Causes of vertical strabismus in children

INTRODUCTION — Strabismus is the term used to describe an anomaly of ocular alignment. Ocular misalignment can occur vertically, horizontally, or torsionally; it can be congenital or acquired, latent or manifest, constant or intermittent, and fixed or variable depending upon the position of gaze. (See "Evaluation and management of strabismus in children", section on 'Terminology'.)

The causes of strabismus can be classified according to the direction of deviation: inward toward the nose (esodeviations), outward (exodeviations), upward (hyperdeviations), or downward (hypodeviations) (figure 1). (See "Evaluation and management of strabismus in children", section on 'Terminology'.)

Vertical strabismus is usually caused by weakness or restriction of one of the eight extraocular muscles involved in vertical eye positioning (table 1). The two medial and two lateral rectus muscles do not contribute significantly to normal vertical ocular alignment and movement.

The causes of vertical strabismus are reviewed here. The evaluation of strabismus and the causes of horizontal strabismus are discussed separately. (See "Evaluation and management of strabismus in children" and "Causes of horizontal strabismus in children".)

NEUROANATOMY — Although the cyclovertical muscles also have secondary functions, three pairs of extraocular muscles move each eye in three primary directions:

●Vertically – Eye movement in superior and inferior directions (elevation and depression)

●Horizontally – Eye movement medially (adduction) and laterally (abduction)

●Torsionally – Incyclotorsion is when the superior part of the eye rotates nasally around its visual axis; excyclotorsion is when the superior part of the eye rotates temporally around its visual axis

The superior oblique muscle is innervated by cranial nerve IV, the lateral rectus muscle by cranial nerve VI, and all others by cranial nerve III (table 1).

Understanding strabismus requires knowledge of the two major principles that govern ocular motility [1]:

●Agonist muscles in both eyes receive equal innervation to ensure coordinated binocular eye movements. Thus, when the right lateral rectus muscle is activated to abduct the right eye, the left medial rectus muscle is activated equally to adduct the left eye (Hering's law).

●Agonist/antagonist muscle pairs of each eye receive reciprocal innervation [2]. Thus, when the right medial rectus muscle contracts to adduct the right eye, its ipsilateral antagonist, the right lateral rectus muscle, relaxes (Sherrington's law).

HYPERDEVIATIONS — In hyperdeviations, the affected eye is elevated relative to the fellow eye. Trochlear nerve (fourth cranial nerve) palsy is the most common cause of vertical strabismus in childhood.

Trochlear palsy — The trochlear nerve innervates the superior oblique muscle. The actions of the superior oblique muscle are incyclotorsion, depression, and abduction of the eye. Trochlear nerve palsy results in weakness of the superior oblique muscle, which results in hypertropia and excyclotropia of the affected eye. Trochlear nerve palsy can be unilateral or bilateral and congenital or acquired [3]. (See "Fourth cranial nerve (trochlear nerve) palsy".)

Clinical features — Children with unilateral trochlear nerve palsy typically present with the head tilted toward the unaffected side (torticollis), a finding that may be present in old photographs if the palsy is longstanding (picture 1). Tilting the head to the opposite side positions the eyes so that stimulation of the palsied muscle is minimized, resulting in reestablishment of eye alignment, fusion, and binocularity. Torticollis may be the only sign of unilateral trochlear nerve palsy noticed by the parents because affected children rarely complain of diplopia or other visual disturbance.

Additional signs and symptoms of unilateral trochlear nerve palsy include (picture 1):

●Hypertropia of the affected eye in the primary gaze (straight-ahead position). The superior oblique muscle acts to depress the eye, and, when it is weak, the antagonist muscles that elevate the eye predominate. This can cause vertical diplopia.

●Ipsilateral over-elevation in adduction (caused by secondary overaction of the inferior oblique muscle, the ipsilateral antagonist muscle to the superior oblique muscle).

●Ipsilateral under-depression in adduction (the position in which the vertical action of the superior oblique muscle is typically maximal).

●Excyclotorsion of the affected eye, which can cause torsional diplopia (the measurement of which requires special testing by an ophthalmologist).

