A prevalence of A-pattern strabismus with exotropia is reported in 9% to 27% of exotropia cases.1–4 Dysfunction of the superior oblique muscle is suggested as the principal cause of horizontal strabismus with A-pattern.3 Superior oblique overaction is an exaggeration of the normal function of the superior oblique muscle that includes intorsion, depression, and abduction.
Dissociated vertical deviation is the tendency for an eye to elevate, abduct, and extort when binocularity is suspended by occlusion or the patient spontaneously dissociates. However, causes of dissociated vertical deviation are poorly understood.5–7 Dissociated vertical deviation generally occurs bilaterally, but asymmetrical cases may appear to be unilateral. It is most commonly associated with infantile strabismus, such as infantile esotropia, but is also associated with intermittent exotropia in some cases.8,9 Thus, coexisting superior oblique overaction with dissociated vertical deviation is an extremely rare condition because the action of superior oblique overaction is depressive and opposite to that of dissociated vertical deviation.
The triad of A-pattern exotropia, superior oblique overaction, and dissociated vertical deviation is referred to as Helveston syndrome or triad exotropia and is a rare, bizarre combination of ocular motility disturbance that was first reported by Helveston in 1969.10 However, further studies have not been reported and clinical features of triad exotropia are still unclear. The purpose of this study was to investigate the clinical features and surgical outcomes in patients who are diagnosed as having triad exotropia manifestations.
Patients and Methods
This study followed the tenets of the Declaration of Helsinki and was approved by the institutional review board at Korea University Medical Center.
Patients who visited the strabismus clinic at the Korea University Anam Hospital between 2007 and 2014 were retrospectively analyzed. All patients were diagnosed as having A-pattern exotropia that was associated with simultaneous bilateral superior oblique overaction and dissociated vertical deviation (Figure 1). A-pattern exotropia was defined when the difference between the angles of deviation at up gaze and down gaze (the A-pattern amount) was more than 10 prism diopters (PD). Patients who underwent strabismus surgery were included and were observed for at least 1 year after primary surgery.
Nine cardinal gaze (top) and 3 translucent occlusion test (bottom) preoperative photographs. Note the A-pattern exotropia with bilateral superior oblique overaction and dissociated vertical deviation.
Visual acuity (logarithm of the minimum angle of resolution [logMAR]), refractive error (diopters [D]), existence of amblyopia, associated ocular or systemic abnormality, angle of deviation in primary position (PD), A-pattern amount (PD), degree of superior oblique overaction and dissociated vertical deviation, and stereoacuity were measured preoperatively. Refractive error was presented as the spherical equivalent (D). A-pattern amount (PD) was defined by the difference between the angle of deviation at up gaze and down gaze.
Amblyopia was defined as having at least two lines of difference in visual acuity between the eyes or worse than 20/40 from 3 to 5 years and 20/30 for more than 5 years. The angle of deviation was determined by the alternate prism and cover test at both distance (6 m) and near (33 cm). The degree of superior oblique overaction was quantified as follows10: (1+) noticeable overaction, (2+) definite overaction, (3+) marked overaction, and (4+) when the cornea was almost entirely covered by the lower eyelid during depression in adduction.10 Dissociated vertical deviation was measured by using the alternate prism and cover test with the eyes in the primary position fixated on an accommodative target at 6 m with full refractive correction. Any concurrent horizontal deviation was initially neutralized with a horizontal prism over the contralateral eye and the dissociated vertical deviation measured in the ipsilateral eye. The degree of dissociated vertical deviation was classified as follows: (1+) less than 5 PD, (2+) 5 to 10 PD, (3+) 10 to 15 PD, and (4+) more than 15 PD.
