J Autism Dev Disord DOI 10.1007/s10803-015-2428-3
ORIGINAL PAPER
Initial Ophthalmic Findings in Turkish Children with Autism Spectrum Disorder Emrah Utku Kabatas1 • Pinar Altiaylik Ozer1 • Gokce Tasdemir Ertugrul1 Bengi Ece Kurtul1 • Sahin Bodur2 • Burcu Ersoz Alan2,3
•
Ó Springer Science+Business Media New York 2015
Abstract Children with autism spectrum disorders (ASD) frequently have ophthalmologic disorders. Due to poor cooperation with ophthalmological examination, ocular abnormalities in such children may be overlooked. We retrospectively studied the records of 324 patients diagnosed as ASD that underwent ophthalmological examination between January 2011 and November 2014 at Dr. Sami Ulus Maternity and Children Research and Training Hospital, Ankara, Turkey. Ophthalmic pathology was noted in 26.9 % of patients with ASD, of which 22 % had significant refractive errors and 8.6 % had strabismus. Comprehensive eye examination by a pediatric
& Emrah Utku Kabatas [email protected] Pinar Altiaylik Ozer [email protected] Gokce Tasdemir Ertugrul [email protected] Bengi Ece Kurtul [email protected] Sahin Bodur [email protected] Burcu Ersoz Alan [email protected] 1
Department of Ophthalmology, Ministry of Health, Dr. Sami Ulus Maternity and Children Research and Training Hospital, Babur Caddesi, Altindag, 06080 Ankara, Turkey
2
Department of Child Psychiatry, Ministry of Health, Dr. Sami Ulus Maternity and Children Research and Training Hospital, Babur Caddesi, Altindag, 06080 Ankara, Turkey
3
Department of Child Psychiatry, Kirikkale University Faculty of Medicine, 71450 Kirikkale, Turkey
ophthalmologist is recommended for all children diagnosed as ASD. Keywords Autism Strabismus Refractive errors Ophthalmologic disorders
Introduction Autism spectrum disorder (ASD) is a neuropsychiatric disorder characterized by repetitive patterns of behavior and persistent deficit in social communication. ASD is diagnosed more commonly in males than in females. The etiology of ASD is not precisely known, but many environmental and genetic factors, such as fragile X syndrome, tuberous sclerosis, congenital rubella, phenylketonuria, and intrauterine valproate exposure, are associated with ASD (Centers for Disease Control and Prevention 2008). A recent study reported that the narrow-sense heritability of autism is 52.4 %, which is thought to be associated with common genetic variants or their interactions with environmental factors (Gaugler et al. 2014). The role of toxic chemical exposure in the development of autism is currently the focus of much research. Plasticizers such as bisphenol A (BPA) and some air-pollutants rich in BPA were reported in some studies as possible causative factors, which are the subjects of further investigation (Stein et al. 2015). The literature contains limited data on ophthalmological evaluation in children with ASD. Ikeda et al. (2013) reported that 40 % of children with autism or a related disorder had an ophthalmic disorder, most commonly a significant refractive error, strabismus, or amblyopia. Due to poor cooperation with ophthalmological examination, ocular abnormalities in children with ASD may be
123
J Autism Dev Disord
overlooked, which can negatively affect their already impaired social and communication skills. The present study aimed to determine the prevalence of ophthalmic abnormalities in Turkish children at the time of diagnosis of ASD, and to highlight the importance of ophthalmological evaluation in children with ASD.
