Treatment Outcomes of Cavernous Sinus Dural Arteriovenous Fistulas: Comparison of Radiosurgery and Endovascular Embolisation

Abstract

Background and Purpose

Endovascular treatment (EVT) and stereotaxic gamma-knife radiosurgery (GKRS) can both effectively treat cavernous sinus dural arteriovenous fistulas (CSDAVF). This study compared the prognostic factors and treatment effectiveness of GKRS and EVT for different CSDAVF types.

Methods

The charts of 200 patients undergoing GKRS and 105 patients undergoing EVT were reviewed for data on symptoms (e.g. orbital, cavernous, ocular, and cerebral). The CSDAVFs were classified into proliferative, restrictive, and late restrictive types. The prognostic factors for complete obliteration (CO) were evaluated in both the GKRS and EVT groups and the latent period to CO was measured. For statistical analysis χ2-tests were used to compare final CO rates for EVT and GKRS across the three CSDAVF types.

Results

The EVT and cavernous symptoms were significant independent predictors of CO. The CO rate after EVT (97.9%) was significantly higher than that after GKRS (63.5%) for restrictive CSDAVFs (P < 0.001) but not for proliferative or late restrictive types. In the GKRS group, cavernous symptoms (hazard ratio, HR: 0.557) and target volume (HR: 0.853) predicted CO, but only target volume remained significant in multivariate analysis. In the EVT group, the latent period to CO was shortest for restrictive CSDAVFs (3.2 ± 1.6 months, P = 0.05).

Conclusion

Angioarchitecture did not affect treatment outcomes. Cavernous symptoms were strongly associated with lower complete obliteration rates in the GKRS but not the EVT group. The EVT method remains the treatment of choice, especially for restrictive CSDAVFs; however, compared to EVT, GKRS had lower complication rates and similar therapeutic effects for proliferative type fistulas.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Abbreviations

CSDAVF:

Cavernous sinus dural arteriovenous fistula

CO:

Complete obliteration

EVT:

Endovascular treatment

GKRS:

Gamma knife radiosurgery

VOS:

Venous outflow score

References

  1. 1.

    Al-Shahi R, Bhattacharya JJ, Currie DG, Papanastassiou V, Ritchie V, Roberts RC, Sellar RJ, Warlow CP. Prospective, population-based detection of intracranial vascular malformations in adults: the Scottish Intracranial Vascular Malformation Study (SIVMS). Stroke. 2003;34:1163–9.

    Article  Google Scholar 

  2. 2.

    Kiyosue H, Hori Y, Okahara M, Tanoue S, Sagara Y, Matsumoto S, Nagatomi H, Mori H. Treatment of Intracranial dural arteriovenous fistulas: current strategies based on location and hemodynamics, and alternative techniques of transcatheter embolization. Radiographics. 2004;24:1637–53.

    Article  Google Scholar 

  3. 3.

    Gross BA, Albuquerque FC, Moon K, McDougall CG. Evolution of treatment and a detailed analysis of occlusion, recurrence, and clinical outcomes in an endovascular library of 260 dural arteriovenous fistulas. J Neurosurg. 2017;126:1884–93.

    Article  Google Scholar 

  4. 4.

    Reynolds MR, Lanzino G, Zipfel GJ. Intracranial dural Arteriovenous fistulae. Stroke. 2017;48:1424–31.

    Article  Google Scholar 

  5. 5.

    Howard BM, Grossberg JA, Prater A, Cawley CM, Dion JE, Tong FC. Incompletely obliterated cranial arteriovenous fistulae are safely and effectively treated with adjuvant ε‑aminocaproic acid. J Neurointerv Surg. 2018;10:698–703.

    Article  Google Scholar 

  6. 6.

    Meyers PM, Halbach VV, Dowd CF, Lempert TE, Malek AM, Phatouros CC, Lefler JE, Higashida RT. Dural carotid cavernous fistula: definitive endovascular management and long-term follow-up. Am J Ophthalmol. 2002;134:85–92.

    Article  Google Scholar 

  7. 7.

    Suh DC, Lee JH, Kim SJ, Chung SJ, Choi CG, Kim HJ, Kim CJ, Kook M, Ahn HS, Kwon SU, Kim JS. New concept in cavernous sinus dural arteriovenous fistula: correlation with presenting symptom and venous drainage patterns. Stroke. 2005;36:1134–9.

    Article  Google Scholar 

  8. 8.

    Lee RJ, Chen CF, Hsu SW, Lui CC, Kuo YL. Cerebellar hemorrhage and subsequent venous infarction followed by incomplete transvenous embolization of dural carotid cavernous fistulas: a rare complication. J Neurosurg. 2008;108:1245–8.

    Article  Google Scholar 

  9. 9.

    Luo CB, Chang FC, Wang AG, Lin CJ, Guo WY, Ting TW. Transvenous coil embolization of cavernous sinus dural arteriovenous fistula on a revised classification. World Neurosurg. 2016;95:357–67.

    Article  Google Scholar 

  10. 10.

