Journal of Pediatric Ophthalmology and Strabismus

Original Article Supplemental Data

Role of Botulinum Toxin Type A in Cyclic Esotropia: A Long-Term Follow-up

Ayse Ipek Akyuz Unsal, MD; Seyhan B. Özkan, MD; Sule Ziylan, MD

Abstract

Purpose:

To describe two patients with childhood cyclic esotropia 8 and 9 years after they underwent botulinum toxin type A treatment to report its long-term outcome.

Methods:

Two patients with sudden onset cyclic esotropia aged 2 and 4 years were included. Botulinum toxin type A injections were performed on the appropriate muscles.

Results:

The first patient was a 2-year-old boy with left dominant alternating esotropia on a cyclic basis. His strabismus ranged from 25 to 45 prism diopters (PD) at near and distance. A botulinum toxin type A injection into the left medial rectus muscle revealed orthotropia at near and distance with a stereopsis of 60 seconds of arc (arcsec). During the 9 years of follow-up, he remained stable. The second patient was a 4-year-old girl who complained of double vision and strabismus. Her deviation was 40 PD at near and 35 PD at distance on a cyclic pattern. She became orthotropic with glasses after a bimedial botulinum toxin A injection. During the 8 years of follow-up, she remained stable with a stereo-acuity of 120 arcsec.

Conclusions:

Considering the consecutive and recurrent deviations with surgical treatment in previous reports, botulinum toxin type A is an appropriate first-line option for the treatment of cyclic deviations, despite its limitations. The results suggest that botulinum toxin type A is an effective method to break the cycle in cyclic esotropia permanently.

[J Pediatr Ophthalmol Strabismus. 2019;56(6):360–364.]

Abstract

Purpose:

To describe two patients with childhood cyclic esotropia 8 and 9 years after they underwent botulinum toxin type A treatment to report its long-term outcome.

Methods:

Two patients with sudden onset cyclic esotropia aged 2 and 4 years were included. Botulinum toxin type A injections were performed on the appropriate muscles.

Results:

The first patient was a 2-year-old boy with left dominant alternating esotropia on a cyclic basis. His strabismus ranged from 25 to 45 prism diopters (PD) at near and distance. A botulinum toxin type A injection into the left medial rectus muscle revealed orthotropia at near and distance with a stereopsis of 60 seconds of arc (arcsec). During the 9 years of follow-up, he remained stable. The second patient was a 4-year-old girl who complained of double vision and strabismus. Her deviation was 40 PD at near and 35 PD at distance on a cyclic pattern. She became orthotropic with glasses after a bimedial botulinum toxin A injection. During the 8 years of follow-up, she remained stable with a stereo-acuity of 120 arcsec.

Conclusions:

Considering the consecutive and recurrent deviations with surgical treatment in previous reports, botulinum toxin type A is an appropriate first-line option for the treatment of cyclic deviations, despite its limitations. The results suggest that botulinum toxin type A is an effective method to break the cycle in cyclic esotropia permanently.

[J Pediatr Ophthalmol Strabismus. 2019;56(6):360–364.]

Introduction

Cyclic esotropia is characterized by alternating periods of esotropia and orthophoria within a certain cycle, which is usually 48 hours but can range between 24 and 96 hours. This rare type of strabismus was described by Burian1 and then Costenbader and Mousel2 in the English literature. More rarely, cyclic exotropia and cyclic vertical or cyclo-vertical deviations were also reported.3–9 Cyclic esotropia typically affects preschool children, but adult onset cases have also been reported.10–13 Although it is thought to be related to the abnormalities in physiologic circadian rhythm, central nervous system pathologies, and factors disturbing fusion, the exact pathophysiologic mechanism remains a mystery.14–18 Several reports identified different types of etiological factors (eg, visual loss due to optic atrophy, high myopia with amblyopia, myopic strabismus fixus, traumatic aphakia, traumatic sixth nerve palsy, retinal detachment surgery, reactivated myopic choroidal neovascularization, retinitis pigmentosa, dysthyroid ophthalmopathy, ocular myositis, strabismus surgery, craniofacial surgery for fronto-orbital fibrous dysplasia, central nervous system disease, and menstrual cycle) that seemed unrelated to one another in origin.4,6–12,15,18–24

