Next Article in Journal
Primary and Secondary Mitochondrial Diseases: Etiologies and Therapeutic Strategies
Next Article in Special Issue
Blood Biomarkers for Triaging Patients for Suspected Stroke: Every Minute Counts
Previous Article in Journal
TNF-α Inhibitors in Combination with MTX Reduce Circulating Levels of Heparan Sulfate/Heparin and Endothelial Dysfunction Biomarkers (sVCAM-1, MCP-1, MMP-9 and ADMA) in Women with Rheumatoid Arthritis
Previous Article in Special Issue
Primary Thrombophilia XVII: A Narrative Review of Sticky Platelet Syndrome in México
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
JCM
Volume 11
Issue 14
10.3390/jcm11144215
jcm-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Systematic Review

Endovascular Treatment of Intracranial Vein and Venous Sinus Thrombosis—A Systematic Review

by
Philipp Bücke
1,*,
Victoria Hellstern
2,
Alexandru Cimpoca
2,
José E. Cohen
3,
Thomas Horvath
1,
Oliver Ganslandt
4,
Hansjörg Bäzner
5 and
Hans Henkes
2,6
1
Department of Neurology, Inselspital, Bern University Hospital, University of Bern, 3010 Bern, Switzerland
2
Neuroradiologische Klinik, Klinikum Stuttgart, 70174 Stuttgart, Germany
3
Department of Neurosurgery, Hadassah Medical Center, Hebrew University Jerusalem, Jerusalem 9103401, Israel
4
Neurochirurgische Klinik, Klinikum Stuttgart, 70174 Stuttgart, Germany
5
Neurologische Klinik, Klinikum Stuttgart, 70174 Stuttgart, Germany
6
Medical Faculty, Universität Duisburg-Essen, 45147 Essen, Germany
*
Author to whom correspondence should be addressed.
J. Clin. Med. 2022, 11(14), 4215; https://doi.org/10.3390/jcm11144215
Submission received: 3 June 2022 / Revised: 13 July 2022 / Accepted: 14 July 2022 / Published: 20 July 2022
(This article belongs to the Special Issue Management of Venous and Arterial Thrombosis)
Browse Figures
Versions Notes

Abstract

:
Background: Cerebral venous sinus or vein thromboses (SVT) are treated with heparin followed by oral anticoagulation. Even after receiving the best medical treatment, numerous patients experience neurological deterioration, intracerebral hemorrhage or brain edema. Debate regarding whether endovascular treatment (EVT) is beneficial in such severe cases remains ongoing. This systematic review summarizes the current evidence supporting the use of EVT for SVT on the basis of case presentations, with a focus on patient selection, treatment strategies and the effects of the COVID-19 pandemic. Methods: This systemic literature review included randomized controlled trials (RCTs) and retrospective observational data analyzing five or more patients. Follow-up information (modified Rankin scale (mRS)) was required to be provided (individual patient data). Results: 21 records (n = 405 patients; 1 RCT, 20 observational studies) were identified. EVT was found to be feasible and safe in a highly selected patient cohort but was not associated with an increase in good functional outcomes (mRS 0–2) in RCT data. In observational data, good functional outcomes were frequently observed despite an anticipated poor prognosis. Conclusion: The current evidence does not support the routine incorporation of EVT in SVT treatment. However, in a patient cohort prone to poor prognosis, EVT might be a reasonable therapeutic option. Further studies determining the patients at risk, choice of methods and devices, and timing of treatment initiation are warranted.

1. Introduction

Cerebral venous sinus or venous thrombosis (SVT) is a rare but potentially severe cause of cerebral hemorrhage or cerebral venous infarction (incidence: 1.32 per 100,000 person-years (2.78 per 100,000 person-years in women 31–50 years of age)) accounting for approximately 0.5% of all stroke cases [1,2,3]. Various factors are associated with the development of SVT [1,4]. Recent publications have reported a considerably higher incidence of SVT in the COVID-19 pandemic because both COVID-19 (reported incidence: 8.8 per 10,000 infections over 3 months) and COVID-19 vaccination (leading to vaccine-induced immune thrombotic thrombocytopenia (VITT)) appear to increase the risk of SVT [5,6]. Figure 1 illustrates the anatomy of the cerebral dural sinus and the deep cerebral veins.
Outcomes after SVT in general are favorable assuming early diagnosis and treatment initiation [8]. Treatment is challenging, and its success highly depends on rapid anticoagulation with unfractionated or low-molecular-weight heparin, even in cases of intracerebral hemorrhage [9,10]. However, probably because of a limited capacity to dissolve an extensive intravenous thrombus load, many patients show deterioration, and as many as 13% eventually die or remain severely disabled despite sufficient anticoagulation therapy [11,12,13]. Patients with coma or altered mental status, intracerebral hemorrhage (ICH), underlying malignancy or an infection of the central nervous system appear to be at risk [12]. Pregnant or postpartum women, chronic hypertension as well as superior sagittal sinus and cortical vein involvement seem to be associated with ICH complications in SVT [14].
Endovascular treatment (EVT) strategies have been proposed to increase the frequency of good functional outcomes in high-risk or deteriorating patients [15,16,17,18,19,20,21,22,23,24,25]. Initially, endovascular thrombolysis with application of the thrombolytic agent locally and at the site of the occluded sinus was described [15,16]. Occasionally, the catheter is left in situ for 24 h or more [16,17]. In addition, several endovascular techniques have been discussed and investigated: rheolytic catheter thrombectomy, direct aspiration thrombectomy, balloon-guided thrombectomy or angioplasty and stent retriever thrombectomy [18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37]. Information on EVT in SVT is sparse and is based primarily on case series and anecdotal data and only a single published randomized controlled trial (RCT) [19,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57]. Therefore, the current guideline recommendations remain vague. Whereas the American Heart Association and the American Stroke Association have together stated that endovascular therapy “may be considered if deterioration occurs despite intensive anticoagulation treatment,” the European Stroke Organisation has not given any advice at all [58,59].
The goal of this systematic review is to provide an overview on the current evidence supporting EVT strategies in patients with SVT. We aimed to identify potential selection criteria for patients who might benefit from an additional EVT. Furthermore, the roles of SARS-CoV-2 infections and VITT are discussed.

2. Materials and Methods

We performed a systematic literature search in the PubMed (20 May 2022) and Medline (20 May 2022) databases by using the following search terms: “sinus thrombosis AND endovascular,” “sinus thrombosis AND thrombectomy,” “[cerebral] venous thrombosis AND endovascular” and “[cerebral] venous thrombosis AND thrombectomy.” For the sub-analysis of patients with SVT caused by SARS-CoV-2 infection or after COVID-19 vaccination, additional search phrases were identified: “COVID-19 AND endovascular (AND thrombosis),” “COVID-19 AND thrombectomy (AND thrombosis),” “vaccination AND endovascular” and “vaccination AND thrombectomy.” All articles published online until 20 May 2022 were screened. Two independent raters performed the literature search (P.B. and H.H.). This review follows the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA 2020) recommendations [60].
All identified publications were required to meet the following predefined inclusion criteria: (1) RCTs or retrospective studies, case series/case reports including more than five patients 18 years of age or older; (2) reported information on functional outcomes (modified Rankin scale (mRS) after discharge (not at the time of discharge)), death and complications (e.g., symptomatic intracranial hemorrhage or procedural complications); (3) inclusion of individual patient or study data only once (screening for repeated publications including identical cases); and (4) publication in English. In the analysis of EVT in patients with COVID-19 and VITT, only articles and manuscripts evaluating endovascular procedures (and the respective indications to treat patients) were eligible. We, therefore, did not consider registry data and meta-analyses reporting the frequency and the number of interventions without mentioning procedure-specific outcome parameters.

