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Strabismus in Children of Birth Weight Less Than 1701 g
Arch Ophthalmol. 2002;120:767-773.
ABSTRACT
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Objective To prospectively study infants of birth weight less than 1701 g in the
East Midlands of England in the mid 1980s at 10 to 12 years of age to determine
the incidence and risk factors for strabismus in children born preterm.
Methods Low-birth-weight children (n = 572) who had been examined during the
neonatal period were invited for a follow-up visit at age 10 to 12 years;
169 eleven-year-old schoolchildren born at full term were also recruited (the
school cohort).
Results Of the original 572 children, 293 consented to further examination.
There was no significant difference between children who were examined and
those who were not in terms of birth weight, gestational age, retinopathy
of prematurity, and cranial ultrasound abnormalities. Compared with the school
cohort (n = 5 [3.0%]; 95% confidence interval, 1.0%-9.1%), the low-birth-weight
cohort had a significant increase in the prevalence of strabismus (n = 59
[20.1%]; 95% confidence interval, 15.9%-25.0%; P<.001).
Compared with published data, there was a relative increase in the occurrence
of exotropia in the low-birth-weight study cohort. Multivariate analysis,
by backward logistic regression, indicated that retinopathy of prematurity,
birth weight, cerebral palsy, anisometropia, and refractive error were all
independently associated with strabismus (P<.05).
Conclusions The results of this study confirm the increased prevalence of strabismus
in a low-birth-weight population. This study also provides more detailed information
on risk factors and strabismus types.
INTRODUCTION
THE INCIDENCE of strabismus is increased in children of low birth weight
compared with those who were born at full term.1-11
Despite this research, several issues have not been addressed. First, no study
has provided a complete breakdown of the strabismus types, which is pertinent
when considering pathogenesis. Because the different types of strabismus vary
in etiology, an analysis that includes all cases of strabismus may not identify
new risk factors for certain types of strabismus in the low-birth-weight population.
Second, although it is known that neonatal factors such as retinopathy of
prematurity (ROP), low birth weight, and neurologic abnormalities are associated
with strabismus, these factors are all closely interrelated. Therefore, multivariate
analysis is required to determine which factors are independently associated
with strabismus. This statistical method has only been used in 2 studies,1, 3 but in one3
the diagnosis of ROP was made retrospectively. In both of these studies, the
age at testing for strabismus was 4 years or younger, before the age by which
all strabismus might have developed.
Herein we present findings from long-term follow-up (10-12 years) of
infants previously studied prospectively who were born in the East Midlands,
England.12-13 These infants underwent
frequent ophthalmic examinations during the first 12 weeks after birth, with
a final examination at corrected age 6 months, which included an assessment
of ocular motility.14
The aims of this follow-up study at 10 to 12 years were to determine
the prevalence and types of strabismus in this low-birth-weight cohort and
to investigate the relationship between the neonatal ophthalmic findings and
the neonatal factors (including birth weight, gestational age, and cranial
ultrasound findings) and subsequent strabismus. These findings were compared
with those from a cohort of schoolchildren born at full term.
SUBJECTS AND METHODS
SUBJECTS
Between July 1, 1985, and May 31 1987, a prospective study of ROP was
undertaken in the 5 neonatal units serving the East Midlands of England (Leicestershire,
Nottinghamshire, and the Southern Derbyshire Health Authorities). All infants
who survived 3 weeks (n = 505), had birth weights of less than 1701 g, and
were born to mothers residing in this geographically defined area who were
enrolled in the study. In addition, 67 infants born to mothers residing outside
the East Midlands but who were transferred to and cared for in 1 of the aforementioned
5 neonatal intensive care units were also assessed. All 572 infants had weekly
ophthalmic examinations 3 to 12 weeks after birth,12
with ROP classified according to the international classification of ROP.15 In addition, 458 infants had an additional examination
at corrected age 6 months,14 which included
an assessment of ocular motility.