Materials and Methods This retrospective study included patients diagnosed as ASD that presented to the ophthalmology clinic at Dr. Sami Ulus Maternity and Children Research and Training Hospital, Ankara, Turkey, between January 2011 and November 2014. The Dr. Sami Ulus Maternity and Children Research and Training Hospital Ethics Committee approved the study protocol, which was carried out in accordance with the tenets of the Declaration of Helsinki. Data were obtained from the patients’ records, including age, gender, general medical and ocular history, and ophthalmological findings. Visual acuity test results, detection of significant refractive errors following cycloplegia, and ocular alignment findings based on cover-uncover, alternate cover, and Hirschberg testing were recorded for each patient. Ophthalmological examination was performed by an ophthalmologist accompanied by a parent in a quiet room. Snellen or HOTV testing was used to determine visual acuity in cooperative children. We noted that pictures were more acceptable to the children that could not as yet read, as they were able to read a row of pictures rather than matching unfamiliar letters. The Kay Picture Test is popular in Europe; based on the logMAR principle, children are shown some familiar pictures in a linear and crowded format. It is now considered comparable to the classical logMAR or Snellen letter testing (Elliott and Firth 2009). The Kay Picture Test or LEA symbols were used to assess visual acuity in children that were uncooperative with the Snellen or HOTV tests. Some patients did not cooperate with any type of acuity testing and visual acuity was measured using preferential looking tests. Anterior segment evaluation via slit-lamp biomicroscopy, cycloplegic retinoscopy, and fundus examination following dilation of the pupils with cyclopentolate 1 % were also performed. The refractive status of each patient was assessed using a hand-held automated refractometer (SureSightTM autorefractor, Welch Allyn), which has lights and sounds that help to focus a child’s attention. Recently revised American Association for Pediatric Ophthalmology and Strabismus (AAPOS) referral criteria were used to define significant refractive errors (Donahue et al. 2012) (Table 1). Data entry and analysis were performed using
123
Statistical Package for the Social Sciences for Windows version, 17.0 (SPSS, Inc., Chicago IL, USA).
Results In all, the records of 324 patients diagnosed as ASD were reviewed. Among these patients, 267 were male (82 %) and 57 were female (18 %). Mean age of the patients at the time of ASD diagnosis was 5 years (18 months–17 years). Visual acuity testing could be performed in 29 patients (9 %), whereas 295 (91 %) did not cooperate with any kind of acuity testing. Automated refractions following cycloplegia were completed in every patient. The patients’ refractive errors according to AAPOS criteria are given in Table 2. Spherical values were between -3.50 D and ?6.00 D. All astigmatism values were recorded in plus cylinder; cylindrical values were between ?0.50 D and ?3.00 D. In total, 28 (8.6 %) patients had strabismus, of which 14 had an exodeviation (50 %), 13 had an esodeviation (46.4 %), and 1 had a hyperdeviation (3.6 %). List of the patients with other ophthalmic problems is given in Table 3. Associated systemic abnormalities were noted in 14.9 % of the patients (Table 4).
Discussion Autism is a disorder of the central nervous system that significantly impairs social interactions of the child. Associated systemic abnormalities may be observed in autistic children, some of which can contribute to deficient communication skills. Ocular abnormalities such as uncorrected refractive errors in children with autism might negatively affect social communication, and due to the challenges of ophthalmological examination in such patients correctable refractive errors may be overlooked. Uncorrected refractive errors and strabismus can lead to severe amblyopia, which parents may not detect. Comprehensive ophthalmological examination may facilitate early diagnosis. Ikeda et al. (2013) reported that 40 % of children with ASD had some type of identifiable ophthalmic problem, most commonly significant refractive error, followed by strabismus, and amblyopia. They also reported that refractive errors were identified in 29 % of patients. In autistic children ophthalmic problems were reported in 33.3 % of patients (Ezegwui et al. 2014), in 27 % (Black et al. 2013), and in 68 % (Singman et al. 2013). In the present study, 26.9 % of the autistic patients had an ocular problem, 22.5 % had a significant refractive error, and 8.6 % had strabismus. Hypermetropia was the most
