Three-dimensional stereotactic atlas of the extracranial vasculature correlated with the intracranial vasculature, cranial nerves, skull and muscles

Abstract

Our objective was to construct a 3D, interactive, and reference atlas of the extracranial vasculature spatially correlated with the intracranial blood vessels, cranial nerves, skull, glands, and head muscles.

The atlas has been constructed from multiple 3T and 7T magnetic resonance angiogram (MRA) brain scans, and 3T phase contrast and inflow MRA neck scans of the same specimen in the following steps: vessel extraction from the scans, building 3D tubular models of the vessels, spatial registration of the extra- and intracranial vessels, vessel editing, vessel naming and color-coding, vessel simplification, and atlas validation.

This new atlas contains 48 names of the extracranial vessels (25 arterial and 23 venous) and it has been integrated with the existing brain atlas.

The atlas is valuable for medical students and residents to easily get familiarized with the extracranial vasculature with a few clicks; is useful for educators to prepare teaching materials; and potentially can serve as a reference in the diagnosis of vascular disease and treatment, including craniomaxillofacial surgeries and radiologic interventions of the face and neck.

Introduction

Knowledge of extracranial vasculature is vital in education, diagnosis of vascular disease, and treatment including craniomaxillofacial surgeries and radiologic interventions of facial arteriovenous malformations. To our best knowledge, a truly three-dimensional (3D), interactive, and reference atlas of the extracranial vasculature has not yet been created.

Our ultimate objective is to create a holistic atlas of the whole adult human brain along with some head and neck. We have constructed so far a 3D atlas from multiple 3 and 7 Tesla in vivo scans of a single brain specimen to ensure spatial consistency and extendibility. This atlas allows the user to create and explore any region of interest along with its surroundings just with a few clicks. The virtual model in the atlas contains structure,¹ intracranial vasculature,² white matter tracts,³ cranial nerves with nuclei,⁴ and head muscles and glands.⁵ Recently, a skull model has been added to the atlas constructed from a high-resolution computed tomography (CT) scan.⁶ The atlas has been placed in the Talairach stereotactic coordinate system⁷ with the origin in the center of the anterior commissure on the midsagittal plane.

The objective of this work is to construct a 3D, interactive, and reference atlas of the extracranial vasculature spatially correlated with the intracranial blood vessels, cranial nerves, skull, glands, and head muscles, and integrated with the existing atlas.

Materials and methods

The atlas was constructed in the following steps: magnetic resonance angiogram (MRA) scan acquisition, vessel extraction from the scans, building 3D tubular models of the vessels, spatial registration of the extra- and intracranial vessels, vessel editing, vessel naming and color-coding, integration of the vessels with the existing brain atlas, vessel simplification, and atlas validation.

Materials

Multiple 3T and 7T MRA brain scans of the same specimen were acquired earlier (to construct the intracranial vessels) and their parameters were specified by Nowinski et al.² They included 3D TOF, SWI, and SPGR pulse sequences. In addition, 3D phase contrast angiography (PCA) and M2D inflow MRA neck scans of the same specimen, ranging from the aortic arch to the circle of Willis, were acquired on a 3T Achieva scanner (Philips Medical Systems). The M2D sequence depicted the arteries and had the following parameters: matrix: 352 × 352 × 261, voxel size 0.568182 × 0.568182 × 1.0 mm³, and slice thickness 2.0 mm. The PCA sequence depicted mainly the veins and had the following parameters: matrix: 512 × 512 × 130, voxel size 0.390625 × 0.390625 × 2.0 mm³, and slice thickness 2.0 mm.

Methods

The vessels were interactively created from the MRA scans by means of a dedicated Vascular Editor developed in our lab⁸ and by importing the extracted models to the brain atlas editor¹ for further fine-tuning and integration with the existing brain atlas. The Vascular Editor provides functions for quick extraction of the vessels on the axial, coronal and sagittal planes; editing of an already extracted vessel on a plane orthogonal to its course; and building centerline and 3D polygonal tubular surface vascular models. The brain atlas is equipped with dedicated tools enabling precise editing of any imported components in the entire cerebral context, facilitated by atlas navigation.¹ By using these tools, the extracranial vessels were enhanced in terms of their smooth course and diameters, fitted to the existing structures, linked with the intracranial vessels, uniquely color-coded and labeled (named) based on Terminologia Anatomica.⁹ Moreover, the indices for the extracranial arteries and veins were created (see Appendix) and integrated with the atlas index.

