Segmental identity and vulnerability in cerebral arteries

Abstract

Clinical experience shows that certain diseases involve specific areas of the vascular tree and remarkably spare others. Topographic differences in the vascular environment already suggest a regional specificity of the vascular anatomy. The biological grounds of such regional differences, although unknown, can account for the specificity of biological responses to stimuli. Such segmental specificities are beyond morphological analysis. They create an invisible discontinuity in an apparently homogenous anatomical, histological and haemodynamic system.We call this property segmental identity and thus vulnerability. Most of this identity is established during development and is preserved throughout life; its expression, however,may vary over time according to various stresses and create various clinical phenotypes. The memory of the evolutionary steps and their chronology is imprinted on the arterial anatomy and thus potentially readable. One can postulate that since the age of each arterial segment is different, its resistance to time and stimuli is most likely variable. The vulnerability of these segments cannot be permanent both in a qualitative and quantitative way. Some genetic functions only seem to be active during a short period of time: during vasculogenesis for example. Therefore either the trigger is always active and the target vulnerability window of the cells time-limited, or the target is permanently exposed and the trigger agent can either be exogenous and rare, or most of the time inactive or inactivated.

Figure 1

A, B) Moya-Moya disease in a young child involving the anterior division of the internal carotid artery bilaterally; note the typical aspect of the lenticulostriate network, as well as the transdural angiogenesis remote from the site of the occlusions. C, D) Bilateral occlusion of the anterior division of the internal carotid artery in a young child presenting with repeated deep-seated strokes. Note the absence of lenticulostriate involvement in response to the occlusive stress; there is no transdural supply demonstrated.

Figure 2

Young child presenting left sided white matter stroke 9 months after chickenpox infection. The lesion involves the anterior division of the internal carotid artery distal to the posterior communicating artery and is spontaneously repaired over 14 months.

Figure 3

Overall schematic view of the cranial arteries. (1) Ventral aorta VA; (2) Dorsal aorta DA; (3) First aortic arch 1AA; (4) Second aortic arch 2AA; (5) Third aortic arch 3AA; (6) Hypoglossal artery HA; (7) Pro-atlantal artery, type I PA 1; (8) Pro-atlantal artery, type II PA 2; (9) Third cervical segmental artery; (10) Longitudinal neural arteries LNA; (11) Para-ventral (lateral) neural artery; (12) Basilar artery (fused ventral arteries) BA; (13) Trigeminal artery Trig.A; (14) Primitive maxillary artery PMA; (15) Dorsal ophthalmic artery DOPHA; (16) Ventral ophthalmic artery VOPHA; (17) Middle cerebral artery MCA; (18) Anterior cerebral artery ACA; (19) Internal carotid posterior (caudal) division ICA Cd; (20) Anterior choroidal artery. AChA

Figure 4

Internal carotid artery embryology: early stage. PA: proatlantal artery - HA: hypoglossal artery - VA: ventral aorta - DA: dorsal aorta - 1 AA: first aortic arch - 2AA: second aortic arch - 3AA: third aortic arch.

Figure 5

A) Intra cranial segments (4 to 7) successively extending between the mandibular (not seen) and the trigeminal-primitive maxillary arteries, the dorsal ophthalmic artery, the ventral ophthalmic artery and the bifurcation. B) internal carotid angiography with the 5th cranial segments arterial boundaries visible: Mandibular artery MA, trigeminal remnant TR, Infero lateral trunk ILT, ophthalmic artery OPH.

Figure 6

Internal carotid artery segments derived from figure 3. Note that each segment lies between the origin of an embryonic vessel; these embryonic arteries determine precisely the segment boundaries.

Figure 7

Projection of the embryologic segment of the internal carotid artery on its final disposition: 1: cervical - 2: ascending intrapetrous - 3: horizontal intrapetrous - 4: ascending foramen lacerum - 5: horizontal intra-cavernous- 6: clinoid - 7: termination. Note that the first cervical segment starts above the carotid glomus.

Figure 8

Common carotid injection in a nine year old child presenting with a cervical pulsatile mass. Note the dysplastic change involving the cervical internal carotid artery and its extension from above the carotid glomus to reach the skull base. The rest of the internal carotid system is normal. This lesion involves the first segment of the internal carotid artery (3rd aortic arch). Courtesy of P. Chewit.

Figure 9

The vertebral artery injection demonstrates a dolichodistal basilar artery above the origin of the trigeminal artery remnant. Note the intradural duplication of the left vertebral artery. (Courtesy of T. Hyogo).

Figure 10

Dolicho siphon of the internal carotid involving the segment leaning between the trigeminal remnant and the dorsal ophthalmic artery remnant (5th segment).

Figure 11

The internal carotid artery presents a dolicho segment in its distal portion. The segment involved lies between the ophthalmic artery and the posterior communicating artery. It corresponds to the last segment of the carotid (7th segment). Courtesy of C. Campos.

Figure 12

Dolicho segment of the A1 portion of the right anterior cerebral artery.

Figure 13

Dolicho segment of the clinoid internal carotid artery extending to its most distal portion (6th and 7th segments). The anomalous segment has opposed to the proper migration of the dorsal ophthalmic artery. The supply to the entire orbital contents arises from the accessory meningeal artery.

Figure 14

Four vessel angiogram demonstrating a rete mirabile type of network compensating for segmental agenesis of epidural segments of the internal carotid and vertebral arteries bilaterally. (Courtesy of T. Hyogo. Published in Neuroradiology 38: 433-436,1996). A, B) On the right side the absence of the portion proximal to the inferolateral trunk promotes reconstitution of the distal siphon through the maxillary artery cavernous branches. C) On the left side the clinoid portion of the carotid is absent, distal to the inferolateral trunk; reconstitution of the siphon bridges the segmental agenesis through the orbit with the deep recurrent ophthalmic artery and retrogradely into the supracavernous ophthalmic artery. D, E, F, G) The vertebral arteries, collateralisation uses the lateral spinal artery channels on the left and a local epidural network on the right.

Figure 15

The disposition illustrated in figure 14 points to the environmental characteristics of both trans dural portions of the internal carotid and vertebral arteries as illustrated by K. Arnautovic (reproduced from J Neurosurg 86: 252-262,1997; with permission).

Figure 16

Fifteen month old infant girl, who presented three epileptic events, with a left sided brachial paresis following the last episode. The three types of vascular growth are expressed in this case: dolicho Al artery segment, internal carotid artery anterior division fusiform aneurysm, Ml (centrifugal) occlusion without evidence of distal embolic obstruction. (Courtesy of R. Piske and C. Campos).