{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,27]],"date-time":"2026-10-27T21:01:50Z","timestamp":1793134910988,"version":"4.5.0"},"reference-count":44,"publisher":"Springer Science and Business Media LLC","issue":"7","license":[{"start":{"date-parts":[[2019,4,1]],"date-time":"2019-04-01T00:00:00Z","timestamp":1554076800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"},{"start":{"date-parts":[[2019,4,1]],"date-time":"2019-04-01T00:00:00Z","timestamp":1554076800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"funder":[{"DOI":"10.13039\/100015521","name":"Stanford Maternal & Child Health Research Institute","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100015521","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100009633","name":"U.S. Department of Health & Human Services | NIH | Eunice Kennedy Shriver National Institute of Child Health and Human Development","doi-asserted-by":"publisher","award":["F32HD91945"],"award-info":[{"award-number":["F32HD91945"]}],"id":[{"id":"10.13039\/100009633","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["J Perinatol"],"published-print":{"date-parts":[[2019,7]]},"DOI":"10.1038\/s41372-019-0357-2","type":"journal-article","created":{"date-parts":[[2019,4,1]],"date-time":"2019-04-01T11:23:53Z","timestamp":1554117833000},"page":"964-973","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":43,"title":["Prenatal and postnatal inflammation-related risk factors for retinopathy of prematurity"],"prefix":"10.1038","volume":"39","author":[{"given":"Gregory P.","family":"Goldstein","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephanie A.","family":"Leonard","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peiyi","family":"Kan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Euna B.","family":"Koo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8383-1720","authenticated-orcid":false,"given":"Henry C.","family":"Lee","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Suzan L.","family":"Carmichael","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2019,4,1]]},"reference":[{"key":"357_CR1","doi-asserted-by":"publisher","first-page":"e164396","DOI":"10.1001\/jamapediatrics.2016.4396","volume":"171","author":"JD Horbar","year":"2017","unstructured":"Horbar JD, Edwards EM, Greenberg LT, Morrow KA, Soll RF, Buus-Frank ME, et al. Variation in performance of neonatal Intensive care units in the United States. JAMA Pediatr. 2017;171:e164396.","journal-title":"JAMA Pediatr"},{"key":"357_CR2","doi-asserted-by":"publisher","first-page":"663","DOI":"10.1001\/archophthalmol.2010.72","volume":"128","author":"WV Good","year":"2010","unstructured":"Early Treatment for Retinopathy of Prematurity Cooperative Group, Good WV, Hardy RJ, Dobson V, Palmer EA, Phelps DL, et al. Final visual acuity results in the early treatment for retinopathy of prematurity study. Arch Ophthalmol. 2010;128:663\u201371.","journal-title":"Arch Ophthalmol"},{"key":"357_CR3","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1007\/s10456-007-9066-0","volume":"10","author":"J Chen","year":"2007","unstructured":"Chen J, Smith LEH. Retinopathy of prematurity. Angiogenesis. 2007;10:133\u201340.","journal-title":"Angiogenesis"},{"key":"357_CR4","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1016\/j.siny.2011.08.007","volume":"17","author":"J Lee","year":"2012","unstructured":"Lee J, Dammann O. Perinatal infection, inflammation, and retinopathy of prematurity. Semin Fetal Neonatal Med. 2012;17:26\u20139.","journal-title":"Semin Fetal Neonatal Med"},{"key":"357_CR5","doi-asserted-by":"publisher","first-page":"2515","DOI":"10.1056\/NEJMra1208129","volume":"367","author":"ME Hartnett","year":"2012","unstructured":"Hartnett ME, Penn JS. Mechanisms and management of retinopathy of prematurity. N Engl J Med. 2012;367:2515\u201326.","journal-title":"N Engl J Med"},{"key":"357_CR6","doi-asserted-by":"publisher","DOI":"10.1186\/s12974-017-0943-1","volume":"14","author":"JC Rivera","year":"2017","unstructured":"Rivera JC, Holm M, Austeng D, Morken TS, Zhou TE, Beaudry-Richard A, et al. Retinopathy of prematurity: inflammation, choroidal degeneration, and novel promising therapeutic strategies. J Neuroinflamm. 