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Cranial dural arteriovenous shunts. Part 1. Anatomy and embryology of the bridging and emissary veins

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Abstract

We reviewed the anatomy and embryology of the bridging and emissary veins aiming to elucidate aspects related to the cranial dural arteriovenous fistulae. Data from relevant articles on the anatomy and embryology of the bridging and emissary veins were identified using one electronic database, supplemented by data from selected reference texts. Persisting fetal pial-arachnoidal veins correspond to the adult bridging veins. Relevant embryologic descriptions are based on the classic scheme of five divisions of the brain (telencephalon, diencephalon, mesencephalon, metencephalon, myelencephalon). Variation in their exact position and the number of bridging veins is the rule and certain locations, particularly that of the anterior cranial fossa and lower posterior cranial fossa are often neglected in prior descriptions. The distal segment of a bridging vein is part of the dural system and can be primarily involved in cranial dural arteriovenous lesions by constituting the actual site of the shunt. The veins in the lamina cribriformis exhibit a bridging-emissary vein pattern similar to the spinal configuration. The emissary veins connect the dural venous system with the extracranial venous system and are often involved in dural arteriovenous lesions. Cranial dural shunts may develop in three distinct areas of the cranial venous system: the dural sinuses and their interfaces with bridging veins and emissary veins. The exact site of the lesion may dictate the arterial feeders and original venous drainage pattern.

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Acknowledgments

We wish to thank Professor V. Runge for his valuable comments on the manuscript and knowledgeable suggestions.

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We declare that we have no conflict of interest.

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Authors and Affiliations

  1. Department of Neuroradiology, University Hospital Zurich, Frauenklinikstrasse 108091, Zurich, Switzerland

    Gerasimos Baltsavias, Venkatraman Parthasarathi, Emre Aydin, Peter Roth & Anton Valavanis

  2. Neurosurgical Department, Ch. Doppler Medical Center, Salzburg, Austria

    Rahman A. Al Schameri

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  1. Gerasimos Baltsavias
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  2. Venkatraman Parthasarathi
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  3. Emre Aydin
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  4. Rahman A. Al Schameri
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  5. Peter Roth
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  6. Anton Valavanis
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Correspondence to Gerasimos Baltsavias.

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Comments

Timo Krings, Toronto, Canada

It is common knowledge that the more sophisticated a classification, the better its predictive value, but the more complicated will be its applicability in everyday clinical care. The classification of dural AVF is a good example for this: The Toronto group proposed the most simplistic (and therefore easy to use) type of classification: “benign” dAVF have no cortical venous reflux, drain toward the heart, and have a good clinical prognosis, whereas “malignant” dAVF demonstrate cortical venous reflux and present with a high risk of hemorrhage and neurologic deficits [1, 2]. From the dichotomic classification, Borden moved on to further classify the malignant dAVF into those that had the reflux through a venous sinus and those that refluxed immedialtey into pial veins [3]. Given the large variability seen in patients with dAVF, it soon became obvious that more groups may even better subclassify these lesions and the Cognard classification had seven distinct subtypes [4].

While these classifications were mainly based upon analysis of the venous drainage assuming that all dAVF constitute the same type of disease, the Bicetre group challenged this assumption based on the finding that certain dAVF had a striking gender predilection [5, 6]. Their classification proposed that the primary role of the vein that is initially affected by the shunt will determine whether or not reflux will occur: If so, role of the affected vein was, to drain the brain, reflux will be present (and interestingly these dAVF had a significant male predilection) whereas those veins that are primarily involved into drainage of the bone will only present with cortical venous reflux if additional (secondary) outflow restrictions are present downstream from the shunt. While this classification helps to understand dAVF and their drainage pattern, it did not add to our treatment decision-making process.

The present classification represents an amalgamation of the different classification systems thus attempting to not only predict reflux but also to better predict clinical presentation and thus guiding our treatment decisions. It is based on the significant experience with and the deep understanding of dural arteriovenous fistulas of the senior author, Prof. Valavanis, who over the course of the past 19 years treated endovascularly the majority of the 211 patients with dAVF reported in this paper, and whose clinical and angiographical data were retrospectively reviewed and meticulously analyzed by the lead author, Dr. Baltsavias who treated several of the patients since 2009 and has to be commended for this major undertaking and for furthering our understanding of dAVF.

