**3. Extracranial-to-intracranial anastomoses**

178 Neuroimaging for Clinicians – Combining Research and Practice

vascular arch (the right aortic arch) to form the proximal part of the subclavian artery and from it originates the VA. On the left side, the seventh cervical intersegmental artery coalesces with the left aortic arch (distal fourth arch–true adult aortic arch) to form the proximal left subclavian artery and from it originates the left VA (Figure 3). By 6 weeks' gestation, the cranial-most end of the ICAs have divided into rostral and caudal divisions. Although the rostral division will form the anterior, middle and anterior choroidal arteries, the caudal division fuses with the dorsal longitudinal neural arteries to form the PCoA. This

results in eventual disappearance of the primitive carotid-basilar anastomoses.

Fig. 3. Diagrammatic sketch of the craniocerebral vasculature at 7 weeks of development. The arch and great vessels are approaching their definitive form. Origins of these vessels from their embryonic precursors are depicted schematically. The fourth and sixth aortic arches are undergoing asymmetric remodeling to supply blood to the upper extremities, dorsal aorta, and lungs. The right sixth arch has involuted (leaving only part of the right pulmonary artery). The right dorsal aorta distal to the origin of the subclavian artery (SCA) is regressing (*dotted lines*) but remains connected to the right fourth arch. The right third and

fourth arches are forming the brachiocephalic trunk; the left fourth arch becomes the definitive aortic arch. The left dorsal aorta becomes the proximal descending aorta. The first six cervical intersegmental arteries have become the definitive vertebral arteries (VAs); the C7 arteries have enlarged to become part of the developing subclavian arteries (SCAs). The longitudinal neural arteries are fusing across the midline to form the definitive basilar artery

(BA). *Permission requested from Osborn AG: Diagnostic Cerebral Angiography (2nd ed). Philadelphia: Lippincott Williams & Wilkins, Wolters Kluwer, 1999, figure 1-4, page 11.* 

been described by Larsen14 and Lasjaunias et al.15

Most of these changes are complete in the adult configuration by 8 weeks of gestation. For a review and further details, please see Osborn's detailed descriptions.22 Further details have For the purpose of grouping these anastomoses, Lasjaunias et al.15,16 and Berenstein et al.3 described regions within the cranial circulation that could be divided on the basis of primitive vascular connections. They divided the regions as follows:


This division, although overlapping, serves to identify vascular territories of concern; that is**,**  functional areas in which anastomotic dysfunction may become most apparent, thereby tailoring angiographic and neurologic examination during intraprocedural monitoring. Even when not apparent on routine angiography, these connections exist as byproducts of a unified vascular development for the entire head and neck region.8 Under situations of increased flow, such as with arteriovenous fistulas (AVFs) or arteriovenous malformations (AVMs), there may be arterio-arterial embolization, resulting in deficits. In other cases, shared venous outflow may complicate options or results. Similarly, simply injecting materials, whether contrast or embolic materials, particularly liquid agents, may result in their crossing the anastomosis to occlude functional vessels supplying neural tissues, thereby creating unintended deficits. In addition, as embolization proceeds and the desired target vessel occludes, putative collateral anastomoses may be at increased risk. This may occur because of their presence as a relative lower-pressure sump (in the face of an occluded principal target vessel), resulting in the preferential shunting of embolic materials into these collaterals.**5** Although these collaterals may increase the risk of embolization procedures in the skull base, they serve to provide critical collaterals in the face of acute or subacute carotid or VB occlusion. They provide an innate bypass that grows under an increased demand from a hypoperfused intracranial territory. A recent review by Geibprasert et al.9 describes these extracranial–intracranial anastomoses in considerable detail. These anastomotic connections are summarized in **Table 1**.


Table 1. Extracranial-to-Intracranial Anastomoses

Intracranial Arterial Collateralization: Relevance in Neuro-Endovascular Procedures 181

underside of the optic nerve in the optic canal. Upon entering the orbit, it maintains its close relationship with the optic nerve traveling towards the posterior globe. The recurrent meningeal artery is a reliable branch often noted by microvascular surgeons along the lateral aspect of the superior orbital fissure and is a branch of the middle meningeal artery. This supplies the contents of the superior orbital fissure and then anastomoses with the second segment of the ophthalmic artery in the orbit. This anastomosis is of particular importance when embolizing the middle meningeal artery branches, particularly for convexity meningiomas. The recurrent meningeal artery can often be visualized as the middle meningeal artery crosses the sphenoid wing. In cases in which embolization is desirable, it is best to obtain distal access close to or in the tumor proper and be vigilant to reflux to this more proximal branch point. In other cases where a branch is not noted, an intraarterial injection of sodium amytal and lidocaine may allow Wada testing32 of the anastomosis,

Fig. 5. Selective ECA angiogram reveals a tumor blush of an anterior cranial fossa

meningioma. The principal supply is the middle meningeal artery (A), which divides into the parietal branch (B) and an enlarged recurrent meningeal branch (C) that, along with the accessory meningeal artery (D), is the principal supply for this tumor (E, tumor blush).

The second group of anastomoses is a product of the shared supply to the ethmoidal sinuses from the anterior and posterior branches of the ophthalmic artery as well as branches from septal, sphenopalatine, and greater palatine branches of the internal maxillary artery.1 These occur along the second and third segments of the ophthalmic artery. In addition, anastomoses may also exist between the ophthalmic artery and deep temporal and infraorbital branches of the internal maxillary artery. These arise particularly because of shared ophthalmic and internal maxillary supply to the lacrimal apparatus (Figure 4). These anastomotic connections carry great significance during embolization for epistaxis. Most of the anastomotic connections through the lacrimal and ethmoidal arteries tend to be very

which may not be apparent (Figures 4 and 5).

