Download PDF
Thromb Haemost 2021; 121(10): 1345-1352
DOI: 10.1055/s-0041-1723991
Stroke, Systemic or Venous Thromboembolism

Dural Arteriovenous Fistula Formation Secondary to Cerebral Venous Thrombosis: Longitudinal Magnetic Resonance Imaging Assessment Using 4D-Combo-MR-Venography

Florian F. Schuchardt
1   Department of Neurology and Neurophysiology, Medical Center – University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany
,
Theo Demerath
2   Department of Neuroradiology, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany
,
Samer Elsheikh
2   Department of Neuroradiology, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany
,
Thomas Wehrum
1   Department of Neurology and Neurophysiology, Medical Center – University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany
,
Andreas Harloff
1   Department of Neurology and Neurophysiology, Medical Center – University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany
,
Horst Urbach
2   Department of Neuroradiology, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany
,
Stephan Meckel
2   Department of Neuroradiology, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany
3   Department of Neuroradiology, Kepler University Hospital Linz, Neuromed Campus, Linz, Austria
› Author Affiliations Funding This work was partially supported by Forschungskommission, Medical Faculty, Albert-Ludwigs-University, Freiburg (SCHU 1097/16).
› Further Information
Also available at
    Permissions and Reprints

Abstract

Background and Purpose Dural arteriovenous fistulae (DAVFs) can develop secondary to cerebral venous thrombosis (CVT). The incidence of DAVF has not yet been investigated prospectively.

Methods Between July 2012 and January 2018, combined static and dynamic 4D MR venography (4D-combo-MRV) was performed in 24 consecutive patients at diagnosis of CVT and after 6 months. 3 Tesla magnetic resonance imaging with time of flight and contrast-enhanced magnetization-prepared rapid acquisition with gradient echo were performed at baseline to evaluate the extent of thrombosis and affected vessel segments. Baseline and follow-up 4D-combo-MRV were assessed for signs of DAVF. Interrater reliability of DAVF detection and the extent of recanalization were analyzed with kappa statistics.

Results DAVFs were detected in 4/30 CVT patients (13.3%, 95% confidence interval [CI] 3.3–26.7). Two of 24 patients (8.3%, 95% CI: 0–20.8) had coincidental DAVF with CVT on admission. At follow-up, de novo formation of DAVF following CVT was seen in 2/24 patients (8.3%, 95% CI: 0–20.8). Both de novo DAVFs were low grade and benign fistulae (Cognard type 1, 2a), which had developed at previously thrombosed segments. Endovascular treatment was required in two high degree lesions (Cognard 2a + b) detected at baseline and in one de novo DAVF (Cognard 1) because of debilitating headache and tinnitus. Thrombus load, vessel recanalization, and frequency of cerebral lesions (hemorrhage, ischemia) were not associated with DAVF occurrence.

Conclusion This exploratory study showed that de novo DAVF formation occurs more frequently than previously described. Although de novo DAVFs were benign, 75% of all detected DAVFs required endovascular treatment. Therefore, screening for DAVF by dynamic MRV, such as 4D-combo-MRV, seems worthwhile in CVT patients.

Keywords

cerebral venous sinus thrombosis - dural arteriovenous fistulae - endovascular treatment - recanalization - 4D-combo-MRV

