Incidence of Strabismus and Amblyopia in Preverbal Children Previously Diagnosed with Pseudoesotropia Ariel L. Silbert Noelle S. Matta, C.O., C.R.C., C.O.T. David I. Silbert, M.D., F.A.A.P.
ABSTRACT Background and Purpose: We previously reported that 12% of children under age 3 diagnosed with pseudoesotropia without significant refractive error later developed strabismus or mild refractive amblyopia. Mohan and Sharma recently reported on fifty-one patients with pseudoesotropia and hyperopia and noted that esotropia developed in 53.9% of the children with >1.50 D of hypermetropia compared to 2.6% of those who had ≤1.50 D hypermetropia, implying a low risk of esotropia unless hyperopia was greater than 1.50 D on initial exam. We reviewed our data to see if we had similar findings in our patients. Method: Medical records between January 1, 2001, and February 26, 2010, were reviewed retrospectively. Three hundred ninety-four patients diagnosed with pseudoesotropia with an otherwise normal examination were reviewed, and 253 with follow-up were analyzed. Results: Forty-six children were 36 months or older at initial presentation; none developed strabismus; 207 children were 1.50 D; eight children (10%) later developed strabismus. One hundred twenty-nine children had hyperopia ≤ 1.50 D, and fourteen (11%) developed strabismus. Our analysis showed an equal risk of strabismus developing in pseudoesotropia patients under age 3 with greater or less than 1.50 D of hyperopia. Conclusion: There is a significant risk of esotropia developing in children under three diagnosed with pseudoesotropia. Hyperopia less than 1.50 D, does not obviate the need for careful follow-up.
INTRODUCTION In 2012, we published our findings on the incidence of strabismus and amblyopia
in preverbal children previously diagnosed with pseudoesotropia.1 A series of 306 patients diagnosed with pseuodoesotropia without any significant refractive error on
From the Family Eye Group, Lancaster, Pennsylvania. Requests for reprints should be addressed to: Noelle S. Matta, C.O., C.R.C., Family Eye Group, 2110 Harrisburg Pike, Suite 215, Lancaster, PA 17601; e-mail: [email protected] © 2013 Board of Regents of the University of Wisconsin System, American Orthoptic Journal, Volume 63, 2013, ISSN 0065-955X, E-ISSN 1553-4448
American Orthoptic Journal
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their initial examination by the American Association for Pediatric Ophthalmology and Strabimsus (AAPOS) referral criteria were evaluated.2 Two hundred and one patients had a follow-up examination as had been recommended. Of these, 10% were later found to have strabismus, and an additional 2% were found to have refractive amblyopia. Roh and Choi evaluated 734 children with strabismus and noted that 102 (13%) had a previous diagnosis of pseudostrabismus. 3 Pritchard and Ellis reviewed 268 medical records and had follow-up on eighty-three patients with a previous history of pseudoesotropia.4 They noted that 12% were later found to have strabismus. Research subsequent to our publication by Anwar and Repka showed that 19.4% of thirty one children previously diagnosed with pseudoesotropia later developed esotropia.5 Most recently, Mohan and Sharma reviewed the records of fifty-one children who had been diagnosed with pseudoesotropia and met their inclusion criteria.6 They noted that refractive accommodative esotropia developed in eight (15.7%) of the children. More interestingly, they noted that 53.9% of the children who had greater than 1.50 D of hypermetropia developed strabismus (7 of 13 children), while only 2.6% of those who had less than or equal to 1.50 D of hypermetropia developed esotropia (1 out of 38 children). They concluded that if children had a diagnosis of pseudoesotropia at less than 3 years of age and had greater than 1.50 D of hypermetropia at initial examination, then they had a high risk for developing esotropia, while implying that those children with less than or equal to 1.50 D were at a low risk for developing later esotropia. We found this to be an interesting association because if shown to be correct, it could simplify follow-up for young children diagnosed with pseudoesotropia. Therefore, we decided to test this hypothesis on
104
