Vestibular testing: On balance....
As with all things veterinary, animal patients cannot tell us their sensory perceptions so we must be deductive sleuths. One is not usually consciously aware of vestibular function yet its disruption makes life a challenge, and cases are common in clinical practice. The vestibular system is responsible for equilibrium and balance, as well as participating in reflexes responsible for eye, head, and body position - both static and kinetic. Vestibular disorders are usually displayed as vertigo or dizziness, nystagmus, ataxia, and/or nausea (Brandt and Strupp, 2004). The review article by Dr Marc Kent and his colleagues at the College of Veterinary Medicine at the University of Georgia that is published in this issue of The Veterinary Journal nicely covers both the normal and abnormal in dogs and cats (Kent et al., 2010).
In most veterinary applications, diagnosis of vestibular disorders relies heavily upon the neurological examination, advanced imaging, and the occasional brainstem auditory evoked response (BAER) and additional resources should become available in the near future. However, cost and availability often limit the extent of the investigation in domestic species to the neurological exam.
It can be difficult to pinpoint the beginning of a discipline in veterinary medicine, but for neurology, based on the publication dates of the earliest neurology texts such as Frauchiger and Fankhauser (1949), McGrath (1956), Hoerlein (1965) and Palmer (1965), it appears to have been in the 1940s and 1950s. There were publications as early as the late 19th century (for example, Dexler, 1896) although the coverage of vestibular function and disease in these early books is quite limited. McGrath (1956) and Hoerlein (1965) both mention cerebellar-vestibular syndrome but provide no diagnostic tools for lesion localization. Palmer (1965) discusses rotational testing and the caloric test. In contrast, the most recent neurology texts (Bagley, 2005; de Lahunta and Glass, 2009; Dewey, 2008; Lorenz and Kornegay, 2004; Mayhew, 2009) dedicate significantly more coverage to vestibular disorders with a growing list of recognized syndromes and the clinical signs that accompany them. Even so, the available ancillary tests to support diagnoses remain small in number.
An important component of the anatomical diagnosis that instructs prognosis assessment and treatment of vestibular disease is distinguishing between peripheral and central disorders. The latter typically have a worse prognosis and the former may be more amenable to therapeutic interventions (Dieterich, 2007). Because few clear-cut differentiating markers exist, textbooks tend to advise the examiner to look for other signs of central disease that would accompany central vestibular disease. For example, many sources point to the presence of vertical nystagmus as indicative of central disease, although we now know this is not always the case (de Lahunta and Glass, 2009). Determining the central-peripheral distinction can be problematic.
Probably the greatest resource in anatomical localization of vestibular lesions in recent years has been the advent of advanced imaging tools, including computerized tomography (CT) and magnetic resonance (MR) imaging (Kent et al., 2010). These modalities allow soft tissue differentiation of brain parenchyma and reduce the distraction of overlying skull structure images that reduce the utility of survey radiographs. MR can be superior to CT imaging in resolving soft tissue abnormalities but CT provides better bone imaging.
Yet disease can exist in the absence of detectable imaging abnormalities. Other available tests include BAER, survey radiographs, post-rotatory nystagmus testing, otoscopy, and cerebrospinal fluid (CSF) analysis (Bagley, 2005; de Lahunta and Glass, 2009). The BAER may be abnormal in peripheral vestibular disorders, especially those resulting from otitis media and interna, and survey radiographs can identify middle ear disease and skull fractures. Post-rotatory nystagmus testing assesses the horizontal semicircular canals, but can be difficult to perform in medium and large sized dogs and is often unpleasant (and potentially hazardous) for the person spinning while holding the subject. Caloric testing, where convective currents are induced in the endolymph of the horizontal semicircular canals by irrigation of the external ear canal with ice cold (30 C) or very warm (44 C) water, still plays an important role in human neurology (Gonçalves et al., 2008), but is unreliable and impractical in animals and seldom used (de Lahunta and Glass, 2009).
Specialty centers in human neurology now have a variety of sophisticated tools for disease localization (Wuyts et al., 2007; Brandt and Strupp, 2005); some of these show potential for veterinary application, while others likely never will. One general tool set, functional brain imaging using positron emission tomography (PET) and functional-MRI (fMRI), provides a clearer view of neural function in peripheral but especially in central disorders than may be seen with standard MR and CT imaging (Dieterich and Brandt, 2008). However, due to cost and special facility needs these tools are likely to remain only in the human and research arenas.
