{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,2]],"date-time":"2026-09-02T12:13:04Z","timestamp":1788351184051,"version":"build-2803163510"},"reference-count":36,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2022,5,2]],"date-time":"2022-05-02T00:00:00Z","timestamp":1651449600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>Objective: To investigate whether there is a linear association between the degree of prematurity and the risk for long-term ophthalmic morbidity among preterm infants. Study design: A population-based, retrospective cohort study, which included all singleton deliveries occurring between 1991 and 2014 at a single tertiary medical center. All infants were divided into four groups according to gestational age categories: extremely preterm births, very preterm births, moderate to late preterm births and term deliveries (reference group). Hospitalizations of offspring up to 18 years of age involving ophthalmic morbidity were evaluated. Survival curves compared cumulative hospitalizations and regression models controlled for confounding variables. Results: During the study period, 243,363 deliveries met the inclusion criteria. Ophthalmic-related hospitalization rates were lower among children born at term (0.9%) as compared with extremely preterm (3.6%), very preterm (2%), and moderate to late preterm (1.4%) born offspring (p &lt; 0.01; using the chi-square test for trends). The survival curve demonstrated significantly different hospitalization rates between the gestational ages (p &lt; 0.001). The regression demonstrated an independent risk for ophthalmic morbidity among extremely preterm born offspring (adjusted hazard ratio 3.8, confidence interval 1.6\u20139.2, p &lt; 0.01), as well as very preterm and moderate to late preterm (adjusted hazard ratio 2.2 and 1.5, respectively) as compared with term deliveries. Conclusions: The risk for long-term ophthalmic-related hospitalization of preterm offspring gradually decreases as the gestational age increases.<\/jats:p>","DOI":"10.3390\/jcm11092562","type":"journal-article","created":{"date-parts":[[2022,5,3]],"date-time":"2022-05-03T08:26:35Z","timestamp":1651566395000},"page":"2562","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["The Association between Gestational Age and Risk for Long Term Ophthalmic Morbidities among Offspring Delivered in Different Preterm Subgroups"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8148-6561","authenticated-orcid":false,"given":"Erez","family":"Tsumi","sequence":"first","affiliation":[{"name":"Department of Ophthalmology, Soroka University Medical Center, Ben-Gurion University of the Negev, Beer-Sheva 8410101, Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6064-6909","authenticated-orcid":false,"given":"Itai","family":"Hazan","sequence":"additional","affiliation":[{"name":"Joyce and Irving Goldman Medical School, Faculty of Health Sciences, Ben-Gurion University of the Negev, Beer-Sheva 8410501, Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tamir","family":"Regev","sequence":"additional","affiliation":[{"name":"Department of Ophthalmology, Soroka University Medical Center, Ben-Gurion University of the Negev, Beer-Sheva 8410101, Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3496-3927","authenticated-orcid":false,"given":"Samuel","family":"Leeman","sequence":"additional","affiliation":[{"name":"Department of Ophthalmology, Soroka University Medical Center, Ben-Gurion University of the Negev, Beer-Sheva 8410101, Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chiya","family":"Barrett","sequence":"additional","affiliation":[{"name":"Department of Ophthalmology, Soroka University Medical Center, Ben-Gurion University of the Negev, Beer-Sheva 8410101, Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Noa","family":"Fried Regev","sequence":"additional","affiliation":[{"name":"Department of Emergency Medicine, Soroka University Medical Center, Ben-Gurion University of the Negev, Beer-Sheva 8410101, Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0454-6874","authenticated-orcid":false,"given":"Eyal","family":"Sheiner","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Soroka University Medical Center, Ben-Gurion University of the Negev, Beer-Sheva 8410101, Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,5,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1007\/s00404-008-0836-8","article-title":"Neonatal outcome in preterm deliveries between 23 and 27 weeks\u2019 gestation with and without preterm premature rupture of membranes","volume":"280","author":"Newman","year":"2009","journal-title":"Arch. Gynecol. Obstet."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1016\/j.clp.2013.07.006","article-title":"Long-term outcomes of moderately preterm, late preterm, and early term infants","volume":"40","author":"Vohr","year":"2013","journal-title":"Clin. Perinatol."