Purpose
To study associations between strabismus and alcohol use, anxiety, and depression among 10- to 17-year-old children in Guangdong, southern China.
Design
Cross-sectional, population-based study.
Methods
Among 7537 children aged 6-17 years from 9 randomly selected primary and middle schools, ocular alignment was assessed with the Hirschberg light reflex, cover-uncover testing, and alternate cover testing at distance (6 m) and near (40 cm). Additionally, 4000 children (53.1%) aged 10+ years received self-administered questionnaires containing screening questions on alcohol use, anxiety, and depression.
Results
Examinations were completed on 7464 of 7537 subjects (99.0%), including 3928 boys (52.6%), with a mean age of 11.1 ± 1.8 years. The prevalence of any strabismus, including exotropia (2.7%), esotropia (0.2%), and intermittent exotropia (3.9%), was 6.8%. Strabismus was more prevalent in urban students (7.3%) and female subjects (7.4%) compared to rural students (6.0%) and male subjects (6.2%) (all P < .05). In multivariate regression models, any strabismus was associated with older age and rural vs urban residence. Among 3903 children (97.6%) answering questionnaires, history of alcohol use (62.3% vs 36.3%) and positive screening responses for depression (26.0% vs 11.6%) and anxiety (10.3% vs 4.9%) were significantly ( P < .01 for all) more common among children with strabismus.
Conclusion
These Chinese children with strabismus had a significantly higher prevalence of alcohol use and possible markers of emotional problems than children without strabismus. Further research should focus on the appropriateness of classifying surgical treatment for strabismus as “cosmetic” (ineligible for reimbursement) under China’s rural health insurance.
Strabismus is a very common eye condition in children that is associated with functional, cosmetic, and psychosocial consequences. Early detection and treatment usually leads to improved outcomes. The reported population prevalence of strabismus in children and teenagers varies widely across populations, from 1%-15.4%. However, many of these estimates rely on the review of medical records rather than examinations. Given the variations in study design and strabismus classification, it is impossible to generalize findings from these studies to all persons.
The strabismus prevalence among Chinese school-aged children (age >6 years) has rarely been reported, and few studies have addressed prevalence with reference to age and urban vs rural residence. Two previous studies from a decade ago, focused principally on refractive error, reported the prevalence of strabismus in Chinese children. He and associates assessed visual impairment in 4368 children aged 5-15 years in the metropolitan area of Guangzhou, southern China. They reported near and distant tropias in 1.9% and 3% of subjects, respectively. Based on a study of 5884 children, also aged 5-15 years, Zhao and associates estimated the strabismus prevalence in a rural population in northern China as 2.8%.
Several studies have demonstrated that adults with ocular misalignment are more likely to have psychosocial problems. However, the prevalence and nature of emotional disorders in school children with strabismus have not previously been determined on a population basis in China. In addition, few if any population-based studies have been conducted to examine the link between strabismus and unhealthy behaviors such as smoking and drinking.
In this study, we report on the prevalence of strabismus and the rate of self-reported alcohol use and markers for depression and anxiety among children with strabismus and unaffected children, in a population-based survey in urban and rural areas in the Shantou district of Guangdong Province, southern China.
Methods
Subject Recruitment
A cross-sectional, population-based survey of school-aged children was conducted during the 2009-2010 academic year. Students provided verbal assent, and their legal guardians provided written consent. This study was approved by the Ethics Committee of the Joint Shantou International Eye Center and was conducted in accordance with the tenets of the Declaration of Helsinki.
A list of the primary, middle, and high schools located in the Shantou district was obtained. Two categories of schools were identified according to the Shantou Education Bureau: urban and rural (in the latter, most of the population worked in agriculture). There were 302 public schools in Shantou’s 3 districts of Jinping, Longhu, and Chenghai: 81 elementary, 51 middle, and 38 high schools in urban areas; and 59 elementary, 41 middle, and 32 high schools in rural areas.
Five urban schools (3 primary, 1 middle, and 1 high school) and 4 rural schools (2 primary, 1 middle, and 1 high school) were randomly selected, for a total of 9 schools. The school sizes ranged from 800-1000 students for the primary schools and 500-700 students for the middle and high schools. In China, school attendance is compulsory through the third year of middle school (approximately 16 years old) and secondary school enrollment rates of greater than 91% have been reported for nearby areas of rural Guangdong. Therefore, the sample is likely to be representative of the population in the age range of 6-17 years.
Ocular Examination
All participants underwent a complete strabismus examination by qualified pediatric ophthalmologists. Ocular alignment was assessed using the Hirschberg light reflex test, uncover test, and alternate cover test, without refractive correction. The Hirschberg test was performed by directing a penlight at the eyes from a distance of 40 cm and observing the location of the light reflex in each eye relative to the center of the pupil. For example, a light reflex located nasal to the pupil would suggest a temporal deviation of the eye, that is, an exotropia. The cover-uncover test (CUT) involved the child fixating on an object at either distance (6 m) or near (40 cm) while 1 eye was covered. The examiner observed the presence or absence of a refixation movement of the uncovered eye: a refixation moving temporally would suggest that the uncovered eye had been deviating nasally, hence an esotropia. The other eye was then tested in the same way. In the alternate cover test (ACT), the eyes were rapidly and alternately occluded. Deviation measured in this fashion represents the total of both manifest (tropia) and latent (phoria) misalignment. The presence of strabismus and its characteristics (constant or intermittent) and type (phoria, exotropia, esotropia) were recorded.