The 3D extracranial vasculature extracted from the brain scans is naturally in register with the 3D intracranial vasculature obtained from the same scans. The part of the 3D vascular model extracted from the neck scans was registered manually with the existing intracranial vasculature by performing three rotations and three translations to align the corresponding vessels existing in both 3D models for the arterial system (including the circle of Willis, basilar artery, vertebral arteries, and the upper parts of the internal carotid arteries) and the venous system (containing the lower part of the superior sagittal sinus, transverse sinuses, sigmoid sinuses, and the upper parts of the internal jugular veins).

The extracranial vessels were placed in the Talairach stereotactic coordinate system⁷ and the readout of distances and stereotactic coordinates (posterior–anterior, inferior–superior, and right–left) was provided.

Atlas validation (against both textual description and images) was done in terms of vascular parcellation, origin, course, branching, diameter, and surrounding structures based on Gray's Anatomy (37^th, 38^th and 40^th eds)^10–12 and other materials including textbooks.^13–19

Results

The extracranial arteries and veins were created and integrated with the currently developed atlas. Figure 1 presents separately the extracranial arteries and veins. All the extra- and intracranial vessels together are shown in Figure 2. The extracranial vessels along with the skull, cranial nerves and muscles are illustrated in Figure 3.

Figure 1.

Extracranial vasculature: a) arteries (anterior and left lateral views); b) veins (anterior and left lateral views). The orientation box in the top-left corner of each view provides the viewing direction (S – superior, I – inferior, A – anterior, P – posterior, L – left, and R – right).

Figure 2.

Extra- and intracranial vessels together (anterior and right lateral views).

Figure 3.

Extracranial vessels along with: a) skull; b) cranial nerves; and c) head muscles.

Discussion

The goal of this work was to create and validate a 3D, realistic, reference and interactive atlas of the extracranial vessels. To our best knowledge, this kind of atlas does not yet exist.

The atlas has several advantages both exploration- and application-wise. Exploration-wise, it shares the advantages with the already created atlas,¹ including continuous navigation in a 3D space, structure labeling and highlighting, assembly/disassembly of any 3D scene with a few clicks, image capturing, and getting distances and stereotactic coordinates. Application-wise, the extracranial vessels can be correlated with the surrounding brain, head, and neck structures, making it useful for students learning the course of the vessels, anatomical correlations, and blood supply and venous drainage of the craniofacial musculature. The atlas may be helpful to study fundamentals of craniofacial, oral, maxillofacial, and reconstructive surgeries as well as common surgical procedures of the face, head, and neck. The course of the vessels can be related to bony and other landmarks so that it will be beneficial for imaging routines including Doppler studies as well as vasospasm treatment, venous cannulation, and interventional radiology procedures of the extracranial vessels, such as treatment of facial arteriovenous malformations and carotid stenting/angioplasty.

Several works address head and neck atlases which include the extracranial vasculature. The Voxel-Man 3D Navigator: Brain and Skull²⁰ has 36 QuickTime movies and, consequently, structures cannot be freely selected or deselected for display and exploration. It includes a few, only major, extracranial vessels, such as the facial, superficial temporal and occipital arteries. Primal’s Interactive Head and Neck²¹ comprises images and animations derived from scans. The content can be dissected layer-by-layer. It contains many small vessels, for instance, some venous plexuses not included into our atlas. However, the structures are divided into predefined subcategories and the user is not able to select or deselect vessels. The content is basically 2D and a smooth atlas exploration is limited. Functions for measuring vessel diameters and distances between structures are not available. A.D.A.M. Interactive Anatomy²² contains images created by medical illustrators. The content is also dissectible layer-by-layer. This atlas has a limited number of vessels and is not stereotactic. In contrast to all these atlases, our atlas is truly 3D, smoothly explorable, dissectible at a level of individual components, stereotactic, user friendly, and provides vessel diameters at any location.

