Uses of the Inferior Oblique Muscle in Strabismus Surgery.

Inferior oblique muscle weakening is typically performed for overaction of the muscle. In this article, we review inferior oblique muscle anatomy, different weakening procedures, and recent surgical techniques that take advantage of the muscle's unique anatomy for the treatment of additional indications such as excyclotorsion and hypertropia in primary gaze.

INTRODUCTION

Overaction (or apparent overaction) of the inferior oblique muscle is a common aspect of new and recurring cases of strabismus. It is more appropriately described as overelevation in adduction in the CEMAS classification system and by others.12345 Children with infantile esotropia often develop overelevation in adduction and/or dissociated vertical deviation (DVD).67 Incomitant eso- and exo-deviations in children and adults frequently show V, X, or Y patterns with overelevation. Fourth cranial nerve palsy can be associated with inferior oblique overaction, resulting in one of the most common forms of vertical strabismus in adults.8 Weakening of one or both inferior oblique muscles may be indicated in all these conditions.

The inferior oblique originates at the periosteum of the maxillary bone near the lacrimal fossa and inserts into the posterior globe near the inferior border of the lateral rectus, passing under the inferior rectus. With the eye in the primary position, the inferior oblique makes a 51° angle with the visual axis and acts an excycloductor. The secondary and tertiary actions are elevation and abduction, respectively [Figure 1a]. The inferior oblique is innervated by the lower portion of the oculomotor nerve.8

Figure 1

Schematic diagram demonstrating the key differences among the various inferior oblique weakening techniques. Each panel depicts the patient's right eye viewed from below; (a) natural position of the inferior oblique muscle indicating the fields of action and the axes of Fick (x, y, and z); (b) recession; (c) anterior transposition; (d) anterior nasal transposition; (e and f) nasal myectomy. See text for details. IO: Inferior oblique muscle; IR: Inferior rectus muscle; LR: Lateral rectus muscle; NFVB: Neurofibrovascular bundle

The anatomy of the inferior oblique muscle is somewhat atypical compared to the other extraocular muscles, which is important for understanding the effects of the various surgical procedures on eye position and ocular motility. In particular, innervation of the muscle occurs through the neurofibrovascular bundle (NFVB), which attaches midway between the origin and the insertion 2 mm temporal to the inferior rectus muscle. After anterior transposition of the muscle, the NFVB ligament will mechanically act as the muscle's new origin.910

Surgical weakening of the inferior oblique is typically performed, either unilaterally or bilaterally, to treat primary or secondary “inferior oblique overaction,” that is, overelevation in adduction, and bilaterally to treat V-pattern esotropia. Additional indications exist as well. Here, we review a selection of surgical weakening procedures of the inferior oblique and indications for such surgeries. We highlight specific properties of the muscle and how to take advantage of these properties for good surgical outcomes.

BRIEF HISTORY

The first studies of the effects of inferior oblique weakening that include anterior transposition were published in the 1940s.111213 However, the term “recession” was commonly used to indicate both traditional recession procedures and anterior transposition. Evaluation of the effectiveness of the various modifications of anterior transposition continued through the 1960s.14 The specific effects of altering the insertion plane by transposing were recognized in the 1980s. For example, Elliott and Nankin15 documented that anterior transposition was associated with limitations in elevation. Subsequently, Kushner1617 defined the anti-elevation syndrome (AES) as the resulting restriction of elevation in abduction if the muscle is transposed over a relatively large distance. Thereafter, David Stager, Sr. identified the NFVB as the ancillary origin of the muscle after transposition.91018 Thereafter, it was possible to predict the effects of transposition with the change in the direction of the torque vector. Placing the new insertion nasally provided a novel method for treating excyclotorsion.1920

INDICATIONS

Primary inferior oblique overaction commonly develops in individuals with infantile esotropia (often after surgical treatment of the original horizontal strabismus), as well as in some children with accommodative esotropia or intermittent exotropia.8 Wilson and Parks estimated the incidence at 72% among individuals with infantile esotropia and greater than 30% in those with acquired esotropia or intermittent exotropia.21 Primary inferior oblique overaction has been reported to represent 16.7% of hypertropias,22 and is commonly associated with DVD. Other less common types of strabismus that may include overelevation in adduction include superior oblique palsy,23 and V, Y, or X pattern strabismus with or without craniosynostosis.242526