3. Results

A total of 456 records were identified and screened on the basis of the predefined search criteria (Figure 2). Only 92 were eligible for full-text evaluation. Eventually, 21 records were eligible for inclusion (reasons for exclusion of records: n = 56—case reports or case series with fewer than five reported events; n = 14—no follow-up data or data on functional outcomes; n = 3—not written in English).
One RCT (Thrombolysis or Anticoagulation for Cerebral Venous Thrombosis; TO-ACT) compared EVT (n = 33) and standard care (i.e., anticoagulation; n = 34) in patients with anticipated poor outcomes (Table 1) [38], which were defined as at least one of the following risk factors: mental status disorder, coma state (Glasgow coma scale (GCS) < 9), ICH or thrombosis of the deep cerebral venous system. Patients with more than 10 days from diagnosis to potential randomization, pregnancy (women in the puerperium were eligible), thrombocytopenia (platelet count < 100 × 109/L), as well as clinical or radiological signs of impending trans-tentorial herniation were excluded. EVT (mechanical thrombectomy with an AngioJet (Boston Scientific, Marlborough, MA, USA), stent retriever, aspiration techniques or microcatheter) in combination with local thrombolytic treatment (urokinase administered continuously for up to 72 h) did not differ from standard care in terms of functional outcomes (mRS, 0–1 at 12 months; 67% vs. 68%; risk ratio, 0.99 (95% CI, 0.71–1.18); Table 1 provides details and information on complications).
Nyberg et al. (2017) have retrospectively analyzed their single-center cohort of patients with SVT and compared outcome data (mRS, 0–2 at 3 months) for patients treated with additional EVT (n = 29) to those receiving anticoagulation only (n = 37; 5-year time span (2011–2015)) [39]. The decision on whether to perform EVT was at the discretion of the treatment team and based on individual decision-making. The two treatment groups did not differ in outcome parameters (e.g., mRS, 0–2: 22% vs. 30%; mortality, n = 6 vs. n = 5; p = 1.0).
Prospective case series, retrospective analyses and case series demonstrated the technical and procedural feasibility and safety of EVT in selected patients (n = 19; details in Table 1) [19,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57]. All reported patients were anticoagulated, and those with an expected poor prognosis (such as ICH or edema, neurological deterioration, coma (e.g., GCS < 9), progressive thrombus material observed on repeated imaging or signs of elevated intracranial pressure (e.g., papilledema)). Individual decision-making based on local experience and preferences was used to decide whether to perform EVT.
A total of 25 publications met the search criteria for COVID-19 and VITT-associated EVT in SVT. Of those, 14 records were excluded (because of lack of reported patient data, review articles and registry data without information on individual patients). Eleven records were eligible for analysis (Table 2) [61,62,63,64,65,66,67,68,69,70,71], comprising case reports and case series only. Of those, four case reports and case series presented data for four patients with COVID-19 and EVT [61,62,63,64]. The decision to perform EVT was made in cases with suspected poor prognosis, with criteria comparable to those described above. Aspiration in combination with local thrombolytic therapy was the preferred endovascular technique [61,62]. The overall outcome was poor [61,62,63].
The first reports of SVT caused by VITT emerged in 2021 [65,66,67,68,69,70,71]. As of 20 May 2022, seven records of EVT in 16 VITT patients were identified [65,66,67,68,69,70,71]. Most cases (n = 15) were attributed to the ChAdOx1 nCoV-19 (AstraZeneca, Cambridge, UK) vaccine [65,66,67,69,70,71]. Only one case appeared to be associated with an mRNA vaccine (mRNA-1273 vaccine; Moderna, Cambridge, MA, USA) [68]. Excluding the latter, the time between vaccination and symptom onset was 4–27 days. Common features (except [68]) were thrombocytopenia, elevated D-dimer levels, and positivity for platelet factor 4 (PF4) antibodies (Table 2). Neurological deterioration potentially resulting in poor outcomes facilitated the use of EVT. The technical strategies described were aspiration plus stent retriever or balloon-guided thrombectomy in selected cases [65,66,67,69]. MRS of 0–1 was observed in seven patients during follow-up [65,66,69]. Three patients died [65,70].

4. Discussion

The overall outcome after SVT can be unfavorable in terms of functional independence and survival [8,11,72]. A total of 75–84% of patients eventually become functionally independent, with excellent functional recovery (mRS, 0–1) [8,11,72]. However, a considerable number of patients remain functionally dependent or disabled (22.2%) or die (up to 14.6%) [11,72]. To identify patients prone to poor prognosis, several risk factors have been identified (independent of treatment strategies): GCS < 9, presence of ICH, involvement of the deep cerebral venous system, mental status disorder (not specified; additional conditions such as underlying malignancy, cerebral or systemic infection, and requirement for hemicraniectomy also apply) [11,72,73,74]. Neurological deterioration—as part of the natural course of the disease or due to factors such as heparin resistance—might necessitate an additional EVT approach to remove the thrombus load [75].
Retrospective and anecdotal data have demonstrated the safety and feasibility of EVT in selected patients, and have shown satisfying results [19,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57]. Yet, because of their lack of a control group and their retrospective nature, those studies have been unable to demonstrate a treatment effect resulting in an outcome benefit. In addition, inconsistencies in the timing of the interventions, indications for surgical procedures such as decompressive hemicraniectomy, etiological considerations (e.g., malignancy or sepsis) and clinical complications interfering with outcomes (e.g., status epilepticus) make an interpretation difficult. To our knowledge, only one RCT (TO-ACT) has compared EVT to standard care in patients with SVT (again, with a suspected unfavorable prognosis, as described above). TO-ACT did not detect a modification of the treatment effect attributable to EVT (see Table 1 for inclusion criteria) [38]. The limitations of this trial include its small sample size (due to early termination recommended by the data and safety monitoring board because of futility), patient selection based on clinical presentations suspected to (and previously reported to) negatively influence outcomes and unrestricted use of available endovascular approaches and devices [38]. Therefore, non-significant but clinically relevant treatment effects as well as subgroups that might actually show considerable benefits remained undetected. In a meta-analysis using individual patient data (not including RCT data), EVT was associated with poor outcomes and mortality [76]. Because each treatment decision was made individually in each case (no clear indication; suspected poor prognosis), generalizability is limited. The baseline characteristics were poorer in EVT patients than in controls. Therefore, these retrospective results must be interpreted very cautiously. Important questions regarding patient selection (clinical versus imaging characteristics) and the timing of the intervention remain unanswered. Waiting until a patient is deteriorating might be too late.
Various treatment strategies have been investigated in EVT for SVT. Local thrombolytic therapy (urokinase or alteplase) was performed in most of the cases [19,38,39,40,41,42,44,45,46,47,48,49,51,52,53,54,55,56,57], with either a single periinterventional bolus or a continual infusion (locally, via a microcatheter) for up to 72 h (or longer, depending on the recanalization success). Yue et al. (2010) combined intraarterial thrombolysis with an endovascular thrombectomy approach (balloon-guided) [57]. Several thrombectomy procedures were discussed in the presented literature: aspiration thrombectomy [19,38,39,40,41,42,46,48,49,51,53,54,55,56], stent retriever thrombectomy [38,39,40,41,42,46,47,48,49,54], balloon-guided thrombectomy/angioplasty [19,38,39,40,41,44,47,51,53,54,57], the (rheolytic) AngioJet device [38,39,40,47,49,50] as well as additional stenting [42,46]. The study by Dashti et al. was the only one performing thrombectomy without local thrombolysis (AngioJet) [50]. A meta-analysis published in 2019 did not detect differences in outcomes stratified by treatment approach [77]. Despite poor baseline characteristics, 70–80% of patients eventually achieved mRS scores of 0–2 in the follow-up [78]. Local thrombolysis in combination with EVT has not been associated with the development or worsening of an ICH (complication rate < 10%) [78]. Further complications observed were subarachnoid hemorrhage, vessel perforation, and treatment failure [38,39,40,41,42,50,52,54]. Experience and routine (i.e., adherence to a local protocol) might be important because centers following one specific approach showed higher recanalization rates (independently of the procedure or the combination of procedures chosen) than centers using various combinations of EVT strategies [77]. However, the described inconsistencies in device allocation and the small number of treated patients make comparisons regarding the superiority of any of the treatment strategies impossible. Thus, future trials are needed to make such a comparison. Endovascular trials in acute ischemic stroke have indicated that devices are crucial in facilitating treatment effects, recanalization rates, and good functional outcomes [79].
Both COVID-19 and COVID-19 vaccination have been reported to be associated with an increase in SVT incidence [5,6]. Patients with COVID-associated SVT (4.2% of all COVID-associated strokes) appear to be older, do not have specific risk factors and experience higher in-hospital mortality (up to 16.7%) [80,81]. In a New York cohort study, two of the 12 patients received endovascular local thrombolysis [5]. SVT associated with COVID-19 vaccination may be more severe and has higher reported mortality rates (39.2% as compared with approximately 2–5% in pre-pandemic SVT) [6]. The mechanism of pathogenesis (VITT; a prothrombotic state associated with an immunoglobin G reaction against PF4) predominantly occurs in adenovirus vector-type vaccinations (ChAdOx1 nCov-19 (AstraZeneca); recombinant adenovirus type 26 vector encoding S glycoprotein of SARS-CoV-2 (Johnson and Johnson/Janssen)) [6,82]. EVT might be reasonable in selected patients meeting the TO-ACT inclusion criteria (Table 1) [38,83]. Although observational data and case reports of EVT in those patients are scarce [65,66,67,68,69,70,71], these studies have indicated the feasibility and safety of EVT and have suggested that EVT can achieve good functional outcomes in a cohort with overall poor prognosis.
This systematic review is limited by the quality (and sample size) of the available data. The disadvantages of the TO-ACT trial have already been discussed. Because of the retrospective design of the remaining data, all the attributed limitations apply (e.g., selection bias or bias by indication) because the rationale for treatment allocation and the number of patients who were potentially eligible for treatment but were not considered are unknown. Therefore, the presented results and the conclusion require very cautious interpretation.
In conclusion, the available data do not support the routine use of EVT strategies in patients with SVT. In patients with a suspected poor outcome (meeting the TO-ACT inclusion criteria), EVT can be performed as part of individual healing attempts. EVT is feasible and safe and might possibly improve functional outcomes. No reasonable recommendation can be made regarding which endovascular technique to use (and in which cases). According to our own experience, patients with substantial thrombus material (without an early response to anticoagulation), those with ICH, those in need of intensive care, and those with VITT do benefit from EVT. Yet, whether patients with clinical and/or imaging risk factors might benefit from early treatment initiation (before deterioration occurs) remains unknown. Further RCTs are warranted to investigate treatment strategies, patient selection, and the timing of the intervention (using predefined therapeutic strategies and reproducible inclusion criteria).

