It is an established fact that vascular risk factors - e.g. age (42), hypertension, diabetes mellitus, cigarette smoking and hyperlipidemia- predispose to vertebrobasilar atherosclerosis and subsequent posterior circulation ischemia or infarction. However, in the past the phenomenon of cervical vertigo - e.g. vertebrobasilar ischemia (VBI) secondary to spondylophytic compression of the vertebral artery (VA) - was considered a myth by some. This was because of the coexistence of vertigo and cervical spondylosis particularly in the elderly and the absence of convincing causal relationship between the two. Nevertheless, recent studies using dynamic neurovascular imaging techniques have established the veracity of the association between vertigo and cervical spondylosis mediated by rotational vertebral artery occlusion (RVAO) (4,8,23,28,32,49-52,55,58, 67,70,73,76,79,88). RVAO occurs when cervical osteophytes impinge on the VA causing transitory or permanent mechanical occlusion during head turning to the same or opposite side. (4,8,23,28,32,49-51,55,58,67,70,73,76,88). When RVAO occurs in the absence of sufficient collateral blood flow, the common presentation with vertigo may be explained by the selective vulnerability of the vestibular labyrinth to ischemia.(7,13,26,47,50,51) This VBI can be devastating and may be antecedent to major posterior circulation infarction.(48).
Nevertheless the subject of spondylotic RVAO has remained controversial. Therefore the objectives of this study were to review the literature on vascular mechanisms for cervical vertigo including the interrelationship among the quartet of vascular risk factors, cervical spondylosis, head rotation and vertigo; and modes of investigation, management and prevention of RVAO.
A systematic review of the literature was carried out. A structured search strategy was conducted according to the Center for Reviews and Dissemination Guidelines using Pubmed and Google Scholar databases.(10) For the Google Scholar database the search item ‘cervical vertigo’ with the exact phrase ‘cervical vertigo’ yielded 687 results out of which only 121 contained the term ‘spondylosis’. The Pubmed search for ‘cervical vertigo’ returned 430 papers. Some of the publications retrieved from Pubmed were also present in Google Scholar. The retrieved publications were screened for possible inclusion. 86 publications describing vascular mechanisms for cervical vertigo were included. Articles that were neither related to cervical vascular pathology nor written in English or German language were excluded. The reference lists of key papers were screened to obtain more publications.
The retrieved papers were reviewed for vascular mechanisms of cervical vertigo including RVAO and the interrelationship among vertigo, head rotation, cervical spondylosis and vascular risk factors. Data was also extracted on anatomical and pathophysiological mechanisms, as well as diagnosis and management strategies for vascular cervical vertigo. Because of the heterogeneity of the publications, a meta-analysis was impossible. However data from the key papers were tabulated (Table 2).
Proposed Mechanisms for Cervical Vertigo.
Vertigo resulting from cervical pathologies has been attributed to many causes.(7,39). It was first described in 1858 by Claude Bernard.(7,39). Brandt in a review article proposed labyrinthine, vestibular, ocular, vascular and toxic mechanisms.(7) Proprioceptive and autonomic mechanisms have also been suggested.(68,72). However, the sympathicotonic mechanism proposed by Barre has been disputed.(7).
Of particular significance due to its commonness is unilateral or bilateral RVAO in cervical spondylosis.(8,9,11,16,23,32,47,49,52,55,57,58,61,67,70,72,75,77,79). Nwaorgu reported the presence of cervical spondylosis in up to 40% of all cervical spine roentgenographs.(47). The anatomy of the vertebral artery and the mechanisms of its occlusion are presented in Table 1.
