Hospital for Sick Children's, The: Atlas of Pediatric Ophthalmology & Strabismus, 1st Edition

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Strabismus

Alex V. Levin

Thomas W. Wilson

Stephen P. Kraft

David Smith

Linda Calpa

Strabismus can be classified into congenital or acquired forms, as well as comitant versus incomitant entities. Congenital strabismus is generally considered a misalignment that manifests within the first 6 months of life, while acquired forms have their onset after that time period. Comitant strabismus implies that the degree of misalignment is the same in all fields of gaze, contrasting with incomitant strabismus, in which the measured angle of the eye turn varies in the different fields of gaze.

Incomitant strabismus can vary in the horizontal or vertical plane, or both. If a horizontal misalignment (esotropia or exotropia) differs in the upgaze and downgaze positions, this leads to pattern strabismus (including A, V, Lambda, Y, or X patterns). A misalignment, either horizontal or vertical, that changes when shifting from the right to left gaze positions generates a horizontal incomitance. Finally, if a vertical misalignment (hypertropia or hypotropia) changes on fixating from upgaze to downgaze, this is termed a vertical incomitance.

Incomitant strabismus can be classified etiologically into innervational and mechanical forms. Innervational entities include innervation deficits (paresis or palsy), which can be supranuclear, nuclear, or infranuclear. Excess innervation of muscles may also occur. Mechanical causes imply restrictions due to problems within the orbit, and these can include abnormalities in the muscles, soft tissues, or bones, as well as lesions within the socket. Restrictions can be caused by congenital disorders or they can be acquired as a result of trauma, surgery, systemic disorders, or other problems.

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  1. Comitant Strabismus
  2. a) Esotropia
 

Figure 1.1 Infantile Esotropia

Infantile esotropia, also referred to as essential infantile esotropia or by the older term congenital esotropia, presents as a manifest deviation with onset before 6 months of age. The angle of deviation is usually over 30 prism diopters. The eye movements are full in the vertical and horizontal planes except for mildly limited abduction of the right eye. As these children often cross-fixate, using the adducted eye to view the contralateral field rather than abducting the ipsilateral eye, it can be difficult to elicit full abduction. A rapid Doll head maneuver or patching the nontested eye may be required to elicit abduction. Infantile esotropia is also associated with inferior oblique overaction (note left eye in upgaze; also see Fig. 1.31), dissociated vertical deviation (Figs. 1.19 and 1.20), latent nystagmus, and, less commonly, manifest nystagmus.

 

Figure 1.2 Alternating Fixation

The top photo shows that when the right eye fixates there is a left esotropia. The bottom photo shows that when the left eye fixates a right esotropia is present. With alternating fixation the deviation switches back and forth from a left esotropia to a right esotropia. This indicates equal vision in each eye (no fixation preference). If the vision were better in one eye, then covering that eye would result in temporary fixation by the fellow eye. That eye would then revert to the esotropic position as soon as the cover was removed from the better eye as the preferred eye takes up fixation. Note also the position of the corneal light reflex (Hirschberg reflex), which is always more lateral relative to the visual axis in the esotropic eye and more central in the fixating eye.

 

Figure 1.3 Ciancia Variant with Cross-Fixation

One subgroup of infantile esotropia, the Ciancia variant, shows nystagmus on attempted abduction of either eye. When fixating with either eye the child adopts a face turn in order to fixate with the eye in the adducted position: In that position the nystagmus dampens. The left photo shows the child fixating with the right eye in adduction, and the right photo shows him fixating with the left eye in adduction. The marked nystagmus on lateral gaze serves to distinguish the Ciancia variant from the more common cross-fixation of infantile esotropia not associated with nystagmus.

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Figure 1.4 Accommodative Esotropia with and without Glasses

The top photo shows a patient with a large right esotropia. The patient has a hyperopic cycloplegic refraction of +4.00. The bottom photo shows the patient wearing glasses and the correction, in which the eyes are straight. The esotropia is now controlled, confirming that this child has accommodative esotropia. Approximately one third of these patients will always need hyperopic correction (glasses or contact lenses) to maintain straight eyes, one third can be tapered out of their correction, and one third will need strabismus surgery because of the development of a nonaccommodative component.

 

Figure 1.5 Partially Accommodative Esotropia

This girl is wearing glasses that correct all of her hyperopia as measured during atropine refraction. The atropine cycloplegia ensures that the full hyperopic refraction is measured. This is particularly important when correction of the nonatropine cycloplegic refraction does not lead to complete straightening of the eye. While wearing the glasses she has a small residual right esotropia, representing the nonaccommodative portion of her esodeviation. Surgery is required to correct the nonaccommodative portion of the strabismus. The child would still wear spectacles postoperatively to correct the accommodative portion of the deviation to keep the eyes straight.

 

Figure 1.6 Esotropia with Convergence Excess

The top photo shows the patient fixating in the distance, where there is no strabismus. The lower photo shows her fixating at one-third meter on an accommodative target: Her left eye deviates inward. This convergence excess form of esotropia can be a subtype of accommodative esotropia, due to the high accommodative convergence–to–accommodation (AC/A) ratio. Convergence excess may also occur with a normal AC/A ratio. The gradient method of determining the AC/A ratio would distinguish between the two possibilities. If the deviation is reduced to zero or close to zero at near with a reading add, this may also suggest a high AC/A ratio.