our much larger patient data set of children diagnosed with pseudoesotropia. PATIENTS AND METHODS Institutional review board approval for this study was granted by Lancaster General Hospital. Parent/ guardian consent was waived. The study adhered to guidelines of the Health Insurance Portability and Accountability Act of 1996. The records of all children diagnosed with pseudoesotropia without regard to age and seen by one pediatric ophthalmologist (DS) between January 1, 2001, and February 26, 2010, were reviewed retrospectively. Patient records were identified based on Current Procedural Terminology (CPT) coding for esotropia. Family history of strabismus or lack of strabismus was not used as an inclusion criteria. Patients without follow-up were excluded from the analysis. The group was stratified according to age: less than 36 months and greater than or equal to 36 months. It was also stratified by initial refraction: greater than 1.50 D in at least one eye and less than or equal to 1.50 D in both eyes. All patients received a comprehensive ophthalmological examination including cycloplegic refraction with cyclopentolate 1% on the first visit. All patients were recommended to have follow-up in 6 months and again after age 3 years (for the younger children) to rule out development of manifest strabismus. Of the 1,249 charts coded for esotropia that were individually reviewed, 394 were diagnosed with pseudoesotropia on their first visit. Twenty-nine of these patients were found to have significant refractive error based on the current AAPOS referral criteria2 and normal alignment. The 2003 AAPOS referral criteria were developed to provide standards as to which children should be referred for vision screening and are as follows:
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• anisometropia (spherical or cylindrical) > 1.5 D • any manifest strabismus • hyperopia > 3.5 D in any meridian • myopia magnitude > 3.0 D in any meridian • any media opacity > 1 mm in size • astigmatism > 1.5 D at 90° or 180° > 1.0 D in the oblique axis ("10° eccentric to 90° or 180°) • ptosis ≤ 1 mm margin reflex distance • visual acuity per age- appropriate standards Of the 394 patients identified, 253 had follow-up (64%). Patients without follow-up were excluded from the analysis. The patients were then divided into two groups: age less than 36 months and greater than or equal to 36 months. RESULTS Of the 253 children analyzed, 207 were under the age of 36 months (82%) and forty-six were age 36 months or older (18%). Looking at children under the age of 36 months, seventy-eight (38%) had refractive error greater than 1.50 D in one eye. Eight of these 78 patients (10%) later developed strabismus. Four of the 8 required surgery for their esotropia, while four had accommodative esotropia corrected by glasses. There were 129 children under the age of 36 months with refractive error less than or equal to 1.50 D. Fourteen of these 129 patients (11%) developed strabismus. Three developed esotropia requiring surgery. One had a microesotropia and amblyopia, but did not require surgery. Two developed an accommodative esotropia correctable with glasses. Six developed exotropia: three required surgery and three had intermittent exotropia. One child had Duane syndrome, and one child later had surgery for primary inferior oblique over-action.
American Orthoptic Journal
There were forty-six children age 36 months or older diagnosed with pseudoesotropia. Of these children, none later developed strabismus on follow-up. For the children under 36 months of age, the average age at presentation was 12 months (range 2-33 months). The average age for these children at follow-up was 34 months (range 4-120 months). For children 36 months or older, the average age at presentation was 62 months (range 36-154 months). The average age for these children at follow-up was 84 months (range 43-160 months). DISCUSSION In our study, the incidence of strabismus found in children diagnosed with pseudoesotropia under 36 months of age was 11%. When stratified by refractive error, 10% of children under 36 months of age with greater than 1.50 D of hypermetropia in one eye and 11% of children under 36 months of age with less than or equal to 1.50 D of hypermetropia developed strabismus. Our data set shows a nearly equal risk of developing strabismus in children under 36 months of age whether or not those children have greater than or less than 1.50 D of hypermetropia. This seems to disprove Mohan and Sharma’s hypothesis.6 When looking at Mohan’s and Sharma’s data set, 6 of 8 patients who developed strabismus had greater than or equal to 4.0 D of hypermetropia. In our original paper, we would have excluded those patients from analysis since they were classified as high risk by AAPOS referral criteria and would have been assumed to be at high risk for developing esotropia. If these six patients are excluded, there are only two patients in Mohan’s and Sharma’s data set who developed strabismus. One out of 6 patients (17%) with greater than 1.50 D but less than 4.0 D of hypermetropia developed strabismus, and we see that 1 out of 38 (3%) patients with less
