Restriction, Paresis, Dissociated Strabismus, and Torticollis Kenneth W

Home , Enophthalmos, Management of strabismus, Prism correction

Complex Strabismus: Restriction, Paresis, Dissociated Strabismus, and Torticollis Kenneth W. Wright

his chapter on complex strabismus reviews the evaluation Tand management of incomitant strabismus associated with rectus muscle paresis and ocular restriction. Other topics include dissociated strabismus complex, torticollis, and nystagmus. Incomitant strabismus is a deviation that changes in different ﬁelds of gaze. Incomitance can be caused by ocular restriction, extraocular muscle paresis, or oblique muscle dysfunction or can be associated with a primary A- or V-pattern. The diagnosis and treatment of oblique muscle dysfunction (palsy and overaction), Brown’s syndrome, and A- and V-patterns are covered in Chapter 9.

PARALYTIC RECTUS MUSCLES AND RESTRICTIVE STRABISMUS: GENERAL PRINCIPLES

If an eye has limited ductions, there are only two basic causes: extraocular muscle paresis or ocular restriction. Therefore, a strabismus associated with limited ductions is secondary to extraocular muscle paresis, ocular restriction, or both.

Paresis Extraocular muscle paresis means weak muscle pull, whereas palsy indicates a complete lack of muscle function. Cranial

323 324 handbook of pediatric strabismus and amblyopia nerve paresis and primary muscle disease are obvious reasons for a weak muscle that can cause limited ocular rotations. A muscle paresis can also be caused by ineffective muscle pull on the eye, or mechanical disadvantage of muscle pull. Clinical examples of conditions that cause mechanical disadvantage of muscle pull include: • A scarred or tethered muscle preventing transmission of muscle pull to the globe (e.g., floor fracture with entrapped inferior rectus muscle) • A posteriorly displaced rectus muscle (e.g., slipped muscle) • A muscle shifted out of its appropriate plane, thus diminishing the vector force in the field of action of the muscle (e.g., high myopia with displaced lateral rectus muscle) Table 10-1 lists the three major causes of a mus-cle paresis: (1) cranial nerve paresis, (2) primary muscle disease, and (3) mechanical disadvantage of muscle pull. Specific types of paralytic strabismus, including sixth and third nerve palsies, are covered later in this chapter.

TABLE 10-1. Causes of Muscle Paresis. Primary muscle Mechanical disadvantage Cranial nerve palsy disease of muscle pull Third nerve palsy Botulism Stretched scar after muscle surgery Fourth nerve palsya Myasthenia gravis Slipped muscle or lost muscle (superior oblique palsy) Sixth nerve palsy CPEO Canine tooth syndrome with scarring of trochlea causing Brown’s syndrome with superior oblique palsy Trauma to muscle Miller–Fisher Floor fracture with an syndrome entrapped inferior rectus (Guillain-Barré) muscle causing limited depression Cranial nerve aberrant Agenesis of an High myopia with large innervation extraocular muscle posterior staphyloma, and syndromes (e.g., often associated slippage of lateral rectus Duane’s syndrome) with a craniofacial below globe reducing lateral disorder rectus abduction force, causing esotropia aSee Chapter 9. chapter 10: complex strabismus 325

Ocular Restriction

Classically, the term ocular restriction describes a mechanical tether or leash that limits ocular rotations. Ocular restriction, however, can be caused by at least two general mechanisms: a mechanical tether on eye movements or misdirected muscle forces that work against the normal agonist muscle function. The term restriction is often loosely used as a general term for limited eye movements; however, a clear distinction should be made between ocular restriction and rectus muscle palsy. If the cause of diminished eye movements is not known, then use the term limited rotations or limitation of eye movements until the etiology is determined. Table 10-2 lists the causes of restrictive strabismus. Mechanical restriction of eye movement is caused by adhesions to an extraocular muscle or sclera, a tight or inelastic extraocular muscle, or an orbital mass. Restrictive adhesions can occur from conjuctival scarring, scarring of Tenon’s capsule, orbital fat adherence, and, rarely, congenital fibrotic bands that attach to the eye or extraocular muscles. Inelastic muscle or muscle fibrosis occurs with thyroid myopathy, local anesthesia myotoxicity, and congenital muscle fibrosis (e.g., monocular elevation deficit and congenital fibrosis syndrome). An orbital mass, such as an orbital hemangioma, or a glaucoma implant can cause ocular restriction either by direct interference of rotation of the eye or by pressure on an extraocular muscle that tightens the muscle. Restriction resulting from misdirected muscle force vectors occurs in conjunction with aberrant innervation of an antagonist muscle and abnormal muscle–pulley location or a displaced extraocular muscle.20,25,83 An example of aberrant innervation causing restriction is limited adduction, often associated with Duane’s syndrome. Restricted adduction occurs because the lateral rectus muscle is aberrantly innervated by part of the medial rectus nerve. When the eye attempts to adduct, the lateral rectus muscles contracts against the contracting medial rectus muscle, thus restricting adduction. An example of displaced extraocular muscle is the V-pattern strabismus and superior oblique muscle underaction that are frequently seen in patients with craniosynostosis.20 These patients have excyclorotation of the orbits that results in superior displacement of the medial rectus muscle and limited ocular depression in adduction. The superiorly displaced medial rectus muscle pulls the eye up in addition to its normal function of 326 handbook of pediatric strabismus and amblyopia staphyloma and slippage of lateral rectus below globe High myopia with large posterior mass effect on globemovement insertion and or pulley movement or displaceSO tendon (acquired syndrome)Brown’s (craniosynostosis, extorted orbit) limited depression after anterior displacement of SO tendon by retinal band (e.g., after strabismus surgery, (e.g., after strabismus surgery, retinal detachment surgery, or periocular trauma) posterior staphyloma syndrome) (Duane’s innervation Mechanical restriction into a muscle (inferior most common) retinal surgery, after strabismus surgery, or periocular trauma) caused by a fibrotic inferior rectus SO muscle tendon complex (see Chapter 9)(inferior rectus most common) around the trochlea scarring or inflammation large bleb causing mass effect on globe antielevation after inferior oblique and anteriorization with J-deformity, TABLE 10-2.TABLE Causes of Ocular Restriction. extraocular muscleTight Thyroid: Graves diseaseCongenital fibrosis syndrome Structural adhesions Fat adherence to muscle or sclera High myopia with large Congenital fibrotic band Congenital cranial nerve aberrant Orbital mass Orbital tumor causing Congenital ectopic extraocular muscle Misdirected muscle forces Fat adherence to extraocular muscle (e.g., Monocular elevation deficit syndrome Congenital Brown’s syndrome: inelastic Congenital Brown’s syndrome: Acquired Brown’s Glaucoma explant withEntrapped muscle after orbital fracture Iatrogenic displaced muscle insertion; Fibrosis after local anesthetic injection SO, superior oblique. chapter 10: complex strabismus 327 adduction and limits depression in the field of action of the superior oblique.20 A rare example of restriction caused by a displaced muscle–pulley was reported by Oh et al.83 They described a patient with limitation of elevation in adduction, or a pseudo- Brown’s syndrome, caused by a congenitally inferiorly displaced lateral rectus muscle and its pulley. These authors hypothesized that the infraplaced lateral rectus muscle and pulley act to pull the eye down, limiting elevation on adduction. Iatrogenic displacement of extraocular muscles during strabismus surgery can also cause limited eye movements. Inferior oblique muscle anteriorization anterior to the inferior rectus insertion can also cause active restriction and limited elevation (see Chapter 2, Fig. 2–17).15,43,114,135 In some cases, restriction and paresis coexist, such as with paretic lateral rectus muscle and secondary contracture of its antagonist medial rectus muscle. It is important to diagnoses the cause of limited ductions to formulate an effective surgical plan. The next section describes methods for diagnosing extraocular muscle paresis and ocular restriction.

Diagnosing Restriction Versus Paresis The principal diagnostic tests that differentiate paresis from restriction include saccadic velocity measurements, forced ductions, and forced-generation test. Other signs influencing diagnosis include intraocular pressure changes in various fields of gaze and lid fissure changes in sidegaze.

SACCADIC VELOCITY MEASUREMENTS Saccadic velocity measurements can help differentiate restriction from paresis by observation, without touching the eye. Therefore, this method is useful in young children as well as adults. Saccadic movements are fast, jerk-like eye movements that require normal rectus muscle function. The rectus muscles are the major movers of the eye and are responsible for saccadic eye movements. The presence of a saccadic eye movement indicates normal rectus muscle function whereas the inability to stimulate a saccade suggests a rectus muscle palsy. A paretic rectus muscle does not have the power to generate a saccadic eye movement, and the eye drifts slowly to the intended ﬁeld of gaze. Strabismus associated with limited ductions and diminished saccadic velocity is caused by a rectus muscle paresis, not an oblique muscle palsy. 328 handbook of pediatric strabismus and amblyopia

In contrast to a rectus muscle paresis, ocular restriction is associated with normal, but shortened, saccadic movements as the eye stops abruptly when the restriction is met. This eye movement pattern of a fast eye movement that stops abruptly as it meets the restriction is termed the dog on a leash; it is anal- ogous to a dog lunging after a cat, then being abruptly stopped by its leash (Fig. 10-1). In patients with limited eye movements, it is important to clinically test for saccadic eye movements before surgery to assess muscle function. At the time of surgery when the patient is under anesthesia, it is impossible to test muscle function. Positive forced ductions at the time of surgery indicate only passive restriction and do not exclude the possibility of coexisting muscle palsy. Horizontal and vertical eye movements can be measured by laboratory tests including electro-oculogram (EOG) recordings and infrared eye trackers. Clinical observation of eye movements can also be used in clinical practice for evaluating the presence of a saccadic movement; this is facilitated through the use of an optokinetic nystagmus (OKN) drum for young children who are not able to follow instructions as well as for cooperative patients to compare eye movements (Fig. 10-2). Rotate the OKN drum and observe the patient’s eyes for a brisk redress

FIGURE 10-1. “Dog on a Leash.” The pattern of a fast eye movement that stops abruptly indicates a mechanical restriction. Upper: cartoon shows a dog on a leash walking toward a cat behind a tree. Lower: The dog sees the cat and leaps for the cat but is stopped abruptly by the leash. chapter 10: complex strabismus 329

FIGURE 10-2. Photograph of a child being examined with an optokinetic nystagmus (OKN) drum. The saccadic movement will be in the direction opposite to the drum rotation. This is a good clinical method to estimate if a saccade is present. movement opposite to the direction of the drum rotation. Compare eye to eye and look for asymmetry of the OKN response. An inability to generate a saccadic movement indicates a paretic rectus muscle.

FORCED DUCTIONS Forced ductions identify the presence of a mechanical restriction to ocular rotation; these are performed by grasping the eye with a forceps and then passively moving the eye into the ﬁeld of limited ocular rotation. If the eye shows a resistance to rotation with the forceps (positive forced ductions), then there is a mechanical restriction. When performing forced ductions for possible rectus muscle restriction, proptose the eye to stretch the rectus muscles. This maneuver will allow identiﬁcation of restriction caused by a tight rectus muscle. If the examiner inadvertently retropulses the eye, the rectus muscles slacken and produce a negative forced-duction test, even if the rectus muscle is tight (Fig. 10-3). The opposite holds true for oblique muscle forced ductions, because retropulsing the eye will stretch the oblique muscles and accentuate a tight oblique muscle. If a restriction is worse with retropulsion of the eye, then the restriction is not caused by a tight rectus muscle but, instead, is 330 handbook of pediatric strabismus and amblyopia

AB FIGURE 10-3A,B. (A) The proper technique for rectus muscle forced ductions includes grasping the conjunctiva with a 2 3 Lester forceps at the limbus, just anterior to the muscle insertion. First, proptose the eye, and then pull the eye away from the muscle being tested, thus placing the rectus muscle on stretch. This maneuver allows identification of even mildly tight or restricted muscles. (B) The improper technique for rectus muscle forced ductions shows the eye being retropulsed during the maneuver, causing iatrogenic slackening of the muscle and a false-normal forced-ductions test. Positive forced ductions that do not improve when the eye is intentionally retropulsed suggest the presence of a nonrectus muscle restriction, such as periocular scarring (e.g., fat adherence). secondary to either a periocular adhesion or a tight oblique muscle. Forced-duction testing can be used as an in-office test using topical anesthesia, or at the time of strabismus surgery. In most cases, the pattern of the eye movements, including the clinical evaluation for saccades, establishes the diagnosis of restriction or paresis. Therefore, in-office forced-duction testing is usually not necessary. If surgery is indicated, forced- duction testing can be performed at the time of surgery to verify the diagnosis. It is important to remember that positive forced ductions does not exclude the presence of a coexisting palsy. In fact, most cases of long-standing rectus muscle palsy also have contracture of the antagonist muscle, so forced ductions will be positive. Preoper- ative evaluation of muscle function by saccadic eye movement chapter 10: complex strabismus 331 testing or the forced-generation test (see next section) is required to diagnose a rectus muscle palsy.

FORCED-GENERATION TEST The forced-generation test directly measures active muscle force and is useful for diagnosing a rectus muscle palsy. To perform this test, the eye is topically anesthetized and grasped with forceps; the patient is asked to look into the ﬁeld of limited rotation. A sterile cotton-tipped applicator can also be used to push against the eye to feel the abduction force, as noted in Chapter 5 (Fig. 5-16A,B). The examiner feels the pull of the muscle against the forceps or cotton-tipped applicator and compares this to the fellow eye or the antagonist muscle. If there is diminished pull from the muscle into the ﬁeld of limited rotation, then a paresis is present. Forced ductions can be used in conjunction with forced-generation testing. If forced ductions are positive and the force-generation test shows poor muscle function, then the diagnosis is a combination of restriction and paresis.

INTRAOCULAR PRESSURE CHANGE ON EYE MOVEMENT Another sign of restriction is increased intraocular pressure on attempted duction into the ﬁeld of limited movements and away from a restriction or tight muscle. Intraocular pressure increases as the eye forcibly attempts to move against the restriction. Patients with thyroid myopathy and strabismus may show increased intraocular pressure when the pressure reading is made with the restricted eye in forced primary position.

