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Abstract
Background The dural vasculature plays a key role in several important conditions, including dural fistulas and subdural collections. While in vivo investigations of intrinsic dural arterial angioarchitecture are rare, no angiographic studies of dural venous drainage exist to our knowledge.
Objective To describe methods by which dural venous drainage might be visualized with current angiographic equipment and technique, and to correlate our results with existing ex vivo literature.
Methods Digital subtraction angiography and 3D angiography (rotational and Dyna CT) of dural neurovasculature were acquired in the context of subdural hematoma embolization and normal dura. Protocols for visualization of dural venous drainage were established, and findings correlated with ex vivo studies.
Results Meningeal arteries supply both the skull and dura. Normal dural enhancement is accentuated by the presence of hypervascular membranes. Intrinsic meningeal veins/sinuses parallel outer layer arteries with well-known tram-tracking appearance. Dura adjacent to main arterial trunks drains via skull base foramina into the pterygopalatine venous plexus, or via emissary veins into the temporalis venous plexus. Dura near the sinuses drains into venous pouches adjacent to the sinus, before emptying into the sinus proper—possibly the same pouches implicated in the angioarchitecture of dural fistulas. Finally, posterior temporoparietal convexity dura, situated in a watershed-like region between middle and posterior meningeal territories, frequently empties into diploic and emissary veins of the skull. Wide variation in balance is expected between these three routes. Drainage patterns appear to correlate with venous embryologic investigations of Padget and ex vivo studies in adults.
Conclusions Continued attention to dural venous drainage may prove useful in the diagnosis and management of dural-based vascular diseases.
- angiography
- meninges
- subdural
- technique
Data availability statement
All data relevant to the study are included in the article or uploaded as supplementary information.
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Introduction
The bulk of literature on dural veins concerns venous sinuses. To our knowledge, no formal angiographic investigation of normal or pathologic dural venous drainage exists, despite the prevalence of important dural-based vascular diseases.
The ex vivo literature is relatively compact, and overall consistent with our in vivo assessment. In embryology, Padget’s work,1 building on that of Streeter, is unsurpassed in both its scope and enduring accuracy. The main themes related to our topic are early separation between cerebral and meningeal venous circulations linked by bridging veins, and manifest plasticity of the dural venous system, in both space and time, to accommodate the needs of enlarging cerebrum; changes that continue after birth. Several manuscripts provide details of this intrinsic dural arteriovenous system and form an important background.2–5
The intrinsic dural arterial anatomy is briefly reviewed here as it relates to the known venous components. Each of three dural layers is associated with its respective vascular network. From outside in, there are periosteal, meningeal, and border zone layers. The corresponding arterial networks are named outer, transitional, and inner (figure 1).
Schematic diagram of intrinsic dural venous system and its drainage. (I–IV) Detail of inserts; BV, bridging vein (cortical); C, arterial network in sinus walls; DV, diploic vein, parietal squamosal region; E, cutaneous artery; F, superficial artery participating in dural supply; FB, frontal branch, MMA; FC, falx cerebri; FO, foramen ovale, FS, foramen spinosum; G, primary arterial anastomotic network of the outer layer (100–300 μm diameter); H, secondary arterial anastomotic network of the outer layer (50–90 μm diameter); JF, jugular foramen; L, venous lakes/pouches in walls of major sinuses; MMA, middle meningeal artery; PVP, pterygopalatine venous plexus; SiS, sigmoid sinus; SS, straight sinus; SSS, superior sagittal sinus; TC, tentorium cerebelli; TVP, temporalis venous plexus.
The periosteal layer of cranial dura contains the outer arterial dural network, encompassing the middle meningeal artery (MMA) and its major branches. The network is a fractal-like structure covering the entire dura. Its primary anastomotic arteries range between 100 and 300 µm,2–4 connect the major dural branches, and are readily visible angiographically (figures 2–4). The secondary anastomotic arteries, measuring 50–90 µm, link the primary arteries and may be visible on cone beam CT or similar high-resolution volumetric imaging, especially when pathologically enlarged. Outer network vessels also participate extensively in supply of the skull, and angiographic enhancement can be difficult to differentiate from that of dura (figures 2–4).2 Finally, the same ex vivo studies suggest the presence of physiologic intradural arteriovenous anastomoses/shunts, of the order of 10 µm in diameter, 2 4 naturally relevant to our specialty in regard to dural arteriovenous fistulas.