Author Contributions

P.B. and H.H.: drafted the article and performed the primary literature research. P.B. wrote the manuscript. V.H.: expert in the endovascular treatment of intracranial venous sinus thrombosis, involved in the data collection and analysis of data concerning endovascular management. A.C.: expert in the endovascular treatment of intracranial venous sinus thrombosis, involved in the data collection and analysis of data concerning the outcome of different endovascular procedures. J.E.C.: endovascular neurosurgeon, contributed to aspects of endovascular and intensive care treatment concepts. T.H.: neurologist with significant stroke experience, analyzed the manuscript concerning the medicinal treatment of VST. O.G.: senior neurosurgeon with significant neurovascular experience, supervised the aspects of surgical treatment of VST. H.B.: senior neurologist with significant stroke experience, supervised the aspects of medicinal treatment of VST. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

There are no data beyond the analyzed publications, which became the basis for this systematic review.

Conflicts of Interest

H.H. is coinventor of the Solitaire stent and the pRESET stent retriever and cofounder of phenox GmbH, femtos GmbH and CONTARA GmbH, which are medical device companies developing and/or selling products for the EVT of neurovascular disorders. All other authors declare no conflicts of interest in the context of this publication.

References

  1. Hopper, A.H.; Klein, J.P. Cerebral Venous Thrombosis. N. Engl. J. Med. 2021, 385, 59–64. [Google Scholar]
  2. Bousser, M.; Ferro, J.M. Cerebral venous thrombosis: An update. Lancet Neurol. 2007, 6, 162–170. [Google Scholar] [CrossRef]
  3. Coutinho, J.M.; Zuurbier, S.M.; Aramideh, M.; Stam, J. The Incidence of Cerebral Venous Thrombosis a Cross-Sectional Study. Stroke 2012, 43, 3375–3377. [Google Scholar] [CrossRef] [Green Version]
  4. Stam, J. Thrombosis of the Cerebral Veins and Sinuses. N. Engl. J. Med. 2005, 352, 1791–1798. [Google Scholar] [CrossRef] [Green Version]
  5. Al-Mufti, F.; Amuluru, K.; Sahni, R.; Bekelis, K.; Karimi, R.; Ogulnick, J.; Cooper, J.; Overby, P.; Nuoman, R.; Tiwari, A.; et al. Cerebral Venous Thrombosis in COVID-19: A New York Metropolitan Cohort Study. AJNR Am. J. Neuroradiol. 2021, 42, 1196–1200. [Google Scholar] [CrossRef]
  6. Jaiswal, V.; Nepal, G.; Dijamco, P.; Ishak, A.; Dagar, M.; Sarfraz, Z.; Shama, N.; Sarfraz, A.; Lnu, K.; Mitra, S.; et al. Cerebral Venous Sinus Thrombosis Following COVID-19 Vaccination: A Systematic Review. J. Prim. Care Community Health 2022, 13, 1–10. [Google Scholar] [CrossRef]
  7. Jung, S.; Mattle, H.; Horvath, T.; Seiffge, D.; Heldner, M.; Meinel, T.; Bühlmann, M.; Prange, U.; Salmen, S.; Humm, A.; et al. Stroke Guidelines of the Bern Stroke Network. Available online: http://www.neurologie.insel.ch/fileadmin/Neurologie/Dokumente/Stroke_Center/Stroke_Guidelines_2021_English.pdf (accessed on 26 May 2022).
  8. Devianne, J.; Legris, N.; Crassard, I.; Bellesme, C.; Bejot, Y.; Guidoux, C.; Pico, F.; Germanaud, D.; Obadia, M.; Rodriguez, D.; et al. Epidemiology, Clinical Features, and Outcome in a Cohort of Adolescents with Cerebral Venous Thrombosis. Neurology 2021, 97, e1920–e1932. [Google Scholar] [CrossRef]
  9. Einhäupl, K.M.; Villringer, A.; Meister, W.; Mehraein, S.; Garner, C.; Pellkofer, M.; Haberl, R.L.; Pfister, H.W.; Schmiedek, P. Heparin treatment in sinus venous thrombosis. Lancet 1991, 338, 597–600. [Google Scholar] [CrossRef]
  10. De Bruijn, S.F.T.M.; Stam, J.; for the Cerebral Venous Sinus Thrombosis Study Group. Randomized, Placebo-Controlled Trial of Anticoagulant Treatment with Low-Molecular-Weight Heparin for Cerebral Sinus Thrombosis. Stroke 1999, 30, 484–488. [Google Scholar] [CrossRef] [Green Version]
  11. Ferro, J.M.; Canhão, P.; Stam, J.; Bousser, M.; Barinagarrementeria, F.; ISCVT Investigators. 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. [Google Scholar]
  12. Lee, S.-K.; Mokin, M.; Hetts, S.W.; Fifi, J.F.; Bousser, M.; Fraser, J.F.; Society of NeuroInterventional Surgery. Current endovascular strategies for cerebral venous thrombosis: Report of the SNIS Standards and Guidelines Committee. NeuroInterv. Surg. 2018, 10, 803–810. [Google Scholar] [CrossRef] [PubMed]
  13. Coutinho, J.M.; Ferro, J.M.; Zuurbier, S.M.; Mink, M.S.; Canhão, P.; Crassard, I.; Majoie, J.B.; Reekers, J.A.; Houdart, E.; de Haan, R.J.; et al. Thrombolysis or anticoagulation for cerebral venous thrombosis: Rationale and design of the TO-ACT trial. Int. J. Stroke 2013, 8, 135–140. [Google Scholar] [CrossRef] [PubMed]
  14. Simaan, N.; Molad, J.; Peretz, S.; Filioglo, A.; Auriel, E.; Hallevi, H.; Seyman, E.; Barnea, R.; Cohen, J.E.; Leker, R.R.; et al. Characteristics of Cerebral Sinus Venous Thrombosis Patients Presenting with Intracerebral Hemorrhage. J. Clin. Med. 2022, 11, 1040. [Google Scholar] [CrossRef]
  15. Rahman, M.; Velat, G.J.; Hoh, B.L.; Mocco, J. Direct thrombolysis for cerebral venous sinus thrombosis. Neurosurg. Focus 2009, 27, E7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  16. Baker, M.D.; Opatowsky, M.J.; Wilson, J.A.; Glazier, S.S.; Morris, P.P. Rheolytic catheter and thrombolysis of dural venous sinus thrombosis: A case series. Neurosurgery 2001, 48, 487–493. [Google Scholar] [CrossRef] [PubMed]
  17. Canhao, P.; Falcao, F.; Ferro, J.M. Thrombolytics for cerebral sinus thrombosis: A systematic review. Cereb. Dis 2003, 15, 159–166. [Google Scholar] [CrossRef]
  18. Choulakian, A.; Alexander, M.J. Mechanical thrombectomy with the penumbra system for treatment of venous sinus thrombosis. J. Neurointerv. Surg. 2010, 2, 153–156. [Google Scholar] [CrossRef]
  19. Jankowitz, B.T.; Bodily, L.M.; Jumaa, M.; Syed, Z.F.; Jovin, T.G. Manual aspiration thrombectomy for cerebral venous sinus thrombosis. J. Neurointerv. Surg. 2013, 5, 534–538. [Google Scholar] [CrossRef]
  20. Kirsch, J.; Rasmussen, P.A.; Masaryk, T.J.; Perl, J., II; Fiorella, D. Adjunctive rheolytic thrombectomy for central venous sinus thrombosis: Technical case report. Neurosurgery 2007, 60, E577–E578. [Google Scholar] [CrossRef]