2017;14:165.","journal-title":"J Neuroinflamm"},{"key":"357_CR7","doi-asserted-by":"publisher","first-page":"e12986","DOI":"10.1111\/aji.12986","volume":"1989","author":"AM Lynch","year":"2018","unstructured":"Lynch AM, Berning AA, Thevarajah TS, Wagner BD, Post MD, McCourt EA, et al. The role of the maternal and fetal inflammatory response in retinopathy of prematurity. Am J Reprod Immunol. 2018;1989:e12986.","journal-title":"Am J Reprod Immunol"},{"key":"357_CR8","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-018-30087-4","volume":"8","author":"A Beaudry-Richard","year":"2018","unstructured":"Beaudry-Richard A, Nadeau-Vall\u00e9e M, Prairie \u00c9, Maurice N, Heckel \u00c9, Nezhady M, et al. Antenatal IL-1-dependent inflammation persists postnatally and causes retinal and sub-retinal vasculopathy in progeny. Sci Rep. 2018;8:11875.","journal-title":"Sci Rep"},{"key":"357_CR9","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1002\/iub.1358","volume":"67","author":"A Szade","year":"2015","unstructured":"Szade A, Grochot-Przeczek A, Florczyk U, Jozkowicz A, Dulak J. Cellular and molecular mechanisms of inflammation-induced angiogenesis. IUBMB Life. 2015;67:145\u201359.","journal-title":"IUBMB Life"},{"key":"357_CR10","doi-asserted-by":"publisher","first-page":"818","DOI":"10.1111\/apm.12223","volume":"122","author":"H Yu","year":"2014","unstructured":"Yu H, Yuan L, Zou Y, Peng L, Wang Y, Li T, et al. Serum concentrations of cytokines in infants with retinopathy of prematurity. APMIS Acta Pathol Microbiol Immunol Scand. 2014;122:818\u201323.","journal-title":"APMIS Acta Pathol Microbiol Immunol Scand"},{"key":"357_CR11","doi-asserted-by":"publisher","first-page":"637","DOI":"10.1016\/S0002-9440(10)62284-5","volume":"166","author":"TA Gardiner","year":"2005","unstructured":"Gardiner TA, Gibson DS, de Gooyer TE, de la Cruz VF, McDonald DM, Stitt AW. Inhibition of tumor necrosis factor-alpha improves physiological angiogenesis and reduces pathological neovascularization in ischemic retinopathy. Am J Pathol. 2005;166:637\u201344.","journal-title":"Am J Pathol"},{"key":"357_CR12","doi-asserted-by":"publisher","DOI":"10.1186\/1742-2094-11-87","volume":"11","author":"HK Hong","year":"2014","unstructured":"Hong HK, Lee HJ, Ko JH, Park JH, Park JY, Choi CW, et al. Neonatal systemic inflammation in rats alters retinal vessel development and simulates pathologic features of retinopathy of prematurity. J Neuroinflamm. 2014;11:87.","journal-title":"J Neuroinflamm"},{"key":"357_CR13","doi-asserted-by":"publisher","first-page":"8125","DOI":"10.1167\/iovs.13-12496","volume":"54","author":"S Tremblay","year":"2013","unstructured":"Tremblay S, Miloudi K, Chaychi S, Favret S, Binet F, Polosa A, et al. Systemic inflammation perturbs developmental retinal angiogenesis and neuroretinal function. Invest Ophthalmol Vis Sci. 2013;54:8125\u201339.","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"357_CR14","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1159\/000320170","volume":"99","author":"W Thomas","year":"2011","unstructured":"Thomas W, Speer CP. Chorioamnionitis: important risk factor or innocent bystander for neonatal outcome? Neonatology. 2011;99:177\u201387.","journal-title":"Neonatology"},{"key":"357_CR15","doi-asserted-by":"publisher","first-page":"125.e1","DOI":"10.1016\/j.ajog.2013.11.032","volume":"210","author":"CA Combs","year":"2014","unstructured":"Combs CA, Gravett M, Garite TJ, Hickok DE, Lapidus J, Porreco R, et al. Amniotic fluid infection, inflammation, and colonization in preterm labor with intact membranes. Am J Obstet Gynecol. 