Ischemic Stroke Secondary to Dynamic Vertebral Artery Stenosis: Case Report and Review of the Literature

Ischemic stroke secondary to dynamic vertebral artery stenosis or occlusion, also known as “bow hunter's syndrome,” is a rare stroke mechanism. We report a case of a 24-year-old man with multiple hereditary exostosis (MHE) diagnosed at childhood. His first presentation to a neurologist was due to neck pain and clinical syndrome suggestive of ischemia in the vertebrobasilar territory. A therapeutic occlusion was done successfully without complication. The patient was discharged two days later on aspirin alone. In follow up one year later he continued to be symptom free. Moreover, this stroke mechanism has been reported extensively in the literature in isolation or secondary to many underlying diseases. In total, there are 168 cases reported in the published English literature, in either case reports or small series. In this review, we found that by far, vertebral artery occlusion at the atlanto-axial (C1-2) level dominated most reported cases. The most frequent presentation that led to further investigation was syncope or pre-syncope provoked by head rotation to one side. To our knowledge, there is no previous report of any stroke syndrome related to MHE before our case. In this paper, we report the first case secondary to MHE and review the literature up to date since the first reported case in 1952.


Introduction
Strokes in the vertebrobasilar territory are commonly due to diseases affecting the vessels, such as atherosclerosis, penetrating small-vessel disease, or arterial dissection [1]. Conversely, non-traumatic dynamic rotational occlusion of the vertebral arteries causing an ischemic stroke or recurrent transient ischemic attack (TIA) is very rare. In 1978, the term bow hunter's stroke was introduced to describe this stroke mechanism [2]. Some of the common symptoms that occur with this syndrome with head rotation are dizziness, nystagmus, and syncope [3]. Since there are no guidelines for the diagnosis of this syndrome, clinicians use different imaging modalities such as cerebral angiogram, magnetic resonance angiography, ultrasonography, or computed tomography angiography [3]. Moreover, the treatment for this syndrome is conservative management that includes neck immobilization or invasive treatment like surgical decompression.
We will present a case of a young man with multiple hereditary exostoses (MHE) diagnosed during childhood, presenting with a minor ischemic stroke followed by TIA related to head rotation. His vascular imaging revealed a dynamic severe narrowing of the left vertebral artery on head-turning to the right, with reproducibility of his symptoms. He was treated by endovascular occlusion of the culprit vessel. A 24-year-old man with MHE was diagnosed in childhood. His syndrome is the result of a de novo gene mutation and has been associated with multiple exostoses (also known as osteochondroma) mainly involving his extremities. He underwent several surgeries in the past to remove these bony lesions that have caused minor disability and moderate pain. He had no established stroke risk factors and has been otherwise healthy.

Case Presentation
His first presentation to a neurologist was two weeks prior to admission. This was when he presented with neck pain and clinical syndrome suggestive of ischemia in the vertebrobasilar territory. He denied any history of trauma or neck manipulation. His main neurological finding at that time was persistent limb ataxia on the left side. His cranial computed tomography (CT) and CT angiography (CTA) reported no parenchymal or vascular abnormality. However, it showed multiple exostoses growing of his vertebrae at C1 -C2 level with narrowing of the vertebral canal. MRI with diffusion-weighted images (DWI) showed restricted diffusion in the left cerebellum and right thalamus. He was discharged on aspirin and scheduled for follow-up. One week after his discharge, he presented to our institution complaining of recurrent isolated spells of loss of vision on the left visual field. His neurological examination showed left superior homonymous quadrantanopsia that lasted only a few hours. On the contrary, the left arm ataxia persisted. Repeat CT of the head showed no evolution of the previous stroke, and CTA demonstrated a left vertebral artery dissection at C2 level. The vertebral exostoses were impinging on the vessel and causing significant narrowing (Figures 1, 2). His neck was immobilized, clopidogrel was added to aspirin, and later he was anticoagulated with fractionated heparin as he continued to experience TIAs manifested by recurrent left quadrantanopsia, left facial numbness, and worsening of limb ataxia on the left while being on dual antiplatelets. A new MRI of the head showed no new infarcts and confirmed the presence of the previously reported restricted diffusion in the left cerebellum and right thalamus (Figures 3, 4). Surgical decompression on his cervical spine was deferred because it was considered a high-risk operation. Thus, the decision was made to perform a cerebral angiogram for consideration of left vertebral artery sacrifice/occlusion. The angiogram confirmed the dynamic nature of the left vertebral artery narrowing with severe stenosis on head-turning to the right (Figures 5, 6). A therapeutic occlusion by a detachable balloon with prior balloon test occlusion was done successfully without any complication. The patient was discharged two days later on aspirin alone. In follow up one year later he continued to be symptom free.

