CHAPTER 13 Neuroophthalmology
Neuroophthalmology is a broad discipline that incorporates important elements of interest to neurosurgeons, neurologists, and ophthalmologists. This chapter offers some clinical tools and examples of common neuroophthalmic disorders, with emphasis on material of importance to neurosurgeons that is not likely to be covered in other chapters of this text. Readers are referred to the authoritative, multivolume Walsh and Hoyt’s Neuro-ophthalmology1 and other excellent texts2–10 for a more detailed discussion of neuroophthalmic conditions.
From the Eye to the Visual Cortex: Afferent Aspects of Vision
History
Accompanying ophthalmic symptoms (e.g., eye pain or redness, diplopia, proptosis, ptosis) and neurological symptoms are important.11 The time that it takes to perform a thorough neuroophthalmic history is well invested because it often saves the patient (and physician) time, frustration, and health care costs.
Examination
It is key to assess vision in each eye separately. Patients are commonly unaware of or tend to minimize the importance of severe loss of vision in one eye if the opposite one is healthy. Unilateral visual loss may be “discovered” when the sound eye is momentarily covered. Frisén, in his detailed treatise, discusses the techniques for and the inherent difficulties in measuring vision.12
Visual acuity is typically measured by using a standard distance chart (Fig. 13-1) and testing one eye at a time with patients wearing their best corrective glasses or contact lenses. A pinhole frequently improves the vision tested at a distance in a patient who does not have the appropriate spectacle correction. A near-vision card is very helpful, as long as the examiner remembers that presbyopic patients (older than 45 years) may need reading glasses.
The visual field extends 60 degrees from fixation nasally to 90 degrees temporally. Even the large 20/400 “E” on the Snellen visual acuity chart occupies less than 2 degrees of this 150-degree panorama. Visual acuity alone is therefore insufficient to fully characterize visual function. Assessment of the visual field can be done with tools as simple as the examiner’s hands or can be formally plotted with kinetic or static perimetry (Fig. 13-2).13 Many patients who cannot perform well in “formal perimetry” are capable of providing remarkable diagnostic information with confrontation testing (Box 13-1).14
All visual field tests are subjective psychophysical instruments that require a cooperative and reasonably intelligent subject. With increasing sophistication of the various types of perimetry—confrontation, Amsler grid, tangent screen, Goldmann (kinetic), and automated (static) perimetry—the tests become more quantifiable and repeatable, but they are also more difficult for some patients to perform accurately.15,16 Quantification is essential for the management of disorders in which decision making depends on the time course of visual loss (e.g., sellar masses, optic nerve disease, idiopathic intracranial hypertension [IIH]). Furthermore, formal visual fields are necessary to document the efficacy of treatment.17
The relative afferent pupillary defect (RAPD) provides an objective comparison of the visual integrity of the two eyes. Its objectivity makes it one of the most important tools in neuro-ophthalmology (Box 13-2).18 RAPDs do not cause the pupils to be unequal in size. Unequal pupils (anisocoria) are caused by efferent disorders.
The cornea should show a crisp, clear “point of light” reflex from the penlight. Assessing the cornea is especially important when disorders affect either the trigeminal or the facial nerve, or both. Poor function of the orbicularis oculi that results in incomplete blinking can lead to corneal epithelial defects or corneal ulcers. Decreased corneal sensation can result in a similar fate. Tarsorrhaphy is a procedure that surgically apposes a portion of the upper and lower lids to protect the eye. This procedure is often required in patients with facial and trigeminal cranial nerve dysfunction, especially when both these cranial nerves are involved. It is generally too late to save vision in an eye if the clinician waits until the patient complains of decreased vision or pain (Fig. 13-3). When diseases (or procedures) affect the facial or trigeminal nerves, an ophthalmologist should be involved from the beginning to address medical or surgical management of the eye.
