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J Stroke > Volume 26(2); 2024 > Article
Shoskes, Shu, Nguyen, Abdalkader, Giles, Amar, Siegler, Henninger, ElNazeir, Kasab, Klein, Heldner, Antonenko, Psychogios, Liebeskind, Field, Liberman, Esenwa, Simpkins, Li, Frontera, Kuohn, Rothstein, Khazaal, Aziz, Mistry, Khatri, Omran, Zubair, Sharma, Starke, Morcos, Romano, Yaghi, and Asdaghi: Prevalence and Associations of Dural Arteriovenous Fistulae in Cerebral Venous Thrombosis: Analysis of ACTION-CVT
Dear Sir:
Dural arteriovenous fistulae (DAVFs) represent approximately 10% of all intracranial vascular malformations [1] with an incidence of 0.16-1.04 per 100,000 person-years [2,3]. Prior studies identified an association between cerebral venous thrombosis (CVT) and DAVF although the direction of causality remains uncertain. In one series, 39% of DAVF patients had a CVT identified within an adjacent or downstream sinus [4], and patients with DAVF have a higher prevalence of thrombophilia, implicating thrombosis in its pathogenesis [5]. We aimed to determine the prevalence and associated factors of DAVF in a large multicenter study of treated CVT.
The Anticoagulation in the Treatment of Cerebral Venous Thrombosis (ACTION-CVT) study was a multicenter retrospective study comparing outcomes among CVT patients treated with a vitamin K antagonist versus direct oral anticoagulants [6]. The study included consecutive patients with acute CVT from January 1, 2015 through December 31, 2020. Patients were identified using the International Classification of Diseases (ICD)-9/10 codes, and diagnoses were confirmed by retrospective review of records and imaging studies. Institutional review board (IRB) approval was obtained at each center and informed consent was waived by IRB.
Abstracted patient variables are included in Table 1. Radiographic variables at time of presentation included venous infarction, cerebral edema, intracranial hemorrhage, and CVT location divided into cortical veins, superficial sinuses (superior sagittal, transverse, or sigmoid sinus), and deep sinuses (internal cerebral veins, straight sinus, or vein of Galen). Information about recanalization was abstracted from radiology reports of imaging obtained subsequent to the initial hospitalization for CVT and was subdivided into complete (full recanalization without residual thrombus), partial (improved opacification/flow but residual thrombus), and no recanalization (no change or worsening in opacification/flow). Characteristics of DAVF (laterality, location, timing, Borden classification, and treatment of DAVF) were retrospectively reviewed by individual sites.
Clinical, imaging, and anticoagulation characteristics of patients with versus without DAVF were compared using chi-square, Fisher’s exact, and rank sum tests as appropriate. Stepwise multivariable logistic regression analysis including clinical variables with P<0.2 in univariate analysis were used to determine factors associated with DAVF, and variables with P<0.05 from the stepwise regression were included in the final logistic regression to identify factors associated with DAVF. Missing data were not imputed for the initial multivariable analysis, and patients with missing data were excluded. In additional analyses, we conducted mean imputation for missing data and built multivariable binary logistic regression models to determine predictors of DAVF using the imputed values.
A total of 1,024 patients met inclusion criteria of whom 62.8% were female with median age of 44 years, and 751 (73.3%) had follow-up imaging available after hospitalization. Over a median follow-up of 284 days (interquartile range [IQR] 111-685 days), 19 patients (1.9%, 95% confidence interval [CI] 1.0%-2.7%) had DAVF. Patients with DAVF had a median age of 55 years, 36.8% were female, and 72.2% were White (Table 1). Patients with DAVF were older (median age 55 [IQR 45-64] vs. 44 [IQR 32-58], P=0.03), more likely to be male (63.2% vs. 36.7%, P=0.03), and less likely to have headache as a presenting CVT symptom (47.4% vs. 75.1%, P=0.01). Other clinical variables did not vary between the two groups (Table 1). Absent venous recanalization on follow-up imaging was more common among patients with DAVF compared to those without (50.0% vs. 14.9%, P<0.01) (Table 2), while there was no difference in CVT location or the presence of venous infarction, hemorrhage, or cerebral edema. In the stepwise binary logistic regression analysis including clinical variables with P<0.2 in univariate analysis (age, sex, headache, seizure, cortical vein involvement, and lack of recanalization), only cortical vein involvement (P=0.01) and absent venous recanalization (P=0.01) met the threshold for significance and in the final regression analysis both cortical vein involvement (OR 8.00, 95% CI 1.63-39.27, P=0.01) and absent venous recanalization on follow-up imaging (OR 6.28, 95% CI 1.60-24.68, P=0.01) were independently associated with detection of DAVF. In additional analyses imputing missing data, headache inversely correlated with DAVF (OR 0.31, 95% CI 0.11-0.85, P=0.020) and no recanalization on follow-up imaging remained a significant predictor of DAVF (OR=5.37, 95% CI 1.56-18.3, P=0.008).