J Autism Dev Disord Table 1 AAPOS criteria for amblyopia and significant refractive errors
Age (months)
Astigmatism (D)
Hypermetropia (D)
Anisometropia (D)
Myopia (D)
12–30
[2.00
[4.50
[2.50
[-3.50
31–48
[2.00
[4.00
[2.00
[-3.00
[48
[1.50
[3.50
[1.50
[-1.50
Additional criteria for the definition of ambliyopia for all children are: Manifest strabismus [8 prism diopters in primary position, Media opacity [1 mm D Diopters
Table 2 Refractive errors in the patients with ASD Type of refractive error
Cases (n)
Emmetropia
251
Hypermetropia
Percent 77.5
27
8.3
6
1.9
Myopia Simple hypermetropic astigmatism
13
4
Simple myopic astigmatism
11
3.4
Compound hypermetropic astigmatism
8
2.5
Compound myopic astigmatism
5
1.5
Mixed astigmatism Anisometropia
1 2
0.3 0.6
Total
324
100
Table 3 Other ocular problems observed in the patients with ASD Ocular disorder
Cases (n)
Percent
Unilateral ptosis
4
1.2
Cataract
2
0.6
Nystagmus
1
0.3
Phthisis bulbi due to retinopathy of prematurity
1
0.3
Table 4 Systemic abnormalities observed in the patients with ASD Associated systemic abnormality
Cases (n)
Percent
Mental retardation
16
4.9
Epilepsy
9
2.8
Cerebral palsy
5
1.5
Congenital sensorineural hearing loss
5
1.5
Hypotonia
4
1.2
Microcephaly
3
0.9
Auricular atresia
2
0.6
Ventricular septal defect
2
0.6
Down syndrome
2
0.6
Di-George syndrome
1
0.3
common refractive error in the present study, as in the study by Ikeda et al. (2013), whereas in contrast, 8.6 % of the present study’s patients had strabismus, versus 21 % as
reported by Ikeda et al. (2013). This difference might be due to differences in ethnicity and multifactorial insults affecting the prevalence of strabismus between the 2 studies’ populations (Cotter et al. 2011). Visual acuity assessment may be the most challenging part of ophthalmic evaluation in children with autism. Ikeda et al. (2013) reported a cooperation rate of 40 % among 154 patients, whereas Ezegwui et al. (2014) reported a cooperation rate of 11.1 % among 18 patients. Differences between the studies might be due to differences in mean age and the severity of autism between study populations. In the present study 9 % of patients cooperated with visual acuity testing, which is in contrast to 88–100 % reported by Coulter et al. (2015) for an eye examination protocol that included tests of visual acuity, refraction, convergence (eye teaming), stereoacuity (depth perception), ocular motility, and ocular health in ASD patients. Their study included children and adolescents aged 9–17 years of age, whereas mean age in the present study was 5 years. The present study was based on initial ophthalmological findings in patients at the time ASD was diagnosed—a protocol unique to the present study. None of the present study’s patients had yet received treatment or rehabilitation for autism; as such, they were all considered as having severe ASD, and assessment of visual acuity was not possible. Despite the low rate of cooperation with recognition acuity testing in the present study, refractive status was assessed in all the patients. Hand held, non-contact automated refractometers might help ophthalmologists examine autistic children and facilitate assessment of refractive status. Classical retinoscopy may be difficult to perform in children with autism due to attention deficit and poor cooperation. In the present study a hand-held pediatric automated refractometer was used, which has spinning lights to focus attention when performing measurements. These lights can focus the attention of ASD patients because they are often interested in stereotypic movements and turning objects. The non-contact nature of the device is also helpful in children that refuse any type of eye contact during examination. In the present study 324 patients with ASD were screened for ocular problems; to the best of our knowledge the present study is, to date, the largest of its kind.
