{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T14:26:14Z","timestamp":1790778374932,"version":"4.1.0"},"reference-count":38,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2022,4,11]],"date-time":"2022-04-11T00:00:00Z","timestamp":1649635200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"French Equipex Program of Investments in the Future","award":["ANR-11-EQPX-0038"],"award-info":[{"award-number":["ANR-11-EQPX-0038"]}]},{"DOI":"10.13039\/501100004431","name":"Fondation de France","doi-asserted-by":"publisher","award":["reference 11779"],"award-info":[{"award-number":["reference 11779"]}],"id":[{"id":"10.13039\/501100004431","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>We report the 51\/2 year prevalence of visual and oculomotor impairments in preterm children born at 24\u201334 weeks\u2019 gestation (WG) using the population-based cohort study EPIPAGE-2, set in France, 2011. The main outcomes were imputed prevalence of refractive errors (REs), strabismus, and binocular visual acuity (VA). Children were clinically assessed by specially trained pediatricians. The population was also analyzed in terms of cerebral palsy at 51\/2 years (no CP, stage 1, stage 2, or stage 3\u20135) and retinopathy of prematurity in the neonatal period (no ROP, stage 1 or 2, or severe ROP). Among the 4441 children included, 2718 (weighted percentage 58.7%) were clinically assessed. REs were reported in 43.1% (95% confidence interval 37.6\u201348.4), 35.2% (32.7\u201337.6), and 28.4% (25.0\u201331.8) of children born at 24\u201326, 27\u201331, and 32\u201334 WG (p &lt; 0.01), respectively; strabismus rates were 19.5% (14.6\u201324.4), 14.8% (12.9\u201316.7), and 8.3% (6.2\u201310.4) (p &lt; 0.001), respectively. Moderate\/severe visual deficiencies (VA &lt; 3.2\/10) were present in 1.7% (0.2\u20133.3) of children born at 24\u201326 WG, and in less than 1% in other groups. A suboptimal VA 5\/10\u20136.3\/10 was measured in 40.6% (35.3\u201345.8) of children born at 24\u201326 WG, 35.8% (33.5\u201338.1) at 27\u201331 WG, and 33.7% (30.4\u201337.0) at 32\u201334 WG. CP and ROP were associated with strabismus and RE. The association between CP and VA was strong, while it was not observed for ROP. In this large cohort of preterm-born children, we found a high prevalence of RE and strabismus regardless of WG, supporting the need for specific attention in this population. High prevalence of suboptimal VA could be challenging for these children at the age of reading and writing acquisition.<\/jats:p>","DOI":"10.3390\/jcm11082139","type":"journal-article","created":{"date-parts":[[2022,4,12]],"date-time":"2022-04-12T02:48:59Z","timestamp":1649731739000},"page":"2139","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["Ophthalmological Impairments at Five and a Half Years after Preterm Birth: EPIPAGE-2 Cohort Study"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5082-230X","authenticated-orcid":false,"given":"Thibaut","family":"Chapron","sequence":"first","affiliation":[{"name":"CRESS, Obstetrical Perinatal and Pediatric Epidemiology Research Team, EPOP\u00e9, INSERM, INRAE, Universit\u00e9 Paris Cit\u00e9, 75004 Paris, France"},{"name":"Pediatric Ophthalmology Department, Rothschild Foundation Hospital, 25 rue Manin, CEDEX 19, 75940 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"V\u00e9ronique","family":"Pierrat","sequence":"additional","affiliation":[{"name":"CRESS, Obstetrical Perinatal and Pediatric Epidemiology Research Team, EPOP\u00e9, INSERM, INRAE, Universit\u00e9 Paris Cit\u00e9, 75004 Paris, France"},{"name":"CHU Lille, Department of Neonatal Medicine, Jeanne de Flandre Hospital, 59000 Lille, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Georges","family":"Caputo","sequence":"additional","affiliation":[{"name":"Pediatric Ophthalmology Department, Rothschild Foundation Hospital, 25 rue Manin, CEDEX 19, 75940 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0577-4251","authenticated-orcid":false,"given":"Mathilde","family":"Letouzey","sequence":"additional","affiliation":[{"name":"CRESS, Obstetrical Perinatal and Pediatric Epidemiology Research Team, EPOP\u00e9, INSERM, INRAE, Universit\u00e9 Paris Cit\u00e9, 75004 Paris, France"},{"name":"Department of Neonatal Medicine, Poissy Saint Germain Hospital, 78300 