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Intracranial dural arteriovenous fistulas: association with cerebral venous thrombosis, baseline aggressiveness, and clinical outcomes. A retrospective multicenter study on 263 consecutive patients and literature review

Clara Cohen, Stéphanie Lenck, Atika Talbi, Héloïse Ifergan, Kévin Premat, Grégoire Boulouis, Kévin Janot, Anne-Laure Boch, Christophe Magni, Denis Herbreteau, Nader Sourour, Eimad Shotar, Valère Barrot, and Frédéric Clarençon

OBJECTIVE

The pathogenesis of intracranial dural arteriovenous fistulas (icDAVFs) is controversial. Cerebral vein thrombosis (CVT) and venous hypertension are recognized predisposing factors. This study aimed to evaluate the incidence of association between icDAVF and CVT and describe baseline aggressiveness and clinical outcomes for icDAVFs associated with CVT. The authors also performed a literature review of studies reporting icDAVF associated with CVT.

METHODS

Two hundred sixty-three consecutive patients in two university hospitals with confirmed icDAVFs were included. A double-blind imaging review was performed to determine the presence or absence of CVT close or distant to the icDAVF. Location, type (using the Cognard classification), aggressiveness of the icDAVF, clinical presentation, treatment modality, and clinical and/or angiographic outcomes at 6 months were also collected. All prior brain imaging was analyzed to determine the natural history of onset of the icDAVF.

RESULTS

Among the 263 included patients, 75 (28.5%) presented with a CVT concomitant to their icDAVF. For 18 (78.3%) of 23 patients with previous brain imaging available, CVT preceding the icDAVF was proven (6.8% of the overall population). Former/active smoking (OR 2.0, 95% CI 1.079–3.682, p = 0.022) and prothrombogenic status (active inflammation or cancer/coagulation trouble) were risk factors for CVT associated with icDAVF (OR 3.135, 95% CI 1.391–7.108, p = 0.003). One hundred eighty-seven patients (71.1%) had a baseline aggressive icDAVF, not linked to the presence of a CVT (p = 0.546). Of the overall population, 11 patients (4.2%) presented with spontaneous occlusion of their icDAVF at follow-up. Seven patients (2.7%) died during the follow-up period. Intracranial DAVF + CVT was not associated with a worse prognosis (modified Rankin Scale score at 3–6 months: 0 [interquartile range {IQR} 0–1] for icDAVF + CVT vs 0 [IQR 0–0] for icDAVF alone; p = 0.055).

CONCLUSIONS

This was one of the largest studies focused on the incidence of CVT associated with icDAVF. For 6.8% of the patients, a natural history of CVT leading to icDAVF was proven, corresponding to 78.3% of patients with previous imaging available. This work offers further insights into icDAVF pathophysiology, aiding in identifying high-risk CVT patients for long-term follow-up imaging. Annual imaging follow-up using noninvasive vascular imaging (CT or MR angiography) for a minimum of 3 years after the diagnosis of CVT should be considered in high-risk patients, i.e., smokers and those with prothrombogenic status.

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Introduction. Dural arteriovenous fistulas: multimodal diagnosis, management, and outcomes

Stavropoula Tjoumakaris, Luca Regli, Menno R. Germans, L. Fernando Gonzalez, Ivan Radovanovic, Michihiro Tanaka, and Georges Rodesch

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Letter to the Editor. Platelet transfusion, not just platelets

Yao Sun, Huiying Zhao, and Youzhong An

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Letter to the Editor. Surgical strategies for basilar invagination with or without atlantoaxial instability

Qiang Jian and Tao Fan

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Long-term outcome of endovascular treatment for indirect carotid-cavernous fistulas

Humain Baharvahdat, Farid Qoorchi Moheb Seraj, Amira Al-Raaisi, Raphael Blanc, Sajjad Najafi, Mohammad Hossein Mirbolouk, Hocine Redjem, Feizollah Ebrahimnia, Simon Escalard, Samira Zabihyan, Jean-Philipe Desilles, Ashkan Mowla, Willian Boisseau, Mikael Mazighi, Stanislas Smajda, and Michel Piotin

OBJECTIVE

Endovascular treatment (EVT) is the primary approach used to treat indirect carotid-cavernous fistulas (CCFs). In this study, the authors evaluated the immediate and long-term efficacy and safety of different endovascular techniques for indirect CCFs.

