REVIEW URRENT C OPINION

Cervicogenic causes of vertigo Timothy C. Hain

Purpose of review Herein we discuss the recent literature concerning cervicogenic vertigo including vertigo associated with rotational vertebral artery syndrome, as well as whiplash and degenerative disturbances of the cervical spine. We conclude with a summary of progress regarding diagnostic methods for cervicogenic vertigo. Recent findings Several additional single case studies of the exceedingly rare rotational vertebral artery syndrome have been added to the literature over the last year. Concerning whiplash and degenerative disturbances of the cervical spine, four reviews were published concerning using physical therapy as treatment, and two reviews reported successful surgical management. Publications regarding diagnostic methodology remain few and unconvincing, but the cervical torsion test appears the most promising. Summary Little progress has been made over the last year concerning cervicogenic vertigo. As neck disturbances combined with dizziness are commonly encountered in the clinic, the lack of a diagnostic test that establishes that a neck disturbance causes vertigo remains the critical problem that must be solved. Keywords cervical, dizziness, proprioception, vascular, vertigo, vestibular function

INTRODUCTION Cervicogenic vertigo is illusory motion deriving from a disturbance of the neck. Although dizziness contains vertigo and imbalance within its definition, in this review we consider the terms ‘cervical vertigo,’ ‘cervicogenic vertigo’, and ‘cervicogenic dizziness’ as the same entity. Cervicogenic vertigo is currently ‘out of fashion’. This is largely because of several influential reviews over the last 20 years. Brandt and Bronstein [1] concluded that ‘the debate on the relevance and mechanism of cervicogenic vertigo is more of theoretical interest than of practical relevance’. Nevertheless, there is clear experimental and clinical evidence that the neck perturbations can induce vertigo and imbalance [2 ,3,4]. We will first discuss recent studies concerning the three main categories of cervicogenic vertigo: vascular, whiplash, and vertigo associated with cervical injuries other than whiplash. We conclude with a review of the current state of the art of diagnosis of cervicogenic vertigo. &

VERTIGO ASSOCIATED WITH IMPINGEMENT OF THE VERTEBRAL ARTERIES IN THE NECK Patients who develop symptomatic occlusion of the vertebral artery on sustained head rotation on

the trunk have cervicogenic vertigo. This most commonly occurs at the atlantoaxial level as the majority of head rotation occurs between C1 and C2. This syndrome was first described in 1978 by Sorensen [5] who reported a patient who became symptomatic when practicing archery. Accordingly, this condition is sometimes called ‘Bow-Hunter syndrome’ but the descriptive term ‘rotational vertebral artery syndrome’ (RVAS) is more useful. Only about 40 proven cases of RVAS were reported in the entire literature as of 2012 [6]. In the largest series, Lu et al. [7] presented nine patients who suffered from RVAS and concluded that the most common cause of arterial compression was an osteophyte (56%), and the most frequent location was at the level of C1 (44%). As RVAS patients are exceedingly rare, the literature consists largely of single case studies. These have continued in the recent literature. Sarkar et al. [8] reported a case of bow-hunter’s syndrome in a

Northwestern University and University of Chicago, Chicago, USA Correspondence to Timothy C. Hain, MD, Emeritus Professor, Northwestern University, Chicago Dizziness and Hearing, 645 N Michigan, Suite 410, Chicago, IL 60611, USA. E-mail: [email protected] Curr Opin Neurol 2015, 28:69–73 DOI:10.1097/WCO.0000000000000161

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KEY POINTS  Cervicogenic vertigo/dizziness is probably common, but it lacks a validated clinical test.  The rotational vertebral artery syndrome is extremely rare.  Physical therapy is the preferred treatment for most kinds of cervicogenic vertigo.  The cervical torsion test is the most promising diagnostic procedure at present.

young man, attributed to muscular hypertrophy. Pinol et al. [9] reported another young man with an anomalous course of the vertebral artery at the level of C6. Ogawa et al. [10] reported a case of downbeat nystagmus induced by neck rotation, anteflexion, and lateral flexion, attributed to reversible vertebral artery occlusion. Although physical therapy is the recommended treatment for most other kinds of cervicogenic vertigo, physical therapy is not effective, and even potentially dangerous for patients with RVAS, as the cause is related to blood flow rather than a process that can be affected with neck manipulation or exercise. Treatment must address the vascular problem [6,7].

