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  • 2020–2021 BCSC Basic and Clinical Science Course™

    Go to Academy Store Learn more and Purchase.

    5 Neuro-Ophthalmology

    Chapter 10: The Patient With Pupillary Abnormalities

    Anisocoria

    Anisocoria Greater in Dim Light

    Anisocoria that is greater in dim light may be caused by a range of conditions. Identifying some of the causes require obtaining a thorough patient history (eg, pharmacologic agents); others can be identified by slit-lamp examination (Table 10-1). In general, causes of anisocoria that have a mechanical or inflammatory origin tend to produce a sluggish pupillary response to light, unlike Horner syndrome and physiologic anisocoria.

    Horner syndrome

    The presence of a lesion at any point along the oculosympathetic pathway results in Horner syndrome, which is characterized clinically by ipsilateral miosis (from unantagonized action of the iris sphincter), facial anhidrosis, ipsilateral upper eyelid ptosis, and mild lower eyelid elevation (upside-down ptosis). The ptosis is due to denervation of the tarsal muscle (Müller muscle) in both the upper and the lower eyelids, producing a noticeably narrower palpebral fissure and the false impression of enophthalmos. In the acute phase, conjunctival hyperemia, facial flushing, and nasal congestion can also be present.

    The distribution of anhidrosis depends on the location of the lesion. Interruption of the central (first-order) or preganglionic (second-order) neuron causes anhidrosis of the ipsilateral head, face, and neck. This may produce a harlequin syndrome, in which one-half of the face is pale and the other half is normal or reddish in color, with the division exactly in the midline. Interestingly, the pale side of the face is the one with the sympathetic deficit because the vessels and perspiratory glands have been denervated, leading to supersensitivity to circulating adrenaline.

    Table 10-1 Causes of Anisocoria Greater in Dim Light and Sluggish Response to Light

    Lesions at or distal to the superior cervical ganglion—that is, the postganglionic (third-order) neuron—result in anhidrosis limited to the ipsilateral forehead. When the lesion is congenital or acquired early in life, iris heterochromia develops (the affected iris appears lighter in color) but might not be detected until the age of 9–12 months.

    One of the clinical challenges in diagnosing Horner syndrome is differentiating it from physiologic anisocoria, because the pupillary reaction to light is normal with both conditions, and physiologic anisocoria may also be greater in dim light. One key difference is that pupillary dilation is intact in physiologic anisocoria, whereas there is dilation lag in Horner syndrome. Pupillary dilation in dim light is the result of sphincter relaxation and dilator contraction. Hence, a normal pupil dilates briskly in dim light. When a sympathetic lesion is present, the affected pupil dilates only by sphincter relaxation. In Horner syndrome, the weakened dilator muscle causes the pupil to dilate more slowly, producing an anisocoria that is greatest at 4–5 seconds and less if remeasured at 15 seconds. The presence of dilation lag is sufficient to differentiate Horner syndrome from physiologic anisocoria.

    The oculosympathetic dysfunction of the pupil can also be confirmed pharmacologically with topical eyedrops of either cocaine or apraclonidine. Cocaine blocks the reuptake of norepinephrine released at sympathetic nerve terminals in the eye, causing pupillary dilation, eyelid retraction, and conjunctival blanching in the unaffected eye. In Horner syndrome, little or no norepinephrine is released into the synaptic cleft. Therefore, cocaine has no effect, and the miotic pupil remains smaller than the fellow pupil. The test is performed by instilling 2 drops of cocaine, 4% or 10%, in each eye 5 minutes apart and measuring the degree of anisocoria after 45 minutes to 1 hour. A postcocaine anisocoria of 1 mm or greater is diagnostic of Horner syndrome on the side of the smaller pupil (see Fig 10-1). Eyes with iris synechiae and a mechanically immobile pupil can cause false-positive cocaine test results, but such findings can be readily distinguished through slit-lamp examination. In addition, after instillation of topical phenylephrine 10% (a strong, direct-acting sympathomimetic drug), a mechanically restricted pupil will remain small, but in Horner syndrome, it will readily dilate.