All surgeries were performed by a single surgeon (SHK). Surgeries consisted of lateral rectus recession or combined surgeries depending on the A-pattern amount and the degree of superior oblique overaction and dissociated vertical deviation. For combined surgeries, all patients underwent bilateral or unilateral lateral rectus recession based on the distance angle of deviation; the surgical amount of recession was determined according to the same surgical dosage table.11 For correction of concurrent A-pattern exotropia, the lateral rectus muscle was recessed with downward transposition when superior oblique overaction was less than 2+. The apparent superior oblique overaction of more than 3+ was corrected by a superior oblique posterior four-fifths tenotomy. The superior oblique tendon scleral insertion was identified. The posterior four-fifths of the fibers of the tendon were separated longitudinally 10 mm from the anterior fifth of the tendon and were tenotomized, leaving the anterior fifth of the superior oblique tendon intact.
Symptomatic dissociated vertical deviation (spontaneous elevation) was also subjected to surgical correction. The amount of superior rectus recession was graded depending on the amount of dissociated vertical deviation in each eye. The muscle was reattached on the sclera with two bites using a double-armed 6-0 polyglactin 910 suture (Vicryl; Ethicon, Inc., Somerville, NJ). After surgery, all patients were evaluated at postoperative months 1, 3, and 6, and every 6 months after that for at least 1 year. The angle of deviation in primary position (PD) at distance and near, the A-pattern amount (PD), and the degree of superior oblique overaction and dissociated vertical deviation were measured at every visit in the same manner as that for the preoperative measurements.
The patients were divided into two groups according to surgery: the horizontal muscle surgery alone and the horizontal muscle surgery with bilateral superior oblique posterior tenotomy (combined surgery) groups. We compared postoperative measurements, success, and reoperation rate in these groups. Success of surgery was defined as exodeviation less than 10 PD or esodeviation less than 5 PD at the final follow-up visit without abnormal head position, diplopia, reading difficulty, large angle of dissociated vertical deviation, or reoperation in the entire follow-up period.
The data were analyzed using SPSS software (version 21.0; SPSS, Inc., Chicago, IL) and the clinical measurements were compared and analyzed using the Mann–Whitney U and Fisher's exact tests. A P value of .05 or less was considered statistically significant.
A total of 40 patients were included in this study. Ten (25%) patients were boys and 30 (75%) patients were girls. The mean age at diagnosis was 5.5 ± 4.6 years (range: 1 to 20 years) and the mean age at surgery was 12.3 ± 12.8 years (range: 2 to 49 years). Among these 40 patients, amblyopia was diagnosed in 18 (45%) patients, with 8 (20%) and 10 (25%) patients having unilateral and bilateral amblyopia, respectively. Ten (25%), 4 (10%), and 2 (5%) patients had latent nystagmus, delayed development, and hemiplegia, respectively. Exodeviation in the primary position was 27.7 ± 11.2 PD (range: 14 to 55 PD) and 28.5 ± 10.9 PD (range: 18 to 60 PD) at distance and near, respectively. The A-pattern amount was 18.8 ± 5.9 PD (range: 12 to 35 PD). The degree of superior oblique overaction was 1.9 ± 1.1 (range: 1 to 4), with 4 (10%) and 36 (90%) patients showing asymmetrical and symmetrical deviation bilaterally, respectively. The degree of dissociated vertical deviation was 2.1 ± 0.9 (range: 1 to 4). Symmetrical dissociated vertical deviation was observed in 16 (40%) patients. Stereoacuity was measured in 20 (50%) patients and 16 of these had gross stereoacuity (800 to 200 seconds of arc) (Table 1).
The postoperative surgical outcomes of the groups are described in Table 2. There were 17 patients in the horizontal muscle surgery alone group and 23 patients in the combined surgery group. The mean follow-up period was 2.1 ± 1.8 years (range: 1 to 5 years) in the horizontal muscle surgery alone group and 1.2 ± 1.2 years (range: 1 to 4 years) in the combined surgery group (P = .16). At the final follow-up visit of the horizontal muscle surgery alone group, the horizontal angle of deviation in primary position was 3.6 ± 5.0 PD (range: 0 to 14 PD) and 2.6 ± 4.4 PD (range: 0 to 12 PD) at distance and near, respectively. At the final visit of the combined surgery group, the angle of deviation was 4.0 ± 6.2 PD (range: 0 to 16 PD) and 3.4 ± 5.6 PD (range: 0 to 14 PD) at distance and near, respectively. There were no significant differences in angle of deviation in primary position between the groups (P = .75 at distance and .89 at near).
