[Skip to Content]
[Skip to Content Landing]
Figure 1.
PRISMA Flowchart of the Systematic Search
PRISMA Flowchart of the Systematic Search

BPD indicates bronchopulmonary dysplasia; and CA, chorioamnionitis.

Figure 2.
Meta-analyses of the Association Between Chorioamnionitis (CA) and Bronchopulmonary Dysplasia (BPD)
Meta-analyses of the Association Between Chorioamnionitis (CA) and Bronchopulmonary Dysplasia (BPD)

Grouped by definition of CA. OR indicates odds ratio.

Figure 3.
Meta-analysis of the Association Between Chorioamnionitis (CA) and Respiratory Distress Syndrome (RDS)
Meta-analysis of the Association Between Chorioamnionitis (CA) and Respiratory Distress Syndrome (RDS)

Grouped by definition of CA and severity of RDS. OR indicates odds ratio.

Figure 4.
Multivariate Metaregression Analysis of Chorioamnionitis (CA) and Bronchopulmonary Dysplasia (BPD) and CA and Respiratory Distress Syndrome
Multivariate Metaregression Analysis of Chorioamnionitis (CA) and Bronchopulmonary Dysplasia (BPD) and CA and Respiratory Distress Syndrome

Multivariate regression model with backward elimination, controlling for difference in gestational age between CA-exposed and CA-unexposed infants. A total of 27 studies were included (coefficient, 0.31; 95% CI, 0.09-0.54; P = .007; R2 equivalent, 0.64). BPD36 indicates BPD with supplemental oxygen requirement at the postmenstrual age of 36 weeks.

Table.  
Meta-analyses of the Association Between Exposure to Chorioamnionitis and Baseline Characteristics and Outcomesa
Meta-analyses of the Association Between Exposure to Chorioamnionitis and Baseline Characteristics and Outcomesa
Supplement.

eFigure 1. Meta-Analysis of the Association Between Chorioamnionitis and All Bronchopulmonary Dysplasia

eFigure 2. Meta-Analysis of the Association Between Histological Chorioamnionitis and Moderate/Severe Bronchopulmonary Dysplasia

eFigure 3. Meta-Analysis of the Association Between Different Types of Chorioamnionitis and Moderate/Severe Bronchopulmonary Dysplasia

eFigure 4. Meta-Analysis of the Association Between Chorioamnionitis and Mild Bronchopulmonary Dysplasia

eFigure 5. Meta-Analysis of the Association Between Chorioamnionitis and Moderate Bronchopulmonary Dysplasia

eFigure 6. Meta-Analysis of the Association Between Chorioamnionitis and Severe Bronchopulmonary Dysplasia

eFigure 7. Meta-Analysis of the Association Between Funisitis and Bronchopulmonary Dysplasia

eFigure 8. Meta-Analysis of Chorioamnionitis and BPD28, Grouped by Use of Adjusted/Unadjusted Odds Ratios

eFigure 9. Meta-Analysis of Chorioamnionitis and BPD36, Grouped by Use of Adjusted/Unadjusted Odds Ratios

eFigure 10. Meta-Analysis of the Association Between Chorioamnionitis and all Respiratory Distress Syndrome

eFigure 11. Meta-Analysis of the Association Between Chorioamnionitis and Severe RDS

eFigure 12. Meta-Regression Plot of Association Between Chorioamnionitis and BPD36 Controlling for Difference in Gestational Age

eFigure 13. Meta-Regression Plot of Association Between Chorioamnionitis and BPD36 Controlling for Risk of RDS

eFigure 14. Meta-Analysis of Chorioamnionitis and BPD28, Grouped by Difference in Gestational Age

eFigure 15. Meta-Analysis of Chorioamnionitis and BPD36, Grouped by Significant/Nonsignificant Difference in Gestational Age

eFigure 16. Funnel Plots Assessing Publication Bias for the Association Between Chorioamnionitis and Bronchopulmonary Dysplasia

