Abstract
The arterial blood supply to the dura mater is rich, complex and is derived from both the internal and external carotid systems. Endovascular management of a variety of intracranial diseases necessitates a thorough understanding of the dural arterial network. In this article we review the normal contributions of the pial arteries to the blood supply of the dura mater and discuss some aspects of its role in the supply of dural arteriovenous shunts (DAVS).
Keywords: Dura, fistula, pial arteries
Introduction
The arterial blood supply to the dura mater is rich, complex and is derived from both the internal and external carotid systems. Endovascular management of a variety of intracranial diseases necessitates a thorough understanding of the dural arterial network. In this article we review the normal contributions of the pial arteries to the blood supply of the dura mater and discuss some aspects of its role in the supply of dural arteriovenous shunts (DAVS).
The meninges
The Egyptians first described the coverings of the brain approximately 5000 years ago but it was Eristratus, in the third century BC, who first coined the term “meninges” and “meninx” (singular), meaning membrane in Greek. Subsequently, Galen described two layers that he termed pacheia and lepte, the tough and the smooth, in the second century A.D. This was translated into Arabic as “umm al-ghalida” (hard mother) and “umm al-raqiqah” (thin mother) after which the Italian monk Stephen of Antioch translated the terms into Latin. The term “al-riqaq” has two meanings, one being smooth and the other being pious. Stephen of Antioch unfortunately chose the latter and the term pia mater has remained in use ever since.
The dura is composed of two layers, an endosteal layer that faces the bone and the meningeal layer facing the brain. These two layers can be seen as separate sheaths at the venous sinuses, optic nerves and foramen magnum. The meningeal layer is continuous with the dural covering of the spinal cord and provides a sleeve-like sheath covering for the cranial nerves as they pass through their cranial foraminae. It fuses with the epineurium of the cranial nerves as they emerge from the cranium with the exception of the optic nerve with which the dural layer fuses with the sclera. The meningeal layer has a similar relationship with the vasculature, where the meningeal layer and the adventitia of the vessels fuse. The meningeal layer folds inward to form the falx cerebri, the falx cerebelli, the tentorium cerebelli and the diaphragm sellae. The endosteal layer is continuous with the pericranium and the periorbital.1
Dural vascular organization
The differentiation of the cranium, dura, arachnoid and pia mater occurs when the embryo has a crown-to-rump length of 12–20 mm. The separation of the vasculature into the extradural, dural and cerebral layers takes place at this stage.2 As the differentiation of the brain coverings progresses the anastomosing channels that connect the deep capillary plexus and the superficial vessels close. The end result is separation of the vessels that surround and supply the brain from those that supply the membranous coverings and the cranium.2,3 The meningeal arteries present after this separation give rise to a dense anastomotic network that divides into primary, secondary and penetrating vessels.
The primary anastomotic arteries are present on the outer surface of the dura and give feeders to the arteries of the cranium, the penetrating dural vessels and secondary anastomotic arteries. These vessels can also supply DAVS.4 They have a straight course, cross the midline, are approximately 100–300 um in diameter and frequently anastomose with each other.
The secondary anastomotic arteries are also present on the outer surface of the dura. These vessels are short, are approximately 20–40 um in diameter, and they form a regular polygonal pattern of anastomotic channels.4
The penetrating arteries can arise from both the primary and the secondary anastomotic arteries. They extend toward the inner surface of the dura and terminate in a rich capillary bed that is separated from the arachnoid by several micrometers.4
The pio-dural arterial supply
Most of the blood supply to the cranial dura mater comes from meningeal arteries originating from the internal carotid artery (ICA), vertebral artery (VA), external carotid artery (ECA) and their branches. However, there is also blood supply to the dura mater originating from pial arteries. These connections are listed below:
-
Anterior cerebral artery (ACA)—olfactory branches and pericallosal branches
Anterior cerebral artery—anterior falcine artery
Posterior cerebral artery (PCA)—the artery of Davidoff and Schechter
Superior cerebellar artery (SCA)—the medial dural tentorial branch
Anterior inferior cerebellar artery (AICA)—the subarcuate artery
Posterior inferior cerebellar artery (PICA)—posterior meningeal artery
These vessels will be discussed with examples of their potential involvement with DAVS.