#### **3.1 Ophthalmic artery anastomoses**

The ophthalmic artery is the principal vascular supply for contents in the orbit.13 It is the principal supply to the central retinal artery, which in turn, supplies the retina and choroid. Occlusion of this vessel will result in monocular blindness. Therefore, visualization of a choroid blush with an ECA injection should raise alarms about potential anatomic variations and dangerous collaterals.25 The ophthalmic artery originates from the ICA; however, during its development, it necessarily develops connections with other sources of supply to the contents of the orbit. The primitive stapedial artery contributes to the middle meningeal artery, and this develops some connections to the ophthalmic artery through the superior orbital fissure.26 The magnitude of this connection may vary; rarely, the middle meningeal and internal maxillary arteries completely assume the principal source of supply to the ophthalmic artery. In cases in which the ophthalmic artery is not visualized, such variation should be suspected.

Fig. 4. An ECA angiogram in a patient with ICA occlusion, with reconstitution of the ICA through collaterals via the ophthalmic artery and the cavernous ICA. The vidian artery (A) is supplying collateral flow from the internal maxillary artery (B) to the petrous ICA (C). The frontal branch of the superficial temporal artery (D) is providing transosseous collaterals to the frontal meningo-pial collaterals, whereas the parietal branch (E) is not involved. The PCoA (F) is involved in the extensive neovascularization through its perforators, typical of Moya Moya disease. The ophthalmic artery (G) is the largest source of retrograde collateral flow to the ICA. It is receiving its supply principally through its ethmoidal arteries (H) via connections with the internal maxillary artery. Another source of supply to the ophthalmic artery is the recurrent meningeal branch (I) of the middle meningeal artery.

The anastomotic connections of the ECA branches with the ophthalmic artery may be divided according to the segments of the ophthalmic artery.13 The first segment of the ophthalmic artery arises as the first supraclinoidal branch of the ICA and travels on the

The ophthalmic artery is the principal vascular supply for contents in the orbit.13 It is the principal supply to the central retinal artery, which in turn, supplies the retina and choroid. Occlusion of this vessel will result in monocular blindness. Therefore, visualization of a choroid blush with an ECA injection should raise alarms about potential anatomic variations and dangerous collaterals.25 The ophthalmic artery originates from the ICA; however, during its development, it necessarily develops connections with other sources of supply to the contents of the orbit. The primitive stapedial artery contributes to the middle meningeal artery, and this develops some connections to the ophthalmic artery through the superior orbital fissure.26 The magnitude of this connection may vary; rarely, the middle meningeal and internal maxillary arteries completely assume the principal source of supply to the ophthalmic artery. In cases in which the ophthalmic artery is not visualized, such

Fig. 4. An ECA angiogram in a patient with ICA occlusion, with reconstitution of the ICA through collaterals via the ophthalmic artery and the cavernous ICA. The vidian artery (A) is supplying collateral flow from the internal maxillary artery (B) to the petrous ICA (C). The frontal branch of the superficial temporal artery (D) is providing transosseous collaterals to the frontal meningo-pial collaterals, whereas the parietal branch (E) is not involved. The PCoA (F) is involved in the extensive neovascularization through its perforators, typical of Moya Moya disease. The ophthalmic artery (G) is the largest source of retrograde collateral flow to the ICA. It is receiving its supply principally through its ethmoidal arteries (H) via connections with the internal maxillary artery. Another source of supply to the ophthalmic

The anastomotic connections of the ECA branches with the ophthalmic artery may be divided according to the segments of the ophthalmic artery.13 The first segment of the ophthalmic artery arises as the first supraclinoidal branch of the ICA and travels on the

artery is the recurrent meningeal branch (I) of the middle meningeal artery.

**3.1 Ophthalmic artery anastomoses** 

variation should be suspected.

underside of the optic nerve in the optic canal. Upon entering the orbit, it maintains its close relationship with the optic nerve traveling towards the posterior globe. The recurrent meningeal artery is a reliable branch often noted by microvascular surgeons along the lateral aspect of the superior orbital fissure and is a branch of the middle meningeal artery. This supplies the contents of the superior orbital fissure and then anastomoses with the second segment of the ophthalmic artery in the orbit. This anastomosis is of particular importance when embolizing the middle meningeal artery branches, particularly for convexity meningiomas. The recurrent meningeal artery can often be visualized as the middle meningeal artery crosses the sphenoid wing. In cases in which embolization is desirable, it is best to obtain distal access close to or in the tumor proper and be vigilant to reflux to this more proximal branch point. In other cases where a branch is not noted, an intraarterial injection of sodium amytal and lidocaine may allow Wada testing32 of the anastomosis, which may not be apparent (Figures 4 and 5).

Fig. 5. Selective ECA angiogram reveals a tumor blush of an anterior cranial fossa meningioma. The principal supply is the middle meningeal artery (A), which divides into the parietal branch (B) and an enlarged recurrent meningeal branch (C) that, along with the accessory meningeal artery (D), is the principal supply for this tumor (E, tumor blush).

The second group of anastomoses is a product of the shared supply to the ethmoidal sinuses from the anterior and posterior branches of the ophthalmic artery as well as branches from septal, sphenopalatine, and greater palatine branches of the internal maxillary artery.1 These occur along the second and third segments of the ophthalmic artery. In addition, anastomoses may also exist between the ophthalmic artery and deep temporal and infraorbital branches of the internal maxillary artery. These arise particularly because of shared ophthalmic and internal maxillary supply to the lacrimal apparatus (Figure 4). These anastomotic connections carry great significance during embolization for epistaxis. Most of the anastomotic connections through the lacrimal and ethmoidal arteries tend to be very

Intracranial Arterial Collateralization: Relevance in Neuro-Endovascular Procedures 183

artery (Figure 7). The superior orbital artery anastomoses with the frontal branches of the superficial temporal artery. This anastomosis may gain relevance in situations in which the ICA is occluded with connections via the superior orbital artery supplying the ophthalmic artery and, in some cases, direct transosseous collaterals to frontal cortical meningo-pial anastomoses (Figure 4). The dorsal nasal artery anastomoses with terminal nasal branches of the facial artery as well as the inferior orbital artery (a terminal branch of the internal maxillary artery) (Figure 7). These anastomoses, particularly the latter, are of great significance during embolization procedures for epistaxis. A high-pressure angiogram through the microcatheter (micro-angiogram) prior to embolization may allow better identification of such dangerous collaterals as compared to an ECA angiogram from a more

