Strabismus, 2014; 22(3): 138–142 ! Informa Healthcare USA, Inc. ISSN: 0927-3972 print / 1744-5132 online DOI: 10.3109/09273972.2014.907814

Results of Bilateral Medial Rectus Recession for Comitant Esotropia in Patients with Developmental Delay Meenakshi Swaminathan, MS, Sanil V. Shah, MS, Shruti Mittal, DNB, and Aarthy Gunasekaran, MPhil Department of Pediatric Ophthalmology, Medical Research Foundation, Chennai, India

ABSTRACT Purpose: There is paucity of literature on surgical outcomes after strabismus surgery in patients with developmental delay. There is no consensus regarding whether standard surgical tables are applicable to these children. The goal of our study was to determine results of strabismus surgery for esotropia among these children. Methods: Two retrospective cohorts of patients, with developmental delay (excluding Down syndrome) and without developmental delay, who underwent bimedial recession for comitant eso-deviation between January 2005 and January 2011, meeting our criteria, were selected. Amount of surgery performed in these children was compared with standard table. This comparison gave us operated angle of deviation. This operated angle of deviation was expressed as percentage of preoperative angle of deviation to get amount of surgery performed. Response to surgery was defined as percentage of change in angle of deviation after surgery to the operated angle of deviation. Amount of surgery performed, response to surgery, and results were compared between two groups. Results: This study included 25 patients with developmental delay and 53 normal children with comitant esotropia. Age, refractive error, and preoperative angle of deviation were comparable in patients with and without developmental delay. Among patients with developmental delay, on average 72.13% ± 16.08 of angle of deviation was operated; response to surgery gained was 134.06% ± 51.62. In the control group, the average amount of surgery done was 89.08% ± 10.83; response gained was 89.83% ± 22.49. Successful outcome (±10 PD of orthophoria) was noted in 60% patients with developmental delay compared to 73.58% in control group. On average 70.67% ± 17.95 angle of deviation was operated in patients with developmental delay with successful outcome. Conclusion: Surgical outcome in patients with developmental delay is very unpredictable. An exaggerated response to standard amounts of bimedial recession should be anticipated in these patients. Though there was no statistically significant difference, operating for 70.67% ± 17.95 angle of deviation is more likely to be successful. Keywords: Strabismus, esotropia, pediatric, developmental delay, surgical dosage, surgical outcome

including developmental delay.1 It is known that children with developmental delays have a higher rate of ophthalmic abnormalities. Strabismus has been found to be one of the most frequent ophthalmic anomalies in these children.2–5 Esotropia has been noted in an

INTRODUCTION According to a World Health Organization (WHO) report, in 2004 around 5% of children aged less than 14 years have a moderate to severe disability

Received 6 December 2012; Revised 14 January 2014; Accepted 12 March 2014; Published online 30 April 2014 Correspondence: Meenakshi Swaminathan, Medical Research Foundation, 18 College Road, Chennai, India. PIN Code: 600 006. E-mail: [email protected]

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Bilateral medial rectus recession in developmental delay average of 30% of all patients with a range of 11% to 51%. Occurrence of exotropia was noted to be around 10%.2 Healthy infants who have had strabismus surgery for esotropia have shown improvement of motor skills comparable to those of healthy children without esotropia.6 So it is likely that optimal surgical correction of strabismus may influence development in children with developmental delay.7 Little has been published about surgical outcomes after strabismus surgery for esodeviation in this group.4,8–15 There is no consensus in the literature regarding whether standard surgical tables are applicable to these children. Few studies reported no difference in surgical outcome in these children, especially those with Down syndrome.9,10,14,15 Whereas others found surgery in these patients less predictable, a high rate of overcorrection with standard surgical schedules and improved outcome with more conservative amount of surgery.10,11 It was postulated that standard surgical tables cannot be applied in these children because of global muscle tone abnormality and different length-tension relationship of muscles of these children.8 Therefore, the goal of our study was to determine results of strabismus surgery for esotropia among developmentally delayed children (aged less than 18 years) without Down syndrome.

MATERIAL AND METHODS This study adhered to the tenets of the Declaration of Helsinki. Records of children with and without developmental delay who underwent bimedial recession surgery for comitant esotropia during a 6-year period from 2005 to 2011 were reviewed. Exclusion criteria were children with Down syndrome, vertical deviation, limited ocular movements, incomitant deviation, strabismus secondary to other eye pathology, previous eye muscle surgery, or postoperative follow-up of less than 6 weeks. Among patients without developmental delay, children having subnormal visual acuity, nystagmus, or other ocular pathology were also excluded. All the children had undergone comprehensive eye examination preoperatively. Ocular examination including angle of deviation, ocular movements, and cycloplegic refraction was performed preoperatively and at the 6-week postoperative visit in all patients. Visual acuity was assessed by CSM method, Snellen’s chart, or Lea symbols depending on age and ability of child. Cooperation for binocular function tests was poor in many patients with developmental delay. Angle of deviation was measured by the use of alternate prism cover test; modified Krimsky method was used when cooperation was poor (same method was used for pre- and !