123
J Autism Dev Disord
In all, 14.9 % of the present study’s patients had associated systemic abnormalities, including mental retardation, followed by epilepsy, cerebral palsy, sensorineural hearing loss, hypotonia, microcephaly, auricular atresia, ventricular septal defect, Down syndrome, and Di-George syndrome. Associated systemic abnormalities in ASD patients have been reported in only a few other studies. Mental retardation was observed in 18 % of ASD patients in Ikeda et al.’s (2013) study and McCabe et al. (2013) reported an association between 22q-11 deletion and ASD. As reported by Ikeda et al. (2013), male predominance among the ASD patients (78 %) was observed in the present study. In conclusion, the present findings highlight the importance of ophthalmological examination in children with ASD, because of the strong association between refractive errors and amblyopia. For ophthalmological examination hand-held, non-contact automated refractometers with spinning lights can facilitate examination in children with autism. Parents and primary care physicians should be made aware of the importance and possibility of ophthalmic evaluation in these children. Larger scale prospective studies are needed to further investigate the prevalence of ophthalmic disorders in children with ASD and to determine the impact that treating such disorders. Conflict of interest The authors declare there are no conflicts of interest—financial or otherwise—related to the materials presented herein.
References Black, K., McCarus, C., Collins, M. L., & Jensen, A. (2013). Ocular manifestations of autism in ophthalmology. Strabismus, 21(2), 98–102.
123
Centers for Disease Control and Prevention. (2008). Prevalence of autism spectrum disorders—Autism and Developmental Disabilities Monitoring Network, fourteen sites, United States. MMWR 2012a; 61(No. SS03):1–19. http://www.cdc.gov/mmwr/ pdf/ss/ss6103.pdf. Cotter, S. A., Varma, R., Tarczy-Hornoch, K., McKean-Cowdin, R., Lin, J., Wen, G., et al. (2011). Risk factors associated with childhood strabismus: The multi-ethnic pediatric eye disease and Baltimore pediatric eye disease studies. Ophthalmology, 118(11), 2251–2261. Coulter, R. A., Bade, A., Tea, Y., Fecho, G., Amster, D., Jenewein, E., et al. (2015). Eye examination testability in children with autism and in typical peers. Optometry and Vision Science, 92(1), 31–43. doi:10.1097/OPX.0000000000000442. Donahue, S. P., Arnold, R., Ruben, J., Silbert, D., Arthur, B., & Neely, D. (2012). Revised guidelines for reporting results from studies of preschool vision screening. JAAPOS, 16(1), e4. doi:10.1016/j.jaapos.2011.12.016. Elliott, M. C., & Firth, A. Y. (2009). The logMAR Kay picture test and the logMAR acuity test: A comparative study. Eye (Lond), 23(1), 85–88. Ezegwui, I. R., Lawrence, L., Aghaji, A. E., Okoye, O. I., Okoye, O., Onwasigwe, E. N., et al. (2014). Refractive errors in children with autism in a developing country. Nigerian journal of clinical practice, 17(4), 467–470. Gaugler, T., Klei, L., Sanders, J. S., Bodea, C. A., Goldberg, A. P., Lee, A. B., et al. (2014). Most genetic risk for autism resides with common variation. Nature Genetics, 46, 881–885. Ikeda, J., Davitt, B. V., Ultmann, M., Maxim, R., & Cruz, O. A. (2013). Brief report: Incidence of ophthalmologic disorders in children with autism. Journal of Autism and Developmental Disorders, 43, 1447–1451. McCabe, K. L., Melville, J. L., Rich, D., Strutt, P. A., Cooper, G., Loughland, C. M., et al. (2013). Divergent patterns of social cognition performance in autism and 22q11.2 deletion syndrome (22q11DS). Journal of Autism and Developmental Disorders, 43, 1926–1934. Singman, E., Matta, N., Fairward, A., & Silbert, D. (2013). Evaluation of plusoptiX photoscreening during examinations of children with autism. Strabismus, 21(2), 103–105. Stein, T. P., Schluter, M. D., Steer, R. A., Guo, L., & Ming, X. (2015). Bisphenol a exposure in children with autism spectrum disorders. Autism Research,. doi:10.1002/aur.1444.
