Journal of Pediatric Ophthalmology and Strabismus

Original Article 

Amblyopia Risk Factors in Premature Children in the First 3 Years of Life

Lauren Hennein, MD; Euna Koo, MD; Julie Robbins, MA; Alejandra G. de Alba Campomanes, MD, MPH

Abstract

Purpose:

To determine the incidence of amblyopia risk factors during the first 3 years of life in premature children.

Methods:

This prospective cohort included 145 premature children (gestational age of less than 37 weeks) who were evaluated for amblyopia risk factors every 6 months until age 3 years. The incidence rate, cumulative incidence, and prevalence of any amblyopia risk factor were assessed in retinopathy of prematurity (ROP) and non-ROP screened groups. Multivariate logistic regression was performed to evaluate variables associated with the development of an amblyopia risk factor.

Results:

The 3-year incidence rates of amblyopia risk factors were similar between the non-ROP and ROP screened groups (18 versus 19 cases per 1,000 person-years, respectively). The 3-year cumulative incidence was also similar: 32% (95% confidence interval [CI]: 18 to 47) in the non-ROP and 14% (95% CI: 5 to 28) in the ROP screened group (P > .05). In the ROP screened group, the prevalence rates were 20% or greater at most time points. In the non-ROP screened group, the prevalence rates were 11% to 14% during the first 18 months and increased to more than 20% at 24 months and thereafter. Astigmatism was the most prevalent amblyopia risk factor in both groups (7% to 18%).

Conclusions:

The incidence of amblyopia risk factors was not significantly different between non-ROP and ROP screened children in our cohort. The prevalence of refractive errors among premature non-ROP screened children was higher than that reported in childhood in the literature. It may be appropriate to screen all children with a history of prematurity for refractive errors around 24 months of age.

[J Pediatr Ophthalmol Strabismus. 2019;56(2):88–94.]

Abstract

Purpose:

To determine the incidence of amblyopia risk factors during the first 3 years of life in premature children.

Methods:

This prospective cohort included 145 premature children (gestational age of less than 37 weeks) who were evaluated for amblyopia risk factors every 6 months until age 3 years. The incidence rate, cumulative incidence, and prevalence of any amblyopia risk factor were assessed in retinopathy of prematurity (ROP) and non-ROP screened groups. Multivariate logistic regression was performed to evaluate variables associated with the development of an amblyopia risk factor.

Results:

The 3-year incidence rates of amblyopia risk factors were similar between the non-ROP and ROP screened groups (18 versus 19 cases per 1,000 person-years, respectively). The 3-year cumulative incidence was also similar: 32% (95% confidence interval [CI]: 18 to 47) in the non-ROP and 14% (95% CI: 5 to 28) in the ROP screened group (P > .05). In the ROP screened group, the prevalence rates were 20% or greater at most time points. In the non-ROP screened group, the prevalence rates were 11% to 14% during the first 18 months and increased to more than 20% at 24 months and thereafter. Astigmatism was the most prevalent amblyopia risk factor in both groups (7% to 18%).

Conclusions:

The incidence of amblyopia risk factors was not significantly different between non-ROP and ROP screened children in our cohort. The prevalence of refractive errors among premature non-ROP screened children was higher than that reported in childhood in the literature. It may be appropriate to screen all children with a history of prematurity for refractive errors around 24 months of age.

[J Pediatr Ophthalmol Strabismus. 2019;56(2):88–94.]

Introduction

Patients with a history of retinopathy of prematurity (ROP) have a higher prevalence of amblyopia risk factors.1,2 The risk is highest in children with a history of severe ROP or very low birth weight, but premature children with mild or even no ROP also have elevated risk of developing amblyopia risk factors and amblyopia.2–5 Given their increased risk for visual disorders, the American Academy of Ophthalmology (AAO) and American Association for Pediatric Ophthalmology and Strabismus (AAPOS) recommend ophthalmologic follow-up within 4 to 6 months after discharge for all children who meet acute-phase ROP screening, regardless of ROP severity. For premature patients who do not meet criteria for acute-phase screening (gestational age from 30 to 37 weeks and birth weight of greater than 1,500 grams), there are no specific recommendations for additional examinations other than the general preschool vision screening recommendations between 3 and 5 years of age in the United States.6,7 Some studies have shown that these children may also have a higher incidence of amblyopia risk factors.4,5,8–11

The purpose of this study was to determine the incidence and timing of presentation of amblyopia risk factors in premature children during the first 3 years of life. Our findings may provide evidence for an alternative screening timeline for premature children.