LID FISSURE CHANGES ON EYE MOVEMENT Ocular restriction caused by a tight rectus muscle or a restrictive adhesion to the globe will cause globe retraction and lid fissure narrowing as the agonist rectus muscle attempts to pull the eye away from the restriction [see Duane’s syndrome (Fig. 10-12), later in this chapter]. These movements occur because the eye is restricted from rotating; therefore, the contracting agonist muscle pulls the eye posteriorly and causes globe retraction and lid fissure narrowing. A rectus muscle paresis will cause the opposite: lid fissure widening and relative proptosis. As the patient looks into the field of action of the paretic rectus muscle, the agonist muscle relaxes secondary to the palsy. The antagonist muscle also relaxes because of 332 handbook of pediatric strabismus and amblyopia

Sherrington’s law, and pressure from orbital fat pushes the eye forward. A patient with a sixth nerve palsy, for example, will show lid ﬁssure widening on attempted abduction (see Fig. 10-10, later in this chapter). This change occurs because the medial rectus muscle relaxes on attempted abduction (Sherrington’s law) and, along with the paretic lateral rectus, it is loose; therefore, the posterior pressure of the orbital fat pushes the eye forward.

MANAGEMENT OF INCOMITANT STRABISMUS: GENERAL PRINCIPLES

Management begins with understanding why the deviation is incomitant. For example, if an incomitant strabismus is associated with severe limitation of ductions, determine whether the limitation is caused by restriction or paresis. If a signiﬁcant restriction is the cause of limited adduction, then one must release the restriction. If severe limitation of ocular rotations is secondary to poor rectus muscle function, then one has to address the muscle weakness. In cases in which the incomitance is associated with little or no limitation of eye movements, the incomitance can be managed by operating on the good eye to match ocular rotations of the deviated eye. Determine where the deviation is greatest and operate to achieve alignment in primary position while reducing the incomitance. Use this strategy: recession procedures have their greatest effect in the ﬁeld of action of the recessed muscle, and resections produce a leash with the greatest effect occurring when the eye rotates away from the resected muscle (see Chapter 11). Recessing the right medial rectus muscle will produce an exodeviation greater in leftgaze and almost no effect in rightgaze, and resecting the right lateral rectus muscle produces an exodeviation that increases in leftgaze. With this strategy in mind, determine what surgery would best correct the following strabismus. Example 1. Trace limitation of abduction of unknown etiology, left eye; negative forced ductions.

Right Primary Left ET2 ET 8 ET 16

ET, estropia. chapter 10: complex strabismus 333

The surgical plan is to recess the right medial rectus muscle 4.0 to 5.0mm, as this will match the right medial rectus muscle to its underacting yoke muscle, the left lateral rectus muscle. Weakening the right medial rectus muscle will slightly reduce adduction but will not affect abduction; this reduces the large esotropia in leftgaze without causing an exotropia in rightgaze. Do not recess the left medial rectus muscle because this surgery has little effect in leftgaze where the esotropia is largest and will produce an exo-deviation in rightgaze. Also, avoid a left lateral rectus resection as this will not strengthen the weak lateral rectus. Instead, it will cause a tight lateral rectus muscle that also has little effect in leftgaze where the esotropia is greatest and will cause an exodeviation in rightgaze. For an incomitant esodeviation that is greater than 10 to 15 prism diopters (PD) in primary position and increases in leftgaze, two-muscle surgery will be required to correct the deviation in primary position. Consider asymmetrical bilateral medial rectus recessions, with a larger recession on the right medial rectus muscle. The Faden operation has also been suggested to reduce incomitance. Adding a Faden to a recession of the medial rectus muscle increases the weakening effect of the recession in adduction and improves the incomitance. The use of the Faden is controversial. If it is used, it is most effective on the medial rectus muscle, as the medial rectus has the shortest arc of contact. The- oretically, the Faden weakens the muscle mostly in the field of action of the muscle, with little effect in primary position; therefore, it may be helpful in reducing incomitance (see Chapter 11). A report on the effect of the Faden procedure on the medial rectus muscles in reducing the AC/A ratio concluded there was a beneficial effect; however, the table of data in this study showed no change of the AC/A ratio. It is likely the Faden procedure has little effect, except in extreme fields of gaze.35 If the limitation is severe, recessing the yoke muscle to match the limitation will not work, as operating on the good eye will not improve the ability of an eye with limited ductions to come to midline. In these cases of moderate to severe limitation of ductions, one must release the restriction or, in the case of a palsy, transpose muscle forces to bring the eye to midline. Recessing the contralateral yoke muscle only works if the limitation is slight, such as a trace to 1 limitation of ductions. Vertical incomitance can be treated with the same strategy as described previously for horizontal strabismus. One special situation that occurs with Grave’s disease and floor fractures is 334 handbook of pediatric strabismus and amblyopia that of a patient with orthotropia in primary position and a hypotropia in upgaze secondary to a tight inferior rectus muscle. In this case, recess both inferior rectus muscles, with a larger recession on the side with the restriction. The diagnosis and management of specific types of restrictive and paralytic strabismus follow.

SPECIFIC TYPES OF RESTRICTIVE STRABISMUS

Fat Adherence Fat adherence is a restrictive form of strabismus occurring after periocular surgery or accidental trauma. Marshall Parks was the first to describe the clinical characteristics and etiology of the fat adherence syndrome or, as it is also called, the adhesive syndrome.84 Normally, Tenon’s capsule and muscle sleeve act as an elastic barrier separating the globe from the surrounding orbital fat. Fat adherence is caused by violation of the posterior Tenon’s capsule, allowing exposure and manipulation of extraconal fat and fascia, which produces an adhesion of these tissues to the sclera. Because the septae within the extraconal fat connect to the periorbita, fibrosis associated with fat adherence can extend from the orbital bone to the sclera (Fig. 10-4). In severe cases, the eye is virtually scarred to the orbital bone, immobilizing ocular rotations. Violation of the muscle sleeve can also result in fat adherence to a rectus muscle causing a tight muscle. Fat adherence most frequently occurs after strabismus surgery involving posterior exposure (especially oblique muscle surgery) and retinal buckle surgery, but can also occur after any periocular surgery, even after blepharoplasty.57,59,134 Fat adherence is difficult to surgically correct, as recurrence of fat adherence after removal of adhesions is very common. Once Tenon’s capsule is violated and a scar established, it is almost impossible to reestablish the delicate fascial barrier to prevent recurrence of scarring. Teflon or silicone sheaths have been used as an artificial barrier, but they become encapsulated in scar and often make the restriction worse. Amniotic membrane transplantation has been used to create a barrier separating periocular fat from the sclera, but the technique is difficult, at best, and remains investigational.138 Surgical correction of fat adherence consists of releasing the scar by dissecting close to chapter 10: complex strabismus 335

FIGURE 10-4A,B. Fat adherence syndrome. (A) Diagram on the right shows the normal anatomy of the periocular fascia with Tenon’s capsule as the barrier separating orbital fat from the sclera and muscle. Diagram to the left shows fat adherence (after violation of Tenon’s capsule) over- lying the rectus muscle in an area away from the rectus muscle over sclera. Note that a ﬁbrous scar extends throughout the fat septae attach- ing periosteum to the muscle and sclera. This scar causes a restrictive leash that limits eye movements. (B) Photograph of fat adherence to the inferior rectus muscle. (Modiﬁed from Parks and Mitchell, 1978, with permission.) sclera and removing the adhesions without repenetrating the orbital fat. (Perform forced ductions after freeing adhesions to evaluate improvement of the restriction.) Dissect carefully with direct visualization, as posterior dissections can be dangerous. 336 handbook of pediatric strabismus and amblyopia

Cases of inadvertent optic nerve transection have occurred, although they are rarely reported. If fat and scar are adherent to a rectus muscle, remove a small amount of the anterior scar, then recess the tight muscle en bloc with the scar rather than trying to dissect all the scar off the muscle. Avoid extensive dissection of scar off the muscle, as this usually results in further fat manipulation and worsening of the adherence. Medical treatment with mitomycin-C has not been effective in reducing postoperative ﬁbrosis and may even increase scarring.17 Injection of peribulbar corticosteroids also fails to prevent postoperative scarring. The best treatment for fat adherence syndrome is prevention: avoid penetration of posterior Tenon’s capsule during the initial surgery. During strabismus surgery, perform minimal dissection of muscle fascia and, when dissecting, dissect close to the muscle to stay away from surrounding orbital fat. If Tenon’s capsule is inadvertently torn so fat is exposed, cover the exposed fat by repairing the Tenon’s tear with 7-0 vicryl suture.

Grave’s Ophthalmopathy Grave’s ophthalmopathy is an autoimmune disease associated with inflammation of the extraocular muscles. Initially, there is an acute phase during which there is a lymphocytic infiltration of the extraocular muscles, resulting in extraocular muscle enlargement and proptosis. This active phase usually lasts several months to more than a year. Orbital imaging studies show thickened extraocular muscles, especially posteriorly. The second phase is a cicatricial phase with quiescence of inflammation and secondary contracture of the muscles. All muscles are usually involved, but the inferior rectus and medial rectus are most severely affected.91 Strabismus is caused by tight fibrotic muscles and can develop in both phases but is most pro- nounced in the cicatricial phase. A restrictive hypotropia caused by tight inferior rectus muscles is the most common type of strabismus, followed by esotropia associated with tight medial rectus muscles. The management of Grave’s ophthalmopathy is careful observation during the acute inflammatory phase. Treatment with systemic steroids and even external beam radiation may be indicated for severe disease; however, radiation therapy is not effective for treatment of the strabismus.126 Orbital decompression is indicated for severe proptosis and visual loss associated chapter 10: complex strabismus 337 with optic nerve compression from inflamed extraocular muscles. In most cases, it is better to perform strabismus surgery after the active phase has subsided and strabismus measurements have stabilized. A report on eight patients whose eyes were operated on during the active phase of thyroid ophthalmopathy noted that all eight patients achieved successful long- term alignment (16 months follow-up); however, half the patients required more than one operation. Regarding the timing of surgery, strabismus surgery is usually performed after orbital decompression surgery, because orbital surgery can alter eye alignment.21,75 The strategy for the treatment of Grave’s ophthalmopathy strabismus is to release the restriction from the tight rectus muscle, with a rectus muscle recession being the procedure of choice. It is not advis- able to use rectus muscle resections, as this tightens an already stiff, inelastic muscle. A right hypotropia less than 15 PD with a tight right inferior rectus muscle can be surgically addressed with a right inferior rectus recession, with or without an adjustable suture technique (Fig. 10-5).8,68 If the deviation in primary position is greater than 18 to 20PD with severe restriction, recess the tight inferior rectus muscle more than 5.0mm and add a recession of the contralateral superior rectus muscle. As a rule, expect 3PD of vertical correction for each millimeter of vertical rectus muscle recession.135 One common problem with correcting thyroid strabismus has been late overcorrection after inferior rectus recession, which occurs in up to 50% of cases.24,56,80 Initially after surgery, there is a successful result. Then, at 4 to 6 weeks after the inferior rectus recession, a consecutive hypertropia on the side of the recession occurs, with underaction of the recessed inferior rectus muscle and ipsilateral lower eyelid retraction.132 R. Friedman suggested that performing asymmetrical bilateral inferior rectus recessions avoids late overcorrection. A report by Cruz and Davitt on eight patients who underwent asymmetrical bilateral inferior rectus recessions showed no overcorrec- tions; however, 25% of these patients were undercorrected.24 Ludwig has suggested that a stretched scar at the new insertion is the cause of the overcorrection. It is hypothesized that, at 4 to 6 weeks after surgery, the absorbable suture loses its strength. The muscle–scleral attachment stretches and causes the tight muscle to retract posteriorly. This author has now switched to nonabsorbable sutures (6-0 Mersiline), and preliminary results have been good, even when using an adjustable suture. 338 handbook of pediatric strabismus and amblyopia

B FIGURE 10-5A,B. Thyroid-associated strabismus. (A) Patient with Graves’ disease and limited elevation, right eye, secondary to a tight right inferior rectus muscle. (B) CT scan shows thyroid-associated changes; the medial inferior and superior rectus muscles are enlarged bilaterally. chapter 10: complex strabismus 339

Congenital Fibrosis of the Extraocular Muscles

Congenital fibrosis of the extraocular muscles (CFEOM) is an autosomal dominant, nonprogressive disorder usually characterized by bilateral congenital ptosis and restrictive external ophthalmoplegia48,49; however, rare unilateral cases have been described (CFEOM 8, 21, 26, 29, 30, 31).28,51 Systemic diseases reported to be associated with CFEOM include Prader–Willi syndrome (CFEOM 25),60 Joubert syndrome (CFEOM 23),3 and cortical and basal ganglia dysplasia (CFEOM 2).123 CFEOM has been mapped to chromosomes 12, 11, and 16 (CFEOM 3, 5, 6, 7, 9, 18, 16).26,51 There can be significant phenotypic heterogeneity with a variety of subtypes of CFEOM found in the same family (CFEOM 6 and 8).96,118 The clinical features of CFEOM have been classified into five groups: (1) generalized fibrosis syndrome,4 (2) fibrosis of inferior rectus with blepharophimosis, (3) strabismus fixus, (4) vertical retraction syndrome,39 and (5) unilateral fibrosis blepharoptosis and enophthalmos (CFEOM 17).32,34,51 The medial rectus muscle is one of the most commonly involved, causing a strabismus fixus esotropia with extreme restriction to abduction (Fig. 10-6). Strabismus fixus is a term for an eye that is fixed and cannot move, usually secondary to severe restriction or a combination of restriction and paresis. The strabismus associated with CFEOM is mostly caused by tight fibrotic muscles, but a component of paresis can also be a factor. As with thyroid- related strabismus, the surgical procedure of choice is a recession of the tight rectus muscle. Resections should be avoided. These CFEOM cases can be technically difficult because exposure of the muscle is limited, especially in cases with a fibrotic medial rectus muscle. The etiology of CFEOM is unknown, but the syndrome is associated with atrophic and fibrotic changes of the extraocular muscles.33 Light and electron microscopy demonstrated replace- ment of normal muscle with collagen, dense fibrous tissue, and areas of degenerated skeletal muscle (CFEOM 29, 30, 31).125 Research suggests that the cause of congenital fibrosis of the extraocular muscles is an abnormality in the development of the extraocular muscle lower motor neurons, with agenesis of the third nerve being most common (CFEOM 1, 14, 11, 10).109 Nakano et al. reported finding three mutations in ARIX gene (also known as PHOX2A) in four pedigrees of congenital fibrosis of the extraocular muscles type 2 (CFEOM 2).79,123 ARIX 340 handbook of pediatric strabismus and amblyopia

FIGURE 10-6. Patient with congenital fibrosis syndrome and a large angle esotropia. There was severe limitation to abduction, bilaterally, and forced ductions at the time of surgery show severe restriction to abduction in both eyes. Bilateral medial rectus recessions (7.0 mm) resulted in good alignment with improved abduction. encodes a homeodomain transcription factor protein shown to be required for development of cranial nerves III and IV in mouse and zebrafish. These findings confirm the hypothesis that CFEOM 2 results from the abnormal development of cranial nerves III and IV and emphasize a critical role for ARIX in the development of these midbrain motor nuclei.37,79