ORIGINAL PAPER
Initial Ophthalmic Findings in Turkish Children with Autism Spectrum Disorder Emrah Utku Kabatas1 • Pinar Altiaylik Ozer1 • Gokce Tasdemir Ertugrul1 Bengi Ece Kurtul1 • Sahin Bodur2 • Burcu Ersoz Alan2,3
•
Ó Springer Science+Business Media New York 2015
Abstract Children with autism spectrum disorders (ASD) frequently have ophthalmologic disorders. Due to poor cooperation with ophthalmological examination, ocular abnormalities in such children may be overlooked. We retrospectively studied the records of 324 patients diagnosed as ASD that underwent ophthalmological examination between January 2011 and November 2014 at Dr. Sami Ulus Maternity and Children Research and Training Hospital, Ankara, Turkey. Ophthalmic pathology was noted in 26.9 % of patients with ASD, of which 22 % had significant refractive errors and 8.6 % had strabismus. Comprehensive eye examination by a pediatric
& Emrah Utku Kabatas [email protected] Pinar Altiaylik Ozer [email protected] Gokce Tasdemir Ertugrul [email protected] Bengi Ece Kurtul [email protected] Sahin Bodur [email protected] Burcu Ersoz Alan [email protected] 1
Department of Ophthalmology, Ministry of Health, Dr. Sami Ulus Maternity and Children Research and Training Hospital, Babur Caddesi, Altindag, 06080 Ankara, Turkey
2
Department of Child Psychiatry, Ministry of Health, Dr. Sami Ulus Maternity and Children Research and Training Hospital, Babur Caddesi, Altindag, 06080 Ankara, Turkey
3
Department of Child Psychiatry, Kirikkale University Faculty of Medicine, 71450 Kirikkale, Turkey
ophthalmologist is recommended for all children diagnosed as ASD. Keywords Autism Strabismus Refractive errors Ophthalmologic disorders
Introduction Autism spectrum disorder (ASD) is a neuropsychiatric disorder characterized by repetitive patterns of behavior and persistent deficit in social communication. ASD is diagnosed more commonly in males than in females. The etiology of ASD is not precisely known, but many environmental and genetic factors, such as fragile X syndrome, tuberous sclerosis, congenital rubella, phenylketonuria, and intrauterine valproate exposure, are associated with ASD (Centers for Disease Control and Prevention 2008). A recent study reported that the narrow-sense heritability of autism is 52.4 %, which is thought to be associated with common genetic variants or their interactions with environmental factors (Gaugler et al. 2014). The role of toxic chemical exposure in the development of autism is currently the focus of much research. Plasticizers such as bisphenol A (BPA) and some air-pollutants rich in BPA were reported in some studies as possible causative factors, which are the subjects of further investigation (Stein et al. 2015). The literature contains limited data on ophthalmological evaluation in children with ASD. Ikeda et al. (2013) reported that 40 % of children with autism or a related disorder had an ophthalmic disorder, most commonly a significant refractive error, strabismus, or amblyopia. Due to poor cooperation with ophthalmological examination, ocular abnormalities in children with ASD may be
123
J Autism Dev Disord
overlooked, which can negatively affect their already impaired social and communication skills. The present study aimed to determine the prevalence of ophthalmic abnormalities in Turkish children at the time of diagnosis of ASD, and to highlight the importance of ophthalmological evaluation in children with ASD.