(A–I) DSA evaluation. (A–C) Patient with chronic subdural hematoma. There is extensive enhancement, which does not extend to the paramedian skull. Venous phase (C) shows tram-tracking veins paralleling the frontal middle meningeal artery branch (arrowheads), drainage into diploic parietosquamosal sinus (arrows), and into the temporalis venous plexus (ball arrow). (D–F) Normal dura. In this subject there is extensive skull enhancement, which can be seen as extending to the paramedian parieto-occipital skull (oval). The venous phase again shows the parietosquamosal sinus draining substantially into the sigmoid. (G–I) Frontal views of another subject with normal dura, showing skull enhancement (oval). There is a venous pouch present adjacent to the superior sagittal sinus (open arrow). The parietosquamosal sinus is shown by the white arrow.
(A–H) Examples of ‘dual volume’ Dyna CT images in various patients. The images are produced by subtraction of a non-contrast Dyna CT from an identical parameter Dyna CT during middle meningeal artery injection. Images (E) and (F) are from a patient with a subdural hematoma. The rest have no pathology. Arrowheads point to dural venous sinuses adjacent to arterial branches (tram-track). Note consistent visualization of primary outer layer dural anastomotic network between major arteries. Arrows point to meningeal and diploic venous channels that do not parallel arteries. Most of these channels are diploic. (G, H) Same patient: examples of normal skull enhancement (ovals) as opposed to dural enhancement in subject E, F.
(A–F) Cross-eye and anaglyph stereo visualization help to differentiate skull from dural enhancement. Patient A–C has no dural pathology. The patchy areas of enhancement, superficial to dural arteries, best seen in stereo, belong to the skull, not dura. Numerous primary outer layer arterial anastomoses (ball arrows) between posterior frontal and parietal middle meningeal artery branches are visible. Arrowheads mark venous channels paralleling the petrosquamosal branch, and connecting with a diploic channel (arrows, possible Padget’s remnant parietosquamosal sinus) draining into the sigmoid sinus. Patient D-F has a chronic subdural hematoma. The patchy enhancement deep to arterial network, best seen on stereo images, is that of dura, not skull.
From the outer periosteal network, penetrating vessels of the transitional network descend through a truly hypovascular meningeal layer to supply a dense capillary inner network, located in the innermost border zone layer, where cells of the same name closely adhere to the arachnoid. This network plays a key role in pathophysiology of chronic subdural hematomas.3 5–8
There are very few studies on the intrinsic dural venous system ex vivo and none we could find in vivo, although it is certainly possible that some exist. The tram-tracking appearance of meningeal venous sinuses along the major outer network arteries such as the MMA is well-known. Several authors reported ex vivo findings of dense venous plexi adjacent to venous sinuses, and their possible relationship to bridging veins, cerebrospinal fluid circulation, and subdural collections.2 5 The therapeutic implications in regard to subdural collections have only been recently realized by the larger neuroendovascular community.9–14
For venous drainage from the dura (in contrast to the intrinsic dural venous system), Padget remains the most relevant source.1 She emphasized early development of both the aforementioned meningeal sinuses and other important osteodural sinus structures, such as the petrosquamosal and tentorial sinuses, and their relationship to adult structures such as the misunderstood sphenoparietal sinus/sinus of Breschet, as highlighted by San Millán Ruiz et al. 15
The dual aims of this manuscript are to describe methods by which dural venous drainage might be visualized with current angiographic equipment and technique, and to correlate our results with existing ex vivo literature.