WHIPLASH ASSOCIATED DISORDER AND VERTIGO Whiplash associated disorder (WAD) is defined as symptoms that follow a neck injury, generally associated with a rear end collision. In patients who experience whiplash, although vertigo is uncommon, about half of them report dizziness and imbalance [11,12]. As these individuals have all experienced perturbations of their neck, and inner ear disorders are rare after neck trauma [13], these are patients with presumed cervicogenic vertigo. Concerning the mechanism, the most prevalent hypothesis is that in WAD, trauma modifies cervical proprioception and produces dizziness through a mismatch between vestibular, visual, and proprioceptive inputs to the vestibular nucleus. Also highly prevalent is the opinion that psychosocial factors including the chance of secondary gain after whiplash plays the predominant role in persistence of subjective symptoms such as pain and dizziness [14]. Modification of cervical proprioception is just one of many other plausible hypotheses for cervical vertigo [1]. There have been no recent studies published concerning the relationship between WAD and dizziness or vertigo. Regarding treatment, Humphreys 70

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et al. [15] and associates reported that 78–80% of patients were improved after 6 months of chiropractic treatment. This result must be considered in the context of the older literature that notes that prognosis for chronic disability after acute whiplash is extremely variable. Humphreys et al. [15] also noted that neck pain patients with dizziness reported significantly higher pain and disability scores at baseline than patients without dizziness. This observation is consistent with the older literature. Recent studies concerning the diagnosis of dizziness accompanying whiplash are discussed in the final section of this review.

DEGENERATIVE CERVICAL DISORDERS AND VERTIGO There are far more patients with cervical arthritis or disk disease in the general population than there are patients with WAD or vertebral artery compromise, and given the assumption that they disturb cervical proprioception and knowing that proprioceptive disturbances of the neck cause imbalance and/or nystagmus in animals [3], it is reasonable to hypothesize that this group is the largest with cervicogenic vertigo. Unfortunately (see following section on testing), lacking a specific test for cervicogenic vertigo, clinicians have no method of separating out patients with dizziness caused by neck disorders, from persons who have both a neck disorder and dizziness. There have been no recent studies on the epidemiology or clinical characteristics of this subgroup of cervicogenic vertigo. Regarding treatment, Reid et al. [16,17] reported good results for ‘Mulligan sustained natural apophyseal glides and Maitland mobilizations’ compared with placebo treatment but no effect on joint repositioning accuracy [16]. There are other recent studies of improvement with physical therapy [18]. On the contrary, Hansson et al. [19] reported that vestibular rehabilitation had no effect on either neck pain or cervical range of motion in patients with whiplash and dizziness. The implication of this result is that vestibular physical therapy is not a substitute for physical therapy for the neck. In our opinion, physical therapy focusing on relieving neck pain and spasm and improving mobility is reasonable treatment for patients thought to have cervicogenic vertigo associated with either whiplash or degenerative disorders of the neck. Regarding surgical treatment, recent studies include that of Ren et al. [20] who reported an excellent outcome in 18 out of 35 patients who underwent percutaneous laser disk decompression. Li et al. [21] also reported good results following more extensive cervical surgery. Freppel et al. [4] Volume 28  Number 1  February 2015

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Cervicogenic causes of vertigo Hain

reported that surgery for cervical radiculopathy reduced the contribution of visual input to postural control. This would be generally thought to be a positive outcome. Although these reports are encouraging, and support the conjecture that the neck disorders cause cervicogenic vertigo, we think that it remains unreasonable to perform cervical surgery for patients thought to have cervicogenic vertigo, but lacking other indications for surgery than dizziness or imbalance.