Materials and Methods This retrospective study included patients diagnosed as ASD that presented to the ophthalmology clinic at Dr. Sami Ulus Maternity and Children Research and Training Hospital, Ankara, Turkey, between January 2011 and November 2014. The Dr. Sami Ulus Maternity and Children Research and Training Hospital Ethics Committee approved the study protocol, which was carried out in accordance with the tenets of the Declaration of Helsinki. Data were obtained from the patients’ records, including age, gender, general medical and ocular history, and ophthalmological findings. Visual acuity test results, detection of significant refractive errors following cycloplegia, and ocular alignment findings based on cover-uncover, alternate cover, and Hirschberg testing were recorded for each patient. Ophthalmological examination was performed by an ophthalmologist accompanied by a parent in a quiet room. Snellen or HOTV testing was used to determine visual acuity in cooperative children. We noted that pictures were more acceptable to the children that could not as yet read, as they were able to read a row of pictures rather than matching unfamiliar letters. The Kay Picture Test is popular in Europe; based on the logMAR principle, children are shown some familiar pictures in a linear and crowded format. It is now considered comparable to the classical logMAR or Snellen letter testing (Elliott and Firth 2009). The Kay Picture Test or LEA symbols were used to assess visual acuity in children that were uncooperative with the Snellen or HOTV tests. Some patients did not cooperate with any type of acuity testing and visual acuity was measured using preferential looking tests. Anterior segment evaluation via slit-lamp biomicroscopy, cycloplegic retinoscopy, and fundus examination following dilation of the pupils with cyclopentolate 1 % were also performed. The refractive status of each patient was assessed using a hand-held automated refractometer (SureSightTM autorefractor, Welch Allyn), which has lights and sounds that help to focus a child’s attention. Recently revised American Association for Pediatric Ophthalmology and Strabismus (AAPOS) referral criteria were used to define significant refractive errors (Donahue et al. 2012) (Table 1). Data entry and analysis were performed using
123
Statistical Package for the Social Sciences for Windows version, 17.0 (SPSS, Inc., Chicago IL, USA).
Results In all, the records of 324 patients diagnosed as ASD were reviewed. Among these patients, 267 were male (82 %) and 57 were female (18 %). Mean age of the patients at the time of ASD diagnosis was 5 years (18 months–17 years). Visual acuity testing could be performed in 29 patients (9 %), whereas 295 (91 %) did not cooperate with any kind of acuity testing. Automated refractions following cycloplegia were completed in every patient. The patients’ refractive errors according to AAPOS criteria are given in Table 2. Spherical values were between -3.50 D and ?6.00 D. All astigmatism values were recorded in plus cylinder; cylindrical values were between ?0.50 D and ?3.00 D. In total, 28 (8.6 %) patients had strabismus, of which 14 had an exodeviation (50 %), 13 had an esodeviation (46.4 %), and 1 had a hyperdeviation (3.6 %). List of the patients with other ophthalmic problems is given in Table 3. Associated systemic abnormalities were noted in 14.9 % of the patients (Table 4).
Discussion Autism is a disorder of the central nervous system that significantly impairs social interactions of the child. Associated systemic abnormalities may be observed in autistic children, some of which can contribute to deficient communication skills. Ocular abnormalities such as uncorrected refractive errors in children with autism might negatively affect social communication, and due to the challenges of ophthalmological examination in such patients correctable refractive errors may be overlooked. Uncorrected refractive errors and strabismus can lead to severe amblyopia, which parents may not detect. Comprehensive ophthalmological examination may facilitate early diagnosis. Ikeda et al. (2013) reported that 40 % of children with ASD had some type of identifiable ophthalmic problem, most commonly significant refractive error, followed by strabismus, and amblyopia. They also reported that refractive errors were identified in 29 % of patients. In autistic children ophthalmic problems were reported in 33.3 % of patients (Ezegwui et al. 2014), in 27 % (Black et al. 2013), and in 68 % (Singman et al. 2013). In the present study, 26.9 % of the autistic patients had an ocular problem, 22.5 % had a significant refractive error, and 8.6 % had strabismus. Hypermetropia was the most