METHODS

The databases of two endovascular centers were retrospectively reviewed to collect the patients with indirect CCFs treated using endovascular techniques between 2013 and 2023. Demographics, clinical presentation, CCF features, EVT characteristics, and clinical and radiological outcomes were evaluated and analyzed. The analysis was performed to compare the clinical and radiological data between different endovascular approaches and different embolic materials.

RESULTS

Ninety-eight patients were included in the study. EVT was successful in 95 patients (96.9%). Immediate complete obliteration of the CCF was achieved in 93.9% of patients, with 98% undergoing embolization with liquid embolic agents (LEAs) and 95.6% undergoing coiling alone. Complete CCF obliteration was higher in the transvenous than in the transarterial approach (94.3% vs 75%, p = 0.010). At ≥ 6 months follow-up, complete CCF obliteration was achieved in all patients (100%). The rate of procedure-related complications was higher following LEAs than with coiling alone (32.0% vs 15.6%). New cranial nerve (CN) palsy was diagnosed in 26.0% and 2.2% after embolization with LEAs and coiling alone, respectively (p = 0.001), with complete CN palsy recovery in 78.6%. Procedure-related intracranial hemorrhage occurred in 3 patients (3.1%). Two patients experienced an ischemic stroke following Onyx migration into the internal carotid artery. Ocular symptoms improved in 93% (83/89) of the patients who were followed.

CONCLUSIONS

In this study, complete obliteration of an indirect CCF was achieved in more than 90% of patients. Despite the occurrence of some new postprocedural ocular CN palsy, ocular symptoms improved in most patients in long-term follow-up. The transvenous approach was the most effective method for treating the indirect CCF. Coiling was safer than LEAs for the embolization of the indirect CCF.

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Long-term treatment outcomes and natural course of low-grade intracranial dural arteriovenous fistulas

Tobias Rossmann, Michael Veldeman, Elias Oulasvirta, Ville Nurminen, Philip-Rudolf Rauch, Andreas Gruber, Martin Lehecka, Mika Niemelä, Jussi Numminen, and Rahul Raj

OBJECTIVE

In contrast to high-grade dural arteriovenous fistula (dAVF), low-grade dAVF is mainly associated with tinnitus and carries a low risk of morbidity and mortality. It remains unclear whether the benefits of active interventions outweigh the associated risk of complications in low-grade dAVF.

METHODS

The authors conducted a retrospective single-center study that included all consecutive patients diagnosed with an intracranial low-grade dAVF (Cognard type I and IIa) during 2012–2022 with DSA. The authors analyzed symptom relief, symptomatic angiographic cure, treatment-related complications, risk for intracerebral hemorrhage (ICH), and mortality. All patients were followed up until the end of 2022.

RESULTS

A total of 81 patients were diagnosed with a low-grade dAVF. Of these, 48 patients (59%) underwent treatment (all primary endovascular treatments), and 33 patients (41%) did not undergo treatment. Nine patients (19%) underwent retreatments. Angiographic follow-up was performed after median (IQR) 7.7 (6.1–24.1) months by means of DSA (mean 15.0, median 6.4 months, range 4.5–83.4 months) or MRA (mean 29.3, median 24.7 months, range 5.9–62.1 months). Symptom control was achieved in 98% of treated patients after final treatment. On final angiographic follow-up, 73% of patients had a completely occluded dAVF. There were 2 treatment-related complications resulting in 1 transient (2%) and 1 permanent (2%) neurological complication. One patient showed recurrence and progression of a completely occluded low-grade dAVF to an asymptomatic high-grade dAVF. No cases of ICH- or dAVF-related mortality were found in either treated patients (median [IQR] follow-up 5.1 [2.0–6.8] years) or untreated patients (median [IQR] follow-up 5.7 [3.2–9.0] years).

CONCLUSIONS

Treatment of low-grade dAVF provides a high rate of symptom relief with small risks for complications with neurological sequela. The risks of ICH and mortality in patients with untreated low-grade dAVF are minimal. Symptoms may not reveal high-grade recurrence, and radiological follow-up may be warranted in selected patients with treated low-grade dAVF. An optimal radiographic follow-up regimen should be developed by a future prospective multicenter registry.

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Microsurgical versus endovascular treatment of ethmoidal dural arteriovenous fistulas: systematic review and meta-analysis with a single-center case series

Chandler N. Berke, Anant Naik, Neil Majmundar, Sean Munier, Raphia Rahman, Ahsan Sattar, Priyank Khandelwal, and James K. Liu

OBJECTIVE

Ethmoidal dural arteriovenous fistulas (DAVFs) are often associated with cortical venous drainage (CVD) and a higher incidence of hemorrhage compared with DAVFs in other locations. They may be treated with open surgical disconnection or with endovascular treatment (EVT). In this systematic review and meta-analysis, the authors compare the outcomes of ethmoidal DAVFs treated with open microsurgery versus EVT and report four additional cases of ethmoidal DAVFs treated with open microsurgery in their institution.

