Craniovertebral Junction Anomalies: An Overlooked Cause of 'Posterior Circulation Stroke'
Correspondence Address: Source of Support: None, Conflict of Interest: None DOI: 10.4103/0028-3886.360916
Source of Support: None, Conflict of Interest: None
Keywords: Atlantoaxial dislocation, infarct, posterior circulation
One-fifth of all ischemic strokes are due to vertebrobasilar ischemic stroke. Vertebral artery dissection (VAD) is a treatable cause of vertebrobasilar ischemic stroke. Dissection of vertebral arteries can be spontaneous or more commonly traumatic.,, Craniovertebral junction (CVJ) anomalies are a rare and often overlooked cause of VAD.,,
CVJ anomaly can present with symptoms due to vertebrobasilar insufficiency (VBI).,,,,, Common symptoms due to VBI are ataxia, drop attacks, vertigo, nausea and vomiting, diplopia, dysarthria, tinnitus, and visual disturbances., Rarely, CVJ anomalies can present as posterior circulation stroke. Cerebellar hypoperfusion has been demonstrated in patients with CVJ anomaly presenting with symptoms of VBI by using single-photon emission computerized tomography (SPECT).
The actual incidence of CVJ anomalies in posterior circulation infarct patients is unknown as CVJ anomalies are very frequently overlooked as a cause of posterior circulation stroke. A testimony to this is provided by the fact that in only 30% of reported cases of posterior circulation stroke, cervical spine X-rays were obtained, while dynamic view (flexion-extension) cervical X-rays were obtained for only 11% of patients.,
There are only a few reported series describing unilateral/bilateral VAD caused by atlantoaxial dislocation (AAD) resulting in posterior circulation stroke.,,,,,,,,,, In the present study, we present clinical features and radiological findings of patients who presented with vertebrobasilar circulation stroke and on investigation were found to be harboring CVJ anomaly. We want to highlight this overlooked aspect of CVJ anomalies.
The medical records of patients managed for posterior circulation infarct associated with congenital CVJ anomaly at our center from January 2009 through August 2013 were retrospectively reviewed from the computerized database of our center. Patients with CVJ anomaly of traumatic, infective, or inflammatory etiology were excluded.
Patients with posterior circulation infarcts were screened for cerebrovascular risk factors, vasculitis, and abnormalities of vertebrobasilar arteries. CT/MR angiography or DSA were also done in patients in whom VBI was suspected. The patients who were found to have VAD were evaluated for possible CVJ anomaly. Cervical spine X-rays including translateral dynamic view were done. CT and MRI of CVJ were also done to evaluate bony and soft tissue abnormalities and any associated cervicomedullary compression.
Patients found to have any bony anomaly were dealt surgically. Patients with reducible AAD underwent posterior fixation alone, while patients with irreducible AAD or basilar invagination underwent either additional transoral decompression or C1-C2 spacer, compression, and distraction, based on the surgeon's preference. The mean follow-up period was 23 months (range: 2–40 months).
A systematic search was performed using the PubMed and MEDLINE databases to identify case reports/series describing posterior circulation infarcts secondary to CVJ anomalies by using the keywords “vertebrobasilar insufficiency,” “craniovertebral junction anomaly,” “bow hunter stroke,” and “Atlanto-axial dislocation.” Searches were restricted to articles in English language and those published up to December 2012. References of these reports were also searched and a total of 10 articles were found; their findings are described in [Table 2].
Seven patients met our inclusion criteria and were included in the study [Table 1]. The mean age was 17.4 years (range: 10–35 years). All the patients were males. The most common symptoms were headache, vomiting, and gait ataxia. All the patients complained of significant headache and vomiting; these symptoms were more common than seen in CVJ anomaly patients with posterior circulation infarcts. Slurring of speech was seen in one patient. One patient had repeated episodes of gait ataxia with left-sided weakness with complete recovery in between the episodes. One patient presented in unconscious state. Four patients complained of vertigo. The median duration of symptoms was 7 days (range: 3 days–12 months).