Double Elevator Palsy or Monocular Elevation Deficit Syndrome Double elevator palsy is classically defined as a congenital inability to elevate one eye, with the limitation occurring in adduction and abduction (Fig. 10-7). One might question why double elevator palsy is included under restrictive strabismus. The term double elevator palsy is a misnomer because, in most cases, the cause for the limited elevation is not a palsy of both elevators but is a tight inferior rectus muscle. Studies using saccadic velocity measurements and forced ductions showed that approximately 70% of patients diagnosed as having a double elevator palsy actually had limited elevation as a result of inferior rectus restriction, not a palsy of the superior rectus and inferior chapter 10: complex strabismus 341 oblique muscles.73,106 A more descriptive term now used is monocular elevation deficit syndrome (MED). MED may be mistaken for Brown’s syndrome, although the limited elevation is worse in adduction than abduction in the latter. Patients with MED present with a hypotropia, a chin elevation, and, often, an ipsilateral ptosis. True congenital ptosis is present in 25% of cases whereas pseudo-ptosis may occur in almost all patients with a large hypotropia.2 In those cases with a true double elevator palsy and a lack of an upgaze saccade, forced ductions at time of surgery usually reveal a tight inferior rectus muscle coexisting with the superior rectus palsy. An interesting finding in approximately 25% of patients with double elevator palsy and congenital ptosis is the Marcus Gunn jaw-winking phenomenon.133 This association indicates a congenital misdirection syndrome involving the oculomotor nerve. It is possible that, as with congenital fibrosis syndrome, the cause of the tight inferior rectus and, in some cases, superior rectus and inferior oblique palsy, is abnormal development of cranial nerves (including the oculomotor nerve) with secondary muscle fibrosis. Surgery for MED is indicated if a significant hypotropia is present in primary position with an associated chin elevation. The type of surgery depends on the cause of the elevation deficit (Table 10-3). If the etiology is a tight inferior rectus muscle and the upgaze saccade is normal, recess the ipsilateral inferior rectus muscle, usually around 5 to 6mm depending on the size of the hypotropia. It is important to evaluate preoperatively for the presence of an upgaze saccade and to perform forced ductions at the time of surgery to make the correct procedural choice. Lack of upgaze saccades, combined with a weak superior rectus muscle on forced generation testing, indicates a true

ABC FIGURE 10-7A–C. Double elevator palsy (monocular deficit syndrome). Child has had limited elevation of the right eye since birth. Note that elevation of right eye is worse in abduction (A) than it is in adduction (C). Patient is fixing with the involved right eye so the left eye is hypertropic as per Hering’s law of yoke muscles (B). Preoperatively, this patient had intact upgaze saccades and a tight inferior rectus muscle on forced- duction testing at the time of surgery. The elevation deficit was success- fully treated with a right inferior rectus muscle recession of 6.5 mm. 342 handbook of pediatric strabismus and amblyopia

TABLE 10-3. Treatment of Double Elevator Palsy (Monocular Elevation Deﬁcit Syndrome). • Tight inferior rectus muscle: good superior rectus function Recess ipsilateral inferior rectus muscle (5–6 mm) • Superior rectus palsy Recess ipsilateral inferior rectus muscle and ipsilateral transposition of half the medial and lateral rectus muscles up to the superior rectus insertion (preferred by author) or Knapp procedure: full-tendon transfer up to the superior rectus muscle

double elevator palsy. In these cases, a recession of the ipsilateral inferior rectus will not correct the hypotropia. Treatment of a true double elevator palsy with weak superior rectus muscle is to perform a transposition of the ipsilateral medial and lateral rectus muscles up to the superior rectus muscle. In patients with the superior rectus palsy type of MED, forced ductions are often positive, and the ipsilateral inferior rectus muscle should be recessed. This author prefers the partial tendon transfer (Hummelsheim) instead of the full-tendon transposition (Knapp) to avoid the possible complication of anterior segment ischemia that can occur up to 20 years after strabismus surgery. In severe cases of hypotropia over 15PD, consider adding a recession of the contralateral superior rectus muscle.

Orbital Floor Fracture Signs of a blowout fracture include diplopia secondary to restricted vertical eye movement, enophthalmos, and numbness of face below the traumatized orbit and along the upper teeth. Restrictive strabismus with limited elevation in orbital floor fractures is caused by entrapment of fat and the inferior rectus muscle at the fracture site (Fig. 10-8). Repair of the floor fracture in most cases will improve ductions. In addition to limited elevation, there can be limited depression on the side of the fracture, often associated with a posterior fracture.108 The cause of the limited depression could be contributed to scarring of the inferior rectus to the floor, thus preventing the inferior rectus muscle from transmitting its contractual pull to the globe. Adherence of the inferior rectus to the floor would also isolate the muscle anterior to the fracture and cause the anterior muscle to slacken on attempted downgaze, producing pseudoinferior rectus palsy. These patients characteristically have a small chapter 10: complex strabismus 343 hypertropia in primary position, underaction of the inferior rectus muscle, and a large hypertropia in downgaze. The key to the diagnosis of a pseudoinferior rectus palsy is normal inferior rectus muscle function and normal saccades when the eye moves from upgaze to primary position, with inferior rectus muscle weakness and slow ocular movements from primary position to downgaze. Treatment of pseudoinferior rectus palsy is to repair the floor fracture. If this does not relieve symptoms, then strabismus surgery is indicated. This author has found that a small (3–4 mm) ipsilateral inferior rectus muscle tightening procedure (Wright plication or resection) helps to eliminate the anterior muscle slack. A contralateral inferior rectus recession works well and produces only a slight limitation of elevation. If the muscle is captured in a trap-door fracture, direct damage to the inferior rectus muscle occurs and can truly weaken the inferior rectus muscles. Small trap-door floor fractures can pinch and strangle the inferior rectus muscle, causing necrosis and muscle damage.11 Because of the potential for permanent damage, some advocate immediate repair within the first few days if there is imaging evidence that the inferior rectus is entrapped.29 Strabismus surgery should be performed after reconstructive orbital surgery. If orbital reconstruction is not indicated, and the patient has persistent diplopia 4 to 8 weeks after the trauma, then strabismus surgery is indicated. The strabismus surgical plan depends on the pattern of the strabismus. Table 10-4 lists patterns of strabismus and their associated treatment.

Myotoxic Effect of Local Anesthetics Injection of local anesthetics such as lidocaine and marcaine into an extraocular muscle can result in myotoxic damage to the muscle and cause strabismus.19,40,46 Elderly patients are especially susceptible to the myotoxic effects of local anesthetics. Immediately after the injection of a local anesthetic into an extraocular muscle, there is an acute paresis of the muscle that lasts for one to several days. Over the next few weeks, localized segmental intramuscular fibrosis occurs secondary to local myotoxicity of the anesthetic. The fibrosis results in a tight and contracted muscle. What is particularly interesting is that, in some cases, the injected muscle overacts, producing a deviation that increases in the field of action of the injected muscle.8,13 This deviation is in contrast to the restriction pattern usually 344 handbook of pediatric strabismus and amblyopia

B FIGURE 10-8A–B. Orbital ﬂoor fracture left eye with entrapment of fat and the inferior rectus muscle. (A) In primary gaze, there is no signiﬁcant deviation. (B) Restricted elevation of left eye in upgaze causes a large right hypertropia. chapter 10: complex strabismus 345

C FIGURE 10-8C. (C) CT scan shows herniation and entrapment of inferior orbital fat into the maxillary antrum. Note that, after removal of the fat and repair of the fracture, the restriction resolved. expected with a tight muscle, where the deviation is greatest in the gaze opposite to the ﬁeld of the muscle’s action. The cause of the muscle overaction is thought to be secondary to intramuscular ﬁbrosis, with stretching of the Z-bands and enhancing

TABLE 10-4. Orbital Floor Fracture: Surgical Plans. Tight inferior rectus muscle (hypotropia) • Small hypotropia (8 PD) in primary position, no deviation in downgaze, and larger hypotropia in upgaze (tight inferior rectus muscle): Asymmetrical bilateral inferior rectus muscle recessions, with a larger ipsilateral recession Add a contralateral superior rectus recession for a large hypotropia in upgaze • Large hypotropia in primary position, worse in upgaze (tight inferior rectus muscle): Hypotropia 8 to 15 PD: recess ipsilateral inferior rectus muscle (3.5–5.0 mm) Hypotropia 15 PD: recess ipsilateral inferior rectus muscle (5–6 mm) PLUS a contralateral superior rectus recession (4–6 mm) Pseudoinferior rectus muscle palsy (hypertropia) • Hypertropia in primary position increases in downgaze with ipsilateral limited depression; intact saccades from upgaze to primary position: Plication of the ipsilateral inferior rectus (3 mm) PLUS contralateral inferior rectus recession (4–5 mm) 346 handbook of pediatric strabismus and amblyopia the action and myosin interaction.19 The fibrosis acts to stretch the muscle fibers that subsequently increases their force, per the Starling’s length tension curve.19 For example, inadvertent injection of the inferior rectus muscle associated with a retrobulbar injection of anesthetic initially results in an ipsilateral hypertropia because of an inferior rectus paresis. Over a few weeks, this changes into an ipsilateral hypotropia with overaction of the inferior rectus muscle, resulting in the hypertropia being greatest in downgaze. Any of the extraocular muscles can be infiltrated during a retrobulbar or peribulbar injection of local anesthetics, with the superior and inferior rectus muscles most commonly affected. One of the findings is segmental enlargement of the injected muscle seen on orbital imaging. Hamed and Mancuso46 reported on eight patients with an ipsilateral hypotropia after a retrobulbar injection of anesthetic, with three patients showing segmental enlargement of the inferior rectus muscle. The treatment is to recess the tight or overacting muscle. This method has produced excellent results, especially in the cases involving an overacting injected muscle, with the deviation larger in the field of action of the muscle. One can help prevent intramuscular injection injury by injecting into the orbital quadrant away from the extraocular muscles, using a blunt cannula and limiting anesthetic volume. The incidence of strabismus after cataract surgery has diminished dramatically since the widespread use of topical anesthesia during surgery.

Strabismus After Retinal Surgery Strabismus can occur virtually after every known retinal surgical procedure.38,57,71,72,103,111,114 The strabismus is usually transient; however, persistent strabismus occurs in approximately 7% of scleral buckling procedures.71,117 Common causes of strabismus after retinal detachment surgery include fat adherence and restriction, a lost or slipped muscle, a displaced superior oblique tendon, a large explant under a rectus muscle, and ectopic fovea.38,47,57,85,110 Other causes of strabismus after retinal surgery include patients with preexisting strabismus before the retinal surgery who then experience sensory strabismus secondary to loss of vision.92,130 Of all the causes of persistent restriction after retinal detachment surgery, fat adherence and periocular scarring is by far the most common and most difficult to treat.1,57,134 Fat adherence is difficult to treat because there chapter 10: complex strabismus 347 is no synthetic substitute to recreate the natural boundary between the orbital fat and the eye and muscle once Tenon’s capsule is violated. Occasionally, a lost muscle is associated with postretinal surgery, as can occur when the traction sutures around the muscle are pulled to gain posterior exposure during the retinal surgery. In elderly patients, the muscle is relatively weak, and overzealous traction on the rectus muscle can result in a splitting of the muscle; this has been termed pulled-in-two syndrome (PITS). Spontaneous disinsertion and posterior slippage of a rectus muscle behind an encircling buckle can also occur, without removal of the muscle at the time of retinal surgery.47,57 In these cases, the silicone band will cheese-wire through the muscle insertion over several months postoperatively, resulting in late slippage of the muscle behind the buckle and causing an underaction of the slipped muscle. The slipped rectus muscle can almost always be found attached to sclera at the posterior edge of the encircling buckle or connected to sclera by a pseudo- tendon. Appropriate treatment is to advance the muscle and reattach the muscle with nonabsorbable suture. Another cause for strabismus after retinal surgery is an oblique muscle that has been displaced anteriorly by an encircling band.57,72 Placement of the band behind the superior oblique tendon pulls the superior oblique tendon anteriorly to the nasal aspect of the superior rectus insertion. The superior oblique tendon now inserts at the nasal side of the superior rectus insertion, anterior to the equator. The new anterior insertion of the superior oblique tendon changes the action of the superior oblique muscle from a depressor to an elevator. These patients typically present with a hypertropia and limitation of depression of the involved eye. Forced ductions, however, show relatively mild restriction to depression as compared to the limitation on ductions and versions. Treatment is to release the entrapped superior oblique tendon from the buckle or, if there is severe scarring, perform a superior oblique tenotomy. If the hypertropia is greater than 5PD in primary position, also perform a recession of the contralateral inferior rectus muscle (consider adjustable suture). The inferior oblique muscle can also be entrapped by an encircling element.57 In this case, the element is passed behind, or splits, the inferior oblique muscle. When the band is tied in place, the muscle is pulled anteriorly, resulting in a hypotropia and excyclotropia. The hypotropia occurs because the inferior oblique is displaced anteriorly to the 348 handbook of pediatric strabismus and amblyopia equator, pulling the front of the eye down. The excyclotropia is caused by the increased tension on the inferior oblique muscle. Torsional diplopia after retinal surgery is not always associated with an entrapped oblique muscle.23 Metz and Norris found two of four patients with torsional diplopia after retinal surgery to have no identifiable abnormality of the oblique muscle.72 The complications of oblique muscle entrapments can be diminished by passing the encircling elements anteriorly, just behind the rectus insertions. Extreme posterior passage of the muscle hook may result in inadvertent hooking of an oblique muscle, especially when working on the superior rectus and lateral rectus muscles. The placement of a retinal explant sponge or buckle is often identified as a primary cause for strabismus after retinal surgery. Transient strabismus after a retinal encircling procedure is fre- quent, occurring in approximately 20% of cases. In our experience, however, a retinal encircling element by itself rarely causes persistent strabismus. Persistent strabismus after retinal surgery usually results from secondary scarring or a displaced muscle, as stated previously.78 Infrequently, however, a retinal explant may be the primary cause of restriction; this occurs when a large explant is placed directly under a rectus muscle. The explant causes the muscle to deviate from its normal course, thus tightening the muscle. For example, a large retinal sponge placed directly under the medial rectus will cause a tightening of the medial rectus, as the medial rectus courses over the large sponge and produces an esotropia. Low-profile encircling elements, such as 240 bands that indent the sclera, do not inter- fere with the course of the rectus muscle and, therefore, do not produce strabismus. Foveal ectopia occurs in association with macular pucker, peeling of the epiretinal membrane, and retinal translocation surgery. Acquired foveal ectopia produces an interesting type of strabismus and diplopia. These patients will observe that objects in the central visual field appear double, with one image being distorted by metamorphosia. Objects in the peripheral field, however, will often be fused, as the peripheral retina may not be involved with the ectopia. Thus, patients who undergo membrane peeling for a macular pucker may experience postoperative diplopia because of foveal ectopia. The image disparities tend to be small with this condition, and prism glasses have been found to be effective in treating this problem. chapter 10: complex strabismus 349

Retinal translocation surgery can result in severe torsional diplopia that prisms cannot correct. Instead, oblique muscle surgery is required to treat the problem.38 Extorsion is induced from macular inferior translocation, and intorsion is secondary to superior macular translocation. Extorsion can be corrected by a large Harada–Ito procedure, possibly with an inferior oblique weakening procedure, whereas intorsion can be corrected with a weakening surgery of the superior oblique muscle, perhaps with a tuck of the inferior oblique muscle. Vertical offset of the rectus muscle can also change torsion, but one must consider the risk of anterior segment ischemia in this group of patients.