In the first part of the manuscript, Dr. Baltsavias introduces the concept of bridging and emissary veins and how they relate to the epidural spaces: While the bridging vein interconnect the pial veins with the dural sinuses, the emissary veins will interconnect the dural sinuses with the extracranial venous system thus being transitory conduits on opposite “borders” of the dural sinuses. The bridging veins represent pial-arachnoidal-dural connectors and are in their distal veno-sinusal junction related to the dural sinuses, i.e., they represent the lateral epidural spaces as proposed by the Bicetre classification. Given their location, shunts into these veins will invariably lead to cortical venous reflux.

The emissary veins on the other hand represent the connection of the dural sinuses to the extradural venous vessels and thus include the jugular bulbs, as well as the cavernous sinus. Shunts at these sites are expected to recuit osteodural feeder and are similar to the “ventral epidural spaces” of the Bicetre classification being primarily involved in drainage of the bone and leading primarily not to cortical venous reflux. The site of the shunt will thus not only dictate the venous drainage pattern but also the type of arterial feeder.

In the second part, the relation between the bridging veins and the leptomeningeal drainage is further evaluated highlighting the presence of thrombotic phenomena in the vast majority of cranial dAVF with purely leptomeningeal drainage. Dr. Baltsavias described three different patterns that can be encountered: a dural AVF engaging a bridging vein with occlusion of the veno-dural transition, a dural AVF into an isolated sinus, and a dural AVF into the veins close to the cribriforme plate.

Within the third part of this work, a revised classification of dAVF is proposed based on a detailed analysis of the angioarchitecture according to three factors: directness of venous drainage (depending on the location of the shunt), exclusiveness of the pial venous drainage (related to venous outflow obstruction), and venous strain (as evidenced by venous congestion or venous ectasias). These factors will lead to eight different subtypes of dural AVF and may be better suited to identify which patients present with aggressive clinical symptoms, which ultimately will benefit the patient by identifying patients at risk.

Finally, in the fourth part of this series, the thus developed classification scheme is tested in the series of the authors, and indeed, they were able to demonstrate that directness, exclusivity and signs for venous decompensation could better predict clinical outcome as compared to the simplistic classification of “benign” and “malignant” shunts.

This classification scheme will help to identify high-risk patients, and the authors have to be commended for their thorough and concise analysis of one of the largest series of dAVF managed at a single institution.

References

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2. van Dijk JM, terBrugge KG, Willinsky RA, Wallace MC. Clinical course of cranial dural arteriovenous fistulas with long-term persistent cortical venous reflux. Stroke. 2002 May;33(5):1233–6

3. Borden JA, Wu JK, Shucart WA. A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg. 1995 Feb;82(2):166–79.

4. Cognard C, Gobin YP, Pierot L, Bailly AL, Houdart E, Casasco A, Chiras J, Merland JJ. Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology. 1995 Mar;194(3):671–80

5. Geibprasert S, Pereira V, Krings T, Jiarakongmun P, Toulgoat F, Pongpech S, Lasjaunias P. Dural arteriovenous shunts: a new classification of craniospinal epidural venous anatomical bases and clinical correlations. Stroke. 2008 Oct;39(10):2783-94.

6. Geibprasert S, Krings T, Pereira V, Pongpech S, Piske R, Lasjaunias P. Clinical characteristics of dural arteriovenous shunts in 446 patients of three different ethnicities. Interv Neuroradiol. 2009 Dec;15(4):395–400.

Michihiro Tanaka, Kamogawa City, Japan

The authors summarize the embryological aspect of the regional bridging and emissary veins based on a systematic review of the literature. They use the nomenclature in a strict way, paying special attention to the difference between bridging and emissary vein in terms of embryological aspect. This approach is quite unique and helps us to understand the functional anatomy of the venous drainage system of the brain and cranium.

Karel terBrugge, Toronto, Canada

Dr. Baltsavias and the Zurich team are to be congratulated on this in-depth review of the intracranial venous vascular anatomy as it pertains to the relationships of the pial venous system draining toward the dural sinuses via the bridging venous system and the emissary veins representing the communication between the dural sinuses and the extracranial venous system except for at the anterior cranial fossa level where this may not occur due to the local absence of a dural sinus and the potential drainage via “bridging” leptomeningeal anastomoses connecting the adjacent pial venous system with the extracranial venous system at the level of the nasal fossa. This explains clearly the fact that patients with brain AVMs may present with nose bleeds and patients with cribriforme plate dural shunts may present with either epistaxis or intracranial hemorrhage.

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Baltsavias, G., Parthasarathi, V., Aydin, E. et al. Cranial dural arteriovenous shunts. Part 1. Anatomy and embryology of the bridging and emissary veins. Neurosurg Rev 38, 253–264 (2015). https://doi.org/10.1007/s10143-014-0590-2

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