İkbal Seza PETRİÇLİ, Caner KARA, Ayşegül ARMAN

Is being small for gestational age a risk factor for strabismus and refractive errors at 3 years of age?

Background. Visual problems, cerebral visual impairment, refractive errors and strabismus are commonly found in preterm infants in long-term follow-ups. The aim of this study was to determine the factors that lead to the development of amblyogenic risk factors, such as high refractive errors, anisometropia and strabismus, in the long-term evaluation of preterm infants.Methods. We retrospectively evaluated children who were screened for retinopathy of prematurity (ROP) and who had a 3rd year ophthalmologic examination. The impacts of sex, gestational age (GA), birth weight (BW), BW for GA, being small for gestational age (SGA), being appropriate for gestational age (AGA), multiple pregnancies and the results of ROP screening on refractive errors and the development of strabismus were evaluated by logistic regression analysis. The SGA and AGA groups were compared in terms of refractive errors and presence of strabismus. Results. Six hundred and eight children, including 317 (52.1%) males and 291 (47.9%) females, were included in the study. The mean GA was 31 ± 3 weeks (24-36), and the mean BW was 1505 ± 435 g (600-2460). The number of SGA-born children was 101 (16.6%). Manifest deviation was detected in 42 (5.6%) children, and optical correction was required in 101 (16.6%) children. Being an SGA infant and multiple pregnancies were risk factors for refractive errors requiring optical correction, and hyperopia (≥3.00 D) was found to be a risk factor for the development of strabismus in the multivariate regression analysis. Additionally, the SGA group was at high risk for strabismus, hyperopia, high astigmatism and the need for optical correction.Conclusions. We concluded that SGA seems to be associated with an increased risk of strabismus and a high refractive error. It should be taken into consideration during follow-up examinations of SGA infants

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1. O’Connor AR, Wilson CM, Fielder AR. Ophthalmological problems associated with preterm birth. Eye (Lond) 2007; 21: 1254-1260.

2. Al Oum M, Donati S, Cerri L, Agosti M, Azzolini C. Ocular alignment and refraction in preterm children at 1 and 6 years old. Clin Ophthalmol 2014; 8: 1263- 1268.

3. Choi MY, Park IK, Yu YS. Long term refractive outcome in eyes of preterm infants with and without retinopathy of prematurity: comparison of keratometric value, axial length, anterior chamber depth, and lens thickness. Br J Ophthalmol 2000; 84: 138-143.

4. O’Connor AR, Stephenson TJ, Johnson A, Tobin MJ, Ratib S, Fielder AR. Strabismus in children of birth weight less than 1701 g. Arch Ophthalmol 2002; 120: 767-773.

5. Cotter SA, Varma R, Tarczy-Hornoch K, et al; Joint Writing Committee for the Mul-ti-Ethnic Pediatric Eye Disease Study and the Baltimore Pediatric Eye Disease Study Groups Risk factors associated with childhood strabismus: the multi-ethnic pediatric eye disease and Baltimore pediatric eye disease studies. Ophthalmology 2011; 118: 2251-2261.

6. Gulati S, Andrews CA, Apkarian AO, Musch DC, Lee PP, Stein JD. Effect of gestational age and birth weight on the risk of strabismus among premature infants. JAMA Pediatr 2014; 168: 850-856.

7. Holmstrom M, el Azazi M, Kugelberg U. Ophthalmological long-term follow up of preterm infants: a population based, prospective study of the refraction and its development. Br J Ophthalmol 1998; 82: 1265-1271.

8. Saw SM, Tong L, Chia KS, et al. The relation between birth size and the results of refractive error and biometry measurements in children. Br J Ophthalmol 2004; 88: 538-542.

9. Lim LS, Chua S, Tan PT, et al. Eye size and shape in newborn children and their relation to axial length and refraction at 3 years. Ophthal Physl Opt 2015; 35: 414-423.

10. Mutti DO, Mitchell GL, Jones LA, et al. Axial growth and changes in lenticular and corneal power during emmetropization in infants. Invest Ophthalmol Vis Sci 2005; 46: 3074-3080.

11. Boghossian NS, Geraci M, Edwards EM, Horbar JD. Morbidity and mortality in small for gestational age infants at 22 to 29 weeks’ gestation. Pediatrics 2018; 141: e20172533.

12. Qiu X, Lodha A, Shah PS, et al; Canadian Neonatal Network Neonatal outcomes of small for gestational age preterm infants in Canada. Am J Perinatol 2012; 29: 87-94.

13. Allegaert K, Vanhole C, Casteels I, et al. Perinatal growth characteristics and associated risk of developing threshold retinopathy of prematurity. J AAPOS 2003; 7: 34-37.

14. Kavurt S, Ozcan B, Aydemir O, Bas AY, Demirel N. Risk of retinopathy of prematurity in small for gestational age premature infants. Indian Pediatr 2014; 51: 804-806.

15. Bardin C, Piuze G, Papageorgiou A. Outcome at 5 years of age of SGA and AGA infants born less than 28 weeks of gestation. Semin Perinatol 2004; 28: 288- 294.

16. Zhao M, Dai H, Deng Y, Zhao L. SGA as a risk factor for cerebral palsy in moderate to late preterm infants: a system review and meta-analysis. Sci Rep 2016; 6: 38853.

17. Stoknes M, Andersen GL, Dahlseng MO, et al. Cerebral palsy and neonatal death in term singletons born small for gestational age. Pediatrics 2012; 130: e1629-e1635.

18. Pinello L, Manea S, Visona Dalla Pozza L, Mazzarolo M, Facchin P. Visual, motor, and psychomotor development in small-for-gestational-age preterm infants. J AAPOS 2013; 17: 352-356.