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Figure 1.7 Accommodative Esotropia with High Accommodative Convergence–to–Accommodation (AC/A) Ratio Treated with Bifocals

The upper image shows the child fixating on an accommodative target in the near position (one-third meter) while looking through the distance portion (upper segment) of the glasses: There is an esotropia. The lower image shows him looking at the same target, but now through the add (lower segment) at near: The deviation is eliminated. This child has a high AC/A ratio. The bifocal add is correcting the excess deviation that occurs at near. Note that the bifocal is executive style and set high enough so that the child can easily fixate through the add in the near fixation position. It is recommended that the top of the segment be set no lower than the inferior edge of the pupil when the patient is fixating in the distance.

 

Figure 1.8 Bifocals Set Too Low

The upper image shows the bifocal set several millimeters below the lower eyelids. The child is viewing a distance target with full hyperopic correction for his accommodative esotropia: The eyes are straight. The lower image shows the child fixating through the bifocal in the near position. While the add is effective in maintaining good alignment for the excess near deviation (convergence excess, see Fig. 1.6), the child has to use an awkward chin-up head posture to be able to use the bifocal segment. Figure 1.7 demonstrates proper spectacle construction for this disorder.

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Figure 1.9 Pseudoesotropia

The wide flat nasal bridge and the prominent epicanthal folds in this Asian child result in covering of the nasal sclera of the left eye particularly when the child is fixating slightly in right gaze. These features combine to give the impression of an esotropia. However, the corneal light reflexes (Hirschberg reflex) are symmetrically centered in each eye, thus ruling out the presence of a manifest deviation. There is no strabismus on the cover test.

 

Figure 1.10 Negative Angle Kappa

In this photo the patient is fixating with her right eye. However, the light reflex in that eye is located slightly temporal within the pupil when compared to the centered reflex in the left eye, giving the child the appearance of a right esotropia. A cover test will show no movement of the right eye on covering the left eye, indicating that there is no strabismus. The off-centered light reflex persists under monocular conditions in the right eye. This is due to a negative angle kappa: A disparity between the visual axis (joining target and fovea) and the anatomic pupillary axis (joining midpupil to fovea). (Compare to Fig. 1.18, positive angle kappa.)

 

Figure 1.11 Factitious Esotropia

This photo shows a marked symmetrical convergence in a patient who has recently had cycloplegic drops placed in both eyes (note that both pupils are dilated). When the patient is asked to focus on a near target the failed attempt at accommodation induces convergence. The light reflex is symmetric in each eye, so there is no true esotropia: The eyes are aligned when fixating on the near target. Convergence spasm in hyperopic noncyclopleged patients presents with a similar clinical appearance except that the pupils are constricted due to the near synkinesis. Convergence spasm can also be associated with psychological disorders.

  1. b) Exotropia
 

Figure 1.12 Basic Exotropia

This child is fixating with the right eye. There is a left exotropia. The angle of deviation is the same on distance and near measurements, representing a basic exotropia. Note that the corneal light reflex (Hirschberg reflex) now appears more nasal relative to the pupil center as compared to the more central reflex in the fixating right eye. As this is a comitant deviation (same amount of deviation in all positions of gaze), the eye movements of both eyes in all directions are equal and full.

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Figure 1.13 Divergence Excess Exotropia

The top photo shows the patient fixating in the distance: The right eye diverges. The lower photo shows the patient fixating at near, where the eyes are straight. This patient therefore has a divergence excess exotropia. However, if after 45 minutes of occlusion of the right eye the deviation at near increases to equal, or almost equal, the distance measurement, then the patient has a simulated divergence excess exotropia. The implication is that fusional convergence is keeping the eyes straight at near. If the near deviation increases through plus lenses held over the two eyes, then it also indicates the presence of a simulated divergence excess, on the basis of accommodative convergence, which is keeping the eyes aligned at near.

 

Figure 1.14 Convergence Weakness Exotropia

The upper photo shows a young child who has a 10 prism diopter right exotropia while fixating at distance. The lower photo shows the child fixating at near, where the right exotropia is larger. When there are little or no deviation at distance and an exodeviation at near accompanied by a decreased near point of convergence, with reduced convergence amplitudes, the convergence weakness is often termed convergence insufficiency. This form of exodeviation may respond to convergence exercises. Convergence insufficiency can also occur in the absence of an actual exodeviation.

 

Figure 1.15 Sensory Exotropia

The photo shows a patient with a dense cataract in the left eye, which precludes binocular vision. Strabismus is common in older children and adults with long-standing sensory deprivation or vision loss due to cataracts or other eye disorders. In younger children sensory esotropia is more common with an incidence almost equal to sensory exodeviation. Sensory esotropia is rare in older children and adults. Surgical correction of sensory deviations is particularly challenging because in many cases there will be a tendency for the poorly seeing eye to drift out of alignment again.

 

Figure 1.16 Infantile Exotropia

The photo shows an infant with a large-angle right exotropia, which presented before the age of 6 months. Infantile exotropia, also known as essential or congenital exotropia, is much rarer than infantile esotropia (Fig. 1.1). The exodeviation is usually very large, almost always over 40 prism diopters. Infantile exotropia has also been reported in association with various neurologic and developmental disorders.

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Figure 1.17 Exotropia with Refractive Error

The top image shows a child with a left exotropia when she does not wear her myopic spectacles. The bottom image shows that her eyes are straight when she wears her glasses. The improvement is likely due to a combination of accommodative convergence and stronger fusional convergence. Improved control of exotropia can also be seen in patients with moderate or high hyperopia who are given their hyperopic correction. Without glasses the patient may choose not to accommodate fully and the exotropia manifests due to lack of fusion and accommodative convergence. When the patient wears the hyperopic correction, fusional convergence may improve, leading to straight eyes.