Glaucoma Explants and Strabismus The incidence of strabismus after glaucoma explant surgery ranges from 10% to 70%, depending on the study.7,90,112 The cause of the strabismus is, for the most part, the large bleb created by the glaucoma explant. Strabismus associated with a large filtering bleb may be caused by the following mechanisms: (1) orbital mass, which displaces the eye (Fig. 10-9); (2) a mass directly under a muscle or tendon; or (3) scarring or adhesions secondary to the surgical dissection during placement of the glaucoma explant. The old Baerveldt implant had been associated with the highest incidence of strabismus; however, modifications of the Baerveldt implant (fenestrated Baerveldt) have reduced the bleb size and subsequently reduced the incidence of strabismus. Valved implants have also reduced the size of the filtering blebs and have subsequently produced the lowest incidence of strabismus. A large explant in the superior nasal quadrant may cause a pseudo-Brown’s syndrome with restricted elevation in adduction, as the bleb displaces and tightens the superior oblique tendon.7,90 Placement of glaucoma explants should be super- otemporal rather than superonasal to avoid the problem of a secondary Brown’s syndrome. The treatment of a bleb-induced strabismus is to reduce the size of the bleb by suturing the bleb wall to the explant so it cannot expand. Additionally, the old explant can be replaced with a newer valved explant. An interesting observation of some patients with strabismus and severe glaucoma is that they do not experience diplopia but, instead, have visual confusion.57 Visual confusion is the simul- taneous perception of two different foveal images in a patient 350 handbook of pediatric strabismus and amblyopia

B FIGURE 10-9A,B. Patient with a glaucoma explant in the left superior temporal quadrant. The glaucoma was controlled; however, it produced a large bleb that limited abduction. (A) Patient is looking left, and the left eye shows severe restriction (4) to abduction. (B) Large temporal bleb is causing a mass effect and restricting abduction of the left eye. chapter 10: complex strabismus 351 with strabismus. These patients see the superimposed images from each fovea. Patients with end-stage glaucoma have tunnel vision and lose their peripheral visual ﬁeld. If these patients acquire strabismus, they may experience confusion rather than a true diplopia, as they only have central vision and are forced to use the fovea of each eye.

High Myopia and Esotropia (Myopic Strabismus Fixus) High myopia, usually greater than 20 diopters, can be associated with an acquired large-angle esotropia along with limited abduction and a hypotropia9,25,50,63,116; this is a form of acquired strabismus fixus and can be either monocular or binocular. Another term for the high myopia esotropia syndrome is heavy eye syndrome, with hypotropia and limited eye movement.116 Restricted abduction is dramatic, and there is limited elevation of the hypotropic eye. Orbital imaging shows an extremely large globe with a posterior staphyloma that fills the orbit, a large inferior displacement of the lateral rectus muscle, and a mild nasal displacement of the superior rectus muscle. The cause of the esotropia and hypotropia is a combination of restriction, because of the massive expansion of the posterior globe against a tight medial rectus muscle, and displaced lateral and superior rectus muscles that change the normal vector forces. Displacement of the lateral rectus muscle inferiorly and superior rectus muscles nasally is most likely caused by the massive expansion of the posterior aspect of the globe into the superior temporal quadrant.64 The lateral rectus muscle shows the most displacement, probably due to the laxity of its pulley system. Slippage of the lateral rectus muscle below the globe weakens the abduction vector and pulls the eye down, thus contributing to the esotropia and hypotropia. The nasally displaced superior rectus muscle also contributes to the esotropia and hypotropia by pulling the eye nasally and diminishing the elevation vector force. Treatment is aimed at realigning the lateral rectus muscle and releasing the medial rectus muscle, which is inevitably tight. This author prefers a large recession of the medial rectus muscle, at least 7 to 8mm on a hang-back suture, and a superior transposition of the lateral rectus muscle with a small resection. The posterior sclera is thin in these cases, and access to the posterior globe is difficult because of the large eye. The hang- back suture of the medial rectus allows for a large recession 352 handbook of pediatric strabismus and amblyopia without passing a posterior suture. Union of the superior and lateral rectus has also been described.

SPECIFIC TYPES OF PARALYTIC STRABISMUS

Sixth Nerve Palsy A persistent, isolated, congenital sixth nerve palsy is extremely rare; however, newborns may have a transient sixth nerve palsy that resolves spontaneously over a few days to a few weeks. A common cause of isolated acquired sixth nerve palsy in early childhood is postviral inﬂammatory neuropathy, which may occur 1 to 3 weeks after a viral illness or immunization or spontaneously without obvious cause. These patients should be followed closely to monitor their improvement and watch for the development of amblyopia. Improvement usually occurs within 6 to 10 weeks. After viral or idiopathic causes, the next most common causes of acquired sixth nerve palsy in children and young adults include closed head trauma and intracranial neo- plasms. Neuroimaging is indicated for acquired sixth nerve palsy if the palsy does not improve rapidly or if other neurological signs are present. Other causes of an acquired sixth nerve palsy include Gradenigo’s syndrome (mastoiditis and sixth nerve palsy), meningitis, myasthenia gravis, and cavernous sinus disease. Sixth nerve palsy is typically associated with limited abduction and an esotropia that increases upon gaze to the side of the palsy (Fig. 10-10). On attempted abduction, there is relative lid ﬁssure widening because both the medial and lateral rectus muscles are relaxed on attempted adduction and the posterior orbital pressure proptoses the eye. Remember that, on attempted abduction, the medial rectus muscle is inhibited (Sherrington’s law). Mild sixth nerve paresis may allow relatively good lateral rectus function and show only a trace limitation of abduction. These patients, however, will have a pattern of divergence paresis with an esotropia that is greater in the distance than at near. The divergence paresis pattern should alert the examiner to the possibility of a sixth nerve paresis. Initial therapy of a traumatic or vascular sixth nerve palsy is observation for 6 months while monitoring the patient for spontaneous recovery. Spontaneous recovery of traumatic sixth chapter 10: complex strabismus 353

B FIGURE 10-10A,B. (A) Photographs of a child with a traumatic right sixth nerve palsy and poor lateral rectus function, evidenced by absent abduction saccades and severe limitation of abduction of the right eye. There is 4 limitation of abduction as the right eye does not go past midline. (B) Results after surgery consisting of a right Hummelsheim transposition and a right medial rectus recession of 6.0 mm. Note the eyes are orthotropic in primary position. There is improved abduction, but abduction remains limited.

nerve palsy is approximately 80% for unilateral cases and 40% for bilateral cases.53 A complete palsy at the initial presentation and bilateral involvement indicate a poor prognosis for recovery.52 During the observation period, alternate monocular occlusion or press-on prisms can be used to eliminate diplopia if a face turn does not allow fusion. To prevent secondary contracture of the medial rectus muscle and increase the chances for recovery, some advocate the use of botulinum injection into the ipsilateral medial rectus muscle.10,74 Botulinum paralyzes the muscle for 3 to 6 months, thus preventing contracture. The hope is that preventing secondary contracture of the medial rectus muscle will increase the chances of recovery without strabismus surgery. The use of botulinum remains controversial, however. Studies comparing botulinum to conservative treatment for the management of nerve palsy have shown no significant difference in recovery rates.53,65 Holmes et al., in a prospective multicenter study of acute traumatic sixth nerve palsy or paresis, reported that patients treated either with botulinum or conservatively had similarly high recovery rates.53 It should be noted that, after a botulinum injection into the medial rectus muscle for a complete sixth nerve palsy, both the medial and lateral rectus will be paralyzed, resulting in essentially no horizontal movement of the paretic eye. Therefore, the patient 354 handbook of pediatric strabismus and amblyopia should be warned that the paretic eye may have decreased movement after the injection. In addition, the surgeon should be aware that the effects of botulinum can last more than 6 months, and surgery should be delayed until the botulinum has dissipated. After the 6-month observation period, lateral rectus muscle function should be evaluated, as this is critical for determining the surgical plan. Lateral rectus muscle function can be assessed by saccadic velocity testing and the active forced-generation test. If the saccadic velocities are less than 60% of normal or the active forced-generation test is estimated to be half of the normal fellow eye, a vertical rectus muscle transposition procedure is indicated. Transposition procedures act by moving innervated vertical rectus muscles to the lateral rectus insertion to provide lateral force. The lateral force of the transposition does not appropriately activate on attempted abduction but, instead, provides a constant lateral force. Transposition of vertical rectus muscles can involve the full muscle (full-tendon transfer) or the muscle can be split longitudinally and only half the muscle is transferred (partial-tendon transfer). In addition to a transposition, patients with significant residual paresis almost always require an ipsilateral medial rectus recession to reduce adduction forces. The vertical rectus muscles provide substantial circulation to the anterior segment. Older adult patients, especially those with arteriosclerotic disease or hyperviscosity syndromes, are at risk for developing anterior segment ischemia after vertical recti transposition, particularly those receiving full-tendon transfers. A partial-tendon transfer procedure should be considered in these patients to maintain anterior circulation and prevent anterior segment ischemia. Modifications of the Hummelsheim partial-tendon transposition include suturing the transposed vertical muscle to the lateral and resecting a few millimeters of the transposed vertical muscle halves.18,82 An important aspect of the partial-tendon transfer is to fully mobilize the muscle being transferred by splitting the vertical rectus muscles for at least 14mm posterior to their insertions.135 If carefully performed, a partial-tendon transfer procedure results in long-term good postoperative eye alignment while reducing the risk of anterior segment ischemia. Other options include full-tendon transposition with injection of botulinum toxin to the medial rectus chapter 10: complex strabismus 355

TABLE 10-5. Surgical Treatment for Sixth Nerve Palsy. Clinical presentation Surgery Excellent lateral rectus function Recess contralateral medial rectus (90%–100%): 5–6 mm (adjustable suture optional) Ductions trace limitation ET in primary position 2 to 8 PD Diplopia to the side of the palsy Good lateral rectus function (80%–90%) Bilateral medial rectus recessions, but Ductions 1 recess the contralateral medial ET in primary position 10 to 20 PD rectus muscle 6 mm and the ipsilateral medial rectus muscle 3–5 mm (adjustable suture advised) Fair lateral rectus function (60%–80%) Ipsilateral medial rectus recession Ductions 2 6 mm (adjustable suture advised); lateral rectus resection or Wright plication 5 mm and contralateral medial rectus recession ET in primary position 20 to 30 PD 3–5 mm (with optional Faden)

Poor lateral rectus function (Ͻ60%) Ipsilateral medial rectus recession Ductions 3 to 4 6–7 mm (adjustable suture in adults or cooperative children), and vertical rectus partial-tendon transposition ET in primary position 30 PD to the lateral rectus muscle (either Jensen or Hummelsheim); author prefers modiﬁed Hummelsheim

ET, exotropia. muscle.102 This treatment, however, may not provide a stable outcome, as an esotropia may recur after 4 to 6 months when the effect of the botulinum dissipates and medial rectus function returns. This author’s recommendations for the surgical treatment of sixth nerve palsy are listed in Table 10-5.

Duane’s Retraction Syndrome The cause of Duane’s retraction syndrome (DRS) has been iden- tiﬁed to be an agenesis of the sixth nerve and nucleus, with the inferior division of the oculomotor nerve (nerve to the medial rectus muscle) splitting to innervate both the medial and lateral rectus muscles.19,31 Because both the medial and lateral rectus muscles are innervated by the nerve to the medial rectus muscle, both muscles ﬁre and contract simultaneously on attempted adduction. This cocontraction of the medial and lateral rectus muscles on adduction gives rise to the term 356 handbook of pediatric strabismus and amblyopia

Duane’s cocontraction syndrome. Cocontraction of the lateral rectus muscle against the medial rectus muscle on adduction causes globe retraction, producing relative enophthalmos and lid ﬁssure narrowing.94 There are various patterns of innervation that account for the four types of Duane’s syndrome. Figure 10-11 shows a diagram of various patterns of abnormal innervation possible in DRS. Table 10-6 explains the various types of DRS as they cor- relate to the innervation patterns noted in Figure 10-11. In Duane’s type I, there is agenesis of the sixth nerve and the sixth nerve nucleus, with part of the medial rectus branch of the third nerve going to the lateral rectus muscle. Because most of the medial rectus branch of the third nerve appropriately goes to the medial rectus muscle, the eye will adduct with cocontraction by the aberrantly innervated lateral rectus muscle. This contraction causes lid ﬁssure narrowing; however, because of the absent

A B C D FIGURE 10-11A–D. Diagrammatic representation of misdirection of nerve ﬁbers in Duane’s syndrome. The aberrant nerve pathway is shown in red, and the dotted lines represent nerve hypoplasia or agenesis. (A) type I: poor abduction and good adduction. Agenesis of the sixth nerve and part of the third nerve splits to innervate both the medial and the lateral rectus muscles, but most of the medial rectus nerve goes to the medial rectus muscle so adduction is intact. (B) Type II: poor adduction and good abduction. Sixth nerve is intact and innervates the lateral rectus muscle, but the medial rectus nerve splits to innervate the medial and lateral rectus muscles. There is poor adduction because the lateral rectus contracts against the medial rectus muscle. (C) Type III: poor adduction and poor abduction. Agenesis of the sixth nerve and part of the third nerve splits to innervate both the medial and the lateral rectus muscles. The split is equal so the eye does not move in or out. (D) Synergistic divergence and paradoxical abduction on attempted adduction. Agenesis of the sixth nerve and part of the third nerve splits to innervate both the medial and the lateral rectus muscles, but most of the medial rectus innervation goes to the lateral rectus muscle. When the eye attempts to adduct, it abducts because the medial rectus nerve innervates the lateral rectus muscle. chapter 10: complex strabismus 357