2014;210:125.e1\u201315.","journal-title":"Am J Obstet Gynecol"},{"key":"357_CR16","doi-asserted-by":"publisher","first-page":"675","DOI":"10.1067\/mob.2000.104207","volume":"182","author":"BH Yoon","year":"2000","unstructured":"Yoon BH, Romero R, Park JS, Kim CJ, Kim SH, Choi JH, et al. Fetal exposure to an intra-amniotic inflammation and the development of cerebral palsy at the age of three years. Am J Obstet Gynecol. 2000;182:675\u201381.","journal-title":"Am J Obstet Gynecol"},{"key":"357_CR17","doi-asserted-by":"publisher","first-page":"665","DOI":"10.1002\/ana.410440413","volume":"44","author":"KB Nelson","year":"1998","unstructured":"Nelson KB, Dambrosia JM, Grether JK, Phillips TM. Neonatal cytokines and coagulation factors in children with cerebral palsy. Ann Neurol. 1998;44:665\u201375.","journal-title":"Ann Neurol"},{"key":"357_CR18","doi-asserted-by":"publisher","first-page":"372","DOI":"10.1016\/j.jpeds.2010.08.051","volume":"158","author":"JB Fortes Filho","year":"2011","unstructured":"Fortes Filho JB, Costa MC, Eckert GU, Santos PGB, Silveira RC, Procianoy RS. Maternal preeclampsia protects preterm infants against severe retinopathy of prematurity. J Pediatr. 2011;158:372\u20136.","journal-title":"J Pediatr"},{"key":"357_CR19","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1016\/j.jpeds.2010.09.010","volume":"158","author":"L Hendson","year":"2011","unstructured":"Hendson L, Russell L, Robertson CMT, Liang Y, Chen Y, Abdalla A, et al. Neonatal and neurodevelopmental outcomes of very low birth weight infants with histologic chorioamnionitis. J Pediatr. 2011;158:397\u2013402.","journal-title":"J Pediatr"},{"key":"357_CR20","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1159\/000357556","volume":"105","author":"S Mitra","year":"2014","unstructured":"Mitra S, Aune D, Speer CP, Saugstad OD. Chorioamnionitis as a risk factor for retinopathy of prematurity: a systematic review and meta-analysis. Neonatology. 2014;105:189\u201399.","journal-title":"Neonatology"},{"key":"357_CR21","doi-asserted-by":"publisher","first-page":"618","DOI":"10.1016\/j.survophthal.2018.04.002","volume":"63","author":"SJ Kim","year":"2018","unstructured":"Kim SJ, Port AD, Swan R, Campbell JP, Chan RVP, Chiang MF. Retinopathy of prematurity: a review of risk factors and their clinical significance. Surv Ophthalmol. 2018;63:618\u201337.","journal-title":"Surv Ophthalmol"},{"key":"357_CR22","doi-asserted-by":"publisher","first-page":"796","DOI":"10.1016\/j.ophtha.2015.12.019","volume":"123","author":"C Slidsborg","year":"2016","unstructured":"Slidsborg C, Jensen A, Forman JL, Rasmussen S, Bangsgaard R, Fledelius HC, et al. Neonatal risk factors for treatment-Demandingretinopathy of prematurity: a Danish National Study. Ophthalmology. 2016;123:796\u2013803.","journal-title":"Ophthalmology"},{"key":"357_CR23","doi-asserted-by":"publisher","first-page":"804","DOI":"10.1016\/j.ophtha.2015.11.003","volume":"123","author":"AK Hutchinson","year":"2016","unstructured":"Hutchinson AK, Melia M, Yang MB, VanderVeen DK, Wilson LB, Lambert SR. Clinical models and algorithms for the prediction of retinopathy of prematurity: a report by the American Academy of Ophthalmology. Ophthalmology. 2016;123:804\u201316.","journal-title":"Ophthalmology"},{"key":"357_CR24","unstructured":"California Perinatal Quality Care Collaborative |. Available at: \n                    https:\/\/www.cpqcc.org\/\n                    \n                  ."},{"key":"357_CR25","unstructured":"Vermont Oxford Network \u2013 Improving care for infants and their families. Available at: \n                    https:\/\/public.vtoxford.org\/\n                    \n                  ."},{"key":"357_CR26","doi-asserted-by":"crossref","unstructured":"Fierson WM, American Academy of Pediatric 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. 