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Gutvirtz, G., Wainstock, T., Sheiner, E., and Pariente, G. (2022). Prematurity and Long-Term Respiratory Morbidity\u2014What Is the Critical Gestational Age Threshold?. J. Clin. Med., 11.","DOI":"10.3390\/jcm11030751"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Davidesko, S., Wainstock, T., Sheiner, E., and Pariente, G. (2020). Long-Term Infectious Morbidity of Premature Infants: Is There a Critical Threshold?. J. Clin. Med., 9.","DOI":"10.3390\/jcm9093008"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Zer, S., Wainstock, T., Sheiner, E., Miodownik, S., and Pariente, G. (2021). Identifying the Critical Threshold for Long-Term Pediatric Neurological Hospitalizations of the Offspring in Preterm Delivery. J. Clin. Med., 10.","DOI":"10.3390\/jcm10132919"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"101109","DOI":"10.1016\/j.siny.2020.101109","article-title":"International comparisons of neurodevelopmental outcomes in infants born very preterm","volume":"25","author":"Torchin","year":"2020","journal-title":"Semin. Fetal. Neonatal Med."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1053\/j.semperi.2016.09.002","article-title":"Early neurodevelopmental outcomes of extremely preterm infants","volume":"40","author":"Rogers","year":"2016","journal-title":"Semin. Perinatol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1254","DOI":"10.1038\/sj.eye.6702838","article-title":"Ophthalmological problems associated with preterm birth","volume":"21","author":"Wilson","year":"2007","journal-title":"Eye"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1111\/cxo.12578","article-title":"The effects of preterm birth on visual development","volume":"101","author":"Leung","year":"2018","journal-title":"Clin. Exp. Optom."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1016\/j.clp.2011.06.011","article-title":"Outcomes of Preterm Infants: Morbidity Replaces Mortality","volume":"38","author":"Allen","year":"2011","journal-title":"Clin. Perinatol."},{"key":"ref_11","unstructured":"(2021, November 16). Preterm Birth. Available online: https:\/\/www.who.int\/news-room\/fact-sheets\/detail\/preterm-birth."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Ben-Shmuel, A., Sheiner, E., Tsumi, E., Wainstock, T., Feinblum, D., and Walfisch, A. (2021). Early-term deliveries and long-term pediatric ophthalmic morbidity of the offspring. Int. J. Gynaecol. Obstet. Off. Organ Int. Fed. Gynaecol. Obstet., 1\u20137.","DOI":"10.1016\/j.ajog.2019.11.306"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1080\/01443610120071974","article-title":"Lack of prenatal care in two different societies living in the same region and sharing the same medical facilities","volume":"21","author":"Sheiner","year":"2001","journal-title":"J. Obstet. Gynaecol. J. Inst. Obstet. Gynaecol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1002\/ijgo.12314","article-title":"The association between inadequate prenatal care and future healthcare use among offspring in the Bedouin population","volume":"139","author":"Sheiner","year":"2017","journal-title":"Int. J. Gynaecol. Obstet. Off. Organ Int. Fed. Gynaecol. Obstet."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1237","DOI":"10.1007\/s00404-011-2153-x","article-title":"Lack of prenatal care in a traditional community: Trends and perinatal outcomes","volume":"285","author":"Sheiner","year":"2012","journal-title":"Arch. Gynecol. Obstet."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.jpeds.2015.10.028","article-title":"Survival, Hospitalization, and Acute-Care Costs of Very and Moderate Preterm Infants in the First 6 Years of Life: A Population-Based Study","volume":"169","author":"Stephens","year":"2016","journal-title":"J. Pediatr."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"101196","DOI":"10.1016\/j.siny.2021.101196","article-title":"Inter-center variability in neonatal outcomes of preterm infants: A longitudinal evaluation of 298 neonatal units in 11 countries","volume":"26","author":"Lui","year":"2021","journal-title":"Semin. Fetal. Neonatal Med."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1055\/s-0032-1316446","article-title":"Visual Function in Preterm Infants without Major Retinopathy of Prematurity or Neurological Complications","volume":"29","author":"Kozeis","year":"2012","journal-title":"Am. J. Perinatol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"79","DOI":"10.3389\/fnins.2013.00079","article-title":"The immune consequences of preterm birth","volume":"7","author":"Melville","year":"2013","journal-title":"Front. Neurosci."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1111\/j.1471-0528.2005.00578.x","article-title":"Role of cytokines in preterm labour and brain injury","volume":"112","author":"Hagberg","year":"2005","journal-title":"BJOG Int. J. Obstet. Gynaecol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2012\/561494","article-title":"The Role of Cytokines and Inflammatory Cells in Perinatal Brain Injury","volume":"2012","author":"McAdams","year":"2012","journal-title":"Neurol. Res. Int."