The term inferior oblique overaction to describe all cases of over elevation in adduction is in some cases misleading because it suggests that hypertrophy or hypercontractility causes the muscle to “overact.” However, superior oblique weakness, co-contraction of the horizontal rectus muscles (Duane syndrome), restriction of rectus muscles, aberrant innervation of the extraocular muscles, or anomalies in the insertion of other extraocular muscles may all result in overelevation in adduction.327 In patients with craniosynostosis, excyclorotation of the globes and orbits alone may cause apparent overaction of the inferior oblique muscles because the medial rectus muscles elevate as well as adduct the globes. For these reasons, the term “overelevation in adduction” may be preferred.1

Other indications for inferior oblique muscle surgery are some Duane syndrome patients with upshoot, sensory hypertropia, cases where the inferior rectus muscle was severed or lost,28 and chin-down head position in patients with nystagmus.29 Patients with craniofacial dysostosis often have significant excyclotorsion due to the exaggerated rotation of the orbits and often because the superior rectus muscles are absent. Anterior nasal transposition (ANT) is helpful in these cases.26 Similarly, inferior rectus aplasia may occur in the absence of craniofacial dysostosis, and these patients benefit from anterior tranposition.28

PRIMARY INFERIOR OBLIQUE SURGICAL PROCEDURES

Recession

The inferior oblique muscle can be recessed3031 along its anatomical path by as much as 14 mm. In these cases, the anterior border is placed 5 mm posterior to the temporal insertion of the inferior rectus muscle [Figure 1b].23 However, caution is advised to avoid damaging the vortex vein.31 Tables for titrating the recession can be found in textbooks.23 The inferior oblique recession is commonly used as a primary weakening procedure in patients with overelevation in adduction.

Anterior transposition

Many current inferior oblique recession techniques include various ranges of transposition of the insertion and are categorized under “anterior transpositions.” The main difference between these procedures and true recessions is that anterior transposition alters the path of the muscle, which is generally more effective at weakening the inferior oblique. Anterior transposition of the inferior oblique muscle has been widely used for the treatment of increased adduction associated with DVD [Figure 1c].3233343536 A recognized risk of anteriorization of the inferior oblique muscle is the potential for postoperative limitation of elevation during abduction, resulting in an apparent inferior oblique overaction in the contralateral eye, often accompanied with Y-pattern exodeviation, or AES.163738

Anterior nasal transposition

Anterior nasal transposition (ANT) is a relatively new procedure,192026 in which the insertion is transposed to a location over the nasal half of the inferior rectus muscle (Figure 1d; typically 2 mm nasal to the nasal border of the inferior rectus muscle and 2 mm posterior to the inferior rectus insertion). The inferior oblique is thus transformed from an extorter into an intorter and from an elevator to a depressor. The ANT can be used to eliminate or reduce severe excyclotorsion. An advantage of this procedure over temporal anterior transposition is that it avoids AES.20 Indications for ANT are bilateral 4th nerve palsy and overelevation combined with severe excyclotorsion, as often seen in patients with cranial dysostosis. In a series of 20 patients with various etiologies, we have shown generally good outcomes after ANT, especially in patients with severe superior oblique palsy and patients with primary inferior oblique overaction.20 However, results for pattern XT and with Duane syndrome-related upshoot were variable.20 ANT was effective in eliminating strabismus, excyclodeviation, and the anomalous head posture in a patient with profound unilateral superior oblique weakness as a result of prior damage to the superior oblique muscle tendon.39 Good outcomes have also been reported in cases of overelevation in adduction combined with DVD.40 This success is likely due to the fact that the ANT procedure makes the inferior oblique muscle into a tonic depressor.40 Details of the ANT surgical procedure have been previously published.1920

Myectomy

Inferior oblique myectomy typically involves the surgical removal of a segment of muscle between the NFVB and the insertion of the muscle.2341 The muscle segment is cauterized prior to removal. The primary advantage is convenience as this procedure is faster than a recession. In addition, there is less risk of surgical intraoperative complication because there is no scleral pass required to reattach the muscle. The disadvantage is the possibility that the muscle may reattach and lead to recurrent overaction. There may also be variable results as the same procedure is used to treat varying degrees of overaction. The inferior oblique recession is advantageous because it is a more tailored weakening procedure based on the degree of overaction. In addition, if the inferior oblique muscle needs to be recovered again, it is easier to find.

