**2. Cranial vascular embryology**

The cranial vasculature begins with the development of a vascular supply to the paired pharyngeal arches. This supply develops as vascular arches that emanate from the ventral aortic sac connect with the paired dorsal aortae. Each pharyngeal arch gets its own vascular arch. These vascular arches then develop and regress in rostrocaudal fashion. The pharyngeal arches become apparent at approximately 3 to 4 weeks' gestation. The pharyngeal arches develop plexiform vascular channels that ultimately connect the ventral aortic sac with the paired dorsal aortae, forming the vascular arch. The first arch gives rise to

Intracranial Arterial Collateralization: Relevance in Neuro-Endovascular Procedures 177

The posterior circulation develops in parallel, first appearing towards the beginning of the fifth gestational week as paired dorsal longitudinal neural arteries. These eventually form the intracranial VA and BA. Further caudally, a plexiform network of the cervical intersegmental arteries anastomoses to form the paired vertebral arteries (VAs). As these channels continue to develop, they reliably develop anastomotic connections with the ICAs, forming the trigeminal, otic, hypoglossal, and proatlantal intersegmental connections (Figure 2). The seventh cervical intersegmental artery coalesces with the right fourth

Fig. 2. Three-dimensional sketch at approximately 5 gestational weeks. Development of the paired plexiform longitudinal neural arteries (*solid black arrows*). The VAs (*open arrows*) form

as longitudinal anastomoses between the seven cervical intersegmental arteries. The proximal connections between the C1-6 arteries and the dorsal aorta (DA) are regressing. For simplification, only one set of longitudinal neural and cervical intersegmental arteries is shown. These vessels are the precursors of the VB circulation. Initially, the longitudinal neural arteries are supplied from below via the intersegmental arteries. At this stage, several temporary connections between the developing VB circulation and the carotid arteries also form. From cephalad to caudad, these arteries are the trigeminal (T), otic (O), hypoglossal (H), and proatlantal intersegmental arteries (P) (this vessel forms slightly later). These transient anastomoses regress as the caudal divisions of the primitive internal carotid arteries (ICAs) anastomose with the cranial ends of the longitudinal neural arteries and form the future posterior communicating arteries (*dotted lines with curved arrows*). Persistence of the transient embryonic interconnections is abnormal and results in a so-called primitive carotid–basilar anastomosis. Sprouting of the external carotid arteries (ECAs) from the proximal common carotid arteries (CCAs) is also depicted. These vessels will annex first and second arch remnants (*solid black areas*). VA, ventral aorta. *Permission requested from Osborn AG: Diagnostic Cerebral Angiography (2nd ed). Philadelphia: Lippincott Williams & Wilkins,* 

*Wolters Kluwer, 1999, figure 1-2A, page 8.* 

the primitive stapedial artery, whereas the second gives rise to the hyoid artery. These arches then regress and coalesce to form the primitive hyoidostapedial artery. These vessels are critical to the vascular development of the skull base. This primitive branch follows the three divisions of the trigeminal nerve such that one trunk that develops along the mandibular division becomes the adult internal maxillary artery; the superior trunk becomes the middle meningeal artery and contributes to the ophthalmic artery. The primitive maxillary artery develops as the meningohypophyseal trunk, whereas the third division becomes the corticotympanic branch, which communicates with the ICA in the petrous canal (Figure 1). An embryologic dorsal ophthalmic artery regresses to become the inferolateral trunk, rarely staying on as a cavernous origin to the adult ophthalmic artery.9 The third vascular arch on either side becomes the cervical ICA, eventually incorporating parts of the dorsal aortae bilaterally to form more cranial sections up the posterior communicating artery (PCoA) segment. From the third arch sprouts the external carotid artery (ECA) trunk, which anastomoses with the primitive hyoidostapedial artery branches to complete the ECA circuitry. Additionally, a pair of plexiform networks, called the ventral pharyngeal arteries, develop early on and connect to the hyoidostapedial trunk. These ventral–pharyngeal networks form prior to the development of the ECA trunk, eventually mostly regressing, but retaining parts that allow for anastomoses between the ascending pharyngeal and caroticotympanic arteries.

Fig. 1. Anatomic diagram turned from anteroposterior to a left anterior oblique (LAO) position depicts the definitive left common carotid artery (CCA) as well as the external carotid artery (ECA) and internal carotid artery (ICA). The embryonic origin of these vessels is also shown. CTA, caroticotympanic artery; small single arrow, stapes; (*arrowhead*), foramen spinosum; (*double arrows*), optic canal; (*open arrows*), carotid canal. Distal ramifications from the internal maxillary artery (IMA), middle meningeal artery (MMA), and orbital branches of the ophthalmic artery (OA) are indicated by the dotted lines. Stapedial artery (STA). *Permission requested from Osborn AG: Diagnostic Cerebral Angiography (2nd ed). Philadelphia: Lippincott Williams & Wilkins, Wolters Kluwer, 1999, figure 2-5, page 35.*