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than or equal to 1.50 D of hypermetropia developed strabismus Mohan and Sharma’s cohort is very small, which may be due to unnecessary exclusions of patients. Their criteria excluded patients who did not have verifiable positive or negative history of strabismus, even though family history was not found to be a statistically significant predictor in their study or in Pritchard and Ellis’s study.4 Mohan and Sharma also required a refraction with atropine sulfate 1% and an ocular alignment assessment with and without refractive correction at follow-up visits for inclusion in their study. This may have further limited their numbers. The inclusion criteria of their study may have inadvertently introduced many biases. A fresh look at the entire data set of all patients diagnosed with pseudoesotropia without these exclusions might provide Mohan and Sharma with a much larger data set and eliminate various biases that may have limited the accuracy of their results. CONCLUSION Our study confirms that children diagnosed with pseudoesotropia under age 36 months have a higher risk than in the general population of developing strabismus regardless of their refractive status. Children 36 months and older diagnosed with pseudoesotropia seem to
106
be unlikely to develop strabismus later, although our numbers for this group are smaller than for the younger group, and thus we cannot say that there is no risk of strabismus developing. Children diagnosed with pseudoesotropia under age 3 should have careful monitoring to make sure that they do not later develop strabismus or amblyopia. REFERENCES 1. Silbert AL, Matta NS, Silbert DI: Incidence of strabismus and amblyopia in preverbal children previously diagnosed with pseudoesotropia. J AAPOS 2012; 16:118-119. 2. Donahue SP, et al.: Preschool vision screening: what should we be detecting and how should we report it? Uniform guidelines for reporting results of preschool vision screening studies. J AAPOS 2003; 7:314-316. 3. Roh IH, Choi MY: Clinical characteristics of strabismus in children with a history of pseudoesotropia. J Korean Ophthalmol Soc 2006; 47:1449-1453. 4. Pritchard C, Ellis GS Jr: Manifest strabismus following pseudostrabismus diagnosis. Am Orthopt J 2007; 57:111-117. 5. Anwar DS, et al.: Incidence of esotropia developing in subjects previously diagnosed with pseudoesotropia: A pilot study. Strabismus 2012; 20:124-126. 6. Mohan K, Sharma A: Development of refractive accommodative esotropia in children initially diagnosed with pseudoesotropia. J AAPOS 2012; 16:266-268.
Key words: pseudoesotropia, esotropia, refractive error, amblyopia
Volume 63, 2013
ABSTRACT Background and Purpose: We previously reported that 12% of children under age 3 diagnosed with pseudoesotropia without significant refractive error later developed strabismus or mild refractive amblyopia. Mohan and Sharma recently reported on fifty-one patients with pseudoesotropia and hyperopia and noted that esotropia developed in 53.9% of the children with >1.50 D of hypermetropia compared to 2.6% of those who had ≤1.50 D hypermetropia, implying a low risk of esotropia unless hyperopia was greater than 1.50 D on initial exam. We reviewed our data to see if we had similar findings in our patients. Method: Medical records between January 1, 2001, and February 26, 2010, were reviewed retrospectively. Three hundred ninety-four patients diagnosed with pseudoesotropia with an otherwise normal examination were reviewed, and 253 with follow-up were analyzed. Results: Forty-six children were 36 months or older at initial presentation; none developed strabismus; 207 children were 1.50 D; eight children (10%) later developed strabismus. One hundred twenty-nine children had hyperopia ≤ 1.50 D, and fourteen (11%) developed strabismus. Our analysis showed an equal risk of strabismus developing in pseudoesotropia patients under age 3 with greater or less than 1.50 D of hyperopia. Conclusion: There is a significant risk of esotropia developing in children under three diagnosed with pseudoesotropia. Hyperopia less than 1.50 D, does not obviate the need for careful follow-up.