Surgical Outcomes According to Superior Oblique Muscle Weakening Surgery
The A-pattern amount in the horizontal muscle surgery alone group (10.9 ± 4.3 PD; range: 8 to 18 PD) was significantly higher than that in the combined surgery group (6.7 ± 2.3 PD; range: 0 to 8 PD) (P = .02). The postoperative degree of superior oblique overaction in the combined surgery group was significantly lower than it was preoperatively (0.4 ± 0.4 and 2.0 ± 1.1, respectively) (P < .01). For the horizontal muscle surgery alone group, the postoperative degree of superior oblique overaction was also lower than it was preoperatively, but the difference was not significant (1.2 ± 0.6 and 1.8 ± 1.0, respectively) (P = .13). The degree of superior oblique overaction was significantly lower in the combined surgery group (0.8 ± 0.5; range: 0 to 1.5) than it was in the horizontal muscle surgery alone group (1.8 ± 1.1; range: 1 to 3) (P = .04). Superior rectus recession for dissociated vertical deviation was performed on 5 (29.4%) and 5 (21.7%) patients in the horizontal muscle surgery alone and combined surgery groups, respectively. The mean A-pattern amount was decreased from 18.6 ± 5.9 to 6.6 ± 3.0 PD and from 18.8 ± 6.1 to 8.0 ± 2.6 PD in patients with and without superior rectus recession, respectively. The mean preoperative degree of dissociated vertical deviation was 3.0 ± 0.6 (range: 2 to 4) and 1.5 ± 0.7 (range: 1 to 3) in patients with and without superior rectus recession, respectively. At the final follow-up visit, the mean degree of dissociated vertical deviation was 0.8 ± 0.7 (range: 0 to 2) and 0.9 ± 0.7 (range: 0 to 2) in patients with and without superior rectus recession, respectively. There was no statistically significant difference (P = .54).
In comparing success rates, 9 (57.1%) and 18 (80%) patients showed success at their final follow-up visit in the horizontal muscle surgery alone and combined surgery groups, respectively. There was a significant difference in success rates between the groups (P = .04). During the follow-up period, 8 (42.9%) patients in the horizontal muscle surgery alone group underwent reoperation. Four patients with deteriorated superior oblique overaction underwent a superior oblique posterior tenotomy. One patient who complained of nystagmus underwent a Kestenbaum operation. Three patients who developed recurrent exotropia with significant superior oblique overaction underwent unilateral lateral rectus recession combined with a superior oblique posterior tenotomy (Table 2). Three (15.4%) patients in the combined surgery group underwent superior rectus muscle recession with dissociated vertical deviation during the follow-up period.
The condition of A-pattern exotropia with dissociated vertical deviation and superior oblique overaction is a rare disorder and poorly understood. To the best of our knowledge, there have been no studies on these conditions since they were first reported in 1969.10 The prevalence and clinical manifestations are also not well known. This study is the first to report the clinical characteristics and surgical outcomes of A-pattern exotropia with dissociated vertical deviation and superior oblique overaction.
Generally, amblyopia is relatively uncommon in patients with exotropia because they maintain central binocular fusion. Chia et al.12 reported that the prevalence of amblyopia was only 16% in patients with basic intermittent exotropia in Asian populations. The prevalence of amblyopia among the patients in this study was 45%. Patients with strabismus often have latent nystagmus; however, only 25% of the patients in this study were seen to have latent nystagmus. Lim et al.13 reported that the prevalence of latent nystagmus was only 3.8% in intermittent exotropia. We speculated that a complex deviation induced reduction of binocularity in the visual cortex and impairment of central fusional ability.14 Some patients (15%) in this study had neurological deficits such as delayed development and hemiplegia. These might be risk factors for the occurrence of these complex forms of strabismus.