  21. La Barge, D.V.; Bishop, F.S.; Stevens, E.A.; Eskandari, R.; Schmidt, R.H.; Skalabrin, E.J.; Ng, P.P. Intrasinus catheter-directed heparin infusion the treatment of dural venous sinus thrombosis. AJNR Am. J. Neuroradiol. 2009, 30, 1672–1678. [Google Scholar] [CrossRef] [Green Version]
  22. Zhang, A.; Collinson, R.L.; Hurst, R.W.; Weigele, J.B. Rheolytic thrombectomy for cerebral sinus thrombosis. Neurocrit Care 2008, 9, 17–26. [Google Scholar] [CrossRef] [PubMed]
  23. Zhen, Y.; Zhang, N.; He, L.; Shen, L.; Yan, K. Mechanical thrombectomy combined with recombinant tissue plasminogen activator thrombolysis in the venous sinus for the treatment of severe tcerebral venous sinus thrombosis. Exp. Ther. Med. 2015, 9, 1080–1084. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Shui, S.F.; Li, T.F.; Han, X.W.; Ma, J.; Guo, D. Balloon dilatation and thrombus extraction for the treatment of cerebral venous sinus thrombosis. Neurol. India 2014, 62, 371–375. [Google Scholar] [CrossRef] [PubMed]
  25. Wasay, M.; Bakshi, R.; Kojan, S.; Bobustuc, G.; Dubey, N.; Unwin, D.H. Nonrandomized comparison of local urokinase thrombolysis versus systemic heparin anticoagulation for superior sagittal sinus thrombosis. Stroke 2001, 32, 2310–2317. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  26. Chow, K.Y.; Gobin, P.; Saver, J.; Kidwell, C.; Dong, P.; Viñuela, F. Endovascular Treatment of Dural Sinus Thrombosis with Rheolytic Thrombectomy and Intra-Arterial Thrombolysis. Stroke 2000, 31, 1420–1425. [Google Scholar] [CrossRef] [PubMed]
  27. Najjar, A.A.; Rasheedi, J.K.; Kurdi, K.I.; Hasan, A.A.; Almekhlafi, M.A.; Baeesa, S.S. Endovascular suction thrombectomy for severe cerebral venous sinus thrombosis: A report of two cases. J. Taibah Univ. Med. Sci. 2018, 13, 87–92. [Google Scholar] [CrossRef]
  28. Lee, D.J.; Ahmadpour, A.; Binyamin, T.; Dahlin, B.C.; Shahlaie, K.; Waldau, B. Management and outcome of spontaneous cerebral venous sinus thrombosis in a 5-year consecutive single-institution cohort. J. NeuroInterv. Surg. 2017, 9, 34–38. [Google Scholar] [CrossRef]
  29. Adachi, H.; Mineharu, Y.; Ishikawa, T.; Imamura, H.; Yamamato, S.; Todo, K.; Yamagami, H.; Sakai, N. Stenting for acute cerebral venous sinus thrombosis in the superior sagittal sinus. Interv. Neuroradiol. 2015, 21, 719–723. [Google Scholar] [CrossRef]
  30. Liao, W.; Liu, Y.; Gu, W.; Yang, J.; Chen, C.; Liu, F.; Zeng, F.; Wang, X. Cerebral Venous Sinus Thrombosis: Successful Treatment of Two Patients Using the Penumbra System and Review of Endovascular Approaches. Neuroradiol. J. 2015, 28, 177–183. [Google Scholar] [CrossRef] [Green Version]
  31. Philips, M.F.; Bagley, L.J.; Sinson, G.P.; Raps, E.C.; Galetta, S.L.; Zager, E.L.; Hurst, R.W. Endovascular thrombolysis for symptomatic cerebral venous thrombosis. J. Neurosurg. 1999, 90, 65–71. [Google Scholar] [CrossRef]
  32. Dandapat, S.; Samaniego, E.A.; Szeder, V.; Siddiqui, F.M.; Duckwiler, G.R.; Kiddy, U.; Guerrero, W.R.; Zheng, B.; Hasan, D.; Derdeyn, C.; et al. 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. Interv. Neuroradiol. 2020, 26, 26–32. [Google Scholar] [CrossRef] [PubMed]
  33. Siddiqui, F.; Weber, M.W.; Dandapat, S.; Scaife, S.; Buhnerkempe, M.; Ortega-Gutierrez, S.; Aksan, N.; Elias, A.; Coutinho, J.M. Endovascular Thrombolysis or Thrombectomy for Cerebral Venous Thrombosis: Study of Nationwide Inpatient Sample 2004–2014. J. Stroke Cereb. Dis. 2019, 6, 1440–1447. [Google Scholar] [CrossRef] [PubMed]
  34. Ma, J.; Shui, S.; Han, X.; Guo, D.; Li, T.; Yan, L. Mechanical thrombectomy with Solitaire AB stents for the treatment of intracranial venous sinus thrombosis. Acta Radiol. 2016, 57, 1524–1530. [Google Scholar] [CrossRef] [PubMed]
  35. Zhang, S.; Hu, Y.; Li, Z.; Huang, D.; Zhang, M.; Wang, C.; Wang, Z. Endovascular treatment for hemorrhagic cerebral venous sinus thrombosis: Experience with 9 cases for 3 years. Am. J. Transl. Res. 2018, 10, 1611–1619. [Google Scholar]
  36. Liao, C.; Liao, N.; Chen, W.; Chen, H.; Shen, C.; Yang, S.; Tsuei, Y. Endovascular Mechanical Thrombectomy and On-Site Chemical Thrombolysis for Severe Cerebral Venous Sinus Thrombosis. Sci. Rep. 2020, 10, 4937. [Google Scholar] [CrossRef] [Green Version]
  37. Li, X.; Li, T.; Fan, Y. Efficacy of intravascular mechanical thrombectomy combined with thrombolysis and anticoagulant therapy in the treatment of cerebral venous sinus thrombosis and its effect on neurological function and coagulation indices. Am. J. Transl. Res. 2021, 13, 6921–6928. [Google Scholar]
  38. Coutinho, J.M.; Zuurbier, S.M.; Bousser, M.; Ji, X.; Canhão, P.; Boos, Y.B.; Crassard, I.; Nunes, A.P.; Uyttenboogaart, M.; Chen, J.; et al. Effect of Endovascular Treatment with Medical Management vs Standard Care on Severe Cerebral Venous Thrombosis: The TO-ACT Randomized Clinical Trial. JAMA Neurol. 2020, 77, 966–973. [Google Scholar] [CrossRef]
  39. Nyberg, E.M.; Case, D.; Nagae, L.M.; Honce, J.M.; Reyenga, W.; Seinfeld, J.; Poisson, S.; Leppert, M.H. The addition of endovascular intervention for dural venous sinus thrombosis: Single-center experience and review of literature. J. Stroke Cereb. Dis. 2017, 26, 2240–2247. [Google Scholar] [CrossRef]
  40. Siddiqui, F.M.; Banerjee, C.; Zuurbier, S.M.; Hao, Q.; Ahn, C.; Pride, G.L.; Wasay, M.; Majoie, C.B.; Liebeskind, D.; Johnsin, M.; et al. Mechanical thrombectomy versus intrasinus thrombolysis for cerebral venous sinus thrombosis: A non-randomized comparison. Interv. Neuroradiol. 2014, 20, 336–344. [Google Scholar] [CrossRef] [Green Version]
  41. Guo, X.; Liu, S.; Guan, S. The clinical analysis and treatment strategy of endovascular treatment for cerebral venous sinus thrombosis combined with intracerebral hemorrhage. Sci. Rep. 2020, 10, 22300. [Google Scholar] [CrossRef]
  42. Andersen, T.H.; Hansen, K.; Truelsen, T.; Cronqvist, M.; Stavngaard, T.; Cortsen, M.E.; Holtmannspötter, M.; Højgaard, J.L.S.; Stensballe, J.; Welling, K.L.; et al. Endovascular treatment for cerebral venous sinus thrombosis—A single center study. Br. J. Neurosurg. 2020, 35, 259–265. [Google Scholar] [CrossRef] [PubMed]