A rotational contralateral VA occlusion was initially considered physiologic after Toole and Tucker found compromised blood flow in vertebral arteries due to head rotation in hemodynamic studies of cadavers.(7) Although this was not supported by initial studies with conventional vertebral angiography at the atlantoaxial joint, recent in vivo studies with better techniques have validated the phenomenon of RVAO across its entire length.(7,79). (Table 1) Mitchel used Transcranial Doppler (TCD) sonography to measure intracranial vertebral artery (VA) blood flow in 30 young, healthy, female subjects, with the cervical spine in the neutral position and with sustained, end-of-range rotation. Statistically significant decreases in blood flow were demonstrated bilaterally with contralateral preponderance.(40). In another study of 240 VAs in 120 normal subjects, he showed significantly decreased blood flow in intracranial VAs following neck rotation. This was also more pronounced in the contralateral VA and supports the works of Sakaguchi, Weintraub, Rossitti et al, Refshauge, Rossitti and Volkmann, Licht et al, Li et al, and Haynes and Milne.(40,41,63,80-86). This decreased blood flow was interpreted to imply mechanical, extrinsic constriction of the vertebral artery.(41) Neck rotation is considered an independent risk factor for VA obstruction and VBI.(79, 82,84) Usually, when one rotates the head, there is compression of the contralateral vertebral artery at the atlantoaxial level, which is compensated by the presence of a normal ipsilateral vertebral artery that provides blood flow to the basilar system. In patients with rotational VBI, one vertebral artery is usually hypoplastic or occluded by atheromatous plaques and there is no significant collateral blood flow from the anterior circulation to the basilar system through the posterior communicating arteries. This explains the typical symptoms of rotational VBI which are caused by a temporary hemodynamically significant compression or complete occlusion of the dominant extracranial vertebral artery during head rotation, with resultant diminished blood flow to the basilar system.(79).
Similarly, rotational VBI was observed in a case-control study by Peterson using TCD ultrasound especially in patients with bilateral VA lesions.(56). In another case-control study involving 52 patients with atherosclerosis and spondylotic changes Ozdemir documented significant RVAO (53) while Barton demonstrated rotational angiographic obstruction at C1/C2 level in 2 patients with VBI.(5).
Thus, it has been shown that the VA can be compressed or occluded at any point from its origin at the subclavian artery to the point of dural entrance into the posterior fossa. (Table1). (40,41,63, 80-86). By far the most common cause of RVAO is an osteophyte arising from the uncinate process and compressing the vertebral artery at some point along its course in the subaxial spine. (79). A fibrous ring adherent to the adventitia is often found at the site of the compression, constricting the artery, and seems to play an important role in the pathogenesis of this syndrome.(79). In relation to the direction of head rotation, the vertebral artery being compressed is usually the contralateral one in cases of compression at C1-C2 and the ipsilateral one when the compression is at the subaxial cervical spine. (79). Hypertrophied facet joint and prolapsed disc can also cause RVAO in patients with cervical spondylosis.(32).
Rotational vertebral artery occlusion and vertebrobasilar ischemia
RVAO is important in those who have vascular risk factors that may compromise the integrity of the Circle of Willis thereby jeopardizing compensatory collateral blood flow. (7,34,47,50,51). The common presentation with vertigo may be due to age-dependent microvascular damage to the vestibular organs, and the fact that the vascular supply to the vestibulocochlear organ, being an end artery, may be more susceptible to vertebrobasilar ischemia (VBI).(31,37,42,47,50). Neurons, axons, and hair cells are known to respond to ischemia by depolarizing, causing transient hyperexcitability with ectopic discharges, manifesting in this scenario as vertigo.(7,69). Vertigo in the absence of other brainstem symptoms and signs is considered to be peripheral in such instances.(7,13,37). Other features of VBI include cerebellar, pontine, medullary, mesencephalic and occipital lobe syndromes manifesting as ataxia, diplopia, dysarthria, visual disturbances, syncope or near syncope, drop attacks, sensory symptoms, motor symptoms, and Wallenberg syndrome.(18,32). Broadly speaking, VBI can result from intraluminal, mural or extrinsic occlusion or stenosis, or retrograde flow in the posterior circulation (subclavian steal syndrome) that is not sufficiently compensated for by collateral circulation. Dissection of the VA is a spontaneous or traumatic cause of VBI.(54,60,62). (Tables1, 2) Acquired mural and intraluminal stenosis and occlusion usually results from vascular risk factors which lead to atherosclerosis, thrombosis and artery-to-artery embolism. (18,20). Hypertension, diabetes mellitus, hyperlipidaemia and cigarette smoking are the strongest modifiable vascular risk factors.(9,18,20). (Tables 1, 2) In summary, extrinsic rotational vertebral artery occlusion resulting from cervical spondylosis in the presence of stenosis of collateral vessels - induced by vascular risk factors - is an important cause of posterior circulation insufficiency manifesting as vertigo.(4,9,23,28,32,49-53,55,58,67,70,73,76,79, 88). A summary of the key publications illustrating the tetrad is presented in Table 2. However, many of the studies did not assess for vascular risk factors other than the documentation of the age of the patient.