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postoperative measurement). Refractive error was measured after cycloplegia with cyclopentolate 1% or homatropine 2% (in patients with CNS or seizure disorders). Glasses were prescribed for amblyopia and accommodative concerns. Refractive errors and amblyopia were treated before surgery. Children with hyperopia and esotropia were treated with full cycloplegic retinoscopy value. Myopes were prescribed full cycloplegic correction. The preoperative and postoperative angle of deviation was calculated for each subject as the mean of distant and near angles if measured by alternate prism cover test, or the Krimsky measurement at near. Preoperative angle of deviation was measured at least twice before surgery by operating surgeon. Surgery was planned by operating strabismologist and small postoperative undercorrection was aimed in all cases. In patients with developmental delay, a greater amount of undercorrection was planned considering the past reports of exaggerated response to standard amount of surgery. Surgery performed on horizontal muscles in each patient was correlated with the standard table used for routine strabismus surgeries (in normal children).16 This comparison with the standard table gave us angle of deviation (B), which would have been corrected in a normal child with the same amount of surgery. This operated angle of deviation (B) was expressed as a percentage of preoperative angle of deviation (A) to get amount of surgery performed. For example, one patient having 25 PD esotropia was operated for both eyes MR recession of 4.0 mm. When compared with the standard surgical table used for routine strabismus surgery, this amount of surgery is supposed to correct 20 PD of esotropia. So amount of surgery performed was 80% of the preoperative angle (amount of surgery performed = [operated angle of deviation 7 preoperative angle of deviation]  100). Response gained was expressed as percentage of change in angle of deviation (preoperative angle – postoperative angle of deviation) to the operated angle of deviation (B). For example, if in the above-mentioned patient postoperative angle of deviation at 6-week followup is 10 PD, change in angle of deviation with 4 mm of bilateral medial rectus recession will be 15 PD. So response gained will be 75% (Response gained = [(Preoperative angle of deviation – Postoperative angle of deviation) * 100 7 Operated angle of deviation]. Amount of medial rectus recession performed in the two groups was also compared. Statistical analysis was done using SPSS software. No complications were observed during or after the surgery. Successful outcome was defined as postoperative angle of deviation within 10 PD of orthophoria. Surgical success was determined at 6-week postoperative follow-up.

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RESULTS Twenty-five children with developmental delays and 53 children without developmental delays meeting our inclusion criteria were included in this study. Among patients with developmental delay, mean age was 4.96 ± 3.25 years (range, 1–12 years) and in the control group mean age was 5.037 ± 2.205 years (range, 1–13 years) at the time of surgery. Out of 25 children with developmental delays who underwent bimedial recession for esotropia, 2 children had hydrocephalus, 1 suffered from hypoxic ischemic encephalopathy, 5 children had cerebral palsy, 1 child had Dandy Walker malformation, 1 child suffered from neonatal encephalopathy, and 15 had nonspecific developmental delay after a neurologist’s opinion, imaging, and genetic workup. Most of the patients had multiple perinatal insults; 8 patients were preterm, 6 had birth asphyxia, 1 had meconium aspiration, 2 had neonatal jaundice, 3 had seizure in postnatal period, 1 had neonatal sepsis, and 1 had neonatal hypoglycemia. In 2 cases the mother had pregnancy-induced hypertension, 2 had diabetes, and 1 had anemia. Consanguinity was present in 4 cases. Nine children had no known perinatal insult. Preoperative angle of deviation, amount of surgery performed, postoperative angle of deviation, and response to surgery gained in patients with developmental delay and without developmental delay are shown Table 1. Out of 25 patients with developmental

delay, successful outcome was noted in 15 (60%) patients at 6 weeks postoperative follow-up. Undercorrection was noted in 7 (28%) patients and overcorrection was noted in 3 (12%) patients. Among normal patients, successful outcome was obtained in 39 (73.58%) patients. Fourteen patients (26.41%) had undercorrection and none had overcorrection. The difference in successful outcome rates in the 2 groups was not statistically significant using Fisher exact test (P = 0.294). Overall, 72.13% ± 16.08 of angle of deviation was operated in patients with developmental delay and 89.08% ± 10.83 in control group (p50.0001) (Table 1). Among patients with developmental delay who had a successful outcome average amount of surgery performed was 70.67% ± 17.95, while in control group average amount of surgery performed was 90.56% ± 9.99. On applying non-parametric ANOVA test, no significant difference was found in the amount of surgery performed in patients with undercorrection, optimal correction, or overcorrection, in either group (Table 2). Though there was a statistically significant difference in average amount of surgery performed between the 2 groups, the difference in amount of medial rectus recession was not statistically significant (P = 0.195) (Table 1). This may be due to difference in preoperative angle of deviation between the 2 groups. The response to surgery gained in patients with developmental delay was 134.06% ± 51.62,