Methods
Institutional review board approval was obtained. Patients in whom the MMA and its major branches were imaged using digital subtraction angiography (DSA), rotational angiography with volume-rendered and maximal intensity projection reconstructions, and Dyna CT, were retrospectively reviewed. Baseline patient characteristics are included in online supplemental table 1.
Supplemental material
Optimal visualization requires general anesthesia with pharmacologic paralysis and apnea during acquisition. The microcatheter must be large enough to permit adequate flow rates to opacify the dura, but not so large as to produce occlusion, or venous drainage might be impeded. The optimal microcatheter tip position is just below the foramen spinosum. The diameter of a normal MMA is about 2 mm, and a 0.021 or 0.027 inch microcatheter is optimal, with 0.018 inch being generally too small for adequate flow rates in adults. The injection is of undiluted contrast, with a rate fast enough to fill the whole MMA; a small degree of reflux implies optimal rate. This rate is typically ~0.5 mL/s. Hand injections are better to determine optimal rate (figure 2).
Dura has a highly variable arteriovenous transit time, typically 10–15 s, substantially longer than normal brain. Variability in transit time is not well understood, but seems to be related to major physiologic factors, such as systemic arterial and venous pressures, cardiac output, intracranial pressure, possibly head positioning, and possibly intrinsic dural factors. Visualizing veins required injection of about 3–5 mL of contrast. The dual requirements for longer injections (6 s at 0.5 mL/s for 3 mL) and longer imaging times contribute, in our opinion, to lack of visualization of normal dural veins under most circumstances. Our typical DSA protocol is 0.5 frames/second (to minimize radiation dose) for 30 s. From the DSA injection, the arteriovenous transit time for each subject is determined, establishing delay times for volumetric imaging of veins using either Dyna CT or rotational angiography. Subtraction of pre-contrast and post-contrast Dyna CT co-registered datasets allows superior spatial resolution. However, current imaging times are too long to enable separation of arterial and venous phases at necessary spatial resolution, resulting in a mixed dataset (figures 3 and 4).
For rotational angiography, imaging starts at the time of optimal venous opacification, as determined by DSA. Typical rotational angiography injection for normal dura is ~0.5 cc/s for 3–5 mL (6–10 s) with 10–15 s X-ray delay. Another method, which we prefer, applies to Siemens systems (Siemens, Munich, Germany), is to inject by hand during the first mask phase of rotational angiography, continue the injection while the C-arm is returning to start position, stopping injection ~2 s before the second subtraction phase. The 2 s allow for contrast to wash out of arteries, producing a relatively pure venous phase. This is then reconstructed as a dual volume dataset. Because undiluted contrast is usually slightly denser than bone, a double-ramp reconstruction can provide some differentiation between skull and MMA branches, thus yielding a triple phase image like most of the volume-rendered images shown here (figures 5 and 6, online supplemental figure 1). Another option is to do two spins—one arterial, and one venous, with subsequent co-registration (online supplemental figure 1C–F).
(A–I) Examples of volume-rendered visualization of osteodural venous drainage in nine different subjects, demonstrating feasibility of consistent venous resolution. All subjects except D (pure venous phase) are examples of ‘triple volume’ technique. Notice consistent presence of tram-tracking venous sinuses paralleling major arteries and emptying into the pterygopalatine venous plexus, and diploic/emissary veins draining vertically across parietal and temporal bones, usually into sigmoid sinus; this channel may correspond to Padget’s parietosquamosal sinus remnant. Subjects H and I have subdural collections. The rest do not.
Same subject as figure 2A–C. Cross-eye stereo pair volume-rendered images of rotational angiography, with contrast injection during ‘mask phase’, producing a ‘triple volume’ set of images, with arterial, venous, and osseous information. Clearly seen are tram-tracking venous sinuses along middle meningeal artery branches, in this case draining into the pterygopalatine venous plexus via the temporalis venous plexus rather than foramen ovale. This drainage pattern seems to be a very common occurrence. In the bottom image pair the temporalis plexus is superficial to the skull. Also present is the frequently seen diploic drainage of the parietosquamosal region. Finally, a channel in the sphenoid wing probably corresponds to the sphenoid portion of the true sphenoparietal sinus or sinus of Breschet.