TRACING THE INDEX CHILDREN
Extensive efforts were made to trace and gain consent from the children
from the original cohort, as described elsewhere.16
Follow-up involved sending up to 3 letters to each child, telephone contact
if possible, and an appeal on local television and radio to encourage parents
to consent. Many children had moved during the 10 years since the last contact,
so the Office of National Statistics was contacted to identify the child's
health authority. From the health authority, the details of the child's general
practitioner were obtained, and he or she was then contacted for the child's
current address.
SCHOOL COHORT
A group of 169 children born at term was assessed because there are
no published data on the prevalence of strabismus and other visual functions
(measured as part of this study, results to be published elsewhere) in children
aged 10 to 12 years. A total of 169 of the 175 children who consented to the
examination were tested under identical conditions as the study cohort. Six
children were not tested because they were absent from school owing to illness.
We were denied access to confidential information on the children who declined
to participate. Ten primary schools in one city (Nottingham) took part in
the control study, in which every child aged 10 to 11 years was given a letter
for their parents asking for consent to an ophthalmic examination. The schools
were selected to reflect the social class mix of the areas from which the
study cohort was drawn.
OPHTHALMIC INVESTIGATIONS
To minimize disruption, the children were tested in a mobile vision
laboratory at home or at school. The testing was carried out by 2 orthoptists
(including A.R.O.). Strabismus was detected and classified using a cover test,
a prism cover test, and an assessment of ocular movements. Stereopsis was
measured using the TNO test. Cycloplegic refraction was measured using an
autorefractor (Retinomax K-plus; Nikon Corp, Melville, NY) after instillation
of 1% cyclopentolate.
STATISTICAL METHODS
All analysis was performed using a statistical software package (SPSS,
Version 8; SPSS Inc, Chicago, Ill). For comparison of categorical variables,  2 or Fisher exact tests were used. The only continuous data reported
are not normally distributed. Therefore, for comparison between groups, a
Mann-Whitney test was used. For multivariate analysis, backward logistic regression
was used, at the 10% level of significance.
Permission for this study was obtained from the Nottingham University
Hospital Ethics Committee.
RESULTS
From the original cohort of 572 low-birth-weight infants (<1701 g),
33 died after the original study was completed, 7 moved outside the United
Kingdom, and 23 could not be traced. At the general practitioner's request,
the families of 2 children were not contacted. This reduced the cohort to
507 children. There were 17 refusals and 197 nonresponders despite repeated
reminders, leaving 293 individuals who consented. From this low-birth-weight
cohort, 39 children were born to mothers who resided outside the East Midlands.
Therefore, the geographically defined cohort consisted of 254 children.
STRABISMUS
The overall prevalence of strabismus in the entire low-birth-weight
cohort was 20.1% (n = 59; 95% confidence interval, 15.9%-25.0%) and in the
school cohort was 3.0% (n = 5; 95% confidence interval, 1.0%-9.1%; P<.001). For the geographically defined study cohort, this prevalence
was 19.3% (n = 49; 95% confidence interval, 14.5%-25.5%) (Table 1).
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Table 1. Prevalence of Strabismus Types in the Study Cohort and in
Published Data*
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Strabismus types differed between the low-birth-weight and school cohorts.
However, the low number of cases in the latter group precluded direct comparison;
thus, published data were used. Kvarnstrom et al19
presented the data from a retrospective study of community visual screening
of 3126 children aged 10 years and younger. Four hundred thirteen children
were referred to the eye clinic, of whom 84 (2.7%) had strabismus. The subdivision
into esotropia, exotropia, microtropia, and symptomatic phorias precludes
direct comparison with this and other studies. Therefore, the studies of Graham17 (4784 children aged 5 years) and Stidwill18 (60 000 adults) were used for comparison of
types of strabismus (no birth weight data are available for either study,
but low-birth-weight infants represent 7% of all births in the United Kingdom). Table 1 gives the prevalence of strabismus
types for the low-birth-weight cohort and the geographically defined cohort
and from the published data. Graham17 reported
the results of all abnormal cover tests as percentages and did not differentiate
phorias and tropias. Stidwill18 reported all
types of binocular anomaly, such as convergence insufficiency, and because
some individuals had more than 1 anomaly, the total exceeded 100% (Table 1). Thus, comparison between our
study and published studies could only be made with respect to the ratio of
esotropia-exotropia, which in our low-birth-weight study cohort was 1:1, in
the cohort of Kvarnstrom et al19 was 2.6:1,
in that of Graham was 4.9:1, and in that of Stidwill was 3.4:1.