    Topical apraclonidine (0.5% or 1%), which is an α2-adrenergic agonist and a weak α1-adrenergic agonist, is used routinely as a pharmacologic diagnostic test for Horner syndrome (Fig 10-2). In most healthy eyes, apraclonidine has little effect on pupil size. In patients with Horner syndrome, the α1-agonist effect dominates because of the supersensitivity of the α1-receptors, resulting in relative mydriasis by contraction of the dilator muscle. For this test, 1 drop of apraclonidine is placed in each eye, and the patient is reassessed 60 minutes later (however, a positive result can often be detected before the 60 minutes have elapsed). Reversal of the anisocoria is considered a positive response and confirms the diagnosis of Horner syndrome. In addition to the pupillary dilation, the upper eyelid ptosis improves as well.

    However, the role of apraclonidine has several limitations in the diagnosis of Horner syndrome. First, in theory, only postganglionic lesions should produce denervation supersensitivity. Although apraclonidine has been shown to trigger pupillary dilation in lesions at all levels of the sympathetic chain, the degree of sensitivity produced by central and preganglionic lesions is unclear. Second, denervation supersensitivity typically occurs several (2 to 5) days after injury to the sympathetic pathway; therefore, its role in acute lesions is questionable. In addition, apraclonidine is generally avoided in young children because it may cause central nervous system (CNS) depression or acute respiratory arrest. Cocaine remains a better choice for this age group, given its lower risk of adverse events. Brimonidine cannot be substituted for apraclonidine in pupil testing for Horner syndrome because it is a highly selective α2-adrenergic agonist and has no significant effect on the α1-receptor on the iris dilator.

    Once a Horner syndrome is confirmed, it is possible to pharmacologically localize the lesion with topical hydroxyamphetamine (1%). Hydroxyamphetamine enhances the release of presynaptic norepinephrine from an intact postganglionic neuron; therefore, the pupil should dilate. If the pupil affected by Horner syndrome does not dilate, a lesion of the postganglionic neuron is suspected. If both pupils dilate well, the lesion is more proximal, in either the first- or second-order neuron (see Chapter 1, Fig 1-37). Because cocaine may interfere with the uptake and hence the efficacy of hydroxyamphetamine, 72 hours should elapse between the 2 tests.

    Because commercial preparations of topical hydroxyamphetamine have been difficult to obtain and its use is associated with a high rate of false-negative results, hydroxyamphetamine for localization of Horner syndrome is rarely used in clinical practice. In most instances, the clinical presentation is sufficient to suggest the site of injury and the necessary evaluation (Table 10-2). The presence of neurologic signs such as ataxia, nystagmus, and hemisensory deficit suggests a medullary lesion, indicating a potential need for magnetic resonance imaging (MRI) of the brain and upper cervical cord. Symptoms such as arm pain, cough, hemoptysis, and swelling in the neck suggest a second-order (preganglionic) lesion in the superior sulcus (Pancoast syndrome) or in the mediastinum, necessitating cervicothoracic imaging (Fig 10-3). Symptoms associated with third-order (postganglionic) neuron injury include numbness over the first as well as the second or third divisions of CN V and double vision resulting from CN VI palsy, owing to the shared location of CN VI and oculosympathetic fibers in the cavernous sinus. Given the extent of the postganglionic fibers, modalities for investigation include MRI, with contrast, of the head, neck, and chest and magnetic resonance angiography (MRA) of the neck or computed tomography (CT) of the head, neck, and chest and computed tomography angiography (CTA) of the neck. If examination of old photographs confirms that Horner syndrome has been present for several years, further investigation will probably be unproductive.

    Figure 10-2 Apraclonidine test for Horner syndrome. A, A patient with suspected oculosympathetic defect (ptosis and miosis) on the right side. B, Following instillation of topical apraclonidine in both eyes, the right pupil has dilated and the anisocoria is now reversed, confirming Horner syndrome on the right side. Note also the resolution of eyelid ptosis, even to the point of retraction on the right side.