The Tetrad in Literature
Kuether, Strek, Ogino and Olzewski published many cases with the tetrad. Although age was the only reported risk factor for vasculopathy,(32,49,50,51,72,) other vascular risk factors might have been present but were neither sought for nor reported. Conversely, Neuheuser reported 1003 cases with vertigo and vascular risk factors. Cervical spondylosis was not investigated for and it was not stated if the vertigo was related to head rotation.(46). However the complete tetrad was present in cases reported by Citow, Nwaorgu, Owolabi, Vilela, Vates, Chen, Ozdemir, Jagiello and Bulsara.(8, 11,14, 29, 47, 52, 53, 77,79). Further studies with particular attention to the identification of vascular risk factors and their effects on the posterior circulation in cases of vertigo in patients with spondylophytic RVAO are warranted.
The cervical vertigo tetrad needs to be distinguished from other causes of vertigo such as benign positional vertigo, Ménière disease, basilar migraine, vestibular neuritis, toxic damage to labyrinths, perilymph fistula, multiple sclerosis, cerebellopontine angle tumors, vestibular epilepsy, and phobic postural vertigo. The distinction is usually possible after a detailed history and clinical examination, but some special bedside tests - eg Dix-Hallpike’s test and other dizziness simulation battery- are often required. The differential diagnosis of vertigo is discussed in greater details elsewhere.(43,74).
Investigation of the tetrad
Plain radiographs of the cervical spine may show flat lordosis, discopathy, osteophytes, and subchondrial sclerosis. The occurrence of both discopathy and osteophytes has an odds ratio of 28.14 for RVAO.(50,90). However, cervical spine radiograph alone may be insufficient to confirm RVAO.(1). Dynamic extracranial and transcranial Doppler and duplex ultrasound of the vertebral, basilar and posterior cerebral arteries (PCA) is a non-invasive time-saving way of visualising RVAO while it has the added advantage of detecting functional flow abnormalities in the posterior circulation resulting from RVAO and vascular risk factors.(47,50). The value of TCD ultrasound in the evaluation and diagnosis of rotational VBI has been shown by many studies.(79). It is very useful as an initial diagnostic tool because of its low costs, reproducibility, ease of use, and the possibility of performing a real-time correlation between the PCA velocities and the symptoms.(63,79 ).
Typically, there is a significant decrease in the PCA velocities of at least 50% but more commonly to a mean of 20% of baseline when patients rotate their head. This is followed by a reactive hyperemic response of at least 10% above baseline velocities when the patient resumes the neutral position, which correlates with the disappearance of symptoms.(79). This reactive hyperemia is a normal response to ischemia and reflects a vasodilatory phenomenon that occurs at the level of arterioles and capillary bed. (79).
Power Doppler is also useful in demonstrating RVAO. However it may not be sensitive enough in advanced spondylosis with masking osteophytes.(29). Carotid Doppler ultrasound may also be used for the detection of steal syndromes resulting from carotid insufficiency.(29,39). However, ultrasound studies are operator-dependent and may be influenced by shadowing and vascular tortuosity.(63).
Dynamic conventional or 2D/3D CT angiograms with progressive head rotation and multiple views are invaluable as part of the workup for those patients who have a confirmed decrease in the PCA velocities on TCD. It demonstrates precisely the nature, cause and location of the vertebral artery compression and shows the vascular anatomy of the anterior and posterior circulation.(8). It is important to visualize the entire course of both vertebral arteries from their origin all the way to the posterior fossa and interpret the results carefully so as to prevent misdiagnosis particularly when surgery is intended.(32,79).
Whereas routine MRI provides information on brain ischemia/infarction it may not reveal the specific cause of dizziness.(15). Such cryptogenic VBI requires dynamic neurovascular imaging to demonstrate the entire vasculature and exclude intermittent or permanent, extrinsic, mural or intraluminal occlusive factors. Dynamic MRA may be useful in this regard.(80,84,85). In evaluating the tetrad, it is paramount to investigate for vascular risk factors such as hypertension, diabetes mellitus, and dyslipidemia among others.
