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Journal Français d'Ophtalmologie
Volume 38, n° 10
pages 934-940 (décembre 2015)
Doi : 10.1016/j.jfo.2015.07.006
Received : 20 February 2015 ;  accepted : 1 July 2015
Refractive errors and refractive development in premature infants
Les erreurs réfractives et le développement de la réfraction chez les nourrissons prématurés
 

O. Ozdemir a, , Z. Ozen Tunay a, D. Erginturk Acar a, U. Acar b
a Ophthalmology Department, Zekai Tahir Burak Women's Health Education and Research Hospital, Ankara, Turkey 
b Ophthalmology Department, Kastamonu Faculty of Medicine, Hacettepe University, Ankara, Turkey 

Corresponding author. Göz Hastalıkları Polikliniği, Zekai Tahir Burak Kadın Sağlığı Eğitim ve Araştırma Hastanesi, Talatpaşa Bulvarı, Altındağ, Ankara, Turkey.
Summary
Purpose

To examine refractive errors and refractive development in premature infants.

Methods

Premature infants in the retinopathy of prematurity (ROP) screening program were recruited and examined longitudinally between 28 and 58 weeks postmenstrual age. For performing cycloplegic retinoscopy, 1% tropicamide was administered, two drops with a 10-minute interval, in order to paralyze accommodation and to achieve cycloplegia. Birth weight, gestational age, gender and acute ROP disease were recorded. The relationship between spherical equivalent, astigmatism and postmenstrual age was evaluated.

Results

A total of 798 readings were obtained from 258 infants (131 females, 127 males) between 28 and 58 weeks postmenstrual age. The median number of examinations was 3 (minimum 1, maximum 7). In the comparisons of birth weight, gestational age, spherical equivalent and astigmatism between genders, there were no statistically significant differences (P >0.05). Gestational age (regression analysis, r 2=0.30, P <0.01) and birth weight (regression analysis, r 2=0.22, P <0.01) had a significant effect on refractive error development. Preterm babies with lower birth weight and those born more prematurely had lower spherical equivalent. The spherical equivalent of the eyes correlated significantly with the postmenstrual age of the infants (r =0.512, P <0.01).

Conclusions

Infants with low gestational age and low birth weight also had low spherical equivalent. Moreover, spherical equivalent correlated with increasing postmenstrual age. However, astigmatism did not correlate with postmenstrual age and did not associate with gestational age or birth weight.

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Résumé
But de l’étude

Examiner les erreurs réfractives ainsi que le développement de la réfraction chez les nourrissons prématurés.

Matériel et méthodes

Les nourrissons prématurés dans le programme de la rétinopathie du prématuré ont été recrutés et examinés longitudinalement entre l’âge post-menstruel de 28 et 58 semaines. Pour effectuer de la rétinoscopie cycloplégique, 1 % tropicamide a été administrés deux goutte avec des intervalles de 10minutes pour paralyser l’accommodation et obtenir l’cycloplégie. Le poids de naissance, l’âge gestationnel, le sexe et la maladie de la rétinopathie du prématuré ont été enregistrés. La relation entre l’équivalent sphérique et l’astigmatisme à l’âge post-menstruel a été évaluée.

Résultats

Un total de 798 lectures ont été obtenus à partir de 258 nourrissons (131 filles, 127 garçons) entre 28 et 58 semaines d’âge post-menstruel. Le nombre d’examen médian était de 3 (minimum 1, maximum de 7). Dans les comparaisons de poids de naissance, l’âge gestationnel, équivalent sphérique et l’astigmatisme entre le sexe, il n’y avait aucune différence statistiquement significative (p >0,05). L’âge gestationnel (analyse de régression, r 2=0,30, p <0,01) et le poids de naissance (analyse de régression, r 2=0,22, p <0,01) ont eu un effet significatif sur le développement de l’erreur de réfraction. Les nourrissons prématurés dont le poids de naissance inférieur et ceux qui sont nés plus prématurément avaient un équivalent sphérique inférieur. L’équivalent sphérique des yeux ont corrélé significativement avec l’âge post-menstruel des nourrissons (r =0,512, p <0,01).