The peripheral vestibular apparatus consists of five paired sensory structures comprising
three semicircular canals that detect angular acceleration and two otolith organs (saccule and utricle) that detect linear acceleration. No single test can assess all five (Wuyts et al., 2007), but tests do exist that individually evaluate each although not all are presently in clinical use. In humans, horizontal canal assessment is done with the caloric test and rotational testing, where electronystagmography (ENG; formerly electrooculography) records eye movements in response to evocation of the vestibulo-ocular reflex; this is often supplemented with or replaced by video-nystagmography. The rotation may be of the whole body while sitting upright during earth vertical axis rotation, or of the head only. The whole body rotation test is said to have greater sensitivity, while caloric testing has greater specificity for peripheral disorders (Wuyts et al., 2007). As described above, caloric testing has been mostly abandoned in veterinary applications and ENG is not routinely used with dogs or cats.
Vertical semicircular canals are more difficult to assess. Responses to impulse head movements in the planes of each of the paired left and right vertical canals can be measured as induced currents in fine wire coils on the sclera when the eyes move in response to the head movement (Halmagyi, 2004). This test has limited clinical use, and is unlikely to prove useful with animal subjects. Utricle assessment can be performed by so-called unilateral centrifugation, where the body is moved a small distance laterally away from the earth-vertical axis during rapid rotational velocities (Wetzig et al., 1990), or by off-vertical axis rotation at constant velocity, which should not stimulate the semicircular canals. However, as with the vertical semicircular canal tests, these tools are not practical for veterinary use.
One test is available to assess the saccule: the vestibular evoked myogenic potential (VEMP; Colebatch et al., 1994; Welgampola and Colebatch, 2005). In awake subjects (where the weight of the head is primarily supported by the sternocleidomastoid muscles) a loud sound stimulus (click or tone burst) elicits a reflex muscle twitch that is detected with surface electromyography (EMG) electrodes, with the EMG peaks occurring at standard latencies. The response is thought to reflect residual sound sensitivity of the sacculus (which through evolution has changed from detecting sound to detecting acceleration), and persists in subjects with severe cochlear hearing loss. It can only be activated when the relevant muscles are active (Welgampola and Colebatch, 2005), in other words only when head weight is actively supported by muscle contraction.
Finally, direct (galvanic) low amplitude current (~ 1 mA) stimulation through electrodes placed on the mastoids activates the vestibular organs, producing head, body, and eye movements that reflect a complex integration of responses from all five vestibular components to the induced spurious acceleration signals (Fitzpatrick and Day, 2004). Left-right asymmetries lateralize dysfunction, but are not specific to any of the vestibular organs.
In veterinary medicine, the VEMP and galvanic stimulation show potential, while the various advanced rotational tests do not. ENG recordings of eye movements during head movements can improve on direct observation, but the cost of equipment and additional testing time argue against their use; the same is true of PET and fMRI. The VEMP has been reported in research applications in the chinchilla, guinea pig, rat, and decerebrate cat (Uchino et al., 1999), but not yet in dogs or intact cats. Of all the tests used in humans, this seems to show the most promise.
The economies of veterinary practice must always address the issue of cost vs. return. Clinics with BAER testing capability will in most cases also be able to perform VEMP testing with the same equipment and at the same testing session. Lesions in one of the peripheral vestibular organs will be frequently accompanied by lesions in others, so saccule testing with the VEMP may prove cost effective in confirming peripheral disease. Application must await laboratory validation in dog and cat populations and comparison with MR and CT imaging for diagnostic utility. On balance, new diagnostic tools and treatments must benefit our patients, but at a tolerable cost. At the same time, adoption of new testing methods may show us that our patients are affected more than we realize, and identified vestibular syndromes in animals may prove to be models for human vestibular disorders like Ménière’s disease, where much still remains to be understood.
The review by Kent et al. (2010) provides us with a timely reminder of how much we still need to learn about vestibular disorders. In 2008, a UK working party report from the Royal College of Physicians noted that patients with hearing and balance disorders ‘can wait years to be seen by an appropriate specialist, and often remain undiagnosed and inadequately managed’. This, it was said, was because dedicated and specialized audiological/vestibular services are only available in a few specialist centres, with no provision in most of the country. The report also commented that there was a severe shortage of state-of-the-art audiology, tinnitus and vestibular clinics, with limited access to integrated multidisciplinary teams with the appropriate specialists. Human medicine may have a long way to go, but veterinary science is still only scratching the surface.