  43. Yang, X.; Wu, F.; Liu, Y.; Duan, J.; Meng, R.; Chen, J.; Li, D.; Fan, Z.; Fisher, M.; Yang, Q.; et al. Predictors of successful endovascular treatment in severe cerebral venous sinus thrombosis. Ann. Clin. Trans. Neur. 2019, 6, 755–761. [Google Scholar] [CrossRef] [PubMed]
  44. Yang, J.; Wang, H.; Chen, Y.; Qiu, M.; Zhang, B.; Chen, Z. Balloon-Assisted Thrombectomy and Intrasinus Urokinase Thrombolysis for Severe Cerebral Venous Sinus Thrombosis. Front. Neurol. 2021, 12, 735540. [Google Scholar] [CrossRef]
  45. Stam, J.; Majoie, C.; Van Delden, O.M.; Van Lienden, K.P.; Reekers, J.A. Endovascular thrombectomy and thrombolysis for severe cerebral sinus thrombosis: A prospective study. Stroke 2008, 39, 1487–1490. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Lu, G.; Shin, J.H.; Song, Y.; Lee, D.H. Stenting of symptomatic lateral sinus thrombosis refractory to mechanical thrombectomy. Interv. Neuroradiol. 2019, 25, 714–720. [Google Scholar] [CrossRef]
  47. Qureshi, A.I.; Grigoryan, M.; Saleem, M.A.; Aytac, E.; Wallery, S.S.; Rodriguez, G.J.; Suri, M.F.K. Prolonged Microcatheter-Based Local Thrombolytic Infusion as a Salvage Treatment After Failed Endovascular Treatment for Cerebral Venous Thrombosis: A Multicenter Experience. Neurocrit Care 2018, 29, 54–61. [Google Scholar] [CrossRef]
  48. Styczen, H.; Tsogkas, I.; Liman, J.; Maus, V.; Psychogios, M.N. Endovascular Mechanical Thrombectomy for Cerebral Venous Sinus Thrombosis: A Single-Center Experience. World Neurosurg. 2019, 127, e1097–e1103. [Google Scholar] [CrossRef]
  49. Mokin, M.; Lopes, D.K.; Binning, M.J.; Veznedaroglu, E.; Liebman, K.M.; Arthur, A.S.; Doss, V.T.; Levy, E.I.; Siddiqui, A.H. Endovascular treatment of cerebral venous thrombosis: Contemporary multicenter experience. Interv. Neuroradiol. 2015, 21, 520–526. [Google Scholar] [CrossRef] [Green Version]
  50. Dashti, S.H.; Hu, V.C.; Fiorella, D.; Mitha, A.P.; Abuquerque, F.C.; McDougall, C.G. Mechanical thrombectomy as first-line treatment for venous sinus thrombosis: Technical considerations and preliminary results using the AngioJet device. J. Neurointerv. Surg. 2011, 5, 49–53. [Google Scholar] [CrossRef]
  51. Lee, C.; Liu, H.; Chen, Y.; Lin, Y.; Wang, J. Suction thrombectomy after balloon maceration for dural venous sinus thrombosis. J. Neurol. Sci. 2016, 365, 76–81. [Google Scholar] [CrossRef]
  52. Poulsen, F.R.; Høgedal, L.; Stilling, M.V.; Birkeland, P.F.; Schultz, M.K.; Rasmussen, J.N. Good clinical outcome after combined endovascular and neurosurgical treatment of cerebral venous sinus thrombosis. Dan. Med. J. 2013, 60, A4724. [Google Scholar] [PubMed]
  53. Mammen, S.; Keshava, S.N.; Moses, V.; Aaron, S.; Ahmed, M.; Chiramel, G.K.; Mani, S.E.; Alexander, M. Role of penumbra mechanical thrombectomy device in acute dural sinus thrombosis. Indian J. Radiol. Imaging 2017, 27, 82–87. [Google Scholar] [CrossRef] [PubMed]
  54. Peng, T.; Dan, B.; Zhang, Z.; Zhu, B.; Liu, J. Efficacy of Stent Thrombectomy Alone or Combined with Intermediate Catheter Aspiration for Severe Cerebral Venous Sinus Thrombosis: A Case-Series. Front. Neurol. 2021, 12, 783380. [Google Scholar] [CrossRef]
  55. Medhi, G.; Parida, S.; Nicholson, P.; Senapati, S.B.; Padhy, B.P.; Medes Pareira, V. Mechanical Thrombectomy for Cerebral Venous Sinus Thrombosis: A Case Series. World Neurosurg. 2020, 140, 148–161. [Google Scholar] [CrossRef]
  56. Tsang, A.C.O.; Hwang, A.C.; Chiu, R.H.Y.; Chan, D.Y.C.; Tsang, F.C.P.; Ho, W.S.; Lee, R.; Leung, G.K.K.; Lui, W.M. Combined aspiration thrombectomy and continuous intrasinus thrombolysis for cerebral venous sinus thrombosis: Technical note and case series. Neuroradiology 2018, 60, 1093–1096. [Google Scholar] [CrossRef] [PubMed]
  57. Yue, X.; Xi, G.; Zhou, Z.H.; Xu, G.; Liu, X. Combined intraarterial and intravenous thrombolysis for severe cerebral venous sinus thrombosis. J. Thromb. Thrombolysis 2010, 29, 361–367. [Google Scholar] [CrossRef]
  58. Saposnik, G.; Barinagarrementeria, F.; Brown, R.D., Jr.; Bushnell, C.D.; Cucchiara, B.; Cushman, M.; deVeber, G.; Ferro, J.M.; Tsai, F.Y. American Heart Association Stroke Council and the Council on Epidemiology and Prevention. 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. [Google Scholar] [CrossRef] [Green Version]
  59. Ferro, J.M.; Bousser, M.; Canhão, P.; Coutinho, J.M.; Crassard, I.; Dentali, F.; Di Minno, M.; Maino, A.; Martinelli, I.; Masuhr, F.; et al. European Stroke Organization guideline for the diagnosis and treatment of cerebral venous thrombosis—Endorsed by the European Academy of Neurology. Eur. J. Neurol. 2017, 24, 1203–1213. [Google Scholar] [CrossRef] [Green Version]
  60. Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. J. Clin. Epidemiol. 2021, 134, 178–189. [Google Scholar] [CrossRef]
  61. Ostovan, V.R.; Foroughi, R.; Rostami, M.; Almasi-Dooghaee, M.; Esmaili, M.; Akbar Bidaki, A.; Behzadi, Z.; Farzadfard, F.; Marbooti, H.; Rahimi-Jaberi, A.; et al. Cerebral venous sinus thrombosis associated with COVID-19: A case series and literature review. J. Neurol. 2021, 268, 3549–3560. [Google Scholar] [CrossRef]
  62. Cavalcanti, D.D.; Raz, E.; Shapiro, M.; Dehkharghani, S.; Yaghi, S.; Lillemoe, K.; Nossek, E.; Torres, J.; Jain, R.; Riina, H.A.; et al. Cerebral Venous Thrombosis Associated with COVID-19. AJNR Am. J. Neuroradiol. 2020, 41, 1370–1376. [Google Scholar] [CrossRef] [PubMed]
  63. Omari, A.; Kally, P.; Schimmel, O.; Kahana, A. Vision Loss Secondary to COVID-19 Associated Bilateral Cerebral Venous Sinus Thromboses. Ophthalmic Plast. Reconstr. Surg. 2022, 38, e65–e67. [Google Scholar] [CrossRef] [PubMed]
  64. Sajjad, A.; Khan, A.F.; Jafri, L.; Kamal, A.K. Successful endovascular mechanical thrombectomy in anticoagulation-resistant COVID-19 associated cerebral venous sinus thrombosis. BMJ Case Rep. 2021, 14, e245405. [Google Scholar] [CrossRef]
  65. Chew, H.S.; Al-Ali, S.; Butler, B.; Rajapakse, D.; Nader, S.K.; Chavda, S.; Lamin, S. Mechanical Thrombectomy for Treatment of Cerebral Venous Sinus Thrombosis in Vaccine-Induced Immune Thrombotic Thrombocytopenia. AJNR Am. J. Neuroradiol. 2022, 43, 98–101. [Google Scholar] [CrossRef] [PubMed]