Viewing the red reflex of the eye can offer valuable information about the optical media of the eye. Cataract and corneal opacities can be seen in the red reflex, and vitreous hemorrhage (as in Terson’s syndrome) will darken or abolish the red reflex. This test requires only a few seconds with the ophthalmoscope and should become a routine step before the fundus is examined (Box 13-3).
Clinical Appearance of the Optic Nerve
The anatomy of the afferent visual system is reviewed in Figure 13-4. Each optic nerve consists of 1.2 million axons that have their origin in the ganglion cells of the retina, travel in the optic nerve and chiasm, and synapse in the lateral geniculate nuclei. These axons ordinarily become myelinated after passing through the plane of the sclera (i.e., lamina cribrosa), which enlarges the nerve from 1.5 mm at the optic disc to 3 to 4 mm behind the globe. The optic nerve head is the origin of the nerve proper and, when viewed through an ophthalmoscope, appears as a flat, pink ellipse from which the retinal vessels radiate (Fig. 13-E1).
Using the ophthalmoscope to examine the fundus (i.e., optic disc, vessels, macula, and retina) is the cornerstone for the diagnosis of afferent visual disorders. The appearance of the optic disc (i.e., edema, pallor, or cupping) is crucial in determining the cause of visual loss, as is evident in the discussion of specific disorders in the following section.19
The list of differential diagnoses for optic disc edema, or swelling, is long (Table 13-1). A variety of mechanisms such as ischemia, inflammation, metabolic disorders, and pressure differentials may produce stasis of axonal flow, which causes swelling of the axons anterior to the lamina cribrosa and elevation of the optic disc. The normally transparent peripapillary nerve fiber layer gradually opacifies and obscures the retinal vessels. The disc margins become indistinct. The optic nerve may become hyperemic as small vessels are dilated, and characteristic splinter hemorrhages may appear at the disc margin in the nerve fiber layer. In addition, deeper hemorrhages may appear in the peripapillary retinal and subretinal layers. The swelling can also compromise venous outflow by enlarging the central veins at the disc, causing tortuosity, and producing retinal hemorrhages near the optic disc (Fig. 13-E2).20 The most common causes of optic disc edema include papilledema (from elevated intracranial pressure), AION, and demyelinating optic neuritis. A common clinical challenge is distinguishing true, pathologic optic disc swelling from anomalous but otherwise normal optic discs.21
Optic atrophy is the final common pathway of optic nerve disease. Virtually all optic nerve insults eventually evolve to optic disc pallor or cupping, or both. Optic disc cupping is enlargement of the central cup as a result of loss of axons; this form of optic atrophy (without pallor of the remaining neuroretinal rim) is characteristic of glaucoma, but it can also be caused by other optic nerve disorders (Fig. 13-E3). Optic nerve pallor refers to a whitish appearance of the normally pink neuroretinal rim (Fig. 13-E4). Some forms of atrophic disc changes suggest their cause, such as the segmental pallor in AION or the temporal pallor typically present in toxic, nutritional, and hereditary optic neuropathies. However, in most cases, optic disc pallor is not diagnostic. The differential diagnosis is broad and includes all the disorders that initially cause disc edema and many entities that can lead to axonal death without first being manifested as disc swelling. Retrogeniculate insults do not cause optic disc pallor (perinatal events being an exception).
Disorders of the Afferent Visual System
Ocular Diseases
All patients who complain of decreased vision need an ophthalmologic evaluation. Even patients with known disorders that can potentially affect vision deserve a thorough ophthalmic examination if their vision changes. For example, in a patient known to have an optic nerve sheath meningioma, unrelated retinal detachment may develop. Anterior segment and retinal disorders are not always obvious on a cursory eye examination and may mimic optic nerve or intracranial disease.22 A few selected ocular disorders that may be confused with neurological vision loss are discussed in this section.
