The combined exposure to intra-amniotic inflammation and neonatal respiratory distress syndrome increases the risk of intraventricular hemorrhage in preterm neonates

References

[1] Gomez R, Romero R, Ghezzi F, Yoon BH, Mazor M, Berry SM. The fetal inflammatory response syndrome. Am J Obstet Gynecol. 1998;179:194–202.10.1016/S0002-9378(98)70272-8Search in Google Scholar

[2] McMenamin JB, Shackelford GD, Volpe JJ. Outcome of neonatal intraventricular hemorrhage with periventricular echodense lesions. Ann Neurol. 1984;15:285–90.10.1002/ana.410150315Search in Google Scholar

[3] Ment LR, Vohr B, Allan W, Katz KH, Schneider KC, Westerveld M, et al. Change in cognitive function over time in very low-birth-weight infants. J Am Med Assoc. 2003;289:705–11.10.1001/jama.289.6.705Search in Google Scholar

[4] Vergani P, Locatelli A, Doria V, Assi F, Paterlini G, Pezzullo JC, et al. Intraventricular hemorrhage and periventricular leukomalacia in preterm infants. Obstet Gynecol. 2004;104:225–31.10.1097/01.AOG.0000130838.02410.b7Search in Google Scholar

[5] Yoon BH, Romero R, Kim CJ, Jun JK, Gomez R, Choi JH, et al. Amniotic fluid interleukin-6: a sensitive test for antenatal diagnosis of acute inflammatory lesions of preterm placenta and prediction of perinatal morbidity. Am J Obstet Gynecol. 1995;172:960–70.10.1016/0002-9378(95)90028-4Search in Google Scholar

[6] Vohr B, Ment LR. Intraventricular hemorrhage in the preterm infant. Early Hum Dev. 1996;44:1–16.10.1016/0378-3782(95)01692-9Search in Google Scholar

[7] Perlman JM, Broyles RS, Rogers CG. Neonatal neurologic characteristics of preterm twin infants <1,250 gm birth weight. Pediatr Neurol. 1997;17:322–6.10.1016/S0887-8994(97)00132-XSearch in Google Scholar

[8] Baschat AA, Gembruch U, Viscardi RM, Gortner L, Harman CR. Antenatal prediction of intraventricular hemorrhage in fetal growth restriction: what is the role of Doppler? Ultrasound Obstet Gynecol. 2002;19:334–9.10.1046/j.1469-0705.2002.00661.xSearch in Google Scholar PubMed

[9] Valcamonico A, Accorsi P, Sanzeni C, Martelli P, La Boria P, Cavazza A, et al. Mid- and long-term outcome of extremely low birth weight (ELBW) infants: an analysis of prognostic factors. J Matern Fetal Neonatal Med. 2007;20:465–71.10.1080/14767050701398413Search in Google Scholar PubMed

[10] Kent AL, Wright IM, Abdel-Latif ME, New South W, Australian Capital Territory Neonatal Intensive Care Units Audit G. Mortality and adverse neurologic outcomes are greater in preterm male infants. Pediatrics. 2012;129:124–31.10.1542/peds.2011-1578Search in Google Scholar PubMed

[11] Stoll BJ, Hansen NI, Bell EF, Shankaran S, Laptook AR, Walsh MC, et al. Neonatal outcomes of extremely preterm infants from the NICHD Neonatal Research Network. Pediatrics. 2010;126:443–56.10.1542/peds.2009-2959Search in Google Scholar

[12] Mukerji A, Shah V, Shah PS. Periventricular/intraventricular hemorrhage and neurodevelopmental outcomes: a meta-analysis. Pediatrics. 2015;136:1132–43.10.1542/peds.2015-0944Search in Google Scholar

[13] Payne AH, Hintz SR, Hibbs AM, Walsh MC, Vohr BR, Bann CM, et al. Neurodevelopmental outcomes of extremely low-gestational-age neonates with low-grade periventricular-intraventricular hemorrhage. JAMA Pediatr. 2013;167:451–9.10.1001/jamapediatrics.2013.866Search in Google Scholar

[14] Larroque B, Marret S, Ancel PY, Arnaud C, Marpeau L, Supernant K, et al. White matter damage and intraventricular hemorrhage in very preterm infants: the EPIPAGE study. J Pediatr. 2003;143:477–83.10.1067/S0022-3476(03)00417-7Search in Google Scholar

[15] Yoon BH, Romero R, Yang SH, Jun JK, Kim IO, Choi JH, et al. Interleukin-6 concentrations in umbilical cord plasma are elevated in neonates with white matter lesions associated with periventricular leukomalacia. Am J Obstet Gynecol. 1996;174:1433–40.10.1016/S0002-9378(96)70585-9Search in Google Scholar

[16] Armstrong DL, Sauls CD, Goddard-Finegold J. Neuropathologic findings in short-term survivors of intraventricular hemorrhage. Am J Dis Child. 1987;141:617–21.10.1001/archpedi.1987.04460060035027Search in Google Scholar

[17] Volpe JJ. Intraventricular hemorrhage and brain injury in the premature infant. Neuropathology and pathogenesis. Clin Perinatol. 1989;16:361–86.10.1016/S0095-5108(18)30637-7Search in Google Scholar

[18] Vohr BR, Wright LL, Dusick AM, Mele L, Verter J, Steichen JJ, et al. Neurodevelopmental and functional outcomes of extremely low birth weight infants in the National Institute of Child Health and Human Development Neonatal Research Network, 1993-1994. Pediatrics. 2000;105:1216–26.10.1542/peds.105.6.1216Search in Google Scholar