Atlas validation was done based on Gray's Anatomy^10–12 and other materials.^{13–19,23–47} Below we discuss the content and features as present in the created atlas against the state of the art. The right common carotid artery originates from the right brachiocephalic artery and the left common carotid artery from the aortic arch whose diameter is 2.5–3.5 cm,²³ taken 2.8 cm in our atlas. The common carotid artery divides into the external carotid artery (ECA) and the internal carotid artery at the level of the cervical vertebrae C4 on the left and right sides in the atlas (with the incident rates of bifurcation of 35% (C4) and 12% (C3 and C5)).¹⁵ The internal carotid artery was described earlier.² The ECA has eight branches (see Appendix) and the smallest branch, the ascending pharyngeal artery, is missing in the atlas. The facial artery originates from the ECA¹² and its diameter at origin is 2.7 mm.²⁴ It courses through the cheek, superficial to the buccinators.¹² The cervical branches of the facial artery are not included. Both the superior and inferior labial branches penetrate the orbicularis oris and run near the superior and inferior labial margins, respectively. The superior labial branch is larger (its diameter at origin is 1.3 mm)²⁵ than the inferior branch (the diameter at origin is 1.2 mm).²⁶ The lateral nasal artery is divided into two branches to supply the dorsum and alae of nose.¹² The occipital artery arises posteriorly from the ECA,¹² almost at the same level as the facial artery.²⁷ The angular artery originates at the medial canthal region;²⁸ its diameter is 0.77 mm.²⁹ In the atlas the posterior auricular artery arises from the ECA just above the occipital artery origin³⁰ (though it also may arise from the occipital artery);³¹ its average diameter is 0.8 mm³⁰ (in the atlas it is set 1.0 mm at origin and 0.6 mm at its end). The ECA has two terminal branches, a larger maxillary artery and a smaller superficial temporal artery. The superficial temporal artery originates in the parotid gland behind the mandible’s neck¹² and divides into a smaller frontal (anterior) and a larger parietal (posterior) branches; at bifurcation its diameter is 1.9 mm.³² The superficial temporal artery gives off the middle temporal artery just above the zygomatic arch.¹² The transverse facial artery runs forward over the masseter³³ in our atlas (it crosses the masseter according to Gray's Anatomy);¹² its diameter at origin is 1.45 mm ± 0.24 mm.³⁴ The maxillary artery arises behind the neck of the mandible¹² and is embedded in the parotid gland. Its first (mandibular) part travels horizontally, first posterior and then medial to the mandible.¹⁷ Its next (pterygoid) part ascends obliquely forwards medial to the temporalis.¹² The last (pterygopalatine) part passes between the upper and lower heads of the lateral pterygoid.¹⁷ Reported diameters of the maxillary artery are variable, including 2.1 ± 0.7 mm,³⁵ 4.08 ± 0.51 mm,³⁶ 3.2 mm;³⁷ this diameter was set 3.5 mm at origin in the atlas. Branches of the maxillary artery include the inferior alveolar artery, middle meningeal artery, and buccal artery;¹² the posterior superior alveolar, infraorbital, sphenopalatine and greater palatine arteries branches are not included in the atlas. Reported diameters of the middle meningeal artery are 1.2 ± 0.2 mm³⁵ and 1.5 ± 0.26 mm³⁸, and 1.2 mm was taken at origin in the atlas. Reported diameters of the inferior alveolar artery are 0.6 ± 0.1 mm³⁵ and 1.23 mm (0.66–1.8 mm),³⁰ and 1.0 mm was set in the atlas. The buccal artery runs over the external surface of the buccinators,³⁹ and its diameter is 0.6 ± 0.2 mm.³⁵