Fig. 7. Selective ICA injection demonstrates an occlusion beyond the origin of the ophthalmic artery. The ICA (A) gives rise to the ophthalmic artery (B), which is its first supraclinoidal branch. The ophthalmic artery then gives rise to multiple ethmoidal arteries (C), terminating as the dorsal nasal artery (D) and the supraorbital artery (E), which passes through the supraorbital notch (G) to anastomose with branches from the frontal branch of the superficial temporal artery. Inferiorly, the dorsal nasal artery anastomoses with the

The anastomoses that fall within this region are complex and prone to multiple variations. Only the principal trunks are seen in good-quality angiograms. Although always there, these collateral pathways only become apparent in cases of increased flow across these connections, such as during petrocavernous AVF embolization or after cervical ICA occlusion (Figures 4, 6, and 8). A systematic discussion has recently been provided in detail by Geibprasert et al.9 To understand the organization of these collaterals, one can attempt to

terminal angular branch of the facial artery (F).

**3.2 Petrocavernous internal carotid artery collaterals** 

proximal location.

small-caliber vessels (less than 80 microns). If embolization is desired, particles chosen should be greater than 150 microns. This prevents inadvertent passage of these particles into the ICA or ophthalmic artery through these collaterals. As noted above, one needs to identify an aberrant ophthalmic artery origin by always performing a cerebral angiogram to identify the origin of the ophthalmic artery from the ICA. Embolization of anterior fossabased tumors, such as olfactory groove meningiomas, is considered high risk because the principal supply to these tumors is from the ethmoidal arteries, and transinternal maxillary or transophthalmic embolization of these branches may have an inordinate increased risk for some of the material refluxing into the central retinal artery or retrograde into the ICA (Figure 5).1 Another consideration is with falcine meningiomas in which the anterior falcine artery, a branch of the ophthalmic artery, may anastomose with frontal branches of the middle meningeal artery, with retrograde flux of embolization materials into the ophthalmic artery from a middle meningeal artery branch embolization. Other situations in which these anastomoses need to be considered are during embolization for tumors in the head and neck region, particularly juvenile angiofibromas. Cavernous sinus DAVFs are particularly challenging because their inherent incorporation of these varied collateral channels may create significant risk for transarterial embolization (Figure 6).

The third group of anastomoses occurs along the third or terminal segments of the ophthalmic artery and its terminal branches, the dorsal nasal artery and superior orbital

Fig. 6. An ECA angiogram in a patient with a surgical ICA occlusion and cavernous DAVF due to a gun shot (A). The hypertrophied ECA trunk (B) is supplying an enlarged internal maxillary artery (C) and its principal branches: middle meningeal artery (D), accessory meningeal artery (E), deep temporal artery (F), and sphenopalatine artery (G). The sphenoparietal artery branches to supply the small infraorbital artery (H), and the numerous septal arteries communicate with the ethmoidal arteries (I) to supply the enlarged ophthalmic artery (J). The enlarged recurrent meningeal branch (K) is noted off the middle meningeal artery. The accessory meningeal artery is seen communicating with the inferolateral trunk and artery of the foramen rotundum (L), with its typical corkscrew shape.

small-caliber vessels (less than 80 microns). If embolization is desired, particles chosen should be greater than 150 microns. This prevents inadvertent passage of these particles into the ICA or ophthalmic artery through these collaterals. As noted above, one needs to identify an aberrant ophthalmic artery origin by always performing a cerebral angiogram to identify the origin of the ophthalmic artery from the ICA. Embolization of anterior fossabased tumors, such as olfactory groove meningiomas, is considered high risk because the principal supply to these tumors is from the ethmoidal arteries, and transinternal maxillary or transophthalmic embolization of these branches may have an inordinate increased risk for some of the material refluxing into the central retinal artery or retrograde into the ICA (Figure 5).1 Another consideration is with falcine meningiomas in which the anterior falcine artery, a branch of the ophthalmic artery, may anastomose with frontal branches of the middle meningeal artery, with retrograde flux of embolization materials into the ophthalmic artery from a middle meningeal artery branch embolization. Other situations in which these anastomoses need to be considered are during embolization for tumors in the head and neck region, particularly juvenile angiofibromas. Cavernous sinus DAVFs are particularly challenging because their inherent incorporation of these varied collateral channels may

The third group of anastomoses occurs along the third or terminal segments of the ophthalmic artery and its terminal branches, the dorsal nasal artery and superior orbital

Fig. 6. An ECA angiogram in a patient with a surgical ICA occlusion and cavernous DAVF due

sphenoparietal artery branches to supply the small infraorbital artery (H), and the numerous septal arteries communicate with the ethmoidal arteries (I) to supply the enlarged ophthalmic artery (J). The enlarged recurrent meningeal branch (K) is noted off the middle meningeal artery. The accessory meningeal artery is seen communicating with the inferolateral trunk and

to a gun shot (A). The hypertrophied ECA trunk (B) is supplying an enlarged internal maxillary artery (C) and its principal branches: middle meningeal artery (D), accessory meningeal artery (E), deep temporal artery (F), and sphenopalatine artery (G). The

artery of the foramen rotundum (L), with its typical corkscrew shape.

create significant risk for transarterial embolization (Figure 6).

artery (Figure 7). The superior orbital artery anastomoses with the frontal branches of the superficial temporal artery. This anastomosis may gain relevance in situations in which the ICA is occluded with connections via the superior orbital artery supplying the ophthalmic artery and, in some cases, direct transosseous collaterals to frontal cortical meningo-pial anastomoses (Figure 4). The dorsal nasal artery anastomoses with terminal nasal branches of the facial artery as well as the inferior orbital artery (a terminal branch of the internal maxillary artery) (Figure 7). These anastomoses, particularly the latter, are of great significance during embolization procedures for epistaxis. A high-pressure angiogram through the microcatheter (micro-angiogram) prior to embolization may allow better identification of such dangerous collaterals as compared to an ECA angiogram from a more proximal location.