Conclusion

Les nourrissons avec de faible âge gestationnel et poids de naissance avaient aussi un faible équivalent sphérique. En outre, l’équivalent sphérique a corrélé avec augmentation de l’âge post-menstruel croissance. Mais, l’astigmatisme ne était pas corrélé avec l’âge post-menstruel et n’était pas associé avec l’âge gestationnel et le poids de naissance.

The full text of this article is available in PDF format.

Keywords : Hyperopia, Myopia, Refraction, Refractive status, Retinopathy of prematurity, Retinoscopy

Mots clés : Hypermétropie, Myopie, Réfraction, État de réfraction, Rétinopathie du prématuré, Rétinoscopie


Introduction

Advances in neonatal care and increasing survival rates have been associated with an increasing number of prematurely born infants [1, 2, 3]. Apart from the immediate sight-threatening complications of retinopathy of prematurity (ROP), it is stated that preterm birth with or without ROP, may also lead to abnormal development of the eyes including refractive errors and strabismus [4, 5, 6].

There are some studies in literature about ocular refractive error and biometric components in premature babies and children [4, 5, 6, 7, 8]. The differences of refractive status between premature and full-term babies, especially in preschool children were documented. Myopia was detected more common in prematurely born children. Most studies recorded changes in the ocular refractive error and biometry, and in many of these studies presence of prematurity was reported as a factor on final refractive status [4, 5, 6, 7].

We aimed to evaluate the refractive status of the premature infants at the earliest measurable weeks of premature life and to investigate the development of refraction in premature infants.

Methods

Participants were enrolled into the study following routine screening for ROP from the Zekai Tahir Burak Women's Health Education and Research Hospital. In the current screening program, infants with a birth weight of ≤1500g or gestational age of 32 weeks or less are examined. The first eye examination is performed at fourth postnatal weeks in our program; even for babies who are under 30th postmenstrual weeks [9]. Selected premature infants with an unstable clinical course like infants needing cardio-respiratory support are also examined by the recommendation of a pediatrician or neonatologist. In this study, infants under than 36 gestation weeks were included. Infants with congenital anomalies, hydrocephalus and congenital eye abnormalities such as cataract or glaucoma were excluded from the study. Infants treated with intravitreal injections and/or laser photocoagulation also were excluded. The study described has been carried out in accordance with The Code of Ethics of the World Medical Association (Declaration of Helsinki) for experiments involving humans. Informed consent was obtained for experimentation with parents.

The weight of the baby at birth was measured with an electronic weighting machine. Gestational age was determined according to the first day of the last normal menstrual period and the day of delivery. If this was not possible, it was determined according to the prenatal ultrasonography [10]. Initial examinations for ROP and refraction measurement were performed between 4th and 5th weeks of chronologic (postnatal) age. Follow-up examinations for ROP screening were planned at approximately 1 to 3 weeks’ intervals according to results of the retinal findings until normal vascularization proceeds to Zone 3. However, refractive errors were measured at approximately one-month intervals.

For the funduscopic examination and cycloplegia, topical phenylephrine hydrochloride 2.5% with topical tropicamide 1% were instilled twice at an interval of 10minutes and were waited for a minimum 30minutes. The eyelids were retracted with the utilization of a pediatric speculum after instillation of topical anesthetic 0.5% proparacaine hydrochloride. We studied the right eye of each infant for obtaining the results. The refraction measurement was performed by streak retinoscopy (Welch Allyn Elite Retinoscope, Welch Allyn Inc., NY, USA). The retinoscope is held at a distance of 2/3m using hand-held trial lenses for finding the neutral point. The refractive error was originally calculated by adding −1.5 diopters (D) to the result [11]. The refraction was measured at the beginning of the ocular examination, before performing any ocular manipulations. After retinoscopy, funduscopy with scleral indentation by an indirect ophthalmoscope (Heine Optotechnik, Herrsching, Germany) was performed. ROP was graded according to The International Classification of Retinopathy of Prematurity [12].

Birth weights, gestational age, gender and, zone, stage and clock hours of acute ROP on the day of the ocular examination were recorded. Spherical equivalent (spherical equivalent=sphere+[cylinder/2]) and cylindrical power measurements were calculated. Astigmatism was recorded and evaluated in minus cylinder notations. The relationships of birth weight, gestational age and gender with spherical equivalent and astigmatism measured initially between 4 and 5 weeks of chronologic (postnatal) age were investigated. Moreover, the correlation of spherical equivalent and astigmatism measured during follow-up of infants with the growing postmenstrual age was examined.