The expected natural evaluation is the break of the cycle and a constant strabismus on an everyday basis if left untreated.25 The main treatment option for cyclic esotropia was surgery on the strabismus day before the development of constant esotropia.1,11,12,26–29 However, surgical intervention for cyclic esotropia may convert the problem into cyclic exotropia or late-onset consecutive exotropia (after 5 years), as well as alternating cycles between esotropia and exotropia.13,29–31 Late recurrence of cyclic esotropia may be observed 16 months later.32 The alternative treatment for cyclic esotropia was botulinum toxin type A injection in limited case reports.33–37 However, the long-term outcome of botulinum toxin type A treatment in cyclic esotropia is unknown. We describe two patients with childhood cyclic esotropia who underwent botulinum toxin type A treatment and were followed up 8 and 9 years later to determine the long-term outcome of botulinum toxin type A treatment.

Patients and Methods

Two patients who presented with sudden onset cyclic esotropia at age 2 and 4 years were included. Both patients underwent full ophthalmologic and orthoptic assessments and cranial magnetic resonance imaging. Botulinum toxin type A was injected into the medial rectus muscles in both patients in a 5-IU dose under ketamine anesthesia with the guidance of electromyography. Follow-up was 9 and 8 years, respectively.

Case 1

A 2-year-old boy was referred with sudden onset esotropia that showed variability day by day. The family and medical history was unremarkable. His ophthalmologic examination revealed left dominant alternating esotropia fluctuating between 25 and 45 prism diopters (PD) at near and distance (Figure 1). Visual acuity seemed to be equal in both eyes. Cycloplegic refraction measurements were +0.75 D in the right eye and +1.00 D in the left eye. Ocular motility, anterior segment, and funduscopic examinations were within the normal range. He could not cooperate with stereopsis tests. Two hours of patching for the right eye was prescribed to avoid amblyopia, and the parents were asked to record the strabismus and non-strabismus periods. It was recorded that he had cyclic esotropia with a 48-hour cycle. The patient did not cooperate with patching.

Case 1 with periods of cyclic esotropia showing (A) strabismus and (B) non-strabismus.

Figure 1.

Case 1 with periods of cyclic esotropia showing (A) strabismus and (B) non-strabismus.

Five IU of botulinum toxin type A was injected into the left medial rectus muscle under ketamine anesthesia with electromyography guidance. He had a transient period of abnormal head posture to the right side and mild ptosis that did not cover the pupillary axis. The abnormal head posture lasted for 2 months and then he was found to be orthophoric in primary position with no fixation preference. His ophthalmologic examination 14 months after botulinum toxin type A injection revealed a visual acuity of 20/20 in both eyes with orthophoria at near and distance and stereopsis of 60 seconds of arc (arcsec) on the TNO stereotest (Good-Lite, Elgin, IL). During the 9 years of follow-up, his ocular findings remained stable (Figure 2).

Case 1 at (A) 1 week after the left medial rectus botulinum toxin type A injection (with left ptosis and orthophoria with abnormal head posture), (B) orthophoria after 14 months of botulinum toxin type A injections, and (C) orthophoria 9 years after botulinum toxin type A injections.

Figure 2.

Case 1 at (A) 1 week after the left medial rectus botulinum toxin type A injection (with left ptosis and orthophoria with abnormal head posture), (B) orthophoria after 14 months of botulinum toxin type A injections, and (C) orthophoria 9 years after botulinum toxin type A injections.

Case 2

A 4-year-old girl who complained of double vision and strabismus that disappeared on some days was admitted to the clinic. Her father and grandfather also had strabismus and her mother's cousin had amblyopia. Her medical history was unremarkable. Her visual acuity was 20/20 in the right eye and 20/30 in the left eye. Ocular motility was within the normal range. On the non-strabismus day, the Lang II test revealed stereopsis of 200 arcsec but no stereopsis was found on the TNO stereotest. With respect to the cycloplegic refractive measurements, fully corrected glasses were prescribed with +1.75 +0.75 @ 50 for the right eye and +2.25 +1.00 @ 105 for the left eye. Because the patient had left amblyopia, 4 hours of patching was prescribed, and the parents were asked to record the periods of strabismus. The family recordings revealed that her strabismus had a 48-hour cycle. Left alternating esotropia was observed with crossed Bagolini test at near and distance with the absence of stereopsis on the strabismus day. Her deviation was 40 PD at near and 35 PD at distance with glasses on a cyclic pattern, and her visual acuity was 20/20 in both eyes with glasses (Figure 3).