Definitions of the Different Types of Strabismus
Children were classified as having strabismus if any tropia was present at distance or near, with or without spectacles. A patient with orthophoria showed no deviation during Hirschberg testing and no eye movement during uncover testing or ACT. A patient with esophoria or exophoria showed a horizontal shift during ACT and no movement of the uncovered eye during CUT. A patient with intermittent exotropia presented no deviation during Hirschberg testing and no movement of the uncovered eye during CUT, but presented exodeviation after prolonged ACT. A patient with exotropia or esotropia exhibited exodeviation or esodeviation, respectively, during Hirschberg testing, as confirmed by CUT and ACT. During analyses, esotropia prevalence was calculated, including intermittent esotropia. In no case did the direction of the strabismus change between CUT and ACT or between near and distance.
Basic Questionnaires
All subjects aged ≥10 years (n = 4000, 53.1%) were given a self-administered basic questionnaire by study personnel before being told the results of their eye assessment. Investigators answered questions raised by the participants. The following information was obtained: age, sex, school, history of school injury in the past 1 year, smoking history, and any history of alcohol use. Subjects were also asked the following 2 screening questions recommended by the United States Preventive Services Task Force and the United Kingdom National Institute for Health and Care Excellence (NICE), which may be as effective in children and adults as longer instruments: “In the past 2 weeks, have you felt down, depressed, or hopeless?” and “In the past 2 weeks, have you felt little interest in doing things?” Following Whooley and associates, a positive response to either question was considered a positive screening result for depression. Subjects were asked the following 2 screening questions related to anxiety, modified from Seitz and based on DSM-IV-TR (American Psychiatric Association, 2000, Diagnostic and statistical manual of mental disorders [4th ed, text revision]) criteria for Generalized Anxiety Disorder: “Do you frequently feel anxious, nervous, or worried?” and “Has this worrying been a problem for 6 months or more?” A “yes” response on both constituted a positive screening test.
Statistical Analysis
Prevalence of the various types of strabismus was calculated as the ratio of the number of individuals affected to the total number of individuals evaluated in the various age and sex and residential (urban vs rural) strata: any strabismus, esotropia, exotropia, and intermittent exotropia. The χ 2 test and multivariate logistic regression were used to compare the proportions and associations of students with different types of strabismus by age group, sex, and residence. Prevalence of self-reported health factors among children with and without strabismus were assessed using the χ 2 test and the generalized estimating equation model. All statistical analyses were performed with the SPSS 18.0 software package (SPSS/IBM Corporation, Chicago, Illinois, USA). A P value of .05 was considered significant.
Results
Of the 7537 children in the sample, 7464 (99.0%) completed the strabismus examinations and were included in the data analysis, including 3928 boys (52.6%) and 3536 girls (47.4%). Forty-three students (0.5%) could not be examined or had no parental consent, and 30 students (0.4%) were absent from school. Urban students (57.2%) outnumbered rural students. Table 1 shows the age, sex, and residential distributions of the study population.
| Characteristic | Total No. (%) | Completing Testing, N (%) | Completed Questionnaire, a N (%) | Did Not Complete Questionnaire, a N (%) |
|---|---|---|---|---|
| Age (y) | ||||
| 6-8 | 2462 (32.7) | 2440 (32.7) | — | — |
| 9-11 | 2657 (35.3) | 2636 (35.3) | 1546 (39.6) | 66 (68.0) |
| 12-14 | 1235 (16.4) | 1227 (16.4) | 1207 (30.9) | 20 (20.6) |
| 15-17 | 1183 (15.7) | 1161 (15.6) | 1150 (29.5) | 11 (11.3) |
| Sex | ||||
| Male | 3968 (52.7) | 3928 (52.6) | 2037 (52.2) | 43 (44.3) |
| Female | 3569 (47.4) | 3536 (47.4) | 1866 (47.8) | 54 (55.7) |
| Area of residence | ||||
| Urban | 4304 (57.1) | 4269 (57.2) | 2224 (57.0) | 56 (57.7) |
| Rural | 3233 (42.9) | 3195 (42.8) | 1679 (43.0) | 41 (42.3) |
| TOTAL | 7537 | 7464 | 3903 | 97 |
a Questionnaire was administered only to children >10 years of age.