Bilateral fourth nerve palsies are suggested by the following combined features:

●A relatively small or no hypertropia in the primary position (both eyes have a vertical deviation, which tend to cancel each other out unless asymmetric).

●Alternating hypertropia on opposing horizontal gaze (eg, right hypertropia in left gaze and left hypertropia in right gaze).

●Ipsilateral hypertropia on head tilt (ie, right hypertropia on right head tilt and left hypertropia on left head tilt). This is known as the Bielschowsky head-tilt test and occurs because of increased action of the superior rectus relative to that of the superior oblique muscle, both of which function to incyclorotate the eye with a tilt of head toward the ipsilateral side. In the normal situation, their vertical functions counteract each other, but when the superior oblique muscle is weak, the function of the superior rectus muscle predominates, resulting in elevation of the eye.

●Underaction of both superior oblique muscles and/or overaction of both inferior oblique muscles.

●Chin-down head posture, which allows the person to maintain fusion.

●Complaint of torsional diplopia that is worse in downgaze.

●Esotropia in downgaze (due to loss of the abduction effect of the superior oblique in downgaze).

Making the distinction between congenital fourth nerve palsy and acquired fourth nerve palsy is important. Patients who have congenital fourth nerve palsy do not usually require additional evaluation, whereas patients who have acquired fourth nerve palsy may need neuroimaging to detect an underlying process that requires prompt intervention (eg, increased intracranial pressure [ICP], tumors of the brainstem, or intracranial infection). (See "Fourth cranial nerve (trochlear nerve) palsy", section on 'Causes of isolated fourth nerve palsy'.)

Clinical features of congenital trochlear nerve palsy include:

●Torticollis, or head tilt, from an early age, often apparent in old photographs. When an abnormal head posture is compensatory (ie, allows binocular fusion and/or avoids diplopia), it usually resolves or improves with occlusion of either eye. This test can be particularly useful when a primary care clinician is trying to differentiate compensatory ocular torticollis from other causes of torticollis (eg, fibrosis of the sternocleidomastoid muscle).

●Facial asymmetry with the dependent side of the face being slightly smaller (ie, ipsilateral hemifacial hypoplasia). The distance between the lateral canthus and the angle of the mouth is shorter on the dependent side. The etiology of the facial asymmetry is not known, although gravity and sleeping position have been suggested to play roles [3-5].

●Large vertical fusion amplitudes, sometimes as much as 10 times the normal range. Vertical fusion amplitude measures the ability of the eyes to fuse images that are misaligned vertically. These supranormal amplitudes develop over a long period of time and are not seen in acute acquired deviations.

Management — Management of trochlear nerve palsy depends upon the etiology. Treatment options include strabismus surgery, prism therapy, or the use of orthoptic exercises. Surgery may involve tightening of the superior oblique tendon or weakening of the antagonist inferior oblique muscle or other vertically acting extraocular muscles. Adding prism to spectacles or using orthoptic exercises are less effective forms of intervention, though sometimes useful.

Oculomotor palsy — The oculomotor nerve controls all extraocular muscles except the lateral rectus and superior oblique muscles. Patients with partial oculomotor nerve palsy may have hyperdeviation of the involved eye if the inferior rectus muscle is more involved than are the other extraocular muscles on either eye. However, most patients with oculomotor nerve palsy present with exotropia and/or hypotropia along with ipsilateral ptosis. (See "Third cranial nerve (oculomotor nerve) palsy in children".)

HYPODEVIATIONS — In hypodeviations, the affected eye is lower relative to the fellow eye. Causes of hypodeviation include fractures of the orbital floor or wall, thyroid-related ophthalmopathy, Brown syndrome, oculomotor palsy, trochlear nerve palsy (if fixating with the palsied eye), and congenital fibrosis of the extraocular muscles.