 

Figure 1.18 Positive Angle Kappa (Pseudoexotropia)

The top photo shows a patient with an apparent left exotropia. The corneal light reflex in the fixating right eye is central. The bottom photo shows the patient's right eye being covered to force fixation with the left eye, which has a vision of 6/6. However, in both images the light reflex in the left eye remains located slightly nasal within the pupil, giving the child the false appearance of a persisting left exotropia. Pseudoexotropia is particularly common following retinopathy of prematurity complicated by a temporal dragging of the macula. To fixate with the fovea, the eye must be held in a turned-out position as the disparity between the visual and anatomic pupillary axes is exaggerated.

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  1. Dissociated Deviations
  2. a) Dissociated Vertical Deviation
 

Figure 1.19 Unilateral Dissociated Vertical Deviation (DVD)

The upper image shows a right hypertropia when the left eye fixates. The middle image shows the left eye being covered to force fixation with the right eye. In the lower image, the right eye continues to fixate but there is no manifest hypotropia of the left eye, confirming the diagnosis of unilateral right DVD. In dissociated vertical deviations, one eye is moving independently of the other (nonyoked innervation) in contrast to “true” vertical deviations, in which a switch of fixation to the hypertropic eye always results in an equal downward deviation of the fellow eye (yoked innervation). DVD with a downward drift has also been rarely reported.

 

Figure 1.20 Bilateral Dissociated Vertical Deviation (DVD)

The upper photo shows that when the patient fixates with the left eye the right eye drifts upward and outward. The lower photo shows that when she fixates with the right eye the left eye drifts upward and outward. Indirect ophthalmoscopy showed excyclotropia of the hyperdeviated eye in each instance. These findings confirm the presence of bilateral DVD. Note that there is never a hypotropia of the fixating eye when fixation is switched (Fig. 1.19). If a patient presents with a latent or manifest DVD in one eye, patching of the fellow eye for several minutes may bring out a bilateral DVD that was not apparent on initial examination. In side gaze, fixation by the adducting eye can be blocked by the nose, causing that eye to drift upward. To differentiate this from overaction of the inferior oblique (Fig. 1.31), a cross-cover test will fail to show a hypotropia of the abducting eye in DVD.

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  1. b) Dissociated Horizontal Deviation
 

Figure 1.21 Dissociated Horizontal Deviation (DHD)

The upper image shows a child with a right exotropia when he fixates with the left eye. This horizontal deviation becomes manifest when there is a lack of visual attention or a disruption in fusion. In the lower image, the child is fixating with his right eye, yet there is no manifest exotropia of the left eye. There is a symmetric low hyperopic refractive error in the two eyes, leading to symmetric accommodative demand for the two eyes. These findings suggest a right dissociated horizontal exodeviation. Most cases of DHD are exodeviations. Dissociated esodeviations are much less common.

III. Incomitant Strabismus: Patterns

  1. a) A-pattern Strabismus
 

Figure 1.22 A-pattern Exotropia with Overaction of the Superior Obliques

The photos show the nine diagnostic positions of a patient with an exotropia in primary position (center photo). The exotropia increases significantly on direct downgaze, while on upward gaze the deviation is much smaller. The overactions of the superior obliques are evident on gazes into the down-right and down-left positions. There is mild underaction of both inferior oblique muscles evident in the upper right and upper left photos.

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Figure 1.23 A-pattern Exotropia without Overaction of the Superior Obliques

This patient has a small exotropia in primary position (center photo) that is larger on downgaze and less on upgaze. There is no overaction of the superior oblique muscles (lower right and lower left images).

 

Figure 1.24 Head Posture with A-pattern Exotropia

The left photo shows the child with a chin-down head posture, viewing straight ahead with eyes in upgaze. The top right photo shows normal alignment in the upgaze position while the bottom right photo shows a large exotropia on downgaze. The chin-down position allows the child to maintain binocular vision.

 

Figure 1.25 A-pattern Esotropia with Overaction of the Superior Obliques

This patient shows an esotropia in primary position (center photo). The esotropia is markedly reduced on downgaze and increases significantly on upgaze. The superior obliques are overacting as seen in the lower right and lower left gaze positions where the adducting eye is relatively hypotropic. The inferior oblique muscles are underacting, as seen in the upper right and upper left gaze positions where the adducting eye is also relatively hypotropic.

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Figure 1.26 A-pattern Esotropia without Overaction of the Superior Obliques

This patient has an esotropia in primary position (center photo) that is markedly reduced on downgaze and increases significantly on upgaze. However, the superior and inferior oblique muscle actions are normal.

 

Figure 1.27 Head Posture with A-pattern Esotropia

The photos show the chin-up posture adopted by a child with A-pattern esotropia. The esotropia is reduced somewhat by wearing his hyperopic glasses (partially accommodative esotropia, Fig. 1.5). As a result, the chin position with spectacles on (left photo) is less severe than the chin-up posturing without glasses (right photo). The anomalous head posture enables the child to retain fusion as the deviation is least in the downgaze field.

  1. b) V-pattern Strabismus
 

Figure 1.28 V-pattern Exotropia with Overaction of the Inferior Obliques

These photos show a patient with exotropia in primary position (center photo). The exodeviation is greatest on upgaze and is almost eliminated on downgaze. The inferior oblique muscles are overacting as seen in the upper right and upper left gaze positions where the adducting eye is relatively hypertropic. In addition, there is some underaction of both superior obliques, as seen in the lower right and lower left gaze positions where the adducting eye is also relatively hypertropic.

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Figure 1.29 V-pattern Exotropia without Overaction of the Inferior Obliques

This child has exotropia in primary position (center photo). The exodeviation is greatest on upgaze and reduces to zero on downgaze. The inferior oblique muscles are acting normally as seen in the upper right and upper left images.