TABLE 10-6. Classification of Duane’s Syndrome. Type I Duane’s: most common Poor abduction and good adduction. The medial rectus muscle receives most of the medial rectus nerve innervation and the lateral rectus receives minimal innervation from the medial rectus nerve, with agenesis of the sixth nerve. Because the medial rectus receives most of the innervation, the Duane’s eye is usually fixed in an adducted position with an esotropia in primary position, and there is a compensatory face turn in the direction of the Duane’s eye (i.e., left face turn for a left Duane’s type I). Type II Duane’s: least common, extremely rare Poor adduction and good abduction. EMG recordings show the lateral rectus muscle to contract appropriately on abduction, but it also contracts paradoxically on adduction; this probably represents a partial innervation of the lateral muscle by the sixth nerve nucleus (as purposeful abduction is present), plus splitting of the medial rectus nerve to innervate the medial and lateral rectus muscles. Type III Duane’s: second most common Poor adduction and poor abduction (the eye has little horizontal movement). Equal innervation of the medial and lateral rectus muscles by the medial rectus nerve, with congenital absence of the sixth nerve. Because the medial and lateral forces are similar, the eye will rest in approximately primary position and there will be no significant face turn. In some cases, an exotropia is present in primary position because the lateral rectus receives slightly more innervation than the medial rectus muscle; this causes a face turn away from the Duane’s eye. Synergistic divergence: extremely rare Paradoxical abduction on attempted adduction and poor abduction. Little or no innervation of the lateral rectus by the sixth nerve. Most of the medial rectus nerve goes to the lateral rectus muscle. On attempted adduction, the lateral rectus is stimulated by the medial rectus nerve and the eye paradoxically abducts.

sixth nerve, there is no abduction (Fig. 10-12). If the medial rectus nerve equally innervates the medial and lateral rectus muscles, then the cocontraction of the lateral rectus muscle will equal the appropriate contraction of the medial rectus muscle, and the eye will have limited adduction in addition to limited abduction because of the sixth nerve agenesis. This pattern of poor adduction and abduction is typical of Duane’s type III (Fig. 10-13). In the rare Duane’s type II syndrome, abduction is intact but is limited because part of the sixth nerve innervates the lateral rectus muscle and part of the medial rectus nerve innervates the lateral rectus muscle. Another rare form of Duane’s syndrome is synergistic divergence. In this syndrome, most of the third nerve that should innervate the medial rectus muscle aberrantly innervates the lateral rectus muscle, causing the Duane’s eye to paradoxically abduct on attempted adduction.124 358 handbook of pediatric strabismus and amblyopia

FIGURE 10-12. Duane’s syndrome type I, left eye. Inset shows a face turn to the left, eyes shifted left to maintain binocular fusion. Composite shows limited abduction in left eye, esotropia in primary position, and lid fissure narrowing of left eye on adduction. Note that in primary position the Duane’s eye (left eye) is fixing so there is a secondary esodeviation of the right eye. A positive Brückner reflex is seen from the esotropic right eye.

FIGURE 10-13. Composite photograph of a child with Duane’s syndrome type III, right eye. There is almost no adduction or abduction in the right eye, and the right eye is ﬁxed in the abducted position. Lid ﬁssure narrowing of right eye occurs on attempted adduction. In primary position, there is an exotropia and this patient adopts a compensatory face turn to the left to keep the eyes aligned in right gaze. chapter 10: complex strabismus 359

A patient with right synergistic divergence will diverge and have a large exotropia on attempted leftgaze.124 Duane’s syndrome is present at birth and is usually unilateral, but it can be bilateral.54 If there is a deviation in primary position, patients with DRS will adopt a compensatory face turn to obtain binocular fusion. The face turn is determined by the resting position of the Duane’s eye. If the medial and lateral rectus muscles receive comparable innervation from the split oculomotor nerve and the eye is centered in primary position, there will be no significant face turn (Duane’s type III). If, however, the medial rectus muscle receives most of the innervation from the oculomotor nerve, then the affected eye will rest in adduction and the patient will have an esotropic DRS with a face turn toward the side of the affected eye (Duane’s type I). Less commonly, the lateral rectus will receive most of the innervation from the oculomotor nerve. In these cases, the Duane’s eye will be abducted, causing an exotropia (XT) in primary position and a face turn toward the opposite side of the Duane’s eye (Duane’s type III with an XT).94 Duane’s syndrome may be associated with an upshoot or a downshoot on attempted adduction, which may resemble inferior oblique and superior oblique overaction (Fig. 10-14). Studies utilizing EMGs have identified a variety of aberrant innervation patterns that explain the vertical movements on adduction.55,107,115 In some cases, the upshoot and downshoot are caused by strong, inappropriate firing of the lateral rectus muscle on adduction. This leash effect pulls the eye up or down, as the eye rotates slightly up or down past the horizontal plane. In other cases, the vertical recti are aberrantly innervated by part of the medial rectus nerve, so the vertical muscle fires on adduction. Other oculomotor misdirection syndromes are associated with Duane’s syndrome, such as Marcus Gunn jaw-winking. Duane’s syndrome is associated with numerous systemic syndromes including Goldenhar’s syndrome, Klippel–Feil syndrome, maternal thalidomide ingestion, fetal alcohol syndrome, and oculocutaneous albinism.31

SURGICAL EVALUATION Indications for surgery in DRS include (1) signiﬁcant misalign- ment of the eyes in primary position, (2) noticeable abnormal head position, (3) narrowing of palpebral ﬁssure due to retrac- 360 handbook of pediatric strabismus and amblyopia

B FIGURE 10-14A,B. Photographs of an upshoot (A) and downshoot (B), right eye, occurring on attempted adduction associated with Duane’s syndrome of right eye. tion, and (4) significant upshoot or downshoot. Usually, surgery is electively performed around age 3 to 8 years, as these patients have excellent fusion and the condition is stable. Rarely will a DRS patient have amblyopia and, when present, it is almost always associated with anisometropia. Amblyopia should be chapter 10: complex strabismus 361 the first priority in these unusual cases. In general, muscle resections should be avoided in DRS, because resections can make the cocontraction and lid fissure narrowing worse.

SURGERY FOR DRS TYPE I WITH ESOTROPIA AND IPSILATERAL FACE TURN In cases with esotropia and Duane’s type I, the Duane’s eye is in an adducted position and there is a face turn toward the Duane’s eye. The medial rectus muscle is usually contracted and tight. The simplest, most effective treatment for Duane’s type I with esotropia is an ipsilateral medial rectus recession (between 5.0 and 7mm). In adult patients, place the medial rectus muscle on an adjustable suture and adjust to a 5° to 10° overcorrection so there is a small exotropia in primary position; this results in stable long-term correction of the face turn. Remember, the lateral rectus muscle is not denervated, as in the case of a sixth nerve palsy, but has innervation provided by part of the medial rectus nerve. This tonic innervation provides stabilizing abduction force, so a muscle transposition procedure is not required. Some have advocated a transposition of the vertical rectus muscles laterally for DRS and esotropia. This procedure is more invasive and has the risk of producing anterior segment ischemia. The transposition procedure also has a risk of inducing a vertical deviation in approximately 15% of patients. This author prefers the simple and effective ipsilateral medial rectus recession for Duane’s type I with esotropia.

SURGERY FOR DRS TYPE III WITH EXOTROPIA AND CONTRALATERAL FACE TURN In a patient with Duane’s and exotropia, it is almost always a Duane’s type III. The eye is resting in abduction, and the face turn is away from the Duane’s eye. There is usually a tight lateral rectus muscle, and these patients require an ipsilateral lateral rectus recession. If there is an upshoot or downshoot associated with the Duane’s type III, then consider a Y-split procedure with the lateral rectus recession.

TREATMENT OF GLOBE RETRACTION Globe retraction can be diminished by recessing both the ipsilateral medial rectus and lateral rectus muscles. In patients with esotropic DRS and severe globe retraction, add a lateral rectus recession, but recess the medial rectus muscle more than the lateral rectus to compensate for the esotropia. In exotropic DRS, 362 handbook of pediatric strabismus and amblyopia recess the lateral rectus more than the medial rectus muscle or, for a large exotropia, recess only the lateral rectus muscle (large recession). For orthotropic DRS without a face turn, recess the medial and lateral rectus muscles the same amount.

TREATMENT OF UPSHOOT AND DOWNSHOOT Two approaches to reduce upshoot and downshoot associated with DRS include these: 1. Y-splitting with recession of the lateral rectus muscle 2. Posterior fixation suture (Faden) of the lateral rectus and appropriate recession of horizontal recti The Y-splitting procedure of the lateral rectus muscle works by placing some of the lateral rectus muscle above and below the horizontal midline, thus preventing an upshoot or downshoot when the eye is in adduction.95,100 By combining a recession of the lateral rectus muscle with the Y-split, one can treat both an exotropia Duane’s type III with an upshoot and downshoot. In patients with orthotropic DRS and a severe upshoot and downshoot, recess the ipsilateral medial rectus muscle along with a recession and Y-split of the ipsilateral lateral rectus muscle. The posterior fixation suture acts to stop slippage of the lateral rectus muscle when the eye rotates up or down, and a concurrent recession reduces cocontraction. The authors have found the Y- splitting procedure is more effective than the posterior fixation suture.

Fourth Nerve Palsy (Superior Oblique Palsy) See Chapter 9.

Third Nerve Palsy Third nerve palsy involves all the extraocular muscles except the lateral rectus and the superior oblique. The strabismus is characterized by the eye being “down and out” with a small hypotropia and a large exotropia (Fig. 10-15). There is limited depression, elevation, and adduction, along with preservation of abduction (intact innervation lateral rectus muscle) and intorsion seen on attempted eye movement down and in (intact innervation superior oblique muscle). Ptosis, pupillary dilata- tion, and hypoaccommodation are also present in a complete third nerve palsy. A congenital third nerve paresis is often chapter 10: complex strabismus 363

FIGURE 10-15. Photograph of a left third nerve palsy; there is a left ptosis and the left eye is “down and out” (left exotropia and hypotropia). partial, without ptosis, with variable amounts of limited elevation, depression, and adduction, with pupillary sparing, and may show oculomotor synkinesis. The two most common causes of pediatric third nerve palsy are idiopathic congenital onset and head trauma. Other causes include migraine, an association with a viral syndrome, an intracranial tumor, or, rarely, a posterior communicating aneurysm.14,62,105 Nontraumatic acquired third nerve palsy cases must undergo a full workup with neuroimaging.62

TREATMENT The treatment of complete third nerve palsy is extremely difﬁ- cult because there are no vertical muscle forces to move nasally, as all the vertical recti are paretic. Superior oblique tendon transfer to the medial rectus insertion has been suggested as a way of providing medial forces.104 This procedure, however, does not increase adduction as it only creates a leash and limits depression of the eye, resulting in a large hypertropia in downgaze. An ipsilateral superior oblique tenotomy, with ipsilateral recession of the lateral rectus and a large resection of medial rectus, is probably the procedure most often used for a third nerve paresis with an exotropia and hypotropia and some medial rectus function. In cases where this procedure has failed to correct the 364 handbook of pediatric strabismus and amblyopia exotropia, this author has split the lateral rectus and transposed the halves to the nasal border of the superior and inferior rectus muscles. This procedure has worked in centering the eye; however, horizontal excursions are minimal. In addition to the difﬁculty in treating the strabismus, patients with a third nerve palsy and ptosis with poor or absent levator function, are at risk for developing corneal exposure if the ptosis is repaired. Ptosis should be managed with a silicone frontalis sling procedure, aiming for intentional undercorrection of the lid position if there is a poor Bell’s phenomenon. The silicone sling procedure has an advantage of being reversible if corneal exposure becomes a problem. Patients should be warned about the risk of corneal exposure and that their diplopia may be worse after lifting the eyelid, as this removes the occlusion. Many wise patients and physicians opt for leaving the ptosis alone if associated with a poor superior rectus muscle function evidenced by a poor Bell’s phenomenon.

Inferior Oblique Paresis See Chapter 9.

Möbius Syndrome Möbius syndrome is characterized by a combination of facial palsy, sixth nerve palsy, partial third nerve palsy, and distal limb abnormalities such as syndactyly, club foot, or even amputation defects.23 There is some degree of intellectual impairment in 75% of patients.23,131 The Möbius infant typically presents with esotropia, limited abduction, lack of facial expression, and diffi- culty feeding caused by a poor sucking reflex. Craniofacial anomalies can occur and include micrognathia, tongue abnormalities, and facial or oral clefts. Ocular motility abnormalities include limited abduction in more than 90% of cases and limited adduction in 65% of cases.23,66,86 Some patients have globe retraction on adduction and failure to abduct, typical of Duane’s syndrome. The inheritance pattern of Möbius syndrome is usually sporadic, and there is great variability of findings,44 suggesting that the syndrome represents a heterogeneous group of neuromuscular disorders.87 Prenatal exposure to misoprostol, the abortion-inducing drug, has been implicated as a risk factor.23,41,120 Treatment of the strabismus is tailored to the individual situation. Patients with a large esotropia, tight medial rectus chapter 10: complex strabismus 365 muscles, and poor abduction are probably best treated with large bilateral medial rectus recessions similar to the treatment of a patient with congenital fibrosis syndrome.

Sinus Surgery and Medial Rectus Muscle Injury Endoscopic sinus surgery can result in severe damage to the medial rectus muscle and even visual loss.31,69,98 This damage occurs when the thin ethmoid bone is violated during endoscopic sinus surgery and the medial rectus muscle is traumatized. In most cases, part of the medial rectus muscle is removed, often in the area of the neuromuscular junction (two-thirds of the way back from the insertion or approximately 25mm posterior to the insertion). On MRI, the medial rectus may be seen to be myectomized and pulled into the ethmoid sinus (Fig. 10-16). The inferior rectus and inferior oblique muscles can also be traumatized, but this is less common.98 Treatment of the adduction deﬁcit and exotropia depends on the extent of the damage to the medial rectus muscle and the state of the innervation.119 Unfortunately, in most cases, there is poor medial rectus muscle function secondary to neuromuscular junction injury or a posterior myectomy. If medial rectus muscle function is poor, a partial-tendon transfer of the vertical rectus muscle to the medial rectus insertion (Hummelsheim) or a procedure to create a nasal tether to pull the eye to midline is indicated.6 Standard exploration and muscle retrieval techniques (used for locating lost muscles) do not work if the injury involves the neuromuscular junction or if a posterior myectomy was performed.