approach has been explored on numerous occasions [26–28]. The cervical torsion test is performed with the same methodology as the ‘vertebral artery test’ [27]. It is a simple procedure wherein nystagmus is monitored with the patient sitting upright in total darkness. The head turned approximately 90 degrees on the trunk for 15 s, keeping their eyes centered in the orbit, first to one side and then to the other. Nystagmus with the head in the center is compared with nystagmus with the head turned. L’HeureuxLebeau et al. [29 ] recently reported that more than 2 degrees per second nystagmus during the cervical torsion test was more common in patients with cervicogenic vertigo than patients with benign paroxysmal positional vertigo. The cervical torsion test is not affected by cognitive variables. Furthermore, it has recently become much easier to perform because of the recent wide availability of videoFrenzel goggles that can detect small amounts of nystagmus at the bedside [30]. The cervical torsion test, with technological improvements, appears to be the best diagnostic possibility on the horizon for cervicogenic vertigo and needs more study. Also using eye movements, the manual therapy community has reported procedures such as the ‘smooth pursuit neck torsion test’: to be useful for diagnosis of cervicogenic vertigo [31,32]. Smooth pursuit, is a complex multiple input system that is vulnerable to cognitive variables, age, and sedation. For this reason, it is unlikely that any smooth pursuit test could ever be of general utility for diagnosis of cervicogenic vertigo. Fischer et al. [28] reviewed many reports of abnormal oculomotor function in whiplash, and found no consistency or underlying pattern. This direction of inquiry appears to be a dead end. The third category of diagnostic tests involves measuring the effect of head on neck movement on balance. Several studies including the very recent literature have reported that postural stability is reduced in patients with cervical injuries such as due to whiplash [33–35]. This is logical as injuries to the neck might disturb the difficult adjustment between the two coordinate systems of the head and body [36]. Bianco et al. [33] recently reported that imbalance can be documented using posturography in patients with whiplash injury compared with controls. Freppel et al. [4] reported that the contribution of visual input to postural control was reduced in patients operated on for degenerative cervical spine disorders. Yu et al. [35] reported that body sway is increased to a greater extent by neck torsion than head forward, comparing whiplash patients to normal controls. On the contrary, L’Heureux-Lebeau et al. [29 ] found no difference in a timed 10-m walk test with head turns between patients with presumed &&

Diagnostic tests for cervicogenic vertigo As of this writing, a specific clinical test is not available for cervicogenic vertigo [2 ,22]. Diagnostic tests can be divided into ones that use blood flow, eye movements, postural sway, and subjective joint position as outcome variables. This diagnosis of vascular cervicogenic vertigo is attained through vascular imaging studies, comparing blood flow with the head in provoking position to neutral positions. As the prevalence of vascular rotational vertigo is exceedingly low, the diagnostic yield is also exceedingly low and the risk of a false positive is exceedingly high. False positives may arise not only from testing error, but also from variability in the population – as vertebral artery blood flow is compromised with full contralateral rotation in healthy individuals [23]. Chang et al. [24] reported a variety of changes on MRI blood flow in cervicogenic vertigo. Overall, given the extreme infrequency of RVAS and the changes in blood flow found in normal individuals, the value of these procedures in vertigo provoked by sustained head rotation is small. Although extremely rare, fear of provoking vertebral territory ischemia has caused some groups within the medical community to advocate use of screening tests such as the ‘vertebral artery test’ or VAT as a routine procedure prior to administering therapy to patients involving neck rotation. This test consists of determining whether the combination of head extension and rotation provokes dizziness. Cote et al. [25] found that the VAT test has little or no predictive value for vertebral artery blood flow. It also seems unlikely that a sustained head rotation test would predict risk from a high acceleration head thrust as is commonly used for treatment of neck facet disorders. Nevertheless, the VAT may have value as a defense against litigation wherein neurological symptoms are attributed to head rotation. A second category of diagnostic testing concerns attempts to document cervical nystagmus – eye movement associated with sustained neck rotation or body rotation under the neck. This logical &

