Impact of Extreme Prematurity, Chorioamnionitis, and Sepsis on Neonatal Monocyte Characteristics and Functions

J Innate Immun. 2024;16(1):470-488. doi: 10.1159/000541468. Epub 2024 Sep 14.

Abstract

Introduction: The innate branch of the immune system is important in early life, in particular for infants born preterm.

Methods: We performed a longitudinal analysis of the peripheral monocyte compartment in extremely preterm children from a randomized, placebo-controlled study of probiotic supplementation. PBMCs and fecal samples were collected at several timepoints during the first months of life. Monocyte characteristics were analyzed by flow cytometry, and LPS-stimulated PBMC culture supernatants were analyzed by Luminex or ELISA. Plasma cytokines and gut microbiota composition were analyzed by ELISA and 16S rRNA-sequencing, respectively.

Results: The extremely preterm infants had persistent alterations in their monocyte characteristics that were further aggravated in chorioamnionitis cases. They showed a markedly reduced TLR4 expression and hampered LPS-stimulated cytokine responses 14 days after birth. Notably, at later timepoints, TLR4 expression and LPS responses no longer correlated. Sepsis during the first weeks of life strongly associated with increased pro-inflammatory, and reduced IL-10, responses also at postmenstrual week 36. Further, we report a correlation between gut microbiota features and monocyte phenotype and responses, but also that probiotic supplementation associated with distinct monocyte phenotypic characteristics, without significantly influencing their responsiveness.

Conclusion: Extremely preterm infants have monocyte characteristics and functional features that deviate from infants born full-term. Some of these differences persist until they reach an age corresponding to full-term, potentially making them more vulnerable to microbial exposures during the first months of life.

Keywords: Chorioamnionitis; Extreme prematurity; Limosilactobacillus reuteri probiotic supplementation; Monocytes; Sepsis.

Publication types

  • Randomized Controlled Trial

MeSH terms

  • Cells, Cultured
  • Chorioamnionitis* / immunology
  • Cytokines / metabolism
  • Female
  • Gastrointestinal Microbiome* / immunology
  • Humans
  • Immunity, Innate
  • Infant, Extremely Premature* / immunology
  • Infant, Newborn
  • Lipopolysaccharides / immunology
  • Longitudinal Studies
  • Male
  • Monocytes* / immunology
  • Pregnancy
  • Probiotics
  • Sepsis* / immunology
  • Sepsis* / microbiology
  • Toll-Like Receptor 4* / metabolism

Substances

  • Toll-Like Receptor 4
  • TLR4 protein, human
  • Cytokines
  • Lipopolysaccharides

Grants and funding

This research was funded by the Swedish Research Council (Dnr 2016-01715, 2020-01839 and 2023-02616 to E.S.-E.; and 921.2014-7060 to T.A.), BioGaia AB (T.A.), the Cancer and Allergy Foundation to E.S.-E., the Hesselman Foundation to E.S.-E., the Golden Jubilee Memorial Foundation to E.S.-E., the Freemasons of Sweden and Stockholm University to E.S.-E., the Swedish Society for Medical Research to T.A., the Swedish Society of Medicine to T.A., the Research Council for South-East Sweden to T.A., ALF Grants to T.A., Region Östergötland to T.A., Medical Inflammation and Infection Center (MIIC), and Linköping University to T.A.