Examination revealed a short neck in two patients. Other cutaneous stigmata of CVJ anomaly (such as high arched palate, low hairline, and neck tilt) were seen in two patients. Spastic quadriparesis was seen in two patients, while one patient had spastic hemiparesis. Cerebellar signs were present in five patients. Nystagmus was seen in two patients.
All patients were worked up on the lines of stroke in young patients. Routine hematological parameters (hemogram, renal and liver function tests) and serum homocysteine levels were within normal limits in all patients. All patients were negative for antiphospholipid antibodies and HIV serology. Hypercholesterolemia was seen in two patients, while protein C and S were normal in all patients. All patients were started on antiplatelet drugs on the diagnosis of stroke, and these were briefly discontinued at the time of surgery.
CT/MRI revealed cerebellar infarct in five patients, while one had PCA territory infarct; one patient had infarcts in both territories [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]. Three patients had unilateral involvement (all on left side), while two had bilateral involvement.
IADSA was done in two patients, CTA and MRA in three patients each and detected dissection. Dissection of a segment of VA was seen in four patients, whereas in one patient (case 4), VA could not be visualized, may be due to thrombosis. One patient showed occlusion of right VA when the head was turned toward right side. VA 3rd segment was involved in four patients.
CVJ imaging revealed AAD in five patients, reducible in four patients and non-reducible in one patient. Occipitalization of atlas was present in five patients, while C2-C3 fusion was seen in one patient. One patient also had platybasia. All patients underwent posterior fixation and made good recovery in our series with no difference from those with CVJ anomaly without posterior circulation stroke.
Two patients deserve special mention. One patient (case 2) presented in unconscious state to us; his GCS when he presented to our emergency department was E1V1M2. NCCT head revealed left cerebellar infarct. Cervical spine X-ray scans revealed reducible AAD. MRA was done, which revealed dissection of left V3 and V4 with thrombosis of basilar artery. In view of poor neurological status of the patient and mass effect in posterior fossa, emergent posterior fossa decompression was done. The patient's neurological status gradually improved to E4VtM6. After weaning him off the ventilator, he underwent C1-C2 posterior fixation. He is doing well at 1-year follow-up.
A 35-year-old male (case 4) developed mild-intensity holocranial headache 10 months back. Next day morning, he woke up to find himself hemiplegic (left side). This weakness improved completely over a period of 10 days. He developed multiple similar episodes involving both sides. He also complained of headache, vertigo, and left-sided weakness. On examination, power was 5/5 in all four limbs and all the deep tendon reflexes were exaggerated along with bilateral extensor plantars. Cerebellar signs were also present. The lateral radiographs of the cervical spine showed occipitalization of the atlas with an atlantodental interval (ADI) of 7 mm, which remained same in flexion and extension. His CT revealed multiple infarcts in right parieto-occipital region (PCA territory) and superior cerebellum. His CTA revealed narrowed left V1 and V2 with focal narrowing at left V2-V3 junction. CT CVJ confirmed the X-ray finding of AAD, along with occipitalized atlas. In addition, basilar invagination was there. He underwent C1-C2 spacer insertion and occipito-C2 fixation. His symptoms improved following surgery. He is doing well at 2 months follow-up.