[19] Futagi Y, Toribe Y, Ogawa K, Suzuki Y. Neurodevelopmental outcome in children with intraventricular hemorrhage. Pediatr Neurol. 2006;34:219–24.10.1016/j.pediatrneurol.2005.08.011Search in Google Scholar

[20] Vohr B, Allan WC, Scott DT, Katz KH, Schneider KC, Makuch RW, et al. Early-onset intraventricular hemorrhage in preterm neonates: incidence of neurodevelopmental handicap. Semin Perinatol. 1999;23:212–7.10.1016/S0146-0005(99)80065-2Search in Google Scholar

[21] Allan WC, Vohr B, Makuch RW, Katz KH, Ment LR. Antecedents of cerebral palsy in a multicenter trial of indomethacin for intraventricular hemorrhage. Arch Pediatr Adolesc Med. 1997;151:580–5.10.1001/archpedi.1997.02170430046010Search in Google Scholar

[22] Dunin-Wasowicz D, Rowecka-Trzebicka K, Milewska-Bobula B, Kassur-Siemienska B, Bauer A, Idzik M, et al. Risk factors for cerebral palsy in very low-birthweight infants in the 1980s and 1990s. J Child Neurol. 2000;15:417–20.10.1177/088307380001500612Search in Google Scholar

[23] Msall ME, Buck GM, Rogers BT, Merke D, Catanzaro NL, Zorn WA. Risk factors for major neurodevelopmental impairments and need for special education resources in extremely premature infants. J Pediatr. 1991;119:606–14.10.1016/S0022-3476(05)82415-1Search in Google Scholar

[24] Patra K, Wilson-Costello D, Taylor HG, Mercuri-Minich N, Hack M. Grades I-II intraventricular hemorrhage in extremely low birth weight infants: effects on neurodevelopment. J Pediatr. 2006;149:169–73.10.1016/j.jpeds.2006.04.002Search in Google Scholar PubMed

[25] Gleissner M, Jorch G, Avenarius S. Risk factors for intraventricular hemorrhage in a birth cohort of 3721 premature infants. J Perinat Med. 2000;28:104–10.Search in Google Scholar

[26] Riskin A, Riskin-Mashiah S, Bader D, Kugelman A, Lerner-Geva L, Boyko V, et al. Delivery mode and severe intraventricular hemorrhage in single, very low birth weight, vertex infants. Obstet Gynecol. 2008;112:21–8.10.1097/AOG.0b013e31817cfdf1Search in Google Scholar PubMed

[27] Bhandari V, Buhimschi CS, Han CS, Lee SY, Pettker CM, Campbell KH, et al. Cord blood erythropoietin and interleukin-6 for prediction of intraventricular hemorrhage in the preterm neonate. J Matern Fetal Neonatal Med. 2011;24:673–9.10.3109/14767058.2010.520048Search in Google Scholar PubMed PubMed Central

[28] Kwak HM, Shin MY, Cha HH, Choi SJ, Lee JH, Kim JS, et al. The efficacy of cefazolin plus macrolide (erythromycin or clarithromycin) versus cefazolin alone in neonatal morbidity and placental inflammation for women with preterm premature rupture of membranes. Placenta. 2013;34:346–52.10.1016/j.placenta.2013.01.016Search in Google Scholar PubMed

[29] Viscardi RM, Hashmi N, Gross GW, Sun CC, Rodriguez A, Fairchild KD. Incidence of invasive Ureaplasma in VLBW infants: relationship to severe intraventricular hemorrhage. J Perinatol. 2008;28:759–65.10.1038/jp.2008.98Search in Google Scholar PubMed PubMed Central

[30] Kasper DC, Mechtler TP, Bohm J, Petricevic L, Gleiss A, Spergser J, et al. In utero exposure to Ureaplasma spp. is associated with increased rate of bronchopulmonary dysplasia and intraventricular hemorrhage in preterm infants. J Perinat Med. 2011;39:331–6.10.1515/jpm.2011.022Search in Google Scholar PubMed

[31] Martinez E, Figueroa R, Garry D, Visintainer P, Patel K, Verma U, et al. Elevated amniotic fluid interleukin-6 as a predictor of neonatal periventricular leukomalacia and intraventricular Hemorrhage. J Matern Fetal Investig. 1998;8:101–7.Search in Google Scholar

[32] Thomas W, Speer CP. Chorioamnionitis: important risk factor or innocent bystander for neonatal outcome? Neonatology. 2011;99:177–87.10.1159/000320170Search in Google Scholar PubMed

[33] Leviton A, Dammann O, Durum SK. The adaptive immune response in neonatal cerebral white matter damage. Ann Neurol. 2005;58:821–8.10.1002/ana.20662Search in Google Scholar

[34] Verma U, Tejani N, Klein S, Reale MR, Beneck D, Figueroa R, et al. Obstetric antecedents of intraventricular hemorrhage and periventricular leukomalacia in the low-birth-weight neonate. Am J Obstet Gynecol. 1997;176:275–81.10.1016/S0002-9378(97)70485-XSearch in Google Scholar

[35] Linder N, Haskin O, Levit O, Klinger G, Prince T, Naor N, et al. Risk factors for intraventricular hemorrhage in very low birth weight premature infants: a retrospective case-control study. Pediatrics. 2003;111:e590–5.10.1542/peds.111.5.e590Search in Google Scholar

[36] Morales WJ, Koerten J. Obstetric management and intraventricular hemorrhage in very-low-birth-weight infants. Obstet Gynecol. 1986;68:35–40.Search in Google Scholar

[37] Ferrari B, Tonni G, Luzietti R, Ciarlini G, Vadora E, Merialdi A. Neonatal complications and risk of intraventricular-periventricular hemorrhage. Clin Exp Obstet Gynecol. 1992;19:253–8.Search in Google Scholar

[38] Levene MI, Fawer CL, Lamont RF. Risk factors in the development of intraventricular haemorrhage in the preterm neonate. Arch Dis Child. 1982;57:410–7.10.1136/adc.57.6.410Search in Google Scholar

[39] Heljic S, Maksic H, Buljina A. Hemorrhagic and hypoxic-ischemic brain lesions in premature infants on artificial ventilation. Med Arh. 2000;54:265–7.Search in Google Scholar

[40] Hill A, Volpe JJ. Seizures, hypoxic-ischemic brain injury, and intraventricular hemorrhage in the newborn. Ann Neurol. 1981;10:109–21.10.1002/ana.410100202Search in Google Scholar

[41] Lou HC. Perinatal hypoxic-ischaemic brain damage and intraventricular haemorrhage. Baillieres Clin Obstet Gynaecol. 1988;2:213–20.10.1016/S0950-3552(88)80073-7Search in Google Scholar

[42] Gomez R, Romero R, Edwin SS, David C. Pathogenesis of preterm labor and preterm premature rupture of membranes associated with intraamniotic infection. Infect Dis Clin North Am. 1997;11:135–76.10.1016/S0891-5520(05)70347-0Search in Google Scholar

[43] Romero R, Mazor M, Wu YK, Sirtori M, Oyarzun E, Mitchell MD, et al. Infection in the pathogenesis of preterm labor. Semin Perinatol. 1988;12:262–79.Search in Google Scholar

[44] Romero R, Sirtori M, Oyarzun E, Avila C, Mazor M, Callahan R, et al. Infection and labor. V. Prevalence, microbiology, and clinical significance of intraamniotic infection in women with preterm labor and intact membranes. Am J Obstet Gynecol. 1989;161:817–24.10.1016/0002-9378(89)90409-2Search in Google Scholar

[45] Romero R, Shamma F, Avila C, Jimenez C, Callahan R, Nores J, et al. Infection and labor. VI. Prevalence, microbiology, and clinical significance of intraamniotic infection in twin gestations with preterm labor. Am J Obstet Gynecol. 1990;163:757–61.10.1016/0002-9378(90)91063-ISearch in Google Scholar

[46] Angus SR, Segel SY, Hsu CD, Locksmith GJ, Clark P, Sammel MD, et al. Amniotic fluid matrix metalloproteinase-8 indicates intra-amniotic infection. Am J Obstet Gynecol. 2001;185: 1232–8.10.1067/mob.2001.118654Search in Google Scholar PubMed

[47] Gibbs RS, Romero R, Hillier SL, Eschenbach DA, Sweet RL. A review of premature birth and subclinical infection. Am J Obstet Gynecol. 1992;166:1515–28.10.1016/0002-9378(92)91628-NSearch in Google Scholar

[48] Yoon BH, Romero R, Park JS, Chang JW, Kim YA, Kim JC, et al. Microbial invasion of the amniotic cavity with Ureaplasmaurealyticum is associated with a robust host response in fetal, amniotic, and maternal compartments. Am J Obstet Gynecol. 1998;179:1254–60.10.1016/S0002-9378(98)70142-5Search in Google Scholar

[49] Yoon BH, Romero R, Moon JB, Shim SS, Kim M, Kim G, et al. Clinical significance of intra-amniotic inflammation in patients with preterm labor and intact membranes. Am J Obstet Gynecol. 2001;185:1130–6.10.1067/mob.2001.117680Search in Google Scholar

[50] Yoon BH, Romero R, Kim M, Kim EC, Kim T, Park JS, et al. Clinical implications of detection of Ureaplasma urealyticum in the amniotic cavity with the polymerase chain reaction. Am J Obstet Gynecol. 2000;183:1130–7.10.1067/mob.2000.109036Search in Google Scholar

[51] Yoon BH, Chang JW, Romero R. Isolation of Ureaplasmaurealyticum from the amniotic cavity and adverse outcome in preterm labor. Obstet Gynecol. 1998;92:77–82.10.1016/S0029-7844(98)00122-7Search in Google Scholar

[52] Oh KJ, Lee SE, Jung H, Kim G, Romero R, Yoon BH. Detection of ureaplasmas by the polymerase chain reaction in the amniotic fluid of patients with cervical insufficiency. J Perinat Med. 2010;38:261–8.10.1515/jpm.2010.040Search in Google Scholar PubMed PubMed Central

[53] Gomez-Lopez N, Romero R, Plazyo O, Panaitescu B, Furcron AE, Miller D, et al. Intra-amniotic administration of HMGB1 induces spontaneous preterm labor and birth. Am J Reprod Immunol. 2016;75:3–7.10.1111/aji.12443Search in Google Scholar PubMed PubMed Central

[54] Kim SM, Romero R, Lee J, Chaemsaithong P, Lee MW, Chaiyasit N, et al. About one-half of early spontaneous preterm deliveries can be identified by a rapid matrix metalloproteinase-8 (MMP-8) bedside test at the time of mid-trimester genetic amniocentesis. J Matern Fetal Neonatal Med. 2016;29:2414–21.10.3109/14767058.2015.1094049Search in Google Scholar PubMed PubMed Central

[55] Romero R, Dey SK, Fisher SJ. Preterm labor: one syndrome, many causes. Science. 2014;345:760–5.10.1126/science.1251816Search in Google Scholar PubMed PubMed Central

[56] Romero R, Espinoza J, Goncalves LF, Kusanovic JP, Friel LA, Nien JK. Inflammation in preterm and term labour and delivery. Semin Fetal Neonatal Med. 2006;11:317–26.10.1016/j.siny.2006.05.001Search in Google Scholar PubMed PubMed Central

[57] Shim SS, Romero R, Hong JS, Park CW, Jun JK, Kim BI, et al. Clinical significance of intra-amniotic inflammation in patients with preterm premature rupture of membranes. Am J Obstet Gynecol. 2004;191:1339–45.10.1016/j.ajog.2004.06.085Search in Google Scholar

[58] Maymon E, Romero R, Chaiworapongsa T, Berman S, Conoscenti G, Gomez R, et al. Amniotic fluid matrix metalloproteinase-8 in preterm labor with intact membranes. Am J Obstet Gynecol. 2001;185:1149–55.10.1067/mob.2001.118165Search in Google Scholar

[59] Kim CJ, Romero R, Chaemsaithong P, Chaiyasit N, Yoon BH, Kim YM. Acute chorioamnionitis and funisitis: definition, pathologic features, and clinical significance. Am J Obstet Gynecol. 2015;213:S29–52.10.1016/j.ajog.2015.08.040Search in Google Scholar

[60] Romero R, Mazaki-Tovi S, Vaisbuch E, Kusanovic JP, Chaiworapongsa T, Gomez R, et al. Metabolomics in premature labor: a novel approach to identify patients at risk for preterm delivery. J Matern Fetal Neonatal Med. 2010;23:1344–59.10.3109/14767058.2010.482618Search in Google Scholar

[61] Romero R, Espinoza J, Kusanovic JP, Gotsch F, Hassan S, Erez O, et al. The preterm parturition syndrome. BJOG. 2006;113 Suppl 3:17–42.10.1111/j.1471-0528.2006.01120.xSearch in Google Scholar

[62] DiGiulio DB, Romero R, Amogan HP, Kusanovic JP, Bik EM, Gotsch F, et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS One. 2008;3:e3056.10.1371/journal.pone.0003056Search in Google Scholar

[63] Yoon BH, Kim CJ, Romero R, Jun JK, Park KH, Choi ST, et al. Experimentally induced intrauterine infection causes fetal brain white matter lesions in rabbits. Am J Obstet Gynecol. 1997;177:797–802.10.1016/S0002-9378(97)70271-0Search in Google Scholar

[64] Dean JM, Farrag D, Zahkouk SA, El Zawahry EY, Hagberg H, Kjellmer I, et al. Cerebellar white matter injury following systemic endotoxemia in preterm fetal sheep. Neuroscience. 2009;160:606–15.10.1016/j.neuroscience.2009.02.071Search in Google Scholar PubMed

[65] Gavilanes AW, Strackx E, Kramer BW, Gantert M, Van den Hove D, Steinbusch H, et al. Chorioamnionitis induced by intraamniotic lipopolysaccharide resulted in an interval-dependent increase in central nervous system injury in the fetal sheep. Am J Obstet Gynecol. 2009;200:437 e1–8.10.1016/j.ajog.2008.12.003Search in Google Scholar PubMed

[66] Lodygensky GA, West T, Stump M, Holtzman DM, Inder TE, Neil JJ. In vivo MRI analysis of an inflammatory injury in the developing brain. Brain Behav Immun. 2010;24:759–67.10.1016/j.bbi.2009.11.005Search in Google Scholar PubMed PubMed Central

[67] Wallace K, Veerisetty S, Paul I, May W, Miguel-Hidalgo JJ, Bennett W. Prenatal infection decreases calbindin, decreases Purkinje cell volume and density and produces long-term motor deficits in Sprague-Dawley rats. Dev Neurosci. 2010;32:302–12.10.1159/000319506Search in Google Scholar PubMed PubMed Central

[68] Sarkar S, Kaplan C, Wiswell TE, Spitzer AR. Histological chorioamnionitis and the risk of early intraventricular hemorrhage in infants born <or =28 weeks gestation. J Perinatol. 2005;25:749–52.10.1038/sj.jp.7211399Search in Google Scholar PubMed

[69] Richardson BS, Wakim E, daSilva O, Walton J. Preterm histologic chorioamnionitis: impact on cord gas and pH values and neonatal outcome. Am J Obstet Gynecol. 2006;195:1357–65.10.1016/j.ajog.2006.03.053Search in Google Scholar PubMed

[70] Rocha G, Proenca E, Quintas C, Rodrigues T, Guimaraes H. Chorioamnionitis and brain damage in the preterm newborn. J Matern Fetal Neonatal Med. 2007;20:745–9.10.1080/14767050701580515Search in Google Scholar PubMed

[71] Moss TJ, Nitsos I, Kramer BW, Ikegami M, Newnham JP, Jobe AH. Intra-amniotic endotoxin induces lung maturation by direct effects on the developing respiratory tract in preterm sheep. Am J Obstet Gynecol. 2002;187:1059–65.10.1067/mob.2002.126296Search in Google Scholar PubMed

[72] Jobe AH, Newnham JP, Willet KE, Moss TJ, Gore Ervin M, Padbury JF, et al. Endotoxin-induced lung maturation in preterm lambs is not mediated by cortisol. Am J Respir Crit Care Med. 2000;162:1656–61.10.1164/ajrccm.162.5.2003044Search in Google Scholar PubMed

[73] Shimoya K, Taniguchi T, Matsuzaki N, Moriyama A, Murata Y, Kitajima H, et al. Chorioamnionitis decreased incidence of respiratory distress syndrome by elevating fetal interleukin-6 serum concentration. Hum Reprod. 2000;15:2234–40.10.1093/humrep/15.10.2234Search in Google Scholar PubMed

[74] Lee J, Seong HS, Kim BJ, Jun JK, Romero R, Yoon BH. Evidence to support that spontaneous preterm labor is adaptive in nature: neonatal RDS is more common in “indicated” than in “spontaneous” preterm birth. J Perinat Med. 2009;37:53–8.10.1515/JPM.2009.036Search in Google Scholar PubMed PubMed Central

[75] Tsuda H, Takahashi Y, Iwagaki S, Kawabata I, Hayakawa H, Kotani T, et al. Intra-amniotic infection increases amniotic lamellar body count before 34 weeks of gestation. J Matern Fetal Neonatal Med. 2010;23:1230–6.10.3109/14767051003615442Search in Google Scholar PubMed

[76] Morken NH, Kallen K, Jacobsson B. Outcomes of preterm children according to type of delivery onset: a nationwide population-based study. Paediatr Perinat Epidemiol. 2007;21:458–64.10.1111/j.1365-3016.2007.00823.xSearch in Google Scholar PubMed

[77] Park JS, Romero R, Yoon BH, Moon JB, Oh SY, Han SY, et al. The relationship between amniotic fluid matrix metalloproteinase-8 and funisitis. Am J Obstet Gynecol. 2001;185:1156–61.10.1067/mob.2001.117679Search in Google Scholar

[78] Salafia CM, Minior VK, Rosenkrantz TS, Pezzullo JC, Popek EJ, Cusick W, et al. Maternal, placental, and neonatal associations with early germinal matrix/intraventricular hemorrhage in infants born before 32 weeks’ gestation. Am J Perinatol. 1995;12:429–36.10.1055/s-2007-994514Search in Google Scholar

[79] Huleihel M, Golan H, Hallak M. Intrauterine infection/inflammation during pregnancy and offspring brain damages: possible mechanisms involved. Reprod Biol Endocrinol. 2004;2:17.10.1186/1477-7827-2-17Search in Google Scholar

[80] Ugwumadu A. Infection and fetal neurologic injury. Curr Opin Obstet Gynecol. 2006;18:106–11.10.1097/01.gco.0000192999.12416.95Search in Google Scholar

[81] Perlman JM. White matter injury in the preterm infant: an important determination of abnormal neurodevelopment outcome. Early Hum Dev. 1998;53:99–120.10.1016/S0378-3782(98)00037-1Search in Google Scholar

[82] Andrews T, Zhang P, Bhat NR. TNFalpha potentiates IFNgamma-induced cell death in oligodendrocyte progenitors. J Neurosci Res. 1998;54:574–83.10.1002/(SICI)1097-4547(19981201)54:5<574::AID-JNR2>3.0.CO;2-0Search in Google Scholar

[83] Kahn MA, De Vellis J. Regulation of an oligodendrocyte progenitor cell line by the interleukin-6 family of cytokines. Glia. 1994;12:87–98.10.1002/glia.440120202Search in Google Scholar

[84] Hurwitz AA, Lyman WD, Guida MP, Calderon TM, Berman JW. Tumor necrosis factor alpha induces adhesion molecule expression on human fetal astrocytes. J Exp Med. 1992;176:1631–6.10.1084/jem.176.6.1631Search in Google Scholar

[85] Cobo T, Palacio M, Martinez-Terron M, Navarro-Sastre A, Bosch J, Filella X, et al. Clinical and inflammatory markers in amniotic fluid as predictors of adverse outcomes in preterm premature rupture of membranes. Am J Obstet Gynecol. 2011;205:126 e1–8.10.1016/j.ajog.2011.03.050Search in Google Scholar

[86] Kim KW, Romero R, Park HS, Park CW, Shim SS, Jun JK, et al. A rapid matrix metalloproteinase-8 bedside test for the detection of intraamniotic inflammation in women with preterm premature rupture of membranes. Am J Obstet Gynecol. 2007;197:292 e1–5.10.1016/j.ajog.2007.06.040Search in Google Scholar

[87] Jacobsson B, Mattsby-Baltzer I, Andersch B, Bokstrom H, Holst RM, Nikolaitchouk N, et al. Microbial invasion and cytokine response in amniotic fluid in a Swedish population of women with preterm prelabor rupture of membranes. Acta Obstet Gynecol Scand. 2003;82:423–31.10.1034/j.1600-0412.2003.00157.xSearch in Google Scholar

[88] Jacobsson B, Mattsby-Baltzer I, Andersch B, Bokstrom H, Holst RM, Wennerholm UB, et al. Microbial invasion and cytokine response in amniotic fluid in a Swedish population of women in preterm labor. Acta Obstet Gynecol Scand. 2003;82:120–8.10.1034/j.1600-0412.2003.00047.xSearch in Google Scholar

[89] Yoon BH, Jun JK, Romero R, Park KH, Gomez R, Choi J-H, et al. Amniotic fluid inflammatory cytokines (interleukin-6, interleukin-1β, and tumor necrosis factor-α), neonatal brain white matter lesions, and cerebral palsy. Am J Obstet Gynecol. 1997;177:19–26.10.1016/S0002-9378(97)70432-0Search in Google Scholar

[90] Oh KJ, Park KH, Kim SN, Jeong EH, Lee SY, Yoon HY. Predictive value of intra-amniotic and serum markers for inflammatory lesions of preterm placenta. Placenta. 2011;32:732–6.10.1016/j.placenta.2011.07.080Search in Google Scholar PubMed

[91] Lee SE, Romero R, Jung H, Park CW, Park JS, Yoon BH. The intensity of the fetal inflammatory response in intraamniotic inflammation with and without microbial invasion of the amniotic cavity. Am J Obstet Gynecol. 2007;197:294 e1–6.10.1016/j.ajog.2007.07.006Search in Google Scholar PubMed

[92] Lee SE, Romero R, Park CW, Jun JK, Yoon BH. The frequency and significance of intraamniotic inflammation in patients with cervical insufficiency. Am J Obstet Gynecol. 2008;198:633 e1–8.10.1016/j.ajog.2007.11.047Search in Google Scholar PubMed

[93] Nien JK, Yoon BH, Espinoza J, Kusanovic JP, Erez O, Soto E, et al. A rapid MMP-8 bedside test for the detection of intra-amniotic inflammation identifies patients at risk for imminent preterm delivery. Am J Obstet Gynecol. 2006;195:1025–30.10.1016/j.ajog.2006.06.054Search in Google Scholar PubMed

[94] Gotsch F, Romero R, Chaiworapongsa T, Erez O, Vaisbuch E, Espinoza J, et al. Evidence of the involvement of caspase-1 under physiologic and pathologic cellular stress during human pregnancy: a link between the inflammasome and parturition. J Matern Fetal Neonatal Med. 2008;21:605–16.10.1080/14767050802212109Search in Google Scholar PubMed PubMed Central

[95] Holst RM, Laurini R, Jacobsson B, Samuelsson E, Savman K, Doverhag C, et al. Expression of cytokines and chemokines in cervical and amniotic fluid: relationship to histological chorioamnionitis. J Matern Fetal Neonatal Med. 2007;20:885–93.10.1080/14767050701752601Search in Google Scholar PubMed

[96] Mazaki-Tovi S, Romero R, Kusanovic JP, Erez O, Gotsch F, Mittal P, et al. Visfatin/Pre-B cell colony-enhancing factor in amniotic fluid in normal pregnancy, spontaneous labor at term, preterm labor and prelabor rupture of membranes: an association with subclinical intrauterine infection in preterm parturition. J Perinat Med. 2008;36:485–96.10.1515/JPM.2008.084Search in Google Scholar PubMed PubMed Central

[97] Bashiri A, Horowitz S, Huleihel M, Hackmon R, Dukler D, Mazor M. Elevated concentrations of interleukin-6 in intra-amniotic infection with Ureaplasma urealyticum in asymptomatic women during genetic amniocentesis. Acta Obstet Gynecol Scand. 1999;78:379–82.Search in Google Scholar

[98] Biggio JR, Jr., Ramsey PS, Cliver SP, Lyon MD, Goldenberg RL, Wenstrom KD. Midtrimester amniotic fluid matrix metalloproteinase-8 (MMP-8) levels above the 90th percentile are a marker for subsequent preterm premature rupture of membranes. Am J Obstet Gynecol. 2005;192:109–13.10.1016/j.ajog.2004.06.103Search in Google Scholar

[99] Fortunato SJ, Menon R. Screening of novel matrix metalloproteinases (MMPs) in human fetal membranes. J Assist Reprod Genet. 2002;19:483–6.10.1023/A:1020362519981Search in Google Scholar

[100] Maymon E, Romero R, Pacora P, Gomez R, Athayde N, Edwin S, et al. Human neutrophil collagenase (matrix metalloproteinase 8) in parturition, premature rupture of the membranes, and intrauterine infection. Am J Obstet Gynecol. 2000;183:94–9.10.1016/S0002-9378(00)99072-0Search in Google Scholar

[101] Andrews WW, Hauth JC, Goldenberg RL, Gomez R, Romero R, Cassell GH. Amniotic fluid interleukin-6: correlation with upper genital tract microbial colonization and gestational age in women delivered after spontaneous labor versus indicated delivery. Am J Obstet Gynecol. 1995;173:606–12.10.1016/0002-9378(95)90290-2Search in Google Scholar

[102] Coultrip LL, Lien JM, Gomez R, Kapernick P, Khoury A, Grossman JH. The value of amniotic fluid interleukin-6 determination in patients with preterm labor and intact membranes in the detection of microbial invasion of the amniotic cavity. Am J Obstet Gynecol. 1994;171:901–11.10.1016/S0002-9378(94)70057-5Search in Google Scholar

[103] Romero R, Yoon BH, Kenney JS, Gomez R, Allison AC, Sehgal PB. Amniotic fluid interleukin-6 determinations are of diagnostic and prognostic value in preterm labor. Am J Reprod Immunol. 1993;30:167–83.10.1111/j.1600-0897.1993.tb00618.xSearch in Google Scholar

[104] Park CW, Lee SM, Park JS, Jun JK, Romero R, Yoon BH. The antenatal identification of funisitis with a rapid MMP-8 bedside test. J Perinat Med. 2008;36:497–502.10.1515/JPM.2008.079Search in Google Scholar

[105] Romero R, Quintero R, Nores J, Avila C, Mazor M, Hanaoka S, et al. Amniotic fluid white blood cell count: a rapid and simple test to diagnose microbial invasion of the amniotic cavity and predict preterm delivery. Am J Obstet Gynecol. 1991;165:821–30.10.1016/0002-9378(91)90423-OSearch in Google Scholar

[106] Yoon BH, Jun JK, Park KH, Syn HC, Gomez R, Romero R. Serum C-reactive protein, white blood cell count, and amniotic fluid white blood cell count in women with preterm premature rupture of membranes. Obstet Gynecol. 1996;88:1034–40.10.1016/S0029-7844(96)00339-0Search in Google Scholar

[107] Yoon BH, Yang SH, Jun JK, Park KH, Kim CJ, Romero R. Maternal blood C-reactive protein, white blood cell count, and temperature in preterm labor: a comparison with amniotic fluid white blood cell count. Obstet Gynecol. 1996;87:231–7.10.1016/0029-7844(95)00380-0Search in Google Scholar

[108] Pacora P, Chaiworapongsa T, Maymon E, Kim YM, Gomez R, Yoon BH, et al. Funisitis and chorionic vasculitis: the histological counterpart of the fetal inflammatory response syndrome. J Matern Fetal Neonatal Med. 2002;11:18–25.10.1080/jmf.11.1.18.25Search in Google Scholar

[109] Kim CJ, Yoon BH, Park SS, Kim MH, Chi JG. Acute funisitis of preterm but not term placentas is associated with severe fetal inflammatory response. Hum Pathol. 2001;32:623–9.10.1053/hupa.2001.24992Search in Google Scholar

[110] Park CW, Moon KC, Park JS, Jun JK, Romero R, Yoon BH. The involvement of human amnion in histologic chorioamnionitis is an indicator that a fetal and an intra-amniotic inflammatory response is more likely and severe: clinical implications. Placenta. 2009;30:56–61.10.1016/j.placenta.2008.09.017Search in Google Scholar

[111] Romero R, Salafia CM, Athanassiadis AP, Hanaoka S, Mazor M, Sepulveda W, et al. The relationship between acute inflammatory lesions of the preterm placenta and amniotic fluid microbiology. Am J Obstet Gynecol. 1992;166:1382–8.10.1016/0002-9378(92)91609-ESearch in Google Scholar

[112] Smulian JC, Vintzileos AM, Lai YL, Santiago J, Shen-Schwarz S, Campbell WA. Maternal chorioamnionitis and umbilical vein interleukin-6 levels for identifying early neonatal sepsis. J Matern Fetal Med. 1999;8:88–94.10.1002/(SICI)1520-6661(199905/06)8:3<88::AID-MFM4>3.0.CO;2-#Search in Google Scholar

[113] Yoon BH, Romero R, Shim JY, Shim SS, Kim CJ, Jun JK. C-reactive protein in umbilical cord blood: a simple and widely available clinical method to assess the risk of amniotic fluid infection and funisitis. J Matern Fetal Neonatal Med. 2003;14:85–90.10.1080/jmf.14.2.85.90Search in Google Scholar PubMed

[114] Yoon BH, Romero R, Park JS, Kim M, Oh SY, Kim CJ, et al. The relationship among inflammatory lesions of the umbilical cord (funisitis), umbilical cord plasma interleukin 6 concentration, amniotic fluid infection, and neonatal sepsis. Am J Obstet Gynecol. 2000;183:1124–9.10.1067/mob.2000.109035Search in Google Scholar PubMed

[115] Chaiworapongsa T, Romero R, Kim JC, Kim YM, Blackwell SC, Yoon BH, et al. Evidence for fetal involvement in the pathologic process of clinical chorioamnionitis. Am J Obstet Gynecol. 2002;186:1178–82.10.1067/mob.2002.124042Search in Google Scholar PubMed

[116] Romero R, Chaemsaithong P, Docheva N, Korzeniewski SJ, Tarca AL, Bhatti G, et al. Clinical chorioamnionitis at term V: umbilical cord plasma cytokine profile in the context of a systemic maternal inflammatory response. J Perinat Med. 2016;44:53–76.10.1515/jpm-2015-0121Search in Google Scholar PubMed PubMed Central

[117] Moon JB, Kim JC, Yoon BH, Romero R, Kim G, Oh SY, et al. Amniotic fluid matrix metalloproteinase-8 and the development of cerebral palsy. J Perinat Med. 2002;30:301–6.10.1515/JPM.2002.044Search in Google Scholar PubMed

[118] Seong HS, Lee SE, Kang JH, Romero R, Yoon BH. The frequency of microbial invasion of the amniotic cavity and histologic chorioamnionitis in women at term with intact membranes in the presence or absence of labor. Am J Obstet Gynecol. 2008;199:375 e1–5.10.1016/j.ajog.2008.06.040Search in Google Scholar PubMed PubMed Central

[119] Sampson JE, Theve RP, Blatman RN, Shipp TD, Bianchi DW, Ward BE, et al. Fetal origin of amniotic fluid polymorphonuclear leukocytes. Am J Obstet Gynecol. 1997;176:77–81.10.1016/S0002-9378(97)80015-4Search in Google Scholar

[120] Sun H, Zhou Y, Xiong H, Kang W, Xu B, Liu D, et al. Prognosis of very preterm infants with severe respiratory distress syndrome receiving mechanical ventilation. Lung. 2015;193:249–54.10.1007/s00408-014-9683-5Search in Google Scholar

[121] Vergani P, Patane L, Doria P, Borroni C, Cappellini A, Pezzullo JC, et al. Risk factors for neonatal intraventricular haemorrhage in spontaneous prematurity at 32 weeks gestation or less. Placenta. 2000;21:402–7.10.1053/plac.1999.0499Search in Google Scholar

[122] Mullaart RA, Hopman JC, Rotteveel JJ, Daniels O, Stoelinga GB, De Haan AF. Cerebral blood flow fluctuation in neonatal respiratory distress and periventricular haemorrhage. Early Hum Dev. 1994;37:179–85.10.1016/0378-3782(94)90077-9Search in Google Scholar

[123] Kusuda S, Ito Y, Kim TJ, Miyagi N, Shishida N, Tanaka Y. Cerebral hemodynamics after exogenous surfactant administration for respiratory distress syndrome in piglet model. J Perinat Med. 2000;28:363–71.10.1515/JPM.2000.046Search in Google Scholar

[124] Perlman JM, Goodman S, Kreusser KL, Volpe JJ. Reduction in intraventricular hemorrhage by elimination of fluctuating cerebral blood-flow velocity in preterm infants with respiratory distress syndrome. N Engl J Med. 1985;312:1353–7.10.1056/NEJM198505233122104Search in Google Scholar

[125] Lemmers PM, Toet M, van Schelven LJ, van Bel F. Cerebral oxygenation and cerebral oxygen extraction in the preterm infant: the impact of respiratory distress syndrome. Exp Brain Res. 2006;173:458–67.10.1007/s00221-006-0388-8Search in Google Scholar

[126] Lauterbach MD, Raz S, Sander CJ. Neonatal hypoxic risk in preterm birth infants: the influence of sex and severity of respiratory distress on cognitive recovery. Neuropsychology. 2001;15:411–20.10.1037/0894-4105.15.3.411Search in Google Scholar

[127] Nelson KB, Grether JK. Potentially asphyxiating conditions and spastic cerebral palsy in infants of normal birth weight. Am J Obstet Gynecol. 1998;179:507–13.10.1016/S0002-9378(98)70387-4Search in Google Scholar

[128] Girard S, Kadhim H, Beaudet N, Sarret P, Sebire G. Developmental motor deficits induced by combined fetal exposure to lipopolysaccharide and early neonatal hypoxia/ischemia: a novel animal model for cerebral palsy in very premature infants. Neuroscience. 2009;158:673–82.10.1016/j.neuroscience.2008.10.032Search in Google Scholar PubMed

[129] Larouche A, Roy M, Kadhim H, Tsanaclis AM, Fortin D, Sebire G. Neuronal injuries induced by perinatal hypoxic-ischemic insults are potentiated by prenatal exposure to lipopolysaccharide: animal model for perinatally acquired encephalopathy. Dev Neurosci. 2005;27:134–42.10.1159/000085985Search in Google Scholar

[130] Eklind S, Mallard C, Leverin AL, Gilland E, Blomgren K, Mattsby-Baltzer I, et al. Bacterial endotoxin sensitizes the immature brain to hypoxic-ischaemic injury. Eur J Neurosci. 2001;13:1101–6.10.1046/j.0953-816x.2001.01474.xSearch in Google Scholar

[131] Hagberg H, Peebles D, Mallard C. Models of white matter injury: comparison of infectious, hypoxic-ischemic, and excitotoxic insults. Ment Retard Dev Disabil Res Rev. 2002;8:30–8.10.1002/mrdd.10007Search in Google Scholar

[132] Choi EK, Park D, Kim TK, Lee SH, Bae DK, Yang G, et al. Animal models of periventricular leukomalacia. Lab Anim Res. 2011;27:77–84.10.5625/lar.2011.27.2.77Search in Google Scholar

[133] Brochu ME, Girard S, Lavoie K, Sebire G. Developmental regulation of the neuroinflammatory responses to LPS and/or hypoxia-ischemia between preterm and term neonates: An experimental study. J Neuroinflammation. 2011;8:55.10.1186/1742-2094-8-55Search in Google Scholar

[134] Maxwell JR, Denson JL, Joste NE, Robinson S, Jantzie LL. Combined in utero hypoxia-ischemia and lipopolysaccharide administration in rats induces chorioamnionitis and a fetal inflammatory response syndrome. Placenta. 2015;36:1378–84.10.1016/j.placenta.2015.10.009Search in Google Scholar

[135] Jantzie LL, Corbett CJ, Berglass J, Firl DJ, Flores J, Mannix R, et al. Complex pattern of interaction between in utero hypoxia-ischemia and intra-amniotic inflammation disrupts brain development and motor function. J Neuroinflammation. 2014;11:131.10.1186/1742-2094-11-131Search in Google Scholar

[136] Roberts D, Dalziel S. Antenatal corticosteroids for accelerating fetal lung maturation for women at risk of preterm birth. Cochrane Database Syst Rev. 2006:CD004454.10.1002/14651858.CD004454.pub2Search in Google Scholar

[137] Deulofeut R, Sola A, Lee B, Buchter S, Rahman M, Rogido M. The impact of vaginal delivery in premature infants weighing less than 1,251 grams. Obstet Gynecol. 2005;105:525–31.10.1097/01.AOG.0000154156.51578.50Search in Google Scholar

[138] Ment LR, Oh W, Ehrenkranz RA, Philip AG, Duncan CC, Makuch RW. Antenatal steroids, delivery mode, and intraventricular hemorrhage in preterm infants. Am J Obstet Gynecol. 1995;172:795–800.10.1016/0002-9378(95)90001-2Search in Google Scholar

[139] Dani C, Poggi C, Bertini G, Pratesi S, Di Tommaso M, Scarselli G, et al. Method of delivery and intraventricular haemorrhage in extremely preterm infants. J Matern Fetal Neonatal Med. 2010;23:1419–23.10.3109/14767051003678218Search in Google Scholar PubMed

[140] Minguez-Milio JA, Alcazar JL, Auba M, Ruiz-Zambrana A, Minguez J. Perinatal outcome and long-term follow-up of extremely low birth weight infants depending on the mode of delivery. J Matern Fetal Neonatal Med. 2011;24:1235–8.10.3109/14767058.2011.552990Search in Google Scholar PubMed

[141] Malloy MH, Onstad L, Wright E. The effect of cesarean delivery on birth outcome in very low birth weight infants. National Institute of Child Health and Human Development Neonatal Research Network. Obstet Gynecol. 1991;77:498–503.Search in Google Scholar