Current status of endovascular treatment for dural arteriovenous fistulae in the tentorial middle region: a literature review
The tentorial middle region (TMR) includes the midline and paramedian tentorium. TMR dural arteriovenous fistulae (DAVFs) are complex. We performed a review of the literature on TMR DAVFs. TMR DAVFs are divided into the following four types: incisural DAVF, Galenic DAVF, straight sinus DAVF and torcular DAVF. TMR DAVFs often drain into pial veins; therefore, most TMR DAVFs are classified as Borden II–III and Cognard types IIb–IV, whose characteristics cause TMR DAVFs to be prone to hemorrhage. TMR DAVFs have a very disappointing natural progression, and treatment is necessary. TMR DAVFs have extensive arterial supply and complex venous drainages, making them difficult to treat. Currently, for TMR DAVF, endovascular treatment (EVT) has become a better option. In EVT, transarterial embolization is the first-line treatment. Many complications can occur when treating TMR DAVFs, but complete EVT can generally achieve good clinical outcomes. In this review, three educational cases with demonstrating figures are provided to elaborate TMR DAVFs.
KeywordsTentorial middle region Dural arteriovenous fistula Endovascular treatment Review
Tentorial dural arteriovenous fistulae (DAVFs) are located on the tentorium and can extend from their attachment to the clinoid processes and petrous ridges anteriorly to the torcula posteriorly [1, 2]. Tentorial DAVFs can be divided into marginal, lateral, and medial subtypes . The medial subtype tentorial DAVFs are located in the tentorial middle region (TMR), including the midline and paramedian tentorium, and should be called TMR DAVFs [3, 4].
Compared with marginal and lateral subtype tentorial DAVFs, TMR DAVFs have a deeper midline location, more complex angioarchitecture and critical neuroanatomies. These DAVFs are different from the other tentorial DAVFs and are difficult to understand. Therefore, it is imperative to discuss TMR DAVFs separately from the other tentorial DAVFs. The natural progression of TMR DAVFs is very disappointing. Therefore, TMR DAVFs should be treated .
Currently, endovascular treatment (EVT) has become a better option for TMR DAVFs than radiotherapy and surgery [1, 6, 7]. For TMR DAVFs, surgical treatment is difficult due to the deep location and complex structures [3, 8]. Radiotherapy is usually not solely used in TMR DAVFs because of the risk of hemorrhage between treatment and occlusion [9, 10]. Currently, a comprehensive review of TMR DAVFs is lacking. In this study, we performed a literature review of TMR DAVFs. In addition, three educational cases with example figures are provided.
Critical vessels in the TMR
The arterial supply to the TMR DAVFs includes the middle meningeal artery (MMA) [11, 12]; the medial tentorial artery (MTA) [4, 13, 14, 15, 16, 17, 18, 19]; the meningeal branch of occipital artery (OA) [11, 12]; the posterior meningeal artery (PMA) ; the tentorial branches of the posterior cerebral artery (PCA), which is also called the artery of Davidoff and Schechter (ADS); and the superior cerebellar artery (SCA), which is also called the artery of Wollschlaeger and Wollschlaeger [3, 21, 22, 23].
The main venous drainages for TMR DAVFs include the vein of Galen, the internal cerebral vein (ICV), the basal vein (BV) of Rosenthal, the straight sinus (SS), the cerebral and cerebellar cortical veins (CVs), and the lateral mesencephalic vein (LMV) as well as spinal venous drainage [3, 8, 24, 25, 26, 27, 28]. The LMV is important in TMR DAVFs because it connects the infratentorial and supratentorial compartments and joins the BV of Rosenthal and the petrosal system . The LMV is involved in the venous drainage of 31% of tentorial DAVFs .
TMR DAVF classification
Incisural DAVFs are located along the free edge of the tentorium [2, 33, 34]. Their main feeding arteries include the MMA and MTA [3, 4, 8, 16]. The draining veins of incisural DAVFs are not clearly associated with a venous sinus, with drainage occurring supratentorially into the medial and inferior temporal veins, into the BV of Rosenthal and LMVs in the ambient cistern, or even via cervical perimedullary venous drainage [3, 8, 16, 19, 35].
Galenic DAVFs are located at the midline of the posterior margin of the tentorial incisura [3, 4]. Their feeding arteries enter inferiorly from the ADS, anteriorly from the MTA, superiorly from the MMA/falcine artery, and posteriorly from the PMA [3, 4, 30]. The venous drainage of Galenic DAVFs can be supratentorial, infratentorial, or both and include the vein of Galen, the BV of Rosenthal, CVs, and mesencephalic veins [3, 5, 30, 36].