Case 2 with periods of cyclic esotropia showing strabismus (A) with and (B) without glasses and (C) non-strabismus.

Figure 3.

Case 2 with periods of cyclic esotropia showing strabismus (A) with and (B) without glasses and (C) non-strabismus.

Because the patient's cyclic esotropia did not respond to the refractive correction, she underwent bimedial botulinum toxin type A injection of 5 IU under ketamine anesthesia. Adduction was not restricted after the botulinum toxin type A injection.

She was orthophoric with glasses by the second month of botulinum toxin type A injections. By the third month, she complained of diplopia and the prism cover test revealed 8 PD of esotropia at near. Therefore, bifocal lenses were prescribed with +3.00 addition, and she became orthophoric without diplopia. During the 8 years of follow-up, she remained stable with stereoacuity of 120 arcsec and bifocal lenses were successfully weaned off (Figure 4).

Case 2 (A–B) 2 months after botulinum toxin type A injection with glasses. (C) Orthophoria with bifocal lenses at 4 months after botulinum toxin type A injection. (D) Eight years after botulinum toxin type A injection without glasses.

Figure 4.

Case 2 (A–B) 2 months after botulinum toxin type A injection with glasses. (C) Orthophoria with bifocal lenses at 4 months after botulinum toxin type A injection. (D) Eight years after botulinum toxin type A injection without glasses.

Discussion

In the presented patients, botulinum toxin type A injection was found to be successful either as a cycle-breaking or a curative agent. Both of our patients had orthophoria and a good level of stereopsis in the long term.

Cyclic esotropia is a rare and idiopathic motility disorder characterized by alternating periods of nonstrabismus and strabismus that range between 24 and 96 hours and most frequently manifest between the ages of 3 and 4 years. Typically, a large angle of strabismus is seen with suppression on strabismus days. It usually presents as acquired non-accommodative esotropia, but it may also be observed in the form of accommodative, congenital, or consecutive esotropia.23,33,38–41 Adult onset acquired cases are usually seen following problems that disturb fusion.10,21 The underlying mechanism of cyclic esotropia could be the decompensation of a latent strabismus by a triggering event on fusion. In our second patient, diplopia suggested the disruption of the fusion and botulinum toxin type A injection may have helped to rebuild the “weak fusion mechanism” as reported previously.42 We called it “weak fusion” because the patient required bifocal lenses to maintain the orthophoric period provided by botulinum toxin type A.

Cyclic esotropia should be treated early before development of constant sensorial adaptations. Prisms as a non-invasive treatment option or botulinum toxin type A as a minimally invasive treatment option were previously used in some case reports with variable success.33–37,43 Voide et al.43 suggested prisms as a non-invasive therapy for cyclic esotropia and reported a successful result in a case at 24 months of follow-up. Wipf et al.37 initially prescribed prisms in two of their three patients who ended up with failure, whereas all of their three patients achieved orthotropia after botulinum toxin type A injection. In our patients, we did not prefer prisms because of their negative effect on visual acuity and contrast sensitivity that may be an obstacle for the control of the cyclic deviation. The negative effects of prisms on visual acuity, contrast sensitivity, and fusion increase with the power in both Fresnel and conventional prisms. It was previously demonstrated that 20 PD Fresnel prisms decrease visual acuity by four lines, whereas conventional prisms of the same amount decrease it by two lines.44,45 Paired 25 PD disrupted fusion in 80% of cases with Fresnel prisms and 20% of cases with conventional prisms.45 Considering the large angle of strabismus in our patients, prism therapy was not a good option to restore binocular vision.

To the best of our knowledge, Riordan-Eva et al.33 were the first to use and report the effect of botulinum toxin type A on two adult patients with cyclic esotropia. Recurrent injections of botulinum toxin type A temporarily improved strabismus in their patients. In another study, botulinum toxin type A injections broke the cycle, but the patient required surgery to achieve orthotropia.35 In childhood cyclic esotropia, successful results with botulinum toxin type A were reported in only 5 cases, with follow-up ranging from 8 to 16 months.34,36,37 However, the reported late recurrence, 16 months after surgery, suggested the need for long-term follow-up for cyclic esotropia.32 The cycle disappeared after a single dose of botulinum toxin type A in both patients, and the effect was permanent for a minimum of 8 years.