The supratrochlear and supraorbital veins unite to form the angular vein near the angle of the eye.⁴⁰ The facial vein joins the anterior division of the retromandibular vein (just anteroinferior to the mandibular angle) and opens into the internal jugular vein.^12,40 The facial vein diameter is between 2.2–3.2 mm and the common facial vein is slightly larger at 2.4–3.5 mm,³³ taken 3.2 mm in the atlas. The superficial temporal vein (whose diameter is between 2.1–3.3 mm,⁴¹ taken 2.6 mm in the atlas) unites with the maxillary vein within the parotid gland to form the retromandibular vein.^12,42 The transverse facial vein joins the superficial temporal vein within the parotid gland.¹² The posterior auricular vein connects to the occipital vein and unites with the posterior division of the retromandibular vein to form the external jugular vein^42,43 as is in the atlas; generally, the occipital vein may pass to either the internal jugular, posterior auricular, deep cervical or vertebral veins.¹² The posterior auricular vein diameter is reported between 0.3–2.0 mm.⁴⁴ However, taking into account that this vein is a continuation of the external jugular vein, which has a highly variable diameter (between 0–16 mm)⁴⁵, the diameter of the posterior auricular vein was set to 3.2 mm in the atlas. The external jugular vein ends in the subclavian vein.¹² The right external jugular vein is larger in diameter (6.0 mm in the atlas) than the left one (5.5 mm in the atlas).⁴⁶ The vertebral and deep cervical veins are not present in our atlas because we have not included the suboccipital venous plexus due to its irregular pattern and incompleteness. The anterior jugular, lingual and occipital emissary veins are missing, but the mastoid emissary and condylar emissary veins are present.

Hence, this validation indicates that the constructed model of the extracranial vessels can be considered typical.

Although, to our best knowledge, this is the first 3D, reference, and stereotactic atlas of the extracranial vasculature, it has several limitations. One of them is certain incompleteness as indicated in the above validation, as some vessels were not visible, or not completely present. Note that the number of the intracranial vessels in our atlas is more than 1300; however, they have been obtained by employing multiple 3 and 7T acquisitions, while the 3T scans resulted only in about 350 vessels. We may expect that 7T head and neck acquisitions may increase the content of this atlas in the future. Some vessels are not subdivided into segments, such as the maxillary artery (having subdivision into the mandibular, pterygoid and pterygopalatine parts)¹² or the retromandibular vein (subdivided into the anterior and posterior divisions).⁴⁷ The vascular variants are not available as our objective was to construct a reference atlas. Based on this reference atlas, extracranial variants could be incorporated, as we have done earlier for intracranial arterial variants.⁴⁸

In summary, we have created a 3D reference and stereotactic atlas of the extracranial arteries and veins from in vivo MRA scans of the head and neck. This atlas is valuable for medical students and residents to easily get familiarized with extracranial vasculature with a few clicks. It is also useful for educators to prepare teaching materials. It may potentially serve as a reference in head and neck scan reading as well as performing craniomaxillofacial surgeries and radiologic interventions of facial arteriovenous malformations.

Appendix: List of the extracranial vessels

Extracranial arteries

Aortic arch

Brachiocephalic artery

Subclavian artery

Common carotid artery

Internal carotid artery, cervical part

External carotid artery

Superior thyroid artery

Lingual artery

Facial artery

Inferior labial branch

Superior labial branch

Lateral nasal branch

Angular artery

Occipital artery

Posterior auricular artery

Superficial temporal artery

Transverse facial artery

Superficial temporal artery, frontal branch

Superficial temporal artery, parietal branch

(Ext.) Middle temporal artery

Maxillary artery

Inferior alveolar artery

Middle meningeal artery

Buccal artery

Vertebral artery, extracranial part

Extracranial veins

Superior vena cava

Brachiocephalic vein

Subclavian vein

Internal jugular vein

Facial vein

Angular vein

Supratrochlear veins

Supraorbital vein

Superior labial vein

Inferior labial vein

Retromandibular vein

Maxillary vein

Superficial temporal veins

Superficial temporal veins, frontal branches

Superficial temporal veins, parietal branches

Transverse facial vein

Middle temporal vein

External jugular vein

Posterior auricular vein

(Ext.) Occipital vein

Emissary veins

Condylar emissary vein

Mastoid emissary vein

Funding

This research was funded by Agency for Science, Technology and Research (ASTAR), Singapore.

Conflict of interest

The authors declare no conflict of interest.