For both Dyna CT and rotational angiography, cross-sectional reconstructions are very useful for visualization as well, particularly displaying to advantage the diploic veins, and venous pouches in walls of major venous sinuses (online supplemental figure 2, figures 7 and 8).
Angiographic examples of dural venous pouches (arrows) adjacent to the sinuses. Most are localized to the sigmoid sinus, and appear relatively early in the angiographic sequence compared with other dural venous structures. The possible relationship of these features to genesis of dural fistulas needs further investigation. Note tram-tracking meningeal veins (arrowheads).
Dural venous pouches. Multiple Dyna CT and rotational angiography maximal intensity projection images of dural venous pouches (arrows) in walls of venous sinuses, again predominantly sigmoid. Notice several ‘lakes’ in the tentorium cerebelli, at the limit of current equipment resolution (arrowheads).
Results
The main difficulty with studying both dural arterial supply and venous drainage is separating it from that of the skull, with osseous convexity supplied to a large and variable extent by the MMA. Skull parenchymal blush is well seen on tangential DSA views, which prove supply to visualized areas but no definitive information on other portions of the skull (figures 2 and 4). Stereoscopic volumetric images can also aid visualization (figure 4). With this in mind, and acknowledging that in all vascular anatomy, and venous anatomy especially, variation is the rule, some consistent observations emerge.
Venous channels in the periosteal dural layer, paralleling the course of the MMA and its major branches, are readily demonstrated. Occasionally, they can be shown adjacent to the smaller primary anastomotic network of the outer dural arterial layer (figure 1), at the limit of current angiographic resolution, and correlate well with ex vivo images of Roland et al and others2 4 (figures 3 and 4). Presumably, the parallel arrangement of meningeal arteries and veins exists throughout the outer layer network.
The main middle meningeal vein paralleling the MMA is usually depicted as draining into the pterygopalatine venous plexus via the skull base foramina, typically the ovale (rather than spinosum). However, in our experience, this vein very frequently opens via a convexity emissary venous channel into the temporalis venous plexus before reaching the skull base (figures 1, 5 and 6, online supplemental figure 2). Occasionally, it drains into a diploic structure in the sphenoid wing—probably the sinus of Breschet/sphenoid portion of the true sphenoparietal sinus (figure 6).1 15
Dura adjacent to major venous sinuses usually drains into these sinuses, with contrast collecting into venous plexi/pouches in walls of the sinus before emptying into the sinus proper, in agreement with ex vivo observations.1 2 This can be seen on both DSA and volumetric images (figures 7 and 8), especially in the sigmoid region. Though typically present, the pouches seem to be variable in size and sometimes angiographically absent, possibly reflecting dominance of other routes of venous drainage or supply by other meningeal arteries. One potentially important observation is that these pouches tend to appear earlier than other venous structures in the angiographic sequence, as discussed below.
The third mode of drainage is via diploic/emissary veins of the skull away from major meningeal veins (figures 2–6, online supplemental figures 1 and 2). The most consistent example is a vertically oriented diploic channel coursing through parietal and temporal bones into the sigmoid sinus (or less frequently via emissary vein into a suboccipital venous plexus). This channel may be related to Padget’s remnant of the petrosquamosal sinus, and in our experience is a relatively consistent structure in adult skulls.1 Its location at a kind of watershed zone between middle and posterior meningeal arterial territories may also be relevant as a collector of venous egress in a region remote from the other two venous drainage pathways (figures 2 and 5–6, online supplemental figures 1 and 2). Studies of petrosquamosal sinus in adults are limited.16 17
Overall, the three drainage pathways are in balance, with dominance of one usually corresponding to the paucity of others, consistent with many other vascular arrangements.
Patients with subdural collections proved to be good subjects for visualization of veins due to overall hyperproliferation of dural tissues (membranes), facilitating venous opacification using a shorter arteriovenous transit time (figures 2–4). Drainage patterns are similar.