Treatment is multidisciplinary involving the otorhinolaryngologist, orthopaedic surgeon, physiotherapist, neurologists, psychiatrist, and neurosurgeons.(6,47). Conservative approach consists of control of vascular risk factors and neck immobilization either by instructing the patient to refrain from excessive head turning or by the use of cervical collar.(16,32). While immobilization of the neck reduces friction between the VA and the osteophyte, anti-inflammatory drugs may facilitate healing by reducing inflammation and fibrotic constriction of the VA. Surgical treatment, where indicated, must be tailored to the identified cause of the obstruction.(79). Surgery is indicated when symptoms are incapacitating and recurrent and diagnostic tests clearly demonstrate a hemodynamically significant compression of the VA as being responsible for the symptoms.(44,79). Options include fascial decompression, vertebral artery decompression (anterior and posterior approach). (8). osteophytectomy, C1-C2 fusion, decompressive foraminotomy, decompressive transverse foramenectomy and discectomy. (8,32,79). Intraoperative and postoperative dynamic angiography and dynamic TCD ultrasound may be useful in the evaluation of the outcome of the surgery.(8,32,78). Overall success rate for surgery was put at 85% by Kuether. (32).
Cases of cervical vertigo have been reported in literature with resolution effected by conservative (16) or surgical therapy such as facetectomy or transverse foraminotomy with removal of the osteophyte. (4,8,14,32,44,49).
RVAO with VBI in addition to vertebral artery dissection may have implications for manipulative procedures undertaken by physiotherapists and chiropractors in the management of cervical spondylosis and neck trauma.(12,41). Care should be taken to avoid RVAO in patients at risk during cervical manipulation and perhaps during tracheal intubation.(82). Those at risk can be identified by clinical or Doppler ultrasound screening for RVAO.(12,89). Proper management of RVAO can prevent stroke.(79).
Based on this systematic review, a syndrome comprising the tetrad of vascular risk factors, cervical spondylosis, head rotation and vertigo is being proposed. Patients presenting with this syndrome should be evaluated for modifiable cardiovascular risk factors. Management could be conservative or surgical.
Table 1: mechanisms of vertebrobasilar insufficiency
|Intraluminal occlusion||Thrombosis, embolism (87)|
|Mural factors||Atherosclerosis resulting from vascular risk factors, hypoplasia (13). arterial dissection (35, 36,54,60,62,87,89).|
|Extrinsic factors (V0 to V4) (32, 87).||Osteophytes (9) - With the head rotated to side with osteophyte: ipsilateral VA compressed against osteophyte, contralateral VA compressed at the foramina.(32). Chiropractic manipulation, surgical positioning, rheumatoid subluxation. Beauty parlor stroke.(19,21,83,86)|
|V0 (32)||Compressions at the scalenovertebral angle by ligaments of scalenus anterior (Power’s syndrome) (49, 58). scalenus medius musle, longus colli muscle(17), deep fascia.|
|V1||Factors compressing V0 , Thoracic outlet syndrome (66)|
|V2|| C2 to C6: osteophytes compressing the VA anteriorly from the uncinate process or posteriorly from the facet complex. (9). Prolapsed disc.(77).