INTRODUCTION In 2012, we published our findings on the incidence of strabismus and amblyopia
in preverbal children previously diagnosed with pseudoesotropia.1 A series of 306 patients diagnosed with pseuodoesotropia without any significant refractive error on
From the Family Eye Group, Lancaster, Pennsylvania. Requests for reprints should be addressed to: Noelle S. Matta, C.O., C.R.C., Family Eye Group, 2110 Harrisburg Pike, Suite 215, Lancaster, PA 17601; e-mail: [email protected] © 2013 Board of Regents of the University of Wisconsin System, American Orthoptic Journal, Volume 63, 2013, ISSN 0065-955X, E-ISSN 1553-4448
American Orthoptic Journal
103
PSEUDOESOTROPIA
their initial examination by the American Association for Pediatric Ophthalmology and Strabimsus (AAPOS) referral criteria were evaluated.2 Two hundred and one patients had a follow-up examination as had been recommended. Of these, 10% were later found to have strabismus, and an additional 2% were found to have refractive amblyopia. Roh and Choi evaluated 734 children with strabismus and noted that 102 (13%) had a previous diagnosis of pseudostrabismus. 3 Pritchard and Ellis reviewed 268 medical records and had follow-up on eighty-three patients with a previous history of pseudoesotropia.4 They noted that 12% were later found to have strabismus. Research subsequent to our publication by Anwar and Repka showed that 19.4% of thirty one children previously diagnosed with pseudoesotropia later developed esotropia.5 Most recently, Mohan and Sharma reviewed the records of fifty-one children who had been diagnosed with pseudoesotropia and met their inclusion criteria.6 They noted that refractive accommodative esotropia developed in eight (15.7%) of the children. More interestingly, they noted that 53.9% of the children who had greater than 1.50 D of hypermetropia developed strabismus (7 of 13 children), while only 2.6% of those who had less than or equal to 1.50 D of hypermetropia developed esotropia (1 out of 38 children). They concluded that if children had a diagnosis of pseudoesotropia at less than 3 years of age and had greater than 1.50 D of hypermetropia at initial examination, then they had a high risk for developing esotropia, while implying that those children with less than or equal to 1.50 D were at a low risk for developing later esotropia. We found this to be an interesting association because if shown to be correct, it could simplify follow-up for young children diagnosed with pseudoesotropia. Therefore, we decided to test this hypothesis on
104
our much larger patient data set of children diagnosed with pseudoesotropia. PATIENTS AND METHODS Institutional review board approval for this study was granted by Lancaster General Hospital. Parent/ guardian consent was waived. The study adhered to guidelines of the Health Insurance Portability and Accountability Act of 1996. The records of all children diagnosed with pseudoesotropia without regard to age and seen by one pediatric ophthalmologist (DS) between January 1, 2001, and February 26, 2010, were reviewed retrospectively. Patient records were identified based on Current Procedural Terminology (CPT) coding for esotropia. Family history of strabismus or lack of strabismus was not used as an inclusion criteria. Patients without follow-up were excluded from the analysis. The group was stratified according to age: less than 36 months and greater than or equal to 36 months. It was also stratified by initial refraction: greater than 1.50 D in at least one eye and less than or equal to 1.50 D in both eyes. All patients received a comprehensive ophthalmological examination including cycloplegic refraction with cyclopentolate 1% on the first visit. All patients were recommended to have follow-up in 6 months and again after age 3 years (for the younger children) to rule out development of manifest strabismus. Of the 1,249 charts coded for esotropia that were individually reviewed, 394 were diagnosed with pseudoesotropia on their first visit. Twenty-nine of these patients were found to have significant refractive error based on the current AAPOS referral criteria2 and normal alignment. The 2003 AAPOS referral criteria were developed to provide standards as to which children should be referred for vision screening and are as follows:
Volume 63, 2013
SILBERT
• anisometropia (spherical or cylindrical) > 1.5 D • any manifest strabismus • hyperopia > 3.5 D in any meridian • myopia magnitude > 3.0 D in any meridian • any media opacity > 1 mm in size • astigmatism > 1.5 D at 90° or 180° > 1.0 D in the oblique axis ("10° eccentric to 90° or 180°) • ptosis ≤ 1 mm margin reflex distance • visual acuity per age- appropriate standards Of the 394 patients identified, 253 had follow-up (64%). Patients without follow-up were excluded from the analysis. The patients were then divided into two groups: age less than 36 months and greater than or equal to 36 months. RESULTS Of the 253 children analyzed, 207 were under the age of 36 months (82%) and forty-six were age 36 months or older (18%). Looking at children under the age of 36 months, seventy-eight (38%) had refractive error greater than 1.50 D in one eye. Eight of these 78 patients (10%) later developed strabismus. Four of the 8 required surgery for their esotropia, while four had accommodative esotropia corrected by glasses. There were 129 children under the age of 36 months with refractive error less than or equal to 1.50 D. Fourteen of these 129 patients (11%) developed strabismus. Three developed esotropia requiring surgery. One had a microesotropia and amblyopia, but did not require surgery. Two developed an accommodative esotropia correctable with glasses. Six developed exotropia: three required surgery and three had intermittent exotropia. One child had Duane syndrome, and one child later had surgery for primary inferior oblique over-action.