Poissy, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elsa","family":"Kermorvant-Duchemin","sequence":"additional","affiliation":[{"name":"Department of Neonatal Medicine, Necker\u2013Enfants Malades University Hospital, AP-HP, Universit\u00e9 Paris Cit\u00e9, 75015 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9887-0992","authenticated-orcid":false,"given":"Youssef","family":"Abdelmassih","sequence":"additional","affiliation":[{"name":"Pediatric Ophthalmology Department, Rothschild Foundation Hospital, 25 rue Manin, CEDEX 19, 75940 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"William","family":"Beaumont","sequence":"additional","affiliation":[{"name":"Pediatric Ophthalmology Department, Rothschild Foundation Hospital, 25 rue Manin, CEDEX 19, 75940 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amandine","family":"Barjol","sequence":"additional","affiliation":[{"name":"Pediatric Ophthalmology Department, Rothschild Foundation Hospital, 25 rue Manin, CEDEX 19, 75940 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guylene","family":"Le Meur","sequence":"additional","affiliation":[{"name":"Clinique Ophtalmologique, CHU Nantes, 1 Place Alexis Ricordeau, CEDEX 1, 44093 Nantes, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Val\u00e9rie","family":"Benhamou","sequence":"additional","affiliation":[{"name":"CRESS, Obstetrical Perinatal and Pediatric Epidemiology Research Team, EPOP\u00e9, INSERM, INRAE, Universit\u00e9 Paris Cit\u00e9, 75004 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laetitia","family":"Marchand-Martin","sequence":"additional","affiliation":[{"name":"CRESS, Obstetrical Perinatal and Pediatric Epidemiology Research Team, EPOP\u00e9, INSERM, INRAE, Universit\u00e9 Paris Cit\u00e9, 75004 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pierre-Yves","family":"Ancel","sequence":"additional","affiliation":[{"name":"CRESS, Obstetrical Perinatal and Pediatric Epidemiology Research Team, EPOP\u00e9, INSERM, INRAE, Universit\u00e9 Paris Cit\u00e9, 75004 Paris, France"},{"name":"Clinical Research Unit, Center for Clinical Investigation P1419, APHP, CUP, 75014 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"H\u00e9lo\u00efse","family":"Torchin","sequence":"additional","affiliation":[{"name":"CRESS, Obstetrical Perinatal and Pediatric Epidemiology Research Team, EPOP\u00e9, INSERM, INRAE, Universit\u00e9 Paris Cit\u00e9, 75004 Paris, France"},{"name":"Department of Neonatal Medicine, Cochin-Port Royal Hospital, FHU PREMA, AP-HP Centre, 75014 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,4,11]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"n741","DOI":"10.1136\/bmj.n741","article-title":"Neurodevelopmental outcomes at age 5 among children born preterm: EPIPAGE-2 cohort study","volume":"373","author":"Pierrat","year":"2021","journal-title":"BMJ"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1136\/archdischild-2015-309581","article-title":"Early and long-term outcome of infants born extremely preterm","volume":"102","author":"Johnson","year":"2016","journal-title":"Arch. Dis. Child."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1111\/1471-0528.14832","article-title":"Cognitive, motor, behavioural and academic performances of children born preterm: A meta-analysis and systematic review involving 64 061 children","volume":"125","author":"Allotey","year":"2017","journal-title":"BJOG Int. J. Obstet. Gynaecol."},{"key":"ref_4","first-page":"1","article-title":"Vision Abnormalities in Children and Young Adults with Cerebral Palsy; A Systematic Review","volume":"3","author":"Heydarian","year":"2022","journal-title":"Semin. Ophthalmol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"250","DOI":"10.1001\/archpediatrics.2009.297","article-title":"Prevalence of and Early-Life Influences on Childhood Strabismus","volume":"164","author":"Pathai","year":"2010","journal-title":"Arch. Pediatr. Adolesc. Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1001\/jamaophthalmol.2016.0391","article-title":"Ophthalmologic Outcome of Extremely Preterm Infants at 6.5 Years of Age","volume":"134","author":"Hellgren","year":"2016","journal-title":"JAMA Ophthalmol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1177\/0883073815599258","article-title":"Strabismus at Age 2 Years in Children Born before 28 Weeks\u2019 Gestation","volume":"31","author":"VanderVeen","year":"2015","journal-title":"J. Child Neurol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1001\/jamaophthalmol.2019.4502","article-title":"Individual Risk Prediction for Sight-Threatening Retinopathy of Prematurity Using Birth Characteristics","volume":"138","author":"Pivodic","year":"2020","journal-title":"JAMA Ophthalmol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"822","DOI":"10.1111\/apa.14209","article-title":"Impaired cognitive ability at 2.5 years predicts later visual and ophthalmological problems in children born very preterm","volume":"107","author":"Hreinsdottir","year":"2017","journal-title":"Acta Paediatr."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1136\/bjo.2005.081653","article-title":"Contrast sensitivity in 10 year old preterm and full term children: A population based study","volume":"90","author":"Larsson","year":"2006","journal-title":"Br. J. Ophthalmol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.earlhumdev.2007.11.005","article-title":"Long term ophthalmic sequelae of prematurity","volume":"84","author":"Fielder","year":"2008","journal-title":"Early Hum. Dev."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Williams, C., Northstone, K., Sabates, R., Feinstein, L., Emond, A., and Dutton, G.N. (2011). Visual Perceptual Difficulties and Under-Achievement at School in a Large Community-Based Sample of Children. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0014772"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1167\/iovs.07-0869","article-title":"The Effect of Amblyopia on Fine Motor Skills in Children","volume":"49","author":"Webber","year":"2008","journal-title":"Investig. Opthalmology Vis. Sci."},{"key":"ref_14","unstructured":"(2022, January 15). D\u00e9ficits Visuels: D\u00e9pistage et Prise en Charge chez le Jeune Enfant. Rapport 2002, Available online: http:\/\/hdl.handle.net\/10608\/163."},{"key":"ref_15","unstructured":"(2022, January 28). Healthy Child Programme: Pregnancy and the First 5 Years of Life. GOV.UK, Available online: https:\/\/www.gov.uk\/government\/publications\/healthy-child-programme-pregnancy-and-the-first-5-years-of-life."},{"key":"ref_16","unstructured":"(2018, September 18). Recommandations Fran\u00e7aises pour le Depistage de la Retinopathie des Prematures-pdf. Available online: https:\/\/docplayer.fr\/19824265-Recommandations-francaises-pour-le-depistage-de-la-retinopathie-des-prematures.html."},{"key":"ref_17","unstructured":"NICE Guideline (2022, January 15). Development Follow-Up of Children and Young People Born Preterm, Available online: https:\/\/www.nice.org.uk\/guidance\/ng72."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Ancel, P.-Y., and Goffinet, F. (2014). EPIPAGE 2: A preterm birth cohort in France in 2011. BMC Pediatr., 14.","DOI":"10.1186\/1471-2431-14-97"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1428","DOI":"10.1093\/ije\/dyaa282","article-title":"Cohort Profile: The Etude Epid\u00e9miologique sur les Petits Ages Gestationnels-2 (EPIPAGE-2) preterm birth cohort","volume":"50","author":"Lorthe","year":"2021","journal-title":"Int. J. Epidemiology"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"j3448","DOI":"10.1136\/bmj.j3448","article-title":"Neurodevelopmental outcome at 2 years for preterm children born at 22 to 34 weeks\u2019 gestation in France in 2011: EPIPAGE-2 cohort study","volume":"358","author":"Pierrat","year":"2017","journal-title":"BMJ"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1093\/ije\/dyz227","article-title":"Cohort Profile: The French national cohort of children (ELFE): Birth to 5 years","volume":"49","author":"Charles","year":"2020","journal-title":"Int. J. Epidemiol."},{"key":"ref_22","first-page":"199","article-title":"Comparaison de deux \u00e9chelles logarithmique d\u2019acuit\u00e9 visuelle de loin pour l\u2019enfant: Rossano et Sander-Zanlonghi","volume":"31","author":"Zanlonghi","year":"1999","journal-title":"J. Fran\u00e7ais Orthopt."},{"key":"ref_23","unstructured":"(2021, September 16). Vision impairment and Blindness. Available online: https:\/\/www.who.int\/news-room\/fact-sheets\/detail\/blindness-and-visual-impairment."