Fig. 7. Selective ICA injection demonstrates an occlusion beyond the origin of the ophthalmic artery. The ICA (A) gives rise to the ophthalmic artery (B), which is its first supraclinoidal branch. The ophthalmic artery then gives rise to multiple ethmoidal arteries (C), terminating as the dorsal nasal artery (D) and the supraorbital artery (E), which passes through the supraorbital notch (G) to anastomose with branches from the frontal branch of the superficial temporal artery. Inferiorly, the dorsal nasal artery anastomoses with the terminal angular branch of the facial artery (F).

#### **3.2 Petrocavernous internal carotid artery collaterals**

The anastomoses that fall within this region are complex and prone to multiple variations. Only the principal trunks are seen in good-quality angiograms. Although always there, these collateral pathways only become apparent in cases of increased flow across these connections, such as during petrocavernous AVF embolization or after cervical ICA occlusion (Figures 4, 6, and 8). A systematic discussion has recently been provided in detail by Geibprasert et al.9 To understand the organization of these collaterals, one can attempt to

Intracranial Arterial Collateralization: Relevance in Neuro-Endovascular Procedures 185

trunk of the ascending pharyngeal artery) and the accessory meningeal artery to provide a branch to the pterygovaginal canal, which ends by anastomosing with internal maxillary

Fig. 9. Selective microinjection in an occluded ICA demonstrating connections with

extracranial vessels. The ICA (A) is occluded at the distal cavernous segment. Its cavernous branches, the meningohypophyseal trunk (B) and inferolateral trunk (C) are noted. The inferolateral trunk is anastomosing with branches of the internal maxillary artery, particularly the sphenopalatine artery (F), through the artery of the foramen rotundum. More inferiorly, the primitive mandibular (petrous) branch anastomoses with the vidian artery (D), which originates from the sphenopalatine artery. Further inferiorly, the caroticotympanic artery is seen anastomosing with the ascending pharyngeal artery (G); and, together, these vessels are supplying the artery of the pterygovaginal canal (E).

The third branch of note is the primitive maxillary artery remnant, the meningohypophyseal trunk. This branch has widespread connections along the posterior cavernous sinus and clivus. Anteriorly, it anastomoses through its tentorial branch (of Bernasconi and Cassinari) with petrous branches from the middle meningeal artery. These branches are particularly noted during angiography for superior petrosal sinus or transverse-sigmoid junction DAVFs (Figure 10). More posteriorly, its major branch, the lateral clival artery, anastomoses extensively with neuromeningeal branches of the ascending pharyngeal artery, including

The most proximal branch of the ICA is the caroticotympanic artery in the petrous canal.10,21,23,30 This embryologic remnant of the hyoid artery anastomoses with the tympanic plexus, which is supplied by the tympanic branches of the ascending pharyngeal artery, stylomastoid artery from the posterior auricular artery, and petrotympanic branches of the

branches that supply the hypoglossal and jugular foramina.

middle meningeal artery (Figure 9).

artery branches (Figure 9).

look at these putative connections in terms of branches of the ICA, which are involved in the anastomosis. The first branch traveling rostrocaudal or distal to proximal along the ICA is the inferolateral trunk off the ICA in the cavernous sinus.

Fig. 8. An ECA angiogram following successful bypass with a radial artery graft from the ECA to the MCA. The radial artery graft (A) can be seen overlaid on the cavernous sinus anastomosis. Parietal branch of the middle meningeal artery (B). Occipital artery (C). Internal maxillary artery trunk (D). The caroticotympanic artery (E) anastomoses with branches from the ascending pharyngeal branches (F) to reconstitute the ICA. The accessory meningeal artery (G) is anastomosing with the inferolateral trunk branches. Additionally, the ethmoidal vessels (H) are supplying the ophthalmic artery (K). The inferolateral trunk is anastomosing with branches from the middle meningeal branches at the foramen spinosum (J) and through the artery of the foramen rotundum more anteriorly.

The inferolateral trunk has multiple branches, which supply the anterior and middle parts of the cavernous sinus structures.4,15,17,30 It is a remnant of an embryologic dorsal ophthalmic artery and connects to its ECA counterparts principally along the foramina of cranial nerves or in the meningeal walls of the cavernous sinus. Anteriorly, it communicates with the internal maxillary artery through the artery of the foramen rotundum; laterally, it collateralizes with the cavernous branches of the middle meningeal artery, which arise soon after the artery exits the foramen spinosum; and, posteriorly, it communicates with the accessory meningeal artery through the artery of foramen ovale (Figure 8).

The second branch in this order is a remnant of the primitive stapedial artery and the subsequent mandibular trunk off the stapediohyoid artery, a small branch that pierces the foramen lacerum arising either directly off the carotid artery or as a branch off the meningohypophyseal trunk, which enters the vidian canal to anastomose with the sphenopalatine artery (a branch of the internal maxillary artery in the sphenopalatine fossa).29 It also anastomoses with the superior pharyngeal artery (a branch of the pharyngeal

look at these putative connections in terms of branches of the ICA, which are involved in the anastomosis. The first branch traveling rostrocaudal or distal to proximal along the ICA is

Fig. 8. An ECA angiogram following successful bypass with a radial artery graft from the ECA to the MCA. The radial artery graft (A) can be seen overlaid on the cavernous sinus anastomosis. Parietal branch of the middle meningeal artery (B). Occipital artery (C). Internal maxillary artery trunk (D). The caroticotympanic artery (E) anastomoses with branches from the ascending pharyngeal branches (F) to reconstitute the ICA. The accessory meningeal artery (G) is anastomosing with the inferolateral trunk branches. Additionally, the ethmoidal vessels (H) are supplying the ophthalmic artery (K). The inferolateral trunk is anastomosing with branches from the middle meningeal branches at the foramen spinosum

The inferolateral trunk has multiple branches, which supply the anterior and middle parts of the cavernous sinus structures.4,15,17,30 It is a remnant of an embryologic dorsal ophthalmic artery and connects to its ECA counterparts principally along the foramina of cranial nerves or in the meningeal walls of the cavernous sinus. Anteriorly, it communicates with the internal maxillary artery through the artery of the foramen rotundum; laterally, it collateralizes with the cavernous branches of the middle meningeal artery, which arise soon after the artery exits the foramen spinosum; and, posteriorly, it communicates with the

The second branch in this order is a remnant of the primitive stapedial artery and the subsequent mandibular trunk off the stapediohyoid artery, a small branch that pierces the foramen lacerum arising either directly off the carotid artery or as a branch off the meningohypophyseal trunk, which enters the vidian canal to anastomose with the sphenopalatine artery (a branch of the internal maxillary artery in the sphenopalatine fossa).29 It also anastomoses with the superior pharyngeal artery (a branch of the pharyngeal

(J) and through the artery of the foramen rotundum more anteriorly.

accessory meningeal artery through the artery of foramen ovale (Figure 8).

the inferolateral trunk off the ICA in the cavernous sinus.

trunk of the ascending pharyngeal artery) and the accessory meningeal artery to provide a branch to the pterygovaginal canal, which ends by anastomosing with internal maxillary artery branches (Figure 9).