Aplasia of Extraocular Muscles Although virtually all extraocular muscles have been described as being congenitally absent, the inferior rectus is most commonly affected.13,70,101 The condition is often associated with craniofacial dysostosis, anencephaly, or other congenital head anomalies.8,22,42,88,113 Aplasia of the inferior rectus, superior rectus, and superior oblique muscles can occur in otherwise healthy children without craniofacial abnormalities.27,58,67 Figure 10-17 depicts a case in which this author surgically explored to ﬁnd aplasia of the right inferior rectus and hypoplasia of the left inferior rectus muscle. This child was healthy and presented with a right hypertropia and bilateral limited depression, right eye more than left eye. An absent rectus muscle is managed by 366 handbook of pediatric strabismus and amblyopia

B FIGURE 10-16A–B. Photographs of patient with right medial rectus injury associated with sinus surgery. (A) Rightgaze, full motility. (B) Primary position with right exotropia. chapter 10: complex strabismus 367

D FIGURE 10-16C–D. (C) Leftgaze, showing no signiﬁcant adduction of right eye. This patient had no adduction saccade. (D) MRI shows the posterior aspect of the right medial rectus has been myectomized, and the posterior cut end of the muscle is entrapped in the ethmoid sinus. 368 handbook of pediatric strabismus and amblyopia

B FIGURE 10-17A,B. Photographs of bilateral asymmetrical inferior rectus muscle hypoplasia (surgeon’s view) at the time of surgery. Patient presented with a right hypertropia and severe limitation of depression, rightgaze. (A) The left eye has an underdeveloped inferior rectus muscle. (B) The right inferior rectus muscle shows only the anterior ciliary vessels, but there is no inferior rectus muscle (i.e., aplasia of the inferior rectus muscle). chapter 10: complex strabismus 369 a Hummelsheim-type transposition procedure to substitute for the absent muscle.

Craniosynostosis Causes for strabismus associated with craniosynostosis include divergent orbits, displaced extraocular muscles agenesis of extraocular muscles, and extorsion of the orbits.22,42,88,113 A common pattern of strabismus seen in patients with a variety of craniosynostosis syndromes is exotropia with apparent severe bilateral inferior oblique overaction, superior oblique underaction, and a large V-pattern (Fig. 10-18). The possible causes for the inferior oblique overaction and V-pattern can be an absence of the superior oblique tendon or extorted orbits.9 Extorted orbits shift the medial rectus up and the lateral rectus down so the medial rectus pulls the adducting eye up and the lateral rectus pulls the abducting eye down, which simulates inferior oblique overaction. Likewise, the inferior rectus muscle are displaced nasally and the superior rectus muscle temporally so that in downgaze the eyes converge and in upgaze they diverge.20

FIGURE 10-18. Photograph of patient with Pfeiffer syndrome. Motility exam showed an exotropia, inferior oblique overaction, superior oblique underaction, and V-pattern. Note the extreme underaction of the right superior oblique muscle as the patient looks down and to the left. 370 handbook of pediatric strabismus and amblyopia

DISSOCIATED VERTICAL DEVIATION AND DISSOCIATED HORIZONTAL DEVIATION

Dissociated vertical deviation (DVD) is the tendency for an eye to elevate, abduct, and extort, when binocularity is suspended by occlusion or the patient spontaneously dissociates (often when fatigued). DVD is almost always bilateral, but asymmetrical cases may appear to be unilateral. Prolonged occlusion of the eye that appears not to have DVD, however, will almost always disclose a latent DVD. Note that, with a true hypertropia, there is a corresponding hypotropia of the fellow eye and, on alternate cover testing when the hypertropic eye moves down into primary position, the fellow eye also moves down to become hypotropic. Thus, a true hypertropia is consistent with Hering’s law of yoke muscles. In contrast, DVD violates Hering’s law of yoke muscles because covering the right eye makes the right eye drift up, and covering the left eye makes the left eye drift up with no corresponding hypotropia of the fellow eye (Fig. 10-19). One can think of DVD as two individual hypertropias that are dissociated, thus the term, dissociated vertical deviation. DVD increases on head tilt: head tilt to the right increases a right DVD and head tilt to the left increases a left DVD. DVD occurs when normal binocular visual development is disrupted and is associated with congenital esotropia, congenital exotropia,11 congenital media opacities (e.g., monocular congenital cataracts), and even unilateral optic nerve hypoplasia. Rarely, this author has seen patients with primary DVD; that is, no horizontal strabismus, and no history of previous strabismus surgery (Fig. 10-19). These patients usually have some degree of stereoacuity, sometimes high-grade stereoacuity. On version testing, DVD can mimic inferior oblique overaction because the vision of the adducting eye is blocked by the bridge of the nose; this dissociates the eyes, causing the DVD of the adducting eye to be manifest. The two can be distinguished, however, as DVD has no true hypotropia of the opposite eye, and the hyperdeviation is the same in abduction as in adduction. With inferior oblique overaction, there is a hypotropia of the opposite eye and the deviation increases as the eye moves into adduction. DVD and inferior oblique overaction often coexist with congenital esotropia.127 The cause of dissociated vertical deviation is unknown. Guyton hypothesized that abnormal binocular development causes unbalanced input to the vestibular system, resulting in chapter 10: complex strabismus 371

B FIGURE 10-19A,B. Photographs of bilateral dissociated vertical deviation (DVD). Patient has primary DVD with excellent stereoacuity and has never had strabismus surgery. (A) The left eye is covered to manifest the left DVD. (B) The right eye is covered and discloses a right DVD. Note that the eye behind the cover is not only elevated but is also slightly exodeviated. 372 handbook of pediatric strabismus and amblyopia latent nystagmus with a cyclovertical movement. Cycloversion/ vertical vergence is invoked to damp the cyclovertical nystagmus (a cyclovertical “nystagmus blockage” phenomenon), aiding vision in the fixing eye. Unfortunately, this mechanism also produces unavoidable and undesirable elevation and extorsion of the fellow eye that results in DVD.45 This author has a theory about the neurophysiological basis for DVD. It is interesting that DVD is associated with disruption of early binocular visual development. The interstitial nucleus of Cajal is a brainstem nucleus that regulates cyclovertical movements. The interstitial nucleus of Cajal receives inhibitory input from binocular cells in the occipital cortex, and these inhibitory pathways act to control this nucleus. Lesions around the interstitial nucleus of Cajal that interrupt the binocular inhibitory input result in nucleus disinhibition, which is clinically manifested as seesaw nystagmus. Seesaw nystagmus is a dissociated cyclovertical/horizontal nystagmus. When seesaw nystagmus occurs in infancy, it can look quite similar to DVD. Infantile strabismus or a dense monocular congenital cataract disrupts binocular visual development and reduces binocular cortical cells. Perhaps the lack of binocular cortical cells associated with congenital strabismus or a unilateral blurred retinal image in infancy, results in reduced binocular inhibitory input to the interstitial nucleus of Cajal or similar cyclovertical brainstem nuclei. Reduced binocular inhibitory input would cause disinhibition of these cyclovertical nuclei, giving rise to what we see clinically as DVD. If early surgery for infantile esotropia improves binocularity, then children who have had early surgery should have less DVD. Recent reports on the incidence of DVD in children who have had early surgery for infantile esotropia, however, remain unchanged from reports 30 years previous.81,136 Even though the incidence may be the same, the severity of DVD seems to have diminished over the past few decades. It is this author’s opinion, along with the observations of senior expert strabismologists, that the incidence of severe DVD requiring surgery has decreased. Performing surgery for a large, cosmetically obvious DVD in the 1970s and early 1980s was commonplace. As a res- ident in ophthalmology, this author remembers operating every month on several DVD patients. Over the past several years, there have only been a few cases requiring surgery, and usually on older adults with DVD. The author’s visits to countries where surgeons continue to operate late, after 2 years of age, have disclosed that a very high prevalence of big, surgically chapter 10: complex strabismus 373 significant DVD persists. Perhaps, with the advent of early inter- vention of infantile esotropia in this country, our children with infantile esotropia have been able to establish better binocular fusion, thus reducing the severity, but not the incidence, of the DVD. In this author’s report on very early surgery for congenital esotropia (surgery between 13 and 19 weeks of age), four of seven patients had DVD on last examination (2–8 years; mean, 4 years).136 This DVD, however, was very small and could only be demonstrated by prolonged cover testing. None of the patients required DVD surgery, although one had surgery for inferior oblique overaction. M cell afferent pathway development is responsible for motor fusion and control. Because M cell development starts very early, around 6 weeks to 2 months of age, perhaps our “very early surgery” is not early enough to establish strong motor fusion and eliminate DVD.137 The treatment of DVD is surgical, and surgery is indicated if the DVD exists to the point that it becomes a cosmetic problem. DVD is most often bilateral, and bilateral surgery is usually performed. An exception is with amblyopia, where surgery is performed only on the amblyopic eye. With amblyopia of 2 lines or more, the patient will always fixate with the sound eye, and the sound eye will not manifest the DVD. Most consider superior rectus recessions as the treatment choice for pure DVD without inferior oblique overaction. If DVD and inferior oblique overaction coexist, then an anterior transposition of the inferior oblique is indicated, as this will address both problems with one procedure.12,43,93,121 Strabismus surgery rarely, if ever, cures DVD. Dissociated horizontal deviation (DHD), which may be unilateral or bilateral, is a subtype of DVD that often occurs in patients who have had previous strabismus surgery for congenital esotropia.129 This is a dissociated condition like DVD, but the exocomponent of DVD is exaggerated. Cover/uncover testing may show no shift or a small esotropia, but prolonged occlusion produces an exodeviation. Think of DHD when examining patients with a small residual esotropia, who also have a dissociated exodeviation. The treatment of DHD is recession of the ipsilateral lateral rectus muscle.128

Torticollis and Face Turns This section covers the approach to patients who present with an abnormal head posture. Abnormal head posturing includes torticollis (head tilt), chin elevation and depression, and face 374 handbook of pediatric strabismus and amblyopia turn. These forms of head posturing can occur independently or in combination, as a patient with a superior oblique palsy will often have both a head tilt and a face turn. Torticollis can be secondary to a musculoskeletal abnormality of the neck or to an ocular problem compensated by head posturing. A simple initial test to determine the cause is to ask the patients to close their eyes and observe for several seconds to see if the head posturing spontaneously improves. If the face turn improves when the eyes are closed, this suggests an ocular cause. Next, passively move the patient’s head from side to side with the patient’s eyes closed. If the range of motion of the head and neck is normal, this verifies that the head posturing is an ocular torticollis; however, a stiff neck indicates a musculoskeletal problem. By far the most common ocular causes of abnormal head posturing are nystagmus with a null point and incomitant strabismus with compensatory head posturing to allow fusion. A face turn is often identified by observing the patient’s head posture. A better way to evaluate the presence of a face turn is to observe the position of the eyes. Normal patients with straight eyes and no face turn will have both eyes centered within the palpebral fissures. If a face turn is present, there will be a gaze preference with the eyes constantly shifted opposite to the face turn. For example, a face turn to the right is associated with eyes shifted to the left (Fig. 10-20), and a chin elevation will have the eyes shifted down. When examining a patient for a face turn, first observe the position of the eyes and the presence of a gaze preference. Next, turn or tilt the head opposite to the compensatory position to place the eyes into the non- preferred field of gaze. If there is a face turn to the right, turn the head to the left; if there is a head tilt to the right, tilt the head to the left. While the head is held opposite to the compensatory position, observe for nystagmus or strabismus. If nystagmus occurs or increases with a forced face turn to the opposite side, then a compensatory face turn is present to keep the eyes in the area of the null point. If strabismus is produced by forced head tilt, or turns the eye in with a previously fusing patient, then the compensatory head posturing is adopted to maintain fusion, keeping the eyes in the field of gaze where the eyes are aligned. In addition to face turns and head tilts, chin elevations or depres- sions can be compensatory for nystagmus or strabismus, and chin elevations compensate for ptosis. The degree of face turn can be measured by using an ortho- pedic goniometer placed on the head. Any protractor will work chapter 10: complex strabismus 375

FIGURE 10-20. Photograph of ocular torticollis in a patient with nystagmus. Patient has a face turn to the right to place the eyes at the null point in leftgaze. The best way to identify a face turn is to evaluate the position of the eyes. If there is a strong gaze preference for an eccentric gaze position, then consider the possibility of a compensatory face turn. as the line of sight is compared to the direction of the face, with the nose as the pointer.77 An alternative method for measuring face turn associated with Duane’s syndrome or unilateral limited eye movement is to place a prism over the eye with limited rotation, with the apex pointing toward the direction of the deviated eye. The prism is progressively increased until the face turn is corrected. The amount of prism required to neu- tralize the face turn is recorded in prism diopters. Prism diopters can be converted to degrees by dividing by 2. Prism correction of head posturing can also be used to measure face turns associated with nystagmus.

Incomitant Strabismus Causing Compensatory Head Posturing Head posturing compensates for incomitant strabismus by placing the eyes in a field of gaze where the eyes are best aligned to achieve binocular fusion. For example, a patient with a left sixth nerve palsy will have a large esotropia in leftgaze and straight eyes in rightgaze. These patients will adopt a face turn to the left to keep their eyes aligned in rightgaze. An incomitant 376 handbook of pediatric strabismus and amblyopia strabismus where the eyes are aligned in an eccentric field of gaze can cause an abnormal head posture; this includes cranial nerve palsies, restrictive strabismus, A- or V-patterns, and primary oblique dysfunction. For example, patients with fusion and an A-pattern exotropia or V-pattern esotropia will show a chin depression (eyes straighter in upgaze), whereas an A-pattern esotropia or V-pattern exotropia will show a chin elevation (eyes straighter in downgaze). The treatment of an abnormal head posture caused by incomitant strabismus is simply to correct the strabismus in primary position and provide a large field of single binocular vision. If the fixing eye has limited ductions, then move the eye with limited movements to primary position, and the normal eye will follow.