eTable 1. Characteristics of All Included Studies

eTable 2. Meta-Regression Analyses of Risk of BPD and Covariates

eTable 3. Newcastle-Ottawa Quality Assessment of Included Studies

1.
Farstad  T, Bratlid  D, Medbø  S, Markestad  T; Norwegian Extreme Prematurity Study Group.  Bronchopulmonary dysplasia—prevalence, severity and predictive factors in a national cohort of extremely premature infants.  Acta Paediatr. 2011;100(1):53-58. doi:10.1111/j.1651-2227.2010.01959.xPubMedGoogle ScholarCrossref
2.
Jobe  AH, Bancalari  E.  Bronchopulmonary dysplasia.  Am J Respir Crit Care Med. 2001;163(7):1723-1729. doi:10.1164/ajrccm.163.7.2011060PubMedGoogle ScholarCrossref
3.
Kramer  BW.  Antenatal inflammation and lung injury: prenatal origin of neonatal disease.  J Perinatol. 2008;28(suppl 1):S21-S27. doi:10.1038/jp.2008.46PubMedGoogle ScholarCrossref
4.
Kramer  BW, Kallapur  S, Newnham  J, Jobe  AH, eds.  Prenatal Inflammation and Lung Development: Seminars in Fetal and Neonatal Medicine. Amsterdam, the Netherlands: Elsevier; 2009. doi:10.1016/j.siny.2008.08.011
5.
Higgins  RD, Jobe  AH, Koso-Thomas  M,  et al.  Bronchopulmonary dysplasia: executive summary of a workshop.  J Pediatr. 2018;197:300-308. doi:10.1016/j.jpeds.2018.01.043PubMedGoogle ScholarCrossref
6.
Abman  SH, Collaco  JM, Shepherd  EG,  et al; Bronchopulmonary Dysplasia Collaborative.  Interdisciplinary care of children with severe bronchopulmonary dysplasia.  J Pediatr. 2017;181:12-28.e1. doi:10.1016/j.jpeds.2016.10.082PubMedGoogle ScholarCrossref
7.
Stoll  BJ, Hansen  NI, Bell  EF,  et al; Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network.  Trends in care practices, morbidity, and mortality of extremely preterm neonates, 1993-2012.  JAMA. 2015;314(10):1039-1051. doi:10.1001/jama.2015.10244PubMedGoogle ScholarCrossref
8.
Shahzad  T, Radajewski  S, Chao  C-M, Bellusci  S, Ehrhardt  H.  Pathogenesis of bronchopulmonary dysplasia: when inflammation meets organ development.  Mol Cell Pediatr. 2016;3(1):23. doi:10.1186/s40348-016-0051-9PubMedGoogle ScholarCrossref
9.
Speer  CP.  Chorioamnionitis, postnatal factors and proinflammatory response in the pathogenetic sequence of bronchopulmonary dysplasia.  Neonatology. 2009;95(4):353-361. doi:10.1159/000209301PubMedGoogle ScholarCrossref
10.
Hartling  L, Liang  Y, Lacaze-Masmonteil  T.  Chorioamnionitis as a risk factor for bronchopulmonary dysplasia: a systematic review and meta-analysis.  Arch Dis Child Fetal Neonatal Ed. 2012;97(1):F8-F17. doi:10.1136/adc.2010.210187PubMedGoogle ScholarCrossref
11.
Thomas  W, Speer  CP.  Chorioamnionitis is essential in the evolution of bronchopulmonary dysplasia—the case in favour.  Paediatr Respir Rev. 2014;15(1):49-52.PubMedGoogle Scholar
12.
Lacaze-Masmonteil  T.  That chorioamnionitis is a risk factor for bronchopulmonary dysplasia—the case against.  Paediatr Respir Rev. 2014;15(1):53-55.PubMedGoogle Scholar
13.
Van Marter  LJ, Dammann  O, Allred  EN,  et al; Developmental Epidemiology Network Investigators.  Chorioamnionitis, mechanical ventilation, and postnatal sepsis as modulators of chronic lung disease in preterm infants.  J Pediatr. 2002;140(2):171-176. doi:10.1067/mpd.2002.121381PubMedGoogle ScholarCrossref
14.
Been  JV, Zimmermann  LJ.  Histological chorioamnionitis and respiratory outcome in preterm infants.  Arch Dis Child Fetal Neonatal Ed. 2009;94(3):F218-F225. doi:10.1136/adc.2008.150458PubMedGoogle ScholarCrossref
15.
Watterberg  KL, Demers  LM, Scott  SM, Murphy  S.  Chorioamnionitis and early lung inflammation in infants in whom bronchopulmonary dysplasia develops.  Pediatrics. 1996;97(2):210-215.PubMedGoogle Scholar
16.
Viscardi  RM.  Perinatal inflammation and lung injury.  Semin Fetal Neonatal Med. 2012;17(1):30-35. doi:10.1016/j.siny.2011.08.002PubMedGoogle ScholarCrossref
17.
Behbodi  E, Villamor-Martínez  E, Degraeuwe  PL, Villamor  E.  Chorioamnionitis appears not to be a risk factor for patent ductus arteriosus in preterm infants: a systematic review and meta-analysis.  Sci Rep. 2016;6:37967. doi:10.1038/srep37967PubMedGoogle ScholarCrossref
18.
Villamor-Martinez  E, Cavallaro  G, Raffaeli  G,  et al.  Chorioamnionitis as a risk factor for retinopathy of prematurity: an updated systematic review and meta-analysis.  PLoS One. 2018;13(10):e0205838. doi:10.1371/journal.pone.0205838PubMedGoogle Scholar
19.
Villamor-Martinez  E, Fumagalli  M, Mohammed Rahim  O,  et al.  Chorioamnionitis is a risk factor for intraventricular hemorrhage in preterm infants: a systematic review and meta-analysis.  Front Physiol. 2018;9:1253. doi:10.3389/fphys.2018.01253PubMedGoogle ScholarCrossref
20.
Stroup  DF, Berlin  JA, Morton  SC,  et al.  Meta-analysis of observational studies in epidemiology: a proposal for reporting: Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group.  JAMA. 2000;283(15):2008-2012. doi:10.1001/jama.283.15.2008PubMedGoogle ScholarCrossref
21.
Moher  D, Liberati  A, Tetzlaff  J, Altman  DG; PRISMA Group.  Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.  PLoS Med. 2009;6(7):e1000097. doi:10.1371/journal.pmed.1000097PubMedGoogle Scholar
22.
Wells  GA, Shea  B, O’Connell  D,  et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomized studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.htm. Accessed December 1, 2016.
23.
Wan  X, Wang  W, Liu  J, Tong  T.  Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range.  BMC Med Res Methodol. 2014;14(1):135. doi:10.1186/1471-2288-14-135PubMedGoogle ScholarCrossref
24.
Wan  X, Wang  W, Liu  J, Tong  T. Calculator for article ‘Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range’ 2014. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4383202/bin/12874_2014_1175_MOESM2_ESM.xlsx. Accessed September 2, 2019.
25.
Borenstein  M, Hedges  LV, Higgins  J, Rothstein  HR. Subgroup analyses. In:  Introduction to Meta-analysis. Chichester, UK: John Wiley & Sons Ltd; 2009:149-186. doi:10.1002/9780470743386.ch19
26.
Borenstein  M, Hedges  LV, Higgins  J, Rothstein  HR. Identifying and quantifying heterogeneity.  Introduction to Meta-analysis. Chichester, UK: John Wiley & Sons Ltd; 2009:107-126. doi:10.1002/9780470743386.ch16
27.
Borenstein  M, Hedges  LV, Higgins  J, Rothstein  HR. Meta-regression.  Introduction to Meta-analysis. Chichester, UK: John Wiley & Sons Ltd; 2009:187-203. doi:10.1002/9780470743386.ch20
28.
Abele-Horn  M, Genzel-Boroviczény  O, Uhlig  T, Zimmermann  A, Peters  J, Scholz  M.  Ureaplasma urealyticum colonization and bronchopulmonary dysplasia: a comparative prospective multicentre study.  Eur J Pediatr. 1998;157(12):1004-1011. doi:10.1007/s004310050987PubMedGoogle ScholarCrossref
29.
Abele-Horn  M, Peters  J, Genzel-Boroviczény  O, Wolff  C, Zimmermann  A, Gottschling  W.  Vaginal ureaplasma urealyticum colonization: influence on pregnancy outcome and neonatal morbidity.  Infection. 1997;25(5):286-291. doi:10.1007/BF01720398PubMedGoogle ScholarCrossref
30.
Ahn  HM, Park  EA, Cho  SJ, Kim  YJ, Park  HS.  The association of histological chorioamnionitis and antenatal steroids on neonatal outcome in preterm infants born at less than thirty-four weeks’ gestation.  Neonatology. 2012;102(4):259-264. doi:10.1159/000339577PubMedGoogle ScholarCrossref
31.
Arayici  S, Kadioglu Simsek  G, Oncel  MY,  et al.  The effect of histological chorioamnionitis on the short-term outcome of preterm infants ≤32 weeks: a single-center study.  J Matern Fetal Neonatal Med. 2014;27(11):1129-1133. doi:10.3109/14767058.2013.850668PubMedGoogle ScholarCrossref
32.
Barrera-Reyes  RH, Ruiz-Macías  H, Segura-Cervantes  E.  Neurodevelopment at one year of age [corrected] in preterm newborns with history of maternal chorioamnionitis  [in Spanish].  Ginecol Obstet Mex. 2011;79(1):31-37.PubMedGoogle Scholar
33.
Baud  O, Zupan  V, Lacaze-Masmonteil  T,  et al.  The relationships between antenatal management, the cause of delivery and neonatal outcome in a large cohort of very preterm singleton infants.  BJOG. 2000;107(7):877-884. doi:10.1111/j.1471-0528.2000.tb11086.xPubMedGoogle ScholarCrossref
34.
Been  JV, Rours  IG, Kornelisse  RF, Jonkers  F, de Krijger  RR, Zimmermann  LJ.  Chorioamnionitis alters the response to surfactant in preterm infants.  J Pediatr. 2010;156(1):10-15.e1. doi:10.1016/j.jpeds.2009.07.044PubMedGoogle ScholarCrossref
35.
Alfiero Bordigato  M, Piva  D, Di Gangi  IM, Giordano  G, Chiandetti  L, Filippone  M.  Asymmetric dimethylarginine in ELBW newborns exposed to chorioamnionitis.  Early Hum Dev. 2011;87(2):143-145. doi:10.1016/j.earlhumdev.2010.11.004PubMedGoogle ScholarCrossref
36.
Botet  F, Figueras  J, Carbonell-Estrany  X, Narbona  E.  The impact of clinical maternal chorioamnionitis on neurological and psychological sequelae in very-low-birth weight infants: a case-control study.  J Perinat Med. 2011;39(2):203-208. doi:10.1515/jpm.2011.005PubMedGoogle ScholarCrossref
37.
Bry  KJ, Jacobsson  B, Nilsson  S, Bry  K.  Gastric fluid cytokines are associated with chorioamnionitis and white blood cell counts in preterm infants.  Acta Paediatr. 2015;104(6):575-580. doi:10.1111/apa.12947PubMedGoogle ScholarCrossref
38.
Chisholm  KM, Heerema-McKenney  A, Tian  L,  et al.  Correlation of preterm infant illness severity with placental histology.  Placenta. 2016;39:61-69. doi:10.1016/j.placenta.2016.01.012PubMedGoogle ScholarCrossref
39.
Choi  CW, Kim  BI, Joung  KE,  et al.  Decreased expression of transforming growth factor-beta1 in bronchoalveolar lavage cells of preterm infants with maternal chorioamnionitis.  J Korean Med Sci. 2008;23(4):609-615. doi:10.3346/jkms.2008.23.4.609PubMedGoogle ScholarCrossref
40.
De Felice  C, Toti  P, Parrini  S,  et al.  Histologic chorioamnionitis and severity of illness in very low birth weight newborns.  Pediatr Crit Care Med. 2005;6(3):298-302. doi:10.1097/01.PCC.0000160658.35437.65PubMedGoogle ScholarCrossref
41.
Dempsey  E, Chen  M-F, Kokottis  T, Vallerand  D, Usher  R.  Outcome of neonates less than 30 weeks gestation with histologic chorioamnionitis.  Am J Perinatol. 2005;22(3):155-159. doi:10.1055/s-2005-865020PubMedGoogle ScholarCrossref
42.
Dessardo  NS, Dessardo  S, Mustać  E, Banac  S, Petrović  O, Peter  B.  Chronic lung disease of prematurity and early childhood wheezing: is foetal inflammatory response syndrome to blame?  Early Hum Dev. 2014;90(9):493-499. doi:10.1016/j.earlhumdev.2014.07.002PubMedGoogle ScholarCrossref
43.
Dexter  SC, Malee  MP, Pinar  H, Hogan  JW, Carpenter  MW, Vohr  BR.  Influence of chorioamnionitis on developmental outcome in very low birth weight infants.  Obstet Gynecol. 1999;94(2):267-273.PubMedGoogle Scholar
44.
Dexter  SC, Pinar  H, Malee  MP, Hogan  J, Carpenter  MW, Vohr  BR.  Outcome of very low birth weight infants with histopathologic chorioamnionitis.  Obstet Gynecol. 2000;96(2):172-177.PubMedGoogle Scholar
45.
Ecevit  A, Anuk-İnce  D, Yapakçı  E,  et al.  Association of respiratory distress syndrome and perinatal hypoxia with histologic chorioamnionitis in preterm infants.  Turk J Pediatr. 2014;56(1):56-61.PubMedGoogle Scholar
46.
Erdemir  G, Kultursay  N, Calkavur  S,  et al.  Histological chorioamnionitis: effects on premature delivery and neonatal prognosis.  Pediatr Neonatol. 2013;54(4):267-274. doi:10.1016/j.pedneo.2013.03.012PubMedGoogle ScholarCrossref
47.
Fung  G, Bawden  K, Chow  P, Yu  V.  Long-term outcome of extremely preterm infants following chorioamnionitis.  HK J Paediatr. 2003;8(2):87-92.Google Scholar
48.
Gagliardi  L, Rusconi  F, Bellù  R, Zanini  R; Italian Neonatal Network.  Association of maternal hypertension and chorioamnionitis with preterm outcomes.  Pediatrics. 2014;134(1):e154-e161. doi:10.1542/peds.2013-3898PubMedGoogle ScholarCrossref
49.
García-Muñoz Rodrigo  F, Galán Henríquez  G, Figueras Aloy  J, García-Alix Pérez  A.  Outcomes of very-low-birth-weight infants exposed to maternal clinical chorioamnionitis: a multicentre study.  Neonatology. 2014;106(3):229-234. doi:10.1159/000363127PubMedGoogle ScholarCrossref
50.
González-Luis  G, Jordán García  I, Rodríguez-Miguélez  J, Botet Mussons  F, Figueras Aloy  J.  Neonatal morbidity and mortality in very low birth weight infants according to exposure to chorioamnionitis  [in Spanish].  An Esp Pediatr. 2002;56(6):551-555.PubMedGoogle ScholarCrossref
51.
Gray  PH, Hurley  TM, Rogers  YM,  et al.  Survival and neonatal and neurodevelopmental outcome of 24-29 week gestation infants according to primary cause of preterm delivery.  Aust N Z J Obstet Gynaecol. 1997;37(2):161-168. doi:10.1111/j.1479-828X.1997.tb02245.xPubMedGoogle ScholarCrossref
52.
Hendson  L, Russell  L, Robertson  CM,  et al.  Neonatal and neurodevelopmental outcomes of very low birth weight infants with histologic chorioamnionitis.  J Pediatr. 2011;158(3):397-402. doi:10.1016/j.jpeds.2010.09.010PubMedGoogle ScholarCrossref
53.
Hitti  J, Tarczy-Hornoch  P, Murphy  J, Hillier  SL, Aura  J, Eschenbach  DA.  Amniotic fluid infection, cytokines, and adverse outcome among infants at 34 weeks’ gestation or less.  Obstet Gynecol. 2001;98(6):1080-1088.PubMedGoogle Scholar
54.
Jones  MH, Corso  AL, Tepper  RS,  et al.  Chorioamnionitis and subsequent lung function in preterm infants.  PLoS One. 2013;8(12):e81193. doi:10.1371/journal.pone.0081193PubMedGoogle Scholar
55.
Jónsson  B, Rylander  M, Faxelius  G.  Ureaplasma urealyticum, erythromycin and respiratory morbidity in high-risk preterm neonates.  Acta Paediatr. 1998;87(10):1079-1084. doi:10.1111/j.1651-2227.1998.tb01418.xPubMedGoogle ScholarCrossref
56.
Kaukola  T, Tuimala  J, Herva  R, Kingsmore  S, Hallman  M.  Cord immunoproteins as predictors of respiratory outcome in preterm infants.  Am J Obstet Gynecol. 2009;200(1):100.e1-100.e8. doi:10.1016/j.ajog.2008.07.070PubMedGoogle ScholarCrossref
57.
Kim  SY, Choi  CW, Jung  E,  et al.  Neonatal morbidities associated with histologic chorioamnionitis defined based on the site and extent of inflammation in very low birth weight infants.  J Korean Med Sci. 2015;30(10):1476-1482. doi:10.3346/jkms.2015.30.10.1476PubMedGoogle ScholarCrossref
58.
Kirchner  L, Helmer  H, Heinze  G,  et al.  Amnionitis with Ureaplasma urealyticum or other microbes leads to increased morbidity and prolonged hospitalization in very low birth weight infants.  Eur J Obstet Gynecol Reprod Biol. 2007;134(1):44-50. doi:10.1016/j.ejogrb.2006.09.013PubMedGoogle ScholarCrossref
59.
Lau  J, Magee  F, Qiu  Z, Houbé  J, Von Dadelszen  P, Lee  SK.  Chorioamnionitis with a fetal inflammatory response is associated with higher neonatal mortality, morbidity, and resource use than chorioamnionitis displaying a maternal inflammatory response only.  Am J Obstet Gynecol. 2005;193(3, pt 1):708-713. doi:10.1016/j.ajog.2005.01.017PubMedGoogle ScholarCrossref
60.
Lee  Y, Kim  H-J, Choi  S-J,  et al.  Is there a stepwise increase in neonatal morbidities according to histological stage (or grade) of acute chorioamnionitis and funisitis? effect of gestational age at delivery.  J Perinat Med. 2015;43(2):259-267. doi:10.1515/jpm-2014-0035PubMedGoogle ScholarCrossref
61.
Liu  Z, Tang  Z, Li  J, Yang  Y.  Effects of placental inflammation on neonatal outcome in preterm infants.  Pediatr Neonatol. 2014;55(1):35-40. doi:10.1016/j.pedneo.2013.05.007PubMedGoogle ScholarCrossref
62.
Mehta  R, Nanjundaswamy  S, Shen-Schwarz  S, Petrova  A.  Neonatal morbidity and placental pathology.  Indian J Pediatr. 2006;73(1):25-28. doi:10.1007/BF02758255PubMedGoogle ScholarCrossref
63.
Mestan  K, Yu  Y, Matoba  N,  et al.  Placental inflammatory response is associated with poor neonatal growth: preterm birth cohort study.  Pediatrics. 2010;125(4):e891-e898. doi:10.1542/peds.2009-0313PubMedGoogle ScholarCrossref
64.
Miralles  R, Hodge  R, Kotecha  S.  Fetal cortisol response to intrauterine microbial colonisation identified by the polymerase chain reaction and fetal inflammation.  Arch Dis Child Fetal Neonatal Ed. 2008;93(1):F51-F54. doi:10.1136/adc.2006.110130PubMedGoogle ScholarCrossref
65.
Misra  R, Shah  S, Fowell  D,  et al.  Preterm cord blood CD4+ T cells exhibit increased IL-6 production in chorioamnionitis and decreased CD4+ T cells in bronchopulmonary dysplasia.  Hum Immunol. 2015;76(5):329-338. doi:10.1016/j.humimm.2015.03.007PubMedGoogle ScholarCrossref
66.
Miyazaki  K, Furuhashi  M, Ishikawa  K,  et al.  Impact of chorioamnionitis on short- and long-term outcomes in very low birth weight preterm infants: the Neonatal Research Network Japan.  J Matern Fetal Neonatal Med. 2016;29(2):331-337. doi:10.3109/14767058.2014.1000852PubMedGoogle ScholarCrossref
67.
Mu  SC, Lin  CH, Chen  YL,  et al.  Impact on neonatal outcome and anthropometric growth in very low birth weight infants with histological chorioamnionitis.  J Formos Med Assoc. 2008;107(4):304-310. doi:10.1016/S0929-6646(08)60091-1PubMedGoogle ScholarCrossref
68.
Nasef  N, Shabaan  AE, Schurr  P,  et al.  Effect of clinical and histological chorioamnionitis on the outcome of preterm infants.  Am J Perinatol. 2013;30(1):59-68. doi:10.1055/s-0032-1321501PubMedGoogle Scholar
69.
Nicaise  C, Gire  C, Fagianelli  P,  et al.  Neonatal consequences of preterm premature rupture of membrane (PPROM) at 24-34 WG: 118 singleton pregnancies  [in French].  J Gynecol Obstet Biol Reprod (Paris). 2002;31(8):747-754.PubMedGoogle Scholar
70.
Nishimaki  S, Shima  Y, Sato  M,  et al.  Urinary β2-microglobulin in premature infants with chorioamnionitis and chronic lung disease.  J Pediatr. 2003;143(1):120-122. doi:10.1016/S0022-3476(03)00249-XPubMedGoogle ScholarCrossref
71.
Ogunyemi  D, Murillo  M, Jackson  U, Hunter  N, Alperson  B.  The relationship between placental histopathology findings and perinatal outcome in preterm infants.  J Matern Fetal Neonatal Med. 2003;13(2):102-109. doi:10.1080/jmf.13.2.102.109PubMedGoogle ScholarCrossref
72.
Oh  S-H, Kim  J-j, Do  H-j, Lee  BS, Kim  K-S, Kim  EA-R.  Preliminary study on neurodevelopmental outcome and placental pathology among extremely low birth weight infants.  Korean J Perinatol. 2015;26(1):67-77. doi:10.14734/kjp.2015.26.1.67Google ScholarCrossref
73.
Ohyama  M, Itani  Y, Yamanaka  M,  et al.  Re-evaluation of chorioamnionitis and funisitis with a special reference to subacute chorioamnionitis.  Hum Pathol. 2002;33(2):183-190. doi:10.1053/hupa.2002.31291PubMedGoogle ScholarCrossref
74.
O’Shea  TM, Klinepeter  KL, Meis  PJ, Dillard  RG.  Intrauterine infection and the risk of cerebral palsy in very low-birthweight infants.  Paediatr Perinat Epidemiol. 1998;12(1):72-83. doi:10.1111/j.1365-3016.1998.00081.xPubMedGoogle ScholarCrossref
75.
Pappas  A, Kendrick  DE, Shankaran  S,  et al; Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network.  Chorioamnionitis and early childhood outcomes among extremely low-gestational-age neonates.  JAMA Pediatr. 2014;168(2):137-147. doi:10.1001/jamapediatrics.2013.4248PubMedGoogle ScholarCrossref
76.
Perrone  S, Toti  P, Toti  MS,  et al.  Perinatal outcome and placental histological characteristics: a single-center study.  J Matern Fetal Neonatal Med. 2012;25(suppl 1):110-113. doi:10.3109/14767058.2012.664344PubMedGoogle ScholarCrossref
77.
Plakkal  N, Soraisham  AS, Trevenen  C, Freiheit  EA, Sauve  R.  Histological chorioamnionitis and bronchopulmonary dysplasia: a retrospective cohort study.  J Perinatol. 2013;33(6):441-445. doi:10.1038/jp.2012.154PubMedGoogle ScholarCrossref
78.
Polam  S, Koons  A, Anwar  M, Shen-Schwarz  S, Hegyi  T.  Effect of chorioamnionitis on neurodevelopmental outcome in preterm infants.  Arch Pediatr Adolesc Med. 2005;159(11):1032-1035. doi:10.1001/archpedi.159.11.1032PubMedGoogle ScholarCrossref
79.
Prendergast  M, May  C, Broughton  S,  et al.  Chorioamnionitis, lung function and bronchopulmonary dysplasia in prematurely born infants.  Arch Dis Child Fetal Neonatal Ed. 2011;96(4):F270-F274. doi:10.1136/adc.2010.189480PubMedGoogle ScholarCrossref
80.
Redline  RW, Wilson-Costello  D, Hack  M.  Placental and other perinatal risk factors for chronic lung disease in very low birth weight infants.  Pediatr Res. 2002;52(5):713-719. doi:10.1203/00006450-200211000-00017PubMedGoogle ScholarCrossref
81.
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(5):1357-1365. doi:10.1016/j.ajog.2006.03.053PubMedGoogle ScholarCrossref
82.
Rocha  G, Proença  E, Quintas  C, Rodrigues  T, Guimarães  H.  Chorioamnionitis and neonatal morbidity  [in Portuguese].  Act Med Port. 2006;19(3):207-212. PubMedGoogle Scholar
83.
Sato  M, Nishimaki  S, Yokota  S,  et al.  Severity of chorioamnionitis and neonatal outcome.  J Obstet Gynaecol Res. 2011;37(10):1313-1319. doi:10.1111/j.1447-0756.2010.01519.xPubMedGoogle ScholarCrossref
84.
Schlapbach  LJ, Ersch  J, Adams  M, Bernet  V, Bucher  HU, Latal  B.  Impact of chorioamnionitis and preeclampsia on neurodevelopmental outcome in preterm infants below 32 weeks gestational age.  Acta Paediatr. 2010;99(10):1504-1509. doi:10.1111/j.1651-2227.2010.01861.xPubMedGoogle ScholarCrossref
85.
Seliga-Siwecka  JP, Kornacka  MK.  Neonatal outcome of preterm infants born to mothers with abnormal genital tract colonisation and chorioamnionitis: a cohort study.  Early Hum Dev. 2013;89(5):271-275. doi:10.1016/j.earlhumdev.2012.10.003PubMedGoogle ScholarCrossref
86.
Smit  AL, Been  JV, Zimmermann  LJ,  et al.  Automated auditory brainstem response in preterm newborns with histological chorioamnionitis.  J Matern Fetal Neonatal Med. 2015;28(15):1864-1869. doi:10.3109/14767058.2014.971747PubMedGoogle ScholarCrossref
87.
Soraisham  AS, Singhal  N, McMillan  DD, Sauve  RS, Lee  SK; Canadian Neonatal Network.  A multicenter study on the clinical outcome of chorioamnionitis in preterm infants.  Am J Obstet Gynecol. 2009;200(4):372.e1-372.e6. doi:10.1016/j.ajog.2008.11.034PubMedGoogle ScholarCrossref
88.
Soraisham  AS, Trevenen  C, Wood  S, Singhal  N, Sauve  R.  Histological chorioamnionitis and neurodevelopmental outcome in preterm infants.  J Perinatol. 2013;33(1):70-75. doi:10.1038/jp.2012.49PubMedGoogle ScholarCrossref
89.
Stepan  M, Cobo  T, Maly  J,  et al.  Neonatal outcomes in subgroups of women with preterm prelabor rupture of membranes before 34 weeks.  J Matern Fetal Neonatal Med. 2016;29(14):2373-2377.PubMedGoogle Scholar
90.
Strunk  T, Doherty  D, Jacques  A,  et al.  Histologic chorioamnionitis is associated with reduced risk of late-onset sepsis in preterm infants.  Pediatrics. 2012;129(1):e134-e141. doi:10.1542/peds.2010-3493PubMedGoogle ScholarCrossref
91.
Suppiej  A, Franzoi  M, Vedovato  S, Marucco  A, Chiarelli  S, Zanardo  V.  Neurodevelopmental outcome in preterm histological chorioamnionitis.  Early Hum Dev. 2009;85(3):187-189. doi:10.1016/j.earlhumdev.2008.09.410PubMedGoogle ScholarCrossref
92.
Thomas  W, Seidenspinner  S, Kramer  BW,  et al.  Airway concentrations of angiopoietin-1 and endostatin in ventilated extremely premature infants are decreased after funisitis and unbalanced with bronchopulmonary dysplasia/death.  Pediatr Res. 2009;65(4):468-473. doi:10.1203/PDR.0b013e3181991f35PubMedGoogle ScholarCrossref
93.
Trevisanuto  D, Peruzzetto  C, Cavallin  F,  et al.  Fetal placental inflammation is associated with poor neonatal growth of preterm infants: a case-control study.  J Matern Fetal Neonatal Med. 2013;26(15):1484-1490. doi:10.3109/14767058.2013.789849PubMedGoogle ScholarCrossref
94.
Tsiartas  P, Kacerovsky  M, Musilova  I,  et al.  The association between histological chorioamnionitis, funisitis and neonatal outcome in women with preterm prelabor rupture of membranes.  J Matern Fetal Neonatal Med. 2013;26(13):1332-1336. doi:10.3109/14767058.2013.784741PubMedGoogle ScholarCrossref
95.
van Vliet  EO, de Kieviet  JF, van der Voorn  JP, Been  JV, Oosterlaan  J, van Elburg  RM.  Placental pathology and long-term neurodevelopment of very preterm infants.  Am J Obstet Gynecol. 2012;206(6):489.e1-489.e7. doi:10.1016/j.ajog.2012.03.024PubMedGoogle ScholarCrossref
96.
Watterberg  KL, Gerdes  JS, Gifford  KL, Lin  H-M.  Prophylaxis against early adrenal insufficiency to prevent chronic lung disease in premature infants.  Pediatrics. 1999;104(6):1258-1263. doi:10.1542/peds.104.6.1258PubMedGoogle ScholarCrossref
97.
Wirbelauer  J, Thomas  W, Speer  CP.  Response of leukocytes and nucleated red blood cells in very low-birth weight preterm infants after exposure to intrauterine inflammation.  J Matern Fetal Neonatal Med. 2011;24(2):348-353. doi:10.3109/14767058.2010.497568PubMedGoogle ScholarCrossref
98.
Xie  A, Zhang  W, Chen  M,  et al.  Related factors and adverse neonatal outcomes in women with preterm premature rupture of membranes complicated by histologic chorioamnionitis.  Med Sci Monit. 2015;21:390-395. doi:10.12659/MSM.891203PubMedGoogle ScholarCrossref
99.
Young  KC, Del Moral  T, Claure  N, Vanbuskirk  S, Bancalari  E.  The association between early tracheal colonization and bronchopulmonary dysplasia.  J Perinatol. 2005;25(6):403-407. doi:10.1038/sj.jp.7211297PubMedGoogle ScholarCrossref
100.
Zanardo  V, Savio  V, Giacomin  C, Rinaldi  A, Marzari  F, Chiarelli  S.  Relationship between neonatal leukemoid reaction and bronchopulmonary dysplasia in low-birth-weight infants: a cross-sectional study.  Am J Perinatol. 2002;19(7):379-386. doi:10.1055/s-2002-35612PubMedGoogle ScholarCrossref
101.
Zanardo  V, Vedovato  S, Suppiej  A,  et al.  Histological inflammatory responses in the placenta and early neonatal brain injury.  Pediatr Dev Pathol. 2008;11(5):350-354. doi:10.2350/07-08-0324.1PubMedGoogle ScholarCrossref