DAVF was detected at a median of 44 days from diagnosis of CVT (IQR 0-242) (Table 3). Overall, 8 (42.1%) patients were diagnosed with DAVF within 7 days of CVT diagnosis and 11 (57.9%) were noted to have the DAVF on follow-up imaging (median 194 days). Eight fistulae were Borden type I (42.1%), five were Borden type II (26.3%), and six were Borden type III (31.5%). The majority of patients (n=15, 78.9%) underwent surgical or endovascular treatment of the DAVF.
In this international multicenter cohort of 1,024 patients diagnosed with CVT, 19 (1.9%) DAVF were identified including 11 that were not recognized during initial hospitalization for CVT. Cortical vein thrombosis and absent recanalization on follow-up imaging were independently associated with DAVF.
Our findings are in keeping with prior studies on this subject demonstrating a higher prevalence of DAVF among patients with CVT as compared to the reported incidence rate of DAVF in population-based studies [2,3]. In an International Cerebral Venous Thrombosis Consortium study, DAVF was detected in 2.4% of CVT patients and was associated with male gender, chronic CVT, and older age [7]. Several pathophysiological events have been proposed to underly the de novo formation of DAVF after CVT including neovascularization secondary to venous hypertension caused by CVT [8] or enlargement of pre-existing shunts between meningeal arteries and dural venous sinuses. The observation that venous hypertension appears to play a role in DAVF formation offers an explanation as to why absent CVT recanalization is a risk factor of DAVT. Cortical vein thrombosis has not been associated with DAVF in prior studies, but has previously been described in 17%-61% of patients with CVT [9,10], and involvement of cortical veins is associated with higher prevalence of venous infarction/hemorrhage and worse outcomes [10].
Despite the strengths of a large international multicenter cohort, our study has several limitations. Limited information regarding characteristics of DAVFs was available, restricting our ability to comment on clinical symptoms suggestive of DAVF or the decision to treat or observe the DAVF. Furthermore, ACTIONCVT did not capture all lab values of systemic hypercoagulability (such as d-dimer) and given the known association between hypercoagulability and DAVF, this reflects an area of potential future study. Follow-up imaging was not systematically obtained for all patients (performed in 751/1,024 [73.9%] within the cohort), different sites had variable imaging practices, and the indication for choosing the imaging modality was not reported. Only 4% of patients underwent digital subtraction angiography (DSA) in our study (which may result in under-recognition as it is the gold standard for detection of DAVF) and it is likely that those that underwent DSA did so due to concern for DAVF on initial imaging. Finally, the direction of causality between DAVF and CVT remains uncertain given the possibility of a DAVF being missed on initial imaging, and it is possible that in some cases that the presence of a DAVF was the reason for lack of venous recanalization and not the result of lack of recanalization of a CVT.
In this large multicenter study of patients with CVT, cortical vein thrombosis and lack of venous recanalization at follow-up were independently associated with DAVF. The present study reinforces the association between CVT and DAVF as both concomitant diagnoses as well as the potential for DAVF formation after CVT identification.


Funding statement
Conflicts of interest
The authors have no financial conflicts of interest.
Author contribution
Conceptualization: ASh, LS, SY, NA. Study design: ASh, LS, SY, NA. Methodology: ASh, LS, SY, NA. Data collection: LS, TN, MA, JG, JA, JS, NH, ME, SK, PK, MH, KA, MP, DL, TF, AL, CE, ASi, GL, JF, LK, AR, OK, YA, EM, PK, SO, AZ, RSh, SY. Investigation: all authors. Statistical analysis: LS, SY. Writing—original draft: ASh, LS, SY, NA. Writing—review & editing: all authors. Approval of final manuscript: all authors.

Table 1.
