Maternal Microbe-specific Modulation of Inflammatory Response in Extremely Low-gestational-age Newborns

Overview

Journal mBio

Publisher American Society for Microbiology

Specialty Microbiology

Date 2011 Jan 26

PMID 21264056

Citations 72

Authors

Raina N Fichorova

Andrew B Onderdonk

Hidemi Yamamoto

Mary L Delaney

Andrea M DuBois

Elizabeth Allred

Alan Leviton

Affiliations

Soon will be listed here.

Abstract

The fetal response to intrauterine inflammatory stimuli appears to contribute to the onset of preterm labor as well as fetal injury, especially affecting newborns of extremely low gestational age. To investigate the role of placental colonization by specific groups of microorganisms in the development of inflammatory responses present at birth, we analyzed 25 protein biomarkers in dry blood spots obtained from 527 newborns delivered by Caesarean section in the 23rd to 27th gestation weeks. Bacteria were detected in placentas and characterized by culture techniques. Odds ratios for having protein concentrations in the top quartile for gestation age for individual and groups of microorganisms were calculated. Mixed bacterial vaginosis (BV) organisms were associated with a proinflammatory pattern similar to those of infectious facultative anaerobes. Prevotella and Gardnerella species, anaerobic streptococci, peptostreptococci, and genital mycoplasmas each appeared to be associated with a different pattern of elevated blood levels of inflammation-related proteins. Lactobacillus was associated with low odds of an inflammatory response. This study provides evidence that microorganisms colonizing the placenta provoke distinctive newborn inflammatory responses and that Lactobacillus may suppress these responses.

Citing Articles

Neonatal inflammation and its association with asthma and obesity in late childhood among individuals born extremely preterm.

Emmanuel C, Oran A, Jensen E, Fichorova R, Gower W, Perrin E Pediatr Res. 2024; 96(7):1749-1758.

PMID: 38914762 DOI: 10.1038/s41390-024-03325-x.

Perinatal inflammation, fetal growth restriction, and long-term neurodevelopmental impairment in Bangladesh.

Lee A, Cherkerzian S, Tofail F, Folger L, Ahmed S, Rahman S Pediatr Res. 2024; 96(7):1777-1787.

PMID: 38589559 DOI: 10.1038/s41390-024-03101-x.

Molecular detection of bacteria, placental inflammation, and neonatal sepsis risk.

Franklin A, Freedman A, Wylie K, Mangold K, Wang V, Price E J Perinatol. 2023; 44(1):46-54.

PMID: 37700009 DOI: 10.1038/s41372-023-01775-5.

Zika virus co-opts microRNA networks to persist in placental niches detected by spatial transcriptomics.

Barrozo E, Seferovic M, Hamilton M, Moorshead D, Jochum M, Do T Am J Obstet Gynecol. 2023; 230(2):251.e1-251.e17.

PMID: 37598997 PMC: 10840961. DOI: 10.1016/j.ajog.2023.08.012.

SARS-CoV-2 niches in human placenta revealed by spatial transcriptomics.

Barrozo E, Seferovic M, Castro E, Major A, Moorshead D, Jochum M Med. 2023; 4(9):612-634.e4.

PMID: 37423216 PMC: 10527005. DOI: 10.1016/j.medj.2023.06.003.

References

Muglia L, Katz M . The enigma of spontaneous preterm birth. N Engl J Med. 2010; 362(6):529-35. DOI: 10.1056/NEJMra0904308. View

Odendaal H, Popov I, Schoeman J, Grove D . Preterm labour--is Mycoplasma hominis involved?. S Afr Med J. 2002; 92(3):235-7. View

Uehara A, Takada H . Synergism between TLRs and NOD1/2 in oral epithelial cells. J Dent Res. 2008; 87(7):682-6. DOI: 10.1177/154405910808700709. View

Goldenberg R, Andrews W, Goepfert A, Faye-Petersen O, Cliver S, Carlo W . The Alabama Preterm Birth Study: umbilical cord blood Ureaplasma urealyticum and Mycoplasma hominis cultures in very preterm newborn infants. Am J Obstet Gynecol. 2008; 198(1):43.e1-5. PMC: 2278008. DOI: 10.1016/j.ajog.2007.07.033. View

Creaven P, PLAGER J, Dupere S, Huben R, Takita H, Mittelman A . Phase I clinical trial of recombinant human tumor necrosis factor. Cancer Chemother Pharmacol. 1987; 20(2):137-44. DOI: 10.1007/BF00253968. View