2013; 131:189\u201395.","DOI":"10.1542\/peds.2012-2996"},{"key":"357_CR27","doi-asserted-by":"publisher","first-page":"529","DOI":"10.1017\/S2040174417000204","volume":"8","author":"SA Segovia","year":"2017","unstructured":"Segovia SA, Vickers MH, Reynolds CM. The impact of maternal obesity on inflammatory processes and consequences for later offspring health outcomes. J Dev Orig Health Dis. 2017;8:529\u201340.","journal-title":"J Dev Orig Health Dis"},{"key":"357_CR28","doi-asserted-by":"publisher","first-page":"1500","DOI":"10.3109\/14767058.2014.961009","volume":"28","author":"SM Kim","year":"2015","unstructured":"Kim SM, Romero R, Park JW, Oh KJ, Jun JK, Yoon BH. The relationship between the intensity of intra-amniotic inflammation and the presence and severity of acute histologic chorioamnionitis in preterm gestation. J Matern Fetal Neonatal Med. 2015;28:1500\u20139.","journal-title":"J Matern Fetal Neonatal Med"},{"key":"357_CR29","doi-asserted-by":"publisher","first-page":"462","DOI":"10.1016\/j.diabet.2016.06.001","volume":"42","author":"AB Boisen","year":"2016","unstructured":"Boisen AB, Knorr S, Hansen TK, Vlachova Z, Bytoft B, Damm P, et al. Signs of low-grade systemic inflammation in female offspring of women with type 1 diabetes: the EPICOM study. Diabetes Metab. 2016;42:462\u20135.","journal-title":"Diabetes Metab"},{"key":"357_CR30","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1007\/s13224-017-0988-1","volume":"68","author":"K Sharma","year":"2018","unstructured":"Sharma K, Singh R, Kumar M, Gupta U, Rohil V, Bhattacharjee J. First-trimester inflammatory markers for risk evaluation of pregnancy hypertension. J Obstet Gynaecol India. 2018;68:27\u201332.","journal-title":"J Obstet Gynaecol India"},{"key":"357_CR31","doi-asserted-by":"publisher","first-page":"1337","DOI":"10.1055\/s-0036-1582397","volume":"33","author":"RR Kalagiri","year":"2016","unstructured":"Kalagiri RR, Carder T, Choudhury S, Vora N, Ballard AR, Govande V, et al. Inflammation in complicated pregnancy and its outcome. Am J Perinatol. 2016;33:1337\u201356.","journal-title":"Am J Perinatol"},{"key":"357_CR32","doi-asserted-by":"publisher","first-page":"900","DOI":"10.1080\/14767058.2016.1197900","volume":"30","author":"I Musilova","year":"2017","unstructured":"Musilova I, Andrys C, Drahosova M, Soucek O, Stepan M, Bestvina T, et al. Intraamniotic inflammation and umbilical cord blood interleukin-6 concentrations in pregnancies complicated by preterm prelabor rupture of membranes. J Matern Fetal Neonatal Med. 2017;30:900\u201310.","journal-title":"J Matern Fetal Neonatal Med"},{"key":"357_CR33","doi-asserted-by":"publisher","first-page":"1248","DOI":"10.4049\/jimmunol.1000289","volume":"185","author":"I Cardenas","year":"2010","unstructured":"Cardenas I, Means RE, Aldo P, Koga K, Lang SM, Booth CJ, et al. Viral infection of the placenta leads to fetal inflammation and sensitization to bacterial products predisposing to preterm labor. J Immunol. 2010;185:1248\u201357.","journal-title":"J Immunol"},{"key":"357_CR34","unstructured":"WHO:: Global Database on Body Mass Index. Available at: \n                    http:\/\/apps.who.int\/bmi\/index.jsp?introPage=intro_3.html\n                    \n                  ."},{"key":"357_CR35","doi-asserted-by":"publisher","first-page":"311","DOI":"10.1038\/jp.2014.12","volume":"34","author":"KA Kennedy","year":"2014","unstructured":"Kennedy KA, Wrage LA, Higgins RD, Finer NN, Carlo WA, Walsh MC, et al. Evaluating retinopathy of prematurity screening guidelines for 24- to 27-week gestational age infants. J Perinatol. 2014;34:311\u20138.","journal-title":"J Perinatol"},{"key":"357_CR36","doi-asserted-by":"publisher","first-page":"76","DOI":"10.4103\/2249-4847.134674","volume":"3","author":"SY Al-Abdi","year":"2014","unstructured":"Al-Abdi SY, Al-Aamri MA. A systematic review and meta-analysis of the timing of early intraventricular hemorrhage in preterm neonates: clinical and research implications. J Clin Neonatol. 2014;3:76\u201388.","journal-title":"J Clin Neonatol"},{"key":"357_CR37","doi-asserted-by":"publisher","first-page":"e298","DOI":"10.1542\/peds.2011-2022","volume":"129","author":"WH Yee","year":"2012","unstructured":"Yee WH, Soraisham AS, Shah VS, Aziz K, Yoon W, Lee SK, et al. Incidence and timing of presentation of necrotizing enterocolitis in preterm infants. Pediatrics. 