Statistical analysis

Statistical analysis was performed using the SPSS software (Statistical Package for Social Sciences version 16.0 SPSS, Inc. Chicago, IL, USA). Results are reported as the mean±standard deviation (SD), frequency and percentages. Normal distribution of quantitative data was determined using the Kolmogorov-Smirnov test, and One Way Analysis Of Variance (Anova) test was used for testing homogeneity of variance. For males and females; the values of gestational age, birth weight, spherical equivalent and astigmatism distributed normally (P >0.05); and homogeneously (P >0.05). So that, for comparisons among males and females infants, the parametric test, independent-sample t -test was used.

Simple linear regression analysis was used for analyzing the relationship of birth weight and gestational age with spherical equivalent and astigmatism. The correlation of spherical equivalent and astigmatism with postmenstrual age were calculated with the Pearson product-moment correlation coefficient.

Results

We examined right eyes of 258 infants (131 females, 127 males) between 28 and 58 weeks of postmenstrual age. A total of 798 readings were obtained. Each infant was examined at least one between 4 and 5 weeks of chronologic (postnatal) age and the median examination number was 3 (minimum 1, maximum 7). The mean postmenstrual age of the infants was 40.4±5.6 weeks in the follow-up period. The mean gestational age was 30.6±2.8 weeks (range 23–36 weeks). The mean birth weight was 1498.1±537.6g (range 640–2500g). Female infants had lower birth weight and gestational age. However, there were no statistically significant differences between the gender and these parameters (P >0.05) (Table 1). ROP was diagnosed in 104 infants (40.3%). Sixty-eight infants (26.3%) developed Stage 1, 24 infants (9.3%) Stage 2 and 12 infants (4.6%) Stage 3 ROP.

In the initial and last mean spherical equivalent and astigmatism measurement, male infants had higher spherical equivalent and astigmatism. However, the statistical difference was not significant (P >0.05) (Table 2). In the first examinations, the refractive error was measured in 258 infants. Gestational age (regression analysis, r 2=0.30, P <0.01) and birth weight (regression analysis, r 2=0.22, P <0.01) had a significant effect on refractive error development (Figure 1, Figure 2). The trend of increasing spherical equivalent with an increase of the gestational age and the birth weight can be seen in regression analysis. Preterm babies with lower birth weights and those born more prematurely had lower spherical equivalent, whereas babies born close to term and heavier had higher spherical equivalent. Astigmatism ranged from 0.25 to 3.0 D. There were no significant associations between gestational age (regression analysis, r 2=0.01, P =0.652) and birth weight (regression analysis, r 2=0.01, P =0.661) with astigmatism, in linear regression analysis.



Figure 1


Figure 1. 

The relation between gestational age and spherical equivalent for preterm infants. Regression equation: F (1256)=108,879; P <0.01, spherical equivalent=−4.967+0.221×gestational age.

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Figure 2


Figure 2. 

The relation between birth weight and spherical equivalent for preterm infants. F (1256)=73,989; P <0.01, spherical equivalent=0.022+0.001×birth weight.

Zoom

For correlations, 798 records of 258 infants in the follow-up period were analyzed. The spherical equivalent of the eyes correlated significantly with the growing postmenstrual age of the infants (r =0.512, P <0.01). The increase of spherical equivalent followed a linear pattern during the examination period (Figure 3). However, astigmatism did not correlate with the postmenstrual age (r =0.116, P <0.01). From weeks 28 to 58, there was no significant change in the astigmatism error.



Figure 3


Figure 3. 

The correlation between spherical equivalent and postmenstrual age from 798 records of 258 infants (r =0.512, P <0.01).

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Discussion

Numerous studies have reported an increased risk of refractive errors in prematurely born infants [13, 14, 15, 16]. Furthermore, school age children have born prematurely show higher prevalence of myopia, hyperopia and astigmatism [17]. Full-term newborn babies are known to be hypermetropic at birth. Refractive errors at first months of life are related to gestational age. Preterm babies can have myopia, which decreases as gestational age increases [18]. The preterm infants demonstrated more myopia during the first months of life and astigmatism than full-term infants [19]. In this analyzed examination, the measurements with hyperopia were the majority with refraction ranging from 0.25 D to 7.0 D and the measurements with myopia were among −0.50 to −2.50 D.