It is to be noted that in the “normal” disposition there are no connections between middle cerebral artery (MCA) branches and the dural arteries, possibly because the MCA is phylogenetically speaking a “young” artery as it annexes the telencephalon.
ACA branches
The dural supply from the ACA can arise at two levels, one proximally and one distally.5 The proximal dural supply, via olfactory branches, is related to the olfactory nerve and bulb. These arteries can anastomose with the ethmoidal arteries in the region of the cribriform plate. A true, persistent primitive olfactory artery (PPOA) is a rare remnant that occurs with an incidence between 0.14% and 0.29%.6,7
Embryologically the primitive olfactory artery is the rostral division of the primitive ICA.8 It divides into two branches—the medial and lateral olfactory arteries. The medial olfactory artery is the forerunner to the ACA and the lateral olfactory artery the forerunner to the lateral striate, anterior choroidal and Heubner arteries, and later the MCA. During embryological development the medial olfactory artery sends a branch along the olfactory tract. This small branch usually regresses. However, in the case of PPOA there is no regression. If present these branches supply the medial third of the floor of the anterior fossa.
To date four different variants of the PPOA have been described. In type 1 the artery arises directly from the ICA, courses along the olfactory tract and then makes a hairpin turn to supply the distal ACA territory.9 The normal A1 segment is absent. In type 2 the artery arises from the normal A1 and then passes through the cribriform plate to supply the nasal cavity.10 Type 3 represents a transitional type between the aforementioned variants with the PPOA having two separate branches. The superior branch forms the callosomarginal artery and the anterior branch extends toward the cribriform plate. Type 4 arises from the A1 segment and initially courses along the olfactory tract before turning back and taking on the role of an accessory MCA.11
To date we are aware of only one published case of a PPOA, supplying an anterior cranial fossa DAVS (Figure 1).10
Figure 1.
Left ICA angiogram, lateral view (a) showing a DAVS fed by the persistent primitive olfactory artery arising (type 2) from the right ACA (black arrow), forming a venous pouch (black arrow head), and oblique views in the early (b) and late (c) arterial phases demonstrating the DAVS. Note the lack of contribution or hypertrophy of the ophthalmic artery (black arrow heads). (Courtesy Dr S. Tsutsumi, Neurologia Medico-Chirurgica, Tokyo, Japan). ICA: internal carotid artery; DAVS: dural arteriovenous shunts; ACA: anterior cerebral artery.
The distal dural supply from the anterior cerebral artery comes via the pericallosal artery. This artery can send branches to the free margin of the falx cerebri (Figures 2 and 3). These anastomose with the anterior falcine artery and the dural branches of the PCA.5
Figure 2.
Lateral angiogram ((b) is a magnified image) with the catheter in the right internal carotid artery. A dural vessel (white arrows) can be seen to arise from the pericallosal artery before traveling anteriorly and supplying a DAVS that drains into the superior sagittal sinus. DAVS: dural arteriovenous shunts.
Figure 3.
Cadaveric dissection, left frontal antero-superior view, demonstrating a normal dural falcine branch derived from the pericallosal artery. F: falx; FL: left frontal lobe; *branch of the pericallosal artery; °falcine artery.
PCA
In 1965 Wollschläger and Wollschläger described a meningeal artery derived from the PCA. They named this the artery of Davidoff and Schechter (ADS) in honor of their mentors (Figures 4 and 5; the angiogram and cadaveric dissection are from different patients). It is sometimes seen on routine angiography. In a recent anatomical study the artery was found to always be a branch of the P2 segment of the PCA;12 however, it can also originate from the P1 segment as is seen in Figure 4. It classically travels posterolaterally under the SCA and superior to the trochlear nerve to pierce the deep surface of the tentorium cerebelli close to the midpoint of the ipsilateral incisura. After this the vessel travels posteriorly as it takes a sharp upward course to supply the medial part of the tentorium and the posterior third of the falx cerebri (Figure 4). It can occur bilaterally but it is more commonly unilateral and is more common in males and on the left side. It may divide into two branches—an anterior branch that pierces the tentorium and extends along the falx cerebri antero-superiorly, and a posterior branch that extends superiorly. The two branches form an approximately 45-degree angle with each other. In the non-pathological state the vessel is approximately 0.8 mm in diameter12 but it can dilate in pathological states such as with meningiomas,13 hemangioblastomas14 and DAVS.