  66. Wolf, M.E.; Luz, B.; Niehaus, L.; Bhogal, P.; Bäzner, H.; Henkes, H. Thrombocytopenia and Intracranial Venous Sinus Thrombosis after “COVID-19 Vaccine AstraZeneca” Exposure. J. Clin. Med. 2021, 10, 1599. [Google Scholar] [CrossRef] [PubMed]
  67. Cleaver, J.; Ibitoye, R.; Morrison, H.; Flood, R.; Crewdson, K.; Marsh, A.; Abhinav, K.; Bosnell, R.; Crossley, R.; Mortimer, A. Endovascular treatment for vaccine-induced cerebral venous sinus thrombosis and thrombocytopenia following ChAdOx1 nCoV-19 vaccination: A report of three cases. J. NeuroInterv. Surg. 2021, 1–6. [Google Scholar] [CrossRef]
  68. Gurjar, H.; Dhallu, M.; Lvovsky, D.; Sadullah, S.; Chilimuri, S. A Rare Case of Coronavirus Disease 2019 Vaccine-Associated Cerebral Venous Sinus Thrombosis Treated with Mechanical Thrombectomy. Am. J. Case Rep 2022, 23, e935355. [Google Scholar] [CrossRef]
  69. Mirandola, L.; Arena, G.; Pagliaro, M.; Boghi, A.; Naldi, A.; Castellano, D.; Vaccarino, A.; Silengo, D.; Aprà, F.; Cavallo, R.; et al. Massive cerebral venous sinus thrombosis in vaccine-induced immune thrombotic thrombocytopenia after ChAdOx1 nCoV-19 serum: Case report of a successful multidisciplinary approach. Neurol. Sci. 2022, 43, 1499–1502. [Google Scholar] [CrossRef]
  70. Chou, J.; Kim, S.; Kim, S.R.; Jin, J.Y.; Choi, S.W.; Kim, H.; Yoo, J.H.; Park, I.S.; Kim, S.R. Intracerebral Hemorrhage due to Thrombosis with Thrombocytopenia Syndrome after Vaccination against COVID-19: The First Fatal Case in Korea. J. Korean Med. Sci. 2021, 36, e223. [Google Scholar] [CrossRef]
  71. Waraich, A.; Williams, G. Haematuria, a widespread petechial rash, and headaches following the Oxford AstraZeneca ChAdOx1 nCoV-19 Vaccination. BMJ Case Rep. 2021, 14, e245440. [Google Scholar] [CrossRef]
  72. Karsy, M.; Harmer, J.R.; Guan, J.; Brock, A.A.; Ravindra, V.M.; Chung, L.S.; Tkach, A.; Majersik, J.J.; Park, M.S.; Schmidt, R.H. Outcomes in adults with cerebral venous sinus thrombosis: A retrospective cohort study. J. Clin. Neurosci. 2018, 53, 34–40. [Google Scholar] [CrossRef]
  73. Yeo, L.L.L.; Lye, P.P.S.; Yee, K.W.; Cunli, Y.; Ming, T.T.; Ho, A.F.; Sharma, V.K.; Chan, B.P.; Tan, B.Y.; Gopinathan, A. Deep Cerebral Venous Thrombosis Treatment Endovascular Case using Aspiration and Review of the Various Treatment Modalities. Clin. Neuroradiol. 2020, 30, 661–670. [Google Scholar] [CrossRef] [PubMed]
  74. Pfefferkorn, T.; Crassard, I.; Linn, J.; Dichgans, M.; Boukobza, M.; Bousser, M. Clinical features, course and outcome in deep cerebral venous system thrombosis: An analysis of 32 cases. J. Neurol. 2009, 256, 1839–1845. [Google Scholar] [CrossRef] [PubMed]
  75. King, A.B.; O’Duffy, A.E.; Kumar, A.B. Heparin Resistance and Anticoagulation Failure in a Challenging Case of Cerebral Venous Sinus Thrombosis. Neurohospitalist 2015, 6, 118–121. [Google Scholar] [CrossRef]
  76. Xu, Z.; Li, X.; Feng, D.; Wang, T.; Xu, X.; Deng, R.; Zhou, X.; Chen, G. Endovascular Therapy Versus Anticoagulation for Treatment of Cerebral Venous Sinus Thrombosis A Meta-Analysis. Neurologist 2022, 27, 69–73. [Google Scholar] [CrossRef]
  77. Lewis, W.; Saber, H.; Sadeghi, M.; Rajah, G.; Narayanan, S. Transvenous Endovascular Recanalization for Cerebral Venous Thrombosis: A Systematic Review and Meta-Analysis. World Neurosurg. 2019, 130, 341–350. [Google Scholar] [CrossRef] [PubMed]
  78. Ilyas, A.; Chen, C.H.-J.; Raper, D.M.; Ding, D.; Buell, T.; Mastorakos, P.; Liu, K.C. Endovascular mechanical thrombectomy for cerebral venous sinus thrombosis: A systematic review. J. Neurointerv. Surg. 2017, 9, 1086–1092. [Google Scholar] [CrossRef]
  79. Boyle, K.; Joundi, R.A.; Aviv, R.I. An historical and contemporary review of endovascular therapy for acute ischemic stroke. Neurovasc Imaging. 2017, 3, 1. [Google Scholar] [CrossRef]
  80. Shahjouei, S.; Tsivgoulis, G.; Farahmand, G.; Koza, E.; Mowla, A.; Sadr, A.V.; Kia, A.; Far, A.V.; Mondello, S.; Cernigliaro, A.; et al. SARS-CoV-2 and Stroke Characteristics A Report from the Multinational COVID-19 Stroke Study Group. Stroke 2021, 52, e117–e130. [Google Scholar] [CrossRef]
  81. Mowla, A.; Shakibajahromi, B.; Shahjouei, S.; Borhani-Haghighi, A.; Rahimian, N.; Baharvadhdat, H.; Naderi, S.; Khorvash, F.; Altafi, D.; Ebrahimzadeh, S.A.; et al. Cerebral venous sinus thrombosis associated with SARS-CoV-2; a multinational case series. J. Neurol. Sci. 2020, 419, 117183. [Google Scholar] [CrossRef]
  82. McGonagle, D.; De Marco, G.; Bridgewood, C. Mechanisms of Immunothrombosis in Vaccine-Induced Thrombotic Thrombocytopenia (VITT) Compared to Natural SARS-CoV-2 Infection. J. Autoimmun. 2021, 121, 102662. [Google Scholar] [CrossRef] [PubMed]
  83. Mahajan, A.; Hirsch, J.A. Cerebral venous thrombosis after COVID-19 vaccination: The role for endovascular treatment. J. NeuroInterv. Surg. 2022, 1–2. [Google Scholar] [CrossRef] [PubMed]
Jcm 11 04215 g001 550
Figure 1. Illustration of the anatomy of the cerebral sinus and veins [7].
Figure 1. Illustration of the anatomy of the cerebral sinus and veins [7].
Jcm 11 04215 g001
Jcm 11 04215 g002 550
Figure 2. Flow diagram visualizing the selection process for the included publications.
Figure 2. Flow diagram visualizing the selection process for the included publications.
Jcm 11 04215 g002
Table
Table 1. Summary of the 21 records included in this systematic review.
Table 1. Summary of the 21 records included in this systematic review.
ReferenceTreatmentOutcome AssessmentLocalizationComplications
Author (Year)Study TypePeriodn (N)Inclusion Criteria/Treatment AllocationPre-ICHEndovascular TreatmentControl GroupFU (Month)OutcomeDeathRecanal.SSSSSSig STSDVCatheter *ICH **Other
Coutinho et al. (2020) [38]RCT2011–201633 (67)High probability of poor outcome, at least 1 of the following risk factors: mental status disorder, coma state (GCS <9), ICH, or thrombosis of the deep cerebral venous system (exclusion: duration from diagnosis of more than 10 days, pregnancy (women in the puerperium were eligible); thrombocytopenia (platelet count, <100 × 109/L), clinical and radiological signs of impending transtentorial herniation)n = 22n = 33; LT (alteplase, urokinase; up to 72 h): n = 17 (52%); MT: n = 30 (91%) (AngioJet [n = 14], SR [n = 5], B [n = 3], aspiration (A) [n = 3; Penumbra], microcatheter [n = 3], other [n = 9]) n = 34; standard care6, 12mRS 0–1 (12 months): n = 22 (67%) vs. n = 23 (68%); risk ratio 0.99