Fig. 9. Selective microinjection in an occluded ICA demonstrating connections with extracranial vessels. The ICA (A) is occluded at the distal cavernous segment. Its cavernous branches, the meningohypophyseal trunk (B) and inferolateral trunk (C) are noted. The inferolateral trunk is anastomosing with branches of the internal maxillary artery, particularly the sphenopalatine artery (F), through the artery of the foramen rotundum. More inferiorly, the primitive mandibular (petrous) branch anastomoses with the vidian artery (D), which originates from the sphenopalatine artery. Further inferiorly, the caroticotympanic artery is seen anastomosing with the ascending pharyngeal artery (G); and, together, these vessels are supplying the artery of the pterygovaginal canal (E).

The third branch of note is the primitive maxillary artery remnant, the meningohypophyseal trunk. This branch has widespread connections along the posterior cavernous sinus and clivus. Anteriorly, it anastomoses through its tentorial branch (of Bernasconi and Cassinari) with petrous branches from the middle meningeal artery. These branches are particularly noted during angiography for superior petrosal sinus or transverse-sigmoid junction DAVFs (Figure 10). More posteriorly, its major branch, the lateral clival artery, anastomoses extensively with neuromeningeal branches of the ascending pharyngeal artery, including branches that supply the hypoglossal and jugular foramina.

The most proximal branch of the ICA is the caroticotympanic artery in the petrous canal.10,21,23,30 This embryologic remnant of the hyoid artery anastomoses with the tympanic plexus, which is supplied by the tympanic branches of the ascending pharyngeal artery, stylomastoid artery from the posterior auricular artery, and petrotympanic branches of the middle meningeal artery (Figure 9).

Intracranial Arterial Collateralization: Relevance in Neuro-Endovascular Procedures 187

The neuromeningeal trunk of the ascending pharyngeal artery anastomoses with the VA, through connections at C3 through muscular collaterals, and more rostrally, as the remnant

More caudally, the cervical branches of the subclavian artery anastomose with proximal sections of the VAs (C3-7). The ascending cervical artery arises from the thyrocervical trunk, while the deep cervical artery arises from the costocervical trunk. Both these branches form connections with the segmental vertebral branches through muscular collaterals. They are

First and foremost, one needs to be aware of the potential for collateral anastomotic channels. Such knowledge facilitates angiographic visualization. Even if the initial proximal external carotid or subclavian angiograms do not result in the visualization of these collaterals, we recommend that selective microcatheter angiograms be performed in as distal a position as is reasonably attainable immediately prior to embolization. These higher pressure selective injections are more likely to reveal these putative connections. If there is no visualization, a second element to further bolster confidence is to perform a Wada test with sodium amytal (75 mg) and lidocaine (30 mg) intraarterially through the microcatheter from the position planned for embolization and then immediately after injection to test for loss of appropriate neural function including that of the cranial nerves. Thirdly, if embolization is desired, polyvinyl alcohol particles, which considerably exceed the size (150 microns or greater) of most of these non-angiographically visualized collaterals (50-80 microns), should be used. Liquid embolics, such as glue (N-butyl cyanoacrylate; Trufill, Codman Neurovascular, Raynham, MA) and Onyx (EV3, Irvine, California), provide superior visualization; however, they are not discriminatory with respect to vessel size and, therefore, their use may be associated with a higher likelihood of collateral vessel occlusion. Angiographic visualization does not preclude embolization. One may attempt to attain distal purchase beyond the collateral communication and pay great attention to reflux during the embolization procedure. If such positioning is not attainable, pre-embolization occlusion of the collateral channel is another strategy. Typically, coil embolization of the collateral channel will not result in ischemic injury because of the multiple sources of vascular supply at the skull base; however, subsequent embolization of the intended vessel will prevent inadvertent passage of embolic materials through the occluded vessel to critical

In contrast to the extracranial-to-intracranial collateral anastomoses described above, which may be less obvious on non-superselective angiography, many of the ICA-to-ICA or ICA-to-VB anastomoses are rather easily identified and commonly seen. These common known collateral anastomoses as parts of the circle of Willis include the following: 1) anterior communicating artery (ACoA) connecting bilateral anterior cerebral arteries (ACAs); and 2) PCoA connecting the ipsilateral ICA to the posterior cerebral artery (PCA). Less obvious anastomoses occur among the various terminal cortical branches from each of the major vascular territories. The middle cerebral artery (MCA) branches anastomose with branches

of the primitive hypoglossal artery with the odontoid arch vascular system.11,19

**3.4 Extracranial to intracranial collateralization and complication avoidance in** 

commonly noted to reconstitute the distal VA after proximal occlusion.

**neurointervention procedures** 

neural structures.

**4. Intracranial anastomoses** 

Fig. 10. A CCA angiogram revealing a transverse-sigmoid junction DAVF. ICA (A). The middle meningeal artery's (B) petrous branch (C) is supplying the DAVF, as is the tentorial branch (D) of the meningohypophyseal trunk of the ICA. The transosseous branches from the occipital artery (E) are a major supply to the DAVF (F).

These branches become most apparent as vascular sources for cavernous and petroclival meningiomas or for tympanic or jugular foramen glomus tumors. Because of the critical supply to cranial nerves and their ganglia in these foramina, embolization of these vessels carries potential for lower cranial nerve dysfunction.