 

Figure 1.30 Head Posture with V-pattern Exotropia

The left photo shows the chin-up posture adopted by this child with V-pattern exotropia. The top right photo shows the child's large exotropia on upgaze. The lower right photo shows the normal alignment in downgaze. With the chin elevated the child is able to view straight ahead with eyes in downgaze, thus maintaining normal ocular alignment and good binocular vision.

 

Figure 1.31 V-pattern Esotropia with Overaction of the Inferior Obliques

This child has a small esotropia in primary position (center photo). The esodeviation is greatest on downgaze and reduces to zero on upgaze. The inferior oblique muscles are overacting, as seen in the upper right and upper left gaze positions where the adducting eye is hypertropic. In addition, there is some underaction of both superior obliques as seen in the lower right and lower left gaze positions where the adducting eye is, again, hypertropic.

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Figure 1.32 V-pattern Esotropia without Overaction of the Inferior Obliques

This child's small esotropia in primary position (center photo) increases on downgaze and decreases on upgaze. The inferior oblique muscles are acting normally, as are the superior obliques.

 

Figure 1.33 Head Posture with V-pattern Esotropia

The photo shows an older boy with an extreme chin-down posture due to V-pattern esotropia caused by bilateral superior oblique paresis. There was a large esotropia in primary position, which increased in downgaze, associated with excyclotropia. Only in his preferred head position, where he is fixating in extreme upgaze, can he regain fusion.

  1. b) Other-pattern Strabismus
 

Figure 1.34 Y-pattern Strabismus

This patient has straight eyes in primary position (center photo) and in downgaze. There is a large exotropia in upgaze. On looking up and to the right (upper left photo), the left eye is abducted, and on looking up and to the left (upper right photo), the right eye is abducted. Y-pattern strabismus can be caused by tightness or inferior malposition of the lateral rectus muscles or, occasionally, by overaction of the inferior obliques.

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Figure 1.35 Lambda-pattern Strabismus

This patient has a small exotropia in primary position (center photo) that measures the same in upgaze. There is a much larger exotropia in the downgaze position. On looking down and to the right (lower left photo) and down and to the left (lower right photo), the superior obliques appear to overact. However, this pattern can also be caused by superior malpositions of the lateral rectus muscles.

 

Figure 1.36 X-pattern Strabismus

This patient has an exotropia in primary position (center photo), which increases significantly on both upgaze and downgaze. There is mild limitation of adduction of each eye (center right and center left photos). There are apparent overactions of both the superior and inferior obliques in each eye, although this feature can also be caused by overrotation of the globes within the orbits due to a lack of full adduction. This pattern is most commonly seen in long-standing exotropia where the lateral rectus muscles have become contractured, a condition termed the tight lateral rectus syndrome.

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  1. Incomitant Strabismus: Paretic
  2. a) Grading Ocular Muscle Actions
 

Figure 1.37 Grading Abduction Deficits (Courtesy of W.E. Scott, MD)

This composite figure shows various degrees of abduction limitation in the left eye ranging from normal abduction (grade 0) to complete failure of abduction (grade –4). The upper right picture shows normal abduction (0). The upper left picture shows some lateral rectus weakness (–1), consistent with approximately 25% limitation. In the lower panel, from left to right, the photos show 50% limitation (–2), 75% limitation (–3), and total (100%) limitation (–4). The designations for adduction limitations (not shown) are done in a similar fashion. Limitations of adduction or abduction must be correlated with monocular movements of the eyes (ductions) to ensure that there is no pseudolimitation brought on by fixation with the fellow eye.

 

Figure 1.38 Grading Inferior Oblique Actions (Courtesy of W.E. Scott, MD)

This figure shows nine grades of right inferior oblique action. The center photo shows normal (0) action. The underactions are mild (grade -1, left center), 50% limitation (-2, lower left), 75% limitation (-3, lower center), and total limitation (-4, lower right). The overactions are mild (+1, right center), moderate (+2, upper right), severe (+3, upper center), and complete (+4, upper left).Another way to grade under- and overaction of the oblique muscles is to equate one grade with 1 mm of difference in the inferior limbus (for inferior oblique grading) and superior limbus (for superior oblique grading) between the eyes. For example, if in adduction the right inferior limbus is 2 mm higher than the left inferior limbus, then the right eye is designated to have +2 overaction.

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Figure 1.39 Grading Superior Oblique Actions (Courtesy of W.E. Scott, MD)

This figure shows the nine grades of right superior oblique action: four grades of overaction (+1 to +4), normal action (0), and four grades of underaction (-1 to -4). The superior oblique action is graded in the same fashion and in the same array as for the inferior oblique (Fig. 1.38). Note that in cases of extreme overaction, the affected eye abducts in downgaze in addition to extreme depression(upper left photo).

  1. b) Third Nerve Paresis (Oculomotor Nerve Paresis)
 

Figure 1-40 A: Complete Third Nerve Palsy

This patient with a right third nerve palsy is fixating with his left eye in the primary position. There is severe right ptosis.

 

Figure 1-40 B: Complete Third Nerve Palsy

This figure shows the nine diagnostic positions of gaze, with the ptotic right upper eyelid held up to show the eye movements. In the center image of the figure, he shows a right large-angle exotropia and right hypotropia. The right pupil is dilated and nonreactive with loss of accommodation due to paresis of the parasympathetic fibers, which originate in the Edinger-Westphal nucleus in the midbrain and travel to the eye with the inferior division of cranial nerve III. There are complete adduction and elevation deficits, and the depression of the eye is limited. The origin of the third nerve palsy is likely intracranial as all branches are involved. Possible causes include trauma, tumor, and vascular malformation. New onset of a nontraumatic third nerve palsy should lead to neurologic evaluation. When the pupil is spared the cause is usually due to a vasculopathic cause such as diabetes, but a neurologic assessment is still recommended.