American Orthoptic Journal
There were forty-six children age 36 months or older diagnosed with pseudoesotropia. Of these children, none later developed strabismus on follow-up. For the children under 36 months of age, the average age at presentation was 12 months (range 2-33 months). The average age for these children at follow-up was 34 months (range 4-120 months). For children 36 months or older, the average age at presentation was 62 months (range 36-154 months). The average age for these children at follow-up was 84 months (range 43-160 months). DISCUSSION In our study, the incidence of strabismus found in children diagnosed with pseudoesotropia under 36 months of age was 11%. When stratified by refractive error, 10% of children under 36 months of age with greater than 1.50 D of hypermetropia in one eye and 11% of children under 36 months of age with less than or equal to 1.50 D of hypermetropia developed strabismus. Our data set shows a nearly equal risk of developing strabismus in children under 36 months of age whether or not those children have greater than or less than 1.50 D of hypermetropia. This seems to disprove Mohan and Sharma’s hypothesis.6 When looking at Mohan’s and Sharma’s data set, 6 of 8 patients who developed strabismus had greater than or equal to 4.0 D of hypermetropia. In our original paper, we would have excluded those patients from analysis since they were classified as high risk by AAPOS referral criteria and would have been assumed to be at high risk for developing esotropia. If these six patients are excluded, there are only two patients in Mohan’s and Sharma’s data set who developed strabismus. One out of 6 patients (17%) with greater than 1.50 D but less than 4.0 D of hypermetropia developed strabismus, and we see that 1 out of 38 (3%) patients with less
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than or equal to 1.50 D of hypermetropia developed strabismus Mohan and Sharma’s cohort is very small, which may be due to unnecessary exclusions of patients. Their criteria excluded patients who did not have verifiable positive or negative history of strabismus, even though family history was not found to be a statistically significant predictor in their study or in Pritchard and Ellis’s study.4 Mohan and Sharma also required a refraction with atropine sulfate 1% and an ocular alignment assessment with and without refractive correction at follow-up visits for inclusion in their study. This may have further limited their numbers. The inclusion criteria of their study may have inadvertently introduced many biases. A fresh look at the entire data set of all patients diagnosed with pseudoesotropia without these exclusions might provide Mohan and Sharma with a much larger data set and eliminate various biases that may have limited the accuracy of their results. CONCLUSION Our study confirms that children diagnosed with pseudoesotropia under age 36 months have a higher risk than in the general population of developing strabismus regardless of their refractive status. Children 36 months and older diagnosed with pseudoesotropia seem to
106
be unlikely to develop strabismus later, although our numbers for this group are smaller than for the younger group, and thus we cannot say that there is no risk of strabismus developing. Children diagnosed with pseudoesotropia under age 3 should have careful monitoring to make sure that they do not later develop strabismus or amblyopia. REFERENCES 1. Silbert AL, Matta NS, Silbert DI: Incidence of strabismus and amblyopia in preverbal children previously diagnosed with pseudoesotropia. J AAPOS 2012; 16:118-119. 2. Donahue SP, et al.: Preschool vision screening: what should we be detecting and how should we report it? Uniform guidelines for reporting results of preschool vision screening studies. J AAPOS 2003; 7:314-316. 3. Roh IH, Choi MY: Clinical characteristics of strabismus in children with a history of pseudoesotropia. J Korean Ophthalmol Soc 2006; 47:1449-1453. 4. Pritchard C, Ellis GS Jr: Manifest strabismus following pseudostrabismus diagnosis. Am Orthopt J 2007; 57:111-117. 5. Anwar DS, et al.: Incidence of esotropia developing in subjects previously diagnosed with pseudoesotropia: A pilot study. Strabismus 2012; 20:124-126. 6. Mohan K, Sharma A: Development of refractive accommodative esotropia in children initially diagnosed with pseudoesotropia. J AAPOS 2012; 16:266-268.
Key words: pseudoesotropia, esotropia, refractive error, amblyopia
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