#### **3.3 Vertebrobasilar anastomoses**

As noted above, the VB system develops through posterior paired longitudinal arteries that coalesce rostrally to form the basilar artery (BA), while inferiorly they remain separate as VAs. Rostrally, this system is supplied through collaterals of which only the PCoA remains in most adults. Primitive anastomoses include the trigeminal artery, which remains as a branch to Meckel's cave; the otic artery, as the labyrinthine artery; the hypoglossal artery, as an artery to the hypoglossal canal; and the proatlantal artery, as the occipital artery and its connections to the VA over the first cervical vertebra and separately at the second cervical vertebra, through segmental vertebral branches. Although regressed, these connections may remain viable and become prominent under conditions of increased flow. Rarely, they remain as principal supply to the posterior circulation with regression of the more proximal VB system.18,24,27

The occipital artery routinely has a prominent connection to the VA as it emerges from the C1 transverse foramen. Embolization of dural arteriovenous fistulas (DAVFs), particularly those involving the transverse sinuses at the transverse sigmoid junction or torcula, can have enlarged occipital feeders; and care must be exercised to ensure that no inadvertent posterior circulation embolization occurs. In other situations, this route may be used to treat intracranial lesions, such as acute occlusions,33 or other pathologic conditions.

Fig. 10. A CCA angiogram revealing a transverse-sigmoid junction DAVF. ICA (A). The middle meningeal artery's (B) petrous branch (C) is supplying the DAVF, as is the tentorial branch (D) of the meningohypophyseal trunk of the ICA. The transosseous branches from

These branches become most apparent as vascular sources for cavernous and petroclival meningiomas or for tympanic or jugular foramen glomus tumors. Because of the critical supply to cranial nerves and their ganglia in these foramina, embolization of these vessels

As noted above, the VB system develops through posterior paired longitudinal arteries that coalesce rostrally to form the basilar artery (BA), while inferiorly they remain separate as VAs. Rostrally, this system is supplied through collaterals of which only the PCoA remains in most adults. Primitive anastomoses include the trigeminal artery, which remains as a branch to Meckel's cave; the otic artery, as the labyrinthine artery; the hypoglossal artery, as an artery to the hypoglossal canal; and the proatlantal artery, as the occipital artery and its connections to the VA over the first cervical vertebra and separately at the second cervical vertebra, through segmental vertebral branches. Although regressed, these connections may remain viable and become prominent under conditions of increased flow. Rarely, they remain as principal supply to the posterior circulation with regression of the more proximal

The occipital artery routinely has a prominent connection to the VA as it emerges from the C1 transverse foramen. Embolization of dural arteriovenous fistulas (DAVFs), particularly those involving the transverse sinuses at the transverse sigmoid junction or torcula, can have enlarged occipital feeders; and care must be exercised to ensure that no inadvertent posterior circulation embolization occurs. In other situations, this route may be used to treat

intracranial lesions, such as acute occlusions,33 or other pathologic conditions.

the occipital artery (E) are a major supply to the DAVF (F).

carries potential for lower cranial nerve dysfunction.

**3.3 Vertebrobasilar anastomoses** 

VB system.18,24,27

The neuromeningeal trunk of the ascending pharyngeal artery anastomoses with the VA, through connections at C3 through muscular collaterals, and more rostrally, as the remnant of the primitive hypoglossal artery with the odontoid arch vascular system.11,19

More caudally, the cervical branches of the subclavian artery anastomose with proximal sections of the VAs (C3-7). The ascending cervical artery arises from the thyrocervical trunk, while the deep cervical artery arises from the costocervical trunk. Both these branches form connections with the segmental vertebral branches through muscular collaterals. They are commonly noted to reconstitute the distal VA after proximal occlusion.

#### **3.4 Extracranial to intracranial collateralization and complication avoidance in neurointervention procedures**

First and foremost, one needs to be aware of the potential for collateral anastomotic channels. Such knowledge facilitates angiographic visualization. Even if the initial proximal external carotid or subclavian angiograms do not result in the visualization of these collaterals, we recommend that selective microcatheter angiograms be performed in as distal a position as is reasonably attainable immediately prior to embolization. These higher pressure selective injections are more likely to reveal these putative connections. If there is no visualization, a second element to further bolster confidence is to perform a Wada test with sodium amytal (75 mg) and lidocaine (30 mg) intraarterially through the microcatheter from the position planned for embolization and then immediately after injection to test for loss of appropriate neural function including that of the cranial nerves. Thirdly, if embolization is desired, polyvinyl alcohol particles, which considerably exceed the size (150 microns or greater) of most of these non-angiographically visualized collaterals (50-80 microns), should be used. Liquid embolics, such as glue (N-butyl cyanoacrylate; Trufill, Codman Neurovascular, Raynham, MA) and Onyx (EV3, Irvine, California), provide superior visualization; however, they are not discriminatory with respect to vessel size and, therefore, their use may be associated with a higher likelihood of collateral vessel occlusion. Angiographic visualization does not preclude embolization. One may attempt to attain distal purchase beyond the collateral communication and pay great attention to reflux during the embolization procedure. If such positioning is not attainable, pre-embolization occlusion of the collateral channel is another strategy. Typically, coil embolization of the collateral channel will not result in ischemic injury because of the multiple sources of vascular supply at the skull base; however, subsequent embolization of the intended vessel will prevent inadvertent passage of embolic materials through the occluded vessel to critical neural structures.