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1016\/j.siny.2007.07.001","article-title":"Visual Outcomes and Perinatal Adversity","volume":"12","author":"Fielder","year":"2007","journal-title":"Semin. Fetal. Neonatal. Med."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/j.jgyn.2015.08.008","article-title":"Customized and non-customized French intrauterine growth curves. II\u2014Comparison with existing curves and benefits of customization","volume":"45","author":"Ego","year":"2015","journal-title":"J. Gynecol. Obstet. Biol. Reprod."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1001\/jamapediatrics.2014.3351","article-title":"Survival and Morbidity of Preterm Children Born at 22 Through 34 Weeks\u2019 Gestation in France in 2011: Results of the EPIPAGE-2 Cohort Study","volume":"169","author":"Ancel","year":"2015","journal-title":"JAMA Pediatr."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"International Committee for the Classification of Retinopathy of Prematurity (2005). The International Classification of Retinopathy of Prematurity revisited. Arch. Ophthalmol., 123, 991\u2013999.","DOI":"10.1001\/archopht.123.7.991"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"e20154372","DOI":"10.1542\/peds.2015-4372","article-title":"Gross Motor Milestones and Subsequent Development","volume":"138","author":"Ghassabian","year":"2016","journal-title":"Pediatrics"},{"key":"ref_29","unstructured":"Brown, T. (2013). Movement Assessment Battery for Children: 2nd Edition (MABC-2). Encyclopedia of Autism Spectrum Disorders, Springer."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1159\/000513225","article-title":"Screening for Retinopathy of Prematurity in Very Preterm Children: The EPIPAGE-2 Cohort Study","volume":"118","author":"Chapron","year":"2021","journal-title":"Neonatology"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1002\/sim.4067","article-title":"Multiple imputation using chained equations: Issues and guidance for practice","volume":"30","author":"White","year":"2010","journal-title":"Stat. Med."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Rubin, D.B. (1987). Frontmatter. Multiple Imputation for Nonresponse in Surveys, John Wiley & Sons, Inc.","DOI":"10.1002\/9780470316696"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.ajo.2020.06.001","article-title":"Effect of Prematurity on Foveal Development in Early School-Age Children","volume":"219","author":"Demir","year":"2020","journal-title":"Am. J. Ophthalmol."},{"key":"ref_34","first-page":"541","article-title":"Visual function is reduced in young adults formerly born prematurely: A population-based study","volume":"104","author":"Larsson","year":"2019","journal-title":"Br. J. Ophthalmol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2233","DOI":"10.1097\/IAE.0000000000002301","article-title":"Visual Function and Optical Coherence Tomography Angiography Features in Children Born Preterm","volume":"39","author":"Balasubramanian","year":"2019","journal-title":"Retina"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Tremblay, E., Vannasing, P., Roy, M.-S., Lefebvre, F., Kombate, D., Lassonde, M., Lepore, F., McKerral, M., and Gallagher, A. (2014). Delayed Early Primary Visual Pathway Development in Premature Infants: High Density Electrophysiological Evidence. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0107992"},{"key":"ref_37","unstructured":"(2021, September 16). Assessment of Visual Function\u2014EFCNI. Available online: https:\/\/newborn-health-standards.org\/assessment-visual-function\/."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1111\/j.1469-8749.1994.tb11760.x","article-title":"Relation between neonatal cranial ultrasound abnormalities and cerebral visual impairment in infancy","volume":"36","author":"Eken","year":"1994","journal-title":"Dev. Med. Child. Neurol"}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/11\/8\/2139\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:52:04Z","timestamp":1760136724000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/11\/8\/2139"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,4,11]]},"references-count":38,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2022,4]]}},"alternative-id":["jcm11082139"],"URL":"https:\/\/doi.org\/10.3390\/jcm11082139","relation":{},"ISSN":["2077-0383"],"issn-type":[{"value":"2077-0383","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,4,11]]}}}