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The tonic pupil is characterised by poor reactivity to light, a slow tonic constriction and redilation to a near target, and supersensitivity to topical dilute pilocarpine.1 Most instances do not have an identifiable cause; however, a variety of conditions including herpes zoster, orbital trauma including surgery, and paraneoplastic syndromes may result in tonic pupils. The mechanism(s) which produce tonic pupils are not known, although axonal loss within the ciliary ganglion is generally believed to result in supersensitivity of the iris sphincter muscle. Giant cell arteritis (GCA) has been reported as an uncommon cause of tonic pupils.2 Furthermore, the cause of tonic pupils in GCA is unknown and direct evidence for an ischaemic cause is not convincing.
We used orbital colour Doppler imaging to study orbital and ocular blood flow in a patient with GCA, unilateral visual loss, and bilateral tonic pupils.
A 58 year old woman presented with visual loss of the left eye for 2 days. She had had neck discomfort and intermittent jaw claudication over the previous 2 weeks. She had no past medical or ocular problems.
Visual acuity was 20/20 in the right eye and no light perception in the left eye. The right pupil reacted briskly to light, with a normal consensual response, the left was amaurotic. She identified all of the Ishihara pseudoisochromatic colour plates with the right eye, and automated perimetry of the right eye was normal. Extraocular motility was normal. Funduscopy of the right eye (Fig 1A) was normal, and the left optic disc was pale and swollen, with retinal cotton wool infarcts within the retina, chiefly within the left macula (Fig 1B). The superficial temporal arteries were supple, pulsatile, and non-tender. The Westergren erythrocyte sedimentation rate (ESR) was 114 mm in the first hour.
She was hospitalised and received intravenous methylprednisolone 250 mg every 6 hours. Temporal artery biopsy was positive for GCA, including the presence of numerous giant cells. After 12 doses of methylprednisolone she was discharged on 80 mg of oral prednisone per day.
Six days later her visual acuity remained 20/20, and with a +2.00 dioptre add over a plano lens she read J1 print at 13 inches with the right eye. Automated perimetry and funduscopy of the right eye remained normal. However, the right pupil now reacted sluggishly to light (Fig 2A) while the left remained amaurotic. In addition, there was light near dissociation in both eyes, with bilateral tonic constriction to a near target followed by slow redilation. Slit lamp examination on the right revealed an irregular pupil (Fig 2B) with sectoral iridoplegia. Both pupils constricted following the instillation of topical 0.125% pilocarpine (Fig 2C).
She remained asymptomatic in her right eye and neuro-ophthalmic examination was unchanged 12 days later, except that her right pupil no longer reacted to direct light. Both pupils constricted slowly and tonically to a near target. Orbital colour Doppler imaging revealed no blood flow in the left central retinal artery (CRA), and blood flow in the right CRA was attenuated at 4.7 cm/s (normal 10 cm/s). There was no flow detected in the short posterior ciliary arteries of the left eye, and attenuated flow in the short posterior ciliary arteries on the right. Although her ESR fell to 4 mm in the first hour and her jaw claudication resolved, the prednisone dose was maintained because of the attenuated blood flow within the right orbit. Her vision remained unchanged and her pupils remained non-reactive to light but with denervation supersensitivity, confirmed by constriction to 0.125% pilocarpine, 2 months after the onset of visual loss.
Five earlier reports have documented tonic pupils in patients with GCA. Davis and coworkers described a 69 year old woman who developed polymyalgia and anisocoria.2 The involved pupil constricted to 2.5% methacholine. In another report of tonic pupils from GCA mild supersensitivity to 0.1% pilocarpine was noted; however, the patient had counting fingers vision in each eye from bilateral optic neuropathy, suggesting that the light near dissociation may have been caused by bilateral afferent dysfunction.3 The authors cited pathological studies which have suggested ischaemia of the extraocular muscles as a cause of ophthalmoplegia in some patients with GCA,4 and they implied that ischaemia was the cause of tonic pupils in their patient, although the site of damage was not specified. Currie and Lessell reported a 63 year old woman who had jaw claudication and loss of vision bilaterally from sequential anterior ischaemic optic neuropathy owing to biopsy proved GCA.5 After losing vision in each eye she developed bilateral tonic pupils which constricted markedly to 0.08% pilocarpine. These authors suggested that impaired orbital blood flow, including the blood supply to the ciliary ganglia or its postganglionic ciliary nerves, resulted in loss of axons and denervation supersensitivity, although no orbital blood flow studies were performed. They speculated that tonic pupils in patients with GCA may be overlooked because of the severity of visual loss.
Other authors have suggested that ischaemic damage may not be the sole cause of tonic pupils in patients with GCA. Bilateral tonic pupils with conjunctival injection were the only ocular manifestations in a 60 year old woman with biopsy proved GCA.6 Because there was no other clinical evidence of orbital or ocular ischaemia the authors postulated that damage to the ciliary ganglion may be mediated by an immunological mechanism. However, they did not quantitate the orbital or ocular blood flow, and our patient shows that clinical signs of ischaemia, except for tonic pupils, may be absent despite markedly decreased orbital blood flow.
Wilhelm reported five patients with bilateral visual loss from anterior ischaemic optic neuropathy or central retinal artery occlusion and tonic pupils from GCA.7 Assessment of orbital blood flow was performed using ultrasonography in three of these patients. In two patients no flow was noted in the supratrochlear arteries, while blood flow in the third was normal. The author noted that the ultrasonographic results supported ischaemia as a cause for the tonic pupils. In the patient with normal orbital blood flow, ischaemia below the resolution of ultrasonography was presumed to cause the tonic pupils.
The blood supply to the ciliary ganglion arises from several sources. Eliskova studied 18 human cadaveric orbits after injection of dye into the internal carotid artery.8 The ciliary ganglion was supplied with blood from one to four arteries, with the posterior lateral ciliary artery and the lateral muscular artery the most common sources, followed by the ophthalmic and central retinal artery. The vasculature of the ganglion itself is composed of a network of capillaries.
Orbital colour Doppler imaging is a non-invasive way to quantitate blood flow to the orbit and eye. Decreased blood flow in the ophthalmic artery, central retinal artery, and short posterior ciliary arteries may be detected on orbital colour Doppler imaging in patients with GCA.9 Markedly reduced blood flow was found with orbital colour Doppler imaging in both orbits in our patient, despite her visual loss being unilateral. We were unable to find a previous report of bilateral tonic pupils in a patient with unilateral visual loss from GCA. Although anterior segment ischaemia can cause loss of iris sphincter tone, we do not believe that the pupillary findings in our patient resulted from iris ischaemia. Iris ischaemia would result in poorly reactive pupils to both light and accommodation, without a tonic near reaction or denervation hypersensitivity. Therefore, the findings in our patient strongly suggest that the tonic pupils resulted from ischaemic damage to the ciliary ganglion or the postganglionic ciliary nerves which are responsible for pupillary constriction.
The authors do not have any proprietary interests in any of the contents of this manuscript.
Dr Foroozan is supported by the Heed Ophthalmic Foundation, Cleveland, OH, USA.
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