Clinical features of A-pattern exotropia with dissociated vertical deviation and superior oblique overaction such as pattern deviation, symmetry, and degree of dissociated vertical deviation and superior oblique overaction presented variably in this study. Thus, surgical treatment was considered based on individual conditions of strabismus. Helveston10 reported that bilateral superior oblique tenotomy had a beneficial effect on the A-pattern exotropia component of this type of strabismus. We analyzed surgical results of two groups and found significantly different surgical success rates. However, reoperation rates were not significantly different. We suggested that horizontal muscle surgery alone might be effective when the degree of superior oblique overaction is minimal, abnormal head position such as chin-up position for fusion is absent, and A-pattern deviation of exotropia is not clinically apparent. Superior oblique weakening surgery could cause aggravation of preexisting dissociated vertical deviation. The patients sometimes have high-grade fusion, and bilateral superior oblique weakening might carry a significant risk factor for secondary superior oblique paresis or asymmetry and postoperative diplopia.15 Previous studies reported that surgical success rates for intermittent exotropia varied from 56% to 88% depending on the surgical method and the length of the follow-up period.16,17 In this study, the surgical success rates in patients who underwent horizontal muscle surgery alone or combined with bilateral superior oblique tenotomy were 57.1% and 80%, respectively.
There are some limitations in this study. First, the sample size was relatively small and medical records were retrospectively reviewed. Second, the follow-up period was relatively short. Third, the surgical techniques used in the study were variable.
The triad of A-pattern exotropia, dissociated vertical deviation, and superior oblique overaction is an uncommon condition and is treated with different surgical techniques. The surgical success rate in this study varied from 57.1% to 80% depending on whether weakening of the superior oblique muscle was performed. This study may provide a better understanding of this type of obscure, complex strabismus.
- von Noorden GK, Olsen CL. Diagnosis and surgical management of vertically incomitant horizontal strabismus. Am J Ophthalmol. 1965;60:434–442. doi:10.1016/0002-9394(65)90707-5 [CrossRef]
- Scott WE, Drummond GT, Keech RV. Vertical offsets of horizontal recti muscles in the management of A and V pattern strabismus. Aust N Z J Ophthalmol. 1989;17:281–288. doi:10.1111/j.1442-9071.1989.tb00534.x [CrossRef]
- Knapp P. Vertically incomitant horizontal strabismus: the so-called “A” and “V” syndromes. Trans Am Ophthalmol Soc. 1959;57:666–669.
- Costenbader F. Symposium: the A and V patterns in strabismus. Introduction. Trans Am Acad Ophthalmol Otolaryngol. 1964;68:354–355.
- Helveston EM. Dissociated vertical deviation: a clinical and laboratory study. Trans Am Ophthalmol Soc. 1980;78:734–779.
- Brodsky MC. Dissociated vertical divergence: a righting reflex gone wrong. Archives of Ophthalmology. 1999;117:1216–1222. doi:10.1001/archopht.117.9.1216 [CrossRef]
- Bielschowsky A. Disturbances of the vertical motor muscles of the eyes. Arch Ophthalmol. 1938;20:175–200. doi:10.1001/archopht.1938.00850200013001 [CrossRef]
- Clarke WN, Noel LP. Surgical results in intermittent exotropia. Can J Ophthalmol. 1981;16:66–69.
- Biglan AW, Davis JS, Cheng KP, Pettapiece MC. Infantile exotropia. J Pediatr Ophthalmol Strabismus. 1996;33:79–84.