102.
Alshehri  MA.  Are preterm infants at high altitude at greater risk for the development of bronchopulmonary dysplasia?  J Trop Pediatr. 2014;60(1):68-73. doi:10.1093/tropej/fmt079PubMedGoogle ScholarCrossref
103.
Ameenudeen  SA, Boo  NY, Chan  LG.  Risk factors associated with chronic lung disease in Malaysian very low birthweight infants.  Med J Malaysia. 2007;62(1):40-45.PubMedGoogle Scholar
104.
Bagchi  A, Viscardi  RM, Taciak  V, Ensor  JE, McCrea  KA, Hasday  JD.  Increased activity of interleukin-6 but not tumor necrosis factor-α in lung lavage of premature infants is associated with the development of bronchopulmonary dysplasia.  Pediatr Res. 1994;36(2):244-252. doi:10.1203/00006450-199408000-00017PubMedGoogle ScholarCrossref
105.
Baier  RJ, Loggins  J, Kruger  TE.  Interleukin-4 and 13 concentrations in infants at risk to develop bronchopulmonary dysplasia.  BMC Pediatr. 2003;3(1):8. doi:10.1186/1471-2431-3-8PubMedGoogle ScholarCrossref
106.
Baker  CD, Balasubramaniam  V, Mourani  PM,  et al.  Cord blood angiogenic progenitor cells are decreased in bronchopulmonary dysplasia.  Eur Respir J. 2012;40(6):1516-1522. doi:10.1183/09031936.00017312PubMedGoogle ScholarCrossref
107.
Bose  C, Laughon  M, Allred  EN,  et al; Elgan Study Investigators.  Blood protein concentrations in the first two postnatal weeks that predict bronchopulmonary dysplasia among infants born before the 28th week of gestation.  Pediatr Res. 2011;69(4):347-353. doi:10.1203/PDR.0b013e31820a58f3PubMedGoogle ScholarCrossref
108.
Brener Dik  PH, Niño Gualdron  YM, Galletti  MF, Cribioli  CM, Mariani  GL.  Bronchopulmonary dysplasia: incidence and risk factors  [in Spanish].  Arch Argent Pediatr. 2017;115(5):476-482.PubMedGoogle Scholar
109.
Cederqvist  K, Haglund  C, Heikkilä  P,  et al.  Pulmonary trypsin-2 in the development of bronchopulmonary dysplasia in preterm infants.  Pediatrics. 2003;112(3, pt 1):570-577. doi:10.1542/peds.112.3.570PubMedGoogle ScholarCrossref
110.
Choi  CW, Kim  BI, Park  JD, Koh  YY, Choi  JH, Choi  JY.  Risk factors for the different types of chronic lung diseases of prematurity according to the preceding respiratory distress syndrome.  Pediatr Int. 2005;47(4):417-423. doi:10.1111/j.1442-200x.2005.02081.xPubMedGoogle ScholarCrossref
111.
Colaizy  TT, Morris  CD, Lapidus  J, Sklar  RS, Pillers  D-AM.  Detection of ureaplasma DNA in endotracheal samples is associated with bronchopulmonary dysplasia after adjustment for multiple risk factors.  Pediatr Res. 2007;61(5, pt 1):578-583. doi:10.1203/pdr.0b013e318045be03PubMedGoogle ScholarCrossref
112.
de Felice  C, Latini  G, Parrini  S,  et al.  Oral mucosal microvascular abnormalities: an early marker of bronchopulmonary dysplasia.  Pediatr Res. 2004;56(6):927-931. doi:10.1203/01.PDR.0000145259.85418.1DPubMedGoogle ScholarCrossref
113.
Demirel  N, Bas  AY, Zenciroglu  A.  Bronchopulmonary dysplasia in very low birth weight infants.  Indian J Pediatr. 2009;76(7):695-698. doi:10.1007/s12098-009-0110-5PubMedGoogle ScholarCrossref
114.
Fujioka  K, Shibata  A, Yokota  T,  et al.  Association of a vascular endothelial growth factor polymorphism with the development of bronchopulmonary dysplasia in Japanese premature newborns.  Sci Rep. 2014;4:4459. doi:10.1038/srep04459PubMedGoogle ScholarCrossref
115.
Fukunaga  S, Ichiyama  T, Maeba  S,  et al.  MMP-9 and TIMP-1 in the cord blood of premature infants developing BPD.  Pediatr Pulmonol. 2009;44(3):267-272. doi:10.1002/ppul.20993PubMedGoogle ScholarCrossref
116.
Gantar  IŠ, Babnik  J, Cerar  LK, Šinkovec  J, Wraber  B.  Prenatal and postnatal risk factors for developing bronchopulmonary dysplasia.  Signa Vitae. 2011;6(2):46-51. doi:10.22514/SV62.102011.6Google ScholarCrossref
117.
Ghezzi  F, Gomez  R, Romero  R,  et al.  Elevated interleukin-8 concentrations in amniotic fluid of mothers whose neonates subsequently develop bronchopulmonary dysplasia.  Eur J Obstet Gynecol Reprod Biol. 1998;78(1):5-10. doi:10.1016/S0301-2115(97)00236-4PubMedGoogle ScholarCrossref
118.
EXPRESS Group.  Incidence of and risk factors for neonatal morbidity after active perinatal care: extremely preterm infants study in Sweden (EXPRESS).  Acta Paediatr. 2010;99(7):978-992. doi:10.1111/j.1651-2227.2010.01846.xPubMedGoogle ScholarCrossref
119.
Guimarães  H, Rocha  G, Vasconcellos  G,  et al.  Risk factors for bronchopulmonary dysplasia in five Portuguese neonatal intensive care units.  Rev Port Pneumol. 2010;16(3):419-430. doi:10.1016/S0873-2159(15)30039-8PubMedGoogle ScholarCrossref
120.
Guo  MM-H, Chung  C-H, Chen  F-S, Chen  C-C, Huang  H-C, Chung  M-Y.  Severe bronchopulmonary dysplasia is associated with higher fluid intake in very low-birth-weight infants: a retrospective study.  Am J Perinatol. 2015;30(2):155-162. doi:10.1055/s-0034-1376393PubMedGoogle ScholarCrossref
121.
Hansen  AR, Barnés  CM, Folkman  J, McElrath  TF.  Maternal preeclampsia predicts the development of bronchopulmonary dysplasia.  J Pediatr. 2010;156(4):532-536. doi:10.1016/j.jpeds.2009.10.018PubMedGoogle ScholarCrossref
122.
Hikino  S, Ohga  S, Kinjo  T,  et al.  Tracheal aspirate gene expression in preterm newborns and development of bronchopulmonary dysplasia.  Pediatr Int. 2012;54(2):208-214. doi:10.1111/j.1442-200X.2011.03510.xPubMedGoogle ScholarCrossref
123.
Hyödynmaa  E, Korhonen  P, Ahonen  S, Luukkaala  T, Tammela  O.  Frequency and clinical correlates of radiographic patterns of bronchopulmonary dysplasia in very low birth weight infants by term age.  Eur J Pediatr. 2012;171(1):95-102. doi:10.1007/s00431-011-1486-6PubMedGoogle ScholarCrossref
124.
Ikeda  S, Kihira  K, Yokoi  A, Tamakoshi  K, Miyazaki  K, Furuhashi  M.  The levels of the neutrophil elastase in the amniotic fluid of pregnant women whose infants develop bronchopulmonary dysplasia.  J Matern Fetal Neonatal Med. 2015;28(4):479-483. doi:10.3109/14767058.2014.921674PubMedGoogle ScholarCrossref
125.
Iwatani  S, Mizobuchi  M, Tanaka  S,  et al.  Increased volume of tracheal aspirate fluid predicts the development of bronchopulmonary dysplasia.  Early Hum Dev. 2013;89(2):113-117. doi:10.1016/j.earlhumdev.2012.08.007PubMedGoogle ScholarCrossref
126.
Kalra  VK, Aggarwal  S, Arora  P, Natarajan  G.  B-type natriuretic peptide levels in preterm neonates with bronchopulmonary dysplasia: a marker of severity?  Pediatr Pulmonol. 2014;49(11):1106-1111. doi:10.1002/ppul.22942PubMedGoogle ScholarCrossref
127.
Kandasamy  J, Roane  C, Szalai  A, Ambalavanan  N.  Serum eotaxin-1 is increased in extremely-low-birth-weight infants with bronchopulmonary dysplasia or death.  Pediatr Res. 2015;78(5):498-504. doi:10.1038/pr.2015.152PubMedGoogle ScholarCrossref
128.
Karagianni  P, Rallis  D, Fidani  L,  et al.  Glutathion-S-transferase P1 polymorphisms association with broncopulmonary dysplasia in preterm infants.  Hippokratia. 2013;17(4):363-367.PubMedGoogle Scholar
129.
Karagianni  P, Tsakalidis  C, Kyriakidou  M,  et al.  Neuromotor outcomes in infants with bronchopulmonary dysplasia.  Pediatr Neurol. 2011;44(1):40-46. doi:10.1016/j.pediatrneurol.2010.07.008PubMedGoogle ScholarCrossref
130.
Kazzi  SNJ, Kim  UO, Quasney  MW, Buhimschi  I.  Polymorphism of tumor necrosis factor-α and risk and severity of bronchopulmonary dysplasia among very low birth weight infants.  Pediatrics. 2004;114(2):e243-e248. doi:10.1542/peds.114.2.e243PubMedGoogle ScholarCrossref
131.
Akram Khan  M, Kuzma-O’Reilly  B, Brodsky  NL, Bhandari  V.  Site-specific characteristics of infants developing bronchopulmonary dysplasia.  J Perinatol. 2006;26(7):428-435. doi:10.1038/sj.jp.7211538PubMedGoogle ScholarCrossref
132.
Kim  D-H, Kim  H-S, Shim  S-Y,  et al.  Cord blood KL-6, a specific lung injury marker, correlates with the subsequent development and severity of atypical bronchopulmonary dysplasia.  Neonatology. 2008;93(4):223-229. doi:10.1159/000111100PubMedGoogle ScholarCrossref
133.
Klinger  G, Sokolover  N, Boyko  V, Sirota  L, Lerner-Geva  L, Reichman  B; Israel Neonatal Network.  Perinatal risk factors for bronchopulmonary dysplasia in a national cohort of very-low-birthweight infants.  Am J Obstet Gynecol. 2013;208(2):115.e1-115.e9. doi:10.1016/j.ajog.2012.11.026PubMedGoogle ScholarCrossref
134.
Koroglu  OA, Yalaz  M, Levent  E, Akisu  M, Kültürsay  N.  Cardiovascular consequences of bronchopulmonary dysplasia in prematurely born preschool children.  Neonatology. 2013;104(4):283-289. doi:10.1159/000354542PubMedGoogle ScholarCrossref
135.
Lamboley-Gilmert  G, Lacaze-Masmonteil  T; Neonatologists of the Curosurf Postmarketing French Study.  The short-term outcome of a large cohort of very preterm infants treated with poractant alfa (Curosurf) for respiratory distress syndrome: a postmarketing phase IV study.  Paediatr Drugs. 2003;5(9):639-645. doi:10.2165/00148581-200305090-00006PubMedGoogle ScholarCrossref
136.
Lapcharoensap  W, Gage  SC, Kan  P,  et al.  Hospital variation and risk factors for bronchopulmonary dysplasia in a population-based cohort.  JAMA Pediatr. 2015;169(2):e143676. doi:10.1001/jamapediatrics.2014.3676PubMedGoogle Scholar
137.
Lardón-Fernández  M, Uberos  J, Molina-Oya  M, Narbona-López  E.  Epidemiological factors involved in the development of bronchopulmonary dysplasia in very low birth-weight preterm infants.  Minerva Pediatr. 2017;69(1):42-49.PubMedGoogle Scholar
138.
Leroy  S, Caumette  E, Waddington  C, Hébert  A, Brant  R, Lavoie  PM.  A time-based analysis of inflammation in infants at risk of bronchopulmonary dysplasia.  J Pediatr. 2018;192:60-65.e1. doi:10.1016/j.jpeds.2017.09.011PubMedGoogle ScholarCrossref
139.
Li  Y, Cui  Y, Wang  C, Liu  X, Han  J.  A risk factor analysis on disease severity in 47 premature infants with bronchopulmonary dysplasia.  Intractable Rare Dis Res. 2015;4(2):82-86. doi:10.5582/irdr.2015.01000PubMedGoogle ScholarCrossref
140.
Lin  H-C, Su  B-H, Chang  J-S, Hsu  C-M, Tsai  C-H, Tsai  F-J.  Nonassociation of interleukin 4 intron 3 and 590 promoter polymorphisms with bronchopulmonary dysplasia for ventilated preterm infants.  Biol Neonate. 2005;87(3):181-186. doi:10.1159/000082937PubMedGoogle ScholarCrossref
141.
Lodha  A, Sauvé  R, Bhandari  V,  et al.  Need for supplemental oxygen at discharge in infants with bronchopulmonary dysplasia is not associated with worse neurodevelopmental outcomes at 3 years corrected age.  PLoS One. 2014;9(3):e90843. doi:10.1371/journal.pone.0090843PubMedGoogle Scholar
142.
Lohmann  P, Luna  RA, Hollister  EB,  et al.  The airway microbiome of intubated premature infants: characteristics and changes that predict the development of bronchopulmonary dysplasia.  Pediatr Res. 2014;76(3):294-301. doi:10.1038/pr.2014.85PubMedGoogle ScholarCrossref
143.
Mahlman  M, Karjalainen  MK, Huusko  JM,  et al.  Genome-wide association study of bronchopulmonary dysplasia: a potential role for variants near the CRP gene.  Sci Rep. 2017;7(1):9271. doi:10.1038/s41598-017-08977-wPubMedGoogle ScholarCrossref
144.
Mailaparambil  B, Krueger  M, Heizmann  U, Schlegel  K, Heinze  J, Heinzmann  A.  Genetic and epidemiological risk factors in the development of bronchopulmonary dysplasia.  Dis Markers. 2010;29(1):1-9. doi:10.1155/2010/925940PubMedGoogle ScholarCrossref
145.
May  C, Patel  S, Kennedy  C,  et al.  Prediction of bronchopulmonary dysplasia.  Arch Dis Child Fetal Neonatal Ed. 2011;96(6):F410-F416. doi:10.1136/adc.2010.189597PubMedGoogle ScholarCrossref
146.
McGowan  EC, Kostadinov  S, McLean  K,  et al.  Placental IL-10 dysregulation and association with bronchopulmonary dysplasia risk.  Pediatr Res. 2009;66(4):455-460. doi:10.1203/PDR.0b013e3181b3b0faPubMedGoogle ScholarCrossref
147.
Mittendorf  R, Covert  R, Montag  AG,  et al.  Special relationships between fetal inflammatory response syndrome and bronchopulmonary dysplasia in neonates.  J Perinat Med. 2005;33(5):428-434. doi:10.1515/JPM.2005.076PubMedGoogle ScholarCrossref
148.
Morrow  LA, Wagner  BD, Ingram  DA,  et al.  Antenatal determinants of bronchopulmonary dysplasia and late respiratory disease in preterm infants.  Am J Respir Crit Care Med. 2017;196(3):364-374. doi:10.1164/rccm.201612-2414OCPubMedGoogle ScholarCrossref
149.
Novitsky  A, Tuttle  D, Locke  RG, Saiman  L, Mackley  A, Paul  DA.  Prolonged early antibiotic use and bronchopulmonary dysplasia in very low birth weight infants.  Am J Perinatol. 2015;32(1):43-48. doi:10.1055/s-0034-1373844PubMedGoogle ScholarCrossref
150.
Rindfleisch  MS, Hasday  JD, Taciak  V, Broderick  K, Viscardi  RM.  Potential role of interleukin-1 in the development of bronchopulmonary dysplasia.  J Interferon Cytokine Res. 1996;16(5):365-373. doi:10.1089/jir.1996.16.365PubMedGoogle ScholarCrossref
151.
Rocha  G, Ribeiro  O, Guimarães  H.  Fluid and electrolyte balance during the first week of life and risk of bronchopulmonary dysplasia in the preterm neonate.  Clinics (Sao Paulo). 2010;65(7):663-674. doi:10.1590/S1807-59322010000700004PubMedGoogle ScholarCrossref
152.
Rojas  MX, Rojas  MA, Lozano  JM, Rondón  MA, Charry  LP.  Regional variation on rates of bronchopulmonary dysplasia and associated risk factors.  ISRN Pediatr. 2012;2012:685151. doi:10.5402/2012/685151PubMedGoogle Scholar
153.
Sampath  V, Garland  JS, Helbling  D,  et al.  Antioxidant response genes sequence variants and BPD susceptibility in VLBW infants.  Pediatr Res. 2015;77(3):477-483. doi:10.1038/pr.2014.200PubMedGoogle ScholarCrossref
154.
Schena  F, Francescato  G, Cappelleri  A,  et al.  Association between hemodynamically significant patent ductus arteriosus and bronchopulmonary dysplasia.  J Pediatr. 2015;166(6):1488-1492. doi:10.1016/j.jpeds.2015.03.012PubMedGoogle ScholarCrossref
155.
Serenius  F, Ewald  U, Farooqi  A, Holmgren  PA, Håkansson  S, Sedin  G.  Short-term outcome after active perinatal management at 23-25 weeks of gestation: a study from two Swedish perinatal centres, part 3: neonatal morbidity.  Acta Paediatr. 2004;93(8):1090-1097. doi:10.1111/j.1651-2227.2004.tb02722.xPubMedGoogle ScholarCrossref
156.
Shima  Y, Nishimaki  S, Nakajima  M, Kumasaka  S, Migita  M.  Urinary β-2-microglobulin as an alternative marker for fetal inflammatory response and development of bronchopulmonary dysplasia in premature infants.  J Perinatol. 2011;31(5):330-334. doi:10.1038/jp.2010.129PubMedGoogle ScholarCrossref
157.
Soliman  N, Chaput  K, Alshaikh  B, Yusuf  K.  Preeclampsia and the risk of bronchopulmonary dysplasia in preterm infants less than 32 weeks’ gestation.  Am J Perinatol. 2017;34(6):585-592. doi:10.1055/s-0036-1594017PubMedGoogle ScholarCrossref
158.
Stichel  H, Bäckström  E, Hafström  O, Nilsson  S, Lappalainen  U, Bry  K.  Inflammatory cytokines in gastric fluid at birth and the development of bronchopulmonary dysplasia.  Acta Paediatr. 2011;100(9):1206-1212. doi:10.1111/j.1651-2227.2011.02286.xPubMedGoogle ScholarCrossref
159.
Streubel  AH, Donohue  PK, Aucott  SW.  The epidemiology of atypical chronic lung disease in extremely low birth weight infants.  J Perinatol. 2008;28(2):141-148. doi:10.1038/sj.jp.7211894PubMedGoogle ScholarCrossref
160.
Tokuriki  S, Okuno  T, Ohta  G, Ohshima  Y.  Carboxyhemoglobin formation in preterm infants is related to the subsequent development of bronchopulmonary dysplasia.  Dis Markers. 2015;2015:620921. doi:10.1155/2015/620921PubMedGoogle Scholar
161.
Viscardi  RM, Muhumuza  CK, Rodriguez  A,  et al.  Inflammatory markers in intrauterine and fetal blood and cerebrospinal fluid compartments are associated with adverse pulmonary and neurologic outcomes in preterm infants.  Pediatr Res. 2004;55(6):1009-1017. doi:10.1203/01.pdr.0000127015.60185.8aPubMedGoogle ScholarCrossref
162.
Wang  K, Huang  X, Lu  H, Zhang  Z.  A comparison of KL-6 and Clara cell protein as markers for predicting bronchopulmonary dysplasia in preterm infants.  Dis Markers. 2014;2014:736536. doi:10.1155/2014/736536PubMedGoogle Scholar
163.
Watterberg  KL, Gerdes  JS, Cole  CH,  et al.  Prophylaxis of early adrenal insufficiency to prevent bronchopulmonary dysplasia: a multicenter trial.  Pediatrics. 2004;114(6):1649-1657. doi:10.1542/peds.2004-1159PubMedGoogle ScholarCrossref
164.
Choi  CW, Kim  BI, Kim  HS, Park  JD, Choi  JH, Son  DW.  Increase of interleukin-6 in tracheal aspirate at birth: a predictor of subsequent bronchopulmonary dysplasia in preterm infants.  Acta Paediatr. 2006;95(1):38-43. doi:10.1080/08035250500404085PubMedGoogle ScholarCrossref
165.
Xie  L, Chee  YY, Wong  KY, Cheung  YF.  Cardiac mechanics in children with bronchopulmonary dysplasia.  Neonatology. 2016;109(1):44-51. doi:10.1159/000441051PubMedGoogle ScholarCrossref
166.
Yoon  BH, Romero  R, Kim  KS,  et al.  A systemic fetal inflammatory response and the development of bronchopulmonary dysplasia.  Am J Obstet Gynecol. 1999;181(4):773-779. doi:10.1016/S0002-9378(99)70299-1PubMedGoogle ScholarCrossref
167.
Zhang  H, Fang  J, Su  H, Chen  M.  Risk factors for bronchopulmonary dysplasia in neonates born at ≤1500 g (1999-2009).  Pediatr Int. 2011;53(6):915-920. doi:10.1111/j.1442-200X.2011.03399.xPubMedGoogle ScholarCrossref
168.
Curley  AE, Sweet  DG, Thornton  CM,  et al.  Chorioamnionitis and increased neonatal lung lavage fluid matrix metalloproteinase-9 levels: implications for antenatal origins of chronic lung disease.  Am J Obstet Gynecol. 2003;188(4):871-875. doi:10.1067/mob.2003.215PubMedGoogle ScholarCrossref
169.
Durrmeyer  X, Kayem  G, Sinico  M, Dassieu  G, Danan  C, Decobert  F.  Perinatal risk factors for bronchopulmonary dysplasia in extremely low gestational age infants: a pregnancy disorder-based approach.  J Pediatr. 2012;160(4):578-583.e2. doi:10.1016/j.jpeds.2011.09.025PubMedGoogle ScholarCrossref
170.
Eriksson  L, Haglund  B, Odlind  V, Altman  M, Kieler  H.  Prenatal inflammatory risk factors for development of bronchopulmonary dysplasia.  Pediatr Pulmonol. 2014;49(7):665-672. doi:10.1002/ppul.22881PubMedGoogle ScholarCrossref
171.
Honma  Y, Yada  Y, Takahashi  N, Momoi  MY, Nakamura  Y.  Certain type of chronic lung disease of newborns is associated with Ureaplasma urealyticum infection in utero.  Pediatr Int. 2007;49(4):479-484. doi:10.1111/j.1442-200X.2007.02391.xPubMedGoogle ScholarCrossref
172.
Kent  A, Dahlstrom  JE.  Chorioamnionitis/funisitis and the development of bronchopulmonary dysplasia.  J Paediatr Child Health. 2004;40(7):356-359. doi:10.1111/j.1440-1754.2004.00366.xPubMedGoogle ScholarCrossref
173.
Kewitz  G, Wudel  S, Hopp  H, Hopfenmüller  W, Vogel  M, Roots  I.  Below median birth weight in appropriate-for-gestational-age preterm infants as a risk factor for bronchopulmonary dysplasia.  J Perinat Med. 2008;36(4):359-364. doi:10.1515/JPM.2008.056PubMedGoogle ScholarCrossref
174.
Kim  BI, Choi  CW, Park  JD, Kim  CJ, Choi  JH.  The effect of histologic chorioamnionitis on the development of respiratory distress syndrome and chronic lung disease in preterm infants.  Korean J Pediatr. 2004;47(2):150-156.Google Scholar
175.
Lahra  MM, Beeby  PJ, Jeffery  HE.  Intrauterine inflammation, neonatal sepsis, and chronic lung disease: a 13-year hospital cohort study.  Pediatrics. 2009;123(5):1314-1319. doi:10.1542/peds.2008-0656PubMedGoogle ScholarCrossref
176.
Lee  HJ, Kim  E-K, Kim  H-S, Choi  CW, Kim  BI, Choi  J-H.  Chorioamnionitis, respiratory distress syndrome and bronchopulmonary dysplasia in extremely low birth weight infants.  J Perinatol. 2011;31(3):166-170. doi:10.1038/jp.2010.113PubMedGoogle ScholarCrossref
177.
Metcalfe  A, Lisonkova  S, Sabr  Y, Stritzke  A, Joseph  KS.  Neonatal respiratory morbidity following exposure to chorioamnionitis.  BMC Pediatr. 2017;17(1):128. doi:10.1186/s12887-017-0878-9PubMedGoogle ScholarCrossref
178.
Paananen  R, Husa  A-K, Vuolteenaho  R, Herva  R, Kaukola  T, Hallman  M.  Blood cytokines during the perinatal period in very preterm infants: relationship of inflammatory response and bronchopulmonary dysplasia.  J Pediatr. 2009;154(1):39-43.e3. doi:10.1016/j.jpeds.2008.07.012PubMedGoogle ScholarCrossref
179.
Rocha  G, Proença  E, Areias  A,  et al.  HLA and bronchopulmonary dysplasia susceptibility: a pilot study.  Dis Markers. 2011;31(4):199-203. doi:10.1155/2011/236082PubMedGoogle ScholarCrossref
180.
Shima  Y, Kumasaka  S, Migita  M.  Perinatal risk factors for adverse long-term pulmonary outcome in premature infants: comparison of different definitions of bronchopulmonary dysplasia/chronic lung disease.  Pediatr Int. 2013;55(5):578-581. doi:10.1111/ped.12151PubMedGoogle ScholarCrossref
181.
Štimac  M, Juretić  E, Vukelić  V, Matasić  NP, Kos  M, Babić  D.  Effect of chorioamnionitis on mortality, early onset neonatal sepsis and bronchopulmonary dysplasia in preterm neonates with birth weight of <1,500 grams.  Coll Antropol. 2014;38(1):167-171.PubMedGoogle Scholar
182.
Torchin  H, Lorthe  E, Goffinet  F,  et al.  Histologic chorioamnionitis and bronchopulmonary dysplasia in preterm infants: the epidemiologic study on low gestational ages 2 cohort.  J Pediatr. 2017;187:98-104.e3. doi:10.1016/j.jpeds.2017.05.019PubMedGoogle ScholarCrossref
183.
Natarajan  G, Glibetic  M, Thomas  RL, Aranda  JV.  Chorioamnionitis and ontogeny of circulating prostaglandin and thromboxane in preterm infants.  Am J Perinatol. 2008;25(8):491-497. doi:10.1055/s-0028-1085068PubMedGoogle ScholarCrossref
184.
Villamor-Martinez  E, Fumagalli  M, Mohammed Rahim  O,  et al.  Chorioamnionitis is a risk factor for intraventricular hemorrhage in preterm infants: a systematic review and meta-analysis.  Front Physiol. 2018;9:1253. doi:10.3389/fphys.2018.01253PubMedGoogle ScholarCrossref
185.
Villamor-Martinez  E, Cavallaro  G, Raffaeli  G,  et al.  Chorioamnionitis as a risk factor for retinopathy of prematurity: an updated systematic review and meta-analysis.  PLoS One. 2018;13(10):e0205838. doi:10.1371/journal.pone.0205838PubMedGoogle Scholar
186.
Villamor-Martínez  E, Pierro  M, Cavallaro  G, Mosca  F, Kramer  B, Villamor  E.  Probiotic supplementation in preterm infants does not affect the risk of bronchopulmonary dysplasia: a meta-analysis of randomized controlled trials.  Nutrients. 2017;9(11):E1197. doi:10.3390/nu9111197PubMedGoogle Scholar
187.
Jobe  AH, Bancalari  EH.  Controversies about the definition of bronchopulmonary dysplasia at 50 years.  Acta Paediatr. 2017;106(5):692-693. doi:10.1111/apa.13775PubMedGoogle ScholarCrossref
188.
Poindexter  BB, Feng  R, Schmidt  B,  et al; Prematurity and Respiratory Outcomes Program.  Comparisons and limitations of current definitions of bronchopulmonary dysplasia for the prematurity and respiratory outcomes program.  Ann Am Thorac Soc. 2015;12(12):1822-1830. doi:10.1513/AnnalsATS.201504-218OCPubMedGoogle ScholarCrossref
189.
Beam  KS, Aliaga  S, Ahlfeld  SK, Cohen-Wolkowiez  M, Smith  PB, Laughon  MM.  A systematic review of randomized controlled trials for the prevention of bronchopulmonary dysplasia in infants.  J Perinatol. 2014;34(9):705-710. doi:10.1038/jp.2014.126PubMedGoogle ScholarCrossref
190.
Shennan  AT, Dunn  MS, Ohlsson  A, Lennox  K, Hoskins  EM.  Abnormal pulmonary outcomes in premature infants: prediction from oxygen requirement in the neonatal period.  Pediatrics. 1988;82(4):527-532.PubMedGoogle Scholar
191.
Walsh  MC, Wilson-Costello  D, Zadell  A, Newman  N, Fanaroff  A.  Safety, reliability, and validity of a physiologic definition of bronchopulmonary dysplasia.  J Perinatol. 2003;23(6):451-456. doi:10.1038/sj.jp.7210963PubMedGoogle ScholarCrossref
192.
McElrath  TF, Hecht  JL, Dammann  O,  et al; ELGAN Study Investigators.  Pregnancy disorders that lead to delivery before the 28th week of gestation: an epidemiologic approach to classification.  Am J Epidemiol. 2008;168(9):980-989. doi:10.1093/aje/kwn202PubMedGoogle ScholarCrossref
193.
Jobe  AH, Kallapur  SG.  Chorioamnionitis, surfactant, and lung disease in very low birth weight infants.  J Pediatr. 2010;156(1):3-4. doi:10.1016/j.jpeds.2009.08.009PubMedGoogle ScholarCrossref
194.
Revello  R, Alcaide  MJ, Dudzik  D, Abehsera  D, Bartha  JL.  Differential amniotic fluid cytokine profile in women with chorioamnionitis with and without funisitis.  J Matern Fetal Neonatal Med. 2016;29(13):2161-2165. PubMedGoogle Scholar
195.
Gantert  M, Been  JV, Gavilanes  AW, Garnier  Y, Zimmermann  LJ, Kramer  BW.  Chorioamnionitis: a multiorgan disease of the fetus?  J Perinatol. 2010;30(suppl):S21-S30. doi:10.1038/jp.2010.96PubMedGoogle ScholarCrossref
196.
Bax  L, Moons  KG.  Beyond publication bias.  J Clin Epidemiol. 2011;64(5):459-462. doi:10.1016/j.jclinepi.2010.09.003PubMedGoogle ScholarCrossref
197.
Jin  ZC, Zhou  XH, He  J.  Statistical methods for dealing with publication bias in meta-analysis.  Stat Med. 2015;34(2):343-360. doi:10.1002/sim.6342PubMedGoogle ScholarCrossref
198.
Higgins  RD, Saade  G, Polin  RA,  et al; Chorioamnionitis Workshop Participants.  Evaluation and management of women and newborns with a maternal diagnosis of chorioamnionitis: summary of a workshop.  Obstet Gynecol. 2016;127(3):426-436. doi:10.1097/AOG.0000000000001246PubMedGoogle ScholarCrossref
199.
Thompson  SG, Higgins  JP.  How should meta-regression analyses be undertaken and interpreted?  Stat Med. 2002;21(11):1559-1573. doi:10.1002/sim.1187PubMedGoogle ScholarCrossref
Limit 200 characters
Limit 25 characters
Conflicts of Interest Disclosure