A total of 263 children were evaluated at corrected age 6 months and
at 10 to 12 years. Comparison between these 2 periods is shown in Table 2. The 6-month data do not give precise
details of the classification of strabismus. Therefore, it is not possible
to determine whether the diagnosis has changed in the intervening period.
Also, in cases in which onset was after 6 months, no data are available on
surgical procedures that may have led to a change in diagnosis. However, all
children with a manifest deviation at 6 months had a manifest deviation at
10 to 12 years.
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Table 2. Strabismus Types According to Age at Onset*
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The data were summarized into 2 groups—esotropia and exotropia
(Table 2)—and strabismus
type does not depend on age at onset (P = .3). Small
numbers in the subgroups precluded direct comparison of the various types
of esotropic and exotropic deviations.
One hundred fifty-two children (51.9%) in the low-birth-weight cohort
had ROP in the neonatal period: 98 in stage 1, 40 in stage 2, and 14 in stage
3 or 4. The prevalence of strabismus increases with increasing severity of
acute ROP stage (2trend = 18.70; P<.001) (Figure 1). There
is a statistically significant difference between the groups with esotropia
and exotropia and the prevalence of ROP (Fisher exact test, P = .02). No children with esotropia had severe ROP, whereas 23% of
those with exotropia had severe ROP.
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Strabismus by stage of retinopathy of prematurity (ROP).
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OCULAR MOVEMENTS
Ocular movements were assessed in the 9 positions of gaze. Muscle imbalances,
that is, underactions and overactions or limitations, were categorized by
the direction of action of the individual extraocular muscles and the extent
of imbalance, which was graded as very slight, slight, slight +, moderate,
and marked. Only muscle imbalances graded greater than slight were classed
as an ocular motility disturbance. In the low-birth-weight cohort, 10 children
had an ocular muscle imbalance compared with 1 child in the school cohort.
Statistical analysis is inappropriate owing to the small numbers.
The most commonly occurring ocular muscle imbalance was overaction of
the inferior oblique (n = 9), which in 6 instances was associated with another
type of manifest strabismus. This group includes identical twins with left
monocular elevation deficiency.20
STEREOPSIS
The median stereoacuity of the low-birth-weight and school cohorts was
60 seconds of arc (normal), but there was a statistically significant difference
between the 2 cohorts (P<.001) (interquartile
range: low-birth-weight cohort, 60-240; school cohort, 60-60). Because the
TNO is limited to measuring a specific range of stereoacuities, some children
are outside this scale. Therefore, to allow inclusion of all children in the
analysis, those with no demonstrable stereoacuity on TNO were assigned an
arbitrary code of 9999. After removal of all cases of strabismus from the
analysis, there was no longer a statistical difference between the low-birth-weight
and school cohorts (P = .5).
ABNORMALITIES IN NEUROIMAGING
Cranial ultrasound was performed during the neonatal period on 325 children
in the original cohort,14 and these data are
available for 174 of this low-birth-weight follow-up cohort. Because small
numbers preclude analysis of the individual types of cranial ultrasound defect,
the data were categorized into normal, mild anomalies (germinal layer or intraventricular
hemorrhage, transient ventricular dilation, or persistent flare), and moderate
or severe anomalies (parenchymal hemorrhage, persistent ventricular dilation,
or cystic periventricular dilation). There was a significant association between
ultrasound defects and strabismus (22 = 21.3; P<.001). The percentages of strabismus in each group
were 19.8% (19/96) in the normal group, 19.7% (12/61) in those with mild abnormalities,
and 70.6% (12/17) in those with severe abnormalities.