In most studies, it was reported that the refractive error was not associated with gender. Saw et al. investigated the association of birth parameters with refraction in 1413 children and stated that the refraction measures were similar in boys and girls [20]. In the study of The Multi-Ethnic Pediatric Eye Disease Study Writing Committee with 6024 children aged 6–72 months, there was no significant gender difference in astigmatism [21]. In the present paper, we found that both of the spherical equivalent and astigmatic error were similar in female and male infants.

The premature infants are at risk of multiple complications and morbidities related to visual development. Infants normally have mild hypermetropia. Although refractive error of the newborn eye usually ranges from between +2.0 and +4.0 D, preterm infants seem to have severe myopia and hyperopia [22, 23]. Dobson et al. reported that premature infants had higher incidences of myopia and anisometropia than those reported for full-term infants. Infants with shorter gestational weeks had more severe myopia and astigmatism [24]. In our study, infants with lower gestational age were with lower spherical equivalent. Most of the myopic values were achieved in infants with gestational age less than 28 weeks. We detected the highest myopic value as −2.5 D in a baby born at 28 gestational weeks and the highest spherical equivalent as +7.0 D in an infant born at 32 gestational weeks.

Preterm infants with a birth weight of 1500 grams or less have an increased risk of refractive errors [4]. Varghese et al. performed refraction measurements within the first week of life in 599 newborn babies. The mean spherical equivalent was found myopic (−1.76 D) in babies born less than 1000g and hypermetropic (+4.55 D) in babies born more than 2701g. They had shown that birth weight had a higher correlation to mean spherical equivalent than gestational age. They suggested that birth weight rather than gestational age could be considered as criteria in screening of refractive error, especially in developing countries [18]. A similar result has been reported by Modrzejewska et al. They studied preterm infants at 6 months of life and demonstrated that birth weight in hyperopic infants ranged between 1556g and 1621g, whereas infants with myopia weighed less, between 810g and 1234g [25]. We measured most of myopic values in infants with less than 1000g birth weights. The spherical equivalent was positively correlated with the birth weight.

In the present paper, there was a consistently augmentation of the spherical equivalent with the growing postmenstrual age. Especially from the 50th postmenstrual week, all measurements of spherical equivalent were above +2.0 D. Similar findings have been demonstrated by Cook et al. They examined premature infants longitudinally between 32 and 52 weeks’ postmenstrual age. At the beginning of the study, most infants were myopic, became emmetropic around term, and were hypermetropic toward the end of the study [1].

In the literature, there are few studies whether the gestational age or birth weight is associated with astigmatism. Saunders et al. measured cycloplegic refraction of 59 preterm infants at birth, term, 6 months, 12 months, and 48 months. They identified gestational age as the more important factor relating to astigmatic error and showed that the babies born earlier were with the higher astigmatic error. The measure of astigmatism at birth decreases with gestational age and similarly less astigmatism is seen when birth weight is higher [26]. In contradistinction to this report, it was notified that the incidence of astigmatism did not change along with increasing corrected gestational age in infants at 40–44 weeks [27]. In our study, no association was found between astigmatism and gestational age or birth weight. Furthermore, the astigmatic error did not vary with the growing postmenstrual age.

Cycloplegic retinoscopy is essential to determine the true refractive error. Using tropicamide for retinoscopy is one of the limitations of this study. The cyclopentolate, homatropine and atropine are the better cycloplegic agent [28]. However, we did not prefer them because of avoiding side effects like respiratory depression, allergic reaction, confusion, etc, in premature infants. Furthermore, tropicamide eye drops have also cycloplegic effect. Egashira et al. demonstrated that tropicamide was an acceptable and useful cycloplegic agent for refractive errors [29]. Others limitations of this study may include the number of infants enrolled, a short follow-up for postmenstrual age and/or lack of control group consisting of infants with full-term.

In summary, this investigation has shown that gestational age and birth weight both are related with refractive status in premature babies. Infants with low gestational age and low birth weight had also low spherical equivalent. Moreover, the spherical equivalent increased positively along with the growing postmenstrual age. Conversely, astigmatism did not correlate with the postmenstrual age and did not associate with the birth weight and the gestational age. The gender of infants had no effect on their refractive status.

Disclosure of interest

The authors declare that they have no competing interest.

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