Identify all potential conflicts of interest that might be relevant to your comment.

Conflicts of interest comprise financial interests, activities, and relationships within the past 3 years including but not limited to employment, affiliation, grants or funding, consultancies, honoraria or payment, speaker's bureaus, stock ownership or options, expert testimony, royalties, donation of medical equipment, or patents planned, pending, or issued.

Err on the side of full disclosure.

If you have no conflicts of interest, check "No potential conflicts of interest" in the box below. The information will be posted with your response.

Not all submitted comments are published. Please see our commenting policy for details.

Limit 140 characters
Limit 3600 characters or approximately 600 words
    Original Investigation
    Pediatrics
    November 6, 2019

    Association of Chorioamnionitis With Bronchopulmonary Dysplasia Among Preterm Infants: A Systematic Review, Meta-analysis, and Metaregression

    Author Affiliations
    • 1Department of Pediatrics, School for Oncology and Developmental Biology, Maastricht University Medical Center, Maastricht, the Netherlands
    • 2Pediatric Cardiology Department, Hospital Ramón y Cajal, Madrid, Spain
    JAMA Netw Open. 2019;2(11):e1914611. doi:10.1001/jamanetworkopen.2019.14611
    Key Points español 中文 (chinese)

    Question  Is chorioamnionitis a risk factor for developing bronchopulmonary dysplasia in preterm infants?

    Findings  This systematic review, meta-analysis, and metaregression found that chorioamnionitis was associated with an increased risk of bronchopulmonary dysplasia in preterm infants but also found significant differences in baseline characteristics between infants with and infants without chorioamnionitis. A multivariate metaregression model combining the difference in gestational age and the odds of respiratory distress syndrome was associated with 64% of the variance in the association between chorioamnionitis and bronchopulmonary dysplasia.

    Meaning  Exposure to chorioamnionitis is associated with a higher risk of developing bronchopulmonary dysplasia in preterm infants, but this association may be modulated by gestational age and risk of respiratory distress syndrome.

    Abstract

    Importance  Bronchopulmonary dysplasia (BPD), a chronic lung disease of prematurity, remains one of the major and most common complications of very preterm birth. Insight into factors associated with the pathogenesis of BPD is key to improving its prevention and treatment.

    Objective  To perform a systematic review, meta-analysis, and metaregression of clinical studies exploring the association between chorioamnionitis (CA) and BPD in preterm infants.

    Data Sources  PubMed and Embase were searched without language restriction (last search, October 1, 2018). Key search terms included bronchopulmonary dysplasia, chorioamnionitis, and risk factors.

    Study Selection  Included studies were peer-reviewed studies examining preterm (<37 weeks’ gestation) or very low-birth-weight (<1500 g) infants and reporting primary data that could be used to measure the association between exposure to CA and the development of BPD.

    Data Extraction and Synthesis  The Meta-analysis of Observational Studies in Epidemiology (MOOSE) guideline was followed. Data were independently extracted by 2 researchers. A random-effects model was used to calculate odds ratios (ORs) and 95% CIs. Heterogeneity in effect size across studies was studied using multivariate, random-effects metaregression analysis.

    Main Outcomes and Measures  The primary outcome was BPD, defined as supplemental oxygen requirement on postnatal day 28 (BPD28) or at the postmenstrual age of 36 weeks (BPD36). Covariates considered as potential confounders included differences between CA-exposed and CA-unexposed infants in gestational age, rates of respiratory distress syndrome (RDS), exposure to antenatal corticosteroids, and rates of early- and late-onset sepsis.

    Results  A total of 3170 potentially relevant studies were found, of which 158 met the inclusion criteria (244 096 preterm infants, 20 971 CA cases, and 24 335 BPD cases). Meta-analysis showed that CA exposure was significantly associated with BPD28 (65 studies; OR, 2.32; 95% CI, 1.88-2.86; P < .001; heterogeneity: I2 = 84%; P < .001) and BPD36 (108 studies; OR, 1.29; 95% CI, 1.17-1.42; P < .001; heterogeneity: I2 = 63%; P < .001). The association between CA and BPD remained significant for both clinical and histologic CA. In addition, significant differences were found between CA-exposed and CA-unexposed infants in gestational age, birth weight, odds of being small for gestational age, exposure to antenatal corticosteroids, and early- and late-onset sepsis. Chorioamnionitis was not significantly associated with RDS (48 studies; OR, 1.10; 95% CI, 0.92-1.34; P = .24; heterogeneity: I2 = 90%; P < .001), but multivariate metaregression analysis with backward elimination revealed that a model combining the difference in gestational age and the odds of RDS was associated with 64% of the variance in the association between CA and BPD36 across studies.

    Conclusions and Relevance  The results of this study confirm that among preterm infants, exposure to CA is associated with a higher risk of developing BPD, but this association may be modulated by gestational age and risk of RDS.

    Introduction

    Bronchopulmonary dysplasia (BPD), a chronic lung disease of prematurity, remains one of the major and most common complications of very preterm birth.1-7 The degree of prematurity is the most important predisposing risk factor for BPD, but inflammatory and/or infectious events are suggested to play a key role in the initiation, progression, and severity of BPD.3-5,8-13 The pulmonary inflammatory response may have been initiated in utero, in the setting of chorioamnionitis (CA).3-5,8-10

    Besides the aforementioned detrimental effects, clinical observations support the concept that fetal exposure to infection or inflammation may also be beneficial to the very preterm lung.4,14,15 Watterberg et al15 were the first to report that CA was associated with an increased risk for BPD but a reduced risk for respiratory distress syndrome (RDS). This observation led to the hypothesis that CA exposure accelerated functional lung maturation but increased the vulnerability of the preterm lung to postnatal injury.4,14,16 However, the data supporting this hypothesis are inconsistent, and subsequent studies during the past 20 years have found that CA was associated with increased, decreased, or no risk of either BPD or RDS.4,14,16

    The role of CA as a potential pathogenic factor for BPD has already been the subject of a systematic review and meta-analysis. Hartling et al10 included 59 studies (15 295 preterm infants). They found in unadjusted analyses that CA was significantly associated with BPD (odds ratio [OR], 1.89; 95% CI, 1.56-2.30). They found substantial statistical heterogeneity and evidence of publication bias. They also observed that infants exposed to CA had a significantly lower gestational age and birth weight than infants who were not exposed to CA. Moreover, studies adjusting for important confounders (including gestational age and/or birth weight) showed more conservative measures of association between CA and BPD. They concluded that “despite a large body of evidence, CA cannot be definitely considered a risk factor for BPD.”10(pF8)

    After the publication of the meta-analysis by Hartling et al,10 many more studies assessing the association between CA and BPD have been published. Some of these studies are of high methodological quality and included a large number of infants. Therefore, in the present study, we aimed to update and expand the meta-analysis of Hartling et al.10 In addition, we investigated not only the association between CA and BPD but also the association between CA and RDS and how these 2 associations correlate. We also analyzed the role of potential confounders or intermediate factors, such as gestational age, birth weight, the presence of fetal inflammatory response (ie, funisitis), exposure to antenatal corticosteroids, sepsis, or patent ductus arteriosus, in the association between CA and BPD.

    Methods

    We based the method for this systematic review, meta-analysis, and metaregression on earlier meta-analyses on the associations between CA and patent ductus arteriosus,17 CA and retinopathy of prematurity,18 and CA and intraventricular hemorrhage.19 The study was conducted according to the Meta-analysis of Observational Studies in Epidemiology (MOOSE) reporting guideline20 and the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) reporting guideline.21 A protocol was developed prospectively that detailed the specific objectives, criteria for study selection, approach to assessing study quality, clinical outcomes, and statistical methods. The study is reported according to the PRISMA checklist.

    Sources and Search Strategy

    A comprehensive literature search was undertaken using the PubMed/MEDLINE and Embase databases from their inception to October 1, 2018. The search terms involved various combinations of the following key words: chorioamnionitis, intrauterine infection, intrauterine inflammation, antenatal infection, antenatal inflammation, bronchopulmonary dysplasia, chronic lung disease, risk factors, outcome, cohort, and case-control. No language limit was applied. Narrative reviews, systematic reviews, case reports, letters, editorials, and commentaries were excluded but were read to identify potential additional studies. Additional strategies to identify studies included a manual review of reference lists from key articles that fulfilled our eligibility criteria and other systematic reviews on CA, use of the “related articles” feature in PubMed, and use of the “cited by” tool in Web of Science and Google Scholar.

    Study Selection

    Studies were included if they examined preterm (gestational age <37 weeks) or very low-birth-weight (<1500 g) infants and reported primary data that could be used to measure the association between exposure to CA and the development of BPD. Therefore, we selected studies assessing the outcomes of infants exposed to CA when BPD was one of the reported outcomes and studies assessing the risk factors for BPD when CA was one of the reported risk factors. To identify relevant studies, 2 of us (A.M.T.G. and E.V.) independently screened the results of the searches and applied inclusion criteria using a structured form. Discrepancies were resolved through discussion or consultation with a third reviewer (P.D.).

    Data Extraction

    Two of us (A.M.T.G. and P.D.) extracted data from relevant studies using a predetermined data extraction form, and 3 of us (E.V.-M., M.A.-F., and E.V.) checked data extraction for accuracy and completeness. Discrepancies were resolved by consulting the primary report. Data extracted from each study included citation information, language of publication, location where research was conducted, time period of the study, study objectives, study design, definitions of CA and BPD, inclusion and exclusion criteria, patient characteristics, and results (including raw numbers, summary statistics, and adjusted analyses on CA and BPD when available). Studies that did not define CA were assumed to use a clinical definition. Bronchopulmonary dysplasia defined as supplemental oxygen requirement on postnatal day 28 was coded as BPD28. Bronchopulmonary dysplasia defined as oxygen requirement at the postmenstrual age (PMA) of 36 weeks (with or without physiological challenge of supplemental oxygen withdrawal) was coded as BPD36. Using these definition criteria, BPD28 was considered to include all severities of BPD, whereas BPD36 was considered to include a combination of moderate and severe BPD.2 Data on separate categories of BPD (mild, moderate, and severe) were collected when available.

    Quality Assessment

    Methodological quality was assessed using the Newcastle-Ottawa Scale for cohort or case-control studies.22 This scale uses a rating system (range, 0-9 points; higher scores indicate reduced bias) that scores 3 aspects of a study: selection (0-4 points), comparability (0-2 points), and exposure or outcome (0-3 points). Studies were evaluated as though the association between CA and BPD was the primary outcome. Two of us (E.V.-M. and E.V.) independently assessed the methodological quality of each study. Discrepancies were resolved through discussion.

    Statistical Analysis

    Studies were combined and analyzed using Comprehensive Meta-Analysis, version 3.0 software (Biostat Inc). For dichotomous outcomes, the OR with 95% CI was calculated from the data provided in the studies. Odds ratios adjusted for potential confounders were extracted from the studies reporting these data. For continuous outcomes, the mean difference with 95% CI was calculated. When studies reported continuous variables as median and range or interquartile range, we estimated the mean and SD using the method of Wan et al23 and the calculator they provided.24

    Owing to anticipated heterogeneity, summary statistics were calculated with a random-effects model. This model accounts for variability between studies as well as within studies. Subgroup analyses were conducted according to the mixed-effects model.25 In this model, a random-effects model is used to combine studies within each subgroup, and a fixed-effect model is used to combine subgroups and yield the overall effect. The study-to-study variance (τ2) is not assumed to be the same for all subgroups. This value is computed within subgroups and not pooled across subgroups. Statistical heterogeneity was assessed by use of the Cochran Q statistic and by use of the I2 statistic, which is derived from the Q statistic and describes the proportion of total variation that is due to heterogeneity beyond chance.26 We used the Egger regression test and funnel plots to assess publication bias.

    To explore differences between studies that might be expected to influence the effect size, we performed random effects (method of moments) univariate and multivariate metaregression analyses.27 The potential sources of variability defined a priori were CA type (clinical or histologic), differences in gestational age and birth weight between infants with and infants without CA, use of antenatal corticosteroids, mode of delivery, rate of small-for-gestational-age infants, rate of premature rupture of membranes, rate of preeclampsia, rate of early-onset sepsis, rate of late-onset sepsis, rate of RDS, and mortality. Covariates were selected for further modeling if they significantly (P < .05) modified the association between CA and BPD. Subsequently, preselected covariates were included in a backward multiple metaregression analysis with P = .05 as a cutoff point for removal. P < .05 (P < .10 for heterogeneity) was considered statistically significant. All tests were 2-tailed.

    Results
    Description of Studies

    Of 3170 potentially relevant studies, 158 (5.0%)13,15,28-183 met the inclusion criteria. The PRISMA flow diagram of the search process is shown in Figure 1. The included studies evaluated 244 096 preterm infants and included 20 791 CA cases and 24 335 cases of BPD of any severity. The included studies and their characteristics are summarized in eTable 1 in the Supplement. Seventy-six studies15,28-101,183 were designed from the perspective of CA; they examined the outcomes of preterm infants with or without CA, and BPD was one of these outcomes. Sixty-seven studies100,102-167 were designed from the perspective of BPD; they studied risk factors for BPD, and CA was one of these risk factors. Sixteen studies13,168-182 were designed to primarily examine the association between CA and BPD. Forty-eight included studies examined the association between CA and RDS.

    Forty-two studies defined CA clinically, and 97 studies defined CA histologically. Six studies provided BPD outcomes for infants with histologic and clinical CA separately.68,75,80,116,127,146 One study required infants to have both histologic and clinical CA to be considered exposed to CA.84 Nine studies defined CA using a microbiological definition.28,29,47,53,58,64,131,135,152 Finally, 16 studies102,104,105,108,113,120,123,128-130,139,141,148,155,160,170 did not define CA and, for the purposes of analysis, were considered to evaluate clinical CA.

    Most studies included infants with a gestational age less than 32 weeks or a birth weight less than 1500 g, as described in eTable 1 in the Supplement. Eighty-one studies included infants who were 32 weeks’ gestational age or more preterm, 27 studies included infants who were at most 32 to 34 weeks’ gestational age, and 10 studies included infants who were less than 34 to 37 weeks’ gestational age. Nine studies included infants who had a birth weight of less than 1000 g, 49 studies included infants who had a birth weight of 1500 g or less, and 2 studies included infants who had a birth weight of 2000 g or less. Finally, 4 studies used inclusion criteria (clarified per study in eTable 1 in the Supplement) other than gestational age or birth weight.

