Ординатура / Офтальмология / Английские материалы / Handbook of Pediatric Strabismus and Amblyopia_Wright, Spiegel, Thompson_2006

right eye is fixing (Fig. 3-21A). The paretic eye receives the same1 innervation and turns in slightly because the left lateral rectus muscle is slightly weaker than its antagonist, the left medial rectus muscle. The secondary deviation is larger because the weak left lateral rectus muscle must receive a tremendous amount of innervation ( 4) to bring the left eye into primary position when the paretic eye fixates (Fig. 3-21B). Both the paretic left lateral rectus and its yoke muscle, the right medial rectus, receive 4 innervation because of Hering’s law. This excess drive to the healthy right medial rectus muscle causes a large secondary nasal deviation of the right eye. This same mechanism of primary and secondary deviations also applies to restrictions.

Primary overaction of oblique muscles can also cause incomitance. What we clinically refer to as primary muscle overaction, however, may actually represent a previous paresis of the antagonist and secondary overaction of the agonist muscle.

References

1.Archer SM. Stereotest artifacts and the strabismus patient. Arch Clin Exp Ophthalmol 1988;226:313–316.

2.Burden AL. The stigma of strabismus. Arch Ophthalmol 1994;112: 302.

3.Clarke WN, Noel LP. Stereoacuity testing in the monofixation syndrome. J Pediatr Ophthalmol Strabismus 1990;27:161–163.

4.Donzis PB, et al. Effect of binocular variations of Snellen’s visual acuity on Titmus stereoacuity. Arch Ophthalmol 1983;101:930–932.

5.Kushner BJ. Exotropic deviations: a functional classification and approach to treatment. Am Orthopt J 1988;38:81–93.

6.Levy NS, Glick EB. Stereoscopic perception and Snellen visual acuity. Am J Ophthalmol 1974;78:722–724.

7.Parks MM. The monofixation syndrome. Trans Am Ophthalmol Soc 1969;12(42):1246.

8.Reincke RD, Simons K. A new stereoscopic test for amblyopia screening. Am J Ophthalmol 1974;78:714–721.

appropriate binocular visual stimulation. Requirements for normal binocular visual development include clear and equal retinal stimulation and proper eye alignment (see Table 4-1).

Binocular vision and fusion have been found to be present between 1.5 and 2 months of age,4,26 while stereopsis develops later, between 3 and 6 months of age.2,3,17 This author cared for a patient with a transient congenital sixth nerve palsy who presented at 3 weeks of age with a compensatory face turn to obtain binocular fusion. This single case suggests that early motor fusion may be present as early as 3 weeks of age.

NEONATAL ALIGNMENT

Eye alignment is variable during the first few weeks of life. In a study by Sondhi et al.39 of 2271 newborns, 67% showed an exodeviation, 30% had essentially straight eyes, 2% swung between esoand exodeviations, and only 1% had an esodeviation. By 2 months of age, all the esodeviations resolved, and 97% of exodeviations cleared by 6 months. Thus, almost all newborns have straight eyes or an exotropia, but esotropia is rare. The presence of an exodeviation at birth allows our innate strong fusional convergence to align the eyes. An esotropia, on the other hand, is more difficult to control because fusional divergence is weak.

EYE MOVEMENT DEVELOPMENT AND SMOOTH PURSUIT ASYMMETRY

Neonates typically have sporadic, jerky eye movements made up of saccadic eye movements without smooth pursuit. Initially, saccades are hypometric, but they continue to improve throughout infancy and childhood. Smooth pursuit eye movements develop after 4 to 6 weeks of age, with most infants having accurate smooth pursuit by 2 months of age. Horizontal smooth pursuit develops for targets moving in a temporal to nasal direction before pursuit movements in a nasal to temporal direction develop. This developmental lag in nasally directed smooth pursuit is called smooth pursuit asymmetry and is only seen under monocular conditions with one eye covered. During development, nasal to temporal pursuit movements are hypometric, requiring saccadic intrusion eye movements to keep up

with the moving target.1 Smooth pursuit asymmetry can be detected clinically by testing monocular optokinetic nystagmus (OKN). Neonates will show a diminished OKN response with the drum rotating nasal to temporal as compared to temporal to nasal. Normally, smooth pursuit asymmetry becomes symmetrical between 4 to 6 months of age.31,32 If binocular visual development is disrupted during the first few months of life (e.g., congenital esotropia and a unilateral cataract), smooth pursuit asymmetry and OKN asymmetry will persist throughout life.12,41,42,54,55 Smooth pursuit asymmetry does not interfere with normal visual function or the ability to read, as it is not present under binocular viewing. It is, however, an important phenomenon that shows a physiological link between ocular motor development and the development of binocular vision.

VISUAL DEVELOPMENTAL MILESTONES

Central fixation and accurate smooth pursuit are important clinical milestones of normal visual development (Table 4-2). Most children will show central fixation and accurate smooth pursuit eye movements by 2 to 3 months of age, but some infants may show delayed visual maturation. Poor fixation at 6 months of age is usually pathological, and should prompt a full evaluation

TABLE 4-2. Important Visual Developmental Milestones.

for oculomotor or afferent visual pathway disease, including electrophysiology and neuroimaging studies.

Abnormal Visual Development

A unilateral or bilateral blurred retinal image or strabismus will disrupt early visual development and can cause permanent visual loss. Following is a discussion of cortical suppression and amblyopia.