(95% CI 0.71–1.18)		12 months;
n = 4 (12%)
[vs. n = 1 (3%)]		SSS (6–12 months): 79% vs. 52%, 1.52 (1.02–2.27);
SS (6 months): 96% vs. 86%, 1.13 (0.95–1.33)		n = 23 (70%)n = 17 (52%)l: n = 12 r: n = 15l: n = 16 r: n = 22n = 14 (42%)n = 3 (9%)n = 6 (18%)
(hem. compl.)		NA
Nyberg et al. (2017) [39]retrosp2011–201529 (66)SVT (anticoagulation), decision of treatment teamn = 17 (n = 10 in CC)LT n = 29 (24–72 h); n = 21 additional MT (A, SR, B, AngioJet or combination; not specified)n = 37; standard care3mRS 0–2: 22 vs. 30 (p = 1.0)n = 6 (vs. n = 5)n = 11; full (n = 8), partial (n = 3)n = 25n = 0n = 21n = 25n = 7NNn = 9NN
Siddiqui et al. (2014) [40]retrosp1995–201263 (NN)SVT (anticoagulation) and either coma (GCS < 9), ICH or deteriorationn = 29n = 63; n = 29 LT only, n = 34 MT (plus LT n = 27; AngioJet n = 28, A n = 3, SR n = 1. B n = 2) [LT bolus and continuously depending on recanalization]NA3n = 53; mRS 0–1: n = 33n = 11full (n = 21), partial (n = 18)NNNNNNNNNNn = 5n = 3NN
Guo et al. (2020) [41]retrosp2010–201956 (227 sc)SVT under anticoagulation; ICH, lack of improvement or deterioration of symptomsn = 56n = 56; LT only (n = 41; duration: 7 days); additional MT (n = 15) [SR n = 5, A n = 3, B n = 3, combined n = 4)NA6n = 54; mRS 0–2: n = 49n = 3(full and partial); LT n = 39; MT n = 14NNNNNNNNNNn = 0LT n = 7, MTn = 1NN
Andersen et al. (2020) [42]retrosp2007–201828 (NN)SVT under anticoagulation; clinical deterioration and/or impaired consciousnessn = 18n = 28; LT (n = 26; 12–72 h), A (n = 3), SR (n = 3),
combined (more than 2 techniques; n = 4) incl. PTA and stenting (n = 2)		NA6mRS 0–2: n = 20n = 5full (n = 15), partial (n = 11), no (n = 2)n = 16n = 15n = 15n = 16n = 7n = 1 (retrop. hem.)n = 8NA
Yang et al. (2019) [43]pros CS2014–201821 (27 sc)SVT (anticoagulation) with: ICH, mental status impairment, coma (GCS < 9), DV thrombosis, cortical venous thrombosis, intracranial hypertension, or papilledemaNNNNNA12mRS 0–2: n = 21n = 0full (n = 5), partial (n = 9)n = 16n = 0n = 17n = 19n = 14NNNNNN
Yang et al. (2021) [44]retrosp2017–201923 (NN)SVT (anticoagulation) with: deterioration after the initiation of anticoagulation, lethargy or coma, venous infarction with hemorrhagic transformation or ICHn = 8n = 23; MT (B) plus LT (urokinase)NA6n = 21; mRS 0–1: n = 21n = 0full (n = 9), partial (n = 13)n = 20n = 11n = 21n = 21NNn = 2 (failure)n = 1NN
Stam et al. (2008) [45]pros CSNN20 (NN)SVT (heparin) with assumed poor prognosis: altered mental status, coma, extensive edema, ICH, infarctionn = 14n = 20, LT only (n = 15 additional MT [rheolytic catheter])NA3 (−6)mRS 0–2: n = 12n = 6NNNNNNNNNNn = 20NNn = 1 (ICH progress)NN
Lu et al. (2019) [46]retrosp2015–201814 (NN)SVT (best medical treatment); decision of treatment teamn = 1n = 14; MT (SR or A, combination), additional stenting in n = 5 (in case of failure of SR or A; re- occlusion)NA2 (−16)n = 5 (stenting); mRS 0–1: n = 4n = 0NNn = 0n = 0n = 0n = 5NANNn = 2 (increase)NN
Qureshi et al. (2018) [47]retrosp2006–2011/2016/201714 (NN)SVT (anticoagulation), deteriorationn = 7n = 13 LT, MT: AngioJet n = 9, B n = 2, SR n = 2 (combined) [LT bolus, up to 22 h after MT in case of incomplete recanalization]NA1 (−3)mRS 0–2: n = 10n = 1full (n = 3), partial (n = 4)n = 10n = 1n = 10n = 13n = 0NNNNNN
Styczen et al. (2019) [48]retrosp2011–201813 (NN)SVT (heparin) with assumed poor prognosis: altered mental status or coma, involvement of DV, ICHn = 7n = 13; MT (A n = 4, A plus SR n = 9)NA3 (median)mRS 0–2: n = 12n = 1full (n = 4), partial (n = 7)n = 9n = 5n = 7n = 10NNn = 1 (perf)n = 3NN
Mokin et al. (2015) [49]retrosp2010–201313 (NN)SVT (plus/minus anticoagulation), decision of treatment teamNNn = 13 (LT n = 2 [sinus or ia]; A n = 2; LT plus A n = 3; A plus SR n = 2; AngioJet n = 2, combined n = 3)NA3n = 11; mRS 0–2: n = 5n = 1full (n = 5), partial (n = 8)n = 10n = 7n = 0n = 11n = 0NNNNNN
Dashti et al. (2011) [50]retrosp2009/201013 (NN)NA; decision of treatment teamNNn = 13; AngioJetNANNn = 9; mRS 0–1: n = 7n = 2full (n = 6), partial (n = 7)n = 9NNNNNNNNNNNNn = 1 (re- occl)
Lee et al. (2016) [51]retrosp2008–201510 (NN)SVT under anticoagulation; MT in case of ICH, deep venous thrombosis, deteriorationn = 9n = 10; MT (B plus A [combination]) plus LT (n = 3; before 2013; bolus)NA3mRS 0–1: n = 8n = 1NNn = 6n = 3n = 5n = 9NAn = 0n = 1NN
Poulsen et al. (2013) [52]retrosp2007–20119 (NN)SVT (anticoagulation), deteriorationn = 4n = 6 MT (n = 5 prior LT [24–72 h]; not specified); n = 5 LT onlyNA6mRS 0–2: n = 8n = 1full (n = 2), partial (n = 4)n = 5n = 4n = 0n = 9n = 0n = 0n = 1 (SAH)n = 3 (hem. [eVD])
Mammen et al. (2017) [53]retrosp(4 years)8 (243 sc)SVT (anticoagulation), no response or deteriorationn = 1n = 8 (MT, A [Penumbra] plus additional B (n = 7) and LT (n = 3; bolus)NA6mRS 0–2: n = 5n = 1full (n = 3), partial (n = 4)n = 5n = 5n = 2n = 6n = 3n = 0n = 0n = 0
Peng et al. (2021) [54]retrosp2017–20207 (NN)SVT (anticoagulation); one risk factor (poor outcome): coma (GCS < 9), ICH, DV thrombosisn = 4n = 7 MT (SR; plus A n = 4; plus B n = 4; plus heparin n = 4, plus LT n = 1 [bolus])NA3mRS 0–2: n = 6n = 0full (n = 4), partial (n = 3)n = 7n = 0n = 4n = 5n = 0n = 0n = 0n = 0
Mehdi et al. (2020) [55]retrosp2018/20197 (NN)SVT (anticoagulation), clinical and imaging deterioration (no signs of herniation)n = 3n = 7 (MT; A) plus LT (n = 4; bolus 20 min)NA1 (3, 6)mRS 0–1: n = 5n = 0partial (n = 7)n = 6n = 4n = 0n = 3n = 0n = 0n = 0n = 0
Tsang et al. (2018) [56]CS2014–20186 (NN)SVT (anticoagulation) with deterioration or ICHNNn = 6; MT (A [Penumbra]) plus LT (urokinase)NA3mRS 0–1: n = 5n = 1NNn = 5n = 2n = 3n = 4NNn = 0n = 0n = 0
Jankowitz et al. (2013) [19]retrosp2009–20116 (27 sc)SVT (best medical treatment); clinical (progressive deficits, coma) or radiological (hem., edema) deteriorationn = 4n = 6; MT (A) (n = 6), additional LT n = 4 (bolus)NA6mRS 0–2: n = 4n = 1n = 6n = 3n = 2n = 1n = 3NAn = 0NNn = 0