TABLE 1. Comparison of patients with and without developmental delay. Developmental delay group (n = 25)

Control group (n = 53)

p value*

4.96 ± 3.25 18:7 +1.225 ± 2.02 44.4 ± 13.25 4.08 ± 11.28 72.13 ± 16.08 134.06 ± 51.62 5.04 ± 1.27

5.037 ± 2.205 34:19 +2.17 ± 1.62 39.25 ± 10.35 8.57 ± 7.66 89.08 ± 10.83 89.83 ± 22.49 5.39 ± 0.68

0.46 – 0.0655 0.1091 0.0344 50.0001 50.0001 0.1948

Age (years) Male:Female Spherical equivalent (D) Preoperative angle of deviation (PD) Post operative angle of deviation (PD) Amount of surgery performed (%) Response gained (%) Amount of Medial Rectus recession (mm) *Comparison of 2 groups using Mann-Whitney test.

TABLE 2. Comparison of outcomes in patients with and without developmental delay. Outcome No. of patients Developmental delay group Control group Amount of surgery performed (%) Developmental delay group Control group Response to surgery (%) Developmental delay group Control group

Successful outcome

Undercorrection

Overcorrection

p value

15 (60%) 39 (73.58%)

7 (28%) 14 (26.41%)

3 (12%) 0

– –

70.67 ± 17.95 90.56 ± 9.99

72.05 ± 12.32 84.97 ± 12.34

79.63 ± 17.01 –

0.5843* 0.1857y

143.36 ± 43.10 96.77 ± 19.15

90.63 ± 33.33 70.5 ± 20.128

188.98 ± 62.16 –

0.0118* 0.0003y

*Statistical comparison using nonparametric ANOVA test. yStatistical comparison using Mann-Whitney test. Strabismus

Bilateral medial rectus recession in developmental delay while in the control group the response to surgery was 89.28% ± 23.06. The difference was significant statistically between patients with and without developmental delay using Mann-Whitney test (Tables 1 and 2).

DISCUSSION Patients with developmental delay have a high prevalence of strabismus. But there have been very few studies regarding this topic. Hiles et al. performed surgery according to standard principles and noted a 77% success rate in children with nonaccommodative esotropia and cerebral palsy, even in the presence of severe motor involvement or mental retardation.4 Habot-Wilner and colleagues found a higher rate of surgical failure due to undercorrection in developmentally delayed children who received on average 0.84 mm lesser amount of recession of the medial rectus muscles when compared with developmentally normal children who received a standard amount of recession at 17 months mean postoperative follow-up. They noted surgical success in 56%, undercorrection in 38% and overcorrection in 8% of developmentally delayed children.8 In another study by Habot-Wilner and colleagues on the same topic with mean of 0.75 mm reduced surgical dosage and longer postoperative follow-up (5.3 ± 3years) showed successful outcome in 37.5%, undercorrection in 42%, and overcorrection in 21% of children with developmental delay. They also noted exotropic drift on long-term follow up in these patients.7 Yahalom et al. evaluated results of strabismus surgery in patients with Down syndrome and found an 87.5% success rate with standard amount of surgery.9 Ruttum and colleagues reported a 66% success rate in children with Down syndrome after surgery for esotropia.10 However, the difference in amount of surgery compared to their standard approach was not specified. Similarly, Claudio I. Perez et al and Motley et al. found that the presence of Down syndrome had no effect on success rates for bimedial recession. However, children with Down syndrome were not included in our study. Pickering and coworkers demonstrated exaggerated response and tendency towards consecutive exotropia after bimedial recession and improved outcome with conservative surgery.11,12 Similarly, a study done by Van Riju et al. showed larger correction per millimeter of recession surgery and same correction per millimeter of Recess-Resect surgery.13 It is known that esotropia is more stable than exotropia and there is tendency for exodrift in the long term. All patients in this study, both normal and developmentally delayed, were operated with planned undercorrection in the postoperative period. !