J Autism Dev Disord Table 1 AAPOS criteria for amblyopia and significant refractive errors
Age (months)
Astigmatism (D)
Hypermetropia (D)
Anisometropia (D)
Myopia (D)
12–30
[2.00
[4.50
[2.50
[-3.50
31–48
[2.00
[4.00
[2.00
[-3.00
[48
[1.50
[3.50
[1.50
[-1.50
Additional criteria for the definition of ambliyopia for all children are: Manifest strabismus [8 prism diopters in primary position, Media opacity [1 mm D Diopters
Table 2 Refractive errors in the patients with ASD Type of refractive error
Cases (n)
Emmetropia
251
Hypermetropia
Percent 77.5
27
8.3
6
1.9
Myopia Simple hypermetropic astigmatism
13
4
Simple myopic astigmatism
11
3.4
Compound hypermetropic astigmatism
8
2.5
Compound myopic astigmatism
5
1.5
Mixed astigmatism Anisometropia
1 2
0.3 0.6
Total
324
100
Table 3 Other ocular problems observed in the patients with ASD Ocular disorder
Cases (n)
Percent
Unilateral ptosis
4
1.2
Cataract
2
0.6
Nystagmus
1
0.3
Phthisis bulbi due to retinopathy of prematurity
1
0.3
Table 4 Systemic abnormalities observed in the patients with ASD Associated systemic abnormality
Cases (n)
Percent
Mental retardation
16
4.9
Epilepsy
9
2.8
Cerebral palsy
5
1.5
Congenital sensorineural hearing loss
5
1.5
Hypotonia
4
1.2
Microcephaly
3
0.9
Auricular atresia
2
0.6
Ventricular septal defect
2
0.6
Down syndrome
2
0.6
Di-George syndrome
1
0.3
common refractive error in the present study, as in the study by Ikeda et al. (2013), whereas in contrast, 8.6 % of the present study’s patients had strabismus, versus 21 % as
reported by Ikeda et al. (2013). This difference might be due to differences in ethnicity and multifactorial insults affecting the prevalence of strabismus between the 2 studies’ populations (Cotter et al. 2011). Visual acuity assessment may be the most challenging part of ophthalmic evaluation in children with autism. Ikeda et al. (2013) reported a cooperation rate of 40 % among 154 patients, whereas Ezegwui et al. (2014) reported a cooperation rate of 11.1 % among 18 patients. Differences between the studies might be due to differences in mean age and the severity of autism between study populations. In the present study 9 % of patients cooperated with visual acuity testing, which is in contrast to 88–100 % reported by Coulter et al. (2015) for an eye examination protocol that included tests of visual acuity, refraction, convergence (eye teaming), stereoacuity (depth perception), ocular motility, and ocular health in ASD patients. Their study included children and adolescents aged 9–17 years of age, whereas mean age in the present study was 5 years. The present study was based on initial ophthalmological findings in patients at the time ASD was diagnosed—a protocol unique to the present study. None of the present study’s patients had yet received treatment or rehabilitation for autism; as such, they were all considered as having severe ASD, and assessment of visual acuity was not possible. Despite the low rate of cooperation with recognition acuity testing in the present study, refractive status was assessed in all the patients. Hand held, non-contact automated refractometers might help ophthalmologists examine autistic children and facilitate assessment of refractive status. Classical retinoscopy may be difficult to perform in children with autism due to attention deficit and poor cooperation. In the present study a hand-held pediatric automated refractometer was used, which has spinning lights to focus attention when performing measurements. These lights can focus the attention of ASD patients because they are often interested in stereotypic movements and turning objects. The non-contact nature of the device is also helpful in children that refuse any type of eye contact during examination. In the present study 324 patients with ASD were screened for ocular problems; to the best of our knowledge the present study is, to date, the largest of its kind.