Craniovertebral junction anomalies
CVJ anomalies include abnormalities of the occipital bone surrounding the foramen magnum, atlas, and axis vertebrae. They can be congenital or acquired, and the latter can be infectious, inflammatory, or traumatic in origin.,,, Bony anomalies may involve the occiput (basilar invagination and platybasia) or the atlas (occipitalisation of the atlas and atlanto-axial dislocation) or axis (odontoid malformations) and other vertebrae (Klippel–Feil anomaly). Bony CVJ anomalies can be associated with soft tissue anomalies such as Chiari malformation or syrinx. CVJ anomalies are reported to be more common in India as compared to in West, and AAD is the most common CVJ anomaly seen in India. The mean age of presentation of patients with CVJ anomalies is 25 years. Considerable advances have been made in the management of CVJ anomalies.,,,,,
Symptoms of craniovertebral junction anomalies
Most of the symptoms of CVJ anomalies result from the compression of the cervical spinal cord, lower cranial nerves, and brainstem. The classical clinical features include motor deficits, with spastic quadriparesis being the most common, sensory disturbances including posterior column involvement, and lower cranial nerve deficits. Rarely, symptoms due to VBI may be the presenting symptom of a patient with CVJ anomaly and even more rare is posterior circulation infarct as the initial presentation of an undetected CVJ anomaly., Common symptoms due to VBI are ataxia, drop attacks, vertigo, nausea and vomiting, diplopia, dysarthria, tinnitus, and visual disturbances. Wadia et al. reported VBI with posterior circulation stroke symptoms in three patients in their series of 115 patients. VBI was reported in three patients out of 40 in another study, while no patient in this series had stroke. Several other authors have also reported VBI in relation to Klippel–Feil deformity, occipitocervical anomalies., There are few case reports of CVJ anomaly patients whose first presentation was posterior circulation stroke in literature and are summarized in [Table 2]. Vigorous neck movements preceded the symptoms in many of these patients, which included wresting, cervical traction, and intubation.,, In some reports, no obvious neck movement preceded the symptom onset.,,,
Vertebral artery dissection
VAD is an important cause of vertebrobasilar territory stroke, especially in young patients, and accounts for 20% of all ischemic strokes. However, VAD is not as well-known as are internal carotid artery dissections and its incidence is not precisely known. Once thought to be relatively uncommon, VAD is now being recognized more frequently, but it is still frequently overlooked in many younger patients with typical symptoms. Though 4% of all strokes are attributed to arterial dissection, this figure is much higher (45%) in stroke patients less than 45 years of age. VAD can be either spontaneous or more commonly secondary to trauma. In a series of 24 patients with VAD, 83% of dissections were temporally related to trauma. Trauma can be either significant, such as sport activities and chiropractic manipulation, or sometimes, even trivial trauma can lead to VAD. Spontaneous VAD might occur in the setting of underlying disorders such as fibromuscular dysplasia, hypertension, atherosclerosis, migraine, arteritis, or Marfans disease. VAD can be bilateral in 15%–61%, and these patients have a more severe presentation as compared to unilateral VAD.,, One case of bilateral VAD secondary to AAD has been reported in the literature.
CVJ anomaly is an overlooked cause of VAD. The association of CVJ anomalies with VBI is well known despite scarcity of literature. This association is important as treatment of CVJ anomaly might eliminate the risk of vertebrobasilar territory stroke.
The third part of the VA is tortuous with two loops in normal individuals., C1-C2 subluxation causes an increase in the distance and the obliquity of the respective foramen transversorium of C1 and C2. As atlas intermittently slides over the axis, it causes stretching and trauma to the small segment of the artery that is firmly anchored in the transverse foramina of the axis and atlas.,, Intimal injury leads to platelet aggregation and thrombus formation. This thrombus can produce VBI by either occluding the lumen of the vessel or by acting as a source of microemboli, which migrate into the distal circulation.
However, only a few patients with AAD develop posterior circulation infarct. This has been explained by the variation in the dominance of vertebral arteries and variable flow through posterior communicating arteries supplying the posterior circulation.,
Clinical features favoring dissection are neck pain or headache, transient ischemic attacks, ischemic stroke, and tinnitus., In a series of 26 patients with VAD, occipital or neck pain was the most common symptom of VAD, followed by vertigo and nausea. Other symptoms included unilateral facial numbness and unsteadiness. Headache and/or neck pain was a warning sign in 53%, preceding onset of stroke by upto 14 days. VAD has some contribution to sleep apnea, altered sensorium, and myelopathy as well, in addition to VBI. Few cases of sudden death due to VA occlusion have been reported in the literature.
It is important to identify these symptoms in time as a patient with CVJ anomaly with these symptoms is at risk of developing posterior circulation stroke; neck stabilization can help avoid this catastrophic event that can be fatal in some patients. As these symptoms are not well defined, they are usually overlooked. One of our patients (case 4) was having recurrent TIA in posterior circulation for 10 months, and this treatable cause was overlooked in him.
