Chapter 6

Introduction

Ocular motor nerve palsies in children pose a different clinical paradigm than those in adults and require a specialized knowledge base for proper evaluation and treatment. Children with acute ocular motor nerve palsies come to medical attention because of diplopia, abnormal head posture, ptosis, ocular misalignment, or systemic disease. Those with chronic ocular motor nerve palsies are often referred because of strabismic amblyopia.

Neurologically-impaired children have a predilection for developing comitant as well as incomitant forms of strabismus. In strabismic children with a history of neurological disease (e.g., brain tumors, congenital hydrocephalus, and meningitis), signs of ocular motor nerve palsy (e.g., incomitance, pupillary abnormalities, and torticollis) should be carefully sought. Conversely, in children with diagnosed cranial nerve palsies, other signs of neurological disease should be ruled out with a thorough neurological evaluation. Assessing objective torsion is now an integral part of the strabismus examination.207 Coexistent neurological signs frequently assist the examiner in clinically localizing the lesion and determining its pathophysiology. For example, signs of fever and nuchal rigidity raise the possibility of meningitis, while coexistent signs of dorsal midbrain syndrome suggest tumor, hydrocephalus, or shunt failure.

As with other neuro-ophthalmologic disorders, there is little overlap in the differential diagnosis of ocular motor nerve palsies in children versus adults.234 This disparity reflects the relative preponderance of congenital ocular motor nerve palsies in children and the unique predisposition of children to develop certain disorders (e.g., benign recurrent sixth nerve palsy, ophthalmoplegic migraine, bacterial meningitis), as well as the comparative rarity of aneurysms and vasculopathic palsies in children.287

An initial impression can be gained by observing a child’s head posture prior to formal evaluation. A large head turn in an esotropic child suggests an acute sixth nerve palsy, while a head tilt in the absence of obvious strabismus suggests trochlear nerve palsy. Although the abrupt, recent onset of

torticollis associated with acquired cranial nerve palsy is rarely overlooked by parents, it is not uncommon for torticollis associated with congenital palsies to go unnoticed.

When a cranial nerve palsy is suspected, one must rule out masquerading restrictive disorders and neuromuscular disease. This process begins with a carefully taken history, which includes the following questions:

1. Is there a history of antecedent head trauma? Traumatic cranial nerve palsies may be single or multiple and may involve any of the ocular motor nerves.583 Usually, a history of recent head trauma is well established, and there is little question as to the traumatic nature of the palsy. However, cranial nerve palsies due to parasellar tumors may occasionally be precipitated by mild head trauma. In a child with a cranial nerve palsy, the coexistence of a blowout fracture or a skew deviation can complicate the diagnostic task.19,136,418 Perinatal cranial trauma should also be considered with inquiry about difficult forceps delivery, breech presentation, cephalohematoma, and cranial molding in the perinatal period. Photographs taken in the perinatal period may be informative in this regard. In patients with a severe head trauma, the response to surgical treatment may be inexorably compromised by disruption of sensory or motor fusion.440,441,463 Those with loss of motor fusion from a vergence system disorder can often superimpose images momentarily, but cannot maintain fusion through a head movement, or a small proximal or distal shift in the fixation target.462,463

2. Is there a history of variability throughout the day?

Diplopia or ptosis that is minimal on awakening and becomes worse as the day progresses suggests myasthenia gravis.

3. Is there a history of headache? A history of headache suggests the possibilities of elevated intracranial pressure, meningitis, and ophthalmoplegic migraine.

4. Is the child otherwise neurologically normal (by history)?

Coexistent neurological signs often suggest a specific mechanism or site of ocular motor nerve injury.

5. Are the symptoms relating to the condition old or of recent onset? The diagnosis of a congenital ocular motor nerve

palsy should be considered in any child with long-standing signs and no diplopia. The ocular motility deficits associated with congenital third nerve palsy or Duane syndrome are often noticed by the parents, in contrast to congenital trochlear nerve palsy, which may escape detection because of the absence of obvious strabismus. However, observing old family photographs confirms the presence of a longstanding head tilt. It is not unusual for a congenital trochlear nerve palsy to first become symptomatic during the teenage years due to a gradual increase in the size of the deviation or a decompensation in fusional control. The facial asymmetry associated with congenital trochlear nerve palsy is frequently overlooked by inexperienced observers. This finding also takes time to develop and may not be sufficiently advanced to be diagnostically helpful in early childhood.