123
J Autism Dev Disord
In all, 14.9 % of the present study’s patients had associated systemic abnormalities, including mental retardation, followed by epilepsy, cerebral palsy, sensorineural hearing loss, hypotonia, microcephaly, auricular atresia, ventricular septal defect, Down syndrome, and Di-George syndrome. Associated systemic abnormalities in ASD patients have been reported in only a few other studies. Mental retardation was observed in 18 % of ASD patients in Ikeda et al.’s (2013) study and McCabe et al. (2013) reported an association between 22q-11 deletion and ASD. As reported by Ikeda et al. (2013), male predominance among the ASD patients (78 %) was observed in the present study. In conclusion, the present findings highlight the importance of ophthalmological examination in children with ASD, because of the strong association between refractive errors and amblyopia. For ophthalmological examination hand-held, non-contact automated refractometers with spinning lights can facilitate examination in children with autism. Parents and primary care physicians should be made aware of the importance and possibility of ophthalmic evaluation in these children. Larger scale prospective studies are needed to further investigate the prevalence of ophthalmic disorders in children with ASD and to determine the impact that treating such disorders. Conflict of interest The authors declare there are no conflicts of interest—financial or otherwise—related to the materials presented herein.
References Black, K., McCarus, C., Collins, M. L., & Jensen, A. (2013). Ocular manifestations of autism in ophthalmology. Strabismus, 21(2), 98–102.
123
Centers for Disease Control and Prevention. (2008). Prevalence of autism spectrum disorders—Autism and Developmental Disabilities Monitoring Network, fourteen sites, United States. MMWR 2012a; 61(No. SS03):1–19. http://www.cdc.gov/mmwr/ pdf/ss/ss6103.pdf. Cotter, S. A., Varma, R., Tarczy-Hornoch, K., McKean-Cowdin, R., Lin, J., Wen, G., et al. (2011). Risk factors associated with childhood strabismus: The multi-ethnic pediatric eye disease and Baltimore pediatric eye disease studies. Ophthalmology, 118(11), 2251–2261. Coulter, R. A., Bade, A., Tea, Y., Fecho, G., Amster, D., Jenewein, E., et al. (2015). Eye examination testability in children with autism and in typical peers. Optometry and Vision Science, 92(1), 31–43. doi:10.1097/OPX.0000000000000442. Donahue, S. P., Arnold, R., Ruben, J., Silbert, D., Arthur, B., & Neely, D. (2012). Revised guidelines for reporting results from studies of preschool vision screening. JAAPOS, 16(1), e4. doi:10.1016/j.jaapos.2011.12.016. Elliott, M. C., & Firth, A. Y. (2009). The logMAR Kay picture test and the logMAR acuity test: A comparative study. Eye (Lond), 23(1), 85–88. Ezegwui, I. R., Lawrence, L., Aghaji, A. E., Okoye, O. I., Okoye, O., Onwasigwe, E. N., et al. (2014). Refractive errors in children with autism in a developing country. Nigerian journal of clinical practice, 17(4), 467–470. Gaugler, T., Klei, L., Sanders, J. S., Bodea, C. A., Goldberg, A. P., Lee, A. B., et al. (2014). Most genetic risk for autism resides with common variation. Nature Genetics, 46, 881–885. Ikeda, J., Davitt, B. V., Ultmann, M., Maxim, R., & Cruz, O. A. (2013). Brief report: Incidence of ophthalmologic disorders in children with autism. Journal of Autism and Developmental Disorders, 43, 1447–1451. McCabe, K. L., Melville, J. L., Rich, D., Strutt, P. A., Cooper, G., Loughland, C. M., et al. (2013). Divergent patterns of social cognition performance in autism and 22q11.2 deletion syndrome (22q11DS). Journal of Autism and Developmental Disorders, 43, 1926–1934. Singman, E., Matta, N., Fairward, A., & Silbert, D. (2013). Evaluation of plusoptiX photoscreening during examinations of children with autism. Strabismus, 21(2), 103–105. Stein, T. P., Schluter, M. D., Steer, R. A., Guo, L., & Ming, X. (2015). Bisphenol a exposure in children with autism spectrum disorders. Autism Research,. doi:10.1002/aur.1444.