Nystagmus Causing Compensatory Head Posturing A compensatory head posture can stabilize nystagmus by placing the eyes at the null point. If the null point is to the right, the patient will shift the eyes to the right and have a face turn to the left. Head posturing associated with nystagmus can take the form of a face turn, chin elevation or depression, or a head tilt. A compensatory face turn associated with congenital nystagmus can be treated using eye muscle surgery to move the eye position from the null point to primary position.77 The general surgical principles for correcting a face turn are as follows5:

1. Kestenbaum–Anderson–Parks (Kestenbaum) procedure: With a compensatory face turn to the right, the eyes will be shifted to the left. Therefore, to correct the face turn, move the eyes to the right into primary position (Fig. 10-21), which is done by moving the right eye out (right medial rectus recession–right lateral rectus resection) and moving the left eye in (left lateral rectus recession and a left medial rectus resection). The amount of surgery for a speciﬁc amount of face turn is listed in Table 10-7. Note, Parks Poker Straight 5-6-7-8 (medial recession 5mm, medial resection 6 mm, lateral recession 7 mm, and lateral resection 8mm) is a way of remembering the amount of surgery for a small face turn. In most cases, however, larger amounts of surgery are needed.77 Large recessions and resections are needed for a face turn associated with nystagmus. Postoperative chapter 10: complex strabismus 377

FIGURE 10-21. Drawing showing how to correct a face turn to the right associated with nystagmus using the Kestenbaum procedure. The view is looking down on a face turn to the right with eyes in leftgaze at the null point. Surgically correct the face turn by simply moving the eyes into primary position. The arrows in the diagram indicate moving the eyes to the right to place the eyes in primary position. The left eye is shifted nasally (recess lateral rectus muscle and resect the medial rectus muscle) and the right eye moved temporally (recess medial rectus muscle and resect the lateral rectus muscle) to correct the face turn.

TABLE 16-7. Kestenbaum Procedure for Nystagmus with a Face Turn to the Right (Eyes Shifted Right). Left eye Right eye Face turn Recess lateral Resect medial Recess medial Resect lateral (degrees) rectus (mm) rectus (mm) rectus (mm) rectus (mm) 20 7 6 5 8 30 9 8 6.5 10 45 10 8.5 7 11 50 11 9.5 8 12.5

See Figures 10-20, 10-21. Source: Modified from Refs. 5, 135, permission. 378 handbook of pediatric strabismus and amblyopia limitation of ocular movements is to be expected, deemed to be an acceptable trade-off. 2. Vertical head posturing: Chin depression (eyes up) is treated with large bilateral superior rectus recessions (8–9mm) and inferior rectus resections (6–7mm). For large chin depres- sions, this can be combined or performed in stages, the superior rectus recessions first, then inferior rectus resections later if necessary. Chin elevations (eyes down) can be treated similarly by recessing the inferior rectus muscles (7–8mm) and resecting the superior rectus muscles (6–7mm).99 Surgical therapy should be based on the greatest amount of abnormal head posture measured at distance and near. For example, if the face turn is obvious at distance and not at near, full correction directed at the face turn in the distance should be undertaken. When strabismus coexists with nystagmus, the head posture can be corrected by moving the fixing eye to primary position. Then adjust the fellow eye to compensate for the residual strabismus. Compensatory head tilts are also associated with nystagmus, which can be corrected by rotating the eyes back to primary position. A head tilt to the right can be treated by surgically extorting the right eye and intorting the left eye.122

SURGICAL TREATMENT OF NYSTAGMUS: NO FACE TURN Although the Kestenbaum–Anderson–Parks procedure is directed toward eliminating the abnormal horizontal face turn associated with nystagmus, another approach has been described to damp nystagmus in patients without a face turn. Simultane- ous retroequatorial recessions of all four horizontal rectus muscles have been reported to decrease the amplitude of nystagmus and improve visual acuity.30,36,97 The precise mechanism responsible for damping the nystagmus is not known, and the long-term effect remains unknown. Vision improves only in cases of motor nystagmus, not in patients with sensory nystagmus who have an abnormal afferent pathway.

Additional Causes of Ocular Torticollis Less common mechanisms for head posturing do exist. Rarely, a patient with diplopia adopts a head posture that induces maximal image separation rather than fusion, thus making sup- pression of the diplopic image easier. Other reasons for abnor- chapter 10: complex strabismus 379 mal head posturing include compensation for visual ﬁeld defects, restriction of the good eye in monocular patients, manifest latent nystagmus with a face turn to keep the ﬁxing eye in adduction, ptosis with chin elevation, tilting for monocular torsion, and cosmetic reasons. Other causes include asymmetrical dissociated vertical deviation, refractive error in which the patient adopts a face turn presumably to partially block the pupil, inducing a pinhole effect that provides better visual acuity.

References

1. Amemiya T, Yoshida H, Harayama K, et al. Long-term results of retinal detachment surgery. Ophthalmologica 1978;177:64–69. 2. Anderson RL, Baumgartner SA. Strabismus and ptosis. Arch Oph- thalmol 1980;98:1062–1067. 3. Appleton RE, Chitayat D, Jan JE, Kennedy R, Hall JG. Joubert’s syndrome associated with congenital ocular ﬁbrosis and histidinemia. Arch Neurol 1989;46(5):579–582. 4. Apt L, Axelrod RN. Generalized ﬁbrosis of the extraocular muscles. Am J Ophthalmol 1978;85(6):822–829. 5. Archer SM. Strabismus surgery planning. In: Del Monte MA, Archer SM (eds) Atlas of pediatric ophthalmology and strabismus surgery. New York: Churchill Livingstone, 1993:14. 6. Awad AH, Shin GS, Rosenbaum AL, Goldberg RL. Autogenous fascia augmentation of a partially extirpated muscle with a subperiosteal medial orbitotomy approach. J AAPOS. 1997;1(3):138–142. 7. Ball SF, Ellis GS, Herrington RG, Liang K. Brown’s superior oblique tendon syndrome after Baerveldt glaucoma implant. Arch Ophthal- mol 1991;110:1368. 8. Barnes RJ. Anencephaly with absence of superior oblique tendon. Surv Ophthalmol 1972;16:371–374. 9. Bagshaw J. The ‘heavy eye’ phenomenon. A preliminary report. Br J Ophthalmol 1966;23:73–78. 10. Biglan AW, et al. Management of strabismus with botulinum A toxin. Ophthalmology 1989;96:935–943. 11. Biglan AW, Davis JS, Cheng KP, Pettapiece MC. Infantile exotropia. J Pediatr Ophthalmol Strabismus 1996;33(2):79–84. 12. Black BC. Results of anterior transposition of the inferior oblique muscle in incomitant dissociated vertical deviation. JAAPOS 1997; 1(2):83–87. 13. Brady AP, Stack JP, O’Keeffe M. Congenital absence of extraocular muscles: MR demonstration. J Comput Assist Tomogr 1992;16(3): 490–491. 14. Branley MG, Wright KW, Borchert MS. Third nerve palsy due to cerebral artery aneurysm in a child. Aust NZ J Ophthalmol 1992;20: 137–140. 380 handbook of pediatric strabismus and amblyopia

15. Bremer DL, Rogers GL, Quick LD. Primary-position hypotropia after anterior transposition of the inferior oblique. Arch Ophthalmol 1986;104:229–232. 16. Brodsky MC. Hereditary external ophthalmoplegia synergistic divergence, jaw winking, and oculocutaneous hypopigmentation: a congenital fibrosis syndrome caused by deficient innervation to extraocular muscles. Ophthalmology 1998;105(4):717–725. 17. Brooks SE, Ribeiro GB, Archer SM, Elner VM, Del Monte MA. Fat adherence syndrome treated with intraoperative mitomycin-C: a rabbit model. J Pediatr Ophthalmol Strabismus 1996;33(1):21–27. 18. Brooks SE, Olitsky SE, de Ribeiro G. Augmented Hummelsheim procedure for paralytic strabismus. J Pediatr Ophthalmol Strabismus 2000;37(4):189–195; quiz 226–227. 19. Capo H, Guyton DL. Ipsilateral hypermetropia after cataract surgery. Ophthalmology 1996;103:721–730. 20. Cheng H, Burdon MA, Shun-Shin GA, Czypionka S. Dissociated eye movements in craniosynostosis: a hypothesis revisited. Br J Oph- thalmol 1993;77:563–568. 21. Coats DK, Paysse EA, Plager DA, Wallace DK. Early strabismus surgery for thyroid ophthalmopathy. Ophthalmology 1999;106(2): 324–329. 22. Coats DK, Ou R. Anomalous medial rectus muscle insertion in a child with craniosynostosis. Binoc Vis Strabismus Q 2001;16(2):119– 120. 23. Cronenberger MF, de Castro Moreira JB, Brunoni D, et al. Ocular and clinical manifestations of Möbius’ syndrome. J Pediatr Ophthalmol Strabismus 2001;38(3):156–162. 24. Cruz OA, Davitt BV. Bilateral inferior rectus muscle recession for correction of hypotropia in dysthyroid ophthalmopathy. JAAPOS 1999;3(3):157–159. 25. Demer JL, von Noorden GK. High myopia as an unusual cause of restrictive motility disturbance. Surv Ophthalmol 1989;33:281– 284. 26. Doherty EJ, Macy ME, Wang SM, Dykeman CP, Melanson MT, Engle EC. CFEOM3: a new extraocular congenital fibrosis syndrome that maps to 16q24.2–q24.3. Investig Ophthalmol Vis Sci 1999;40(8): 1687–1694. 27. Drummond GT, Keech RV. Absent and anomalous superior oblique and superior rectus muscles. Can J Ophthalmol 1989;24(6):275–279. 28. Effron L, Price RL, Berlin AJ. Congenital unilateral orbital fibrosis with suspected prenatal orbital penetration. J Pediatr Ophthalmol Strabismus 1985;22(4):133–136. 29. Egbert J, May K, Kersten R, Kulwin D. Pediatric orbital floor fracture: direct extraocular muscle involvement. Ophthalmology 2000; 107:1875–1879. 30. Egbert JE, Anderson JH, Summers CG. Increased duration of low retinal slip velocities following retroequatorial placement of horizontal recti. J Pediatr Ophthalmol Strabismus 1995;32(6):359–363. chapter 10: complex strabismus 381

31. Eitzen JP, Elsas FJ. Strabismus following endoscopic intranasal sinus surgery. J Pediatr Ophthalmol Strabismus 1991;28(3):168–170. 32. Engle EC, Goumnerov BC, McKeown CA, et al. Oculomotor nerve and muscle abnormalities in congenital fibrosis of the extraocular muscles. Ann Neurol 1997;41(3):314–325. 33. Engle EC, Marondel I, Houtman WA, et al. Congenital fibrosis of the extraocular muscles (autosomal dominant congenital external ophthalmoplegia): genetic homogeneity, linkage refinement, and physical mapping on chromosome 12. Am J Hum Genet 1995;57(5): 1086–1094. 34. Engle EC, Kunkel LM, Specht LA, Beggs AH. Mapping a gene for congenital fibrosis of the extraocular muscles to the centromeric region of chromosome 12. Nat Genet 1994;7(1):69–73. 35. Brodsky MC, Fray KJ. Surgical management of intermittent exotropia with high AC/A ratio. J Am Assoc Pediatr Ophthalmol Strabismus 1998;2:330–332. 36. Fioretto M, Burtolo C, Fava GP. New surgical method for nystagmus without null point. Ophthalmologica 1991;203(4):180–183. 37. Flaherty MP, Grattan-Smith P, Steinberg A, Jamieson R, Engle EC. Congenital fibrosis of the extraocular muscles associated with cortical dysplasia and maldevelopment of the basal ganglia. Ophthal- mology 2001;108(7):1313–1322. 38. Fujii GY, Kah-Guan AE, Pieramici DJ, et al. Macular translocation: unifying concepts, terminology, and classification. Am J Ophthal- mol 1992;114:72–80. 39. Gillies WE, Harris AJ, Brooks AM, Rivers MR, Wolfe RJ. Congeni- tal fibrosis of the vertically acting extraocular muscles. A new group of dominantly inherited ocular fibrosis with radiologic findings. Ophthalmology 1995;102(4):607–612. 40. Grimmet MR, Lambert S. Superior rectus overcorrection after cataract extraction. Am J Ophthalmol 1992;114:72–80. 41. Goldberg AB, Greenberg MB, Darney PD. Misoprostol and preg- nancy. N Engl J Med 2001;344(1):38–47. 42. Greenberg MF, Pollard ZF. Absence of multiple extraocular muscles in craniosynostosis. J Am Assoc Pediatr Ophthalmol Strabismus 1998;2(5):307–309. 43. Guemes A, Wright KW. Effect of graded anterior transposition of the inferior oblique muscle on versions and vertical deviation in primary position. J Am Assoc Pediatr Ophthalmol Strabismus 1998;2(4):201– 206. 44. Gusek-Schneider GC, Langenbucher A, Seitz B. Association of keratoconus and Möbius’ syndrome. J Pediatr Ophthalmol Strabismus 2001;38(1):47–48. 45. Guyton DL. Dissociated vertical deviation: etiology, mechanism, and associated phenomena. Costenbader lecture. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(3):131–144. 46. Hamed, Mancuso. Inferior rectus muscle contracture syndrome after retrobulbar anesthesia. Ophthalmology 1991;98:1506–1512. 382 handbook of pediatric strabismus and amblyopia

47. Hamlet YJ, Goldstein JH, Rosenbaum JD. Dehiscence of lateral rectus muscle following intrascleral buckling procedure. Ann Oph- thalmol 1982;14:694–697. 48. Harley RD, Rodrigues MM, Crawford JS. Congenital fibrosis of the extraocular muscles. J Pediatr Ophthalmol Strabismus 1978;15(6): 346–358. 49. Harley RD, Rodrigues MM, Crawford JS. Congenital fibrosis of the extraocular muscles. Trans Am Ophthalmol Soc 1978;76:197–226. 50. Hayashi T, Iwashige H, Maruo T. Clinical features and surgery for acquired progressive esotropia associated with severe myopia. Acta Ophthalmol Scand 1999;77(1):66–71. 51. Hertel RW, Katowitz JA, Young PL, et al. Congenital unilateral fibrosis, blepharoptosis, and enophthalmos syndrome. Ophthalmology 1992;99:347–355. 52. Holmes JM, Beck RW, Kip KE, Droste PJ, Leske DA. Predictors of nonrecovery in acute traumatic sixth nerve palsy and paresis. Oph- thalmology 2001;108(8):1457–1460. 53. Holmes JM, Beck RW, Kip KE, Droste PJ, Leske DA. Botulinum toxin treatment versus conservative management in acute traumatic sixth nerve palsy or paresis. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(3):145–149. 54. Hotchkiss MG, Miller NR, Clark AW, et al. Bilateral Duane’s retraction syndrome: a clinical-pathologic case report. Arch Ophthalmol 1980;98:870–874. 55. Huber A. Electrophysiology of the retraction syndromes. Br J Oph- thalmol 1974;58:293–300. 56. Hudson HL, Feldon SE. Late overcorrection of hypotropia in Grave’s ophthalmopathy. Ophthalmology 1992;99:356–360. 57. Hwang JM, Wright KW. Combined study on the causes of strabismus after retinal surgery. Korean J Ophthalmol 1994;8(2):83–91. 58. Ingham PN, McGovern ST, Crompton JL. Congenital absence of the inferior rectus muscle. Aust NZ J Ophthalmol 1986;14(4):355–358. 59. Jameson NA, Good WV, Hoyt CS. Fat adherence simulating inferior oblique palsy following blepharoplasty. Arch Ophthalmol 1992; 110(10):1369. 60. Kalpakian B, Bateman JB, Sparkes RS, Wood GK. Congenital ocular fibrosis syndrome associated with the Prader–Willi syndrome. J Pediatr Ophthalmol Strabismus 1986;23(4):170–173. 61. Kanski JJ, Elkington AR, Davies MS. Diplopia after retinal detachment surgery. Am J Ophthalmol 1973;76:38–40. 62. Kodsi SR, Younge BR. Acquired oculomotor, trochlear, and abducent cranial nerve palsies in pediatric patients. Am J Ophthalmol 1992; 114(5):568–574. 63. Krzizok TH, Kaufmann H, Traupe H. New approach in strabismus surgery in high myopia. Br J Ophthalmol 1997;81:625–630. 64. Krzizok TH, Schroeder BU. Measurement of recti eye muscle paths by magnetic resonance imaging in highly myopic and normal sub- jects. Investig Ophthalmol Vis Sci 1999;40(11):2554–2560. chapter 10: complex strabismus 383

