, even after BM. In our series, the GC occasionally got clogged during suction. However, after removal of the GC, as used in the ADAPT technique in acute ischemic stroke [25], large thrombi could be retrieved. The GC is then inserted into the target sinus again, and this would be easier if the long sheath was placed beyond the jugular bulb. Small macerated thrombi could then be removed easily by suction. The diameters of dural sinuses are usually much larger than the intracranial arteries. Current stent-retrievers for ischemic stroke are not large enough to catch the thrombi in the major dural sinuses. Multiple attempts may be needed for piece-by-piece retrieval of long-segment thrombi. However, too much manipulation of a stent-retriever is not suggested. There is currently no report using only a stent-retriever for DVST. Its role is usually the fragmentation of thrombi, which can be easily replaced by balloon catheters in our series. Use of an undersized balloon in a low inflation pressure could decrease the risk of sinus wall injury. Because the cortical vein is upstream to the thrombotic sinus, an undersized balloon is less likely to cause new cortical vein orifice occlusion by snow-plowing effect. From our initial experience, we found that low-dose LT had little effect. When BM succeeded, ST always succeeded in our series, and therefore, LT was deemed unnecessary. Our method was successful in all acute DVST segments but was unsuccessful in one segment of chronic, partially recanalized DVST which had been shown on MRI for 2 years. When BM fails, it may suggest organized thrombus or stenosis other than acute thrombosis. In such a situation, LT was usually ineffective and might increase the risk of hemorrhage progression. No lower-segment protective device was used in our series. The segment-by-segment approach from the upper to lower segments could prevent dislodgement of the macerated thrombi which may cause massive PE. One patient (case #2) experienced PE 25 days after procedure. The source of the PE was more likely the synchronous deep vein thrombosis of lower extremities because the PE had not occurred soon after the procedure. Simultaneous thrombosis of both dural sinuses and deep veins in a patient with hypercoagulability has been reported [26]. This combination is rare, but should be kept in mind in patients with hypercoagulability. In patients with DVST, complete recanalization may not be realistically achievable as most thrombotic cortical veins cannot be recanalized by ET. However, if the downstream sinus can be recanalized, more collateral drainage may be established, and the venous congestion may be relieved. In our series, when venous congestion was significantly decreased on catheter angiography, the procedure was usually successful. The residual DVST or cortical thrombosis could be successfully treated with anticoagulation. If catheter angiography did not show relief of venous congestion, the outcome was always poor. If the patients developed coma before the procedure, the outcome was also poor (2/ 4 of our patients with coma had poor outcomes). This may be associated with poor venous collaterals and large areas of venous congestion. The current concept of “failed medical treatment” remains ambiguous. More studies are necessary to predict the outcome of medical treatment. Early ET may be needed in certain cases. The ages of our patients (average age, 53 ± 15 years) were significantly higher than those in a recent systemic review (average age, 35 ± 14 years) [20]. Two patients b40 years of age were seen in early stage of our series. Increased awareness of DVST in young patients

with headache and early anticoagulation treatment may reduce the need for ET. Most of our patients were diagnosed after several days of headache. The worst outcomes occurred in two patients diagnosed after 10 and 14 days of headache, respectively. This may partially explain the extension of DVST and severity of venous congestion that progressed over time. Most young patients with early diagnosis of DVST can be treated successfully with anticoagulation alone. A major limitation of our series was its small number of cases. Because DVST is a rare disease and the overall prognosis after medical treatment is good, most reported series using ET had small numbers. There is no randomized trial to show the efficacy of ET in DVST. A randomized study is currently underway [27], although the results are not yet published. At the current stage, aggressive ET should be used with caution.

5. Conclusion BM followed by ST is a promising endovascular technique in the treatment of acute DVST. Patients with DVST prone to poor outcomes (coma, hemorrhage, deep sinus involvement, refractory to anticoagulation) should be treated earlier before an irreversible condition occurs. ET for chronic DVST with acute deterioration remains challenging.

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