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In the present study we noted a 60% success rate with an average of 72.13% ± 16.08 of surgery in patients with developmental delay, whereas in the control group the success rate was 73.5% with an average of 89.08% ± 10.83 of surgery. When compared to standard tables, we noted 134.06% ± 51.62 response to surgery in patients with developmental delay as opposed to 89.83 ± 22.49 response in normal patients. This suggests an exaggerated response to standard doses. A higher standard deviation noted in these patients suggests variability of response. When amount of surgery was compared (Table 2) with outcome in the developmental delay group, no significant difference was found. Mean amount of surgery performed in patients with optimal outcome was 70.67 ± 17.95. The average amount of surgery performed was higher in the undercorrection group compared to the optimal correction group, suggesting unpredictability of response to strabismus surgery in this group of patients. Most studies in the past have compared bimedial recession performed in millimeters in patients with developmental delay to normal patients, in order to analyze the surgical outcome. In our study, patients with developmental delay had a mean reduction in bimedial recession of 0.35 mm compared to the normal group. However, in our study we analyzed the strabismus outcomes using the amount of surgery performed as a percentage rather than using actual millimeters of bimedial recession performed. The reasons for this are multifold. Firstly, undercorrection in millimeters would not give a linear response across the entire range of deviations. That is, 0.35 mm of undercorrection would not give the same response for 70 PD esotropia as for 30 PD esotropia. Secondly, in our study, normal patients were also planned for undercorrection. Thus standardization was necessary to compare the two groups. Thirdly, by calculating the amount of surgery, we can find the target angle to be aimed for in patients with developmental delay, which would give the optimal outcome. In conclusion, response to strabismus surgery in patients with developmental delay (excluding Down syndrome) is very unpredictable. An exaggerated response to standard amounts of bimedial recession must be anticipated while planning surgery in these patients. As such, aiming for undercorrection is more likely to give better results. Though there is no statistically significant difference, operating for a target angle of 70.6% of angle of deviation is more likely to be successful.

DECLARATION OF INTEREST The authors declare no conflict of interest.

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REFERENCES 1. World Health Organization. The global burden of disease: 2004 update. http:// www.who.int/healthinfo/global_ burden_disease/ GBD_report_2004update_part3.pdf 2. Bankes JLK. Eye defects of mentally handicapped children. Br J Ophthalmol 1974;2:533–535. 3. Seaber JH, Chandler AC. A five-year study of patients with cerebral palsy and strabismus. In: Moore S, Mein J, Stockbridge L, eds. Orthoptics: past, present, future. New York, NY: Grune and Stratton; 1976:271–277. 4. Hiles DA, Wallar PH, McFarlane F. Current concepts in the management of strabismus in children with cerebral palsy. Ann Ophthalmol 1975;7:789–798. 5. Sandfeld Nielsen L, Skov L, Jensen H. Visual dysfunctions and ocular disorders in children with developmental delay: II. Aspects of refractive errors, strabismus and contrast sensitivity. Acta Ophthalmol Scand 2007;85: 419–426. 6. Drover JR, Stager Sr DR, Morale SE, et al. Improvement in motor development following surgery for infantile esotropia. J AAPOS 2008;12:136–140. 7. Habot-Wilner Z, Spierer A, Barequet IS, Wygnanski-Jaffe T. Long-term results of esotropia surgery in children with developmental delay. J AAPOS 2012;16:32–35. 8. Habot-Wilner Z, Spierer A, Glovinsky J, Wygnanski-Jaffe T. Bilateral medial rectus muscle recession: Results in children with developmental delay compared with normally developed children. J AAPOS 2006;10:150–154.

9. Yahalom C, Mechoulam H, Cohen E, Anteby I. Strabismus surgery outcome among children and young adults with Down syndrome. J AAPOS 2010;14:117–119. 10. Ruttum MS, Kivlin JD, Hong P. Outcome of surgery for esotropia in children with Down Syndrome. Am Orthoptic J 2004;54:98–101. 11. Pickering JD, Simon JW, Lininger LL, et al. Exaggerated effect of bilateral medial rectus recession in developmentally delayed children. J Pediatr Ophthalmol Strabismus 1994;31:374–377. 12. Pickering JD, Simon JW, Ratliff CD, et al. Alignment Success following medial rectus recessions in normal and delayed children. J Pediatr Ophthalmol Strabismus 1995;32: 225–227. 13. Van Rijn LJ, Langenhorst AE, Krijnen JS, et al. Predictability of strabismus surgery in children with developmental disorders and/or psychomotor retardation. Strabismus 2009;17:117–127. 14. Perez CL, Zuazo F, Zanolli MT, et al. Esotropia surgery in children with Down syndrome. J AAPOS 2013;17: 477–479. 15. Motley W, Melson A, Gray M, Salisbury SR. Outcomes of strabismus surgery for esotropia in children with Down syndrome compared with matched controls. J Pediatr Ophthalmol Strabismus 2012;49:211–214. 16. Rosenbaum AL, Santiago AP. Surgical dose tables. In: Clinical strabismus management: Principles and surgical techniques. Philadelphia: W. B. Saunders Company, 1999. 552–554.

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Results of bilateral medial rectus recession for comitant esotropia in patients with developmental delay.

There is paucity of literature on surgical outcomes after strabismus surgery in patients with developmental delay. There is no consensus regarding whe...
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