In the most severe group of each neurologic abnormality, there is a
large increase in the prevalence of strabismus (cystic periventricular leukomalacia,
70%; parenchymal ventricular hemorrhage, 100%; and persistent ventricular
dilation, 71%), suggesting that no single ultrasound finding is responsible
for the increase in strabismus in this subgroup of the low-birth-weight population.
Esotropia and exotropia occurred equally in association with cranial ultrasound
abnormalities diagnosed in the neonatal period (22
= 2.29; P = .3).
REFRACTIVE ERROR
To compare refractive error with the presence of strabismus, the spherical
equivalent, measured in diopter spheres (DS), was calculated, and the more
ametropic eye was used. The prevalence of strabismus was statistically associated
with refractive error (23 = 39.2; P<.001) (Table 3). Hypermetropia
is frequently associated with strabismus, and because it has been shown that
hypermetropia greater than 3.00 DS is a risk factor for amblyopia, we used
3.00 DS as the cutoff value for low hypermetropia and low myopia.21-25
There was no difference in the prevalence of refractive errors between the
esotropia and exotropia groups. However, there was a statistically significant
increase in the prevalence of anisometropia in the exotropia group (21 = 9.85; P = .002). Only 3.8%
of the esotropia group had anisometropia greater than 1.00 DS, whereas 40%
of the exotropia group had anisometropia.
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Table 3. Strabismus and the Relationship With Refractive Status*
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MULTIVARIATE ANALYSIS
The first stage was to perform univariate analysis to determine which
factors are associated with strabismus in the low-birth-weight cohort (Table 4). Also, from a review of the literature,
several other risk factors for strabismus were identified26
and, where possible, were included in the analysis: birth weight, gestational
age, and cerebral palsy (data from parent questionnaires). However, although
maternal age, maternal smoking, and ethnic origin have also been shown to
be risk factors for strabismus, they were not significantly associated on
univariate analysis in this low-birth-weight cohort.
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Table 4. Univariate Analysis for Strabismus*
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To determine which factors are associated with strabismus after controlling
for potential confounders, a backward logistic regression analysis was performed
that included the variables that were significant on univariate analysis.
The final model showed that ROP (any stage), refractive error (greatest risk
>+3.00 DS), birth weight (<1500 and  1000 g), anisometropia, and cerebral
palsy were all independently associated with the presence of strabismus at
age 10 to 12 years (25 = 32.31; P<.001) (Table 5). The
results of the backward logistic regression were confirmed by a forward stepwise
logistic regression. Using the risk factors shown in Table 5 to predict strabismus, the sensitivity of this model was
65.3% and the specificity was 86.0%.
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Table 5. Multivariate Analysis to Predict Strabismus*
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COMMENT
The results of this study confirm the increased prevalence of strabismus
in this low-birth-weight population of children with a birth weight less than
1701 g. It is the first study, to our knowledge, to report specific types
and prevalence of strabismus on an epidemiologic basis at age 10 to 12 years.
The number of children consenting to be assessed was 293 (51.2%) of
the 572 in the original cohort. This follow-up was not planned at the time
of the original investigation, family contact was not maintained, and this
long gap without communication probably accounts for some of the response
failure. Also, at a test age of 10 to 12 years the child is also involved
in the decision to participate, which may also have affected the consent rate.
However, we16 discussed elsewhere that there
was no significant difference between children assessed at follow-up and those
not assessed in terms of birth weight, gestational age, ROP, or cranial ultrasound
abnormalities. Sensitivity analysis shows that even if there were no cases
of strabismus in the 246 children not assessed (children known to be alive
at age 10 to 12 years), there would still be a significant difference in the
prevalence of strabismus between the low-birth-weight cohort and the school
cohort.