Patients and Methods

This retrospective chart review of a prospective cohort complied with the Health Insurance Portability and Accountability Act and followed the tenets of the Declaration of Helsinki. This study received institutional review board approval from the University of California San Francisco.

Study Population

All premature infants (defined as a gestational age of less than 37 weeks) born at Zuckerberg San Francisco General Hospital (ZSFG) between October 2011 and August 2013 were included (N = 292). A comprehensive ophthalmological examination at the corrected age of 6 months was recommended at discharge from the hospital, regardless of whether the child met criteria for acute-phase ROP screening. Current guidelines in the United States recommend ROP screening in those with a gestational age of less than 30 weeks or birth weight of greater than 1,500 grams,6,7 but guidelines at ZSFG at the time of the study screened for ROP in those with a gestational age of less than 32 weeks or birth weight of less than 1,500 grams, so this criterion was used in our study. Patients who had undergone ROP screening (ROP screened) were observed until full ROP regression was observed and the retina was fully vascularized; these patients were then scheduled for an examination at 6 months of corrected age. Patients who died before the first examination or did not present for at least one of the six follow-up examinations during the study period were excluded.

Clinical Examinations

Baseline variables were collected from the medical records: sex, race, ethnicity, gestational age, birth weight, worst stage and zone of ROP, intrauterine toxic exposure, and medical comorbidities. Intrauterine growth restriction was defined as a birth weight less than the 10th percentile on the Fenton growth chart.12 A family history of requiring glasses in childhood, strabismus, amblyopia, or childhood vision problems in any first-degree relative was elicited at the first visit from the child's caregiver.

Patients underwent a comprehensive ophthalmological examination at 6-month intervals until 3 years of age. At each clinic visit, a visual function assessment, extraocular motor examination, cycloplegic refraction with retinoscopy, anterior segment, and dilated funduscopic examination were performed. A single pediatric ophthalmologist (AGD) performed the majority of the examinations and cycloplegic refractions.

The main outcome measure was the presence of at least one amblyopia risk factor in at least one eye as defined by the age-specific AAO guidelines (from birth to 3 years).7 These amblyopia risk factors were weighted equally and were recorded as either present or absent. Refractive error thresholds were defined according to age as defined by the Preferred Practice Pattern Guidelines from the American Academy of Ophthalmology Pediatric Ophthalmology and Strabismus Panel.7 Anisometropia was defined as the difference between the meridians of greatest error in each eye. Strabismus was measured in each patient using the light reflex test, cover–uncover test, and alternate cover test if appropriate. Strabismus was defined as any tropia at distance or near fixation, whether intermittent or constant. The presence of pure phorias was recorded but not included in the definition of amblyopia risk factor. A media opacity was defined as greater than 1 mm in size. Abnormal posterior segment findings were defined as any abnormality on dilated fundus examination that was considered to be of visual significance.

Statistical Analysis

The age at diagnosis of the amblyopia risk factor was defined as the earliest age at which the examination revealed any of the conditions described above. The 3-year cumulative incidence was defined as the number of new cases of an amblyopia risk factor over the 3-year study period divided by the total number of patients in the study. The cumulative incidence of amblyopia risk factors was calculated in the ROP and non-ROP screened groups separately by right censoring each patient at first instance of any amblyopia risk factor using the LIFETEST procedure for non-parametric survival analysis of competing risk. The 3-year incidence rate was defined as the number of new cases of an amblyopia risk factor over the 3-year study period divided by the patients at risk over 3 years. By taking into account only those at risk during the 3 years, the incidence rate minimizes the effects of loss to follow-up compared to cumulative incidence and prevalence. The incidence rate was calculated by using the actuarial method to assume an amblyopia risk factor developed at the halfway point between follow-up examinations. The point prevalence was defined as the number of patients who had any amblyopia risk factor at a particular follow-up time divided by the total number of patients seen at that time point.