    Sixty-five studies provided data on BPD28, and 108 studies provided data on BPD36. Fifteen studies provided data on the incidence of mild BPD, 7 studies provided data on the incidence of moderate BPD, and 8 studies provided data on the incidence of severe BPD.

    Analysis Based on Unadjusted Data

    Meta-analysis found a positive association between exposure to CA and BPD28 (65 studies; OR, 2.32; 95% CI, 1.88-2.86; P < .001; heterogeneity: I2 = 84%; P < .001) (Figure 2A). When subdividing by definition of CA, we found that the association with BPD28 remained significant for histologic CA (OR, 2.58; 95% CI, 1.99-3.34), clinical CA (OR 1.77, 95% CI, 1.21-2.61), and microbiological CA (OR, 2.99; 95% CI, 1.03-8.68) (Figure 2A; eFigure 1 in the Supplement). We also found a significant positive association between CA and BPD36 (108 studies; OR, 1.29; 95% CI, 1.17-1.42; P < .001; heterogeneity: I2 = 63%; P < .001) (Figure 2B). This association was also significant when pooling only studies of histologic CA (OR, 1.33; 95% CI, 1.18-1.51) (Figure 2B; eFigure 2 in the Supplement) and clinical CA (OR, 1.24; 95% CI, 1.03-1.49) (Figure 2B; eFigure 3 in the Supplement).

    When further stratified by grade of BPD, meta-analysis did not find a significant association between CA and mild BPD (15 studies; Figure 2C; eFigure 4 in the Supplement), moderate BPD (7 studies; Figure 2D; eFigure 5 in the Supplement), or severe BPD (8 studies; Figure 2E; eFigure 6 in the Supplement). Twenty-three of the 158 included studies also reported on funisitis and risk of BPD. Meta-analysis did not find a difference between infants exposed to CA with funisitis and infants exposed to CA without funisitis in the risk of BPD28 (OR, 1.26; 95% CI, 0.61-2.59) or the risk of BPD36 (OR, 1.19; 95% CI, 0.77-1.83) (eFigure 7 in the Supplement).

    Analysis of Adjusted Data

    To examine confounding factors, we pooled studies that provided adjusted data on the association between CA and BPD. Eleven studies reported adjusted data on BPD28. Meta-analysis of these adjusted data showed a significant association between CA and BPD28 (OR, 1.68; 95% CI, 1.28-2.21) (eFigure 8 in the Supplement). When the unadjusted data on BPD28 from the 11 studies were pooled, the OR increased to 2.17 (95% CI, 1.71-2.76). However, metaregression did not find this increase in effect size to be statistically significant (P = .17).

    Twenty-one studies reported adjusted data on BPD36. Meta-analysis of these adjusted data showed a significant association between CA and BPD36 (OR, 1.25; 95% CI, 1.01-1.54) (eFigure 9 in the Supplement). When the unadjusted data on BPD36 of the 21 studies were pooled, the OR increased to 1.65 (95% CI, 1.37-2.00). Metaregression did not find this increase in effect size to be statistically significant (P = .05).

    Analysis of Covariates and Metaregression

    We performed additional meta-analyses to explore the possible differences in baseline characteristics between the groups exposed or nonexposed to CA. As summarized in the Table, infants exposed to CA showed a significantly lower gestational age (difference in means, –1.20 weeks; 95% CI, –1.48 to –0.92 weeks) and birth weight (difference in means, –48 g; 95% CI, –66 to –30 g) and significantly lower rates of birth by cesarean delivery (OR, 0.35; 95% CI, 0.28-0.43), small for gestational age (OR, 0.34; 95% CI, 0.26-0.44), and preeclampsia (OR, 0.16; 95% CI, 0.11-0.23). Moreover, infants exposed to CA showed significantly higher rates of exposure to antenatal corticosteroids (OR, 1.39; 95% CI, 0.98-1.97), premature rupture of membranes (OR, 3.66; 95% CI, 3.02-4.44), early-onset sepsis (OR, 3.18; 95% CI, 2.41-4.19), late-onset sepsis (OR, 1.32; 95% CI, 1.10-1.58), and mortality (OR, 1.48; 95% CI, 1.28-1.71). In contrast, meta-analysis did not demonstrate a significant association between CA and all RDS (OR, 1.10; 95% CI, 0.92-1.34; P = .24; heterogeneity: I2 = 90%; P < .001) (Figure 3; eFigure 10 in the Supplement) or severe RDS (defined by the necessity of surfactant and/or mechanical ventilation) (Figure 3; eFigure 11 in the Supplement).

    Relevant covariates were preselected using univariate metaregression analyses. Results of all univariate analyses are presented in eTable 2 in the Supplement. For BPD28, we found that mean difference in gestational age significantly explained heterogeneity in effect size across studies (eTable 2 in the Supplement). For BPD36, we found that mean difference in gestational age (eFigure 12 and eTable 2 in the Supplement), mean difference in birth weight (eTable 2 in the Supplement), and RDS risk (eFigure 13 and eTable 2 in the Supplement) significantly explained heterogeneity in effect size across studies; these variables were therefore considered for further modeling. Backward multiple metaregression analysis, including all studies on BPD36 with complete data for these 3 covariates (gestational age, birth weight, and RDS; k = 25), revealed that heterogeneity in effect size across studies was significantly explained by the mean difference in gestational age (coefficient, –0.23; 95% CI, −0.40 to −0.06; P = .008) and risk of RDS (coefficient, 0.31; 95% CI, 0.09-0.54; P = .007). We retested this model, including all studies with complete data on mean difference in gestational age and risk of RDS (k = 27) (Figure 4). This final model had a total explained variance of 64% (R2 equivalent). The variance did not seem to be inflated owing to multicollinearity (variance inflation factor = 1.08). Each week that infants with CA are born earlier than control infants resulted in an increase in BPD36 log OR of 0.23 (the equivalent of going from an OR of 1.00 to an OR of 1.70). Each point increase in the RDS log OR resulted in an increase in the BPD36 log OR of 0.31 (the equivalent of going from an OR of 1.00 to an OR of 2.04).

    To further assess gestational age as a confounding factor, we performed a meta-analysis of studies in which the mean difference in gestational age was not significant (P > .05). As shown in eFigure 14 in the Supplement, we observed no differences in BPD28 risk in studies with similar gestational age (6 studies). On the other hand, when a significant difference in gestational age was observed (P < .05), CA was significantly associated with BPD28 (20 studies; OR, 2.00; 95% CI, 1.49-2.69) (eFigure 14 in the Supplement). We found similar results for BPD36. Meta-analysis of studies in which the mean difference in gestational age was not significant did not find an association between CA and BPD36 (15 studies; eFigure 15 in the Supplement), whereas meta-analysis of studies in which the difference in gestational age was significant found a significant association between CA and BPD36 risk (32 studies; OR, 1.43; 95% CI, 1.23-1.67).

    Quality Assessment

    The quality of each study according to the Newcastle-Ottawa Scale is summarized in eTable 3 in the Supplement. Studies received a quality score of 6 points (2 studies), 7 points (21 studies), 8 points (112 studies), or 9 points (23 studies), out of a possible 9 points. Studies were downgraded in quality most frequently for not adjusting the risk of BPD for confounders (133 studies), for not defining CA clearly (16 studies), and for not defining BPD precisely (3 studies).

    Publication Bias

    Neither visual inspection of funnel plots (eFigure 16 in the Supplement) nor the Egger test suggested publication or selection bias. There was an insufficient number of studies with other BPD definitions (ie, mild, moderate, or severe) to evaluate publication bias.

    Discussion

    The present study is a substantial update to the systematic review of Hartling et al,10 including a larger number of studies (158 vs 59), a much larger number of infants (244 096 vs 15 295), and a wider range of analysis of covariates. Our study confirms the results of Hartling et al10 and adds new information on the role of funisitis and RDS, which have not been previously systematically reviewed, to our knowledge. Chorioamnionitis was a significant risk factor for BPD28 (all BPD) and for BPD36 (moderate and severe BPD), but a significant association with severe BPD was not demonstrated. Exposure to funisitis was not significantly associated with a higher risk of BPD compared with exposure to CA in the absence of funisitis. Meta-analysis did not demonstrate a significant association between CA and RDS. As in earlier meta-analyses of CA and morbidities,17,184,185 we found significant differences between CA-exposed and CA-unexposed infants in gestational age, birth weight, odds of being small for gestational age, exposure to antenatal corticosteroids, early- and late-onset sepsis, and patent ductus arteriosus. Multivariate metaregression analysis revealed that a model combining the difference in gestational age and the odds of RDS explained 64% of the variance in the association between CA and BPD36 across studies. In conclusion, our results confirm the positive association between CA and BPD in preterm infants, but the pathogenic effect of CA on BPD may be modulated by the effect of CA on gestational age and risk of RDS.

    As discussed elsewhere,186 one important limitation inherent to any meta-analysis of BPD is the heterogeneity of the definition of the condition.187-189 The first clinical definition for BPD was adopted as infants requiring supplemental oxygen on postnatal day 28.5,187 In 1988, the definition was refined to oxygen use at 36 weeks of PMA,190 and 12 years later, a categorization of BPD as mild, moderate, or severe was proposed.2 Mild BPD included infants who received oxygen or respiratory support at the postnatal age of 28 days but who were breathing room air at 36 weeks PMA. When infants required supplemental oxygen at 36 weeks PMA, BPD was classified as moderate (need for <30% oxygen) or severe (need for ≥30% oxygen and/or positive airway pressure).2 A further refinement in the definition included a physiological challenge of supplemental oxygen withdrawal to test for oxygen need at 36 weeks PMA.191 Most of the studies included in our meta-analysis defined BPD using the 36 weeks of PMA criteria (BPD36). Therefore, they provided data on combined moderate and severe BPD. This combination fails to differentiate the infants with more severe BPD, who remain dependent on mechanical ventilation and more often have severe complications, including pulmonary hypertension, poor growth, and neurodevelopmental problems.6 Only 7 studies provided separate data on severe BPD. Meta-analysis could not demonstrate a significant association between CA and severe BPD, but the small number of studies is the main limitation of this subanalysis.

    Another main difficulty when assessing CA as a risk factor for neonatal adverse outcomes is the absence of a “healthy” control group. Possible causes of very preterm birth (ie, gestational age <32 weeks) can be divided into 2 main categories: infection and/or inflammation and dysfunctional placentation.192 Chorioamnionitis is associated with infection and/or inflammation, and we and others have previously found that infants exposed to CA differ substantially from nonexposed infants in relevant clinical characteristics and outcomes.17,184,185 We replicated these findings in the present study and found that CA-exposed infants were born earlier (1.2 weeks) and weighed less (48 g) than infants without CA. In addition, they were more frequently exposed to antenatal corticosteroids, they were less frequently small for gestational age, and they had higher rates of early- and late-onset sepsis, as well as a higher mortality rate. We performed metaregression to analyze how these differences between the CA-exposed and the nonexposed infants affected the association between CA and BPD. Univariate metaregression showed that differences in gestational age and birth weight, as well as rate of RDS, significantly modified the CA-associated risk of BPD36. As already mentioned, multivariate regression found that 64% of variance in CA-associated BPD risk was explained by the differences in gestational age and rate of RDS.

    The so-called Waterberg hypothesis or early-protection, late-damage effect suggests that CA may be associated with a reduction in RDS but an increase in BPD.4,14,16 To test this hypothesis, we also analyzed the association between CA and RDS in the included studies. In contrast to BPD, meta-analysis of unadjusted data could not demonstrate a significant association between CA and the development of RDS. Prematurity is the most important risk factor for RDS. The CA-exposed infants were born 1.2 weeks earlier but did not show a higher rate of RDS. This finding may suggest some degree of protection against RDS, compatible with the Waterberg hypothesis. In contrast, metaregression showed a significant positive association between the effect size of the CA-RDS association and the effect size of the CA-BPD association (eFigure 12 in the Supplement). In other words, the studies showing a higher risk of RDS in the CA group also showed a higher risk of BPD. Nevertheless, our results should be interpreted with caution because the criteria for the definition of RDS varied substantially among the different studies. As pointed out by Jobe and Kallapur,193 although RDS is the diagnosis assigned to most preterm infants, it is unlikely that they have only 1 lung disease at birth. We therefore restrained the analysis to the studies defining a more severe form of RDS (ie, RDS requiring surfactant and/or mechanical ventilation), which, however, did not modify the lack of association between CA and RDS.

    It remains unclear whether the most severe grades of CA with a fetal inflammatory response further increase the risk for developing BPD and/or RDS. Funisitis is considered the histologic counterpart of the fetal inflammatory response syndrome.194,195 Been et al34 showed that the presence of funisitis categorized infants at risk for severe RDS who were less responsive to surfactant treatment. In contrast, infants exposed to CA without funisitis had less severe RDS than did infants without the CA exposure. Therefore, exposure to CA and/or funisitis may be more strongly associated with the severity than with the incidence of respiratory complications. Our meta-analysis did not demonstrate that the presence of funisitis significantly increased the risk of BPD or RDS compared with CA in the absence of funisitis (eFigure 7 in the Supplement). However, our meta-analysis is limited by the small number of studies providing data on funisitis. In addition, infants with funisitis also presented with differences in basal characteristics (including lower gestational age) compared with infants with CA without funisitis.17,184,185

    Limitations and Strengths

    Hartling et al10 noted 2 problems that made the interpretation of their results difficult: significant publication bias and substantial statistical heterogeneity. Our larger study showed a similarly high degree of heterogeneity, but we did not find statistical evidence of publication bias. Egger regression can test only for data trends that may be caused by selective reporting, publication, or inclusion.196 Even highly significant data trends do not necessarily mean that the results of the primary analysis are biased.196 In addition, the Egger regression test has a high type I error rate and may generate false-positives when dealing with many studies and a high degree of heterogeneity.197

    Some additional limitations of our systematic review and meta-analysis deserve consideration. First, the published literature showed great heterogeneity in the definition of CA and in the assessment of confounders. In particular, criteria for the use of the term clinical CA are highly variable, and recent recommendations propose restricting the term chorioamnionitis to pathologic diagnosis.198 In addition, the term funisitis was not included in our search strategy. Second, only a limited number of studies evaluated the association between CA and BPD as their main objective. Similarly, adjusted data were available only from a subset of all studies included in the meta-analysis. In addition, we had to rely on the adjusted analyses as presented in the published reports and the variables for which they adjusted, which were not consistent across studies. Third, metaregression uses summary data at the study level, which means that we cannot comment on data of individual infants within a study and that there is a risk of ecological bias.199 The main strengths of the present study are the large number of studies included and the use of rigorous methods, including duplicate screening, inclusion, and data extraction to reduce bias; meta-analysis of baseline and secondary characteristics; and the use of metaregression to control for potential confounders.

    Conclusions

    Overall, the results of this study confirm that, among preterm infants, exposure to CA is associated with a higher risk of developing BPD, but this association may be modulated by gestational age and risk of RDS. Bronchopulmonary dysplasia remains a persistent problem in part because advances in neonatal care have improved the survival of the youngest and smallest infants, who are more prone to develop BPD.5 Our data show that CA is frequently the cause of prematurity among these youngest and smallest infants. This higher degree of prematurity may alter the association between CA and BPD. In addition, CA may initiate the pathogenic sequence leading to BPD but also may alter the rate of exposure to other anti-inflammatory or proinflammatory stimuli, such as antenatal corticosteroids, RDS, patent ductus arteriosus, mechanical ventilation, oxygen, and sepsis. Nevertheless, CA, RDS, and BPD are imprecise diagnoses and have been partially changed over time, making the analysis of their associations and correlations difficult.

    Back to top
    Article Information

    Accepted for Publication: September 16, 2019.

    Published: November 6, 2019. doi:10.1001/jamanetworkopen.2019.14611

    Open Access: This is an open access article distributed under the terms of the CC-BY License. © 2019 Villamor-Martinez E et al. JAMA Network Open.

    Corresponding Authors: Eduardo Villamor-Martinez, MSc, MA, Department of Pediatrics, Maastricht University Medical Center, Postbus 5800, 6202 AZ Maastricht, the Netherlands (e.villamormartinez@maastrichtuniversity.nl); Eduardo Villamor, MD, PhD, Department of Pediatrics, Maastricht University Medical Center, Postbus 5800, 6202 AZ Maastricht, the Netherlands (e.villamor@mumc.nl).

    Author Contributions: Mr Villamor-Martinez and Dr Villamor had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

    Concept and design: Villamor.

    Acquisition, analysis, or interpretation of data: All authors.

    Drafting of the manuscript: Villamor-Martinez, Ghazi, Villamor.

    Critical revision of the manuscript for important intellectual content: All authors.

    Statistical analysis: Villamor-Martinez, Ghazi, Kramer, Villamor.

    Obtained funding: Zimmermann, Kramer, Villamor.

    Administrative, technical, or material support: Villamor-Martinez, Degraeuwe, Kramer, Villamor.

    Supervision: Villamor-Martinez, Zimmermann, Villamor.

    Conflict of Interest Disclosures: None reported.

    Additional Contributions: Mohammed A. Kilani, MD, Maastricht University Medical Center, Maastricht, the Netherlands, provided assistance in data collection and analysis as part of his medical training, and he was not compensated.