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cervicogenic vertigo and benign paroxysmal positional vertigo patients. Thus, a test of gait speed failed to detect cervicogenic vertigo but tests of sway appear to be often positive. These studies of postural stability add to a substantial previous literature suggesting that patients with cervicogenic vertigo sway more than normal controls. Impairment of postural stability occurs in many other disorders than cervicogenic vertigo and postural instability can be simulated. Whereas postural stability testing is not diagnostic of cervicogenic vertigo due to its lack of specificity and vulnerability to cognitive factors, a normal posturography sway test might be helpful in reducing the likelihood of cervicogenic vertigo. Finally, it has also been proposed that reduced cervical proprioception or joint position error might be a diagnostic sign of cervicogenic vertigo [37]. L’Heureux-Lebeau et al. [29 ] reported that there was elevated joint position error in 25 patients with cervicogenic vertigo. Unfortunately, as this procedure requires cooperation from the individual, it is vulnerable to cognitive variables. More data are needed to decide if this methodology is helpful in clinical diagnosis. To summarize, other than in the extremely rare RVAS cases, we do not have a clinical test that can prove that a neck disturbance causes vertigo. Vestibular laboratory tests serve to exclude inner ear disorders as an alternative cause of vertigo. Imaging studies are useful to detect structural injury to the neck, which increases the probability of cervicogenic vertigo, but they do not establish cause. This leaves the clinician with a group of patients who might have cervicogenic vertigo, but without a way to prove or disprove the diagnosis. Thus, the diagnostic situation for cervicogenic vertigo resembles that of other common clinical diagnoses in the dizzy population such as vestibular migraine [38], or chronic subjective dizziness [39], that also lack objective tests to rule them in or out. &&

CONCLUSION Although experimental and clinical epidemiologic data suggest that cervicogenic vertigo is a significant source of dizziness, in 2014 it remains ‘out of fashion.’ The key problem remains a lack of a sensitive and specific test that differentiates between the chance coincidence of a neck injury and dizziness, and the situation where the neck injury actually causes dizziness. Acknowledgements None. 72

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Financial support and sponsorship None. Conflicts of interest There are no conflicts of interest.

REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Brandt T, Bronstein AM. Cervical vertigo. J Neurol Neurosurg Psychiatry 2001; 71:8–12. 2. Yacovino DA, Hain TC. Clinical characteristics of cervicogenic-related dizzi& ness and vertigo. Semin Neurol 2013; 33:244–255. This is a recent review of cervicogenic vertigo. 3. de Jong PT, de Jong JM, Cohen B, et al. Ataxia and nystagmus induced by injection of local anesthetics in the neck. Ann Neurol 1977; 1:240– 246. 4. Freppel S, Bisdorff A, Colnat-Coulbois S, et al. Visuo-proprioceptive interactions in degenerative cervical spine diseases requiring surgery. Neuroscience 2013; 255:226–232. 5. Sorensen BF. Bow hunter’s stroke. Neurosurgery 1978; 2:259–261. 6. Cornelius JF, George B, N’Dri Oka D, et al. Bow-hunter’s syndrome caused by dynamic vertebral artery stenosis at the cranio-cervical junction – a management algorithm based on a systematic review and a clinical series. Neurosurg Rev 2012; 35:127–135; discussion 135. 7. Lu DC, Zador Z, Mummaneni PV, et al. Rotational vertebral artery occlusionseries of 9 cases. Neurosurgery 2010; 67:1066–1072; discussion 1072. 8. Sarkar J, Wolfe SQ, Ching BH, et al. Bow Hunter’s syndrome causing vertebrobasilar insufficiency in a young man with neck muscle hypertrophy. Ann Vasc Surg 2014; 28:1032.e1–1032.e10. 9. Pinol I, Ramirez M, Salo G, et al. Symptomatic vertebral artery stenosis secondary to cervical spondylolisthesis. Spine 2013; 38:E1503–E1505. 10. Ogawa Y, Itani S, Otsuka K, et al. Intermittent positional downbeat nystagmus of cervical origin. Auris Nasus Larynx 2014; 41:234–237. 11. Oosterveld WJ, Kortschot HW, Kingma GG, et al. Electronystagmographic findings following cervical whiplash injuries. Acta Otolaryngol 1991; 111: 201–205. 12. Skovron ML. Epidemiology of Whiplash. In: Szpalski M, Gunzburg R, editors. Whiplash injuries: current concepts in preventions, diagnosis, and treatment of the cervical whiplash syndrome. Philadelphia: Lippincott-Raven; 1998. pp. 61–67. 13. Mallinson AI, Longridge NS. Dizziness from whiplash and head injury: differences between whiplash and head injury. Am J Otol 1998; 19:814–818. 14. Kasch H, Bach FW, Jensen TS. Handicap after acute whiplash injury: a 1-year prospective study of risk factors. Neurology 2001; 56:1637–1643. 15. Humphreys BK, Peterson C. Comparison of outcomes in neck pain patients with and without dizziness undergoing chiropractic treatment: a prospective cohort study with 6 month follow-up. Chiropr Man Therap 2013; 21:3. 16. Reid SA, Rivett DA, Katekar MG, et al. Comparison of mulligan sustained natural apophyseal glides and maitland mobilizations for treatment of cervicogenic dizziness: a randomized controlled trial. Phys Ther 2014; 94:466– 476. 10.2522/ptj.20120483. 17. Reid SA, Callister R, Katekar MG, et al. Effects of cervical spine manual therapy on range of motion, head repositioning and balance in participants with cervicogenic dizziness: a randomized controlled trial. Arch Phys Med Rehabil 2014; 95:1603–1612. 10.1016/j.apmr.2014.04.009. 18. Racicki S, Gerwin S, Diclaudio S, et al. Conservative physical therapy management for the treatment of cervicogenic headache: a systematic review. J Man Manip Ther 2013; 21:113–124. 19. Hansson EE, Persson L, Malmstrom EM. Influence of vestibular rehabilitation on neck pain and cervical range of motion among patients with whiplashassociated disorder: a randomized controlled trial. J Rehab Med 2013; 45:906–910. 20. Ren L, Guo B, Zhang J, et al. Mid-term efficacy of percutaneous laser disc decompression for treatment of cervical vertigo. Eur J Orthop Surg Traumatol 2014; 24 (Suppl 1):S153–S158. 21. Li J, Gu T, Yang H, et al. Sympathetic nerve innervation in cervical posterior longitudinal ligament as a potential causative factor in cervical spondylosis with sympathetic symptoms and preliminary evidence. Med Hypotheses 2014; 82:631–635. 22. Reneker JC, Clay Moughiman M, Cook CE. The diagnostic utility of clinical tests for differentiating between cervicogenic and other causes of dizziness after a sports-related concussion: an international Delphi study. J Sci Med Sport 2014; doi: 10.1016/j.jsams.2014.05.002. [Epub ahead of print]