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Figure 1.41 Congenital Third Nerve Palsy

A 3-month-old infant with congenital third nerve palsy shows an exotropia and hypotropia of the right eye along with ptosis. In children who are otherwise normal, birth trauma or intrauterine insults are the likeliest causes. Amblyopia is commonly seen in these children.

 

Figure 1.42 Paresis of Inferior Division of Third Cranial Nerve

Photos of nine diagnostic positions show a right eye with an exotropia along with a right hypertropia (rather than a hypotropia) in primary position (center photo). The eye has mildly limited adduction and a severe limitation of depression. Elevation is slightly limited only in the adducted position, as the superior rectus muscle still functions. There is no ptosis. The pupil is slightly dilated. This is most often caused by viral illness, neoplasm, or trauma.

 

Figure 1.43 Paresis of Superior Division of Third Nerve

This patient with a paresis of the superior division of the left third nerve has a left hypotropia in primary position (center photo).There is also left ptosis due to paresis of the levator palpebrae. The eye is unable to elevate in all upgaze fields due to the paretic left superior rectus muscle. Causes include meningitis and trauma.

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Figure 1.44 Aberrant Regeneration of Third Nerve: Pseudo von Graefe Sign

This patient has a chronic right third nerve paresis with right ptosis. On attempted adduction and depression of the right eye the right upper eyelid elevates, indicating aberrant regeneration between the right levator palpebrae muscle and the inferior division of the involved third nerve: Stimulation of the inferior division through attempted use of the inferior or medial rectus results in simultaneous contraction of the levator palpebrae. The aberrant innervation can occur within several weeks of the insult to the nerve. Causes include trauma or a space-occupying lesion, such as a tumor or aneurysm in the cavernous sinus.

 

Figure 1.45 Aberrant Regeneration of the Third Nerve: Pupil Involvement

This patient has old bilateral third nerve paresis, in which the right paresis has almost recovered. There is aberrant regeneration in the right eye involving the pupil: The pupil is dilated, but it constricts on gaze to the left and on downward gaze, indicating aberrant regeneration between the pupil constrictor fibers and the nerves to the medial and inferior rectus muscles (inferior division of third cranial nerve). If the history does not suggest trauma as a cause, then investigation for a tumor or aneurysm should be undertaken.

  1. c) Fourth Nerve Paresis (Superior Oblique Paresis)
 

Figure 1.46 Three-step Test (Including Bielschowsky Head-tilt Test)

The top image shows an incomitant vertical deviation in the horizontal plane, with a left hypertropia in primary position (upper center photo). The causative weak vertical muscle can be one of the depressors of the left eye (superior oblique or inferior rectus), or one of the elevators of the right eye (inferior oblique or superior rectus). The deviation decreases in left gaze and increases in right gaze, thus isolating the possible weak muscles to the left superior oblique or the right superior rectus as these muscles have their principal vertical actions on right gaze. In the bottom images, we see the same patient on head tilt to the right and left shoulders. There is no hypertropia on tilting to the patient's right, but there is a large left hypertropia on tilting to the left. This indicates a positive head-tilt test. It is also termed a positive Bielschowsky head-tilt test, or a significant head-tilt difference. The findings isolate the candidate muscle to an incyclotorter of the left eye (which still implicates the left superior oblique) or one of the excyclotorters of the right eye (neither of which was a candidate muscle). Therefore, of the two candidate muscles isolated in the second step, the left superior oblique is confirmed as the weak muscle.

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Figure 1.47 Unilateral Superior Oblique Paresis

This patient has a left hypertropia that worsens in the right gaze position and decreases in left gaze. There is a V pattern with an esotropia in downgaze. The left superior oblique muscle is underacting, and its antagonist, the left inferior oblique muscle, is overacting. In the lower panel the center photo shows the compensatory head posture consisting of a right head tilt and slight right face turn. The right and left images in the bottom panel show the positive head-tilt test, with a left hypertropia on left tilt that vanishes on right tilt, confirming the diagnosis of a left superior oblique paresis. Superior oblique palsy may be congenital or acquired. Patients with congenital superior oblique palsy may not be diagnosed until they are no longer able to maintain fusion and begin to experience diplopia and/or show a manifest strabismus in the primary position. Old photographs may show long-standing compensatory head tilt and facial asymmetry. These patients may have markedly enlarged vertical fusional amplitudes. Common causes of acquired fourth cranial nerve palsy include head trauma and intracranial tumors.

 

Figure 1.48 Bilateral Superior Oblique Paresis

Bilateral superior oblique paresis may be suspected in the presence of a reversing hypertropia: A right hypertropia on left gaze and a left hypertropia on right gaze. These deviations are most noticeable on downgaze to the right and left. There is large V pattern, with an esotropia in downgaze and exotropia in upgaze. Both superior oblique muscles are underacting. The bottom left photo shows right hypertropia on right head tilt, while the bottom right photo shows a left hypertropia on left head tilt, thus confirming the diagnosis of bilateral superior oblique paresis. In the primary position the eyes may be orthotropic or a hypertropia in the eye with an asymmetrically worse superior oblique palsy may be seen. Differential diagnoses include alternating skew deviation (Fig. 1.68), craniofacial syndromes with exorbitism (Chapter 14: Craniofacial), primary overaction of the inferior obliques (Fig. 1.28), and bilateral dissociated vertical deviation (Fig. 1.20).