Yue et al. (2010) [57]retrosp2005–20086 (28 sc)SVT (anticoagulation) with deterioration or assumed poor prognosis: coma, altered mental state, seizure, space-occupying lesions (edema or [hemorrhagic] infarct)n = 2n = 6; MT (B) plus ia T (urokinase)NA3 (−6)mRS 0: n = 5n = 1full (n = 5)n = 6n = 4n = 6n = 6n = 20n = 0n = 0n = 0
* catheter complications such as perforation; ** ICH; new hemorrhage or worsening of a pre-existing intracerebral hemorrhage; n, number of patients; N, total number of patients (patients screened: indicated by [sc]; ICH, intracerebral hemorrhage; FU, follow-up; Recanal., recanalization; SSS, sagittal superior sinus; SS, straight sinus; S Sig, sigmoid sinus; TS, transverse sinus; DV, deep cerebral veins; RCT, randomized controlled trial; restrosp, retrospective, pros, prospective; CS, case series; GCS, Glasgow Coma Scale; SVT, sinus or cerebral vein thrombosis; MT, mechanical thrombectomy; NN, unknown; NA, not applicable; LT, local (intrasinus) thrombolysis; A, aspiration thrombectomy; SR, stent retriever thrombectomy; B, balloon guided thrombectomy or angioplasty; PTA, percutaneous transluminal angioplasty; ia, intra-arterial; T, thrombolysis; mRS, modified Rankin Scale; hem, hemorrhagic or hemorrhage; retrop., retroperitoneal; compl, complication; perf, perforation; SAH, subarachnoid hemorrhage; occl, occluison.
Table
Table 2. Case reports of endovascular therapy in SVT due to COVID-19 or VITT.
Table 2. Case reports of endovascular therapy in SVT due to COVID-19 or VITT.
Reference EtiologyLaboratory FindingsTreatmentOutcomeLocationComplications
Author (Year)Study TypenCOVID-19 (C-19), VITTd (After Index) Treatment AllocationEndovascular TreatmentmRSRecanalization
Ostovan et al. (2021) [62]case series1 (of 9)C-195 (?)TP (140 T/uL), elevated D-dimer levels (>10.000 ng/mL)ICHLT plus MT (A)6fullSSS, TSNN
Cavalcanti et al. (2020) [63]case series1 (of 3)C-1910TP (141 T/uL), elevated D-dimer levels (>55.000 ng/mL)edema, rapid deteriorationMT (A) plus LT (micro-catheter, cont.)6partialSSS, TS, SS, DVNN
Omari et al. (2022) [64]case report1C-1930NNvisual deterioration, intracranial hypertensionNNNNNNTS, S Sigblindness
Sajjad et al. (2021) [65]case report1C-1920TP (NN), PF4 antibodies (NN), elevated D-dimer levels (6.3 mg/L)ICH plus edema, coma, deteriorationFogarty catheter2fullSSSNN
Chew et al. (2021) [66]case series6VITT (ChAdOx1 nCoV-19) *10 (−14)TP (11 T-91 T/uL), PF4 antibodies and D-dimer levels NNICH (n = 5), progressive thrombus material, deterioration (coma)Aspiration (Penumbra)0–1: n = 3; 6: n = 2satisf. (n = 5)NNn = 1 (ICH-progression)
Wolf et al. (2021) [67]case series3VITT (ChAdOx1 nCoV-19)4 (−17)TP (60 T–92 T/uL), PF4 antibodies (positive), elevated D-dimer levels (2120–22,800 ng/mL)SAH (1); ICH (2); coma due to bilateral thalamic edema (3)MT (A [1, 3] plus B [2]) 0 (1, 3); 1 (2)fullSSS, TS (1), SSS, TS, S Sig (2)2 MT sessions needed (2)
Cleaver at al. (2021) [68]case series3VITT (ChAdOx1 nCoV-19)8 (−27)TP (85 T/uL [1], 23 T/uL [2], 35 T/uL [3]); PF4-antibodies positive (all), elevated D-dimer levels (15.83–30.34 μg/mL)progr. ICH/SAH, edema and deterioration (1); progr. ICH and thrombus material (2); new ICH, status epilepticus, intubation (3)MT (A [1], A plus SR [2]) 2 (all)full (2), partial (1, 3)SSS (1), SS, S Sig, TS (2), SSS, S Sig, TS (3)NN
Gurjar et al. (2022) [69]case report1VITT (mRNA-1273 vaccine) **3 monthsTP (139 T/uL), PF4 antibodies (negative), elevated D-dimer levels (16.666 ng/mL)coma, progressive symptomsMT (not specified)3fullSSS, TS, S SigNN
Mirandola et al. (2022) [70]case report1VITT (ChAdOx1 nCoV-19)15TP (40 T/uL), PF4 antibodies (positive), elevated D-dimer levels (18 mcg/mL)progressive thrombus material, edema, coma and seizure requiring intubationMT (A plus SR)0partial (SS), full (rest)SSS, SS, TS, S SigNN
Choi et al. (2021) [71]case report1VITT (ChAdOx1 nCoV-19)12TP (14 T/uL), PF4 antibodies (positive), elevated D-dimer levels (>32.5 mg/L [reference: < 0.5])progressive coma MT (not specified)6fullS SigNN
Waraich et al. (2021) [72]case report1VITT (ChAdOx1 nCoV-19)13TP (14 T/uL), PF4 antibodies NN, elevated D-dimer levels (62.342 ng/mL)deterioration, SAH, seizures requiring CPRNNNN (2 ***)fullSSS, TS, S SigNN
* ChAdOx1 nCoV-19, AstraZeneca vaccine; ** mRNA-1273 vaccine, Moderna; *** not specified, mRS assumed by the authors depending on the symptom description provided; n, number; VITT, vaccine-induced thrombotic thrombocytopenia; d, days; mRS, modified Rankin Scale; TP, thrombocytopenia; PF4; platelet factor 4; T, thousand; ICH, intracerebral hemorrhage; SHA, subarachnoid hemorrhage; CPR, cardiopulmonary resuscitation; NN, unknown; SSS, sagittal superior sinus; SS, straight sinus; S Sig, sigmoid sinus; TS, transverse sinus; DV, deep cerebral veins; SVT, sinus or cerebral vein thrombosis; MT, mechanical thrombectomy; LT, local (intrasinus) thrombolysis; A, aspiration thrombectomy; SR, stent retriever thrombectomy; B, balloon guided thrombectomy or angioplasty; cont, continuous.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Bücke, P.; Hellstern, V.; Cimpoca, A.; Cohen, J.E.; Horvath, T.; Ganslandt, O.; Bäzner, H.; Henkes, H. Endovascular Treatment of Intracranial Vein and Venous Sinus Thrombosis—A Systematic Review. J. Clin. Med. 2022, 11, 4215. https://doi.org/10.3390/jcm11144215

AMA Style

Bücke P, Hellstern V, Cimpoca A, Cohen JE, Horvath T, Ganslandt O, Bäzner H, Henkes H. Endovascular Treatment of Intracranial Vein and Venous Sinus Thrombosis—A Systematic Review. Journal of Clinical Medicine. 2022; 11(14):4215. https://doi.org/10.3390/jcm11144215

Chicago/Turabian Style

Bücke, Philipp, Victoria Hellstern, Alexandru Cimpoca, José E. Cohen, Thomas Horvath, Oliver Ganslandt, Hansjörg Bäzner, and Hans Henkes. 2022. "Endovascular Treatment of Intracranial Vein and Venous Sinus Thrombosis—A Systematic Review" Journal of Clinical Medicine 11, no. 14: 4215. https://doi.org/10.3390/jcm11144215

APA Style

Bücke, P., Hellstern, V., Cimpoca, A., Cohen, J. E., Horvath, T., Ganslandt, O., Bäzner, H., & Henkes, H. (2022). Endovascular Treatment of Intracranial Vein and Venous Sinus Thrombosis—A Systematic Review. Journal of Clinical Medicine, 11(14), 4215. https://doi.org/10.3390/jcm11144215

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop