{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,13]],"date-time":"2026-01-13T23:40:10Z","timestamp":1768347610862,"version":"3.49.0"},"reference-count":33,"publisher":"Springer Science and Business Media LLC","issue":"9","license":[{"start":{"date-parts":[[2022,7,14]],"date-time":"2022-07-14T00:00:00Z","timestamp":1657756800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,7,14]],"date-time":"2022-07-14T00:00:00Z","timestamp":1657756800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"Clinical Research Fund of Chinese Academy of Medical Sciences","award":["2021-I2M-C&T-B-089"],"award-info":[{"award-number":["2021-I2M-C&T-B-089"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Eur J Pediatr"],"abstract":"<jats:title>Abstract\n<\/jats:title><jats:p>The purpose of this study is to explore risk factors of acute placental inflammatory lesions and the potential postnatal serum biomarkers for predicting the severity of intrauterine infection in preterm infants. We performed a retrospective analysis of premature infants with or without acute placental inflammatory lesions and their mothers by chart review for clinical data and placental histopathology. The preterm infants with acute placental inflammatory lesions had a higher rate of premature rupture of membranes (PROM), a longer duration of PROM, and a higher level of serum sialic acid (SIA) than those of the non-inflammation group (all <jats:italic>p<\/jats:italic>\u2009&lt;\u20090.001). According to the different inflammatory histological structures, preterm infants with funisitis had a dominant longer duration of PROM than others (<jats:italic>p<\/jats:italic>\u2009&lt;\u20090.05), and their gestational age was youngest among all the infants (<jats:italic>p<\/jats:italic>\u2009&lt;\u20090.05). Furthermore, they had the highest content of serum SIA above other groups. The preterm infants in the acute histological chorioamnionitis group showed a similar trend of clinical manifestation and laboratory parameters with the funisitis group. Moreover, the closer the placental lesions were to the fetus, the lower the gestational age of preterm infants was, and the higher the serum SIA content was.<\/jats:p><jats:p><jats:italic>Conclusion<\/jats:italic>: We utilized a simple and precise anatomically category method of placental inflammatory histopathology for pediatricians to distinguish the extent of fetal inflammatory response for representing early-onset infectious diseases of preterm infants. SIA might be one of the potential early-stage serum biomarkers to reflect the severe intrauterine infections and could guide the postnatal anti-infection treatment.<\/jats:p><jats:p><jats:table-wrap><jats:table><jats:tbody>\n                    <jats:tr>\n                      <jats:td colspan=\"2\"><jats:bold>What is Known:<\/jats:bold>\u2022\u00a0<jats:italic>Acute placental inflammatory lesion contributes to preterm birth and a series of complications in preterm infants.<\/jats:italic>\u2022\u00a0<jats:italic>C-reactive protein and interleukin-6 in neonatal blood can be used as biomarkers for potential early-onset sepsis, but they are influenced by the postnatal physiological changes of preterm infants.<\/jats:italic><\/jats:td>\n                    <\/jats:tr>\n                    <jats:tr>\n                      <jats:td colspan=\"2\"><jats:bold>What is New:<\/jats:bold>\u2022\u00a0<jats:italic>The value of serum sialic acids of preterm infants within 1-hour afterbirth may be one of the rapid postnatal biomarkers for evaluating the severity of intra-amniotic infection.<\/jats:italic>\u2022\u00a0<jats:italic>The closer the placental lesions are to the fetus, the higher the content of serum sialic acid is.<\/jats:italic><\/jats:td>\n                    <\/jats:tr>\n                  <\/jats:tbody><\/jats:table><\/jats:table-wrap><\/jats:p>","DOI":"10.1007\/s00431-022-04545-1","type":"journal-article","created":{"date-parts":[[2022,7,14]],"date-time":"2022-07-14T00:02:46Z","timestamp":1657756966000},"page":"3429-3438","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Risk factors and postnatal biomarkers for acute placental inflammatory lesions and intrauterine infections in preterm infants"],"prefix":"10.1007","volume":"181","author":[{"given":"Die","family":"Liu","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jing","family":"Liu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Fang","family":"Ye","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yunchao","family":"Su","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jiaoying","family":"Cheng","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5803-2556","authenticated-orcid":false,"given":"Qi","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2022,7,14]]},"reference":[{"key":"4545_CR1","doi-asserted-by":"publisher","first-page":"S29","DOI":"10.1016\/j.ajog.2015.08.040","volume":"213","author":"CJ Kim","year":"2015","unstructured":"Kim CJ, Romero R, Chaemsaithong P, Chaiyasit N, Yoon BH, Kim YM (2015) Acute chorioamnionitis and funisitis: definition, pathologic features, and clinical significance. Am J Obstet Gynecol 213:S29-52","journal-title":"Am J Obstet Gynecol"},{"key":"4545_CR2","doi-asserted-by":"publisher","first-page":"570","DOI":"10.1111\/apm.12847","volume":"126","author":"A Heerema-McKenney","year":"2018","unstructured":"Heerema-McKenney A (2018) Defense and infection of the human placenta. APMIS 126:570\u2013588","journal-title":"APMIS"},{"issue":"Suppl","key":"4545_CR3","doi-asserted-by":"publisher","first-page":"S21","DOI":"10.1038\/jp.2010.96","volume":"30","author":"M Gantert","year":"2010","unstructured":"Gantert M, Been JV, Gavilanes AW, Garnier Y, Zimmermann LJ, Kramer BW (2010) Chorioamnionitis: a multiorgan disease of the fetus? J Perinatol 30(Suppl):S21-30","journal-title":"J Perinatol"},{"key":"4545_CR4","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1159\/000320170","volume":"99","author":"W Thomas","year":"2011","unstructured":"Thomas W, Speer CP (2011) Chorioamnionitis: important risk factor or innocent bystander for neonatal outcome? Neonatology 99:177\u2013187","journal-title":"Neonatology"},{"key":"4545_CR5","doi-asserted-by":"publisher","first-page":"751","DOI":"10.1016\/S1473-3099(14)70710-8","volume":"14","author":"T Strunk","year":"2014","unstructured":"Strunk T, Inder T, Wang X, Burgner D, Mallard C, Levy O (2014) Infection-induced inflammation and cerebral injury in preterm infants. Lancet Infect Dis 14:751\u2013762","journal-title":"Lancet Infect Dis"},{"issue":"Suppl 2","key":"4545_CR6","doi-asserted-by":"publisher","first-page":"S69","DOI":"10.1016\/S0378-3782(12)70019-1","volume":"88","author":"CP Hornik","year":"2012","unstructured":"Hornik CP, Fort P, Clark RH, Watt K, Benjamin DK Jr, Smith PB, Manzoni P, Jacqz-Aigrain E, Kaguelidou F, Cohen-Wolkowiez M (2012) Early and late onset sepsis in very-low-birth-weight infants from a large group of neonatal intensive care units. Early Hum Dev 88(Suppl 2):S69-74","journal-title":"Early Hum Dev"},{"key":"4545_CR7","doi-asserted-by":"publisher","DOI":"10.1542\/peds.2018-2896","volume":"142","author":"KM Puopolo","year":"2018","unstructured":"Puopolo KM, Benitz WE, Zaoutis TE, COMMITTEE ON FETUS AND NEWBORN; COMMITTEE ON INFECTIOUS DISEASES, (2018) Management of neonates born at \u226434 6\/7 weeks\u2019 gestation with suspected or proven early-onset bacterial sepsis. Pediatrics 142:e20182896","journal-title":"Pediatrics"},{"key":"4545_CR8","doi-asserted-by":"publisher","first-page":"423","DOI":"10.1515\/jpm.2011.038","volume":"39","author":"M Kovo","year":"2011","unstructured":"Kovo M, Schreiber L, Ben-Haroush A, Asalee L, Seadia S, Golan A, Bar J (2011) The placental factor in spontaneous preterm labor with and without premature rupture of membranes. J Perinat Med 39:423\u2013429","journal-title":"J Perinat Med"},{"key":"4545_CR9","doi-asserted-by":"publisher","first-page":"698","DOI":"10.5858\/arpa.2015-0225-CC","volume":"140","author":"TY Khong","year":"2016","unstructured":"Khong TY, Mooney EE, Ariel I et al (2016) Sampling and definitions of placental lesions: amsterdam placental workshop group consensus statement. Arch Pathol Lab Med 140:698\u2013713","journal-title":"Arch Pathol Lab Med"},{"key":"4545_CR10","doi-asserted-by":"publisher","first-page":"435","DOI":"10.1007\/s10024-003-7070-y","volume":"6","author":"Redline RW, Faye-Petersen O, Heller D, Qureshi F, Savell V, Vogler C; Society for Pediatric Pathology, Perinatal Section, Amniotic Fluid Infection Nosology Committee","year":"2003","unstructured":"Redline RW, Faye-Petersen O, Heller D, Qureshi F, Savell V, Vogler C; Society for Pediatric Pathology, Perinatal Section, Amniotic Fluid Infection Nosology Committee (2003) Amniotic infection syndrome: nosology and reproducibility of placental reaction patterns. Pediatr Dev Pathol 6:435\u2013448","journal-title":"Pediatr Dev Pathol"},{"key":"4545_CR11","volume-title":"Williams obstetrics","author":"FG Cunningham","year":"2018","unstructured":"Cunningham FG, Leveno KJ, Bloom SL et al (2018) Williams obstetrics, 25th edn. McGraw-Hill, New York","edition":"25"},{"key":"4545_CR12","volume-title":"Practical neonatology","author":"XM Shao","year":"2011","unstructured":"Shao XM, Ye HM, Qiu XS (2011) Practical neonatology, 4th edn. People\u2019s medical publishing company, Beijing (Chinese)","edition":"4"},{"key":"4545_CR13","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1016\/j.pedneo.2017.09.001","volume":"59","author":"CC Peng","year":"2018","unstructured":"Peng CC, Chang JH, Lin HY, Cheng PJ, Su BH (2018) Intrauterine inflammation, infection, or both (Triple I): a new concept for chorioamnionitis. Pediatr Neonatol 59:231\u2013237","journal-title":"Pediatr Neonatol"},{"key":"4545_CR14","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1080\/jmf.13.2.102.109","volume":"13","author":"D Ogunyemi","year":"2003","unstructured":"Ogunyemi D, Murillo M, Jackson U, Hunter N, Alperson B (2003) The relationship between placental histopathology findings and perinatal outcome in preterm infants. J Matern Fetal Neonatal Med 13:102\u2013109","journal-title":"J Matern Fetal Neonatal Med"},{"key":"4545_CR15","doi-asserted-by":"publisher","first-page":"450.e1","DOI":"10.1016\/j.ajog.2013.12.024","volume":"210","author":"JA Bastek","year":"2014","unstructured":"Bastek JA, Weber AL, McShea MA, Ryan ME, Elovitz MA (2014) Prenatal inflammation is associated with adverse neonatal outcomes. Am J Obstet Gynecol 210:450.e1\u201310","journal-title":"Am J Obstet Gynecol"},{"key":"4545_CR16","doi-asserted-by":"publisher","DOI":"10.1155\/2013\/412831","volume":"2013","author":"R Galinsky","year":"2013","unstructured":"Galinsky R, Polglase GR, Hooper SB, Black MJ, Moss TJ (2013) The consequences of chorioamnionitis: preterm birth and effects on development. J Pregnancy 2013:412831","journal-title":"J Pregnancy"},{"key":"4545_CR17","doi-asserted-by":"crossref","unstructured":"Frascoli M, Coniglio L, Witt R et al (2018) Alloreactive fetal T cells promote uterine contractility in preterm labor via IFN-\u03b3 and TNF-\u03b1. Sci Transl Med 10:eaan2263","DOI":"10.1126\/scitranslmed.aan2263"},{"key":"4545_CR18","doi-asserted-by":"publisher","first-page":"S76","DOI":"10.1055\/s-0040-1714257","volume":"37","author":"S Perniciaro","year":"2020","unstructured":"Perniciaro S, Casarin J, Nosetti L, Binda C, Salvatore S, Ghezzi F, Agosti M (2020) Early- and late-respiratory outcome in very low birth weight with or without intrauterine inflammation. Am J Perinatol 37:S76\u2013S83","journal-title":"Am J Perinatol"},{"key":"4545_CR19","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1186\/s13052-020-00895-4","volume":"46","author":"J Miao","year":"2020","unstructured":"Miao J, Ren Z, Rao Y, Xia X, Wang J, Xu F, Zhang X, Yang J (2020) Pathological staging of chorioamnionitis contributes to complications in preterm infants. Ital J Pediatr 46:127","journal-title":"Ital J Pediatr"},{"key":"4545_CR20","doi-asserted-by":"publisher","first-page":"663","DOI":"10.1056\/NEJM199803053381006","volume":"338","author":"S Parry","year":"1998","unstructured":"Parry S, Strauss JF 3rd (1998) Premature rupture of the fetal membranes. N Engl J Med 338:663\u2013670","journal-title":"N Engl J Med"},{"key":"4545_CR21","first-page":"791","volume-title":"Fanaroff and Martin\u2019s neonatal perinatal medicine disease of the fetus and infant","author":"MS Edwards","year":"2006","unstructured":"Edwards MS (2006) Postnatal bacterial infections. In: Martin RJ, Fanaroff AA, Walsh MC (eds) Fanaroff and Martin\u2019s neonatal perinatal medicine disease of the fetus and infant, vol 2, 8th edn. Mosby Elsevier, Philadelphia, pp 791\u2013804","edition":"8"},{"key":"4545_CR22","doi-asserted-by":"publisher","first-page":"60","DOI":"10.1373\/49.1.60","volume":"49","author":"C Chiesa","year":"2003","unstructured":"Chiesa C, Pellegrini G, Panero A, Osborn JF, Signore F, Assumma M, Pacifico L (2003) C-reactive protein, interleukin-6, and procalcitonin in the immediate postnatal period: influence of illness severity, risk status, antenatal and perinatal complications, and infection. Clin Chem 49:60\u201368","journal-title":"Clin Chem"},{"key":"4545_CR23","doi-asserted-by":"publisher","first-page":"134","DOI":"10.1016\/j.jaut.2017.07.011","volume":"83","author":"A Varki","year":"2017","unstructured":"Varki A (2017) Are humans prone to autoimmunity? Implications from evolutionary changes in hominin sialic acid biology. J Autoimmun 83:134\u2013142","journal-title":"J Autoimmun"},{"key":"4545_CR24","doi-asserted-by":"publisher","first-page":"1619","DOI":"10.1002\/glia.23945","volume":"69","author":"C Klaus","year":"2021","unstructured":"Klaus C, Liao H, Allendorf DH, Brown GC, Neumann H (2021) Sialylation acts as a checkpoint for innate immune responses in the central nervous system. Glia 69:1619\u20131636","journal-title":"Glia"},{"key":"4545_CR25","doi-asserted-by":"publisher","first-page":"2632","DOI":"10.3390\/molecules25112632","volume":"25","author":"M Nagasundaram","year":"2020","unstructured":"Nagasundaram M, Horstkorte R, Gnanapragassam VS (2020) Sialic acid metabolic engineering of breast cancer cells interferes with adhesion and migration. Molecules 25:2632","journal-title":"Molecules"},{"key":"4545_CR26","doi-asserted-by":"publisher","first-page":"173","DOI":"10.1186\/s12944-019-1113-5","volume":"18","author":"C Zhang","year":"2019","unstructured":"Zhang C, Chen J, Liu Y, Xu D (2019) Sialic acid metabolism as a potential therapeutic target of atherosclerosis. Lipids Health Dis 18:173","journal-title":"Lipids Health Dis"},{"key":"4545_CR27","doi-asserted-by":"publisher","first-page":"1270","DOI":"10.1038\/s41467-021-21550-4","volume":"12","author":"E Rodriguez","year":"2021","unstructured":"Rodriguez E, Boelaars K, Brown K et al (2021) Sialic acids in pancreatic cancer cells drive tumour-associated macrophage differentiation via the Siglec receptors Siglec-7 and Siglec-9. Nat Commun 12:1270","journal-title":"Nat Commun"},{"key":"4545_CR28","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1038\/s41586-020-2311-z","volume":"582","author":"KC Shade","year":"2020","unstructured":"Shade KC, Conroy ME, Washburn N, Kitaoka M, Huynh DJ, Laprise E, Patil SU, Shreffler WG, Anthony RM (2020) Sialylation of immunoglobulin E is a determinant of allergic pathogenicity. Nature 582:265\u2013270","journal-title":"Nature"},{"key":"4545_CR29","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0080520","volume":"8","author":"F Hanisch","year":"2013","unstructured":"Hanisch F, Weidemann W, Gro\u00dfmann M, Joshi PR, Holzhausen HJ, Stoltenburg G, Weis J, Zierz S, Horstkorte R (2013) Sialylation and muscle performance: sialic acid is a marker of muscle ageing. PLoS ONE 8:e80520","journal-title":"PLoS ONE"},{"key":"4545_CR30","doi-asserted-by":"publisher","first-page":"171","DOI":"10.1159\/000299408","volume":"15","author":"I Halbrecht","year":"1983","unstructured":"Halbrecht I, Komlos L, Levinsky H, Goldman J, Allalouf A (1983) Sialic acid in lymphocytes and sera from mothers and their newborns after normal deliveries. Gynecol Obstet Invest 15:171\u2013176","journal-title":"Gynecol Obstet Invest"},{"key":"4545_CR31","first-page":"407","volume":"6","author":"CZ Hua","year":"2014","unstructured":"Hua CZ, Sun L, Ruan LL (2014) Analysis of serum sialic acid level in preterm infants at birth. Zhonghua Wei Chan Yi Xue Za Zhi 6:407\u2013409 (Chinese)","journal-title":"Zhonghua Wei Chan Yi Xue Za Zhi"},{"key":"4545_CR32","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1078\/0065-1281-00669","volume":"104","author":"A Cern\u00e1","year":"2002","unstructured":"Cern\u00e1 A, Janega P, Martanovic P, Lis\u00fd M, Bab\u00e1l P (2002) Changes in sialic acid expression in the lung during intrauterine development of the human fetus. Acta Histochem 104:339\u2013342","journal-title":"Acta Histochem"},{"key":"4545_CR33","doi-asserted-by":"publisher","first-page":"336","DOI":"10.1186\/s12974-018-1367-2","volume":"15","author":"EP Demina","year":"2018","unstructured":"Demina EP, Pierre WC, Nguyen ALA, Londono I, Reiz B, Zou C, Chakraberty R, Cairo CW, Pshezhetsky AV, Lodygensky GA (2018) Persistent reduction in sialylation of cerebral glycoproteins following postnatal inflammatory exposure. J Neuroinflammation 15:336","journal-title":"J Neuroinflammation"}],"container-title":["European Journal of Pediatrics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00431-022-04545-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00431-022-04545-1\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00431-022-04545-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,8,22]],"date-time":"2022-08-22T11:07:53Z","timestamp":1661166473000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00431-022-04545-1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,7,14]]},"references-count":33,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2022,9]]}},"alternative-id":["4545"],"URL":"https:\/\/doi.org\/10.1007\/s00431-022-04545-1","relation":{},"ISSN":["1432-1076"],"issn-type":[{"value":"1432-1076","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,7,14]]},"assertion":[{"value":"22 March 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"12 June 2022","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 June 2022","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 July 2022","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The study was conducted retrospectively from data obtained for clinical purposes. It was approved by the Ethics Committee of China-Japan Friendship Hospital and it was performed in accordance with the Declaration of Helsinki.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent to participate"}},{"value":"Not applicable.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent to publication"}},{"value":"The authors declare no competing interests.","order":5,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}