Professor of Neuroscience,
Comparative Biomedical Sciences,
Louisiana State University,
School of Veterinary Medicine,
Baton Rouge, LA 70803,
Bagley, R.S. 2005. Fundamentals of Veterinary Clinical Neurology. Blackwell, Ames, IA.
Brandt, T., Strupp, M. 2005. General vestibular testing. Clinical Neurophysiology 116, 406-426.
Colebatch, J.G., Halmagyi, G.M., Skuse, N.F. 1994. Myogenic potentials generated by a click-evoked vestibulocollic reflex. Journal of Neurology, Neurosurgery, and Psychiatry 57, 190-197.
De Lahunta, A., Glass, E. 2009. Veterinary Neuroanatomy and Clinical Neurology. 3rd ed. Saunders Elsevier, St. Louis, MO.
Dewey, C.W. 2008. A Practical Guide to Canine and Feline Neurology. 2nd ed. Wiley-Blackwell, Ames, IA.
Dexler, H. 1896. Beitrage zur Pathologie und pathologischen Anatomie der Compressionsmyelitis des Hundes. Österreichische Zeitschrift für wissenschaftliche Veterinäkunde 7, 1-124. [Contributing to the pathology and pathological anatomy of the Compressionsmyelitis of the dog]."
Dieterich, M. 2007. Central vestibular disorders. Journal of Neurology 254, 559-568.
Dieterich, M., Brandt, T. 2008. Functional brain imaging of peripheral and central vestibular disorders. Brain 131, 2538-2552.
Fitzpatrick, R.C., Day B.L. 2004. Probing the human vestibular system with galvanic stimulation. Journal of Applied Physiology, 96, 2301 16.
Frauchiger, E and R. Fankhauser. 1949. Die Nervenkrankheiten unserer Hunde [The Nervouse Diseases of our Dogs]. Huber, Bern.
Gonçalves, D.U., Felipe, L., Lima, T.M. 2008. Interpretation and use of caloric testing. Brazilian Journal of Otorhinolaryngology 74, 440-446.
Halmagyi, G.M. 2004. Garnett Passe and Rodney Williams Memorial Lecture: New clinical tests of unilateral vestibular dysfunction. Journal of Otolaryngology and Otology 118, 589-600.
Hoerlein, B.F. 1965. Canine Neurology. Diagnosis and Treatment. W.B. Saunders Co., Philadelphia, PA.
Kent, M., Platt, S.R., Schatzberg, S.J. 2010. The neurology of balance: Function and dysfunction of the vestibular system in dogs and cats. The Veterinary Journal xx, xxx-xxx.
Lorenz, M.D., Kornegay, J.N. 2004. Handbook of Veterinary Neurology. 4th ed. Saunders Elsevier, St. Louis, MO.
Mayhew, I.G.J. 2009. Large Animal Neurology. 2nd ed. Wiley-Blackwell, Ames, IA.
McGrath, J.C. 1956. Neurologic Examination of the Dog, With Clinicopathologic Observations. Kimpton, London.
Palmer, A.C. 1965. Introduction to Animal Neurology. Blackwell, F.A. Davis Co., Philadelphia, PA.
Uchino, Y., Sato, H., Sasaki, M., Imagawa, M., Ikegami, H., Isu, N., Graf, W. 1999. Sacculocollic reflex arcs in cats. Journal of Neurophysiology 77, 3003-3012.
Welgampola, M.S., Colebatch, J.G. 2005. Characteristics and clinical applications of vestibular-evoked myogenic potentials. Neurology 64, 1682-1688.
Wetzig, J., Reiser, M., Martin, E., Bregenzer, N., von Baumgarten, R.J. 1990. Unilateral centrifugation of the otoliths as a new method to determine bilateral asymmetries of the otolith apparatus in man. Acta Astronautica 21,519-525.
Wuyts, F.L., Furman, J., Vanspauwen, R., Van de Heyning, P. 2007. Vestibular function testing. Current Opinions In Clinical Neurology 20, 19-24.