    Chen CJ, Lee CC, Ding D, Starke RM, Chivukula S, Yen CP, Moosa S, Xu Z, Pan DH, Sheehan JP. Stereotactic radiosurgery for intracranial dural arteriovenous fistulas: a systematic review. J Neurosurg. 2015;122:353–62.

    Article  Google Scholar 

  11. 11.

    Gemmete JJ, et al. Endovascular techniques in the treatment of carotid-cavernous fistulas. Philadelphia: Lippincott Williams & Wilkins; 2000.

    Google Scholar 

  12. 12.

    Tonetti DA, Gross BA, Jankowitz BT, Atcheson KM, Kano H, Monaco EA, Niranjan A, Lunsford LD. Stereotactic radiosurgery for dural arteriovenous fistulas without cortical venous reflux. World Neurosurg. 2017;107:371–5.

    Article  Google Scholar 

  13. 13.

    Yang HC, Kano H, Kondziolka D, Niranjan A, Flickinger JC, Horowitz MB, Lubsfird LD. Stereotactic radiosurgery with or without embolization for intracranial dural arteriovenous fistulas. Neurosurgery. 2010;67(2010):1276–83. discussion 1284–5.

    Article  Google Scholar 

  14. 14.

    Steiner L, Lindquist C, Adler JR, Torner JC, Alves W, Steiner M. Clinical outcome of radiosurgery for cerebral arteriovenous malformations. J Neurosurg. 1992;77:1–8.

    CAS  Article  Google Scholar 

  15. 15.

    Wu HM, Pan DH, Chung WY, Guo WY, Liu KD, Shiau CY. Gamma Knife surgery for the management of intracranial dural arteriovenous fistulas. J Neurosurg. 2006;105(Suppl):43–51.

    Article  Google Scholar 

  16. 16.

    Luo CB, Chang FC, Teng MM, Guo WY, Ting TW. Transvenous embolization of cavernous sinus dural arteriovenous fistula via angiographic occlusive inferior petrous sinus. J Chin Med Assoc. 2015;78:526–32.

    Article  Google Scholar 

  17. 17.

    Biondi A, Milea D, Cognard C, Ricciardi GK, Bonneville F, van Effenterre R. Cavernous sinus dural fistulae treated by transvenous approach through the facial vein: report of seven cases and review of the literature. AJNR Am J Neuroradiol. 2003;24:1240–6.

    PubMed  PubMed Central  Google Scholar 

  18. 18.

    Yu SC, Cheng HK, Wong GK, Chan CM, Cheung JY, Poon WS. Transvenous embolization of dural carotid-cavernous fistulae with transfacial catheterization throught the superior ophthalmic vein. Neurosurgery. 2007;60:1032–7. discussion 1037–8.

    Article  Google Scholar 

  19. 19.

    Jung KH, Kwon BJ, Chu K, Noh Y, Lee ST, Cho YD, Han MH, Roh JK. Clinical and angiographic factors related to the prognosis of cavernous sinus dural arteriovenous fistula. Neuroradiology. 2010;53:983–92.

    Article  Google Scholar 

  20. 20.

    Young CS, Schwartz ML, O’Brien P, Ramaseshan R. Stereotactic radiotherapy for AVMs: the University of Toronto experience. Acta Neurochir Suppl (Wien). 1995;63:57–9.

    CAS  Google Scholar 

  21. 21.

    Ducruet AF, Albuquerque FC, Crowley RW, McDougall CG. The evolution of endovascular treatment of carotid cavernous fistulas: a single-center experience. World Neurosurg. 2013;80:538–48.

    Article  Google Scholar 

  22. 22.

    Sasaki H, Nukui H, Kaneko M, Mitsuka S, Hosaka T, Kakizawa T, Kimura R, Nagaseki Y, Naganuma H. Long-term observations in cases with spontaneous carotid-cavernous fistulas. Acta Neurochir (Wien). 1988;90:117–20.

    CAS  Article  Google Scholar 

  23. 23.

    Kurata A, Miyasaka Y, Kunii M, Nagai S, Ohmomo T, Morishima H, Fujii K, Kan S. The value of long-term clinical follow-up for cases of spontaneous carotid cavernous fistula. Acta Neurochir (Wien). 1998;140:65–72.

    CAS  Article  Google Scholar 

  24. 24.

    Kobkitsuksakul C, Jiarakongmun P, Chanthanaphak E, Pongpech S. Radiographic evaluation and clinical implications of venous connections between dural arteriovenous fistula of the cavernous sinus and cerebellum and the Pontomedullary venous system. World Neurosurg. 2015;84:1112–6.

    Article  Google Scholar 

  25. 25.

    Kim DJ, Kim DI, Suh SH, Kim J, Lee SK, Kim EY, Chung TS. Results of transvenous embolization of cavernous dural arteriovenous fistula: a single-center experience with emphasis on complications and management. AJNR Am J Neuroradiol. 2006;27:2078–82.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Satomi J, Satoh K, Matsubara S, Nakajima N, Nagahiro S. Angiographic changes in venous drainage of cavernous sinus dural arteriovenous fistulae after palliative transarterial embolization or observational management: a proposed stage classification. Neurosurgery. 2005;56:494–502.

