Annals of the New York Academy of Sciences 956:438-440 (2002)
Deborah L. Downey, John S. Stahl, Roongroj Bhidayasiri, Joy Derwenskus, Nancy L. ADAMS, Robert L. Ruff and R. Johm Leigh
Neurology Service, Veterans Affairs Medical Center, and Case Western University, Cleveland Ohio 44106, USA
Address for correspondence: R. John Leigh, Department of Neurology, Case Western Reserve University and University Hospitals of Cleveland, 11100 Euclid Avenue, Cleveland, OH 44106. Voice: 216-421-3040; fax: 216-231-3461.
Ann. N.Y. Acad. Sci. 956: 438-440 (2002).
Determining the effectiveness of treatments for multiple sclerosis (MS) is complicated because of two factors: (1) the clinical course is unpredictable; and (2) the disease may remain active, as evident on MRI, even though neither the patient nor the physician can detect progression. Thus, there is a need to improve clinical methods for evaluating patients with MS that extend the system introduced by Kurtzke 40 years ago.[2,3] The goal of our study was to determine whether an examination that specifically tests saccades and vestibular eye movements is more sensitive than conventional clinical examinations in identifying brainstem and cerebellar dysfunction in MS.[3,4]
We examined 50 patients (8 female) with MS seen consecutively in our VA outpatient Neurology Clinic between August 1999 and April 2000. The study was approved by our Institutional Review Board. Kurtzke Functional Neurological Status (FSS) and Expanded Disability Status Scale (EDSS) scores in each patient were based on agreement between two examiners.[2,5] We assessed corrected, near visual acuity (Rosenbaum card, expressed as a decimal); visual fields by confrontation; color vision using Ishihara plates (correct responses expressed as decimal of total); pupillary size and reactions; and the presence of optic disc pallor by direct ophthalmoscopy. The eye movements examination consisted of: (1) observing range of movement and covering each eye in turn to test for static ocular alignment; (2) observation of fixation stability in central gaze, and eccentric horizontal, and eccentric vertical gaze; (3) observation of the speed, accuracy, and conjugacy of horizontal and vertical saccades (rapid eye movements) made between two stationary targets (a pencil tip and the examiner's nose); (4) observation of horizontal and vertical smooth pursuit of a moving target (inaccuracy being determined by the presence of corrective saccades); (5) observation of the vestibulo-ocular reflex (VOR) using small but rapid "head thrusts," and noting occurrence of corrective saccades;4 and (6) observation of vergence in response to moving a target in the midsagittal plane towards the patient's nose. We developed an "ocular motor scoring system," which is summarized in Table 1. We formulated this system on the basis of knowledge that some normal subjects show nystagmus on horizontal eccentric gaze and many normal subjects have mild impairment of smooth pursuit. Accordingly, patients were divided into two groups: those with a normal ocular motor (NOM) score of 2 or less, and those with an abnormal ocular motor (AOM) score of greater than 2. We then compared EDSS disability scores and FSS functional scores in the NOM and AOM groups. Statistical comparisons were made using the Mann-Whitney rank sum test.
TABLE 1. Summary of ocular motor scoring system and frequency of abnormal findings
We found that 22 of 50 patients (1 female) had AOM scores (median 4.5, mean 5.1), while 28 of 50 patients (7 female) had NOM scores (median 0, mean 0.6). The frequencies of occurrence of findings in the AOM group is summarized in the table. The commonest abnormality was saccadic dysmetria, taking the form of either overshoots (hypermetria) or an inappropriate vector (e.g., requiring a vertical correction following a horizontal saccade). With conventional testing, limitation of movement or ocular deviation was present in 7 patients, all in the AOM group; nystagmus was present in 14 patients, of whom 12 were in the AOM group. Five patients in the AOM group showed no limitation of movement and no nystagmus.
The age of patients in the AOM group (median 49 years) and NOM group (median 47 years) did not significantly differ; nor did the duration of disease (AOM median 22 years; NOM median 28 years). However, the Kurtzke EDSS scores in the AOM group (median 5.2) were significantly greater (p = 0.02) than the scores for the NOM group (median 3.5). Kurtzke FSS scores were greater in the AOM group for cerebellar functions (p = 0.03) and brainstem functions (p < 0.01). However, Kurtzke FSS scores for pyramidal, sensory, bowel/bladder, and mental functions were not different in the AOM and NOM groups. Visual acuity was significantly lower (p < 0.01) in the AOM group compared with NOM group (medians 0.65 versus 0.8), as was color vision (medians 0.79 versus 1.0). Of the NOM group, 13 of 28 had bilaterally normal optic discs compared with only 1 of 22 AOM patients. Relative afferent pupillary defects occurred in 3 of 28 NOM patients and 5 of 22 AOM patients.
In summary, we found that MS patients with abnormal eye movements were more disabled than patients with normal eye movements. Most of the signs that we elicited and scored are not part of the standard Kurtzke FSS scores of brainstem or cerebellar function, and five patients in the AOM group would not have been detected by conventional testing because they had full range of movements and no nystagmus. Clinical examination of eye movements, with attention to dynamic properties of saccades and the vestibulo-ocular reflex, takes only a few minutes to perform, but may provide better information concerning the presence of brainstem and cerebellar disease. Prospective studies are required to determine whether development of abnormalities with this testing is predictive of disease activity and progressive disability in MS.
This work was supported by the Department of Veterans Affairs, NIH Grant EY06717, and the Evenor Armington Fund.
© 2002 New York Academy of Sciences