19. Lindström L, Wikström AK, Bergman E, Lundgren M. Born small for gestational age and poor school performance - how small is too small? Horm Res Paediatr 2017; 88: 215-223.

20. Gur Z, Tsumi E, Wainstock T, Walter E, Sheiner E. Association between delivery of small-forgestational age neonate and long-term pediatric ophthalmic morbidity. Arch Gynecol Obstet 2018; 298: 1095-1099.

21. Akova-Budak B, Kivanc SA, Olcaysu OO. Association of birth parameters with refractive status in a sample of caucasian children aged 4-17 years. J Ophthalmol 2015; 2015: 635682.

22. Lindqvist S, Vik T, Indredavik MS, Brubakk AM. Visual acuity, contrast sensitivity, peripheral vision and refraction in low birthweight teenagers. Acta Ophthalmol Scand 2007; 85: 157-164.

23. Rutstein RP, Wesson MD, Gotlieb S, Biasini FJ. Clinical comparison of the visual parameters in infants with intrauterine growth retardation vs. Infants with normal birth weight. Am J Optom Physiol Opt 1986; 63: 697-701.

24. Lindqvist S, Vik T, Indredavik MS, Skranes J, Brubakk AM. Eye movements and binocular function in low birthweight teenagers. Acta Ophthalmol 2008; 86: 265-274.

25. Evensen KA, Lindqvist S, Indredavik MS, Skranes J, Brubakk AM, Vik T. Do visual impairments affect risk of motor problems in preterm and term low birth weight adolescents? Eur J Paediatr Neurol 2009; 13: 47-56.

26. Ulusal görme taraması rehberi. Sağlık Bakanlığı (Ministry of Health) https://dosyamerkez.saglik.gov. tr/eklenti/31819,ulusal-gorme-taramasek63667410- 5c05-4899-99f9-d5c20a336709pdf.Pdf?0 Published 2019. (Accessed 4 February 2020).

27. Grossman DC, Curry SJ, Owens DK, et al; US Preventive Services Task Force. Vision screening in children aged 6 months to 5 years: US preventive services task force recommendation statement. JAMA 2017; 318: 836-844.

28. Wallace DK, Morse CL, Melia M, et al; American Academy of Ophthalmology Pre-ferred Practice Pattern Pediatric Ophthalmology/Strabismus Panel Pediatric eye evaluations preferred practice pattern(r): I. Vision screening in the primary care and community setting; II. comprehensive ophthalmic examination. Ophthalmology 2018; 125: P184-P227.

29. Fenton TR, Kim JH. A systematic review and metaanalysis to revise the Fenton growth chart for preterm infants. BMC Pediatr 2013; 13: 59.

30. International Committee for the Classification of Retinopathy of Prematurity. The international classification of retinopathy of prematurity revisited. Arch Ophthalmol 2005; 123: 991-999.

31. Schalij-Delfos NE, de Graaf ME, Treffers WF, Engel J, Cats BP. Long term follow up of premature infants: detection of strabismus, amblyopia, and refractive errors. Br J Ophthalmol 2000; 84: 963-967.

32. Özdemir M, Koylu S. Ocular growth and morbidity in preterm children without retinopathy of prematurity. Jpn J Ophthalmol 2009; 53: 623-628.

33. Perez-Roche T, Altemir I, Gimenez G, et al. Effect of prematurity and low birth weight in visual abilities and school performance. Res Dev Disabil 2016; 59: 451-457.

34. Perez-Roche T, Altemir I, Gimenez G, et al. Face recognition impairment in small for gestational age and preterm children. Res Dev Disabil 2017; 62: 166- 173.

35. Ley D, Marsal K, Dahlgren J, Hellstrom A. Abnormal retinal optic nerve morphology in young adults after intrauterine growth restriction. Pediatr Res 2004; 56: 139-143.

36. Thordstein CM, Sultan BL, Wennergren MM, Törnqvist E, Lindecrantz KG, Kjellmer I. Visual evoked potentials in disproportionately growthretarded human neonates. Pediatr Neurol 2004; 30: 262-270.

37. 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.e1-e2.

38. Multi-ethnic Pediatric Eye Disease Study G. 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.

39. Pathai S, Cumberland PM, Rahi JS. Prevalence of and early-life influences on childhood strabismus: findings from the millennium cohort study. Arch Pediatr Adolesc Med 2010; 164: 250-257.

40. Robaei D, Kifley A, Gole GA, Mitchell P. The impact of modest prematurity on visual function at age 6 years: findings from a population-based study. Arch Ophthalmol 2006; 124: 871-877.

41. Fieß A, Kölb-Keerl R, Schuster AK, et al. Prevalence and associated factors of strabismus in former preterm and full-term infants between 4 and 10 years of age. BMC Ophthalmol 2017; 17: 228.

42. Bruce A, Santorelli G. Prevalence and risk factors of strabismus in a UK multi-ethnic birth cohort. Strabismus 2016; 24: 153-160.

43. Ip JM, Robaei D, Kifley A, Wang JJ, Rose KA, Mitchell P. Prevalence of hyperopia and associations with eye findings in 6- and 12-year-olds. Ophthalmology 2008; 115: 678-685. e1.

44. Fierson WM; American Academy of Pediatrics Section on Ophthalmology; American Academy of Ophthalmology; American Association for Pediatric Ophthalmology and Strabismus; American Association of Certified Orthoptists. Screening examination of premature infants for retinopathy of prematurity. Pediatrics 2018; 142: e20183061. Pediatrics 2019; 143: e20183810