C1 to C2: obliquus capitis inferior muscle, intertransversarius muscle, vertebral subluxation. kinking and stretching of the contralateral vertebral artery with 30 degrees head rotation.(32). Looped VA (64)
|V3||Hyper-rotation of the atlantoaxial joint- Bow hunter’s syndrome. (27, 49, 63,71). C1 to foramen magnum: muscles (32), atlanto-occipital membrane hypertrophy (32), Vertebral subluxation, Atlantoaxial joint dislocation with stretched loop sign;(33,65) craniovertebral junction anomalies, (2,59) hypoplacia, (59) narrowing at point of dural penetration, (3). Rotational kinking and stretching of the contralateral VA . (32) os odontoideum (24) C1 root schwannoma (30)|
|V4 (32)||Vascular anomalies eg termination of VA in posterior inferior cerebellar artery (37), stenosis, aneurysms, arteriovenous malformations|
|Hemodynamic||Subclavian steal syndrome, Absent posterior communicating artery.|
Table 2: review of articles on cervical vertigo
|Authors and years||No of cases||Reported vascular risk factors||Extrinsic compression of the VA||Presence of rotational vertigo/dizziness|
|Sullivan HG, (73) 1975||1||Not reported||Embolic occlusion of PCA triggered by spondylotic VA compression||Not stated|
|Rock EH (61) 1989||Microatheromatous stenosis||Vertigo only|
|Fujimoto S (22) 1989||2 out of 14 cases||Rotational obstruction and spondylosis||Vertigo, dysarthria, syncope|
|Kuether T (32) 1997 (Reviewed articles not duplicated in this paper.)||3 illustrative cases, plus a review of 19 articles with 131 cases from 1965 to 1985.||Only age reported, other vascular risk factors not mentioned.||3 presented cases and 119 reviewed cases showed angiographic evidence of compression of V0 , V1, V2 or V3||Rotational vertigo present in the 3 presented cases and some of the reviewed cases|
|Matsuyama,(38) 1997||1||Left VA rotational occlusion at C1,C2||Wallenberg’s syndrome|
|Strek P, (72) 1998||130||Age (blood flow abnormality in the VA by Duplex sonography worsened with age)||Cervical spondylosis (discopathy and or steophytes in all cases||Vertigo, tinnitus|
|Galm R (25) 1998||67||Not reported||Cervical spine dysfunction in 31 cases||vertigo|
|Jagiello T (29) 1998||428 patients with VBI and spondylosis||age||Power doppler showed significant RVAO in 17%||Symptoms of VBI including vertigo during head rotation in 66%|
|Citow JS, (14) 1999||1||Age, angina, ICA stenosis||Compression of the VA at C5 by osteophyte||Vertigo triggered by neck extension, change from supine to upright position or vice versa|
|Nan-Fu Chen, (11) 2000||1||Hypertension, age cerebral infarction, carotid atherosclerosis||Osteophytic compression of the right VA with neck turning to the right and luminal reduction to less than half its original size on CTA||Vertigo on turning head 60 degree to right|
|Vates GE (77) 2002||1||Age||Rotational occlusion of the left VA at C4/C5 by herniated intervertebral disc||Vertigo on turning the head to the left > 45o|
|Ogino M (49) 2002||1||Age, 66yr||Compression of the right VA by osteophyte from C4 uncinate process and hypertrophied C3 transverse process. Resolved by resection||Severe vertigo with head turned to the right|
|Nwaorgu et al, (47) 2003||43||Age (mean age 49.2 years), hypertension in 7 %,||Cervical spondylosis in 74% of cases||Vertigo in all cases. Not mentioned if rotational.|
|Neuheuser HK, (46) 2005||n = 1,003, response rate 87%||Age (univariate analysis) Hypertension and dyslipidemia independent effect||No radiological assessment was done||Vestibular vertigo|
|Cagnie B, (9) 2005||111 transverse foramina||Not reported||About half of the osteophytes of the uncinate and of the superior articular process partially covered the transverse foramina obstructing the V2|
|Netuka D (45) 2005||1||Rotational compression of left VA at C1, C2||vertigo|
|Vilela MD (79) 2005||10||Age, hypertension, smoking, cholesterol||RVAO demonstrated by Transcranial Doppler, MRI, CTA MRA||Rotational Vertigo, syncope , tinnitus|
|Ozdemir H (53) 2005||52 patients with VBI and cervical spondylosis||RVAO by doppler||VBI symptoms|
|Olszewski J (50) 2006||80||Age .Basilar artery flow abnormality worsened with age||Flow abnormalities in BA worsened with grade of radiological severity of cervical spondylosis||40 patients had vertigo. Flow abnormality worsened by neck rotation|
|Bulsara KR, (8) 2006||1||Age, Hypertension, diabetes mellitus,||Obstruction of the right VA with head turning to the right by osteophyte at C5-C6 foramen transversarium||Dizziness with head rotation|
|Owolabi MO (52) 2007||2||Hypertension, hyperlipidemia, age||Cervical spondylosis,||Rotational Vertigo relieved by neck collar|
|Tsutsumi S (75) 2008||1||Age||Cervical spondylosis||Rotational VBI symptoms, presyncope|
|Petridis AK, (57) 2008||1||Cervical spondylosis||Rotational VBI symptoms, drop attacks|