2012;129:e298\u2013304.","journal-title":"Pediatrics"},{"key":"357_CR38","doi-asserted-by":"publisher","first-page":"190","DOI":"10.1093\/aje\/kwr525","volume":"176","author":"T Lange","year":"2012","unstructured":"Lange T, Vansteelandt S, Bekaert M. A simple unified approach for estimating natural direct and indirect effects. Am J Epidemiol. 2012;176:190\u20135.","journal-title":"Am J Epidemiol"},{"key":"357_CR39","volume-title":"Explanation in causal inference: methods for mediation and interaction","author":"TJ Vanderweele","year":"2015","unstructured":"Vanderweele TJ. Explanation in causal inference: methods for mediation and interaction. New York, NY, US: Oxford University Press; 2015."},{"key":"357_CR40","unstructured":"R: The R Project for Statistical Computing. Available at: \n                    https:\/\/www.r-project.org\/\n                    \n                  ."},{"key":"357_CR41","doi-asserted-by":"publisher","first-page":"e0205838","DOI":"10.1371\/journal.pone.0205838","volume":"13","author":"E Villamor-Martinez","year":"2018","unstructured":"Villamor-Martinez E, Cavallaro G, Raffaeli G, Mohammed Rahim OMM, Gulden S, Ghazi AMT, et al. Chorioamnionitis as a risk factor for retinopathy of prematurity: An updated systematic review and meta-analysis. PLoS ONE. 2018;13:e0205838.","journal-title":"PLoS ONE"},{"key":"357_CR42","doi-asserted-by":"publisher","first-page":"1062","DOI":"10.1093\/aje\/kwr230","volume":"174","author":"AJ Wilcox","year":"2011","unstructured":"Wilcox AJ, Weinberg CR, Basso O. On the pitfalls of adjusting for gestational age at birth. Am J Epidemiol. 2011;174:1062\u20138.","journal-title":"Am J Epidemiol"},{"key":"357_CR43","doi-asserted-by":"publisher","first-page":"82","DOI":"10.1038\/sj.jp.7211040","volume":"24","author":"JR York","year":"2004","unstructured":"York JR, Landers S, Kirby RS, Arbogast PG, Penn JS. Arterial oxygen fluctuation and retinopathy of prematurity in very-low-birth-weight infants. J Perinatol. 2004;24:82\u20137.","journal-title":"J Perinatol"},{"key":"357_CR44","doi-asserted-by":"publisher","first-page":"992","DOI":"10.1001\/archophthalmol.2012.243","volume":"130","author":"C Wu","year":"2012","unstructured":"Wu C, L\u00f6fqvist C, Smith LEH, VanderVeen DK, Hellstr\u00f6m A.WINROP Consortium Importance of early postnatal weight gain for normal retinal angiogenesis in very preterm infants: a multicenter study analyzing weight velocity deviations for the prediction of retinopathy of prematurity. Arch Ophthalmol. 2012;130:992\u20139.","journal-title":"Arch Ophthalmol"}],"container-title":["Journal of Perinatology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.nature.com\/articles\/s41372-019-0357-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/s41372-019-0357-2","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/s41372-019-0357-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,20]],"date-time":"2023-05-20T21:28:13Z","timestamp":1684618093000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41372-019-0357-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,4,1]]},"references-count":44,"journal-issue":{"issue":"7","published-print":{"date-parts":[[2019,7]]}},"alternative-id":["357"],"URL":"https:\/\/doi.org\/10.1038\/s41372-019-0357-2","relation":{},"ISSN":["0743-8346","1476-5543"],"issn-type":[{"value":"0743-8346","type":"print"},{"value":"1476-5543","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,4,1]]},"assertion":[{"value":"5 December 2018","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"15 February 2019","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"21 February 2019","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"1 April 2019","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Compliance with ethical standards"}},{"value":"The authors declare that they have no conflict of interest.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}}]}}