SS DAVFs are located at the falcotentorial junction . Their main feeding arteries include the PMA, the MTA, the MMA, and the meningeal branch of the OA [3, 4]. SS DAVFs infratentorially drain into the vermian or superior cerebellar veins; when the SS is occluded, the venous drainage is redirected into the vein of Galen or its tributaries [3, 38, 39].
Tentorial sinus DAVFs are also included in the SS DAVF classification; they share similar feeding arteries and draining veins .
Torcular DAVFs are located at the midline of the posterior margin of the falcotentorial junction . Their main feeding arteries include the PMA, MMA, MTA and ADS [3, 4, 5]. Torcular DAVFs drain supratentorially into the medial and inferior occipital veins along the sagittal and transverse sinuses or the BV of Rosenthal . All torcular DAVFs are associated with sinus thrombosis and show bidirectional drainage relative to the tentorium .
Falx cerebelli and superior sagittal sinus DAVFs that are close to torcular herophili are also classified as torcular DAVFs; they share similar feeding arteries and draining veins .
The classification of TMR DAVFs is shown in Fig. 1.
Angioarchitecture and grading
When TMR DAVFs are supplied, some small branches may become hypertrophic and amenable to catheterization [19, 36, 38, 41, 42]. TMR DAVFs frequently have retrograde drainage through CVs and deep drainage through the vein of Galen, which causes hemorrhage, bilateral thalamic venous hypertension, or the perimedullary venous plexus [35, 43, 44, 45]. The draining vein may become variceal due to the high flow [1, 39, 46]. Even more rarely, the draining vein can dilate into a giant venous ampulla, causing mass effects [46, 47].
Borden and Cognard grades
Retrograde CV drainage is very common in TMR DAVFs [3, 48]. Therefore, most TMR DAVFs are classified as Borden II-III [16, 49] and Cognard IIb-IV [50, 51]. For example, in 2008, Lawton et al. examined 31 cases, of which 26 (84%) had Borden III DAVFs and five (16%) had Borden II DAVFs . In another study (Tomak et al., 2003) with 22 tentorial DAVFs, all cases were classified as Borden type III . Therefore, TMR DAVFs have the most aggressive neurological behavior, with 97% of cases causing hemorrhage or progressive focal neurological deficits [39, 52].
Outline of EVT
TMR DAVFs often drain exclusively to CVs. Advancing a microcatheter through the elongated, ecstatic, and fragile pial veins is considered quite difficult and risky, which prevents transvenous embolization (TVE); therefore, transarterial embolization (TAE) is the first-line treatment [1, 38, 39]. The embolic agents include coils, liquid embolic agents (Onyx; Micro Therapeutics Inc., Irvine, CA) and n-butyl cyanoacrylate (NBCA) (Histoacryl, Yocan Medical, Toronto, CA), or both in combination [5, 8].
If there is a single feeding artery, TAE is simple; even placing a coil in the origin of the tentorial artery may close the fistula . However, most TMR DAVFs have multiple feeding arteries, making individual catheterization quite difficult. Thus, identifying the most suitable feeder choice is very important. This choice should be based on the tortuosity, diameter and length of the feeding artery as well as the distance between the microcatheter tip and the fistula; it is recommended that the microcatheter tip be positioned at or immediately adjacent to the fistula .
During TAE, the goal is the penetration of the liquid embolic agents to all fistula points and proximal venous outflows to ensure complete embolization. Meanwhile, the TAE must preserve the patency of the vein of Galen and the SS to avoid symptomatic venous hypertension. Sometimes, selective transarterial or transvenous occlusion of the draining vein should also be the goal of EVT, when occlusion of the cortical vein or part of a nonfunctional sinus guarantees definitive occlusion of the fistula .
TVE may be attempted if occlusion of the fistula point of TMR DAVFs is not achieved using TAE or if venous access to the fistula is simple [48, 53]. TVE with coils is the best treatment option . For example, in Deasy et al. (1999), two TMR DAVFs were treated successfully with transvenous coil embolization via the internal jugular vein and the SS . In addition, TAE and TVE can be combined, but the combination is uncommon [1, 23, 48, 53, 55].
For simple TMR DAVFs, complete obliteration should be easy to achieve, but for some complex and malignant DAVFs, it is difficult to achieve 100% obliteration; thus, the next goal is to reduce the blood flow to and pressure on the TMR DAVFs . Patients with these DAVFs should be controlled by DSA and, after eventual hypertrophy of the residual feeders, either the EVT should be reattempted or radiosurgery should be proposed.
