Cervical carotid and circle of willis arterial anatomy of macaque monkeys: a comparative anatomy study

Abstract

Macaque monkeys are used in many research applications, including cerebrovascular investigations. However, detailed catalogs of the relevant vascular anatomy are scarce. We present our experience with macaque vessel patterns as determined by digital subtraction angiography of 34 different monkeys. We retrospectively analyzed digital subtraction angiograms obtained during experimental internal carotid artery (ICA) catheterization and subsequent injection of 1-methyl 4-phenyl 1,2,3,6-tetrahydropyridine. Results were catalogued according to vascular distribution and variants observed. Macaque monkeys have a bovine aortic arch. The carotid vessels generally bifurcate, but are occasionally observed to divide into three vessels. The external carotid gives rise primarily to two trunks: an occipital branch and a common vessel that subsequently gives off the lingual, facial, and superior thyroid arteries. The internal maxillary artery may be present as a terminal branch of the external carotid or as a branch of the occipital artery. The ICA is similar in course to that of the human. The anterior circle of Willis was intact in all monkeys in our study. Its primary difference from that of the human is the union of the bilateral anterior cerebral arteries as a single (azygous) median vessel. Macaque cervical carotid and circle of Willis arterial anatomy differs from humans in a couple of specific patterns. Knowledge of these differences and similarities between human and macaque anatomy is important in developing endovascular macaque models of human diseases, such as ischemic stroke.

Fig. 1

The brachiocephalic trunk (1) injection in macaque monkeys appears to give rise to the left common carotid (2), right common carotid (3), and right subclavian (4) arteries. Three-dimensional reference view on right.

Fig. 2

(a) Reference view; (b) right carotid artery injection demonstrating the more typical scenario of the common carotid artery dividing into internal and external branches; (c) right carotid artery injection shows a carotid “trifurcation” configuration.

Fig. 3

(a) Three-dimensional reference image; (b, c) the internal maxillary artery and its branches; (d) a variant in which the occipital artery gives off the internal maxillary artery.

Fig. 4

(a,c) are reference views depicting the most commonly used projections for ideal visualization of the internal carotid artery; (b) demonstrates the course of the ICA and its branches, with the black arrow denoting the choroidal blush of the retinal vessels; (d) an anteroposterior view of the ICA and coincidentally imaged vessels; arrowheads denote the anterior and posterior ethmoidal arteries.

Fig. 5

The circle of Willis as seen from an inferior projection. Elements of the posterior and anterior circulation are well-visualized.

Fig. 6

The anterior cerebral artery in lateral (a) and AP (b) projections. The black arrow denotes the origin of the callosomarginal artery in each. Note the absence of an anterior communicating artery and azygous nature of the ACA in (b).

Fig. 7

(a) Reference view showing head position of the following two images; (b) and (c) represent early and late phase angiograms of the MCA, respectively. The arrowhead indicates the posterior communicating artery, and the black arrow the PCA. (d) An AP view demonstrating the course of the MCA.

Fig. 8

(a) Reference view depicting head positioning in the following images; (b) shows catheterization of the right vertebral artery (indicated by arrowhead), with contrast subsequently filling the anterior circulation; (c) shows a monkey in whom the vertebral artery (indicated by arrowhead) was seen as a background finding.