    References
    1.
    Farstad  T, Bratlid  D, Medbø  S, Markestad  T; Norwegian Extreme Prematurity Study Group.  Bronchopulmonary dysplasia—prevalence, severity and predictive factors in a national cohort of extremely premature infants.  Acta Paediatr. 2011;100(1):53-58. doi:10.1111/j.1651-2227.2010.01959.xPubMedGoogle ScholarCrossref
    2.
    Jobe  AH, Bancalari  E.  Bronchopulmonary dysplasia.  Am J Respir Crit Care Med. 2001;163(7):1723-1729. doi:10.1164/ajrccm.163.7.2011060PubMedGoogle ScholarCrossref
    3.
    Kramer  BW.  Antenatal inflammation and lung injury: prenatal origin of neonatal disease.  J Perinatol. 2008;28(suppl 1):S21-S27. doi:10.1038/jp.2008.46PubMedGoogle ScholarCrossref
    4.
    Kramer  BW, Kallapur  S, Newnham  J, Jobe  AH, eds.  Prenatal Inflammation and Lung Development: Seminars in Fetal and Neonatal Medicine. Amsterdam, the Netherlands: Elsevier; 2009. doi:10.1016/j.siny.2008.08.011
    5.
    Higgins  RD, Jobe  AH, Koso-Thomas  M,  et al.  Bronchopulmonary dysplasia: executive summary of a workshop.  J Pediatr. 2018;197:300-308. doi:10.1016/j.jpeds.2018.01.043PubMedGoogle ScholarCrossref
    6.
    Abman  SH, Collaco  JM, Shepherd  EG,  et al; Bronchopulmonary Dysplasia Collaborative.  Interdisciplinary care of children with severe bronchopulmonary dysplasia.  J Pediatr. 2017;181:12-28.e1. doi:10.1016/j.jpeds.2016.10.082PubMedGoogle ScholarCrossref
    7.
    Stoll  BJ, Hansen  NI, Bell  EF,  et al; Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network.  Trends in care practices, morbidity, and mortality of extremely preterm neonates, 1993-2012.  JAMA. 2015;314(10):1039-1051. doi:10.1001/jama.2015.10244PubMedGoogle ScholarCrossref
    8.
    Shahzad  T, Radajewski  S, Chao  C-M, Bellusci  S, Ehrhardt  H.  Pathogenesis of bronchopulmonary dysplasia: when inflammation meets organ development.  Mol Cell Pediatr. 2016;3(1):23. doi:10.1186/s40348-016-0051-9PubMedGoogle ScholarCrossref
    9.
    Speer  CP.  Chorioamnionitis, postnatal factors and proinflammatory response in the pathogenetic sequence of bronchopulmonary dysplasia.  Neonatology. 2009;95(4):353-361. doi:10.1159/000209301PubMedGoogle ScholarCrossref
    10.
    Hartling  L, Liang  Y, Lacaze-Masmonteil  T.  Chorioamnionitis as a risk factor for bronchopulmonary dysplasia: a systematic review and meta-analysis.  Arch Dis Child Fetal Neonatal Ed. 2012;97(1):F8-F17. doi:10.1136/adc.2010.210187PubMedGoogle ScholarCrossref
    11.
    Thomas  W, Speer  CP.  Chorioamnionitis is essential in the evolution of bronchopulmonary dysplasia—the case in favour.  Paediatr Respir Rev. 2014;15(1):49-52.PubMedGoogle Scholar
    12.
    Lacaze-Masmonteil  T.  That chorioamnionitis is a risk factor for bronchopulmonary dysplasia—the case against.  Paediatr Respir Rev. 2014;15(1):53-55.PubMedGoogle Scholar
    13.
    Van Marter  LJ, Dammann  O, Allred  EN,  et al; Developmental Epidemiology Network Investigators.  Chorioamnionitis, mechanical ventilation, and postnatal sepsis as modulators of chronic lung disease in preterm infants.  J Pediatr. 2002;140(2):171-176. doi:10.1067/mpd.2002.121381PubMedGoogle ScholarCrossref
    14.
    Been  JV, Zimmermann  LJ.  Histological chorioamnionitis and respiratory outcome in preterm infants.  Arch Dis Child Fetal Neonatal Ed. 2009;94(3):F218-F225. doi:10.1136/adc.2008.150458PubMedGoogle ScholarCrossref
    15.
    Watterberg  KL, Demers  LM, Scott  SM, Murphy  S.  Chorioamnionitis and early lung inflammation in infants in whom bronchopulmonary dysplasia develops.  Pediatrics. 1996;97(2):210-215.PubMedGoogle Scholar
    16.
    Viscardi  RM.  Perinatal inflammation and lung injury.  Semin Fetal Neonatal Med. 2012;17(1):30-35. doi:10.1016/j.siny.2011.08.002PubMedGoogle ScholarCrossref
    17.
    Behbodi  E, Villamor-Martínez  E, Degraeuwe  PL, Villamor  E.  Chorioamnionitis appears not to be a risk factor for patent ductus arteriosus in preterm infants: a systematic review and meta-analysis.  Sci Rep. 2016;6:37967. doi:10.1038/srep37967PubMedGoogle ScholarCrossref
    18.
    Villamor-Martinez  E, Cavallaro  G, Raffaeli  G,  et al.  Chorioamnionitis as a risk factor for retinopathy of prematurity: an updated systematic review and meta-analysis.  PLoS One. 2018;13(10):e0205838. doi:10.1371/journal.pone.0205838PubMedGoogle Scholar
    19.
    Villamor-Martinez  E, Fumagalli  M, Mohammed Rahim  O,  et al.  Chorioamnionitis is a risk factor for intraventricular hemorrhage in preterm infants: a systematic review and meta-analysis.  Front Physiol. 2018;9:1253. doi:10.3389/fphys.2018.01253PubMedGoogle ScholarCrossref
    20.
    Stroup  DF, Berlin  JA, Morton  SC,  et al.  Meta-analysis of observational studies in epidemiology: a proposal for reporting: Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group.  JAMA. 2000;283(15):2008-2012. doi:10.1001/jama.283.15.2008PubMedGoogle ScholarCrossref
    21.
    Moher  D, Liberati  A, Tetzlaff  J, Altman  DG; PRISMA Group.  Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.  PLoS Med. 2009;6(7):e1000097. doi:10.1371/journal.pmed.1000097PubMedGoogle Scholar
    22.
    Wells  GA, Shea  B, O’Connell  D,  et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomized studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.htm. Accessed December 1, 2016.
    23.
    Wan  X, Wang  W, Liu  J, Tong  T.  Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range.  BMC Med Res Methodol. 2014;14(1):135. doi:10.1186/1471-2288-14-135PubMedGoogle ScholarCrossref
    24.
    Wan  X, Wang  W, Liu  J, Tong  T. Calculator for article ‘Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range’ 2014. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4383202/bin/12874_2014_1175_MOESM2_ESM.xlsx. Accessed September 2, 2019.
    25.
    Borenstein  M, Hedges  LV, Higgins  J, Rothstein  HR. Subgroup analyses. In:  Introduction to Meta-analysis. Chichester, UK: John Wiley & Sons Ltd; 2009:149-186. doi:10.1002/9780470743386.ch19
    26.
    Borenstein  M, Hedges  LV, Higgins  J, Rothstein  HR. Identifying and quantifying heterogeneity.  Introduction to Meta-analysis. Chichester, UK: John Wiley & Sons Ltd; 2009:107-126. doi:10.1002/9780470743386.ch16
    27.
    Borenstein  M, Hedges  LV, Higgins  J, Rothstein  HR. Meta-regression.  Introduction to Meta-analysis. Chichester, UK: John Wiley & Sons Ltd; 2009:187-203. doi:10.1002/9780470743386.ch20
    28.
    Abele-Horn  M, Genzel-Boroviczény  O, Uhlig  T, Zimmermann  A, Peters  J, Scholz  M.  Ureaplasma urealyticum colonization and bronchopulmonary dysplasia: a comparative prospective multicentre study.  Eur J Pediatr. 1998;157(12):1004-1011. doi:10.1007/s004310050987PubMedGoogle ScholarCrossref
    29.
    Abele-Horn  M, Peters  J, Genzel-Boroviczény  O, Wolff  C, Zimmermann  A, Gottschling  W.  Vaginal ureaplasma urealyticum colonization: influence on pregnancy outcome and neonatal morbidity.  Infection. 1997;25(5):286-291. doi:10.1007/BF01720398PubMedGoogle ScholarCrossref
    30.
    Ahn  HM, Park  EA, Cho  SJ, Kim  YJ, Park  HS.  The association of histological chorioamnionitis and antenatal steroids on neonatal outcome in preterm infants born at less than thirty-four weeks’ gestation.  Neonatology. 2012;102(4):259-264. doi:10.1159/000339577PubMedGoogle ScholarCrossref
    31.
    Arayici  S, Kadioglu Simsek  G, Oncel  MY,  et al.  The effect of histological chorioamnionitis on the short-term outcome of preterm infants ≤32 weeks: a single-center study.  J Matern Fetal Neonatal Med. 2014;27(11):1129-1133. doi:10.3109/14767058.2013.850668PubMedGoogle ScholarCrossref
    32.
    Barrera-Reyes  RH, Ruiz-Macías  H, Segura-Cervantes  E.  Neurodevelopment at one year of age [corrected] in preterm newborns with history of maternal chorioamnionitis  [in Spanish].  Ginecol Obstet Mex. 2011;79(1):31-37.PubMedGoogle Scholar
    33.
    Baud  O, Zupan  V, Lacaze-Masmonteil  T,  et al.  The relationships between antenatal management, the cause of delivery and neonatal outcome in a large cohort of very preterm singleton infants.  BJOG. 2000;107(7):877-884. doi:10.1111/j.1471-0528.2000.tb11086.xPubMedGoogle ScholarCrossref
    34.
    Been  JV, Rours  IG, Kornelisse  RF, Jonkers  F, de Krijger  RR, Zimmermann  LJ.  Chorioamnionitis alters the response to surfactant in preterm infants.  J Pediatr. 2010;156(1):10-15.e1. doi:10.1016/j.jpeds.2009.07.044PubMedGoogle ScholarCrossref
    35.
    Alfiero Bordigato  M, Piva  D, Di Gangi  IM, Giordano  G, Chiandetti  L, Filippone  M.  Asymmetric dimethylarginine in ELBW newborns exposed to chorioamnionitis.  Early Hum Dev. 2011;87(2):143-145. doi:10.1016/j.earlhumdev.2010.11.004PubMedGoogle ScholarCrossref
    36.
    Botet  F, Figueras  J, Carbonell-Estrany  X, Narbona  E.  The impact of clinical maternal chorioamnionitis on neurological and psychological sequelae in very-low-birth weight infants: a case-control study.  J Perinat Med. 2011;39(2):203-208. doi:10.1515/jpm.2011.005PubMedGoogle ScholarCrossref
    37.
    Bry  KJ, Jacobsson  B, Nilsson  S, Bry  K.  Gastric fluid cytokines are associated with chorioamnionitis and white blood cell counts in preterm infants.  Acta Paediatr. 2015;104(6):575-580. doi:10.1111/apa.12947PubMedGoogle ScholarCrossref
    38.
    Chisholm  KM, Heerema-McKenney  A, Tian  L,  et al.  Correlation of preterm infant illness severity with placental histology.  Placenta. 2016;39:61-69. doi:10.1016/j.placenta.2016.01.012PubMedGoogle ScholarCrossref
    39.
    Choi  CW, Kim  BI, Joung  KE,  et al.  Decreased expression of transforming growth factor-beta1 in bronchoalveolar lavage cells of preterm infants with maternal chorioamnionitis.  J Korean Med Sci. 2008;23(4):609-615. doi:10.3346/jkms.2008.23.4.609PubMedGoogle ScholarCrossref
    40.
    De Felice  C, Toti  P, Parrini  S,  et al.  Histologic chorioamnionitis and severity of illness in very low birth weight newborns.  Pediatr Crit Care Med. 2005;6(3):298-302. doi:10.1097/01.PCC.0000160658.35437.65PubMedGoogle ScholarCrossref
    41.
    Dempsey  E, Chen  M-F, Kokottis  T, Vallerand  D, Usher  R.  Outcome of neonates less than 30 weeks gestation with histologic chorioamnionitis.  Am J Perinatol. 2005;22(3):155-159. doi:10.1055/s-2005-865020PubMedGoogle ScholarCrossref
    42.
    Dessardo  NS, Dessardo  S, Mustać  E, Banac  S, Petrović  O, Peter  B.  Chronic lung disease of prematurity and early childhood wheezing: is foetal inflammatory response syndrome to blame?  Early Hum Dev. 2014;90(9):493-499. doi:10.1016/j.earlhumdev.2014.07.002PubMedGoogle ScholarCrossref
    43.
    Dexter  SC, Malee  MP, Pinar  H, Hogan  JW, Carpenter  MW, Vohr  BR.  Influence of chorioamnionitis on developmental outcome in very low birth weight infants.  Obstet Gynecol. 1999;94(2):267-273.PubMedGoogle Scholar
    44.
    Dexter  SC, Pinar  H, Malee  MP, Hogan  J, Carpenter  MW, Vohr  BR.  Outcome of very low birth weight infants with histopathologic chorioamnionitis.  Obstet Gynecol. 2000;96(2):172-177.PubMedGoogle Scholar
    45.
    Ecevit  A, Anuk-İnce  D, Yapakçı  E,  et al.  Association of respiratory distress syndrome and perinatal hypoxia with histologic chorioamnionitis in preterm infants.  Turk J Pediatr. 2014;56(1):56-61.PubMedGoogle Scholar
    46.
    Erdemir  G, Kultursay  N, Calkavur  S,  et al.  Histological chorioamnionitis: effects on premature delivery and neonatal prognosis.  Pediatr Neonatol. 2013;54(4):267-274. doi:10.1016/j.pedneo.2013.03.012PubMedGoogle ScholarCrossref
    47.
    Fung  G, Bawden  K, Chow  P, Yu  V.  Long-term outcome of extremely preterm infants following chorioamnionitis.  HK J Paediatr. 2003;8(2):87-92.Google Scholar
    48.
    Gagliardi  L, Rusconi  F, Bellù  R, Zanini  R; Italian Neonatal Network.  Association of maternal hypertension and chorioamnionitis with preterm outcomes.  Pediatrics. 2014;134(1):e154-e161. doi:10.1542/peds.2013-3898PubMedGoogle ScholarCrossref
    49.
    García-Muñoz Rodrigo  F, Galán Henríquez  G, Figueras Aloy  J, García-Alix Pérez  A.  Outcomes of very-low-birth-weight infants exposed to maternal clinical chorioamnionitis: a multicentre study.  Neonatology. 2014;106(3):229-234. doi:10.1159/000363127PubMedGoogle ScholarCrossref
    50.
    González-Luis  G, Jordán García  I, Rodríguez-Miguélez  J, Botet Mussons  F, Figueras Aloy  J.  Neonatal morbidity and mortality in very low birth weight infants according to exposure to chorioamnionitis  [in Spanish].  An Esp Pediatr. 2002;56(6):551-555.PubMedGoogle ScholarCrossref
    51.
    Gray  PH, Hurley  TM, Rogers  YM,  et al.  Survival and neonatal and neurodevelopmental outcome of 24-29 week gestation infants according to primary cause of preterm delivery.  Aust N Z J Obstet Gynaecol. 1997;37(2):161-168. doi:10.1111/j.1479-828X.1997.tb02245.xPubMedGoogle ScholarCrossref
    52.
    Hendson  L, Russell  L, Robertson  CM,  et al.  Neonatal and neurodevelopmental outcomes of very low birth weight infants with histologic chorioamnionitis.  J Pediatr. 2011;158(3):397-402. doi:10.1016/j.jpeds.2010.09.010PubMedGoogle ScholarCrossref
    53.
    Hitti  J, Tarczy-Hornoch  P, Murphy  J, Hillier  SL, Aura  J, Eschenbach  DA.  Amniotic fluid infection, cytokines, and adverse outcome among infants at 34 weeks’ gestation or less.  Obstet Gynecol. 2001;98(6):1080-1088.PubMedGoogle Scholar
    54.
    Jones  MH, Corso  AL, Tepper  RS,  et al.  Chorioamnionitis and subsequent lung function in preterm infants.  PLoS One. 2013;8(12):e81193. doi:10.1371/journal.pone.0081193PubMedGoogle Scholar
    55.
    Jónsson  B, Rylander  M, Faxelius  G.  Ureaplasma urealyticum, erythromycin and respiratory morbidity in high-risk preterm neonates.  Acta Paediatr. 1998;87(10):1079-1084. doi:10.1111/j.1651-2227.1998.tb01418.xPubMedGoogle ScholarCrossref
    56.
    Kaukola  T, Tuimala  J, Herva  R, Kingsmore  S, Hallman  M.  Cord immunoproteins as predictors of respiratory outcome in preterm infants.  Am J Obstet Gynecol. 2009;200(1):100.e1-100.e8. doi:10.1016/j.ajog.2008.07.070PubMedGoogle ScholarCrossref
    57.
    Kim  SY, Choi  CW, Jung  E,  et al.  Neonatal morbidities associated with histologic chorioamnionitis defined based on the site and extent of inflammation in very low birth weight infants.  J Korean Med Sci. 2015;30(10):1476-1482. doi:10.3346/jkms.2015.30.10.1476PubMedGoogle ScholarCrossref
    58.
    Kirchner  L, Helmer  H, Heinze  G,  et al.  Amnionitis with Ureaplasma urealyticum or other microbes leads to increased morbidity and prolonged hospitalization in very low birth weight infants.  Eur J Obstet Gynecol Reprod Biol. 2007;134(1):44-50. doi:10.1016/j.ejogrb.2006.09.013PubMedGoogle ScholarCrossref
    59.
    Lau  J, Magee  F, Qiu  Z, Houbé  J, Von Dadelszen  P, Lee  SK.  Chorioamnionitis with a fetal inflammatory response is associated with higher neonatal mortality, morbidity, and resource use than chorioamnionitis displaying a maternal inflammatory response only.  Am J Obstet Gynecol. 2005;193(3, pt 1):708-713. doi:10.1016/j.ajog.2005.01.017PubMedGoogle ScholarCrossref
    60.
    Lee  Y, Kim  H-J, Choi  S-J,  et al.  Is there a stepwise increase in neonatal morbidities according to histological stage (or grade) of acute chorioamnionitis and funisitis? effect of gestational age at delivery.  J Perinat Med. 2015;43(2):259-267. doi:10.1515/jpm-2014-0035PubMedGoogle ScholarCrossref
    61.
    Liu  Z, Tang  Z, Li  J, Yang  Y.  Effects of placental inflammation on neonatal outcome in preterm infants.  Pediatr Neonatol. 2014;55(1):35-40. doi:10.1016/j.pedneo.2013.05.007PubMedGoogle ScholarCrossref
    62.
    Mehta  R, Nanjundaswamy  S, Shen-Schwarz  S, Petrova  A.  Neonatal morbidity and placental pathology.  Indian J Pediatr. 2006;73(1):25-28. doi:10.1007/BF02758255PubMedGoogle ScholarCrossref
    63.
    Mestan  K, Yu  Y, Matoba  N,  et al.  Placental inflammatory response is associated with poor neonatal growth: preterm birth cohort study.  Pediatrics. 2010;125(4):e891-e898. doi:10.1542/peds.2009-0313PubMedGoogle ScholarCrossref
    64.
    Miralles  R, Hodge  R, Kotecha  S.  Fetal cortisol response to intrauterine microbial colonisation identified by the polymerase chain reaction and fetal inflammation.  Arch Dis Child Fetal Neonatal Ed. 2008;93(1):F51-F54. doi:10.1136/adc.2006.110130PubMedGoogle ScholarCrossref
    65.
    Misra  R, Shah  S, Fowell  D,  et al.  Preterm cord blood CD4+ T cells exhibit increased IL-6 production in chorioamnionitis and decreased CD4+ T cells in bronchopulmonary dysplasia.  Hum Immunol. 2015;76(5):329-338. doi:10.1016/j.humimm.2015.03.007PubMedGoogle ScholarCrossref
    66.
    Miyazaki  K, Furuhashi  M, Ishikawa  K,  et al.  Impact of chorioamnionitis on short- and long-term outcomes in very low birth weight preterm infants: the Neonatal Research Network Japan.  J Matern Fetal Neonatal Med. 2016;29(2):331-337. doi:10.3109/14767058.2014.1000852PubMedGoogle ScholarCrossref
    67.
    Mu  SC, Lin  CH, Chen  YL,  et al.  Impact on neonatal outcome and anthropometric growth in very low birth weight infants with histological chorioamnionitis.  J Formos Med Assoc. 2008;107(4):304-310. doi:10.1016/S0929-6646(08)60091-1PubMedGoogle ScholarCrossref
    68.
    Nasef  N, Shabaan  AE, Schurr  P,  et al.  Effect of clinical and histological chorioamnionitis on the outcome of preterm infants.  Am J Perinatol. 2013;30(1):59-68. doi:10.1055/s-0032-1321501PubMedGoogle Scholar