    (Courtesy of Aki Kawasaki, MD.)

    Table 10-2 Features Associated With Horner Syndrome, Based on Lesion Location

    Figure 10-3 Horner syndrome involving the second-order neuron. A, This patient demonstrates right-sided ptosis and miosis in bright light. B, The anisocoria increases in the dark. C, Following instillation of hydroxyamphetamine eyedrops (1%), both pupils dilate, indicating that the third-order neuron is intact. D, CT scan demonstrates a right apical lung mass (Pancoast tumor) (arrow).

    (Parts A–C courtesy of Lanning B. Kline, MD; part D courtesy of M. Tariq Bhatti, MD.)

    Horner syndrome associated with pain deserves special attention. Painful postganglionic Horner syndrome is a distinct clinical entity associated with several causes, most importantly an internal carotid artery dissection (Fig 10-4). Pain from dissection is usually located around the temple and orbit, and may extend to the throat. Patients with painful postganglionic Horner syndrome may also have amaurosis fugax and altered taste (dysgeusia). This condition must be recognized promptly because in the acute stage, stroke is a possible complication. MRI typically shows an intramural hemorrhage of the internal carotid artery, but in some cases, MRA, CTA, or, in rare instances, cerebral arteriography is needed to detect evidence of the dissection (see Chapter 14).

    Trigeminal autonomic cephalgias, such as cluster headache, may also cause painful Horner syndrome during an acute attack (see Chapter 12). The Horner syndrome often resolves but may become permanent after repeated attacks. Some patients, usually middle-aged men, have Horner syndrome and daily unilateral headaches not characteristic of cluster headache. This condition, for which no underlying pathology can be identified, is called Raeder paratrigeminal syndrome. This syndrome is a diagnosis of exclusion made after careful evaluation for underlying pathology in the parasellar and cavernous sinus regions. If the site of the lesion is unknown, imaging of the brain, neck, spine, carotid arteries, chest, and pulmonary apex is indicated. This could be done with either MRI and MRA or CT and CTA.

    Congenital Horner syndrome is usually caused by birth trauma to the brachial plexus. Nontraumatic Horner syndrome in infants and children raises the possibility of neuroblastoma arising in the sympathetic chain of the chest. In these circumstances, MRI of the head, neck, and chest is indicated. MRI of the abdomen may also be considered if clinical suspicion is high. Urinalysis for elevated levels of catecholamines and their metabolites is generally less sensitive than imaging studies in detecting neuroblastoma.

    Figure 10-4 Internal carotid artery dissection. A, Axial magnetic resonance imaging (MRI) scan shows blood (arrow) in the wall of the right internal carotid artery (“crescent moon” sign). B, Catheter angiogram demonstrates “string” sign (arrows), confirming internal carotid artery dissection. A = anterior, L = left, P = posterior, R = right.

    (Part A courtesy of Karl C. Golnik, MD; part B courtesy of Lanning B. Kline, MD.)

    Barrea C, Vigouroux T, Karam J, Milet A, Vaessen S, Misson JP. Horner syndrome in children: a clinical condition with serious underlying disease. Neuropediatrics. 2016; 47(4):268–272.

    Dewan MA, Harrison AR, Lee MS. False-negative apraclonidine testing in acute Horner syndrome. Can J Ophthalmol. 2009;44(1):109–110.

    Mahoney NR, Liu GT, Menacker SJ, Wilson MC, Hogarty MD, Maris JM. Pediatric Horner syndrome: etiologies and roles of imaging and urine studies to detect neuroblastoma and other responsible mass lesions. Am J Ophthalmol. 2006;142(4):651–659.

    Morales J, Brown SM, Abdul-Rahim AS, Crosson CE. Ocular effects of apraclonidine in Horner syndrome. Arch Ophthalmol. 2000;118(7):951–954.

    Excerpted from BCSC 2020-2021 series: Section 5 - Neuro-Ophthalmology. For more information and to purchase the entire series, please visit https://www.aao.org/bcsc.

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