Introduction

Course of the vertebral artery and location of its branches may significantly differ from the classic type. For example, according to Argenson et al. [1] in 10.1 % of cases the vertebral artery enters the transversary foramina at levels other to C6. Yamazaki et al. [2] found the vertebral artery passing between the posterior arch of atlas and arch of axis in 8 % of patients operated for diseases of cranio-vertebral junction. In 2 % of these patients the vertebral artery formed a loop around the posterior arch of atlas.

Case report

In the material of 50 specimens of suboccipital region a case of unilateral atypical branching pattern of atlantic part of the vertebral artery was observed in the specimen from the body of a 62-year-old man who died after head trauma. All the specimens were collected during routine forensic autopsies, injected with coloured gelatine and fixed in formaldehyde solution. The vertebral arteries of the discussed specimen had diameter of 4.61 mm on the left and 4.50 mm on the right measured just behind the dura. Microsurgical dissection of the atlantic part of the left vertebral artery (V3) revealed following branches: two articular (with diameters of 0.52 and 0.42 mm), two muscular (with diameters 1.74 and 1.80 mm), posterior spinal artery of extradural origin (with diameter of 0.82 mm). Additionally, at the anterior edge of the bony groove on the posterior arch of atlas the vertebral artery gave of a large branch measuring 3.32 mm in diameter at this point. This branch coursed epiduraly downwards between the anterior and posterior roots of the first cervical nerve, then together with the second cervical nerve made a loop between the arches of the atlas and axis vertebrae and just posterior and lateral to the lateral atlanto-axial joint it anastomosed with the terminal segment of transversary part of the veretebral artery (V2) within the C1 transversary foramen having diameter of 2.86 mm (Fig. 1). The arterial segment passing between the arches of atlas and axis was giving off arterioles to the lateral atlanto-axial joint, a branch supplying the second spinal nerve (0.60 mm in diameter) and a muscular branch (1.24 mm in diameter). Otherwise the specimen showed usual anatomy of soft and bony structures.

Fig. 1
figure 1

Dissections of the discussed specimen. a Superior–posterior view: the posterior atlanto-occipital membrane (PAOM) and dura (D) were cut to visualise the vertebral artery—its atlantic (V3) segment continuous with the intradural one (V4). The inferior arm of the arterial ring (arrow) branches of the V3 and runs downwards epiduraly, anterior to the dorsal root and ganglion of the first cervical nerve (drgC1). The V3 gives of also deep and superficial muscular branches (dmb, smb) and posterior spinal artery (PSA). OCIM obliquus capitis inferior muscle, XI spinal root of the accessory nerve, dbC1 dorsal branch of the first cervical nerve (suboccipital nerve). b Anterior–inferior view. c Inferior view: course of the inferior arm of the discussed arterial ring is shown in relationship with the lateral atlanto-axial joint (J inferior articular surface of atlas and articular capsule are visible) and with the second cervical nerve (C2) and its anterior branch (abC2). vrC2 ventral roots of C2 nerve, mb muscular branch, V2 terminal part of the transversary segment of vertebral artery, ES epidural space

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Discussion

The loop of vertebral artery encircling the posterior arch of atlas vertebra was first described by Kadyi in 1888 [3] in his monograph on vascularisation of spinal cord and, earlier, by Herberg in 1845 as quoted by him. There is significant number of papers discussing fenestrations and duplications of the vertebral artery based on angiographic imaging examinations [4–9]. Lasjaunias [5, 10] basing on his experience with classic angiography in numerous anatomical variants and abnormalities and earlier embryological studies of Padget [11], proposed a schematic ‘grid’ model explaining embryology of normal and abnormal vertebro-basilar system. The transversary segment (V2) of vertebral artery originates from sequence of primitive anastomoses between the cervical intersegmental arteries, while the horizontal loop of atlantic segment (V3) of vertebral artery originates from the proatlantic intersegmental artery located between the skull and spine. If the first cervical intersegmental artery does not disappear during development, the vertebral artery runs between arches of the atlas and axis vertebrae. If both proatlantic and first cervical intersegmental arteries persist with their anastomoses, the ‘window’ within the vertebral artery develops, encircling the posterior arch of atlas, like in the case presented here. Lasjaunias [5] differentiated the true fenestration, which is a local split of vascular lumen, from the duplication, where vessels have different course before they fuse again. Like in our case, arms of local duplication have origin in different embryonic vascular trunks. Such atypical development may be accidental, but may have also complex genetic basis, as such variations in the vertebral artery course are more frequently seen in patients with Down syndrome examined because of atlanto-axial subluxation [12].

To our best knowledge, there are only two cases of vertebral artery passing between the atlas and axis together with the C2 spinal nerve described in contemporary literature and verified by anatomical dissection [7, 13, 14]. In these cases vertebral artery pierced the dura below the level of atlas vertebra, but the C1 transversary foramen and suboccipital space contained no artery. The authors mentioned above in cases of vertebral artery duplication usually describe the arterial branch visualised in the vertebral canal as located intraduraly. Reliable assessment of the true location of the artery in the vertebral canal seems to be hardly possible if just classic angiographic pictures are available. Modern diagnostic tools like CT and MR imaging with three-dimensional reconstructions give much more complete information and are necessary for good pre-operative assessment in every case. The variation presented here, however rare, may seriously complicate C0–C1–C2 stabilisation procedures or make vertebral artery transposition during far lateral/transcondylar approaches very difficult.

Conclusion

In the case presented here the whole ring of duplicated vertebral artery surrounding the posterior arch of atlas was located extraduraly. Similar variations of vertebral artery enlarge the risk of serious complications of surgical and percutaneous interventions, like blockades or C1–C2 space puncture. Surgeons performing laminectomies or instrumental stabilisations should be aware of possible epidural location of atypical vertebral artery.