Orbital fracture — Entrapment of the inferior rectus muscle and/or surrounding tissues caused by fractures of the orbital floor results in depression of the involved eye and restriction to elevation of this eye [6]. Fractures of the orbital floor usually are caused by direct blows to the orbit, commonly called "blowout fractures." Orbital fractures can also cause hyperdeviations, but much less commonly than they cause hypodeviations. (See "Orbital fractures".)

Clinical features — Clinical features of inferior rectus entrapment include a hypotropia of the affected eye and limited ability to elevate and/or depress the affected eye. Diplopia may be present in straight-ahead gaze (primary gaze) or may manifest only when the child looks up or down. In addition, enophthalmos caused by displacement of orbital contents into the maxillary sinus may be present. Children also can feel nauseated when attempting to elevate the eyes.

Management — Surgical intervention is necessary in patients who have orbital blowout fractures that are associated with strabismus, limited extraocular motility, and/or significant enophthalmos. However, unless there is a clear indication for emergency surgery (eg, orbital hematoma resulting in orbital compartment syndrome), patients with blowout fractures usually are observed for 7 to 10 days before surgical intervention is performed. The waiting period permits resolution of inflammation and edema, which may result in improved eye movement.

During the observation period, intranasal decongestant sprays and oral antibiotics are often prescribed (to cover for sinus flora). In addition, patients are advised to avoid blowing their nose. These measures are taken to prevent orbital infection and orbital emphysema by limiting the spread of air and sinus flora into the orbit. (See "Orbital fractures", section on 'Initial management'.)

Thyroid-related eye disease — Thyroid-related eye disease is a common cause of vertical strabismus in adults, but it is rare in children. The clinical features, diagnosis, and management of thyroid-related eye disease are discussed in detail separately. (See "Clinical features and diagnosis of thyroid eye disease" and "Treatment of thyroid eye disease".)

Brown syndrome — Brown syndrome, also known as the superior oblique tendon sheath syndrome, is an uncommon form of restrictive vertical strabismus that may be unilateral or bilateral and congenital or acquired (eg, due to trauma or inflammatory disorders such as rheumatoid arthritis). Brown syndrome is characterized by anomalous interaction between the trochlea and the superior oblique muscle tendon, which results in restriction of normal movement of the superior oblique tendon through the trochlea [7].

Clinical features — Children with Brown syndrome have limited ability to elevate the involved eye, particularly when it is adducted (picture 2). They may complain of discomfort when attempting to elevate the involved eye and may or may not have diplopia in primary (straight-ahead) gaze.

Brown syndrome may be difficult to diagnose in infants and young children who often do not cooperate with the examination, which requires a specific oblique gaze position (up and in) to detect. As in Duane syndrome and trochlear nerve palsy, torticollis may be the first indication of Brown syndrome. Affected children usually keep their chin up and head tilted toward the unaffected side to maintain single binocular vision. However, if the affected eye is covered, head position may return to normal. (See 'Clinical features' above.)

Management

●Congenital Brown syndrome – Children with congenital Brown syndrome who have any of the following may require surgical intervention:

•Strabismus in the primary position (straight-ahead gaze)

•Significant torticollis

•Significant anomalous eye movements in side gaze

The surgical procedure involves transection of the superior oblique tendon by tenotomy/tenectomy or lengthening the tendon using a silicone tendon expander or other lengthening procedures [8].

●Acquired Brown syndrome – Acquired Brown syndrome often resolves spontaneously. If it persists, it can be treated with antiinflammatory agents, such as oral nonsteroidal antiinflammatory drugs and corticosteroids or regional injection of corticosteroids into the superonasal orbit around the trochlea.

Oculomotor palsy — Patients with complete oculomotor nerve palsy present with exotropia, hypotropia, ptosis, and mydriasis (figure 2). Those with incomplete or partial third nerve palsy will have hypotropia if the superior rectus or inferior oblique muscles are more involved than are the other extraocular muscles. (See "Third cranial nerve (oculomotor nerve) palsy in children".)

Patients who are suspected of having oculomotor nerve palsy should be referred to an ophthalmologist who is skilled in the evaluation and management of ocular motility abnormalities. Neuroimaging may be necessary to determine the underlying etiology (table 2). Strabismus surgery is usually required. (See "Third cranial nerve (oculomotor nerve) palsy in children", section on 'Evaluation' and "Evaluation and management of strabismus in children", section on 'Alignment'.)