Discussion
Vertebral artery dissection is a common mechanism for vertebrobasilar strokes especially in the young population [4]. Other rare mechanisms have been described and one of them is the dynamic occlusion of the vertebral artery on head rotation. In a study of 1108 patients undergoing cerebral angiogram for different indications, rotational occlusion of either vertebral artery happened in 5% of the patients. Not all of them were symptomatic and the most predictive symptoms for positive angiogram were fainting and dimming of vision [5]. Husni et al. found that in 23 symptomatic patients with rotational occlusion of either vertebral artery, the other one would be either hypoplastic (22 patients) or critically narrowed at its origin (one patient) [6].
Probably the first described case was the one by Ford in 1952. He described a patient with syncope, vertigo, and disturbed vision provoked by voluntary head rotation. The proposed mechanism was intermittent obstruction of the vertebral artery due to a defect in the odontoid process and excessive mobility of the second cervical vertebra [7]. In 1978 a paper describing vertebrobasilar stroke caused by a similar mechanism in a man while practicing archery introduced the term "bow hunter's stroke," which was later adopted in most similar reports in the literature [2]. Many case reports or small series have been published since then, describing patients with different vertebrobasilar stroke syndromes sharing the same mechanism related to head rotational movement. We will list and summarize the findings of those cases published in English at Medline since the case of Sorensen [2] in 1978 ( Table 1). In total, there are 168 cases reported in the English literature, in either case reports or small series. In this review, we chose to include only the cases that documented dynamic and symptomatic occlusion of the vertebral artery by cerebral angiogram. Only one case that did not respect this criteria and CTA was the only study performed is included [8]. Although some papers proposed a definition that would only include cases with vertebral artery occlusion at the atlantoaxial level, we thought differently as some other reviewers did and included cases where the vessel was involved at lower cervical or even higher (cranio-cervical junction) levels.
In this review, we found that by far, vertebral artery occlusion at the atlanto-axial (C1-2) level dominated most reported cases 100 out of 168 (59.52%). The remaining reports describe cases where the vessel occlusion happened at the lower cervical spine level, except two reports that described occlusion due to obstruction at cranio-cervical junction [9,10]. The most frequent presentation that led to further investigation was syncope or pre-syncope provoked by head rotation to one side. Conservative management with antiplatelet or anticoagulant therapy and sometimes with neck immobilization was the option in 23.21%. Only 3.6% of them failed this approach and required some intervention with either fusion or decompressive surgery. In those where the outcome of treatment was reported during follow-up 144 cases out of 168 (85.7%), the surgical intervention by either fusion or decompressive surgery was favorable compared to conservative therapy. Moreover, recurrent symptoms occur in 3%, and stroke happening in 2.4%. We should not draw firm conclusions from this comparison given that most of the literature on this subject is coming from the surgical field and the potential for publication bias is high. Endovascular interventions were only reported in nine cases. The cases treated with endovascular stent are five [11][12][13][14][15]. Moreover, there are four cases treated with coil embolization [16][17][18][19].
Hereditary multiple exostoses (HME) is a genetic bone disease characterized by the development of benign bone tumors and exostoses [osteochondromas] growing off the metaphysis of long bones. It is caused by a mutation in the EXT1 or EXT2 genes, which are both tumor suppressor genes. Most cases are inherited in autosomal dominant trait, and sporadic cases are less often [43]. The most common level for spinal involvement in HME is at C2 level. Neurological complications of this disease are all related to tissue compression by the enlarging exostoses. Nerves, roots, and spinal cord compression have been reported [44]. We will list and summarize the findings of all published cases in English at Medline since the case of Sorensen in 1978 (Table 1). Therefore, to our knowledge, there is no previous report of any stroke syndrome related to HME before our case.  $ Reported immediate outcome in all cases and further follow up in few of them.
* Only 12 out of 21 in the report were typical cases.
The stroke mechanism in our patient is interesting because either vascular injury in the form of vertebral artery dissection or dynamic stenosis of the vessel on head rotation could explain his symptoms. However, more likely both mechanisms have been responsible for his clinical course, with the initial stroke being related to the dissection and the later TIA's on head-turning related to the dynamic stenosis of the narrow and compromised vertebral artery.

Conclusions
Although rare, vertebrobasilar stroke can be caused by dynamic vascular occlusion or stenosis. The hallmark of this presentation is that head turning provokes symptoms. Once suspected, dynamic angiography should be done to confirm the diagnosis. Hereditary multiple exostoses can be associated with different neurological complications and ischemic stroke is one of them, which we believe that our case is the first one to report.

Additional Information Disclosures
Human subjects: Consent was obtained or waived by all participants in this study. Conflicts of interest: In compliance with the ICMJE uniform disclosure form, all authors declare the following: Payment/services info: All authors have declared that no financial support was received from any organization for the submitted work. Financial relationships: All authors have declared that they have no financial relationships at present or within the previous three years with any organizations that might have an interest in the submitted work. Other relationships: All authors have declared that there are no other relationships or activities that could appear to have influenced the submitted work.