Leitich H, Bodner-Adler B, Brunbauer M, Kaider A, Egarter C, Husslein P . Bacterial vaginosis as a risk factor for preterm delivery: a meta-analysis. Am J Obstet Gynecol. 2003; 189(1):139-47. DOI: 10.1067/mob.2003.339. View

Hillier S, Krohn M, Rabe L, Klebanoff S, Eschenbach D . The normal vaginal flora, H2O2-producing lactobacilli, and bacterial vaginosis in pregnant women. Clin Infect Dis. 1993; 16 Suppl 4:S273-81. DOI: 10.1093/clinids/16.supplement_4.s273. View

Hecht J, Onderdonk A, Delaney M, Allred E, Kliman H, Zambrano E . Characterization of chorioamnionitis in 2nd-trimester C-section placentas and correlation with microorganism recovery from subamniotic tissues. Pediatr Dev Pathol. 2008; 11(1):15-22. DOI: 10.2350/07-06-0285.1. View

Hecht J, Fichorova R, Tang V, Allred E, McElrath T, Leviton A . Relationship Between Neonatal Blood Protein Concentrations and Placenta Histologic Characteristics in Extremely Low GA Newborns. Pediatr Res. 2010; 69(1):68-73. PMC: 3066075. DOI: 10.1203/PDR.0b013e3181fed334. View

10.

Macfarlane S, Furrie E, Cummings J, Macfarlane G . Chemotaxonomic analysis of bacterial populations colonizing the rectal mucosa in patients with ulcerative colitis. Clin Infect Dis. 2004; 38(12):1690-9. DOI: 10.1086/420823. View

11.

Leviton A, Allred E, Kuban K, Hecht J, Onderdonk A, OShea T . Microbiologic and histologic characteristics of the extremely preterm infant's placenta predict white matter damage and later cerebral palsy. the ELGAN study. Pediatr Res. 2009; 67(1):95-101. PMC: 2794973. DOI: 10.1203/PDR.0b013e3181bf5fab. View

12.

Zeuthen L, Fink L, Metzdorff S, Kristensen M, Licht T, Nellemann C . Lactobacillus acidophilus induces a slow but more sustained chemokine and cytokine response in naïve foetal enterocytes compared to commensal Escherichia coli. BMC Immunol. 2010; 11:2. PMC: 2831831. DOI: 10.1186/1471-2172-11-2. View

13.

Castell J, Geiger T, Gross V, Andus T, Walter E, Hirano T . Plasma clearance, organ distribution and target cells of interleukin-6/hepatocyte-stimulating factor in the rat. Eur J Biochem. 1988; 177(2):357-61. DOI: 10.1111/j.1432-1033.1988.tb14384.x. View

14.

Cockle J, Gopichandran N, Walker J, Levene M, Orsi N . Matrix metalloproteinases and their tissue inhibitors in preterm perinatal complications. Reprod Sci. 2007; 14(7):629-45. DOI: 10.1177/1933719107304563. View

15.

Zakharova E, Grandhi J, Wewers M, Gavrilin M . Mycoplasma suppression of THP-1 Cell TLR responses is corrected with antibiotics. PLoS One. 2010; 5(3):e9900. PMC: 2845629. DOI: 10.1371/journal.pone.0009900. View

16.

Leitich H, Brunbauer M, Bodner-Adler B, Kaider A, Egarter C, Husslein P . Antibiotic treatment of bacterial vaginosis in pregnancy: a meta-analysis. Am J Obstet Gynecol. 2003; 188(3):752-8. DOI: 10.1067/mob.2003.167. View

17.

Fang H, Fang S, Chiang Chiau J, Yeung C, Chan W, Jiang C . Inhibitory effects of Lactobacillus casei subsp. rhamnosus on Salmonella lipopolysaccharide-induced inflammation and epithelial barrier dysfunction in a co-culture model using Caco-2/peripheral blood mononuclear cells. J Med Microbiol. 2010; 59(Pt 5):573-579. DOI: 10.1099/jmm.0.009662-0. View

18.

Onderdonk A, Hecht J, McElrath T, Delaney M, Allred E, Leviton A . Colonization of second-trimester placenta parenchyma. Am J Obstet Gynecol. 2008; 199(1):52.e1-52.e10. PMC: 2827873. DOI: 10.1016/j.ajog.2007.11.068. View

19.

Rudd P, Brown M, Cassell G . A prospective study of mycoplasma infection in the preterm infant. Isr J Med Sci. 1984; 20(10):899-901. View

20.

Gantert M, Been J, Gavilanes A, Garnier Y, Zimmermann L, Kramer B . Chorioamnionitis: a multiorgan disease of the fetus?. J Perinatol. 2010; 30 Suppl:S21-30. DOI: 10.1038/jp.2010.96. View