Chi-square tests of association and Fisher's exact tests were conducted on point prevalence of amblyopia risk factors at each examination time point. P values of less than .05 were considered statistically significant. Pearson correlation coefficients were calculated for the baseline variables and amblyopia risk factors. Variables that were known to be associated with strabismus or refractive error were included in a multivariate backward elimination logistic regression model. All statistical analyses were performed using SAS software (version 9.4; SAS Institute, Cary, NC).

Results

Patient Characteristics

Of the 292 premature patients (gestational age of less than 37 weeks) born at ZSFG between October 2011 and August 2013, 145 patients were included in this prospective cohort, including 32 patients who met criteria for ROP screening and underwent these examinations. Nineteen patients died before the first examination and 128 patients did not present for at least one outpatient eye examination during the 6- to 36-month study period, so they were excluded from the analysis. Compared to the 145 patients included, the 128 patients who were excluded had significantly lower gestational age (32.9 vs 33.8 weeks, P = .006) and birth weight (1,890 vs 2,270 grams, P < .001). Of the 128 who did not present for at least one out-patient examination, 42 patients qualified for and completed acute-phase ROP screening; of those, only 6 developed ROP (2 patients with stage 1, 1 with stage 2, and 3 with stage 3).

The baseline characteristics of the 145 patients included in this study are summarized in Table 1. Of the 32 ROP screened patients, 10 patients developed ROP (3 patients with stage 1, 5 with stage 2, and 2 with stage 3). The number of patients who presented for each 6-month examination is summarized in Table 2.

Baseline Characteristicsa

Table 1:

Baseline Characteristics

Patients Who Presented for Each 6-Month Examinationa

Table 2:

Patients Who Presented for Each 6-Month Examination

Incidence of Amblyopia Risk Factors

The cumulative incidences of amblyopia risk factors at each 6-month examination until 3 years of life are summarized in Table 3. The cumulative incidence of any amblyopia risk factor was not significantly different between the two groups throughout the 36-month study period (P = .70). The 3-year incidence rates were also similar between the non-ROP and ROP screened groups (18 vs 19 cases per 1,000 person-years, respectively).

Cumulative Incidence of Amblyopia Risk Factors Over the 36-Month Study Perioda,b

Table 3:

Cumulative Incidence of Amblyopia Risk Factors Over the 36-Month Study Period

The cumulative incidence for strabismus and any refractive error were also not significantly different between the two groups throughout the 36-month study period (P = .32 and .20, respectively). Thirteen percent of patients with at least one amblyopia risk factor had both strabismus and an amblyogenic refractive error throughout the study period. No patients were diagnosed as having media opacities or visually significant posterior segment abnormalities throughout the 36-month study period.

Multivariate logistic regression did not find any of the baseline variables to be significantly associated with the development of amblyopia risk factors. A history of neurologic abnormality was significantly associated with the development of strabismus (adjusted odd ratio: 0.1; 95% confidence interval [CI]: 0.02 to 0.43).

Prevalence of Amblyopia Risk Factors

Table 4 summarizes amblyopia risk factor point prevalence rates calculated at each 6-month examination. There were no significant differences between the prevalence rates in the non-ROP and ROP screened groups at any time point during the 36-month study period (all P > .05). In the ROP screened group, the prevalence of any amblyopia risk factor was greater than 20% at most time points, whereas the prevalence of any amblyopia risk factor in the non-ROP screened group was greater than 20% in the latter half of the study period (after 24 months). In non-ROP screened children from 24 to 36 months, the higher prevalence rates were more evident for refractive errors (16% to 22%) than strabismus (3% to 12%). When analyzing refractive error by categories, astigmatism was most common (total prevalence rates ranging from 7% to 18%), followed by hyperopia (2% to 5%), anisometropia (0% to 3%), and then myopia (0% to 2%).