Figure 4.
Individual images from left vertebral catheter angiograms. The initial lateral and frontal angiograms ((a) and (b)) show an enlarged dural branch arising from the P1 segment of the right posterior cerebral artery (white arrows). The vessel travels postero-superiorly before taking a sharp turn antero-superiorly as it pierces the dura. A follow-up angiogram taken several years after partial treatment shows marked regression of the vessel.
Figure 5.
Cadaveric dissection, left postero-superior view. Small arrowheads identify a vessel derived from the P2 segment of the PCA (not shown) that pierces the under surface of the tentorium cerebelli close to the midline and consistent with the artery of Davidoff and Schechter. PCA: posterior cerebral artery.
SCA
A minor supply to the tentorium cerebelli and falcotentorial junction comes from the SCA. The medial tentorial branch arises from the most superior trunk of the SCA (Figures 6 and 7). It travels within the ambient cistern beneath the tentorium after which it enters the posterior half of the incisura. The course of the vessel tends to parallel that of the marginal tentorial artery. The vessel has a typical appearance on catheter angiography with a straight, or slightly concave downward curve in the lateral plane, and a medial curve in the frontal plane.15 In the microsurgical study performed by Ohno et al. the meningeal branch derived from the SCA was found in 28% of the 25 dissected cadaveric adult brains. It is important to note that arterial to arterial anastomoses can occur between this artery and the ADS within the tentorium because of the rich dural anastomotic network previously described.16
Figure 6.
Frontal angiograms, catheter in the left vertebral artery, demonstrating an enlarged dural artery derived from the left SCA (note the duplicated SCA on the left) that travels inferiorly to the tentorium cerebelli before anastomosing with another dural vessel and supplying a DAVS (arrow) in the region of the sigmoid sinus. A repeat angiogram performed after coil embolization of the right sigmoid sinus shows marked regression of the vessel. SCA: superior cerebellar artery; DAVS: dural arteriovenous shunts.
Figure 7.
Cadaveric dissection, right postero-superior view showing a small dural branch (black arrow heads) piercing the undersurface of the tentorium cerebelli and derived from the superior cerebellar artery.
AICA
The subarcuate artery is commonly a branch of the lateral pontine segment of the AICA (Figures 8, 9 and 10). It originates medially to the porus acusticus. The artery penetrates the dura and enters the subarcuate canal. It supplies the superolateral edge of the internal acoustic meatus and adjacent posterior surface of the petrous bone as well as the petrous bone in the region of the semi-circular canals17 and the dura around the acoustic meatus. It anastomoses with the stylomastoid arterial branches, the mastoid branches of the occipital artery and the petrous branches of the middle meningeal artery. These dural anastomoses may be recruited in cases of AICA occlusion.18
Figure 8.
(a) A magnified view from a contrast-enhanced T1-weighted MRI scan demonstrating the DAVS close to the petrous apex (white arrow) and a large venous pouch (dashed white arrow) seen in the pontine cistern. Catheter angiography of the left vertebral artery ((b) and (c)) demonstrates the AICA (two small white arrows) giving rise to a vessel distal to the meatal loop (white arrow) that supplies the fistula (black arrow) and the early venous drainage (dashed arrows). MRI: magnetic resonance imaging; DAVS: dural arteriovenous shunts; AICA: anterior inferior cerebellar artery.
Figure 9.
A right vertebral injection demonstrates supply to a left-sided fistula (black arrow) with arterial supply from the subarcuate (long white arrow) that originates distally to the meatal loop of the AICA (two small white arrows). AICA: anterior inferior cerebellar artery.
Figure 10.
Cadaveric dissection of the internal acoustic meatus and subarcuate region.
(a) A right posterior view of a ponto-cerebellar angle. R: retractor on the right cerebellum; °anterior inferior cerebellar artery (AICA); *subarcuate artery entering the subarcuate canal.
(b) A right superior view of the ponto-cerebellar angle clearly depicting the origin of the subarcuate artery from the anterior inferior cerebellar artery (AICA) close the meatal loop. °AICA; *subarcuate artery entering the subarcuate canal.