METHODS

A literature search of the PubMed and Scopus databases was conducted between December 2021 and May 2022 to identify relevant articles published between 1990 and 2021 using the PRISMA guidelines. References were reviewed and screened by two authors independently, and disagreements were resolved through consensus. Exclusion criteria included non–English-language studies, those with an incorrect study design, those reporting DAVFs in a nonethmoidal location, and studies whose outcomes were not stratified based on DAVF location. Inclusion criteria were any studies reporting on ethmoidal DAVFs treated by either microsurgery or EVT. A risk of bias assessment was performed using the Newcastle-Ottawa Scale. The authors performed a pooled proportional meta-analysis to compare patient outcomes.

RESULTS

Twenty studies were included for analysis. Of 224 patients, 142 were treated with surgery, while 103 were treated with EVT. Seventy percent (148/210) of the patients were symptomatic at presentation, with hemorrhage being the most common presentation (48%). CVD was present in 98% of patients and venous ectasia in 61%. The rates of complete DAVF obliteration with surgery and EVT were 89% and 70%, respectively (95% CI −30% to −10%, p < 0.03). Twenty percent (21/103) of endovascularly treated fistulas required subsequent surgery. Procedure-related complications occurred in 10% of the surgical cases, compared with 13% of the EVT cases. The authors’ case series included 4 patients with ethmoidal DAVFs treated surgically with complete obliteration, without any postoperative complications.

CONCLUSIONS

The complete obliteration rates of ethmoidal DAVF appear to be higher and more definitive with microsurgical intervention than with EVT. While complication rates between the two procedures seem similar, patients treated with EVT may require further interventions for definitive treatment. The limitations of this study include its retrospective nature, the quality of studies included, and the continued evolving technologies of EVT. Future studies should focus on the association between venous drainage pattern and the proclivity toward venous ectasia or rate of hemorrhage at presentation.

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The negative impact of treatment delays on the long-term neurological outcomes of spinal dural arteriovenous fistulas: a longitudinal cohort study

Victor Gabriel El-Hajj, Cornelia Daller, Alexander Fletcher-Sandersjöö, Maria Gharios, Mohamad Bydon, Michael Söderman, Pascal Jabbour, Erik Edström, Adrian Elmi-Terander, and Fabian Arnberg

OBJECTIVE

Dural arteriovenous fistulas are rare vascular malformations that affect the brain and spinal cord. Spinal dural arteriovenous fistulas (sdAVFs) are the most frequently encountered vascular malformation affecting the spinal cord. The object of this study was to evaluate the impact of treatment delays on the long-term neurological outcomes of either open surgical or interventional treatment of sdAVFs.

METHODS

In this retrospective, population-based cohort study, the authors examined consecutive patients with diagnosed sdAVFs at a tertiary care center between 2005 and 2020. Patients were assessed using the Aminoff-Logue disability scale (ALS) at various time points including symptom onset, primary care visit, first specialist outpatient visit, as well as both short and long-term follow-ups. The postoperative long-term ALS gait and bladder grades constituted the primary outcomes of the study.

RESULTS

Among the 34 patients included in the study, the median age was 65 years, and there was a male predominance (71%). Most lesions were in the lumbar region (47%). Significant worsening in ALS gait and bladder grades was observed preoperatively, followed by postoperative improvements (p < 0.05). There was no difference in outcomes between surgical and endovascular treatments. Older age (OR 1.10, 95% CI 1.03–1.17, p = 0.007), worse preoperative ALS gait grades (OR 5.12, 95% CI 2.18–12.4, p < 0.001), and longer time from first specialist outpatient visit to first treatment (OR 1.00, 95% CI 1.00–1.01, p = 0.040) were independently associated with worse long-term gait outcomes. Only the preoperative ALS bladder score was a predictor of worse long-term bladder function (OR 92.7, 95% CI 28.0–306.7, p < 0.001).

CONCLUSIONS

Both surgical and endovascular treatments for sdAVFs led to significant neurological improvements. However, treatment delays were associated with less favorable long-term outcomes. Prompt diagnosis and early intervention prior to symptom progression may enhance recovery and help to preserve neurological function.