65. Lee J, et al. Results of a prospective randomized trial of botulinum toxin therapy in acute unilateral sixth nerve palsy. J Pediatr Oph- thalmol Strabismus 1994;31:283–286. 66. Lengyel D, Zaunbauer W, Keller E, Gottlob I. Mobius syndrome: MRI findings in three cases. J Pediatr Ophthalmol Strabismus 2000;37(5): 305–308. 67. Lin PY, Yen MY. Congenital absence of bilateral inferior rectus muscles: a case report. J Pediatr Ophthalmol Strabismus 1997;34(6): 382–384. 68. Lueder GT, Scott WE, Kutschke PJ, Keech RV. Long-term results of adjustable suture surgery for strabismus secondary to thyroid ophthalmopathy. Ophthalmology 1992;99(6):993–997. 69. Mark LE, Kennerdell JS. Medial rectus injury from intranasal surgery. Arch Ophthalmol 1979;97(3):459–461. 70. Mets MB, Parks MM, Freeley DA, Cornell FM. Congenital absence of inferior rectus muscle: report of three cases and their management. Binoc Vis 1987;2(2):77–86. 71. Mets MB, Wendell ME, Gieser RG. Ocular deviation after retinal detachment surgery. Am J Ophthalmol 1985;99:667–672. 72. Metz HS, Norris A. Cyclotorsional diplopia following retinal detachment surgery. J Pediatr Ophthalmol Strabismus 1987;24(6): 287–290. 73. Metz HS. Double elevator palsy. Arch Ophthalmol 1979;97:901– 909. 74. Metz HS, Dickey CF. Treatment of unilateral acute sixth nerve palsy with botulinum toxin. Am J Ophthalmol 1991;112:381–384. 75. Michel O, Oberlander N, Neugebauer P, Neugebauer A, Russmann W. Follow-up of transnasal orbital decompression in severe Graves’ ophthalmopathy. Ophthalmology 2001;108(2):400–404. 76. Miller NR, Kiel SM, Green WR, Clark AW. Unilateral Duane’s retraction syndrome. Arch Ophthalmol 1982;100:1468–1472. 77. Mitchell PR, Wheeler MB, Parks MM, Kestenbaum surgical procedure for torticollis secondary to congenital nystagmus. J Pediatr Ophthalmol Strabismus 1987;24(2):87–93. 78. Munoz M, Rosenbaum AL. Long-term strabismus complications following retinal detachment surgery. J Pediatr Ophthalmol Strabismus 1987;24(6):309–314. 79. Nakano M, Yamada K, Fain J, et al. Homozygous mutations in ARIX (PHOX2A) result in congenital fibrosis of the extraocular muscles type 2. Nat Genet 2001. 80. Nardi M, Barca L. Hypercorrection of hypotropia in Graves’ ophthalmopathy. Ophthalmology 1993Jan;100(1):1–2. 81. Neely DE, Helveston EM, Thuente DD, Plager DA. Relationship of dissociated vertical deviation and the timing of initial surgery for congenital esotropia. Ophthalmology 2001;108(3):487–490. 82. Neugebauer A, Fricke J, Kirsch A, Russmann W. Modified transposition procedure of the vertical recti in sixth nerve palsy. Am J Oph- thalmol 2001;131(3):359–363. 384 handbook of pediatric strabismus and amblyopia

83. Oh SY, Clark RA, Velez F, Demer JL. Magnetic resonance imaging demonstration of instability of rectus pulleys as cause of incomitant strabismus. Investig Ophthalmol Vis Sci 2001;167:42–44. 84. Parks MM. Causes of the adhesive syndrome In: Symposium on strabismus. Transaction of the New Orleans Academy of Ophthalmol- ogy. St Louis: Mosby, 1978:269–279. 85. Pearlman JT, Christensen RE. Motility problems following retinal detachment surgery. Am Orthopt J 1972;22:64–67. 86. Pedraza S, Gamez J, Rovira A, et al. MRI ﬁndings in Möbius syndrome: correlation with clinical features. Neurology 2000;55(7): 1058–1060. 87. Peleg D, Nelson GM, Williamson RA, Widness JA. Expanded Möbius syndrome. Pediatr Neurol 2001;24(4):306–309. 88. Pinchoff BS, Sandall G. Congenital absence of the superior oblique tendon in craniofacial dysostosis. Ophthalmic Surg 1985;16(6):375– 377. 89. Porter JD, Baker RS. Absence of oculomotor and trochlear motoneurons leads to altered extraocular muscle development in the Wnt-1 null mutant mouse. Dev Brain Res 1997;100(1):121– 126. 90. Prata JA, Minckler DS, Green RL. Pseudo-Brown’s syndrome as a complication of glaucoma drainage implant surgery. Ophthalmic Surg 1993;24:608–611. 91. Prendiville P, Chopra M, Gauderman WJ, Feldon SE. The role of restricted motility in determining outcomes for vertical strabismus surgery in Graves’ ophthalmology. Ophthalmology 2000;107(3):545– 549. 92. Price RL, Pederzolli A. Strabismus following retinal detachment surgery. Am Orthopt J 1982;32:9–17. 93. Quinn AG, Kraft SP, Day C, Taylor RS, Levin AV. A prospective evaluation of anterior transposition of the inferior oblique muscle, with and without resection, in the treatment of dissociated vertical deviation. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(6):348– 353. 94. Raab EL. Clinical features of Duane’s syndrome. J Pediatr Ophthal- mol Strabismus 1986;23:64–68. 95. Raina J, Wright KW, Lin MM, McVey JH. Effectiveness of lateral rectus Y split surgery for correcting the upshoot and downshoot in Duane’s retraction syndrome, Type III. Binoc Vis Strabismus 1997; 12(4):233–238. 96. Reck AC, Manners R, Hatchwell E. Phenotypic heterogeneity may occur in congenital ﬁbrosis of the extraocular muscles. Br J Oph- thalmol 1998;82(6):676–679. 97. Reinecke RD. Retroequatorial placement of horizontal recti. J Pediatr Ophthalmol Strabismus 1996;33(3):201–202. 98. Rene C, Rose GE, Lenthall R, Moseley I. Major orbital complications of endoscopic sinus surgery. Br J Ophthalmol 2001;85(5):598–603 (review). chapter 10: complex strabismus 385

99. Roberts EL, Saunders RA, Wilson ME. Surgery for vertical head position in null point nystagmus. J Pediatr Ophthalmol Strabismus 1996;33(4):219–224. 100. Rogers GL, Bremer DL. Surgical treatment of the upshoot and downshoot in Duane’s retraction syndrome. Ophthalmology 1984;91(11): 1380–1383. 101. Romano PE. Absent or hypoplastic extraocular muscles? J Med Genet 1989;26(3):216. 102. Rosenbaum A, Kushner BJ, Kirschen D. Vertical rectus muscle transposition and botulinum toxin (oculinum) to medial rectus for abducens palsy. Arch Ophthalmol 1989;107:820. 103. Roth AM, Sypnicki BA. Motility dysfunction following surgery for retinal detachment. Am Orthopt J 1975;25:118–121. 104. Saunders RA, Rogers CT. Superior oblique transposition for third nerve palsy. Ophthalmology 1982;89:310. 105. Schumacher-Feero LA, Yoo KW, Solari FM, Biglan AW. Third cranial nerve palsy in children. Am J Ophthalmol 1999;128(2):216– 221. 106. Scott WE, Jackson OB. Double elevator palsy: the signiﬁcance of inferior rectus restriction. Ophthalmology 1977;27:5–10. 107. Scott AB, Wong GY. Duane’s syndrome: an electromyographic study. Arch Ophthalmol 1972;87:142–147. 108. Seiff SR, Good WV. Hypertropia and the posterior blowout fracture: mechanism and management. Ophthalmology 1996;103(1):152– 156. 109. Sener EC, Lee BA, Turgut B, Akarsu AN, Engle EC. A clinically variant ﬁbrosis syndrome in a Turkish family maps to the CFEOM1 locus on chromosome 12. Arch Ophthalmol 2000;118(8):1090–1097. 110. Sewell JJ, Knobloch WH, Eifrig DE. Extraocular muscle imbalance after surgical treatment for retinal detachment. Am J Ophthalmol 1974;78:321. 111. Smiddy WE, Loupe D, Michels RG, et al. Extraocular muscle imbalance after scleral buckling surgery. Ophthalmology 1989;96:1485– 1490. 112. Smith SL, Starita RJ, Fellman RL, Lynn JR. Early clinical experience with the Baerveldt 350-mm2 glaucoma implant and associated extraocular muscle imbalance. Ophthalmology 1993;100:914–918. 113. Snir M, Gilad E, Ben-Sira I. An unusual extraocular muscle anomaly in a patient with Crouzon’s disease. Br J Ophthalmol 1982;66(4):253– 257. 114. Stager DR, Weakley DR, Stager D. Anterior transposition of the inferior oblique: anatomic assessment of the neurovascular bundle. Arch Ophthalmol 1992;110:360–362. 115. Strachan IM, Brown BH. Electromyography of extraocular muscles in Duane’s syndrome. Br J Ophthalmol 1972;56:594–599. 116. Taylor R, Whale K, Raines M. The heavy eye phenomenon: orthop- tic and ophthalmic characteristics. Ger J Ophthalmol 1995;4:252– 255. 386 handbook of pediatric strabismus and amblyopia

117. Theodossiadis G, Nikolakis S, Apostolopoulos M. Immediate postoperative muscular disturbance in retinal detachment surgery. Mod Probl Ophthalmol 1979;20:367–372. 118. Traboulsi EI, Lee BA, Mousawi A, Khamis AR, Engle EC. Evidence of genetic heterogeneity in autosomal recessive congenital fibrosis of the extraocular muscles. Am J Ophthalmol 2000;129(5):658– 662. 119. Trotter WL, Kaw P, Meyer DR, Simon JW. Treatment of subtotal medial rectus myectomy complicating functional endoscopic sinus surgery. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(4):250– 253. 120. Vargas FR, Schuler-Faccini L, Brunoni D, et al. Prenatal exposure to misoprostol and vascular disruption defects: a case-control study. Am J Med Genet 2000;95(4):302–306. 121. Varn MM, Saunders RA, Wilson ME. Combined bilateral superior rectus muscle recession and inferior oblique muscle weakening for dissociated vertical deviation. J Am Assoc Pediatr Ophthalmol Stra- bismus 1997;1(3):134–137. 122. von Noorden GK, Jenkins RH, Rosenbaum AL. Horizontal transposition of the vertical rectus muscles for treatment of ocular torticollis. J Pediatr Ophthalmol Strabismus 1993;30(1):8–14. 123. Wang SM, Zwaan J, Mullaney PB, et al. Congenital fibrosis of the extraocular muscles type 2, an inherited exotropic strabismus fixus, maps to distal 11q13. Am J Hum Genet 1998;63(2):517–525. 124. Wilcox LM, Gittinger JW, Breinen GM. Congenital adduction palsy and synergistic divergence. Am J Ophthalmol 1981;91:1–7. 125. Wilder WM, Williams JP, Hupp SL. Computerized tomographic findings in two cases of congenital fibrosis syndrome. Comput Med Imaging Graph 1991;15(5):361–363. 126. Wilson WB, Prochoda M. Radiotherapy for thyroid orbitopathy. Effects on extraocular muscle balance. Arch Ophthalmol 1995; 113(11):1420–1425. 127. Wilson ME, Parks MM. Primary inferior oblique overaction in congenital esotropia: accommodative esotropia and intermittent exotropia. Ophthalmology 1989;96:952–957. 128. Wilson ME, Saunders RA, Berland JE. Dissociated horizontal deviation and accommodative esotropia: treatment options when an eso- and an exodeviation co-exist. J Pediatr Ophthalmol Strabismus 1995; 32(4):228–230. 129. Wilson ME, McClatchey SK. Dissociated horizontal deviation. J Pediatr Ophthalmol Strabismus 1991;28(2):90–95. 130. Wolff SM. Strabismus after retinal detachment surgery. Trans Am Ophthalmol Soc 1983;81:182–192. 131. Wolff JE, Koutsandreou AC. Analysis of psychomotor development of ten children with Möbius syndrome. Dev Med Child Neurol 2001; 43(1):71–72. 132. Wright KW. Late overcorrection after inferior rectus recession. Oph- thalmology 1996;103(9):1503–1507. chapter 10: complex strabismus 387

133. Wright KW, Liu GY, Murphree AL, et al. Double elevator palsy, ptosis and jaw-winking. Am Orthopt J 1989;39:143–150. 134. Wright KW. The fat adherence syndrome and strabismus after retina surgery. Ophthalmology 1986;93:411–415. 135. Wright KW. Color atlas of strabismus surgery: strategies and techniques. Torrance, CA: Wright, 2000. 136. Wright KW, Edelman PM, McVey JH, Terry A, Lin M. High-grade stereoacuity after early surgery for congenital esotropia. Arch Oph- thalmol 1994;112:913–919. 137. Wright KW. Clinical optokinetic nystagmus asymmetry in treated esotropes. J Pediatr Ophthalmol Strabismus 1996;33(3):153–155. 138. Yamada M, Shinoda K, Hatakeyama A, Nishina S, Mashima Y. Fat adherence syndrome after retinal surgery treated with amniotic membrane transplantation. Am J Ophthalmol 2001;132(2):280–282.