 

Figure 1.49 Fallen Eye Syndrome

This patient has a left superior oblique paresis. When the patient fixates with the paretic left eye, it causes a right hypotropia that is incomitant. The right eye becomes significantly more hypotropic on right gaze (the field of action of the left superior oblique), and this down-drift is termed a “fallen eye.” The presence of a fallen eye may indicate an oblique muscle problem in the fixating eye. If the patient fixates with the nonparetic eye, the hypertropia in the paretic eye (the primary deviation) may be less than the hypotropia seen when fixing with the paretic eye (the secondary deviation).

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Figure 1.50 Fundus Excyclotropia

The upper two photos show bilateral fundus excyclotropia, with the foveae lying at levels below the lower edges of the optic discs. Normally the foveal reflexes lie at levels even with the lower one third of the disc. The lower two photos show reorientation of the foveae close to their normal positions following bilateral modified Harada-Ito procedures to correct the excyclotropia. This reorientation can be observed on the operating room table as the procedure is performed.

  1. d) Sixth Nerve Palsy (Lateral Rectus Paresis)
 

Figure 1.51 Total Unilateral Sixth Nerve Palsy

The upper image shows a child with a left sixth nerve palsy adopting a large left face turn in order to maintain fusion by placing his eyes in right gaze to maintain alignment. In the bottom images, the child's head is being held in the primary position where there is a left esotropia. The deviation increases markedly in left gaze due to the failure of abduction. The angle decreases almost to zero in right gaze. In children, common causes of a sixth cranial nerve palsy include increased intracranial pressure from tumor or trauma and inflammation of the petrous portion of the temporal bone following otitis media (Gradenigo syndrome). Sixth cranial nerve palsy must be distinguished from Duane syndrome (Fig. 1.59).

 

Figure 1.52 Partial Unilateral Sixth Nerve Paresis

The photos of the horizontal gaze positions show a partial limitation of abduction of the left eye, consistent with a partial sixth nerve paresis. As in a complete sixth cranial nerve palsy, there is an esotropia in primary position (center photo), which is incomitant, increasing on ipsilateral gaze (lower photo) and decreasing on contralateral gaze (upper photo). The patient may adopt a face turn to the affected side, but the degree of face turn will be less than that seen in a complete sixth cranial nerve paresis (Fig. 1.51). Likewise, the esotropia in primary position will also be smaller.

 

Figure 1.53 Bilateral Sixth Nerve Palsy

The presence of a very large bilateral esotropia in primary position (center photo) with a complete failure of abduction of each eye on side gazes (upper and lower photos) is a characteristic of a bilateral sixth nerve palsy. The differential diagnoses include infantile esotropia (Fig. 1.1), in which abduction can be improved significantly by Doll eye maneuvers; bilateral Duane syndrome (Fig. 1.60), in which the primary position esotropia is much smaller and characteristic co-contraction on adduction is seen in both eyes; strabismus fixus following a history of long-standing esotropia; the Ciancia variant of the infantile esotropia syndrome (Fig. 1.3); and factitious esotropia (Fig. 1.11). The patient may adopt a face turn to either side not to attain fusion, but rather to see straight ahead with an eye that otherwise cannot abduct well enough to get to the midline (primary position).

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  1. c) Multiple Cranial Nerve Paresis
 

Figure 1.54 Combined Fourth and Sixth Nerve Pareses

In primary position (center photo) this patient has a right esotropia and right hypertropia. There is a limitation of abduction due to a right sixth nerve paresis (center left), along with limitation of depression in the adducted position (bottom right) due to the concurrent right fourth nerve paresis. The right inferior oblique muscle is overacting (upper right). The three-step test (Fig. 1.46) cannot be applied if the third cranial nerve is one of the affected nerves. The presence of multiple simultaneous cranial nerve palsies should lead one to consider meningeal processes (meningitis, meningeal carcinomatosis), severe brain injury, demyelinating disease, and Arnold Chiari malformation as possible causes. Myasthenia gravis, orbital trauma, and Graves disease can lead to unusual eye movement patterns that mimic multiple cranial nerve palsies.

  1. f) Double Elevator Paresis
 

Figure 1.55 Double Elevator Paresis

The top photo shows a young child with a right hypotropia and ptosis. The lower six views show limitation of elevation of the right eye in all of the upgaze fields (upper row) and a comitant right hypotropia in the horizontal plane (lower row). Although this entity is commonly referred to as a double elevator palsy (DEP), it is more appropriately called a monocular elevation deficit, as the cause can be an inferior rectus restriction, a supranuclear deficit of elevation (the classic form of DEP), a superior rectus paresis, or a paresis of both elevators. The child adopted a chin-up position (top center inset image) to attain fusion.

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Figure 1.56 Pseudoptosis

In the upper image a patient with a left monocular elevation deficit is fixating with normal right eye. There is a left hypotropia and ptosis. In the lower image, the patient is fixating with the paretic left eye. The upper eyelid is now almost at its normal position. This confirms that the ptosis seen in the top photo is mainly a pseudoptosis due to the hypotropic position of the eye rather than a true paresis of the levator palpebrae, which is not involved in this child's monocular elevation deficit. The lid position is best addressed by repair of the strabismus rather than ptosis surgery.

 

Figure 1.57 Bell Phenomenon

Although this patient has a right monocular elevation deficit, the single bottom image demonstrates the intact Bell phenomenon in that eye: Full upgaze in response to an attempt to open forcibly closed eyelids. This confirms that the elevators of the right eye are, in fact, functioning and that there is no mechanical restriction to upgaze. This suggests that the elevation deficit is of supranuclear origin as seen in the classic double elevator palsy (Fig. 1.55). Note that the Bell phenomenon is an involuntary movement of the eye, as opposed to the voluntary ductions and versions.