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Safety evaluation of sinus patency after stereotactic radiosurgery for transverse–sigmoid sinus dural arteriovenous fistulas: implications of treatment options for patients with Borden type I fistulas

Motoyuki Umekawa, Yuki Shinya, Hirotaka Hasegawa, Satoshi Koizumi, Atsuto Katano, and Nobuhito Saito

OBJECTIVE

This study aimed to assess the efficacy and safety of stereotactic radiosurgery (SRS) in treating transverse–sigmoid sinus dural arteriovenous fistulas (TSS DAVFs), and to investigate post-SRS sinus patency, focusing on the risk factors associated with treated sinus occlusion.

METHODS

Data from 34 patients treated with SRS between January 2006 and April 2023 were analyzed. Detailed angioarchitecture was confirmed using digital subtraction angiography before SRS. Angiography of the ipsilateral internal carotid artery and vertebral artery was performed to evaluate whether the involved side of the TSS was used for normal venous drainage. TSS stenosis was defined as sinus diameter < 50% of the normal proximal diameter. DAVF shunt obliteration, TSS occlusion, neurological status, and adverse events were also evaluated.

RESULTS

Of the 34 patients, 21 had Borden type I and 14 had Borden type II DAVFs. The median age at SRS was 64 years (interquartile range 54–71 years), and the follow-up period was 31 months (interquartile range 15–94 months). Complete shunt obliteration was achieved in 24 (70.6%) patients. The cumulative 2-, 3-, and 5-year shunt obliteration rates were 49.6%, 71.2%, and 86.0%, respectively. Borden type I had higher obliteration rates (60.5%, 83.1%, and 94.4%, respectively) than Borden type II (41.7%, 51.4%, and 75.7%, respectively; p = 0.034). TSS occlusion occurred in 5 patients (14.7%). The cumulative 1-, 5-, and 10-year TSS occlusion rates were 2.9%, 8.3%, and 23.6%, respectively, across the entire cohort. All occlusions occurred exclusively in the sinuses that were not used for normal venous drainage. Cox proportional analyses revealed that TSS stenosis and the sinus not being used for normal venous drainage were significantly associated with a greater risk of TSS occlusion after SRS (HR 9.44, 95% CI 1.01–77.13; p = 0.049).

CONCLUSIONS

SRS is effective and safe for TSS DAVF and results in favorable shunt obliteration, symptom improvement, and low complication rates. TSS occlusion after SRS is asymptomatic and is limited to sinuses that are not used for normal venous drainage.

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Stereotactic radiosurgery with versus without embolization for intracranial dural arteriovenous fistulas: a systematic review and meta-analysis

Seyed Farzad Maroufi, Mohammad Sadegh Fallahi, Moein Ghasemi, and Jason P. Sheehan

OBJECTIVE

Stereotactic radiosurgery (SRS) has been established as a safe and alternative treatment for dural arteriovenous fistulas (dAVFs). While embolization alone is the most commonly used modality for the treatment of dAVFs, the adjunctive use of embolization with SRS, with the growing use of SRS, has gained increasing interest in the past few years. However, the relative efficacy and safety of SRS combined with embolization versus SRS alone for dAVFs remains uncertain. Hence, this systematic review aimed to evaluate the efficacy of SRS with adjunctive embolization for intracranial dAVFs.

METHODS

A systematic review and meta-analysis was conducted by searching electronic databases, including PubMed, Embase, and the Cochrane Library, up to August 2023. All studies evaluating the utilization of adjunctive embolization and SRS for dAVFs were included. Risk of bias was assessed using the Newcastle-Ottawa Scale. A meta-analysis was conducted on the suitable outcomes.

RESULTS

Eighteen studies involving 715 patients were included. The mean age of the participants in the study was 64.30 years in the adjunctive embolization group and 60.51 years in the SRS-alone group. In the adjunctive embolization group 41.3% of patients were female, compared with 47.1% in the SRS-only group. The dAVF obliteration rates were 64.7% and 65.7% in the adjunctive embolization and SRS-alone groups, respectively. These obliteration rates were comparable between the two groups (p = 0.96), as were the symptom improvement rates (p = 0.35). Adverse events were rare, and were more commonly associated with the adjunctive embolization procedure, although further causal analysis was not possible.

CONCLUSIONS

This study provides evidence that adjunctive embolization plus SRS provides similar obliteration and symptom improvement rates compared with SRS alone, with both having very limited SRS-related adverse events. Considering the added burden and adverse events of additional endovascular treatment, the authors recommend embolization be reserved for more complex dAVFs or when embolization can potentially be curative alone or provide more rapid symptomatic relief or protection during the radiosurgical latency period.