SECONDARY INFERIOR OBLIQUE SURGICAL PROCEDURES

Residual or recurrent symptoms of inferior oblique overaction are common.15364243 Further weakening of the inferior oblique muscle can be accomplished by a further recession (re-recession). However, if the muscle was already maximally recessed or previously transposed, or if severe weakening is the objective, re-recession may not be an option. Traditional drastic inferior oblique weakening procedures, such as denervation with extirpation or myectomy, are disadvantageous; because they render the muscle definitively nonfunctional, prohibiting any further change or adjustment to the inferior oblique muscle. An alternative option is nasal myectomy.44 In this procedure, a 5-mm section of the muscle is excised along the muscle belly between the NFVB and the origin [Figure 1e and f]. We found resolution or significant improvement in 38 of 40 patients (95%) with recurrent overelevation in adduction at a median of 2 years follow-up after the ANT procedure.44 Nasal myectomy was shown to be an effective procedure for AES.37 An advantage of this procedure is that it renders the nasal portion of the muscle inactive, keeping the temporal aspect intact. Another inactivating procedure that is recoverable is deactivation by suturing the inferior oblique muscle to the orbital wall. Ela-Dalman and colleagues reported good results in a small series of patients for whom the inferior oblique muscle insertion was attached to the periosteum of the lateral orbital wall.45 This procedure would theoretically allow subsequent manipulation of the muscle if required.

COMPLICATIONS AND MANAGEMENT

There are several possible complications of inferior oblique surgery that can occur. The most common may be recurrent or persistent inferior oblique overaction, for which a secondary, more profound weakening procedure is often performed.23 Overcorrection, less common than undercorrection, may respond to conversion of an inferior oblique transposition into a less profound, traditional recession or alternatively one of several superior oblique weakening procedures.46

Immediate recurrent overaction may be due to missed fibers of the inferior oblique at the insertion.47 Some patients may have a split insertion due to a bifed or trifed muscle. Failure to recognize this anomaly will result in the surgery being virtually ineffective. In addition, missing fibers due to a broad insertion will result in the same problem.

As mentioned above, the vortex vein is vulnerable in most inferior oblique recession and transposition procedures. Damaging the vortex vein may result in excessive hemorrhaging (bleeding). In addition, vision-threatening retrobulbar hemorrhages have been reported.48 If Tenon's capsule in damaged, hemorrhage may occur and adipose tissue (fat) may be liberated and may adhere leading to restrictions in motility.4249

Transposition (anterior or anterior nasal) of the inferior oblique results in the posterior temporal fibers being stretched from the ancillary origin at the NFVB to the new insertion. As a result, chronic tension on these fibers may cause posterior retraction of the temporal aspect of the new insertion once the sutures dissolve. This muscle slippage also occurs if the attached fibers have been devitalized due to a crushing hemostat during detachment from the original insertion. We have observed this phenomenon frequently in patients who undergo a second surgery for residual or recurrent overaction after traditional inferior oblique anterior transposition. To avoid posterior retraction (slippage) of the fibers, permanent sutures (e.g. 6–0 Mersilene; Ethicon, Somerville, NJ)20 are recommended along with a protective muscle clamp.50

We advise meticulous attention to suture placement as misplacing of the posterior fibers of the inferior oblique too anteriorly and laterally can result in AES.161738 This results in a limitation of elevation in the abduction and an apparent overelevation in adduction in the contralateral eye. In addition, a Y-pattern exotropia may result. While antielevation syndrome is best avoided, most cases will respond to either an inferior oblique myectomy or repositioning the inferior oblique muscle closer to the border of the inferior rectus muscle.37

Transient pupillary dilation can occur following any procedure that puts excessive tension on the NFVB resulting in a partial 3rd cranial nerve palsy. This complication can be avoided with gentle technique.