Retinal Abnormalities
Macular diseases cause central scotomas or metamorphopsia. Ocular coherence tomography (Fig. 13-E5) is a relatively new noninvasive tool for imaging the macula that has simplified the diagnosis of macular disease, although intravenous fluorescein angiography is still often required. Age-related macular degeneration is a common cause of painless central vision loss in patients older than 50 years; typically, macular pigment changes, whitish macular drusen, or blood is evident with the ophthalmoscope, but the findings may be subtle. Central serous retinopathy causes central scotomas in younger patients (and is often confused with optic neuritis). Epiretinal membranes tend to cause metamorphopsia rather than discrete scotomas and are not always evident on ophthalmoscopy. Macular holes can decrease visual acuity and cause tiny central visual field defects so small that the foveal threshold may be the only abnormal point with automated perimetry. Cystoid macular edema can occur in association with diabetes, uveitis, and retinitis pigmentosa and cause central vision loss. Most of the time, retinal trauma is obvious from the history and fundus examination, but permanent subtle changes from trauma can occur.
Branch retinal artery occlusion causes acute vision loss and focal visual field defects that can be similar to those associated with optic nerve disorders.23,24 Acutely, the fundus examination reveals a whitish yellow opaque area of edematous ischemic retina; frequently, emboli can be seen in the retinal arterioles (Fig. 13-E6).25,26 However, the retinal edema typically clears in days to weeks, with only subtle changes in the caliber of the affected retinal arteriole remaining. Similarly, the retinal edema and “cherry-red spot” from central retinal artery occlusion quickly vanishes but leaves retinal arteriolar narrowing and mild diffuse optic nerve pallor (Fig. 13-E7).
Central retinal vein occlusion27 and branch retinal vein occlusion28 cause marked retinal hemorrhages that are impressive and difficult to miss initially (Fig. 13-E8). Sometimes, venous collateral vessels on the optic disc (opticociliary shunts), tortuous retinal veins, and slight disc pallor remain and mimic the findings of an optic nerve sheath meningioma.
Cancer-associated retinopathy (CAR) is a paraneoplastic syndrome in which autoantibodies are directed against components of the retina; it is usually associated with small cell carcinoma or other visceral malignancies.29–31 The classic triad consists of photosensitivity, ring scotomatous visual field loss, and attenuated retinal arterioles.32 The electroretinogram is typically abnormal, and CAR antibodies may be detected in serum.33,34 A CAR-like syndrome can also occur with melanoma (melanoma-associated retinopathy) and in the setting of systemic autoimmune disorders.35
Papilledema
Elevated intracranial pressure from any cause can be transmitted to the optic nerve head and usually results in bilateral optic disc swelling. There are many causes of optic disc swelling, but the term papilledema refers specifically to the bilateral disc swelling associated with elevated intracranial pressure (Fig. 13-5). The optic disc may be markedly elevated, with hemorrhages of the nerve head and surrounding retina. Usually, there is no visual loss acutely, except for enlargement of the physiologic blind spot from elevation and compression of the peripapillary retina. If acute central visual loss is present, a different diagnosis such as bilateral optic neuritis or bilateral AION (i.e., giant cell arteritis) is more likely. Chronic papilledema can cause loss of the peripheral visual field, with central vision affected only very late in its course.36 The presence of bilateral optic disc edema requires immediate investigation, starting with a blood pressure measurement to evaluate the possibility of malignant hypertension and neuroimaging to rule out an intracranial mass or other abnormality. Normal findings on neuroimaging in the presence of elevated intracranial pressure suggest IIH, also called pseudotumor cerebri.37 IIH typically occurs in obese women between puberty and menopause.38 Men, as well as women who are not overweight, frequently harbor identifiable causes of elevated intracranial hypertension (such as an occult dural arteriovenous malformation, dural venous sinus occlusion, sleep apnea, and other conditions) and should not be considered to have IIH until an exhaustive clinical investigation confirms that there is no identifiable cause. IIH occurs in children, but the same careful scrutiny just noted should be applied to this group as well.39
It is important to understand that all patients with papilledema or known intracranial hypertension must be monitored by an ophthalmologist with serial optic disc evaluations (and photographs) and visual fields. The vision loss with papilledema can be insidious and unappreciated by the patient initially, with severe peripheral visual field loss even in the presence of excellent visual acuity.40
Anterior Ischemic Optic Neuropathy
AION is characterized by sudden, painless loss of vision associated with unilateral optic disc swelling in patients 45 years or older. An infarct of the optic nerve head occurs as a result of occlusion of one or more of the posterior ciliary arteries.41 These vessels originate from the ophthalmic artery in the orbit, enter the globe around the optic nerve, and supply the peripapillary choroid and optic nerve head. AION may occur as a sequela of generalized atherosclerotic disease (i.e., nonarteritic AION)42 or be secondary to vasculitis, most commonly giant cell arteritis (i.e., arteritic AION).43
The most common form of AION is nonarteritic and it is manifested as isolated monocular vision loss. The disc edema and resulting pallor are typically confined to the upper or lower portion of the nerve, with a corresponding altitudinal visual field defect (Fig. 13-6). The visual field defect tends to be permanent, although minimal improvement may occur over time. No treatment has been shown to be effective.