The overall prevalence of strabismus in children aged 6-17 years was 6.8%, including exotropia (2.7%), esotropia (0.2%), and intermittent exotropia (3.9%). Among the different types of strabismus, the proportion of intermittent exotropia (57.3%) was the highest, followed by exotropia (39.9%) and esotropia (2.8%). Strabismus was more prevalent in urban students (7.3%) and girls (7.4%) compared to rural students (6.0%) and boys (6.2%). Table 2 presents the strabismus prevalence in terms of age, sex, and area of residence (rural or urban).
| Esotropia | Exotropia | Intermittent Exotropia | Any Strabismus | |
|---|---|---|---|---|
| Age (y) | ||||
| 6-8 | 9 (0.4%) | 60 (2.5%) | 78 (3.2) | 147 (6.0%) |
| 9-11 | 3 (0.1%) | 91 (3.5%) | 141 (5.3) | 235 (8.9%) |
| 12-14 | 1 (0.1%) | 22 (1.8%) | 12 (1.0) | 35 (2.9%) |
| 15-17 | 1 (0.1%) | 29 (2.5%) | 59 (5.1) | 89 (7.7%) |
| P value | .145 | .017 | <.001 | <.001 |
| Sex | ||||
| Male | 4 (0.1%) | 106 (2.7%) | 134 (3.4%) | 244 (6.2%) |
| Female | 10 (0.3%) | 96 (2.7%) | 156 (4.4%) | 262 (7.4%) |
| P value | .105 | .965 | .026 | .040 |
| Residence | ||||
| Urban | 3 (0.07%) | 127 (3.0%) | 183 (4.3%) | 313 (7.3%) |
| Rural | 11 (0.34%) | 75 (2.3%) | 107 (3.3%) | 193 (6.0%) |
| P value | .015 | .098 | .038 | .023 |
| TOTAL | 14 (0.2%) | 202 (2.7%) | 290 (3.9%) | 506 (6.8%) |
There was no significant difference in prevalence of esotropia by age and sex. Esotropia was slightly more prevalent ( P < .05, Table 2 ) in rural than in urban students, whereas exotropia was similarly prevalent in both. Students aged 9-11 years (5.3%) and 15-17 years (5.1%) had higher intermittent exotropia prevalence rates than the other age groups. There was significant difference in the prevalence rates of intermittent exotropia between the areas of residence (urban 4.3% and rural 3.3%, P < .05). Intermittent exotropia was more prevalent in girls (4.4%) than in boys (3.4%) ( P < .05, Table 2 ).
Multivariate logistic regression models showed that older and urban children tended to have higher prevalence rates of any strabismus. Older age was associated with increased risk for exotropia and intermittent exotropia. Female students were more likely to have intermittent exotropia ( Table 3 ).
| Factors | Esotropia | Exotropia | Intermittent Exotropia | ||||||
|---|---|---|---|---|---|---|---|---|---|
| Beta | Standard error | 95% CI | Beta | Standard error | 95% CI | Beta | Standard error | 95% CI | |
| Age | 0.096 | 0.157 | 0.810-1.496 | 0.109 | 0.029 | 1.054-1.179 | 0.209 | 0.047 | 1.124-1.350 |
| Sex | −0.613 | 0.562 | 0.180-1.629 | 0.052 | 0.149 | 0.786-1.411 | −0.529 | 0.230 | 0.375-0.925 |
| Urban vs rural | −0.156 | 0.062 | 0.758-0.966 | 0.026 | 0.067 | 0.900-1.170 | 0.224 | 0.154 | 0.925-1.693 |
Questionnaires from 3903 students ≥10 years of age (97.6%), including 292 students (7.5%) with strabismus, contained valid data for assessing history of school injury, smoking, and alcohol use and recent history of depression or anxiety. Children completing the questionnaire had a mean age of 12.9 years, 52.2% were boys, and 57% were from urban areas ( Table 1 ). History of alcohol use (62.3% vs 36.3%) and positive response to screening questions for depression (26.0% vs 11.6%) and anxiety (10.3% vs 4.9%) were significantly ( P < .01 for all) more common among children with strabismus, whereas history of injury and smoking did not differ between the groups ( Table 4 ).
| Variable | Without Strabismus | With Strabismus | Beta Coefficient a | Standard Error | 95% Confidence Interval | P Value | |
|---|---|---|---|---|---|---|---|
| Lower | Upper | ||||||
| History of school injury | 590 (16.3%) | 75 (25.7%) | 3.595 | 2.2389 | 1.199 | 2.772 | .221 |
| Ever smoked | 493 (13.7%) | 53 (18.2%) | 4.325 | 1.2670 | 0.583 | 1.365 | .536 |
| Ever used alcohol | 1310 (36.3%) | 182 (62.3%) | 0.321 | 0.0656 | 0.342 | 1.223 | .001 |
| Depression b | 420 (11.6%) | 76 (26.0%) | |||||
| Question#1 | 385 (10.7%) | 69 (23.6%) | 0.433 | 0.1123 | 0.607 | 2.219 | <.0001 |
| Question#2 | 393 (10.9%) | 69 (23.6%) | 0.358 | 0.2241 | 1.487 | 3.325 | <.0001 |
| Anxiety c | 176 (4.9%) | 30 (10.3%) | |||||
| Question#1 | 207 (5.7%) | 36 (12.3%) | 0.457 | 0.389 | 1.554 | 2.221 | .002 |
| Question#2 | 176 (4.9%) | 30 (10.3%) | 0.587 | 0.665 | 1.226 | 3.429 | <.0001 |
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