Discussion
Our results show feasibility of reliable in vivo dural venous phase visualization. Drainage patterns are consistent with both embryologic and ex vivo adult studies as we currently understand them. Detailed description of our protocol allows for reproducibility and improvement by interested groups.
The normal venous pouches/lakes in walls of major sinuses naturally suggest possible connection with dural fistulas. The prevailing hypothesis, supported by several histologic studies,18 19 is that shunts are located within sinus walls; with complex arterial tributaries frequently converging on one or several common channels located in the wall of the sinus proper, before emptying into it. This is particularly well demonstrated in lower-grade fistulas, where the sinus usually maintains its quasi-normal angiographic architecture. A hypothesis that these common channels may be arteries rather than veins,20 is supported by consistent identification of arterial channels within sinuses walls21 22 (figure 1); however it remains a minority view. For example, Kiyosue et al 23 elegantly showed the presence of shunted pouches within sinus walls in their sigmoid dural fistula population, with myriad arterial tributaries converging on these pouches before emptying into the sinus proper.
The physiologic pouches demonstrated in our images are similar to those shown by Kiyosue et al. 23 All structural components of a fistula are present: the dural artery and the pouch emptying into the sinus proper. All that is missing for a low-grade fistula is decreased arteriovenous transit time. To this end, the ex vivo description of possible physiologic precapillary level arteriovenous intradural shunts, mentioned in the introduction section, may be relevant. One surrogate angiographic finding might be a qualitatively shorter dural arteriovenous transit time in one subject versus another, and we have indeed observed that these venous pouches appear relatively early in the angiographic sequence. These remain preliminary observations, with no quantification of timing. The existence of these physiologic shunts remains speculative in our opinion, and further studies are certainly needed. We expect that continued attention to dural venous circulation will help to clarify this and other pathologies, such as osteodural or cranial intraosseous shunts.24
Limitations
Imaging protocols remain in development. Continued advances in angiographic equipment will hopefully allow for more insight into the intrinsic dural venous architecture. For example, the presence of venous lakes in the dura, apart from those adjacent to venous sinuses, and especially in the tentorium cerebelli, is well-known,25–27 but their in vivo visualization in our experience is difficult. No subselective injections of posterior or anterior meningeal arteries were performed, for feasibility and safety reasons. More physiological and pathological case studies (intracranial hypotension, normal pressure hydrocephalus, for example) are needed. Methods for differentiating dural and osseous venous drainage need to be developed.
Conclusion
Reliable visualization of dural venous drainage is feasible. In vivo findings are consistent with existing embryologic and ex vivo studies. Continued attention may yield further insight into dural vascular pathologies.
Data availability statement
All data relevant to the study are included in the article or uploaded as supplementary information.
Ethics statements
Patient consent for publication
Acknowledgments
The authors would like to acknowledge medical illustrator Jonathan Dimes of J Dimes Medivisual Communications for creation of figure 1.
References
Supplementary materials
Supplementary Data
This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.
Footnotes
Twitter @neuroangio1, @eytanraz, @ENossek, @Kittikack1, @ozmir1
Contributors Substantial contributions to the conception or design of the work: MS, ER, EN, MW, OM, PKN. Acquisition, analysis, or interpretation of data for the work: MS, ER, EN, OM, MW, KS, PKN. Drafting the work or revising it critically for important intellectual content: MS, ER, EN, OM, MW, KS, PKN. Final approval of the version to be published: MS, ER, EN, OM, MW, KS, PKN. Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved: all authors.
Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.
Competing interests MS: consultant to Medtronic. ER: Siemens: stockholder; Rapid Medical: travel; Phenox: Site PI PROST trial; Medtronic: Site PI ADVANCE trial. EN: consultant to Rapid Medical. KS: consultant to Kaneka Medix Corporation. MW: educational consultant to Medtronic.
Provenance and peer review Not commissioned; externally peer reviewed.
Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.