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Cervicogenic causes of vertigo Hain 23. Mitchell J. Vertebral artery blood flow velocity changes associated with cervical spine rotation: a meta-analysis of the evidence with implications for professional practice. J Man Manip Ther 2009; 17:46–57. 24. Chang F, Li Z, Xie S, et al. Vertigo-related cerebral blood flow changes on MRI. Spine (Phila Pa 1976) 2014; 39:E1374–E1379. DOI: 10.1097/ BRS.0000000000000468. 25. Cote P, Kreitz BG, Cassidy JD, et al. The validity of the extension-rotation test as a clinical screening procedure before neck manipulation: a secondary analysis. J Man Manip Physiol Ther 1996; 19:159–164. 26. Philipszoon AJ, Bos JH. Neck Torsion Nystagmus. Pract Otorhinolaryngol (Basel) 1963; 25:339–344. 27. Cherchi M, Hain T. Provocative Maneuvers for Vestibular Disorders. In: Eggers S, Zee DS, editors. Vertigo and imbalance: clinical neurophysiology of the vestibular system, Vol. 9. Elsevier; 2010. pp. 111–134. 28. Fischer AJ, Verhagen WI, Huygen PL. Whiplash injury. A clinical review with emphasis on neuro-otological aspects. Clin Otolaryngol Allied Sci 1997; 22:192–201. 29. L’Heureux-Lebeau B, Godbout A, Berbiche D, et al. Evaluation of paraclinical && tests in the diagnosis of cervicogenic dizziness. Otol Neurotol 2014; 35:1858–1865. doi: 10.1097/MAO.0000000000000506. This review compares several diagnostic techniques for cervical vertigo. 30. Hain TC. Head-shaking nystagmus and new technology. Neurology 2007; 68:1333–1334.

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Cervicogenic causes of vertigo.

Herein we discuss the recent literature concerning cervicogenic vertigo including vertigo associated with rotational vertebral artery syndrome, as wel...
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