Prevalence of Amblyopia Risk Factors Over the 36-Month Study Perioda,b

Table 4:

Prevalence of Amblyopia Risk Factors Over the 36-Month Study Period

Discussion

Principal Findings

At 3 years, the incidence rate, cumulative incidence, and prevalence of all amblyopia risk factors in premature children did not significantly differ between those who did and did not qualify for acute-phase ROP screening. After 24 months, the prevalence of amblyopia risk factors in premature children who were not at risk for ROP was between 22% and 25%, which is higher than the reported prevalence in children of that age (15% to 20%).6 In our population, the prevalence was between 7% to 22% for amblyogenic refractive errors and 3% to 13% for strabismus. Accordingly, it may be appropriate to screen premature children around 24 months of age for amblyopia risk factors, including those not eligible for acute-phase ROP screening.

In the Context of the Current Literature

This study investigated amblyopia risk factor frequency in premature children regardless of eligibility for ROP screening during the first 3 years of life. A comparison of strabismus and refractive error frequencies between studies is limited because few studies include premature children who do not qualify for ROP screening and there are varying threshold definitions for significant refractive errors.

Our study population included a high proportion of Hispanic and African-American children (Table 1). Compared to the Multi-Ethnic Pediatric Eye Disease Study (MEPEDS) data on Hispanic and African-American children, we found a higher prevalence of astigmatism and hyperopia at 36 months in our non-ROP screened group. Astigmatism prevalence was reported to be 5.1% in African-American children and 10.7% in Hispanic children aged 36 to 47 months.13 We found a higher 36-month prevalence of astigmatism in our non-ROP screened group: 16% when defined as greater than +2.00 diopters (D) and 24% when defined as greater than +1.50 D. At 36 to 47 months, hyperopia of greater than +4.00 D affects 4.3% of African-American and Hispanic children.14 We found a higher 36-month prevalence of hyperopia in our non-ROP screened group: 8% when defined as greater than +4.50 D and 12% when defined as greater than +4.00 D. Chen et al.15 also found that hyperopia and astigmatism were more prevalent in premature children (gestational age of less than 35 weeks or birth weight of less than 1,500 grams), which included children without ROP, when compared to age-matched children. Thus, screening premature children particularly for hyperopia and astigmatism may be appropriate.

Strabismus has been found to be independently associated with prematurity.16 We found a higher prevalence of strabismus in both our non-ROP and ROP screened groups compared to the Baltimore Pediatric Eye Disease Studies (BPEDS) (12% to 17% vs 1.9% to 2.9% in the BPEDS).17 Our 36-month strabismus prevalence was also much higher than that found in the MEPEDS at 36 to 47 months of 1.9% to 2.6%.18

Limitations

Limitations of our study include the lack of a control group of full-term children. We compared our findings to the MEPEDS and BPEDS baseline data, but there could be significant differences between study populations and amblyopia risk factor definitions that make comparisons of prevalence data challenging. Our cohort did not have a high incidence of severe ROP, which may predispose a child to significantly higher risk for amblyopia risk factors. Another limitation is multiple comparisons between the two groups.

We may have underestimated the frequency of refractive risk factors in our study as defined by Donahue et al.6 Refractive risk factor targets differ slightly between the AAO Preferred Practice Pattern7 and the 2013 AAPOS revised targets.6 We defined amblyopia risk factors according to the age-specific AAO guidelines because they aligned better with our age groups and differentiate the anisometropia subtypes.

In our study, compliance with outpatient comprehensive eye examinations decreased by 60% over the study period (Table 2) despite this being a high-risk population in a relatively captive health care system. Accordingly, our frequencies of amblyopia risk factors may be falsely high because patients who were not perceived as having vision problems may have decided not to return for recommended follow-up. However, the excluded patients had significantly lower gestational age (P = .006) and birth weight (P < .001) compared to those who were included in our study, which may underestimate our cumulative incidence of amblyopia risk factors. Furthermore, the demographic information for patients who had three or more examinations was not significantly different from those who had less than three examinations, with the exception of a history of intrauterine toxic exposure (correlation coefficient: −0.18, P = .029).