  1. g) Inferior Oblique Paresis
 

Figure 1-5 A: Inferior Oblique Paresis

Figure A shows a patient with a left hypertropia in primary position (center image). The hypertropia worsens in left gaze and decreases in right gaze. There is an A-pattern esotropia. The right inferior oblique muscle is underacting (upper right image) and its antagonist, the right superior oblique, is overacting (bottom right image).

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Figure 1-58 B: Inferior Oblique Paresis

Figure B shows the Bielschowsky head-tilt test, with the left hypertropia worsening on left head tilt and lessening on right head tilt. This result confirms the right inferior oblique muscle, an excyclotorter of the right eye, as the weak vertical muscle. Inferior oblique palsy is generally an idiopathic condition, but congenital, traumatic, and vascular causes have rarely been reported.

  1. h) Duane Retraction Syndrome
 

Figure 1.59 Unilateral Duane Syndrome Type I

Duane syndrome is one of the strabismus entities now grouped under the category of congenital cranial disinnervation disorders (CCDDs), which include Moebius syndrome (Fig. 1.73) and congenital fibrosis syndrome (Fig. 1.66). These disorders are all caused by the development of anomalous innervational patterns due to cranial nerve maldevelopment that arises during embryogenesis. This patient has a left esotropia in primary position (center image). She has almost complete failure of abduction of the left eye. On adduction of the affected eye, the eyelid fissure narrows noticeably (center left image), due to retraction of the globe into the orbit. As a result of maldevelopment of the left sixth cranial nerve, reinnervation of the lateral rectus with aberrant fibers from the third cranial nerve causes both the lateral and medial rectus to contract simultaneously on adduction. The adduction of the eye appears full, thus confirming this Duane syndrome as type I.

 

Figure 1.60 Bilateral Duane Syndrome Type I

This patient has bilateral limitations of abduction and bilateral narrowing of the eyelid fissures with globe retraction on adduction to either side (center row). The adduction of each eye is almost full, confirming the diagnosis of bilateral type I Duane syndrome. Notice the near absence of esotropia in primary position (center image), unlike the large esotropia seen in bilateral sixth cranial nerve palsy (Fig. 1.53). In Duane syndrome, neuroimaging and urgent management are rarely required. Several chromosomal aberrations and loci have been associated with Duane syndrome. It may be inherited in an autosomal dominant pattern.

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Figure 1.61 Unilateral Duane Syndrome Type II

This patient has a Duane syndrome of the left eye that produces an incomitant exotropia. The center row of images shows a left exotropia in primary position (center) with limitation of adduction of the left eye and marked retraction causing narrowing of the eyelid fissure, while abduction is full. There is a significant upshoot (upper-left image) and downshoot (bottom-left image) in the adducted position. These findings are consistent with a Type II Duane syndrome. This is the least common among the three classic types of Duane syndrome.

 

Figure 1.62 Unilateral Duane Syndrome Type III

This patient has markedly limited adduction and abduction of the left eye and narrowing of the palpebral fissure on adduction of that eye, consistent with a type III Duane syndrome. The eyes are orthotropic or only minimally misaligned in the primary position. As a result, the patient does not adopt an anomalous head position. In all forms of Duane syndrome, children become unconsciously adept at turning their head from side to side to compensate for their deficient horizontal ductions. As a result, particularly when there is no anomalous head position or strabismus in the primary position, Duane syndrome often goes undiagnosed until later childhood.

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Figure 1.63 Up-shoot and Down-shoot Phenomena in Duane Syndrome

Up-shooting (left image) and down-shooting (right image) in adduction can be seen in all types of Duane syndrome and represent slippage of a tight contracted lateral rectus over the globe or a coinnervation phenomenon involving the lateral and superior rectus or lateral and inferior rectus muscles or, rarely, the lateral rectus and inferior oblique muscles.

  1. Incomitant Strabismus: Restrictive
  2. a) Brown Syndrome
 

Figure 1.64 Unilateral Brown Syndrome

The images show a child with a right congenital idiopathic Brown syndrome. There is a total failure of elevation of the right eye in the adducted position (upper right photo), due to lack of laxity in the superior oblique tendon and its surrounding soft tissues. There is also limited elevation in the straight upward gaze position (upper center image). The action of the right superior oblique in its gaze field (adducted downgaze, lower right image) is normal. There is a V-pattern exotropia. The child may adopt a chin-up position to maintain fusion. Brown syndrome may also be acquired due to trauma or inflammation (e.g., juvenile rheumatoid arthritis). In the latter circumstance, the area of the trochlea may be swollen and tender to palpation.

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Figure 1.65 Bilateral Congenital Brown Syndrome

This patient with bilateral congenital Brown syndrome has markedly limited elevation in the adducted position of both eyes (upper left and upper right images). Each eye shows a mild down-drift (hypotropia) on adduction (center right and left images). There is a V pattern with a large exotropia in the upgaze position (top center image), due to the restrictive anomalies in both superior oblique tendons. The patient may adopt a chin-up position to obtain fusion.