Congenital fibrosis of the extraocular muscles — Congenital fibrosis of the extraocular muscles (CFEOM) can mimic third nerve palsy. CFEOM includes several inherited restrictive strabismus syndromes that affect the extraocular muscles that are innervated by the third and fourth cranial nerves (table 1) [9,10]. In addition to being structurally abnormal, the extraocular muscles can insert anomalously on the eye [11]. Three phenotypes exist: CFEOM1 and CFEOM3 cause hypotropia, whereas CFEOM2 causes exotropia. (See "Causes of horizontal strabismus in children", section on 'Congenital fibrosis of the extraocular muscles'.)

●In the CFEOM1 phenotype, all affected family members have classic CFEOM (eg, bilateral ptosis; anchoring of the eyes 20 to 30 degrees below the horizontal, markedly limited, and aberrant residual eye movements; and an anomalous head posture of the head tilted back in a "chin-up" position). CFEOM1 is an autosomal dominant disorder with a genetic locus that maps to chromosome 12p. Neuropathologic changes suggest that CFEOM1 is caused by a primary defect in the development of the superior division of the oculomotor nerve [12].

●In the CFEOM3 phenotype, not all of the affected family members have the classic findings. They may have unilateral rather than bilateral involvement or they may lack the characteristic ptosis, infraduction, and inability to elevate past the midline. CFEOM3 is an autosomal dominant disorder with reduced penetrance and variable expressivity. It has been mapped to the CFEOM3 locus on 16q24.2-q24.3 and the CFEOM1 locus on chromosome 12 [13,14].

Treatment of CFEOM varies by case; it consists of strabismus surgery to release the restriction caused by the tight muscle(s).

Monocular elevation deficiency — Monocular elevation deficiency (also known as double elevator palsy) occurs commonly in association with ptosis or pseudoptosis of the affected eye. Both elevators of the eye (the inferior oblique and the superior rectus muscles) do not function properly, resulting in hypotropia of the affected eye. With longstanding hypotropia, the inferior rectus muscle becomes contractured, making the distinction from congenital fibrosis of the extraocular muscles often difficult.

Treatment consists of strabismus surgery. If the inferior rectus muscle is tight, the first surgery is release of the restriction. If the inferior rectus is not tight, the first surgery is transposition of all or part of the medial and lateral rectus muscles superiorly to increase the supraduction ability (Knapp procedure or one of its variations).

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SUMMARY AND RECOMMENDATIONS

●Definition – Vertical strabismus is an anomaly of ocular alignment in which the direction of deviation is up (hyperdeviation) or down (hypodeviation). Vertical strabismus usually is caused by weakness or restriction of one of the extraocular muscles involved in vertical eye positioning (table 1). (See 'Introduction' above.)

●Causes of hyperdeviations – In hyperdeviations, the affected eye is elevated relative to the fellow eye in straight-ahead, or primary, position. Causes of hyperdeviations in children include (see 'Hyperdeviations' above):

•Trochlear nerve (fourth cranial nerve) palsy (picture 1) (see 'Trochlear palsy' above)

•Oculomotor nerve (third cranial nerve) palsy (see 'Oculomotor palsy' above)

●Causes of hypodeviations – In hypodeviations, the affected eye is depressed relative to the fellow eye in primary position. Causes of hypodeviation include (see 'Hypodeviations' above):

•Orbital fractures (see 'Orbital fracture' above)

•Thyroid-related eye disease (see "Clinical features and diagnosis of thyroid eye disease")

•Brown syndrome (picture 2) (see 'Brown syndrome' above)

•Oculomotor nerve (third cranial nerve) palsy (figure 2) (see 'Oculomotor palsy' above)

•Congenital fibrosis of the extraocular muscles (see 'Congenital fibrosis of the extraocular muscles' above)

•Double elevator palsy (see 'Monocular elevation deficiency' above)