    Article  Google Scholar 

  27. 27.

    Satomi J, van Dijk JM, 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;97:767–70.

    Article  Google Scholar 

  28. 28.

    Liu HM, Wang YH, Chen YF, Cheng JS, Yip PK, Tu YK. Long-term clinical outcome of spontaneous carotid cavernous sinus fistulae supplied by dural branches of the internal carotid artery. Neuroradiology. 2001;43:1007–14.

    CAS  Article  Google Scholar 

  29. 29.

    Tishler RB, Loeffler JS, Lunsford LD, Duma C, Alexander E 3rd, Kooy HM, Flickinger JC. Tolerance of cranial nerves of the cavernous sinus to radiosurgery. Int J Radiat Oncol Biol Phys. 1993;27:215–21.

    CAS  Article  Google Scholar 

  30. 30.

    Wang J, Wu HC, Wang WW, Zhao HS, Dao RN, Liu WM, Zhou DZ, Wang HY, Du C. Trigeminal cardiac reflex caused by onyx embolization of intracranial dural arteriovenous fistula. Turk Neurosurg. 2016;26:325–30.

    PubMed  PubMed Central  Google Scholar 

  31. 31.

    Zhang X, Guo W, Shen R, Sun J, Yin J, Chen X, Gao L, Chen Z, Zhang Q. Combined use of Onyx and coils for transarterial balloon-assisted embolization of traumatic carotid-cavernous fistulas: a report of 16 cases with 17 fistulas. J Neurointerv Surg. 2016;8:1264–7.

    Article  Google Scholar 

  32. 32.

    Cognard C, Januel AC, Silva NA Jr., Tall P. Endovascular treatment of intracranial dural arteriovenous fistulas with cortical venous drainage: new management using Onyx. AJNR Am J Neuroradiol. 2008;29:235–41.

    CAS  Article  Google Scholar 

  33. 33.

    Ambekar S, Gaynor BG, Peterson EC, Elhammady MS. Long-term angiographic results of endovascularly “cured” intracranial dural arteriovenous fistulas. J Neurosurg. 2016;124:1123–7.

    Article  Google Scholar 

  34. 34.

    Kiyosue H, Tanoue S, Okahara M, Yamashita M, Nagatomi H, Mori H. Recurrence of dural arteriovenous fistula in another location after selective transvenous coil embolization: report of two cases. AJNR Am J Neuroradiol. 2002;23:689–92.

    PubMed  PubMed Central  Google Scholar 

  35. 35.

    Uranishi R, Nakase H, Sakaki T. Expression of angiogenic growth factors in dural arteriovenous fistula. J Neurosurg. 1999;91:781–6.

    CAS  Article  Google Scholar 

  36. 36.

    Hu YS, Lin CJ, Wu H‑M, Guo WY, Luo CB, Wu CC, Chung WY, Liu KD, Yang HC, Lee CC. Lateral sinus dural arteriovenous fistulas: sinovenous outflow restriction outweighs cortical venous reflux as a parameter associated with hemorrhage. Radiology. 2017;285:528–35.

    Article  Google Scholar 

  37. 37.

    Lunsford LD, editor. Modern stereotactic neurosurgery. Boston: Martinus Nijhoff; 1988.

    Google Scholar 

  38. 38.

    Taeshineetanakul P, Krings T, Geibprasert S, Menezes R, Agid R, Terbrugge KG, Schwartz ML. Angioarchitecture determines obliteration rate after radiosurgery in brain arteriovenous malformations. Neurosurgery. 2012;71:1071–8. discussion 1079.

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank Hsin-Yi Huang (Biostatistics Task Force, Taipei Veterans General Hospital) for statistical assistance, and Wallace Academic Editing for manuscript editing.

Funding

Funding

This study was funded by Taipei Veterans General Hospital (grant number: V107C-170, 023) and the Ministry of Science and Technology (grant number: MOST-106-2314-B-010-015-MY2, MOST-106-2314B-075-011).

Author information

Affiliations

Authors

Contributions

Guarantors of integrity of entire study, C.B.L, C.J.L, H.C.Y; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, agrees to ensure any questions related to the work are appropriately resolved, all authors; literature research, C.B.L, H.M.W; clinical studies, W.Y.C, C.C.L, K.D.L; statistical analysis, C.J.L; manuscript editing, C.B.L, C.J.L, H.C.Y.

Corresponding author

Correspondence to Chao-Bao Luo.

Ethics declarations

Conflict of interest

H.-C. Yang, C.-J. Lin, C.-B. Luo, C.-C. Lee, H.-M. Wu, W.-Y. Guo, W.-Y. Chung and K.-D. Liu declare that they have no competing interests.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yang, H., Lin, C., Luo, C. et al. Treatment Outcomes of Cavernous Sinus Dural Arteriovenous Fistulas: Comparison of Radiosurgery and Endovascular Embolisation. Clin Neuroradiol 30, 321–330 (2020). https://doi.org/10.1007/s00062-019-00787-z

Download citation

Keywords

  • Angioarchitecture
  • Arteriovenous fistula
  • Cavernous sinus
  • Endovascular treatment
  • Gamma knife