The proportion of patients lost to follow-up could also influence the generalizability of our study. To further explore the implications of low retention, we conducted a subanalysis that included only those patients who were evaluated at either the 6-, 12-, 30-, or 36-month examination (n = 53). In this sub-analysis, the 3-year prevalence of any amblyopia risk factor (20%), strabismus (13%), and any refractive error (10%) was similar to our 3-year total prevalence (Table 4). Nevertheless, this decline in follow-up is an important observation, and future studies are indicated to decipher how to best detect vision problems in these patients. Incorporating early, repetitive, and effective screening strategies to detect amblyogenic refractive errors19–21 in the primary care setting and in high-risk premature continuity clinics could offer a more efficient strategy to consider.

Finally, our study population was largely Hispanic and of lower socioeconomic status, and thus our results may be more generalizable to these populations. Given that Hispanic children have a higher risk of amblyopia risk factors, including astigmatism,13 hyperopia,14 and myopia,22 our study may overestimate the frequency of amblyopia risk factors. However, the 3-year cumulative incidence of any amblyopia risk factor in Hispanic patients at 36 months (22% with 95% CI: 0.42 to 0.78) was not significantly different than that in the non-Hispanic population (22% with 95% CI: 0.22 to 0.58) (P = .94).

This study demonstrated that at 3 years, the cumulative incidence, incidence rate, and prevalence of all amblyopia risk factors in premature children did not statistically significantly differ between those who were eligible for ROP examinations compared to those who were not. Vision screening in these patients around 24 to 30 months that focuses on detection of refractive errors may be warranted. A prospective study with a full-term control group would be useful to assess the difference in incidence of all amblyopia risk factors and to further assess the need for ophthalmologic examinations in premature children.

References

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  14. Multi-Ethnic Pediatric Eye Disease Study Group. Prevalence of myopia and hyperopia in 6- to 72-month-old African American and Hispanic children: the multi-ethnic pediatric eye disease study. Ophthalmology. 2010;117:140–147.e3. doi:10.1016/j.ophtha.2009.06.009 [CrossRef]
  15. Chen T-C, Tsai T-H, Shih Y-F, et al. Long-term evaluation of refractive status and optical components in eyes of children born prematurely. Invest Ophthalmol Vis Sci. 2010;51:6140–6148. doi:10.1167/iovs.10-5234 [CrossRef]
  16. Cotter SA, Varma R, Tarczy-Hornoch K, et al. Risk factors associated with childhood strabismus: the Multi-Ethnic Pediatric Eye Disease and Baltimore Pediatric Eye Disease Studies. Ophthalmology. 2011;118:2251–2261. doi:10.1016/j.ophtha.2011.06.032 [CrossRef]
  17. Friedman DS, Repka MX, Katz J, et al. Prevalence of amblyopia and strabismus in white and African American children aged 6 through 71 months. The Baltimore Pediatric Eye Disease Study. Ophthalmology. 2009;116:2128–2134-2. doi:10.1016/j.ophtha.2009.04.034 [CrossRef]
  18. Multi-ethnic Pediatric Eye Disease Study Group. Prevalence of amblyopia and strabismus in African American and Hispanic children ages 6 to 72 months. The Multi-ethnic Pediatric Eye Disease Study. Ophthalmology. 2008;115:1229–1236.e1. doi:10.1016/j.ophtha.2007.08.001 [CrossRef]
  19. Committee on Practice and Ambulatory Medicine and Section on OphthalmologyAmerican Academy of Pediatrics. Use of photoscreening for children's vision screening. Pediatrics. 2002;109:524–525. doi:10.1542/peds.109.3.524 [CrossRef]
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  21. Halegoua J, Schwartz RH. Vision photoscreening of infants and young children in a primary care pediatric office: can it identify asymptomatic treatable amblyopic risk factors?Clin Pediatr (Phila). 2015;54:33–39. doi:10.1177/0009922814541805 [CrossRef]
  22. Borchert MS, Varma R, Cotter SA, et al. Risk factors for hyperopia and myopia in preschool children. The Multi-ethnic Pediatric Eye Disease and Baltimore Pediatric Eye Disease Studies. Ophthalmology. 2011;118:1966–1973. doi:10.1016/j.ophtha.2011.06.030 [CrossRef]