6. If a head tilt is present, at what age is it first noted? Does it normalize when the child reclines? A head tilt associated with congenital trochlear nerve palsy is first noted around 6 months of age, when the child acquires head and neck control, while a head tilt due to congenital muscular torticollis is noted within the first few months of life. A head tilt associated with trochlear nerve palsy resolves when the child reclines,540 while one associated with congenital muscular torticollis persists.

Resolution of torticollis in a child with an ocular motor palsy may signal either recovery of the palsy or development of amblyopia and suppression. We reassure the parents that the anomalous head position is (paradoxically) a positive prognostic sign for binocular vision, and advise them to call immediately if the child stops maintaining it. It is not established how much stereopsis or binocularity is lost prior to the disappearance of an abnormal head posture. Therefore, the finding of an abnormal head posture in a young child is no guarantee that the child is maintaining normal binocularity and stereopsis. Close monitoring of vision and early institution of amblyopia therapy is recommended in such children.

While trochlear nerve palsy is the major cause of vertical diplopia in children, other causes must also be considered. The physical examination of the child with incomitant strabismus consists of gross inspection, examination of versions, ductions, field measurements, sensory and acuity testing, and ancillary testing (Double Maddox Rod, Lancaster red–green, Lees screen, forced duction test, active force generation test), as indicated.573 A head tilt toward the side of the lower eye that persists despite a manifest vertical deviation suggests the diagnosis of skew deviation.74,146 Donahue146 have documented that a skew deviation arising from selective unilateral injury to the anterior or posterior canal otolithic pathways on the side of the lower eye can produce ocular motility that is indistinguishable from isolated superior or inferior oblique muscle palsy, respectively.146,147

Following complete resolution of cranial nerve palsies, patients may be left with a comitant strabismus from longstanding disruption of fusion or from secondary extraocular muscle contracture.65 The term muscle contracture refers to a muscle that has been structurally altered by remaining in a shortened position for a prolonged period. This results in an increased, nonlinear resistance to stretch that is greater at longer muscle lengths. Early investigations attributed muscle contracture to fiber atrophy and hyalinization, but it is now known that the number of muscle fiber sarcomeres actually decreases.501

In a long-standing sixth nerve palsy, a medial rectus contracture may develop. To some degree, the clinician can distinguish residual lateral rectus weakness from medial rectus contracture by observing the saccadic velocity during attempted abduction of the eye and by performing active force generation and forced duction testing. In the case of true lateral rectus weakness, the saccadic velocity is slow throughout the refixation movement, whereas with medial rectus contracture, the saccadic velocity is normal until the abduction saccade is abruptly terminated by the tight medial rectus muscle. A medial rectus contracture with no residual lateral rectus weakness produces some degree of forced duction limitation, but if the eye is grasped with forceps and the patient is instructed to look away from the contractured muscle, a normal “pull” on the forceps is felt by the examiner.

The phenomenon of muscle contracture renders a trochlear nerve palsy more horizontally comitant over time. Children with long-standing superior oblique palsies may develop a contracture of the superior rectus muscle in the hypertropic eye if they chronically fixate with their nonparetic eye, or a contralateral inferior rectus contracture if they habitually fixate with the paretic eye. These secondary contractures may confound the diagnosis and alter the surgical strategies to restore normal ocular alignment. For example, the development of a contralateral inferior rectus contracture in a patient with trochlear nerve palsy may cause the hyperdeviation to secondarily become larger in upgaze than in downgaze. The role of medial rectus contracture in the development of horizontal spread of comitance in patients with long-standing sixth nerve palsy, if any, has not been established.

The forced duction test and force generation test play an important role in the neuro-ophthalmologic evaluation of incomitant strabismus in children and in the differentiation of muscle paresis from restrictive strabismus. These tests are most important in the setting of (1) previous orbital trauma, when there is a question of muscle entrapment (as in a blowout fracture); (2) previous ocular surgery, when there is a possibility of iatrogenic peribulbar scarring (as may occur following a scleral buckling procedure); (3) incomitant congenital strabismus with ptosis, when congenital fibrosis syndrome remains a diagnostic consideration;

(4) coexistent signs of orbital inflammation or muscle enlargement on neuroimaging studies, when the diagnosis of rectus muscle inflammation with secondary restriction must be ruled out257,259; and (5) longstanding muscle paresis, when the antagonist of a paretic muscle may have undergone contracture secondary to long-term malpositioning of the eye (as in a contracture of the medial rectus muscle following lateral rectus muscle palsy).