Supplementary Material



Publication History

Received: 17 July 2020

Accepted: 28 December 2020

Article published online:
03 March 2021

© 2021. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 van Dijk JMC, terBrugge KG, Willinsky RA, Wallace MC. Clinical course of cranial dural arteriovenous fistulas with long-term persistent cortical venous reflux. Stroke 2002; 33 (05) 1233-1236
    CrossrefPubMedGoogle Scholar
  • 2 Ferro JM, Lopes MG, Rosas MJ, Ferro MA, Fontes J. Cerebral Venous Thrombosis Portugese Collaborative Study Group. Long-term prognosis of cerebral vein and dural sinus thrombosis. results of the VENOPORT study. Cerebrovasc Dis 2002; 13 (04) 272-278
    CrossrefPubMedGoogle Scholar
  • 3 Ferro JM, Canhão P, Stam J, Bousser MG, 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 (03) 664-670
    CrossrefPubMedGoogle Scholar
  • 4 Preter M, Tzourio C, Ameri A, Bousser MG. Long-term prognosis in cerebral venous thrombosis. Follow-up of 77 patients. Stroke 1996; 27 (02) 243-246
    CrossrefPubMedGoogle Scholar
  • 5 Chen L, Zhao Y, Chen Z, Tee M, Mao Y, Zhou L-F. Multiple dynamic cavernous malformations in a girl: long-term follow-up. Surg Neurol 2009; 72 (06) 728-732
    CrossrefPubMedGoogle Scholar
  • 6 Cognard C, Gobin YP, Pierot L. et al. Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology 1995; 194 (03) 671-680
    CrossrefPubMedGoogle Scholar
  • 7 Cognard C, Houdart E, Casasco A, Gabrillargues J, Chiras J, Merland JJ. Long-term changes in intracranial dural arteriovenous fistulae leading to worsening in the type of venous drainage. Neuroradiology 1997; 39 (01) 59-66
    CrossrefPubMedGoogle Scholar
  • 8 Satomi J, van Dijk JMC, Terbrugge KG, Willinsky RA, Wallace MC. Benign cranial dural arteriovenous fistulas: outcome of conservative management based on the natural history of the lesion. J Neurosurg 2002; 97 (04) 767-770
    CrossrefPubMedGoogle Scholar
  • 9 Kim DJ, terBrugge K, Krings T, Willinsky R, Wallace C. Spontaneous angiographic conversion of intracranial dural arteriovenous shunt: long-term follow-up in nontreated patients. Stroke 2010; 41 (07) 1489-1494
    CrossrefPubMedGoogle Scholar
  • 10 Shah MN, Botros JA, Pilgram TK. et al. Borden-Shucart Type I dural arteriovenous fistulas: clinical course including risk of conversion to higher-grade fistulas. J Neurosurg 2012; 117 (03) 539-545
    CrossrefPubMedGoogle Scholar
  • 11 Reynolds MR, Lanzino G, Zipfel GJ. Intracranial dural arteriovenous fistulae. Stroke 2017; 48 (05) 1424-1431
    CrossrefPubMedGoogle Scholar
  • 12 Nishimura S, Hirai T, Sasao A. et al. Evaluation of dural arteriovenous fistulas with 4D contrast-enhanced MR angiography at 3T. Am J Neuroradiol 2010; 31 (01) 80-85
    CrossrefPubMedGoogle Scholar
  • 13 Farb RI, Agid R, Willinsky RA, Johnstone DM, Terbrugge KG. Cranial dural arteriovenous fistula: diagnosis and classification with time-resolved MR angiography at 3T. Am J Neuroradiol 2009; 30 (08) 1546-1551
    CrossrefPubMedGoogle Scholar
  • 14 Meckel S, Maier M, Ruiz DSM. et al. MR angiography of dural arteriovenous fistulas: diagnosis and follow-up after treatment using a time-resolved 3D contrast-enhanced technique. Am J Neuroradiol 2007; 28 (05) 877-884
    PubMedGoogle Scholar
  • 15 Meckel S, Reisinger C, Bremerich J. et al. Cerebral venous thrombosis: diagnostic accuracy of combined, dynamic and static, contrast-enhanced 4D MR venography. Am J Neuroradiol 2010; 31 (03) 527-535
    CrossrefPubMedGoogle Scholar
  • 16 Schuchardt F, Hennemuth A, Schroeder L. et al. Acute cerebral venous thrombosis: three-dimensional visualization and quantification of hemodynamic alterations using 4-dimensional flow magnetic resonance imaging. Stroke 2017; 48 (03) 671-677
    CrossrefPubMedGoogle Scholar
  • 17 Schuchardt F, Schroeder L, Anastasopoulos C. et al. In vivo analysis of physiological 3D blood flow of cerebral veins. Eur Radiol 2015; 25 (08) 2371-2380
    CrossrefPubMedGoogle Scholar