The precipitating mechanisms of this multifactorial event are not fully understood.44 The architecture of the optic disc is an important factor because affected discs are almost always small and cupless. Patients with nonarteritic AION may have systemic vascular diseases such as systemic hypertension (40%) or diabetes mellitus (20%) or systemic manifestations of atherosclerotic disease such as angina pectoris, previous myocardial infarction, intermittent claudication, or a history of stroke.45,46 Hypercholesterolemia is associated with nonarteritic AION in patients 50 years or younger.47 Unilateral or bilateral nonarteritic AION can occur in predisposed patients with hypotensive episodes in the setting of surgery (including spinal cord surgery with induced hypotension) or trauma. The prognosis for vision is not good in this situation, even with prompt correction of hypotension, hypovolemia, and hypoperfusion.48
There is no proven, effective treatment of nonarteritic AION. Optic nerve sheath fenestration, once considered a potential surgical treatment in the past, was formally studied and shown to be ineffective, possibly even harmful.49,50
Thirty percent to 50% of patients have an event in the second eye, usually years later. Most clinicians advocate the daily use of aspirin because it may theoretically decrease the risk for an event in the contralateral eye.51 As with all functionally monocular patients, care should be taken to protect the unaffected eye from trauma with shatterproof polycarbonate lens eyeglasses.
In all cases of AION, it is vital to determine whether there is any evidence of an arteritic cause (e.g., giant cell arteritis). Untreated giant cell arteritis can cause rapid, sequential, or simultaneous blindness in both eyes. For this reason, the erythrocyte sedimentation rate (ESR) and C-reactive protein (CRP) level should be determined for all patients older than 55 years who have AION. If giant cell arteritis is suspected because of an elevated ESR or CRP, or both, or because of symptoms such as headache, scalp and temple tenderness, myalgias, arthralgias, low-grade fever, anemia, malaise, weight loss, anorexia, or jaw claudication,52 oral or intravenous steroid treatment should be instituted immediately.53 In acute cases, the patient may benefit from high-dose intravenous steroids. Biopsy of the temporal artery should follow within days of steroid therapy.54,55 In arteritic AION, the visual loss is usually profound, and the optic nerve is often diffusely swollen and pale (Fig. 13-E9).
Optic Neuritis
Optic neuritis is typically manifested as unilateral visual loss (often described as a skim, scum, blur, haze, cloud, dimness, or washed-out view) in young adults (15 to 45 years old), with women outnumbering men 5 to 1. The vision worsens progressively over a period of several days and is almost always accompanied by retrobulbar pain that is made worse with eye movement (Fig. 13-7). After 1 or 2 weeks, vision begins to recover slowly. In most cases, vision gradually improves over a period of 3 to 12 months, and in more than 80% of patients, recovery is nearly complete.56 Optic neuritis is caused by demyelination of the optic nerve. Because optic neuritis is commonly associated with multiple sclerosis (MS),57–59 it is no surprise that patients may report other past or present neurological symptoms.