Although information about the outcome of botulinum toxin type A treatment is limited, the results of the treatment seem more successful in children with cyclic esotropia than adults.33–37 The conflicting results could be explained by the difference between the level of visual acuity, the fusional capacity, and the plasticity of a child's brain.

Several reports on cyclic esotropia postulated the effect of surgical treatment, targeting to correct the angle on the strabismus day.1,11,12,27–29 However, consecutive and recurrent deviations may develop years later.13,29–32 On the other hand, Souza-Dias et al.28 reported long-term success with surgery in childhood cyclic esotropia. Reports of childhood onset cyclic esotropia summarizing the effect and follow-up of surgery and botulinum toxin type A treatments are shown in Table A (available in the online version of this article).

Summary of The Reports on Treatment of Childhood Onset Cyclic EsotropiaSummary of The Reports on Treatment of Childhood Onset Cyclic EsotropiaSummary of The Reports on Treatment of Childhood Onset Cyclic Esotropia

Table A:

Summary of The Reports on Treatment of Childhood Onset Cyclic Esotropia

Both surgical treatment and botulinum toxin type A injection aim to provide an orthophoric period with a peripheral mechanical effect and restoration of the periodically unstable binocular cooperation of an unknown origin. Keeping the eyes aligned on strabismus days helps the binocular system build control of the deviation. The disadvantages of surgery are the potential risks of surgery and anesthesia and possible consecutive deviations. Botulinum toxin type A injection is a minimally invasive, easily repeatable, and non-scarring treatment option with satisfactory results. The potential disadvantages of botulinum toxin type A treatment are ptosis that may be amblyogenic in children and vertical deviations that may block the restoration of binocularity.

The current study is limited by the lack of comparative data due to its rarity and the variability of the patient characteristics of cyclic esotropia.

Conclusions

Considering the consecutive and recurrent deviations with surgical treatment in previous reports, botulinum toxin type A seems to be an appropriate first-line option for treatment of cyclic deviations despite the limitations of a non-comparative assumption. Our results suggest that in long-term follow-up, botulinum toxin type A is safe and effective to either break the cycle or permanently control the deviation in cyclic esotropia.

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Summary of The Reports on Treatment of Childhood Onset Cyclic Esotropia