In addition to the normal disposition of the vessel, several alternatives can exist. The artery can originate from the labyrinthine artery or even from a cortical branch. In this latter scenario it is called the cerebellosubarcuate artery19 and originates proximally to the meatal loop, inferiorly to the nerves as they enter the meatus before turning sharply superolaterally to enter the subarcuate canal. The cerebellar branch of this variant supplies the flocculus and adjacent cortex. Infrequently the subarcuate artery can arise from within the internal acoustic canal, and in these cases it takes either a recurrent course through the porus of the canal or by penetrating the meatal roof.
PICA
The posterior meningeal artery can arise from the PICA (Figures 11 and 12), although it can also arise from the vertebral artery, occipital artery, ICA and hypoglossal branch of the ascending pharyngeal artery. Regardless of its origin, the artery is easily identified on lateral projection. It ascends posterosuperiorly almost parallel to the internal occipital crest to reach the attachment of the falx cerebelli. The artery anastomoses with middle meningeal and occipital branches. It supplies the dura over the atlanto-occipital space, the medial and paramedial cerebellar fossa and the falx cerebelli as well as the dura that forms the walls of transverse sinus, the torcula and the dura over the occipital convexity. The artery of the falx cerebelli (Figure 13) can also arise from the PICA and can be seen to travel along the free margin of the falx cereblli with a straight course away from the inner table of the occipital bone.
Figure 11.
Angiography of the left vertebral artery ((a) lateral, (b) Towne’s) shows the posterior meningeal artery (dashed white arrow) arising from the PICA (white arrow) and extending postero-superiorly to supply a DAVS in the superior sagittal sinus. Note the curved course of the posterior meningeal artery as it travels along the inner surface of the calvarium in contrast to the straight course of the artery of the falx cerebelli. PICA: posterior inferior cerebellar artery; DAVS: dural arteriovenous shunt.
Figure 12.
Cadaveric dissection, posterior view of the cranio-spinal junction, showing the posterior meningeal vessel piercing the dura. The origin from the PICA is not shown in this image. D: dura; °: posterior inferior cerebellar artery (PICA); *Posterior meningeal artery.
Figure 13.
A lateral projection of selective catheter angiography in the right vertebral artery that shows the artery of the falx cerebelli, (small white arrows) with its straight course derived from the PICA (long white arrow) and supplying a dural AV fistula (images courtesy of Dr J. Bergdahl, Umea, Sweden). PICA: posterior inferior cerebellar artery; AV: arteriovenous.
Discussion
The normal pio-dural connections cross the subarachnoid membrane and the subdural space at predefined places. They connect the two arterial systems and thus embolic material particles or liquid embolics may pass freely from one system to the other.
Understanding the normal anatomy is essential to safely perform endovascular treatments in or adjacent to the central nervous system. In this regard it is imperative that those practicing this specialty have a thorough knowledge of vessels that may anastomose the dural and pial arterial systems. We have therefore in this article described the common or “normal” dural vessels arising from pial arteries.
The underlying cause for the enlargement of these vessels in patients with DAVS is not fully understood although it is likely the mechanisms involved in the generation and growth of DAVS act not only on the usual dural vessels but pio-dural vessels also. These mechanisms may involve the release of angiogenic growth factors.20–22
Conclusion
In the normal human there may be direct pio-dural arterial connections in six different areas, creating a pathway and connections within the dura mater for the blood supply to arteriovenous shunts or for embolic material. Knowledge of this anatomy is mandatory to reduce the risk for complications from endovascular treatment in this region.
Acknowledgments
We wish to acknowledge Dr S. Tsutsumi for Figure 1 and Dr J. Bergdahl for Figure 12.
Author contributions: Guarantor of integrity: M. Söderman; definition of intellectual content: all authors; literature search: P. Bhogal and G. Rodesch; clinical studies: all authors; data acquisition: P. Bhogal, H.L.D. Makalanda, M. Söderman and P. Mercier; data analysis: P. Bhogal, P. Mercier and M. Söderman; manuscript preparation: P. Bhogal, V. Gontu, P. Mercier, G. Rodesch and P.A. Brouwer; manuscript editing: P. Bhogal and M. Söderman; and manuscript review: H.L.D. Makalanda and P.A. Brouwer.
Funding
The author(s) received no financial support for the research, authorship, and/or publication of this article.
Declaration of conflicting interests
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
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