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1053\/j.semperi.2008.09.009","article-title":"The Role of Transient Hypothyroxinemia of Prematurity in Development of Visual Abilities","volume":"32","author":"Rovet","year":"2008","journal-title":"Semin. Perinatol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"990","DOI":"10.1542\/peds.2004-1309","article-title":"Prenatal risk factors for severe retinopathy of prematurity among very preterm infants of the Australian and New Zealand Neonatal Network","volume":"115","author":"Darlow","year":"2005","journal-title":"Pediatrics"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"F240","DOI":"10.1136\/adc.2004.057570","article-title":"UK population based study of severe retinopathy of prematurity: Screening, treatment, and outcome","volume":"90","author":"Haines","year":"2005","journal-title":"Arch. Dis. Child. Fetal Neonatal Ed."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1317","DOI":"10.1016\/j.ophtha.2003.10.030","article-title":"Incidence of retinopathy of prematurity from 1996 to 2000: Analysis of a comprehensive New York state patient database","volume":"111","author":"Chiang","year":"2004","journal-title":"Ophthalmology"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"85","DOI":"10.3233\/NPM-915142","article-title":"Retinopathy of prematurity in Indonesia: Incidence and risk factors","volume":"10","author":"Sauer","year":"2017","journal-title":"J. Neonatal-Perinat. Med."},{"key":"ref_27","first-page":"204","article-title":"A proposal of screening guideline for retinopathy of prematurity in Taiwan","volume":"43","author":"Chiang","year":"2002","journal-title":"Acta Paediatr. Taiwanica Taiwan Er Ke Yi Xue Hui Za Zhi"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1038\/sj.eye.6701437","article-title":"Severe retinopathy of prematurity: Longitudinal observation of disease and screening implications","volume":"19","author":"Ells","year":"2005","journal-title":"Eye"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1470","DOI":"10.1001\/archopht.120.11.1470","article-title":"Evidence-Based Screening Criteria for Retinopathy of Prematurity: Natural History Data From the CRYO-ROP and LIGHT-ROP Studies","volume":"120","author":"Reynolds","year":"2002","journal-title":"Arch. Ophthalmol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1542\/peds.102.1.31","article-title":"Should Fewer Premature Infants Be Screened for Retinopathy of Prematurity in the Managed Care Era?","volume":"102","author":"Wright","year":"1998","journal-title":"Pediatrics"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"F251","DOI":"10.1136\/adc.2006.096479","article-title":"Severe retinopathy of prematurity in infants <30 weeks\u2019 gestation in New South Wales and the Australian Capital Territory from 1992 to 2002","volume":"92","author":"Todd","year":"2007","journal-title":"Arch. Dis. Child. Fetal Neonatal Ed."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1007\/BF01954508","article-title":"Hypothesis: Myopia of prematurity is caused by postnatal bone mineral deficiency","volume":"153","author":"Pohlandt","year":"1994","journal-title":"Eur. J. Pediatr."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"346","DOI":"10.3928\/01913913-20061101-04","article-title":"Prevalence and development of strabismus in 10-year-old premature children: A population-based study","volume":"43","author":"Rydberg","year":"2006","journal-title":"J. Pediatr. Ophthalmol. Strabismus"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1001\/archopht.116.3.329","article-title":"Strabismus in Premature Infants in the First Year of Life","volume":"116","author":"Bremer","year":"1998","journal-title":"Arch. Ophthalmol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"901","DOI":"10.1016\/j.ophtha.2003.07.017","article-title":"Tear function and ocular surface findings in premature and term babies","volume":"111","author":"Dogru","year":"2004","journal-title":"Ophthalmology"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"337","DOI":"10.3109\/09286580903144746","article-title":"Risk factors for neonatal conjunctivitis in babies of HIV-1 infected mothers","volume":"16","author":"Gichuhi","year":"2009","journal-title":"Ophthalmic Epidemiol."}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/11\/9\/2562\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:05:30Z","timestamp":1760137530000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/11\/9\/2562"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,5,2]]},"references-count":36,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2022,5]]}},"alternative-id":["jcm11092562"],"URL":"https:\/\/doi.org\/10.3390\/jcm11092562","relation":{},"ISSN":["2077-0383"],"issn-type":[{"value":"2077-0383","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,5,2]]}}}