    69.
    Nicaise  C, Gire  C, Fagianelli  P,  et al.  Neonatal consequences of preterm premature rupture of membrane (PPROM) at 24-34 WG: 118 singleton pregnancies  [in French].  J Gynecol Obstet Biol Reprod (Paris). 2002;31(8):747-754.PubMedGoogle Scholar
    70.
    Nishimaki  S, Shima  Y, Sato  M,  et al.  Urinary β2-microglobulin in premature infants with chorioamnionitis and chronic lung disease.  J Pediatr. 2003;143(1):120-122. doi:10.1016/S0022-3476(03)00249-XPubMedGoogle ScholarCrossref
    71.
    Ogunyemi  D, Murillo  M, Jackson  U, Hunter  N, Alperson  B.  The relationship between placental histopathology findings and perinatal outcome in preterm infants.  J Matern Fetal Neonatal Med. 2003;13(2):102-109. doi:10.1080/jmf.13.2.102.109PubMedGoogle ScholarCrossref
    72.
    Oh  S-H, Kim  J-j, Do  H-j, Lee  BS, Kim  K-S, Kim  EA-R.  Preliminary study on neurodevelopmental outcome and placental pathology among extremely low birth weight infants.  Korean J Perinatol. 2015;26(1):67-77. doi:10.14734/kjp.2015.26.1.67Google ScholarCrossref
    73.
    Ohyama  M, Itani  Y, Yamanaka  M,  et al.  Re-evaluation of chorioamnionitis and funisitis with a special reference to subacute chorioamnionitis.  Hum Pathol. 2002;33(2):183-190. doi:10.1053/hupa.2002.31291PubMedGoogle ScholarCrossref
    74.
    O’Shea  TM, Klinepeter  KL, Meis  PJ, Dillard  RG.  Intrauterine infection and the risk of cerebral palsy in very low-birthweight infants.  Paediatr Perinat Epidemiol. 1998;12(1):72-83. doi:10.1111/j.1365-3016.1998.00081.xPubMedGoogle ScholarCrossref
    75.
    Pappas  A, Kendrick  DE, Shankaran  S,  et al; Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network.  Chorioamnionitis and early childhood outcomes among extremely low-gestational-age neonates.  JAMA Pediatr. 2014;168(2):137-147. doi:10.1001/jamapediatrics.2013.4248PubMedGoogle ScholarCrossref
    76.
    Perrone  S, Toti  P, Toti  MS,  et al.  Perinatal outcome and placental histological characteristics: a single-center study.  J Matern Fetal Neonatal Med. 2012;25(suppl 1):110-113. doi:10.3109/14767058.2012.664344PubMedGoogle ScholarCrossref
    77.
    Plakkal  N, Soraisham  AS, Trevenen  C, Freiheit  EA, Sauve  R.  Histological chorioamnionitis and bronchopulmonary dysplasia: a retrospective cohort study.  J Perinatol. 2013;33(6):441-445. doi:10.1038/jp.2012.154PubMedGoogle ScholarCrossref
    78.
    Polam  S, Koons  A, Anwar  M, Shen-Schwarz  S, Hegyi  T.  Effect of chorioamnionitis on neurodevelopmental outcome in preterm infants.  Arch Pediatr Adolesc Med. 2005;159(11):1032-1035. doi:10.1001/archpedi.159.11.1032PubMedGoogle ScholarCrossref
    79.
    Prendergast  M, May  C, Broughton  S,  et al.  Chorioamnionitis, lung function and bronchopulmonary dysplasia in prematurely born infants.  Arch Dis Child Fetal Neonatal Ed. 2011;96(4):F270-F274. doi:10.1136/adc.2010.189480PubMedGoogle ScholarCrossref
    80.
    Redline  RW, Wilson-Costello  D, Hack  M.  Placental and other perinatal risk factors for chronic lung disease in very low birth weight infants.  Pediatr Res. 2002;52(5):713-719. doi:10.1203/00006450-200211000-00017PubMedGoogle ScholarCrossref
    81.
    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(5):1357-1365. doi:10.1016/j.ajog.2006.03.053PubMedGoogle ScholarCrossref
    82.
    Rocha  G, Proença  E, Quintas  C, Rodrigues  T, Guimarães  H.  Chorioamnionitis and neonatal morbidity  [in Portuguese].  Act Med Port. 2006;19(3):207-212. PubMedGoogle Scholar
    83.
    Sato  M, Nishimaki  S, Yokota  S,  et al.  Severity of chorioamnionitis and neonatal outcome.  J Obstet Gynaecol Res. 2011;37(10):1313-1319. doi:10.1111/j.1447-0756.2010.01519.xPubMedGoogle ScholarCrossref
    84.
    Schlapbach  LJ, Ersch  J, Adams  M, Bernet  V, Bucher  HU, Latal  B.  Impact of chorioamnionitis and preeclampsia on neurodevelopmental outcome in preterm infants below 32 weeks gestational age.  Acta Paediatr. 2010;99(10):1504-1509. doi:10.1111/j.1651-2227.2010.01861.xPubMedGoogle ScholarCrossref
    85.
    Seliga-Siwecka  JP, Kornacka  MK.  Neonatal outcome of preterm infants born to mothers with abnormal genital tract colonisation and chorioamnionitis: a cohort study.  Early Hum Dev. 2013;89(5):271-275. doi:10.1016/j.earlhumdev.2012.10.003PubMedGoogle ScholarCrossref
    86.
    Smit  AL, Been  JV, Zimmermann  LJ,  et al.  Automated auditory brainstem response in preterm newborns with histological chorioamnionitis.  J Matern Fetal Neonatal Med. 2015;28(15):1864-1869. doi:10.3109/14767058.2014.971747PubMedGoogle ScholarCrossref
    87.
    Soraisham  AS, Singhal  N, McMillan  DD, Sauve  RS, Lee  SK; Canadian Neonatal Network.  A multicenter study on the clinical outcome of chorioamnionitis in preterm infants.  Am J Obstet Gynecol. 2009;200(4):372.e1-372.e6. doi:10.1016/j.ajog.2008.11.034PubMedGoogle ScholarCrossref
    88.
    Soraisham  AS, Trevenen  C, Wood  S, Singhal  N, Sauve  R.  Histological chorioamnionitis and neurodevelopmental outcome in preterm infants.  J Perinatol. 2013;33(1):70-75. doi:10.1038/jp.2012.49PubMedGoogle ScholarCrossref
    89.
    Stepan  M, Cobo  T, Maly  J,  et al.  Neonatal outcomes in subgroups of women with preterm prelabor rupture of membranes before 34 weeks.  J Matern Fetal Neonatal Med. 2016;29(14):2373-2377.PubMedGoogle Scholar
    90.
    Strunk  T, Doherty  D, Jacques  A,  et al.  Histologic chorioamnionitis is associated with reduced risk of late-onset sepsis in preterm infants.  Pediatrics. 2012;129(1):e134-e141. doi:10.1542/peds.2010-3493PubMedGoogle ScholarCrossref
    91.
    Suppiej  A, Franzoi  M, Vedovato  S, Marucco  A, Chiarelli  S, Zanardo  V.  Neurodevelopmental outcome in preterm histological chorioamnionitis.  Early Hum Dev. 2009;85(3):187-189. doi:10.1016/j.earlhumdev.2008.09.410PubMedGoogle ScholarCrossref
    92.
    Thomas  W, Seidenspinner  S, Kramer  BW,  et al.  Airway concentrations of angiopoietin-1 and endostatin in ventilated extremely premature infants are decreased after funisitis and unbalanced with bronchopulmonary dysplasia/death.  Pediatr Res. 2009;65(4):468-473. doi:10.1203/PDR.0b013e3181991f35PubMedGoogle ScholarCrossref
    93.
    Trevisanuto  D, Peruzzetto  C, Cavallin  F,  et al.  Fetal placental inflammation is associated with poor neonatal growth of preterm infants: a case-control study.  J Matern Fetal Neonatal Med. 2013;26(15):1484-1490. doi:10.3109/14767058.2013.789849PubMedGoogle ScholarCrossref
    94.
    Tsiartas  P, Kacerovsky  M, Musilova  I,  et al.  The association between histological chorioamnionitis, funisitis and neonatal outcome in women with preterm prelabor rupture of membranes.  J Matern Fetal Neonatal Med. 2013;26(13):1332-1336. doi:10.3109/14767058.2013.784741PubMedGoogle ScholarCrossref
    95.
    van Vliet  EO, de Kieviet  JF, van der Voorn  JP, Been  JV, Oosterlaan  J, van Elburg  RM.  Placental pathology and long-term neurodevelopment of very preterm infants.  Am J Obstet Gynecol. 2012;206(6):489.e1-489.e7. doi:10.1016/j.ajog.2012.03.024PubMedGoogle ScholarCrossref
    96.
    Watterberg  KL, Gerdes  JS, Gifford  KL, Lin  H-M.  Prophylaxis against early adrenal insufficiency to prevent chronic lung disease in premature infants.  Pediatrics. 1999;104(6):1258-1263. doi:10.1542/peds.104.6.1258PubMedGoogle ScholarCrossref
    97.
    Wirbelauer  J, Thomas  W, Speer  CP.  Response of leukocytes and nucleated red blood cells in very low-birth weight preterm infants after exposure to intrauterine inflammation.  J Matern Fetal Neonatal Med. 2011;24(2):348-353. doi:10.3109/14767058.2010.497568PubMedGoogle ScholarCrossref
    98.
    Xie  A, Zhang  W, Chen  M,  et al.  Related factors and adverse neonatal outcomes in women with preterm premature rupture of membranes complicated by histologic chorioamnionitis.  Med Sci Monit. 2015;21:390-395. doi:10.12659/MSM.891203PubMedGoogle ScholarCrossref
    99.
    Young  KC, Del Moral  T, Claure  N, Vanbuskirk  S, Bancalari  E.  The association between early tracheal colonization and bronchopulmonary dysplasia.  J Perinatol. 2005;25(6):403-407. doi:10.1038/sj.jp.7211297PubMedGoogle ScholarCrossref
    100.
    Zanardo  V, Savio  V, Giacomin  C, Rinaldi  A, Marzari  F, Chiarelli  S.  Relationship between neonatal leukemoid reaction and bronchopulmonary dysplasia in low-birth-weight infants: a cross-sectional study.  Am J Perinatol. 2002;19(7):379-386. doi:10.1055/s-2002-35612PubMedGoogle ScholarCrossref
    101.
    Zanardo  V, Vedovato  S, Suppiej  A,  et al.  Histological inflammatory responses in the placenta and early neonatal brain injury.  Pediatr Dev Pathol. 2008;11(5):350-354. doi:10.2350/07-08-0324.1PubMedGoogle ScholarCrossref
    102.
    Alshehri  MA.  Are preterm infants at high altitude at greater risk for the development of bronchopulmonary dysplasia?  J Trop Pediatr. 2014;60(1):68-73. doi:10.1093/tropej/fmt079PubMedGoogle ScholarCrossref
    103.
    Ameenudeen  SA, Boo  NY, Chan  LG.  Risk factors associated with chronic lung disease in Malaysian very low birthweight infants.  Med J Malaysia. 2007;62(1):40-45.PubMedGoogle Scholar
    104.
    Bagchi  A, Viscardi  RM, Taciak  V, Ensor  JE, McCrea  KA, Hasday  JD.  Increased activity of interleukin-6 but not tumor necrosis factor-α in lung lavage of premature infants is associated with the development of bronchopulmonary dysplasia.  Pediatr Res. 1994;36(2):244-252. doi:10.1203/00006450-199408000-00017PubMedGoogle ScholarCrossref
    105.
    Baier  RJ, Loggins  J, Kruger  TE.  Interleukin-4 and 13 concentrations in infants at risk to develop bronchopulmonary dysplasia.  BMC Pediatr. 2003;3(1):8. doi:10.1186/1471-2431-3-8PubMedGoogle ScholarCrossref
    106.
    Baker  CD, Balasubramaniam  V, Mourani  PM,  et al.  Cord blood angiogenic progenitor cells are decreased in bronchopulmonary dysplasia.  Eur Respir J. 2012;40(6):1516-1522. doi:10.1183/09031936.00017312PubMedGoogle ScholarCrossref
    107.
    Bose  C, Laughon  M, Allred  EN,  et al; Elgan Study Investigators.  Blood protein concentrations in the first two postnatal weeks that predict bronchopulmonary dysplasia among infants born before the 28th week of gestation.  Pediatr Res. 2011;69(4):347-353. doi:10.1203/PDR.0b013e31820a58f3PubMedGoogle ScholarCrossref
    108.
    Brener Dik  PH, Niño Gualdron  YM, Galletti  MF, Cribioli  CM, Mariani  GL.  Bronchopulmonary dysplasia: incidence and risk factors  [in Spanish].  Arch Argent Pediatr. 2017;115(5):476-482.PubMedGoogle Scholar
    109.
    Cederqvist  K, Haglund  C, Heikkilä  P,  et al.  Pulmonary trypsin-2 in the development of bronchopulmonary dysplasia in preterm infants.  Pediatrics. 2003;112(3, pt 1):570-577. doi:10.1542/peds.112.3.570PubMedGoogle ScholarCrossref
    110.
    Choi  CW, Kim  BI, Park  JD, Koh  YY, Choi  JH, Choi  JY.  Risk factors for the different types of chronic lung diseases of prematurity according to the preceding respiratory distress syndrome.  Pediatr Int. 2005;47(4):417-423. doi:10.1111/j.1442-200x.2005.02081.xPubMedGoogle ScholarCrossref
    111.
    Colaizy  TT, Morris  CD, Lapidus  J, Sklar  RS, Pillers  D-AM.  Detection of ureaplasma DNA in endotracheal samples is associated with bronchopulmonary dysplasia after adjustment for multiple risk factors.  Pediatr Res. 2007;61(5, pt 1):578-583. doi:10.1203/pdr.0b013e318045be03PubMedGoogle ScholarCrossref
    112.
    de Felice  C, Latini  G, Parrini  S,  et al.  Oral mucosal microvascular abnormalities: an early marker of bronchopulmonary dysplasia.  Pediatr Res. 2004;56(6):927-931. doi:10.1203/01.PDR.0000145259.85418.1DPubMedGoogle ScholarCrossref
    113.
    Demirel  N, Bas  AY, Zenciroglu  A.  Bronchopulmonary dysplasia in very low birth weight infants.  Indian J Pediatr. 2009;76(7):695-698. doi:10.1007/s12098-009-0110-5PubMedGoogle ScholarCrossref
    114.
    Fujioka  K, Shibata  A, Yokota  T,  et al.  Association of a vascular endothelial growth factor polymorphism with the development of bronchopulmonary dysplasia in Japanese premature newborns.  Sci Rep. 2014;4:4459. doi:10.1038/srep04459PubMedGoogle ScholarCrossref
    115.
    Fukunaga  S, Ichiyama  T, Maeba  S,  et al.  MMP-9 and TIMP-1 in the cord blood of premature infants developing BPD.  Pediatr Pulmonol. 2009;44(3):267-272. doi:10.1002/ppul.20993PubMedGoogle ScholarCrossref
    116.
    Gantar  IŠ, Babnik  J, Cerar  LK, Šinkovec  J, Wraber  B.  Prenatal and postnatal risk factors for developing bronchopulmonary dysplasia.  Signa Vitae. 2011;6(2):46-51. doi:10.22514/SV62.102011.6Google ScholarCrossref
    117.
    Ghezzi  F, Gomez  R, Romero  R,  et al.  Elevated interleukin-8 concentrations in amniotic fluid of mothers whose neonates subsequently develop bronchopulmonary dysplasia.  Eur J Obstet Gynecol Reprod Biol. 1998;78(1):5-10. doi:10.1016/S0301-2115(97)00236-4PubMedGoogle ScholarCrossref
    118.
    EXPRESS Group.  Incidence of and risk factors for neonatal morbidity after active perinatal care: extremely preterm infants study in Sweden (EXPRESS).  Acta Paediatr. 2010;99(7):978-992. doi:10.1111/j.1651-2227.2010.01846.xPubMedGoogle ScholarCrossref
    119.
    Guimarães  H, Rocha  G, Vasconcellos  G,  et al.  Risk factors for bronchopulmonary dysplasia in five Portuguese neonatal intensive care units.  Rev Port Pneumol. 2010;16(3):419-430. doi:10.1016/S0873-2159(15)30039-8PubMedGoogle ScholarCrossref
    120.
    Guo  MM-H, Chung  C-H, Chen  F-S, Chen  C-C, Huang  H-C, Chung  M-Y.  Severe bronchopulmonary dysplasia is associated with higher fluid intake in very low-birth-weight infants: a retrospective study.  Am J Perinatol. 2015;30(2):155-162. doi:10.1055/s-0034-1376393PubMedGoogle ScholarCrossref
    121.
    Hansen  AR, Barnés  CM, Folkman  J, McElrath  TF.  Maternal preeclampsia predicts the development of bronchopulmonary dysplasia.  J Pediatr. 2010;156(4):532-536. doi:10.1016/j.jpeds.2009.10.018PubMedGoogle ScholarCrossref
    122.
    Hikino  S, Ohga  S, Kinjo  T,  et al.  Tracheal aspirate gene expression in preterm newborns and development of bronchopulmonary dysplasia.  Pediatr Int. 2012;54(2):208-214. doi:10.1111/j.1442-200X.2011.03510.xPubMedGoogle ScholarCrossref
    123.
    Hyödynmaa  E, Korhonen  P, Ahonen  S, Luukkaala  T, Tammela  O.  Frequency and clinical correlates of radiographic patterns of bronchopulmonary dysplasia in very low birth weight infants by term age.  Eur J Pediatr. 2012;171(1):95-102. doi:10.1007/s00431-011-1486-6PubMedGoogle ScholarCrossref
    124.
    Ikeda  S, Kihira  K, Yokoi  A, Tamakoshi  K, Miyazaki  K, Furuhashi  M.  The levels of the neutrophil elastase in the amniotic fluid of pregnant women whose infants develop bronchopulmonary dysplasia.  J Matern Fetal Neonatal Med. 2015;28(4):479-483. doi:10.3109/14767058.2014.921674PubMedGoogle ScholarCrossref
    125.
    Iwatani  S, Mizobuchi  M, Tanaka  S,  et al.  Increased volume of tracheal aspirate fluid predicts the development of bronchopulmonary dysplasia.  Early Hum Dev. 2013;89(2):113-117. doi:10.1016/j.earlhumdev.2012.08.007PubMedGoogle ScholarCrossref
    126.
    Kalra  VK, Aggarwal  S, Arora  P, Natarajan  G.  B-type natriuretic peptide levels in preterm neonates with bronchopulmonary dysplasia: a marker of severity?  Pediatr Pulmonol. 2014;49(11):1106-1111. doi:10.1002/ppul.22942PubMedGoogle ScholarCrossref
    127.
    Kandasamy  J, Roane  C, Szalai  A, Ambalavanan  N.  Serum eotaxin-1 is increased in extremely-low-birth-weight infants with bronchopulmonary dysplasia or death.  Pediatr Res. 2015;78(5):498-504. doi:10.1038/pr.2015.152PubMedGoogle ScholarCrossref
    128.
    Karagianni  P, Rallis  D, Fidani  L,  et al.  Glutathion-S-transferase P1 polymorphisms association with broncopulmonary dysplasia in preterm infants.  Hippokratia. 2013;17(4):363-367.PubMedGoogle Scholar
    129.
    Karagianni  P, Tsakalidis  C, Kyriakidou  M,  et al.  Neuromotor outcomes in infants with bronchopulmonary dysplasia.  Pediatr Neurol. 2011;44(1):40-46. doi:10.1016/j.pediatrneurol.2010.07.008PubMedGoogle ScholarCrossref
    130.
    Kazzi  SNJ, Kim  UO, Quasney  MW, Buhimschi  I.  Polymorphism of tumor necrosis factor-α and risk and severity of bronchopulmonary dysplasia among very low birth weight infants.  Pediatrics. 2004;114(2):e243-e248. doi:10.1542/peds.114.2.e243PubMedGoogle ScholarCrossref
    131.
    Akram Khan  M, Kuzma-O’Reilly  B, Brodsky  NL, Bhandari  V.  Site-specific characteristics of infants developing bronchopulmonary dysplasia.  J Perinatol. 2006;26(7):428-435. doi:10.1038/sj.jp.7211538PubMedGoogle ScholarCrossref
    132.
    Kim  D-H, Kim  H-S, Shim  S-Y,  et al.  Cord blood KL-6, a specific lung injury marker, correlates with the subsequent development and severity of atypical bronchopulmonary dysplasia.  Neonatology. 2008;93(4):223-229. doi:10.1159/000111100PubMedGoogle ScholarCrossref
    133.
    Klinger  G, Sokolover  N, Boyko  V, Sirota  L, Lerner-Geva  L, Reichman  B; Israel Neonatal Network.  Perinatal risk factors for bronchopulmonary dysplasia in a national cohort of very-low-birthweight infants.  Am J Obstet Gynecol. 2013;208(2):115.e1-115.e9. doi:10.1016/j.ajog.2012.11.026PubMedGoogle ScholarCrossref
    134.
    Koroglu  OA, Yalaz  M, Levent  E, Akisu  M, Kültürsay  N.  Cardiovascular consequences of bronchopulmonary dysplasia in prematurely born preschool children.  Neonatology. 2013;104(4):283-289. doi:10.1159/000354542PubMedGoogle ScholarCrossref