#### **4. Intracranial anastomoses**

In contrast to the extracranial-to-intracranial collateral anastomoses described above, which may be less obvious on non-superselective angiography, many of the ICA-to-ICA or ICA-to-VB anastomoses are rather easily identified and commonly seen. These common known collateral anastomoses as parts of the circle of Willis include the following: 1) anterior communicating artery (ACoA) connecting bilateral anterior cerebral arteries (ACAs); and 2) PCoA connecting the ipsilateral ICA to the posterior cerebral artery (PCA). Less obvious anastomoses occur among the various terminal cortical branches from each of the major vascular territories. The middle cerebral artery (MCA) branches anastomose with branches

Intracranial Arterial Collateralization: Relevance in Neuro-Endovascular Procedures 189

Fig. 11. A 40-year-old man presented with amaurosis fugax in the right eye. An imaging study confirmed a partially thrombosed giant aneurysm of the right ICA cavernous segment that likely had caused the embolic event. (A) T1-weighted magnetic resonance image reveals a partially thrombosed cavernous aneurysm (*arrow*). (B and C) Angiography shows the fusiform aneurysm with serpentine channel (*arrow*). (D) Right ICA TBO test with angiogram from left ICA reveals robust cross-filling of the contralateral circulation. The ACoA serves to opacify the right ACA and MCA without delay. (E) The patient tolerated TBO and was

revealed or opacified during angiography only after proximal vessel test occlusion. We typically perform a superselective micro-balloon test occlusion of the proximal vessel (as distal as possible remaining proximal to the aneurysm). Under micro-vessel occlusion we perform proximal angiograms as well as concurrent neurophysiologic testing to demonstrate angiographic and functional collateralization. If the patient tolerates the test occlusion, we then proceed immediately with endovascular embolization permanent occlusion of the tested vessel distal to the test site (Figure 13). If the patient does not tolerate test occlusion, one then has to weigh the risks of vessel-preserving strategies through microsurgical or endovascular means versus the expected neurologic deficit of vessel deconstruction. Obviously, microsurgical bypass anastomosis prior to artery sacrifice is one well-established treatment strategy. It should be noted that Hallacq et al.12 reported a series of 10 cases of P2 PCA aneurysms treated with occlusion of the aneurysm and parent vessel without balloon test occlusion in which no postocclusion occipital lobe ischemia occurred.

successfully treated with right ICA sacrifice.

of the PCA and ACA. The pericallosal branches of the ACA connect to splenial branches of PCA. Distal branches of the superior cerebellar artery (SCA) connect to branches from posterior inferior cerebellar artery (PICA), or to branches from anterior inferior cerebellar artery (AICA). Branches of AICA could also have connection with PICA. These anastomoses not only provide collaterals to preserve potentially affected brain tissue in the case of an occlusion event but also provide crucial collateral supply in the situation if carotid artery or VA sacrifice becomes necessary; also, potentially, the collaterals may be utilized as alternative access routes to the target during interventional procedures. Typically, these distal branch anastomoses are not visible with standard angiogram runs. In order to delineate the present of the anastomoses, a superselective balloon test occlusion is often required.

#### **4.1 Intracranial collateralization in neurointerventional procedures 4.1.1 Flow replacement by collateral vessels**

#### *Intracranial large artery sacrifice*

In patients with fusiform or giant aneurysms of the cavernous or supraclinoidal segment of the carotid artery or supraclinoidal carotid artery dissection with hemorrhage, sacrifice of the ipsilateral ICA can be a simple therapeutic solution with low risk if the ACoA and PCoA provide sufficient cross filling to the affected side. This is especially true if both angiographic and neurophysiologic tests are completed during a temporary balloon occlusion (TBO) test6,28,31 (Figure 11). It should be noted that endovascular strategies for vessel preservation during treatment continue to gradually erode options for vessel sacrifice, e.g., flow diversion technique, (Pipeline stent by EV3) in treating carotid artery giant aneurysms, which previously required carotid sacrifice.

Sacrifice of the VA is an effective strategy for the management of pathologic conditions of the VA, such as dissection with hemorrhage or endovascularly unmanageable aneurysms, simply because most patients are endowed with two vessels; and, after the sacrifice of one, unabated flow typically continues through the other. It is, however, important that the TBO test be performed before a vessel deconstruction procedure is carried out (Figure 12). There are other more complex situations involving the distal VAs, their junction, or the BA in which neither VA can be preserved, so flow reversal is desired. These situations include dissections with hemorrhage and complex, enlarging, symptomatic, or ruptured fusiform aneurysms**.**2,20 The presence of a robust PCoA and a large-caliber ipsilateral PCA P1 segment may allow sacrifice of both VAs, thereby creating flow reversal with a diminution of flow, enough to reduce hemodynamic stresses on the diseased vessel and allowing it to heal. It should be borne in mind that, before such deconstruction, which is undoubtedly high risk, a comprehensive angiographic evaluation, including a VA angiogram with transient bilateral manual carotid artery compression, could be very useful to identify bilateral PCoA. Further hemodynamic and neurophysiologic testing should be completed prior to vessel deconstruction.

#### *Intracranial distal end artery sacrifice*

Occasionally, one may encounter dissecting, mycotic, or ruptured broad-based aneurysms involving the distal ACA, MCA or PCA and considered higher risk for surgical or endovascular reconstruction. Because of well-developed cortical collaterals from ipsilateral ACA to PCA or MCA to PCA or ACA to MCA territories, these collaterals typically are

of the PCA and ACA. The pericallosal branches of the ACA connect to splenial branches of PCA. Distal branches of the superior cerebellar artery (SCA) connect to branches from posterior inferior cerebellar artery (PICA), or to branches from anterior inferior cerebellar artery (AICA). Branches of AICA could also have connection with PICA. These anastomoses not only provide collaterals to preserve potentially affected brain tissue in the case of an occlusion event but also provide crucial collateral supply in the situation if carotid artery or VA sacrifice becomes necessary; also, potentially, the collaterals may be utilized as alternative access routes to the target during interventional procedures. Typically, these distal branch anastomoses are not visible with standard angiogram runs. In order to delineate the present of the anastomoses, a superselective balloon test occlusion is often

In patients with fusiform or giant aneurysms of the cavernous or supraclinoidal segment of the carotid artery or supraclinoidal carotid artery dissection with hemorrhage, sacrifice of the ipsilateral ICA can be a simple therapeutic solution with low risk if the ACoA and PCoA provide sufficient cross filling to the affected side. This is especially true if both angiographic and neurophysiologic tests are completed during a temporary balloon occlusion (TBO) test6,28,31 (Figure 11). It should be noted that endovascular strategies for vessel preservation during treatment continue to gradually erode options for vessel sacrifice, e.g., flow diversion technique, (Pipeline stent by EV3) in treating carotid artery