In young children, the forced duction test must be performed in the operating room under general anesthesia, whereas teenagers may tolerate the necessary manipulation with topical anesthesia. When general anesthesia is used, it is important to avoid succinylcholine or other depolarizing agents that produce prolonged extraocular muscle contracture for up to 20 min.172 In an outpatient setting, anesthesia should be carefully obtained by using topical anesthetic drops combined with placement of an anesthetic-soaked cotton swab over the area of perilimbal sclera to be grasped by the forceps. Attention should be paid to maintaining the eye in its usual arc of rotation. If the eye is pushed into the orbit (as inevitably occurs when a Q-tip is used to rotate the eye), tension is relieved from the rectus muscle, and the examiner may erroneously conclude that the muscle in question is not tight. Conversely, a tight oblique muscle may become slack when the eye is proptosed during rotation. The forced duction test is considered positive when an abnormal limitation of movement is demonstrated and negative when the examiner is able to fully rotate the eye.

In the case of an orbital floor fracture, the location of the fracture is an important determinant of the degree of restriction and paresis that develop. When an orbital floor fracture is posteriorly located, then the main contractile portion of the muscle (the midbelly) may be entrapped, but enough elastic muscle exists anterior to the entrapment site to allow ocular rotation. A posterior orbital floor fracture may result in a combination of mechanical paresis from muscle injury and/or adhesions and neurogenic paresis from damage to its neural input as it enters the muscle in the posterior orbit. In contrast, anterior entrapment may severely restrict elevation of the globe, while the contractility of the muscle is preserved.

A positive forced duction test can also result from anterior scarring of periocular tissue to the globe. In children, who have sustained orbital trauma or had previous ophthalmic surgery, it is important to determine whether a positive forced duction test represents a “leash” or a “reverse leash.” Jampolsky250 has described the technique of retropulsing or proptosing the globe during forced duction testing, to gain additional information regarding the nature of the restriction. In the case of a leash caused by a tight rectus muscle, the rotational excursion of the globe increases as the globe is retroplaced during rotation with the forceps and decreases as it is proptosed. In the case of a reverse leash caused by scarring

of conjunctiva or peribulbar tissue to the anterior aspect of the globe, the opposite occurs. In Brown syndrome, a congenitally restricted superior oblique tendon also produces a reverse leash that becomes more restricted as the globe is manually retroplaced.

The active force generation test is used to estimate contractile power in the setting of entrapment or recovering muscle paresis. This is an important determination, as the antagonist of an entrapped muscle (the superior rectus muscle in the case of a blowout fracture) may appear paretic, or the entrapped muscle itself (the inferior rectus muscle) may be restricted. The eye is grasped with forceps near the limbus and held in a direction opposite the deficient movement, while the child attempts to look in the direction of limitation. Forces developed by the contracting muscle can be felt. While attempts have also been made to quantify the force generation test,498 valuable clinical information can be obtained from the examiner’s subjective assessment.

A saccade produced by a paretic muscle is visibly slower than a normal saccade, causing the eye to appear to drift toward the premature termination of its rotation. Although decreased saccadic velocity is usually seen in the setting of isolated ocular motor paresis, it is not specific to this condition and may also be seen in disease that primarily involves the extraocular muscles (e.g., orbital pseudotumor), the neuromuscular junction (e.g., myasthenia gravis), and the central nervous system (CNS) (e.g., olivopontocerebellar degeneration, chronic progressive external ophthalmoplegia). Nevertheless, the clinical finding of slowed saccadic velocities allows the examiner to quickly tease out the abovementioned paretic disorders from a mixed bag of conditions, including contracture, restriction, and comitant strabismus.

Modern neuroimaging adds increasing information to the diagnostic evaluation of oculomotor nerve palsies. The neuroimaging evaluation of patients with ocular motor nerve palsies have been transformed from a primitive search for causative mass lesions in the brain to a sophisticated set of techniques to directly visualize the intracranial ocular motor nerves and blood vessels, the orbital ocular motor nerves, and the extraocular muscles, both statically and dynamically.139 High-resolution MR imaging can directly demonstrate pathology of the oculomotor and abducens nerves and atrophy of their corresponding extraocular muscles.139 Attention to the orbital extraocular muscles reveals obvious signs of atrophy, hypoplasia, or heterotopia of extraocular muscles that are easily missed by the neuroradiologist, who is necessarily focused on the search for a causative intracranial lesion. High-resolution MR imaging of the head can be combined with quasicoronal orbital MR images in multiple gaze positions to yield enormous information. In cases of traumatic head injury, quasicoronal orbital images can show associated superior oblique muscle atrophy (suggestive of trochlear nerve palsy) or blowout