    135.
    Lamboley-Gilmert  G, Lacaze-Masmonteil  T; Neonatologists of the Curosurf Postmarketing French Study.  The short-term outcome of a large cohort of very preterm infants treated with poractant alfa (Curosurf) for respiratory distress syndrome: a postmarketing phase IV study.  Paediatr Drugs. 2003;5(9):639-645. doi:10.2165/00148581-200305090-00006PubMedGoogle ScholarCrossref
    136.
    Lapcharoensap  W, Gage  SC, Kan  P,  et al.  Hospital variation and risk factors for bronchopulmonary dysplasia in a population-based cohort.  JAMA Pediatr. 2015;169(2):e143676. doi:10.1001/jamapediatrics.2014.3676PubMedGoogle Scholar
    137.
    Lardón-Fernández  M, Uberos  J, Molina-Oya  M, Narbona-López  E.  Epidemiological factors involved in the development of bronchopulmonary dysplasia in very low birth-weight preterm infants.  Minerva Pediatr. 2017;69(1):42-49.PubMedGoogle Scholar
    138.
    Leroy  S, Caumette  E, Waddington  C, Hébert  A, Brant  R, Lavoie  PM.  A time-based analysis of inflammation in infants at risk of bronchopulmonary dysplasia.  J Pediatr. 2018;192:60-65.e1. doi:10.1016/j.jpeds.2017.09.011PubMedGoogle ScholarCrossref
    139.
    Li  Y, Cui  Y, Wang  C, Liu  X, Han  J.  A risk factor analysis on disease severity in 47 premature infants with bronchopulmonary dysplasia.  Intractable Rare Dis Res. 2015;4(2):82-86. doi:10.5582/irdr.2015.01000PubMedGoogle ScholarCrossref
    140.
    Lin  H-C, Su  B-H, Chang  J-S, Hsu  C-M, Tsai  C-H, Tsai  F-J.  Nonassociation of interleukin 4 intron 3 and 590 promoter polymorphisms with bronchopulmonary dysplasia for ventilated preterm infants.  Biol Neonate. 2005;87(3):181-186. doi:10.1159/000082937PubMedGoogle ScholarCrossref
    141.
    Lodha  A, Sauvé  R, Bhandari  V,  et al.  Need for supplemental oxygen at discharge in infants with bronchopulmonary dysplasia is not associated with worse neurodevelopmental outcomes at 3 years corrected age.  PLoS One. 2014;9(3):e90843. doi:10.1371/journal.pone.0090843PubMedGoogle Scholar
    142.
    Lohmann  P, Luna  RA, Hollister  EB,  et al.  The airway microbiome of intubated premature infants: characteristics and changes that predict the development of bronchopulmonary dysplasia.  Pediatr Res. 2014;76(3):294-301. doi:10.1038/pr.2014.85PubMedGoogle ScholarCrossref
    143.
    Mahlman  M, Karjalainen  MK, Huusko  JM,  et al.  Genome-wide association study of bronchopulmonary dysplasia: a potential role for variants near the CRP gene.  Sci Rep. 2017;7(1):9271. doi:10.1038/s41598-017-08977-wPubMedGoogle ScholarCrossref
    144.
    Mailaparambil  B, Krueger  M, Heizmann  U, Schlegel  K, Heinze  J, Heinzmann  A.  Genetic and epidemiological risk factors in the development of bronchopulmonary dysplasia.  Dis Markers. 2010;29(1):1-9. doi:10.1155/2010/925940PubMedGoogle ScholarCrossref
    145.
    May  C, Patel  S, Kennedy  C,  et al.  Prediction of bronchopulmonary dysplasia.  Arch Dis Child Fetal Neonatal Ed. 2011;96(6):F410-F416. doi:10.1136/adc.2010.189597PubMedGoogle ScholarCrossref
    146.
    McGowan  EC, Kostadinov  S, McLean  K,  et al.  Placental IL-10 dysregulation and association with bronchopulmonary dysplasia risk.  Pediatr Res. 2009;66(4):455-460. doi:10.1203/PDR.0b013e3181b3b0faPubMedGoogle ScholarCrossref
    147.
    Mittendorf  R, Covert  R, Montag  AG,  et al.  Special relationships between fetal inflammatory response syndrome and bronchopulmonary dysplasia in neonates.  J Perinat Med. 2005;33(5):428-434. doi:10.1515/JPM.2005.076PubMedGoogle ScholarCrossref
    148.
    Morrow  LA, Wagner  BD, Ingram  DA,  et al.  Antenatal determinants of bronchopulmonary dysplasia and late respiratory disease in preterm infants.  Am J Respir Crit Care Med. 2017;196(3):364-374. doi:10.1164/rccm.201612-2414OCPubMedGoogle ScholarCrossref
    149.
    Novitsky  A, Tuttle  D, Locke  RG, Saiman  L, Mackley  A, Paul  DA.  Prolonged early antibiotic use and bronchopulmonary dysplasia in very low birth weight infants.  Am J Perinatol. 2015;32(1):43-48. doi:10.1055/s-0034-1373844PubMedGoogle ScholarCrossref
    150.
    Rindfleisch  MS, Hasday  JD, Taciak  V, Broderick  K, Viscardi  RM.  Potential role of interleukin-1 in the development of bronchopulmonary dysplasia.  J Interferon Cytokine Res. 1996;16(5):365-373. doi:10.1089/jir.1996.16.365PubMedGoogle ScholarCrossref
    151.
    Rocha  G, Ribeiro  O, Guimarães  H.  Fluid and electrolyte balance during the first week of life and risk of bronchopulmonary dysplasia in the preterm neonate.  Clinics (Sao Paulo). 2010;65(7):663-674. doi:10.1590/S1807-59322010000700004PubMedGoogle ScholarCrossref
    152.
    Rojas  MX, Rojas  MA, Lozano  JM, Rondón  MA, Charry  LP.  Regional variation on rates of bronchopulmonary dysplasia and associated risk factors.  ISRN Pediatr. 2012;2012:685151. doi:10.5402/2012/685151PubMedGoogle Scholar
    153.
    Sampath  V, Garland  JS, Helbling  D,  et al.  Antioxidant response genes sequence variants and BPD susceptibility in VLBW infants.  Pediatr Res. 2015;77(3):477-483. doi:10.1038/pr.2014.200PubMedGoogle ScholarCrossref
    154.
    Schena  F, Francescato  G, Cappelleri  A,  et al.  Association between hemodynamically significant patent ductus arteriosus and bronchopulmonary dysplasia.  J Pediatr. 2015;166(6):1488-1492. doi:10.1016/j.jpeds.2015.03.012PubMedGoogle ScholarCrossref
    155.
    Serenius  F, Ewald  U, Farooqi  A, Holmgren  PA, Håkansson  S, Sedin  G.  Short-term outcome after active perinatal management at 23-25 weeks of gestation: a study from two Swedish perinatal centres, part 3: neonatal morbidity.  Acta Paediatr. 2004;93(8):1090-1097. doi:10.1111/j.1651-2227.2004.tb02722.xPubMedGoogle ScholarCrossref
    156.
    Shima  Y, Nishimaki  S, Nakajima  M, Kumasaka  S, Migita  M.  Urinary β-2-microglobulin as an alternative marker for fetal inflammatory response and development of bronchopulmonary dysplasia in premature infants.  J Perinatol. 2011;31(5):330-334. doi:10.1038/jp.2010.129PubMedGoogle ScholarCrossref
    157.
    Soliman  N, Chaput  K, Alshaikh  B, Yusuf  K.  Preeclampsia and the risk of bronchopulmonary dysplasia in preterm infants less than 32 weeks’ gestation.  Am J Perinatol. 2017;34(6):585-592. doi:10.1055/s-0036-1594017PubMedGoogle ScholarCrossref
    158.
    Stichel  H, Bäckström  E, Hafström  O, Nilsson  S, Lappalainen  U, Bry  K.  Inflammatory cytokines in gastric fluid at birth and the development of bronchopulmonary dysplasia.  Acta Paediatr. 2011;100(9):1206-1212. doi:10.1111/j.1651-2227.2011.02286.xPubMedGoogle ScholarCrossref
    159.
    Streubel  AH, Donohue  PK, Aucott  SW.  The epidemiology of atypical chronic lung disease in extremely low birth weight infants.  J Perinatol. 2008;28(2):141-148. doi:10.1038/sj.jp.7211894PubMedGoogle ScholarCrossref
    160.
    Tokuriki  S, Okuno  T, Ohta  G, Ohshima  Y.  Carboxyhemoglobin formation in preterm infants is related to the subsequent development of bronchopulmonary dysplasia.  Dis Markers. 2015;2015:620921. doi:10.1155/2015/620921PubMedGoogle Scholar
    161.
    Viscardi  RM, Muhumuza  CK, Rodriguez  A,  et al.  Inflammatory markers in intrauterine and fetal blood and cerebrospinal fluid compartments are associated with adverse pulmonary and neurologic outcomes in preterm infants.  Pediatr Res. 2004;55(6):1009-1017. doi:10.1203/01.pdr.0000127015.60185.8aPubMedGoogle ScholarCrossref
    162.
    Wang  K, Huang  X, Lu  H, Zhang  Z.  A comparison of KL-6 and Clara cell protein as markers for predicting bronchopulmonary dysplasia in preterm infants.  Dis Markers. 2014;2014:736536. doi:10.1155/2014/736536PubMedGoogle Scholar
    163.
    Watterberg  KL, Gerdes  JS, Cole  CH,  et al.  Prophylaxis of early adrenal insufficiency to prevent bronchopulmonary dysplasia: a multicenter trial.  Pediatrics. 2004;114(6):1649-1657. doi:10.1542/peds.2004-1159PubMedGoogle ScholarCrossref
    164.
    Choi  CW, Kim  BI, Kim  HS, Park  JD, Choi  JH, Son  DW.  Increase of interleukin-6 in tracheal aspirate at birth: a predictor of subsequent bronchopulmonary dysplasia in preterm infants.  Acta Paediatr. 2006;95(1):38-43. doi:10.1080/08035250500404085PubMedGoogle ScholarCrossref
    165.
    Xie  L, Chee  YY, Wong  KY, Cheung  YF.  Cardiac mechanics in children with bronchopulmonary dysplasia.  Neonatology. 2016;109(1):44-51. doi:10.1159/000441051PubMedGoogle ScholarCrossref
    166.
    Yoon  BH, Romero  R, Kim  KS,  et al.  A systemic fetal inflammatory response and the development of bronchopulmonary dysplasia.  Am J Obstet Gynecol. 1999;181(4):773-779. doi:10.1016/S0002-9378(99)70299-1PubMedGoogle ScholarCrossref
    167.
    Zhang  H, Fang  J, Su  H, Chen  M.  Risk factors for bronchopulmonary dysplasia in neonates born at ≤1500 g (1999-2009).  Pediatr Int. 2011;53(6):915-920. doi:10.1111/j.1442-200X.2011.03399.xPubMedGoogle ScholarCrossref
    168.
    Curley  AE, Sweet  DG, Thornton  CM,  et al.  Chorioamnionitis and increased neonatal lung lavage fluid matrix metalloproteinase-9 levels: implications for antenatal origins of chronic lung disease.  Am J Obstet Gynecol. 2003;188(4):871-875. doi:10.1067/mob.2003.215PubMedGoogle ScholarCrossref
    169.
    Durrmeyer  X, Kayem  G, Sinico  M, Dassieu  G, Danan  C, Decobert  F.  Perinatal risk factors for bronchopulmonary dysplasia in extremely low gestational age infants: a pregnancy disorder-based approach.  J Pediatr. 2012;160(4):578-583.e2. doi:10.1016/j.jpeds.2011.09.025PubMedGoogle ScholarCrossref
    170.
    Eriksson  L, Haglund  B, Odlind  V, Altman  M, Kieler  H.  Prenatal inflammatory risk factors for development of bronchopulmonary dysplasia.  Pediatr Pulmonol. 2014;49(7):665-672. doi:10.1002/ppul.22881PubMedGoogle ScholarCrossref
    171.
    Honma  Y, Yada  Y, Takahashi  N, Momoi  MY, Nakamura  Y.  Certain type of chronic lung disease of newborns is associated with Ureaplasma urealyticum infection in utero.  Pediatr Int. 2007;49(4):479-484. doi:10.1111/j.1442-200X.2007.02391.xPubMedGoogle ScholarCrossref
    172.
    Kent  A, Dahlstrom  JE.  Chorioamnionitis/funisitis and the development of bronchopulmonary dysplasia.  J Paediatr Child Health. 2004;40(7):356-359. doi:10.1111/j.1440-1754.2004.00366.xPubMedGoogle ScholarCrossref
    173.
    Kewitz  G, Wudel  S, Hopp  H, Hopfenmüller  W, Vogel  M, Roots  I.  Below median birth weight in appropriate-for-gestational-age preterm infants as a risk factor for bronchopulmonary dysplasia.  J Perinat Med. 2008;36(4):359-364. doi:10.1515/JPM.2008.056PubMedGoogle ScholarCrossref
    174.
    Kim  BI, Choi  CW, Park  JD, Kim  CJ, Choi  JH.  The effect of histologic chorioamnionitis on the development of respiratory distress syndrome and chronic lung disease in preterm infants.  Korean J Pediatr. 2004;47(2):150-156.Google Scholar
    175.
    Lahra  MM, Beeby  PJ, Jeffery  HE.  Intrauterine inflammation, neonatal sepsis, and chronic lung disease: a 13-year hospital cohort study.  Pediatrics. 2009;123(5):1314-1319. doi:10.1542/peds.2008-0656PubMedGoogle ScholarCrossref
    176.
    Lee  HJ, Kim  E-K, Kim  H-S, Choi  CW, Kim  BI, Choi  J-H.  Chorioamnionitis, respiratory distress syndrome and bronchopulmonary dysplasia in extremely low birth weight infants.  J Perinatol. 2011;31(3):166-170. doi:10.1038/jp.2010.113PubMedGoogle ScholarCrossref
    177.
    Metcalfe  A, Lisonkova  S, Sabr  Y, Stritzke  A, Joseph  KS.  Neonatal respiratory morbidity following exposure to chorioamnionitis.  BMC Pediatr. 2017;17(1):128. doi:10.1186/s12887-017-0878-9PubMedGoogle ScholarCrossref
    178.
    Paananen  R, Husa  A-K, Vuolteenaho  R, Herva  R, Kaukola  T, Hallman  M.  Blood cytokines during the perinatal period in very preterm infants: relationship of inflammatory response and bronchopulmonary dysplasia.  J Pediatr. 2009;154(1):39-43.e3. doi:10.1016/j.jpeds.2008.07.012PubMedGoogle ScholarCrossref
    179.
    Rocha  G, Proença  E, Areias  A,  et al.  HLA and bronchopulmonary dysplasia susceptibility: a pilot study.  Dis Markers. 2011;31(4):199-203. doi:10.1155/2011/236082PubMedGoogle ScholarCrossref
    180.
    Shima  Y, Kumasaka  S, Migita  M.  Perinatal risk factors for adverse long-term pulmonary outcome in premature infants: comparison of different definitions of bronchopulmonary dysplasia/chronic lung disease.  Pediatr Int. 2013;55(5):578-581. doi:10.1111/ped.12151PubMedGoogle ScholarCrossref
    181.
    Štimac  M, Juretić  E, Vukelić  V, Matasić  NP, Kos  M, Babić  D.  Effect of chorioamnionitis on mortality, early onset neonatal sepsis and bronchopulmonary dysplasia in preterm neonates with birth weight of <1,500 grams.  Coll Antropol. 2014;38(1):167-171.PubMedGoogle Scholar
    182.
    Torchin  H, Lorthe  E, Goffinet  F,  et al.  Histologic chorioamnionitis and bronchopulmonary dysplasia in preterm infants: the epidemiologic study on low gestational ages 2 cohort.  J Pediatr. 2017;187:98-104.e3. doi:10.1016/j.jpeds.2017.05.019PubMedGoogle ScholarCrossref
    183.
    Natarajan  G, Glibetic  M, Thomas  RL, Aranda  JV.  Chorioamnionitis and ontogeny of circulating prostaglandin and thromboxane in preterm infants.  Am J Perinatol. 2008;25(8):491-497. doi:10.1055/s-0028-1085068PubMedGoogle ScholarCrossref
    184.
    Villamor-Martinez  E, Fumagalli  M, Mohammed Rahim  O,  et al.  Chorioamnionitis is a risk factor for intraventricular hemorrhage in preterm infants: a systematic review and meta-analysis.  Front Physiol. 2018;9:1253. doi:10.3389/fphys.2018.01253PubMedGoogle ScholarCrossref
    185.
    Villamor-Martinez  E, Cavallaro  G, Raffaeli  G,  et al.  Chorioamnionitis as a risk factor for retinopathy of prematurity: an updated systematic review and meta-analysis.  PLoS One. 2018;13(10):e0205838. doi:10.1371/journal.pone.0205838PubMedGoogle Scholar
    186.
    Villamor-Martínez  E, Pierro  M, Cavallaro  G, Mosca  F, Kramer  B, Villamor  E.  Probiotic supplementation in preterm infants does not affect the risk of bronchopulmonary dysplasia: a meta-analysis of randomized controlled trials.  Nutrients. 2017;9(11):E1197. doi:10.3390/nu9111197PubMedGoogle Scholar
    187.
    Jobe  AH, Bancalari  EH.  Controversies about the definition of bronchopulmonary dysplasia at 50 years.  Acta Paediatr. 2017;106(5):692-693. doi:10.1111/apa.13775PubMedGoogle ScholarCrossref
    188.
    Poindexter  BB, Feng  R, Schmidt  B,  et al; Prematurity and Respiratory Outcomes Program.  Comparisons and limitations of current definitions of bronchopulmonary dysplasia for the prematurity and respiratory outcomes program.  Ann Am Thorac Soc. 2015;12(12):1822-1830. doi:10.1513/AnnalsATS.201504-218OCPubMedGoogle ScholarCrossref
    189.
    Beam  KS, Aliaga  S, Ahlfeld  SK, Cohen-Wolkowiez  M, Smith  PB, Laughon  MM.  A systematic review of randomized controlled trials for the prevention of bronchopulmonary dysplasia in infants.  J Perinatol. 2014;34(9):705-710. doi:10.1038/jp.2014.126PubMedGoogle ScholarCrossref
    190.
    Shennan  AT, Dunn  MS, Ohlsson  A, Lennox  K, Hoskins  EM.  Abnormal pulmonary outcomes in premature infants: prediction from oxygen requirement in the neonatal period.  Pediatrics. 1988;82(4):527-532.PubMedGoogle Scholar
    191.
    Walsh  MC, Wilson-Costello  D, Zadell  A, Newman  N, Fanaroff  A.  Safety, reliability, and validity of a physiologic definition of bronchopulmonary dysplasia.  J Perinatol. 2003;23(6):451-456. doi:10.1038/sj.jp.7210963PubMedGoogle ScholarCrossref
    192.
    McElrath  TF, Hecht  JL, Dammann  O,  et al; ELGAN Study Investigators.  Pregnancy disorders that lead to delivery before the 28th week of gestation: an epidemiologic approach to classification.  Am J Epidemiol. 2008;168(9):980-989. doi:10.1093/aje/kwn202PubMedGoogle ScholarCrossref
    193.
    Jobe  AH, Kallapur  SG.  Chorioamnionitis, surfactant, and lung disease in very low birth weight infants.  J Pediatr. 2010;156(1):3-4. doi:10.1016/j.jpeds.2009.08.009PubMedGoogle ScholarCrossref
    194.
    Revello  R, Alcaide  MJ, Dudzik  D, Abehsera  D, Bartha  JL.  Differential amniotic fluid cytokine profile in women with chorioamnionitis with and without funisitis.  J Matern Fetal Neonatal Med. 2016;29(13):2161-2165. PubMedGoogle Scholar
    195.
    Gantert  M, Been  JV, Gavilanes  AW, Garnier  Y, Zimmermann  LJ, Kramer  BW.  Chorioamnionitis: a multiorgan disease of the fetus?  J Perinatol. 2010;30(suppl):S21-S30. doi:10.1038/jp.2010.96PubMedGoogle ScholarCrossref
    196.
    Bax  L, Moons  KG.  Beyond publication bias.  J Clin Epidemiol. 2011;64(5):459-462. doi:10.1016/j.jclinepi.2010.09.003PubMedGoogle ScholarCrossref
    197.
    Jin  ZC, Zhou  XH, He  J.  Statistical methods for dealing with publication bias in meta-analysis.  Stat Med. 2015;34(2):343-360. doi:10.1002/sim.6342PubMedGoogle ScholarCrossref
    198.
    Higgins  RD, Saade  G, Polin  RA,  et al; Chorioamnionitis Workshop Participants.  Evaluation and management of women and newborns with a maternal diagnosis of chorioamnionitis: summary of a workshop.  Obstet Gynecol. 2016;127(3):426-436. doi:10.1097/AOG.0000000000001246PubMedGoogle ScholarCrossref
    199.
    Thompson  SG, Higgins  JP.  How should meta-regression analyses be undertaken and interpreted?  Stat Med. 2002;21(11):1559-1573. doi:10.1002/sim.1187PubMedGoogle ScholarCrossref
    ×