CORTICAL SUPPRESSION

Strabismus, or a monocular blurred retinal image, causes dissimilar retinal images to fall on corresponding retinal areas of each eye. If the dissimilarity between the retinal images is great and the images cannot be fused, the visually immature adapts by inhibiting cortical activity from the blurred or deviated eye. This cortical inhibition usually involves the central portion of the visual field and is termed cortical suppression. Images that fall within the field of cortical suppression are not perceived, forming an area called a suppression scotoma. Suppression only occurs during binocular conditions with the dominant eye actively viewing or “fixating” and disappears when the dominant eye is occluded. Suppression has been shown to reduce the first positive peak (P-1) of the pattern visual evoked potential (P.VEP) (Fig. 4-2).58 The P-1 reflects early visual processing at the level of striate cortex, so it is likely that suppression occurs at, or before, the primary visual cortex. In Figure 4-2B, both eyes are open and the dominant eye is fixing whereas the nondominant eye is stimulated with the pattern. There is no P-1 response from the nondominant eye because the visual activity from the fixing eye cortically suppresses visual activity from the nondominant eye. Note that (in Fig. 4-2C) if the dominant eye is occluded in a patient with esotropia, there is no suppression and a high-amplitude P-1 is recorded from the nondominant eye.

Cortical suppression interferes with the development of binocular cortical cells, resulting in abnormal binocular vision and poor, or no, stereoscopic vision. If suppression alternates between eyes, visual acuity will develop equally, albeit separately without normal binocular function. Constant suppression of one eye, on the other hand, not only results in poor binocularity but also causes poor vision (i.e., amblyopia).

speaking, amblyopia can refer to poor vision from any cause but, in this volume and in most ophthalmic literature, amblyopia refers to poor vision caused by abnormal visual development secondary to abnormal visual stimulation. Other terms for this type of amblyopia include functional amblyopia and amblyopia ex anopsia. Children are susceptible to amblyopia between birth and 7 years of age.25 The earlier the onset of abnormal stimulation, the greater is the visual deficit. The critical period for visual development is somewhat controversial but probably ranges from 1 week to 3 months of age. For practical purposes, amblyopia is defined as at least 2 Snellen lines difference in visual acuity between the eyes, but amblyopia is truly a spectrum of visual loss, ranging from missing a few letters on the 20/20 line to hand motion vision.

Functional amblyopia, or “amblyopia,” should be distinguished from organic amblyopia, which is poor vision caused by structural abnormalities of the eye or brain that are independent of sensory input, such as optic atrophy, a macular scar, or anoxic occipital brain damage. Functional amblyopia is reversible when treated with appropriate visual stimulation during early childhood, whereas organic amblyopia does not improve by visual stimulation.

Pathophysiology and Classification of Amblyopia

Amblyopia is caused by abnormal visual stimulation during visual development, resulting in abnormalities in the visual centers of the brain. There are two basic forms of abnormal stimulation: pattern distortion (i.e., blurred retinal image) and cortical suppression (i.e., constant suppression of one eye). Pattern distortion and cortical suppression can occur independently or together to cause amblyopia in the visually immature. Amblyopia can be created by blurring one or both retinal images or by inducing strabismus in visually immature animals (Fig. 4-3). Strabismus will cause amblyopia in infant animals if the animal fixates with one eye and constantly suppresses the fellow eye. Strabismic animals that alternate fixation do not develop amblyopia; however, they do not develop binocular vision. Pathological changes associated with induced amblyopia in the animal model occur in the lateral geniculate nucleus (LGN) and the striate cortex.20,21,23,24,44,48,49 Figure 4-4 shows the pathological changes in the lateral geniculate nucleus of a monkey raised

with a monocular blurred retinal image. Normally, there are six nuclear layers of the LGN: three layers corresponding to the right eye and three layers corresponding to the left eye. Because of the blurred retinal image, only three layers corresponding to the eye with the clear retinal image developed. Due to the increased visual stimulation of the good eye, these three layers are darker stained and larger than normal.57 Ocular dominance columns in the striate cortex are also damaged as a result of a unilateral blurred image during early development (Fig. 4-4B).21 Von Noorden46,47 bridged the gap between human and animal research when he identified similar neural anatomic changes in a pathological study of humans with anisometropic amblyopia and strabismic amblyopia. Thus, this evidence has shown that the poor vision found with amblyopia is caused by brain damage.

Clinically, amblyopia is associated with strabismus and strong ocular dominance (monocular suppression), a unilateral blurred retinal image secondary to refractive error or media opacity (pattern distortion and suppression), and bilateral blurred retinal images (bilateral pattern distortion). Table 4-3 lists a classification of amblyopia based on etiology.

Strabismic Amblyopia

Amblyopia can occur in patients with a constant tropia who show strong fixation preference for one eye and constantly suppress cortical activity from the deviated eye. Amblyopia can also occur despite the fact that both eyes have clearly focused retinal images. Patients with strabismus who alternate fixation and alternate suppression do not have amblyopia, but they do have abnormal binocular function. The mechanism for strabismic amblyopia is constant cortical suppression that degrades neuronal connections to the deviated eye. Strabismic amblyopia occurs in approximately 50% of patients with congenital esotropia (a constant tropia), but is very uncommon in patients with intermittent strabismus (e.g., intermittent exotropia) or those with incomitant strabismus (e.g., Duane’s syndrome and Brown’s syndrome) as they maintain central fusion by adopting a compensatory face turn. Strabismic amblyopia can be moderate to severe, and in some cases even results in visual acuity of 20/200 or worse.