DISCUSSION

A wide variety of surgical procedures can weaken the action of the inferior oblique muscle. In addition to the techniques described above, textbooks describe myotomies, myectomies (of the distal portion of the muscle near the insertion), disinsertion, denervation, and denervation with extirpation. In this review, we have highlighted the recent advances in inferior oblique surgery. Although strengthening procedures have also been described, such as advancement or resection of the inferior oblique, the results of those procedures are variable, and the authors have only limited experience in these techniques.

One challenge in understanding (and thus predicting) the effects of these techniques is that most inferior oblique procedures not only weaken the inferior oblique muscle but also modify, quantitatively and qualitatively, the field of action. A well-known example is the limitation of elevation in abduction after anterior transposition and the concurring apparent inferior oblique overaction in the contralateral eye,1638 or AES.1637 Placing the new insertion that is less temporal, or even nasal (as in the ANT procedure),20 to the inferior rectus border avoids the limitations of elevation in abduction.

As excyclorotation is the primary action of the inferior oblique in its natural position, some surgical procedures of the inferior oblique may alleviate torsional deviations. Regardless whether the preoperative torsional deviation is the reason for surgery, the potential for torsional effects of any inferior oblique procedure warrants attention.17 Preferably, torsional changes should also be measured with the double-Maddox rod test, fundus imaging, or iris photography.51

Currently, there is good understanding of the mechanical functionality of the NFVB after inferior oblique anterior transposition.9 However, not all aspects of the effects of inferior oblique muscle surgery can be explained in terms of the geometry of the new insertion. In a thought-provoking editorial, Ellis hypothesized that the entire muscle may assume an altered course or trajectory after transposing, further complicating the prediction of the changed fields of action postoperatively.52 This, in turn, indicates that greater study is needed regarding the response of connective tissue pulleys and pulley bands to inferior oblique surgery.53

As previously mentioned, the traditional term “inferior oblique overaction” is misleading,1345 because it suggests that hypertrophy or hypercontractility causes the muscle to “overact.” The recurrence rate of overelevation after inferior oblique weakening along with the possibility that the inferior oblique muscle is not the primary cause of the problem has stimulated a heightened interest in the anatomy54 and histology of this muscle. To date, several studies have attempted to correlate the histology of the inferior oblique muscle with specific clinical diagnoses. Antunes-Foschini et al. reported a substantial increase in the number of activated satellite cells in inferior oblique muscle specimens from a series of subjects with inferior oblique overaction.55 This suggests that there may have been active modulation of individual myofibers within the inferior oblique muscles of these patients that is above the level in normal inferior oblique muscles. The authors acknowledged that there are multiple causes of overelevation in adduction and described their cohort as highly heterogeneous.55 In addition, there were significant variations in the density of muscle precursor cells in their samples.55 However, the densities were greater than normal in the muscles from every subject in the study. These results suggest that extraocular muscles, in contrast to most other skeletal muscles, maintain a process of continuous myofiber remodeling and that the rate of remodeling appears to change in patients with inferior oblique overaction. In our study of a cohort of patients with over-elevation in adduction of various etiologies (primary “inferior oblique overaction” with and without previous surgery, craniofacial dysostosis), we determined localization and density of connective tissue elements (collagens I, IV, VI, and elastin).5 In primary inferior oblique overaction, all connective tissue components in unoperated specimens were elevated compared with controls. Previously operated muscles showed normal levels of collagens IV and VI but increased collagen I. In unoperated craniofacial dysostosis specimens, only elastin was elevated and density of collagens IV and VI was lower in previously operated versus unoperated specimens. Elevated collagen and elastin levels in the cohort with primary inferior oblique overaction were consistent with the clinical finding of muscle stiffness. On the other hand, normal connective tissue densities in craniofacial dysostosis supported the hypothesis that overelevation in this group reflected anomalous muscle vectors rather than tissue changes. Surgical intervention was associated with changes in the connective tissue matrix in both cohorts. This supports the role of increased muscle stiffness as a factor in strabismus. Understanding of the processes occurring within connective tissue elements in these muscles will be important to all development of new approaches for treating overelevation in adduction and other types of strabismus.