- Helveston EM. A-exotropia, alternating sursumduction, and superior oblique overaction. Am J Ophthalmol. 1969;67:377–380. doi:10.1016/0002-9394(69)92049-2 [CrossRef]
- Raab EL, Parks MM. Recession of the lateral recti: early and late postoperative alignments. Arch Ophthalmol. 1969;82:203–208. doi:10.1001/archopht.1969.00990020205010 [CrossRef]
- Chia A, Roy L, Seenyen L. Comitant horizontal strabismus: an Asian perspective. Br J Ophthalmol. 2007;91:1337–1340. doi:10.1136/bjo.2007.116905 [CrossRef]
- Lim HT, Smith DR, Kraft SP, Buncic JR. Dissociated vertical deviation in patients with intermittent exotropia. J AAPOS. 2008;12:390–395. doi:10.1016/j.jaapos.2007.11.019 [CrossRef]
- Kommerell G. The relationship between infantile strabismus and latent nystagmus. Eye (Lond). 1996;10:274–281. doi:10.1038/eye.1996.58 [CrossRef]
- Plager DA, Buckley EG, Repka MX, Wilson ME. Strabismus Surgery: Basic and Advanced Strategies, 1st ed. American Academy of Ophthalmology Mongraph Series, vol 17. Oxford: Oxford University Press; 2004.
- Richard JM, Parks MM. Intermittent exotropia: surgical results in different age groups. Ophthalmology. 1983;90:1172–1177. doi:10.1016/S0161-6420(83)34410-9 [CrossRef]
- Lee S, Lee YC. Relationship between motor alignment at postoperative day 1 and at year 1 after symmetric and asymmetric surgery in intermittent exotropia. Jpn J Ophthalmol. 2001;45:167–171. doi:10.1016/S0021-5155(00)00351-8 [CrossRef]
- Wright KW, Spiegel PH, eds. Pediatric Ophthalmology and Strabismus, 2nd ed. Berlin: Springer Science & Business Media; 2013.
|No. of patients||40|
|Mean age at diagnosis (y)||5.5 ± 4.6 (range: 1 to 20)|
|Mean age at surgery (y)||12.3 ± 12.8 (range: 2 to 49)|
|Mean refraction (D)||−0.80 ± 1.90b (range: −5.80 to 2.50)|
| Unilateral||8 (20%)|
| Bilateral||10 (25%)|
|Latent nystagmus||10 (25%)|
|Delayed development||4 (10%)|
| Distance||27.7 ± 11.2 (range: 14 to 55)|
| Near||28.5 ± 10.9 (range: 18 to 60)|
| A-pattern amount||18.8 ± 5.9 (range: 12 to 35)|
|Degree of SOOA||1.9 ± 1.1 (range: 1 to 4)|
| Asymmetrical||4 (10%)|
| Symmetrical||36 (90%)|
|Degree of DVD||2.1 ± 0.9 (range: 1 to 4)|
| Asymmetrical||24 (60%)|
| Symmetrical||16 (40%)|
|Measurable stereopsis||20 (50%)|
| None||4 (10%)|
| Gross (800 to 200 sec arc)||16 (40%)|
| Fine (60 sec arc or better)||0 (0)|
Surgical Outcomes According to Superior Oblique Muscle Weakening Surgerya
|Factor||Horizontal Muscle Surgery Alone (n = 17)||Combined Surgery (n = 23)b||P|
|No. of operated muscles||2.0 ± 0.6 (1 to 3)||3.4 ± 0.5 (3 to 4)||< .001c|
|Combined with superior rectus recession||5 (29.4%)||5 (21.7%)||.66d|
|Mean follow up (y)||2.1 ± 1.8 (0.5 to 5)||1.2 ± 1.2 (0.5 to 4)||.16c|
|Angle of deviation (PD)|
| Distance||3.6 ± 5.0 (0 to 14)||4.0 ± 6.7 (0 to 16)||.75c|
| Near||2.6 ± 4.4 (0 to 12)||3.4 ± 5.6 (0 to 14)||.89c|
| A-pattern amount||10.9 ± 4.3 (8 to 18)||6.7 ± 2.3 (0 to 8)||.02c|
|SOOA||1.8 ± 1.1 (1 to 3)||0.8 ± 0.5 (0 to 1.5)||.04c|
|Success||9 (57.1%)||18 (80%)||.04d|
|Reoperation||8 (42.9%)||3 (15.4%)||.18d|