the primitive stapedial artery, whereas the second gives rise to the hyoid artery. These arches then regress and coalesce to form the primitive hyoidostapedial artery. These vessels are critical to the vascular development of the skull base. This primitive branch follows the three divisions of the trigeminal nerve such that one trunk that develops along the mandibular division becomes the adult internal maxillary artery; the superior trunk becomes the middle meningeal artery and contributes to the ophthalmic artery. The primitive maxillary artery develops as the meningohypophyseal trunk, whereas the third division becomes the corticotympanic branch, which communicates with the ICA in the petrous canal (Figure 1). An embryologic dorsal ophthalmic artery regresses to become the inferolateral trunk, rarely staying on as a cavernous origin to the adult ophthalmic artery.9 The third vascular arch on either side becomes the cervical ICA, eventually incorporating parts of the dorsal aortae bilaterally to form more cranial sections up the posterior communicating artery (PCoA) segment. From the third arch sprouts the external carotid artery (ECA) trunk, which anastomoses with the primitive hyoidostapedial artery branches to complete the ECA circuitry. Additionally, a pair of plexiform networks, called the ventral pharyngeal arteries, develop early on and connect to the hyoidostapedial trunk. These ventral–pharyngeal networks form prior to the development of the ECA trunk, eventually mostly regressing, but retaining parts that allow for anastomoses between the ascending

Fig. 1. Anatomic diagram turned from anteroposterior to a left anterior oblique (LAO) position depicts the definitive left common carotid artery (CCA) as well as the external carotid artery (ECA) and internal carotid artery (ICA). The embryonic origin of these vessels

is also shown. CTA, caroticotympanic artery; small single arrow, stapes; (*arrowhead*), foramen spinosum; (*double arrows*), optic canal; (*open arrows*), carotid canal. Distal

ramifications from the internal maxillary artery (IMA), middle meningeal artery (MMA), and orbital branches of the ophthalmic artery (OA) are indicated by the dotted lines. Stapedial artery (STA). *Permission requested from Osborn AG: Diagnostic Cerebral Angiography (2nd ed). Philadelphia: Lippincott Williams & Wilkins, Wolters Kluwer, 1999, figure 2-5, page 35.*

pharyngeal and caroticotympanic arteries.

The posterior circulation develops in parallel, first appearing towards the beginning of the fifth gestational week as paired dorsal longitudinal neural arteries. These eventually form the intracranial VA and BA. Further caudally, a plexiform network of the cervical intersegmental arteries anastomoses to form the paired vertebral arteries (VAs). As these channels continue to develop, they reliably develop anastomotic connections with the ICAs, forming the trigeminal, otic, hypoglossal, and proatlantal intersegmental connections (Figure 2). The seventh cervical intersegmental artery coalesces with the right fourth

Fig. 2. Three-dimensional sketch at approximately 5 gestational weeks. Development of the paired plexiform longitudinal neural arteries (*solid black arrows*). The VAs (*open arrows*) form as longitudinal anastomoses between the seven cervical intersegmental arteries. The proximal connections between the C1-6 arteries and the dorsal aorta (DA) are regressing. For simplification, only one set of longitudinal neural and cervical intersegmental arteries is shown. These vessels are the precursors of the VB circulation. Initially, the longitudinal neural arteries are supplied from below via the intersegmental arteries. At this stage, several temporary connections between the developing VB circulation and the carotid arteries also form. From cephalad to caudad, these arteries are the trigeminal (T), otic (O), hypoglossal (H), and proatlantal intersegmental arteries (P) (this vessel forms slightly later). These transient anastomoses regress as the caudal divisions of the primitive internal carotid arteries (ICAs) anastomose with the cranial ends of the longitudinal neural arteries and form the future posterior communicating arteries (*dotted lines with curved arrows*). Persistence of the transient embryonic interconnections is abnormal and results in a so-called primitive carotid–basilar anastomosis. Sprouting of the external carotid arteries (ECAs) from the proximal common carotid arteries (CCAs) is also depicted. These vessels will annex first and second arch remnants (*solid black areas*). VA, ventral aorta. *Permission requested from Osborn AG: Diagnostic Cerebral Angiography (2nd ed). Philadelphia: Lippincott Williams & Wilkins, Wolters Kluwer, 1999, figure 1-2A, page 8.* 

Intracranial Arterial Collateralization: Relevance in Neuro-Endovascular Procedures 179

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

3. Posterior or VB connections with ascending pharyngeal, occipital, and subclavian artery

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

1. Anterior or ophthalmic artery connections with facial and internal maxillary arteries 2. Middle or petrocavernous ICA branches with internal maxillary and ascending

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

anastomotic connections are summarized in **Table 1**.

Table 1. Extracranial-to-Intracranial Anastomoses

pharyngeal branches

primitive vascular connections. They divided the regions as follows:

branches, especially the ascending and deep cervical arteries.

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.* 

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 been described by Larsen14 and Lasjaunias et al.15
