Pupil Assessment in Optic Nerve Disorders
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Eye (2004) 18, 1175–1181 & 2004 Nature Publishing Group All rights reserved 0950-222X/04 $30.00 www.nature.com/eye Pupil assessment in FD Bremner CAMBRIDGE OPHTHALMOLOGICAL SYMPOSIUM optic nerve disorders Abstract Uses in clinical practice Pupil assessment is invaluable when distinguishing functional Background The normal pupillary from organic visual loss. Its usefulness in constriction to light is an involuntary reflex distinguishing between different causes of that can be easily elicited and observed optic neuropathy and as a prognostic sign is without specialized equipment or discomfort gradually emerging. to the patient. Attenuation of this reflex in Eye (2004) 18, 1175–1181. doi:10.1038/sj.eye.6701560 optic nerve disorders was first described 120 years ago. Since then, pupil examination Keywords: pupil; optic nerve; reflex; afferent has become a routine part of the assessment defect; perimetry of optic nerve disease. Clinical techniques The original cover/ uncover test compares pupillomotor drive in Introduction the two eyes, but requires two working pupils and is relatively insensitive. The swinging Reflexes are extensively used in clinical flashlight test is now the standard clinical tool neurology to assess function in sensory or motor to detect pupillomotor asymmetry. It requires nerves. Reflexes are involuntary and therefore only one working pupil, is easily quantified, serve as objective indicators of function. The and has high sensitivity in experienced hands, optic nerve forms the afferent limb of a number but interpretation of the results needs care. of brainstem reflexes that could potentially be Measurement of the pupil cycle time is the exploited when testing its function, but the most only clinical test that does not rely on useful has proved to be the pupil light reflex comparison with the fellow eye, but it can (PLR): the PLR can be easily observed, causes only be measured in mild to moderate optic no distress or discomfort to the patient, and may nerve dysfunction, is more time consuming, be quantified. Moreover, the symmetry of the and less sensitive. PLR to stimulation of either eye provides an Laboratory techniques Infrared video opportunity to compare the pupillomotor drive Department of Neuro- ophthalmology (Box 142) pupillography allows recordings to be made of in both eyes. National Hospital for the pupil responses to full-field or perimetric Neurology & Neurosurgery light stimulation under tightly controlled Queen Square London History conditions with a high degree of accuracy. WC1N 3BG UK Frustratingly, there is a wide range in reflex Galen of Pergamon is credited as the first gain in normal subjects limiting its usefulness physician to make clinical use of the PLR in the Correspondence: FD Bremner unless comparison is made with the fellow eye 1 second century (common era). When deciding Department of Neuro- or stimulation of unaffected adjacent areas of whether or not to couch a cataract he would ophthalmology (Box 142) the visual field. cover and then uncover each eye in turn while National Hospital for Correlation with other tests In general, the patient gazed out of the window: covering Neurology & Neurosurgery pupillomotor deficit shows good correlation the fellow eye produced disproportionate Queen Square London WC1N 3BG UK with visual field deficit. However, some pupillary dilation when the cataractous eye had Tel: þ 4420 7837 3611 diseases of the optic nerve are associated with retrolental pathology. The association of PLR ext.3382 relative sparing either of pupil function or attenuation and optic nerve disease was not Fax: þ 4420 7676 2041 visual function implying that pupil tests and made until the end of the 19th century when E-mail: fionbremner@ psychophysical tests may assess function in Hirschberg2 described a woman with acute doctors.org.uk different subpopulations of optic nerve visual loss. In view of the normal fundus Received: 4 September fibres. Less is known of the relationship appearance, her visual loss was initially thought 2003 between pupil measurements and to be hysterical, but demonstration of the absent Accepted: 4 September electrodiagnostic tests. PLR on the affected side confirmed the 2003 Pupil assessment FD Bremner 1176 diagnosis of retrobulbar optic neuropathy. After 20 years, quantifiable, and much more sensitive. The test is Gunn3 published a series of cases in which he claimed to deceptively simple, however, and requires considerable have been able to distinguish organic lesions from practice to perform reliably as well as care in its malingering on the basis of comparing pupillary escape interpretation; inexperienced clinicians may induce an (pupil dilation after prolonged light stimulation) in the RAPD by unequal retinal bleaching16 or by off-axis two eyes. Kestenbaum devised a means of quantifying stimulation in patients with strabismus. Patients must this phenomenon in his textbook4 and coined the term not focus on the flashlight since accommodative miosis ‘Marcus Gunn pupil’ to describe such an afferent pupil will be greater when the light is shone in the better eye. defect. Today, this eponym has largely disappeared but Normal subjects may show RAPD up to 3 dB due to observation of the PLR has become an essential element natural asymmetry in pupillomotor drive from the two in the examination routine for any patient with suspected eyes.17 Furthermore, anisocoria will generate RAPDs of optic nerve disease. approximately 1 dB for each 1 mm of anisocoria by limiting the amount of light entering the eye with the smaller pupil.18 Media opacities may induce an RAPD in Clinical techniques the fellow eye by increasing the scatter and thus the A number of techniques for testing the PLR have entered pupillomotor ‘effectiveness’ of the light stimulus.19 Since clinical practice. The original method for detecting an the test is comparative, it cannot detect bilateral afferent pupil defect was Galen’s cover/uncover test. (symmetrical) disease nor can the results be This is based on the principle that when a patient looks at straightforwardly compared between patients. a diffuse but directional light source (eg the window), There are a number of other clinical tests using the PLR both pupils dilate very slightly if one eye is covered to test optic nerve function that have been suggested, but because the total pupillomotor drive has been reduced. the only one to have enjoyed general popularity is In healthy subjects, a similar degree of pupil dilation is measurement of the pupil cycle time (PCT). Stern20 in observed no matter which eye is covered, whereas in 1944 first published the observation that if a small beam unilateral or asymmetric optic nerve disease the pupil of light from a slit-lamp is directed into the eye, the dilation is greater when the ‘good’ eye is covered. It is a subsequent constriction of the pupil turns off the quick and simple test requiring no special equipment, stimulus, leading to pupil dilation that turns the stimulus but has disappeared from the modern clinical repertoire back on producing endless cycling around this feedback because it is impractical (we no longer have open loop. Dysfunction anywhere along the PLR pathway is windows to gaze through) and relatively insensitive.5,6 expected to reduce the frequency of these oscillations and Moreover, the test requires two working pupils, it is therefore prolong their period. The technique was largely qualitative and because a comparison is being made, it is forgotten until it was resurrected and improved by Miller therefore of no use in bilateral (symmetrical) disease. and Thompson in 1978.21 They used a horizontal beam The swinging flashlight test was first described by 0.5 mm thick presented tangential to the inferior pupil Levatin in 19597 and subsequently formalized by margin, timed 30 oscillations using a stopwatch, and Thompson.8,9 Like the cover/uncover test, it is a repeated this five times to give an averaged estimate of technique for comparing the pupillomotor drive in the what they called the pupil cycle time (expressed in ms). two eyes; unilateral or asymmetric optic nerve disease is Using this approach, PCT measurements have since been associated with constriction of both pupils when the made in patients with a wide variety of optic flashlight is shone in the good eye but dilation of both neuropathies (optic neuritis,22–25 compressive optic pupils when the flashlight is shone in the bad eye. neuropathy,26,27 glaucoma, atrophic papilloedema, Relative afferent pupil defects (RAPD) as small as 3 dB traumatic optic neuropathy, and ischaemic optic can be detected clinically, and sensitivity can be further neuropathy25). enhanced by placing a 3 dB neutral density filter (NDF) The technique has the advantages of requiring only a in front of the suspected bad eye to widen the intereye slit-lamp and stopwatch, is simple to perform, and does difference in pupillomotor drive to a detectable level.10 not require a normal fellow eye for comparison. There The degree of RAPD can be easily quantified by placing are, however, a number of technical and theoretical NDF,11 crossed polarizing filters,12–14 or Bagolini filters15 drawbacks. The test as described by Miller and of increasing value in front of the good eye until the Thompson takes 5 min, a long time for both patient and RAPD is neutralized. clinician to concentrate at the slit-lamp. The background The swinging flashlight test is now the most common conditions and intensity of stimulus are not pupil test in clinical practice. Like the cover/uncover standardized. It is difficult or impossible to induce test, it is quick and low-tech, but it has the additional pupillary oscillations in patients with marked optic nerve advantages of requiring only one working pupil, is easily dysfunction, making it a test most suited to patients with Eye Pupil assessment FD Bremner 1177 mild to moderate disease. The PCT measurement is objective and quantitative means of assessing function in influenced by resting pupil diameter28 and will be different areas of the visual field.