Paths of TAE
The MMA has unique characteristics in that it is straight and fixed between the dura. Therefore, the MMA is commonly used to access TMR DAVFs. All MMA branches can be used to access a DAVF [3, 4]. Furthermore, when a DAVF occurs, the MMA often becomes thicker than normal as a result of hemodynamic stress . Even if the branches of the MMA are not the main feeders, the MMA may represent the safest route to access the TMR DAVF because the MMA allows a long reflux [1, 7, 38, 57]. Sometimes, using a dual-lumen balloon to perform the TAE may be very useful .
In TMR DAVFs, the OA can be a good feeding artery; the enlarged meningeal branch of the OA allows the microcatheter to deliver liquid embolic agent [3, 5, 33, 39]. Kim et al. (2015) treated a torcular DAVF; the carefully selected catheterization of the transosseous meningeal branch of the OA was successful in providing the microcatheter with access to the fistula point, then Onyx was injected, filling the retrograde drainage of the CV and obliterating the DAVF .
Case 3 (Fig. 4) was treated via the OA and obtained complete embolization.
However, if the MMA or OA is not available, then the MTA, ADS, ascending pharyngeal artery (APhA) and PMA can be used to perform TAE [8, 39]. However, these arteries can be used only as auxiliary arterial paths because the use of TAE via these feeders to the TMR DAVFs will result in incomplete occlusion with residual filling [1, 47].
TMR DAVFs are difficult to manage, and many complications can occur during EVT . In patients treated with EVT, the rate of complications is 13.5%, and these complications include intraoperative hemorrhage, postoperative ischemia and cranial nerve palsy .
Vessel perforation by microwire and feeding artery rupture because of microcatheter removal during TAE can result in intraoperative hemorrhage [57, 59]. During or after TAE, spontaneous hemorrhage can be disastrous, this complication may be secondary to restriction of the venous outlet, which can result in venous hypertension; then, the venous varix ruptures .
In addition, Wu et al. (2016) found that pial arterial supply may be a risk factor for intracranial hemorrhage during TAE of DAVF through dural feeders; these authors advised that obliterating pial feeding arteries—at least the major ones—before fistula embolization through dural feeders may decrease the risk of hemorrhage .
In fact, these pial arteries are not appropriate to first embolize the TMR DAVFs, as suggested by Wu et al. Because these pial arteries are fragile and easy to rupture, the allowed reflux distance is not sufficient to ensure a safe reflux of Onyx during the creation of the plug; it is difficult to push Onyx into the DAVF. Moreover, Onyx can easily flow into the ICA and VA.
Cranial nerve palsy
Cranial nerve palsy during TAE occurs when the embolizing liquid embolic agent migrates to the nerve-supplying artery . In TMR DAVFs, the oculomotor and trochlear nerves may derive blood supply from the MTA; occlusion of the MTA can result in palsy of these nerves [33, 61, 62].
The facial nerve is divided into three topographical segments: the labyrinthine, tympanic and mastoid segments. The geniculate ganglion is located between the labyrinthine and tympanic segments. The tympanic segment and geniculate ganglion are vascularized by the petrosal artery from the MMA . When embolizing TMR DAVFs from the posterior MMA branch, it is critical to avoid any reflux into the petrosal branch, which supplies the facial nerve . Embolization may compromise the circulation through the petrosal branch and thus cause the facial nerve palsy.
Therefore, it is critical to fully understand the vascular supply to the cranial nerves and the potentially dangerous anastomoses.
When performing TAE, if the pial arteries are chosen as embolizing arteries, reflux can block the normal artery, and brain infarction can occur . Zhang et al. (2010) treated two TMR DAVFs via the PCA and SCA; postoperative cerebellar infarction associated with dorsal pons to mesencephalic infarcts occurred . The TMR DAVF in case 2 (Fig. 3) was supplied by the SCA and AICA; in case 3 (Fig. 4), the DAVF was supplied by the AICA. A long duration of Onyx reflux in these pial arteries will result in brain infarction, even the occlusion of VA; so, these pial arteries cannot be chosen to be first embolized.