Case No (Reference)AgeSexFamily HistoryAssociating Ophthalmic or Systemic DisorderDuration of CyclesDiplopiaAngle of Deviation (PD)TreatmentFinal OutcomeFollow-up
1 (Metz et al. 1995)2 yearsFUnknownSmall hyperopic refractive error Rapid travel over 6 time zones48 hours-L ET 35 PD at near & distanceL MR rec. L LR res.Orthophoric3 months
2 (Cahill et al.1999)3½ yearsFUnremarkableModerate hyperopia +2.50 OU Previous L MR 5 mm rec. L LR 5 mm res.48 hours-L ET 50PDR MR 5 mm rec. R LR 5 mm res.Recurrence 16 months after first surgery. 100 arcsec on Wirt after second surgery15 months
3 (Sohn et al1999) (abstract only)3 yearsMUnknownHead trauma--ETBTXA Bil. MRCyclic pattern & ET disappeared12 months
4 (Drummondet al. 2003)14 yearsFUnknownPrevious L MR 5 rec. L IO rec. Hyperopia R+4.00 (+0.50 x 135), L+4.00 (+0.25 x 160) IO overaction OU48 hours-L ET 30 PD at distance 35 PD at near with glassesR MR 5.5 mm rec. L MR 2.5 mm rec. Bil. IO rec.6 PD at near & distance Accomodative L ET with spectacles 40 arcsec stereopsis at Frisby9 months
5 (Kee et al.2004)6 yearsMUnknownAccomodative ET R +5.50 L +4.7548 hours-ET 25–30 PDBil. MR rec.4 PD esophoria with 50 arcsec stereopsis on Randot3 years
6 (Post et al.2007)2 yearsMUnknownRight amblyopia Hyperopia +0.75 OU48 hours+R ET 45 PD at near & distanceBimedial 6mm rec. & Bil IO myectomyConsecutive intermittant XT 12 PD at near 16 PD at distance5 years
7 (Jones etal. 2014)3 yearsFStrabismic amblyopiaAmblyopia Hypermetropia +1.50 OU48 hours+ET 30PD2.5 IU BTXA Bil. MR8 PD Esophoria 215 arcsec on Frisby6 months
8 (Wipf et al.2018)2¼ yearsMStrabismusRecent croup attack Hypermetropia +1.0 & +0.50 astigmatism OU48 hours+ET 55–65 PD at near & distance5IU BTXA Bil. MR12 PD near & 5 PD distance esophoria 120 arcsec on TNO16 months
9 (Wipf et al.2018)3¾ yearsFUnremarkablePrevious unsuccessful prism treatment Hypermetropia +1.50 OU48 hours-ET 53 PD at distance 60 PD at near5IU BTXA Bil. MR3–6 PD Esophoria with bifocals 120 arcsec on TNO11 months
10 (Wipf et al.2018)3 yearsMUnremarkablePrevious unsuccessful prism treatment Hypermetropia R +0.75 L +1.25 (−0.50 astigmatism OU)48 hours-ET 10 PD on straight days5IU BTXA Bil. MROrthotropia (+) Lang test8 months
11 (Merrill et al.2018) (abstract only) 5 casesAge range: 2–6 years-Unknown2 of 5 cases had abnormal white matter signal in the frontal lob on MRI48 hours+(3cases) −(2 cases)Max. 35 PD ETBimedial rec. in all casesOne patient required reoperation, others not.Unknown
12 (Souza-Diaset al. 2018)5 yearsMUnknownHyperopia +4.0 OU L microtropia on straight days48 hours+L ET 25 PD with spectacles 32 PD without spectaclesBimedial 4 mm rec.Esophoria with 8 PD (+) Lang test5 years
13 (Souza-Diaset al. 2018)7 yearsMUnknownPrevious Bil. 6 mm LR rec. for intermittant XT slight myopia R −1.00 (+0.25 × 90) L −0.75 (+0.50 × 90)48 hours+R ET 20 PD at near & distanceBil. 4 mm MR rec. after unsuccessful 20 PD base out FresnelXT with 5PD at distance Orthophoria at near 40 arcsec stereopsis Stable with 0–8 PD intermittant XT11 years
14 (Souza-Diaset al. 2018)3¼ yearsMUnknownHypermetropia +4.25 OU Mild amblyopia Monofixation S.48 hours-L ET 30 PD at near & distanceBil. 5 mm MR rec.L Microtropia at near & distance5 years
15 (Souza-Diaset al. 2018)6 yearsMUnknownHead Trauma Amblyopia Mild hyperopia R +4.0 (+1.0 × 90) L +3.50 (+1.50 × 90)48 hours+ET 45 PD at near & distance 15 PD V patternBil. 5 mm MR rec.Orthophoria without A or V pattern at near & distance 40 arcsec stereopsis16 years
16 (Souza-Diaset al. 2018)8 yearsFUnknownHead trauma Hypermetropia +0.50 OU previous unsuccessful 0.06% ecothiophate iodide treatment48 hours+ET 30 PD at near & distanceBil. 5mm MR rec.Orthophoria at near & distance11 years
17 Presented study2 yearsMUnremarkableHypermetropia R +0.75 L +1.048 hours-L ET Varying between 25–30 PD5IU BTXA LMROrthotropic 60 arcsec on TNO9 years
18 Presented study4 yearsFStrabismus & amblyopiaHypermetropia R +1.75(+0.75 x 50) L+2.25(+1.00 x 105)48 hours+ET 35 PD at distance 40 PD at near5IU BTXA Bil. MROrthotropic 120 arcsec on TNO8 years
Authors

From the Department of Ophthalmology, Adnan Menderes University, Aydin, Turkey (AIAU, SBO); and the Department of Ophthalmology, Yeditepe University, Istanbul, Turkey (SZ).

The authors have no financial or proprietary interest in the materials presented herein.

Correspondence: Ayse Ipek Akyuz Unsal, MD, Adnan Menderes Üniversitesi, Faculty of Medicine, Department of Ophthalmology, Merkez Kampüsü–Kepez Mevkii, Efeler, 09110 Aydin, Turkey. E-mail: ipekunsal@yahoo.com

Received: May 06, 2019
Accepted: August 19, 2019

10.3928/01913913-20190909-01

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