Characteristics of patients with and without dural arteriovenous fistulae
Characteristics Total (n=1,024) Dural arteriovenous fistula (n=19) No dural arteriovenous fistula (n=1,005) P
 Age (yr) 44 (32-58) 55 (45-64) 44 (32-58) 0.03
 Female sex 643 (62.8) 7 (36.8) 636 (63.3) 0.03
  White 710/1,017 (69.8) 13/18 (72.2) 697/999 (69.8) 0.99
  Black 160/1,017 (15.7) 3/18 (16.7) 157/999 (15.7) 0.99
  Asian 39/1,017 (3.8) 0/18 (0.0) 39/999 (3.9) 0.99
  Hispanic 102/1,013 (10.1) 1/19 (5.3) 101/994 (10.2) 0.71
 Body mass index (kg/m2) 28 (23.90-33.10) 28.4 (24.37-32.5) 28 (23.87-33.1) 0.78
Medical history
 Prior venous thromboembolism 121/1,024 (11.8) 3/19 (15.8) 118/1,005 (11.7) 0.48
 Birth control use 235/1,006 (23.4) 2/19 (10.5) 233/987 (23.6) 0.27
 Active smoking 146/1,018 (14.3) 1/18 (5.6) 145/1,000 (14.5) 0.50
 Recent head trauma 89/1,023 (8.7) 1/19 (5.3) 88/1,004 (8.8) 0.99
 1 or more antiphospholipid antibodies 82/839 (9.7) 0/18 (0.0) 82/821 (10.0) 0.24
 Factor V leiden or prothrombin gene mutation 75/759 (9.9) 3/15 (20.0) 72/684 (10.5) 0.21
 Symptoms to diagnosis (days) 4 (1-10) 2.5 (0-21) 4 (1-10) 0.41
 Symptoms to anticoagulation (days) 5 (2-12) 4.5 (2-23.5) 5 (2-12) 0.68
Presenting symptoms
 Headache 762/1,022 (74.5) 9/19 (47.4) 753/1,003 (75.1) 0.01
 Isolated headache 357/1,023 (34.8) 7/19 (36.8) 350/1,004 (34.9) 0.81
 Papilledema 100/957 (10.4) 1/17 (5.9) 99/940 (10.5) 0.99
 Focal neurologic deficit 401/1,023 (39.1) 5/19 (26.3) 396/1,004 (39.4) 0.34
 Seizure 243/1,023 (22.9) 1/19 (5.3) 242/1,004 (24.1) 0.06
 Encephalopathy 209/1,023 (20.4) 4/19 (21.1) 205/1,004 (20.4) 0.99
 Coma 29/1,023 (2.8) 0/19 (0.0) 29/1,004 (2.9) 0.99
 Unfractionated heparin 768/1,024 (74.8) 13/19 (68.4) 753/1,005 (74.9) 0.59
 Low molecular weight heparin 625/1,024 (61.0) 10/19 (52.6) 615/1,005 (61.2) 0.48
 Vitamin-K antagonist first 579/1,024 (56.6) 13/19 (68.4) 566/1,005 (56.3) 0.36
 Direct oral anticoagulant first 320/1,024 (31.3) 4/19 (21.1) 316/1,005 (31.4) 0.46
 Oral anticoagulation duration (days) 187.5 (61-392.5) 108 (15-375) 188 (61-393) 0.48
Data are presented as median (interquartile range) or n (%).
Table 2.
Imaging characteristics of patients with and without dural arteriovenous fistulae
Characteristics Total (n=1,024) Dural arteriovenous fistulae (n=19) No dural arteriovenous fistulae (n=1,005) P
Venous sinus thrombosis location
 Deep vein 248/1,022 (24.3) 4/19 (21.1) 244/1,003 (24.3) 0.99
 Cortical vein 30/1,022 (2.9) 2/19 (10.5) 28/1,003 (2.8) 0.11
 Superficial veins 744/1,022 (72.8) 13/19 (68.4) 731/1,003 (72.9) 0.61
 Superficial and deep 130/1,022 (12.7) 2/19 (10.5) 128/1,003 (12.8) 0.99
Associated imaging findings
 Venous infarct 273/1,020 (23.2) 6/18 (33.3) 267/1,002 (26.6) 0.59
 Edema 318/1,020 (31.2) 7/18 (38.9) 311/1,002 (31.0) 0.45
 Hemorrhage 389/1,019 (38.2) 6/18 (33.3) 383/1,001 (38.3) 0.81
Timing of follow-up imaging
 Time to recanalization imaging (days) 180 (93-300) 194 (101-545) 180 (92.5-300) 0.39
Follow-up imaging modality
 Computed tomography 253/751 (33.7) 4/13 (30.8) 249/738 (33.7) 0.99
 Magnetic resonance 572/751 (76.2) 7/13 (53.8) 565/738 (76.6) 0.09
 Conventional angiogram 31/751 (4.1) 5/13 (38.5) 26/738 (3.5) <0.01
 No recanalization 114/730 (15.6) 7/14 (50.0) 107/716 (14.9) <0.01
Data are presented as median (interquartile range) or n (%).
Table 3.
Characteristics of dural arteriovenous fistulae identified in cerebral venous thrombosis patients
No. Imaging modality Days from presentation to fistula diagnosis Fistula location Borden classification Treatment
1 MR 0 Posterior fossa 1 Yes
2 CT 0 Right transverse 2 Yes
3 CT 0 Superior sagittal sinus 2 Yes
4 CT 0 Left tentorial draining into torcula 1 Yes
5 CT 0 Right transverse sinus 2 Yes
6 MR 0 Right sigmoid sinus 3 Yes
7 MR 1 Right transverse and sigmoid sinuses 2 Yes
8 DSA 4 Left transverse and sigmoid sinuses 3 Yes
9 MR 28 Right transverse sinus 1 Yes
10 MR 44 Left transverse sinus and cortical veins 2 Yes
11 MR 100 Left transverse sinus 1 No
12 DSA 101 Right transverse sinus 1 No
13 CT 174 Left sigmoid 1 Yes
14 CT 194 Posterior fossa 3 Yes
15 MR 290 Right and left transverse sinuses and deep venous system, intracranial cortical draining veins 3 Yes
16 DSA 333 Right tentorial 3 Yes
17 DSA 492 Left transverse and sigmoid sinuses 1 No
18 MR 660 Posterior fossa 3 Yes
19 DSA 688 Posterior right frontal lobe 1 No
MR, magnetic resonance; CT, computed tomography; DSA, digital subtraction angiography.


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