Peripheral Blood Cell Signatures of Plasmodium falciparum Infection during Pregnancy

Sequestration of Plasmodium falciparum-infected erythrocytes in placental intervillous spaces causes inflammation and pathology. Knowledge of the profiles of immune cells associated with the physiopathology of pregnancy-associated malaria (PAM) is scarce. We conducted a longitudinal, prospective stu...

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Main Authors: Ibitokou, Samad, Oesterholt, Mayke, Brutus, Laurent, Borgella, Sophie, Agbowaï, Carine, Ezinmègnon, Sèm, Lusingu, John, Schmiegelow, Christentze, Massougbodji, Achille, Deloron, Philippe, Troye-Blomberg, Marita, Varani, Stefania, Luty, Adrian J. F., Fievet, Nadine
Format: Online
Language:English
Published: Public Library of Science 2012
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3519836/
id pubmed-3519836
recordtype oai_dc
spelling pubmed-35198362012-12-13 Peripheral Blood Cell Signatures of Plasmodium falciparum Infection during Pregnancy Ibitokou, Samad Oesterholt, Mayke Brutus, Laurent Borgella, Sophie Agbowaï, Carine Ezinmègnon, Sèm Lusingu, John Schmiegelow, Christentze Massougbodji, Achille Deloron, Philippe Troye-Blomberg, Marita Varani, Stefania Luty, Adrian J. F. Fievet, Nadine Research Article Sequestration of Plasmodium falciparum-infected erythrocytes in placental intervillous spaces causes inflammation and pathology. Knowledge of the profiles of immune cells associated with the physiopathology of pregnancy-associated malaria (PAM) is scarce. We conducted a longitudinal, prospective study, both in Benin and Tanzania, including ∼1000 pregnant women in each site with systematic follow-up at scheduled antenatal visits until delivery. We used ex vivo flow cytometry to identify peripheral blood mononuclear cell (PBMC) profiles that are associated with PAM and anaemia, determining the phenotypic composition and activation status of PBMC in selected sub-groups with and without PAM both at inclusion and at delivery in a total of 302 women. Both at inclusion and at delivery PAM was associated with significantly increased frequencies both of B cells overall and of activated B cells. Infection-related profiles were otherwise quite distinct at the two different time-points. At inclusion, PAM was associated with anaemia, with an increased frequency of immature monocytes and with a decreased frequency of regulatory T cells (Treg). At delivery, infected women presented with significantly fewer plasmacytoid dendritic cells (DC), more myeloid DC expressing low levels of HLA-DR, and more effector T cells (Teff) compared to uninfected women. Independent associations with an increased risk of anaemia were found for altered antigen-presenting cell frequencies at inclusion, but for an increased frequency of Teff at delivery. Our findings emphasize the prominent role played by B cells during PAM whenever it arises during pregnancy, whilst also revealing signature changes in other circulating cell types that, we conclude, primarily reflect the relative duration of the infections. Thus, the acute, recently-acquired infections present at delivery were marked by changes in DC and Teff frequencies, contrasting with infections at inclusion, considered chronic in nature, that were characterized by an abundance of immature monocytes and a paucity of Treg in PBMC. Public Library of Science 2012-12-11 /pmc/articles/PMC3519836/ /pubmed/23239967 http://dx.doi.org/10.1371/journal.pone.0049621 Text en © 2012 Ibitokou et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Ibitokou, Samad
Oesterholt, Mayke
Brutus, Laurent
Borgella, Sophie
Agbowaï, Carine
Ezinmègnon, Sèm
Lusingu, John
Schmiegelow, Christentze
Massougbodji, Achille
Deloron, Philippe
Troye-Blomberg, Marita
Varani, Stefania
Luty, Adrian J. F.
Fievet, Nadine
spellingShingle Ibitokou, Samad
Oesterholt, Mayke
Brutus, Laurent
Borgella, Sophie
Agbowaï, Carine
Ezinmègnon, Sèm
Lusingu, John
Schmiegelow, Christentze
Massougbodji, Achille
Deloron, Philippe
Troye-Blomberg, Marita
Varani, Stefania
Luty, Adrian J. F.
Fievet, Nadine
Peripheral Blood Cell Signatures of Plasmodium falciparum Infection during Pregnancy
author_facet Ibitokou, Samad
Oesterholt, Mayke
Brutus, Laurent
Borgella, Sophie
Agbowaï, Carine
Ezinmègnon, Sèm
Lusingu, John
Schmiegelow, Christentze
Massougbodji, Achille
Deloron, Philippe
Troye-Blomberg, Marita
Varani, Stefania
Luty, Adrian J. F.
Fievet, Nadine
author_sort Ibitokou, Samad
title Peripheral Blood Cell Signatures of Plasmodium falciparum Infection during Pregnancy
title_short Peripheral Blood Cell Signatures of Plasmodium falciparum Infection during Pregnancy
title_full Peripheral Blood Cell Signatures of Plasmodium falciparum Infection during Pregnancy
title_fullStr Peripheral Blood Cell Signatures of Plasmodium falciparum Infection during Pregnancy
title_full_unstemmed Peripheral Blood Cell Signatures of Plasmodium falciparum Infection during Pregnancy
title_sort peripheral blood cell signatures of plasmodium falciparum infection during pregnancy
description Sequestration of Plasmodium falciparum-infected erythrocytes in placental intervillous spaces causes inflammation and pathology. Knowledge of the profiles of immune cells associated with the physiopathology of pregnancy-associated malaria (PAM) is scarce. We conducted a longitudinal, prospective study, both in Benin and Tanzania, including ∼1000 pregnant women in each site with systematic follow-up at scheduled antenatal visits until delivery. We used ex vivo flow cytometry to identify peripheral blood mononuclear cell (PBMC) profiles that are associated with PAM and anaemia, determining the phenotypic composition and activation status of PBMC in selected sub-groups with and without PAM both at inclusion and at delivery in a total of 302 women. Both at inclusion and at delivery PAM was associated with significantly increased frequencies both of B cells overall and of activated B cells. Infection-related profiles were otherwise quite distinct at the two different time-points. At inclusion, PAM was associated with anaemia, with an increased frequency of immature monocytes and with a decreased frequency of regulatory T cells (Treg). At delivery, infected women presented with significantly fewer plasmacytoid dendritic cells (DC), more myeloid DC expressing low levels of HLA-DR, and more effector T cells (Teff) compared to uninfected women. Independent associations with an increased risk of anaemia were found for altered antigen-presenting cell frequencies at inclusion, but for an increased frequency of Teff at delivery. Our findings emphasize the prominent role played by B cells during PAM whenever it arises during pregnancy, whilst also revealing signature changes in other circulating cell types that, we conclude, primarily reflect the relative duration of the infections. Thus, the acute, recently-acquired infections present at delivery were marked by changes in DC and Teff frequencies, contrasting with infections at inclusion, considered chronic in nature, that were characterized by an abundance of immature monocytes and a paucity of Treg in PBMC.
publisher Public Library of Science
publishDate 2012
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3519836/
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