  • 18 Qureshi AI. A classification scheme for assessing recanalization and collateral formation following cerebral venous thrombosis. J Vasc Interv Neurol 2010; 3 (01) 1-2
    PubMedGoogle Scholar
  • 19 Aguiar de Sousa D, Lucas Neto L, Arauz A. et al. Early recanalization in patients with cerebral venous thrombosis treated with anticoagulation. Stroke 2020; 51 (04) 1174-1181
    CrossrefPubMedGoogle Scholar
  • 20 Houser OW, Campbell JK, Campbell RJ, Sundt Jr TM. Arteriovenous malformation affecting the transverse dural venous sinus--an acquired lesion. Mayo Clin Proc 1979; 54 (10) 651-661
    PubMedGoogle Scholar
  • 21 Tsai LK, Jeng JS, Liu HM, Wang HJ, Yip PK. Intracranial dural arteriovenous fistulas with or without cerebral sinus thrombosis: analysis of 69 patients. J Neurol Neurosurg Psychiatry 2004; 75 (11) 1639-1641
    CrossrefPubMedGoogle Scholar
  • 22 Hu Y-S, Lin C-J, Wu H-M. et al. Lateral sinus dural arteriovenous fistulas: sinovenous outflow restriction outweighs cortical venous reflux as a parameter associated with hemorrhage. Radiology 2017; 285 (02) 528-535
    CrossrefPubMedGoogle Scholar
  • 23 Kannath SK, Rajan JE, Mukherjee A, Sarma P S. Factors predicting spontaneous thrombosis of aggressive cranial dural arteriovenous fistulas. World Neurosurg 2017; 103: 821.e2-828.e2
    CrossrefPubMedGoogle Scholar
  • 24 Gandhi D, Chen J, Pearl M, Huang J, Gemmete JJ, Kathuria S. Intracranial dural arteriovenous fistulas: classification, imaging findings, and treatment. Am J Neuroradiol 2012; 33 (06) 1007-1013
    CrossrefPubMedGoogle Scholar
  • 25 Borden JA, Wu JK, Shucart WA. A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg 1995; 82 (02) 166-179
    CrossrefPubMedGoogle Scholar
  • 26 Cognard C, Casasco A, Toevi M, Houdart E, Chiras J, Merland J-J. Dural arteriovenous fistulas as a cause of intracranial hypertension due to impairment of cranial venous outflow. J Neurol Neurosurg Psychiatry 1998; 65 (03) 308-316
    CrossrefPubMedGoogle Scholar
  • 27 Zipfel GJ, Shah MN, Refai D, Dacey Jr RG, Derdeyn CP. Cranial dural arteriovenous fistulas: modification of angiographic classification scales based on new natural history data. Neurosurg Focus 2009; 26 (05) E14
    CrossrefPubMedGoogle Scholar
  • 28 Hurst RW, Bagley LJ, Galetta S. et al. Dementia resulting from dural arteriovenous fistulas: the pathologic findings of venous hypertensive encephalopathy. Am J Neuroradiol 1998; 19 (07) 1267-1273
    PubMedGoogle Scholar
  • 29 Aguiar de Sousa D, Lucas Neto L, Canhão P, Ferro JM. Recanalization in cerebral venous thrombosis. Stroke 2018; 49 (08) 1828-1835
    CrossrefPubMedGoogle Scholar
  • 30 Rezoagli E, Martinelli I, Poli D. et al. The effect of recanalization on long-term neurological outcome after cerebral venous thrombosis. J Thromb Haemost 2018; 16 (04) 718-724
    CrossrefPubMedGoogle Scholar
  • 31 Martinelli I, Bucciarelli P, Passamonti SM, Battaglioli T, Previtali E, Mannucci PM. Long-term evaluation of the risk of recurrence after cerebral sinus-venous thrombosis. Circulation 2010; 121 (25) 2740-2746
    CrossrefPubMedGoogle Scholar
  • 32 Pires GS, Ribeiro DD, Oliveira JAQ. et al. Risk factors associated with recurrent venous thromboembolism after a first cerebral venous thrombosis event: a cohort study. Thromb Res 2019; 178: 85-90
    CrossrefPubMedGoogle Scholar
  • 33 Chen L, Mao Y, Zhou L-F. Local chronic hypoperfusion secondary to sinus high pressure seems to be mainly responsible for the formation of intracranial dural arteriovenous fistula. Neurosurgery 2009; 64 (05) 973-983
    CrossrefPubMedGoogle Scholar
  • 34 Luciani A, Houdart E, Mounayer C, Saint Maurice JP, Merland JJ. Spontaneous closure of dural arteriovenous fistulas: report of three cases and review of the literature. Am J Neuroradiol 2001; 22 (05) 992-996
    PubMedGoogle Scholar
  • 35 Ishii M, Yamanouchi T, Oshima R. et al. A Case of Dural Arteriovenous Fistula that Developed 21 Months after Cerebral Venous Sinus Thrombosis [in Japanese]. No Shinkei Geka 2017; 45 (10) 889-895
    PubMedGoogle Scholar