  1. b) Congenital Fibrosis Syndrome
 

Figure 1.66 Congenital Fibrosis Syndrome Type 1 (CFEOM Type 1)

These images show a patient with the most common form of congenital fibrosis syndrome, or CFEOM type 1. The patient is unable to elevate either eye above the midline. In primary position the eyes are ptotic and exotropic; the child is more comfortable fixating in downgaze. The patient will likely use an extreme chin lift in the primary position with or without a face turn. The presence of amblyopia or asymmetry will affect the choice of face position. This syndrome is one example of the group of primary congenital innervational disorders that can lead to severe mechanical restrictions, and which collectively are known as the congenital cranial disinnervation disorders (CCDDs). Other entities included among the CCDDs are Duane syndrome (Figs. 1.59, 1.60, 1.61, 1.62 and 1.63) and Moebius syndrome (Fig. 1.73). Mutations in the kinesin gene (K1F21A) on chromosome 12 result in maldevelopment of the third cranial nerve nuclei and the CFEOM type 1 phenotype, which is transmitted in an autosomal dominant pattern.

 

Figure 1.67 Congenital Fibrosis Syndrome Type 2 (CFEOM Type 2)

These images show a patient with a large exotropia in primary position and limited adduction in each eye. There are also limitations of elevation and depression in both eyes. CFEOM type 2 is due to mutations in the ARIX gene at 11q13, which encodes a transcription factor involved with the development of the nuclei for cranial nerves III and IV. Patients may also show bilateral miosis. There is also another form of this disorder, CFEOM type 3 (not pictured), mapped to 16q24, for which the gene has not yet been cloned.

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  1. Supranuclear Disorders with Strabismus
  2. a) Skew Deviation
 

Figure 1.68 Alternating Hypertropia

Skew deviations are incomitant deviations, which may or may not conform to patterns seen in other established strabismus disorders, due to central nervous system disease. In this patient with a cerebellar tumor, there is a right hypertropia on right gaze (center left image) and a left hypertropia on left gaze (center right image). This should not be confused with the alternating hypertropia of bilateral superior oblique paresis (Fig. 1.48). In the patient pictured here, there is apparent overaction of both superior oblique muscles. However, skew deviation can also manifest itself with apparent underaction of the superior obliques. The patient also had ataxia and nystagmus.

  1. b) Internuclear Ophthalmoplegia
 

Figure 1.69 Internuclear Ophthalmoplegia with Exotropia

The images show the horizontal versions of a patient with a left internuclear ophthalmoplegia (INO) caused by a demyelinating disorder. There is a left exotropia in primary position (center image) and limited adduction of the left eye (left image). Clinically, the patient showed a jerk nystagmus of the right eye in the right gaze direction. INO can occur with or without an exotropia in primary position. The lesion is located in the medial longitudinal fasciculus on the left side, which contains an interconnecting neuron joining the right sixth nerve nucleus with the left medial rectus subnucleus.

 

Figure 1.70 Wall-eyed Bilateral Internuclear Ophthalmoplegia (WEBINO) Syndrome

This patient has bilateral internuclear ophthalmoplegia and a large exotropia, or WEBINO syndrome, caused by a cerebrovascular occlusive event. There is markedly limited adduction of each eye. There was a jerk nystagmus of the abducting eye on both lateral gazes. Such cases arise due to damage to both medial longitudinal fasciculi, leading to disconnection between both sixth nerve nuclei and their connections to the contralateral medial rectus subnuclei. This syndrome is caused by extensive lesions in the brainstem.

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VII. Miscellaneous Disorders

  1. a) Ophthalmoplegias
 

Figure 1.71 Fisher Syndrome

Fisher syndrome is an infrequent variant of the Guillain-Barré syndrome, consisting of a triad of ataxia, areflexia, and ophthalmoplegia without concurrent peripheral neuropathy. This patient has Fisher syndrome following an upper respiratory illness, which is the most common cause. The differential diagnoses include brainstem stroke, pituitary apoplexy, diphtheria, and cerebral sinus thrombosis. There is a partial ophthalmoplegia that includes limited abduction in the right eye and limited abduction, elevation, and adduction in the left eye. There is a mild ptosis of the left upper eyelid.

 

Figure 1.72 Chronic Progressive External Ophthalmoplegia (CPEO)

This woman has bilateral limited horizontal and vertical ductions and ptosis due to CPEO. The elevation and adduction of each eye are most severely affected. The most common subset of CPEO is the Kearns-Sayre syndrome, which has an onset in the first or second decade of life and is due to deletions in mitochondrial DNA. Patients show a progressive ptosis and external ophthalmoplegia, and they develop a salt-and-pepper pigmentary retinopathy and cardiac conduction deficits. This patient did not show any evidence of retinopathy or heart conduction problems.

  1. b) Moebius Syndrome
 

Figure 1.73 Moebius Syndrome

The center image shows the presence of a small right esotropia in primary position and hypoplastic facial muscles. The seventh cranial nerves were weak on both sides (facial diplegia). There is complete failure of abduction of both eyes, but the vertical ductions are normal. Moebius syndrome is another strabismus entity in the overall category of congenital cranial disinnervation disorders, which include Duane syndrome (Figs. 1.59, 1.60, 1.61, 1.62 and 1.63) and congenital fibrosis syndrome (Figs. 1.66 and 1.67). In addition to the eye muscle and facial nerve anomalies, any of the lower cranial nerves can be involved.

 

Figure 1.74 Moebius Syndrome—Nonocular Findings

Moebius syndrome may be associated with limb anomalies such as the abnormal right forearm (phocomelia) shown here (left photo).The patient also had a hypoplasia of the ipsilateral pectoralis muscle (Poland syndrome). One or both sides of the tongue may appear crenulated due to hypoplasia of the 12th cranial nerve (hypoglossal nerve). In this patient the left side of the tongue is affected (right photo). Several chromosomal loci have been associated with Moebius syndrome. It may be inherited as an autosomal disorder with variable expression.