Sacrifice of the VA is an effective strategy for the management of pathologic conditions of the VA, such as dissection with hemorrhage or endovascularly unmanageable aneurysms, simply because most patients are endowed with two vessels; and, after the sacrifice of one, unabated flow typically continues through the other. It is, however, important that the TBO test be performed before a vessel deconstruction procedure is carried out (Figure 12). There are other more complex situations involving the distal VAs, their junction, or the BA in which neither VA can be preserved, so flow reversal is desired. These situations include dissections with hemorrhage and complex, enlarging, symptomatic, or ruptured fusiform aneurysms**.**2,20 The presence of a robust PCoA and a large-caliber ipsilateral PCA P1 segment may allow sacrifice of both VAs, thereby creating flow reversal with a diminution of flow, enough to reduce hemodynamic stresses on the diseased vessel and allowing it to heal. It should be borne in mind that, before such deconstruction, which is undoubtedly high risk, a comprehensive angiographic evaluation, including a VA angiogram with transient bilateral manual carotid artery compression, could be very useful to identify bilateral PCoA. Further hemodynamic and neurophysiologic testing should be completed prior to vessel

Occasionally, one may encounter dissecting, mycotic, or ruptured broad-based aneurysms involving the distal ACA, MCA or PCA and considered higher risk for surgical or endovascular reconstruction. Because of well-developed cortical collaterals from ipsilateral ACA to PCA or MCA to PCA or ACA to MCA territories, these collaterals typically are

**4.1 Intracranial collateralization in neurointerventional procedures** 

giant aneurysms, which previously required carotid sacrifice.

**4.1.1 Flow replacement by collateral vessels** 

*Intracranial large artery sacrifice* 

required.

deconstruction.

*Intracranial distal end artery sacrifice* 

Fig. 11. A 40-year-old man presented with amaurosis fugax in the right eye. An imaging study confirmed a partially thrombosed giant aneurysm of the right ICA cavernous segment that likely had caused the embolic event. (A) T1-weighted magnetic resonance image reveals a partially thrombosed cavernous aneurysm (*arrow*). (B and C) Angiography shows the fusiform aneurysm with serpentine channel (*arrow*). (D) Right ICA TBO test with angiogram from left ICA reveals robust cross-filling of the contralateral circulation. The ACoA serves to opacify the right ACA and MCA without delay. (E) The patient tolerated TBO and was successfully treated with right ICA sacrifice.

revealed or opacified during angiography only after proximal vessel test occlusion. We typically perform a superselective micro-balloon test occlusion of the proximal vessel (as distal as possible remaining proximal to the aneurysm). Under micro-vessel occlusion we perform proximal angiograms as well as concurrent neurophysiologic testing to demonstrate angiographic and functional collateralization. If the patient tolerates the test occlusion, we then proceed immediately with endovascular embolization permanent occlusion of the tested vessel distal to the test site (Figure 13). If the patient does not tolerate test occlusion, one then has to weigh the risks of vessel-preserving strategies through microsurgical or endovascular means versus the expected neurologic deficit of vessel deconstruction. Obviously, microsurgical bypass anastomosis prior to artery sacrifice is one well-established treatment strategy. It should be noted that Hallacq et al.12 reported a series of 10 cases of P2 PCA aneurysms treated with occlusion of the aneurysm and parent vessel without balloon test occlusion in which no postocclusion occipital lobe ischemia occurred.

Intracranial Arterial Collateralization: Relevance in Neuro-Endovascular Procedures 191

Fig. 13. A 48-year-old woman with a subarachnoid hemorrhage due to a left P2–P3 junction ruptured aneurysm. (A and B) Lateral view and anteroposterior (AP) view of original VA angiogram (*arrow in B*). (C and D) Left ICA AP and lateral angiography. (E and F) Left PCA P2 TBO. The left ICA angiogram, while the left P2 was occluded with a balloon, revealed left ACA to PCA cortical collateralization (*black arrow*) with retrograde opacification during the late arterial phase. In F, *open arrow* indicates the balloon; *arrowhead* indicates the retrograde

A sharp reversely angulated origin of a vessel makes superselective ipsilateral catheterization difficult. For instance, access to the PICA or anterior inferior cerebellar artery (AICA) from the VA can be occasionally difficult, or in cases in which the carotid or bilateral VAs are occluded, the PCoA offers a distinct advantage. In these situations, if the caliber of the PCoA is adequate, effective catheterization of the desired vessel can be achieved (Figures 14 and 15). Naturally, a microcatheter can also go from one VA to the other through the VB junction (Figure 12, 16).7 Similarly, during treatment of broad-based aneurysms at the basilar or ICA terminus, ipsilateral placement of a stent may be inadequate for complete coverage of the aneurysm neck, necessitating a Y-configuration with increased risk of thromboembolic complications. In these cases, the following strategies offer distinct advantages: access from the contralateral carotid artery to pass a stent across the AcoA so

partially opacified P2-P3 aneurysm. (G and H) Ultimately, this aneurysm was coil embolized completely with balloon-remodeling technique; and the distal PCA branches

were preserved anterogradely.

Similar patterns of distal arterial collateralization can often be expected in PICA, AICA and SCA circulations. In cases of PICA ruptured dissections or dissecting aneurysms, proximal PICA can be occluded without needs of microsurgical bypass anastomosis. (Figure 21).

Fig. 12. A 38-year-old man with a left PCA territory embolic infarct was found to have a traumatic giant left VA dissecting aneurysm and DAVF from a fall 2 years prior to treatment. (A and B) Three-dimensional and two-dimensional angiograms show a giant left VA dissecting aneurysm and a DAVF. (C) The right VA angiogram demonstrates competent flow in the right VA. (D and E) Due to extremely high flow in the giant aneurysm, the DAVF was unable to be catheterized until occlusion of the left VA at the origin of the aneurysm. The left traumatic vertebral DAVF was catheterized from the right VA through the VB junction to the left VA. The *black arrow* indicates the fistula. *Open arrows* indicate the microcatheter route. (F) The fistula and residual filling of the giant aneurysm were treated successfully with coil occlusion through the contralateral VA to the left vertebral DAVF and giant aneurysm.