Baseline Characteristicsa

CharacteristicNon-ROP Screened (n = 113)ROP Screened (n = 32)Pb
Gestational age, weeks35 (35 to 36)30 (29 to 31)< .001
Birth weight, grams2,510 (2,430 to 2,600)1,400 (1,260 to 1,550)< .001
Presence of intrauterine growth restriction, %6 (2 to 11)9 (0 to 20).69
Sex, % female35 (26 to 44)38 (20 to 55).84
Race/ethnicity.743
Hispanic, %58 (48 to 67)66 (49 to 82)
White, %5 (1 to 9)9 (0 to 20)
African-American, %15 (8 to 22)13 (0 to 24)
Asian, %19 (11 to 26)13 (0 to 24)
Pacific Islander, %1 (0 to 3)0 (N/A)
Other, %3 (0 to 6)0 (N/A)
Family history of childhood eye disorders, %37 (28 to 46)38 (20 to 55).51
Neurologic condition, %4 (0 to 7)34 (18 to 51)< .001
History of intrauterine toxic exposure, %13 (7 to 20)19 (5 to 33).41

Patients Who Presented for Each 6-Month Examinationa

Exam MonthNo. of Patients Examined% Examined

Non-ROP Screened (n = 113)ROP Screened (n = 32)
6101 (89%)20 (63%)83%
1255 (49%)20 (63%)52%
1838 (34%)12 (38%)34%
2432 (28%)12 (38%)30%
3026 (23%)6 (19%)22%
3632 (28%)12 (38%)30%

Cumulative Incidence of Amblyopia Risk Factors Over the 36-Month Study Perioda,b

Exam MonthAny Risk Factor (P = .70)Strabismus (P = .32)Refractive Error (P = .20)



Non-ROP ScreenedROP ScreenedNon-ROP ScreenedROP ScreenedNon-ROP ScreenedROP Screened
612 (5%)4 (6%)1 (0.3%)2 (3%)9 (4%)3 (5%)
1215 (7%)4 (6%)1 (0.3%)2 (3%)13 (7%)3 (5%)
1815 (7%)5 (10%)1 (0.3%)2 (3%)13 (7%)3 (5%)
2419 (13%)6 (14%)2 (1%)3 (6%)17 (13%)3 (5%)
3021 (17%)6 (14%)3 (3%)3 (6%)20 (20%)3 (5%)
3625 (32%)6 (14%)7 (16%)4 (15%)21 (25%)3 (5%)

Prevalence of Amblyopia Risk Factors Over the 36-Month Study Perioda,b

Exam MonthAny Risk Factor (P = .70)Strabismus (P = .32)Refractive Error (P = .20)



Non-ROP ScreenedTotalROP ScreenedNon-ROP ScreenedTotalROP ScreenedNon-ROP ScreenedROP ScreenedTotal
612 (12%)4 (20%)16 (13%)1 (1%)2 (10%)3 (3%)9 (9%)3 (15%)12 (10%)
128 (14%)4 (21%)12 (16%)0 (0%)2 (11%)2 (3%)6 (11%)2 (11%)8 (11%)
184 (11%)4 (36%)8 (16%)1 (3%)1 (8%)2 (4%)2 (6%)1 (12%)3 (7%)
248 (25%)2 (18%)10 (23%)1 (3%)1 (9%)2 (5%)6 (21%)0 (0%)6 (16%)
306 (23%)3 (50%)9 (28%)1 (4%)1 (17%)2 (9%)5 (22%)1 (25%)6 (22%)
367 (22%)2 (17%)9 (20%)4 (12%)2 (17%)6 (13%)4 (16%)0 (0%)4 (11%)
Authors

From the Department of Ophthalmology, University of California San Francisco, San Francisco, California (LH, AGD); the Department of Ophthalmology, Stanford University, Palo Alto, California (EK); and Stanford Cancer Institute, Stanford University, Palo Alto, California (JR).

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

The authors thank Eugene Lowry, MD, for assistance with data analysis and Jennifer Rose-Nussbaumer, MD, for assistance with manuscript preparation.

Correspondence: Alejandra G. de Alba Campomanes, MD, MPH, 10 Koret Way, San Francisco, CA 94143. E-mail: Alejandra.deAlba@ucsf.edu

Received: September 06, 2018
Accepted: December 11, 2018

10.3928/01913913-20190122-02

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