Previous studies have attributed the increase in strabismus in children
born prematurely either wholly or in part to ROP,7, 27
the increase in refractive error,2 and neurologic
impairment.1 These factors are interrelated,
and, therefore, univariate analysis may simply be detecting confounding variables.
Only Pennefather et al3 and Holmstrom et al1 addressed this issue, showing that cicatricial ROP,
refractive error, family history, and general development quotient were each
independently associated with strabismus. Other studies have shown that maternal
age, smoking, and ethnic origin are risk factors for strabismus.26
These factors may be responsible for the differing results we found in that
ROP, birth weight, cerebral palsy, anisometropia, and refractive error were
independently related to strabismus. However, a weakness of our study is the
lack of detailed data on family history, which has a well-known association
with strabismus. Amblyopia in this cohort will be the topic of another article.
Extremely low-birth-weight children (<1000 g) have the greatest risk
for ophthalmic morbidity.16 However, although
birth weight is a risk factor for strabismus, there is no increased risk associated
with the lowest birth weight category, emphasizing that all low-birth-weight
children are at risk of strabismus, irrespective of birth weight.
It is known that constant exotropia, compared with esotropia, is more
likely to be associated with a coexisting ocular or systemic condition, including
ROP and prematurity.28 With the high prevalence
of ocular and systemic problems in the low-birth-weight population, it may
be predicted that there would be an increase in the occurrence of exotropia.
This hypothesis is supported by the findings of our study with a high prevalence
of exotropia, which is reflected in the 1:1 exotropia-esotropia ratio. Although
we identified several risk factors for strabismus in general, only anisometropia
and ROP are specific for exotropia. In the low-birth-weight cohort, there
was an especially high prevalence of intermittent near exotropia (10%).
For 75% of children in our study, the onset of nonaccommodative esotropia
was after corrected age 6 months. However, the precise age at onset is unknown,
as the children were not examined between corrected age 6 months and age 10
years.
In summary, this study confirms the increased prevalence of strabismus
in a low-birth-weight population and provides information on strabismus types.
Analysis has shown that ROP, birth weight, cerebral palsy, and refractive
error are all independently associated with strabismus. However, it is not
possible to use this model to predict the occurrence of strabismus. This study
highlights the importance of screening for strabismus in low-birth-weight
children with and without ROP and demonstrates the impact on ophthalmic services.
However, because age at onset is not known, further research is required to
determine precise screening guidelines.
AUTHOR INFORMATION
Submitted for publication June 7, 2001; final revision received February
8, 2002; accepted February 28, 2002.
The initial study was supported by the UK Medical Research Council and
the follow-up study was supported by the National Health Service Research
and Development Mother and Child Programme (London, England) and by Blindness:
Research for Learning, Work, and Leisure (Birmingham, England).
Corresponding author and reprints: Anna R. O'Connor, PhD, Retina
Foundation of the Southwest, 9900 N Central Expressway, Suite 400, Dallas,
TX 75231 (e-mail: anna.oc{at}prodigy.net).
Anna R. O'Connor, PhD;
Terence J. Stephenson, DM, FRCPCH;
Ann Johnson, MD;
Michael J. Tobin, DLit(Ed);
Sonia Ratib, MSc;
Alistair R. Fielder, FRCP, FRCS, FRCOphth
From the Division of Child Health (Drs O'Connor and Stephenson) and
the Trent Institute for Health Services Research (Ms Ratib), University of
Nottingham, Nottingham, England; the National Perinatal Epidemiology Unit,
University of Oxford, Oxford, England (Dr Johnson); the Department of Special
Education, University of Birmingham, Birmingham, England (Dr Tobin); and the
Department of Ophthalmology, Imperial College School of Medicine, London,
England (Dr Fielder). Dr O'Connor is now with the Retina Foundation of the
Southwest, Dallas, Tex.
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