During TAE for TMR DAVFs, prolonged injection times and excessive reflux were the primary reasons for Marathon flow-guided microcatheter (Micro Therapeutics Inc., Irvine, CA) retention . If the arterial feeders are too tortuous, long and tiny, the difficulty of removing the catheter will increase. When Onyx reflux occurs for too long, retrieval by applying too much traction on an entrapped catheter may increase the risk of vessel rupture . Therefore, it may be safer to leave the microcatheter in the vascular system. For fear of thromboembolic events, in these cases, a daily dose of 100 mg of aspirin should be administered orally for 3 months .
Because of the limitations of Marathon microcatheter retention, considerable interest has been expressed in the development of detachable-tip microcatheters. Currently. detachable-tip microcatheters mainly included the SONIC (Balt, Montmorency, France) and Apollo (Micro Therapeutics Inc., Irvine, CA) Onyx delivery microcatheters , which allow for more controlled and longer injections and better DAVF penetration with minimized risk of microcatheter retention. Therefore, catheter retention may no longer be an issue.
In addition to the above complications, other complications can occur, such as trigeminocardiac reflex , venous rupture , draining vein thrombosis , and microcatheter rupture . During TAE, the liquid embolic agent can cross the fistula point into the ICA or VA though a feeding artery of the TMR DAVF. In these cases, a balloon placed in the ICA or VA is recommended .
After EVT, TMR DAVFs require angiographic follow-up because the immediate “angiographic cure” does not mean complete embolization of TMR DAVFs; moreover, after complete embolization, TMR DAVFs can recur [39, 53].
However, the follow-up interval was uncertain. In the Liu et al. (2014) study of 26 tentorial DAVFs, all patients underwent follow-up with DSA at 3 months after EVT . In the Wu et al. (2018) study of 6 TMR DAVFs, the angiographic follow-up was from 4 to 12 months . Our DSA follow-up time was at approximately 6 months. In TMR DAVFs with partial occlusion, the follow-up interval should be shorter, especially if the retrograde drainage of the CV was not obliterated completely.
Generally, the EVT of tentorial DAVFs yields a good outcome. Gioppo et al. (2017) performed a review of 72 tentorial DAVFs, in which 92.5% were treated via TAE. Complete obliteration was achieved in 86.1% of cases. The rate of clinical improvement was approximately 88.8% . The prognosis of TMR DAVFs may be worse than that of general tentorial DAVFs because the obliteration rate was 66.7% in the TMR DAVFs [38, 62].
The outcome of EVT of TMR DAVFs was acceptable. The clinical outcome of TMR DAVFs at follow-up should be evaluated using a neurological functional scale such as the modified Rankin Scale (mRS); unfortunately, some studies report a subjective “resolution of symptoms”, “complete cure”, or “excellent/good” outcome status . This review recommends the use of the mRS.
For TMR DAVFs, if complete obliteration is impossible, it is necessary to decrease the Borden and Cognard grades, and the retrograde drainage through CVs must be corrected . If the retrograde drainage of CVs is not obliterated, a staged TAE via another feeding artery may be attempted again . If repeated EVT still cannot obliterate the retrograde drainage of CVs, combined surgical removal or radiotherapy can be attempted [3, 4, 33, 34, 65, 66, 67, 68].
Currently, DSA is still the gold standard for monitoring TMR DAVF to exclude recurrence or persisting DAVFs; however, with the development of magnetic resonance imaging (MRI) and MR angiography (MRA), including 3D time-of-flight MRA  and 3D or 4D contrast-enhanced MRA [70, 71], these data can be used to monitor DAVFs. MRI and MRA can visualize the cortical draining veins and usually the arterial feeders before embolization, indicating a Grade II or III TMR DAVF. Therefore, MRI and MRA can be used for late-term follow-up to determine whether the cortical draining vein disappears or reappears if conservative treatment is adopted. However, their value in follow-up imaging is limited.
TMR DAVFs have a very disappointing natural progression. Treatment is difficult because of their extensive arterial supply and complex venous drainages. TMR DAVFs often drain into pial veins and are generally classified as Borden II–III and Cognard IIb–IV and are thus prone to hemorrhage. Currently, EVT has become a better option for TMR DAVFs, among which TAE has become the first-line treatment option. For the path of TAE, MMA is the best choice. Occasionally, TVE alone or combined with TAE may be attempted. TMR DAVFs are difficult to cure, and many complications can occur. Generally, the EVT of TMR DAVFs yields a good outcome.
We would like to acknowledge the reviewers for their helpful comments on this paper.
Compliance with ethical standards
Conflict of interest
The authors have no conflicts of interest.
This work is a review of the literature and did not require ethical approval to be carried out.
Informed consent was obtained from all individual participants included in the study.
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