Non-invasive modalities to diagnose VBI include computed tomogram angiography (CTA), magnetic resonance angiography (MRA), and duplex color flow imaging. VAD can be diagnosed using CTA or MRA. However, DSA is considered the diagnostic gold standard.
Agrawal et al. studied cerebellar perfusion in a cohort of 19 patients with congenital CVJ anomalies, with or without symptoms of VBI, by using SPECT. Cerebellar infarction was seen in two of their patients. They found decreased cerebellar perfusion in a significantly more number of patients in the symptomatic group (75% of symptomatic patients vs. 14% of asymptomatic patients). Cerebellar perfusion improved in 88.9% of symptomatic patients following occipito-cervical fusion.
Angiographic findings in patients with craniovertebral junction anomalies
VA anomalies in patients with CVJ anomaly are well described and range from complex interruption of vascular filling of the basilar artery to significant reduction in the lumen of VA with compensatory hypertrophic changes in the other VA. VA abnormalities in the form of dolichoectasia, focal narrowing, elongation, arterial looping, or abnormal entry into an occipital artery in cases of CVJ anomalies associated with posterior circulation strokes have been noted., Angiographic findings include tapered stenosis or occlusion, string sign, pseudoaneurysm, intimal flap, distal pouch formation, and evidence of fibromuscular dysplasia. Sawlani et al. studied MRA/DSA of seven such patients and described obstruction of the VA at the C1-C2 level on one side. They observed that the contralateral VA on DSA was shortened and the loop of the third segment of the VA was straightened, which was described as a “stretched loop sign” by them. They proposed that it might identify patients with AAD at risk of developing VBI. In another study, an angiogram was performed in nine symptomatic patients and a complete block was demonstrated in two patients in the third segment of VA.
Bow hunters stroke
Another entity described with VBI is bow hunter stroke.,, It depicts VBI caused by mechanical occlusion or stenosis of the dominant VA at the C1-C2 level on head rotation. However, cases due to compression of non-dominant VA have also been reported in the literature. Agarwal et al. highlighted the lack of dynamic cervical spine X-rays in the routine diagnostic workup of bow hunter stroke patients despite the availability of prolific literature on this entity. Dynamic cervical spine X-rays are the most reliable investigation to diagnose AAD, which can easily be missed on MRI and MRA.
All the patients who present with posterior circulation should be investigated for any other possible causes of stroke. As many of these patients are young, these patients should be investigated as per the protocol for stroke in young. Patients should be investigated for protein C, S, and homocysteine levels. These patients should also be started on antiplatelet therapy. Posterior fusion, either C1-C2 or occipitocervical, is an effective method to limit all movements at C1-C2, including translational and rotational.,,, Surgery requires careful exposure of the posterior aspect of C1 and C2 as the VA might get injured during exposure., This, in turn, limits the VA compression and rotational occlusion of the VA. However, this comes at the cost of loss of the physiological movements at the C1-C2 joint. Other surgical options tried in bow hunter stroke patients include decompression of the VA by C1 and C2 transversectomy and anterolateral decompression of the third segment of the VA.,,, Disadvantage of the former is reocclusion as seen in many cases, and the latter is associated with significant risk to the spinal accessory nerve. The advantage of these approaches over posterior fixation is that they do not limit physiological neck movements. Matsuyama et al. compared posterior fixation and VA decompression and concluded that posterior fusion is preferable as it avoids recurrence of VA occlusion and is a less morbid approach. The efficacy of posterior fixation is also supported by the results of Agrawal et al. The outcome following posterior fixation is good as seen in our patients and reports described in the literature.
The outcome following posterior fixation is good as seen in our patients and reports described in the literature. However, there are chances of failure of instrumentation and one needs to closely follow up the patients.
CVJ anomalies can present as posterior circulation infarct. One must evaluate all patients with posterior circulation stroke, especially young patients, for possible CVJ anomalies. Dynamic lateral cervical spine X-ray is an important tool to diagnose AAD. CVJ anomalies represent a treatable cause of VAD. Timely intervention in the form of posterior fixation can help prevent posterior circulation strokes.
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Conflicts of interest
There are no conflicts of interest.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2]