Chemokine modulation in microscopic and submicroscopic Plasmodium falciparum malaria infection in women at delivery in Yaoundé, Cameroon.

In pregnancy-associated malaria, chemokines such as CXCL-4, CXCL-13, CXCL-16, and CCL-24 play critical roles in leucocyte trafficking to tissue sites in the infected placenta where inflammatory reactions are active. However, how plasma levels of these chemokines associate with Plasmodium falciparum...

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Main Authors: Rosette Megnekou, Chris Marco Mbianda Nana, Jean Claude Djontu, Bernard Marie Zambo Bitye, Benderli Christine Nana, Berenice Kenfack Tekougang Zangue, Christiane Josiane Donkeu, Estelle Essangui, Rodrigue Mbea Salawiss, Reine Ndeumou Medouen Seumko'o, Lawrence Ayong, Rose Gana Fomban Leke
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0280615
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author Rosette Megnekou
Chris Marco Mbianda Nana
Jean Claude Djontu
Bernard Marie Zambo Bitye
Benderli Christine Nana
Berenice Kenfack Tekougang Zangue
Christiane Josiane Donkeu
Estelle Essangui
Rodrigue Mbea Salawiss
Reine Ndeumou Medouen Seumko'o
Lawrence Ayong
Rose Gana Fomban Leke
author_facet Rosette Megnekou
Chris Marco Mbianda Nana
Jean Claude Djontu
Bernard Marie Zambo Bitye
Benderli Christine Nana
Berenice Kenfack Tekougang Zangue
Christiane Josiane Donkeu
Estelle Essangui
Rodrigue Mbea Salawiss
Reine Ndeumou Medouen Seumko'o
Lawrence Ayong
Rose Gana Fomban Leke
author_sort Rosette Megnekou
collection DOAJ
description In pregnancy-associated malaria, chemokines such as CXCL-4, CXCL-13, CXCL-16, and CCL-24 play critical roles in leucocyte trafficking to tissue sites in the infected placenta where inflammatory reactions are active. However, how plasma levels of these chemokines associate with Plasmodium falciparum placental malaria and pregnancy outcomes remains not well understood. The present study analyzed the plasma levels of CXCL-4, CXCL-13, CXCL-16, and CCL-24 chemokines in matched peripheral, placental and cord blood in relation with placental malaria (PM), and with submicroscopic parasitaemia. This was a retrospective case-control study (1:3 ratio) involving samples from 134 women (34 PM+ and 100 PM-) enrolled at delivery at the Marie Reine Health Center in Yaoundé, Cameroon between June 2013 and October 2018. Samples were collected just after delivery and used to diagnose microscopic and submicroscopic Plasmodium falciparum infections. Submicroscopic infections were detected by reverse transcription LAMP whereas chemokine levels were determined by Magnetic Luminex Screening Assay. Overall, PM was associated with increased plasma levels of CXCL-13 and CXCL-16 and low levels of CXCL-4 and CCL-24 in both peripheral and placental blood (0.0002 ≤ p ≤ 0.042). Similarly, CCL-24 levels in peripheral and placental blood samples were significantly lower in submicroscopically infected women compared to healthy controls (p = 0.04 and 0.02, respectively). Maternal hemoglobin levels increased with peripheral plasma levels of CXCL-4 (p = 0.005), CXCL-16 (p = 0.03), and CCL-24 (p = 0.002) while birth weight was lower for babies born from women with high levels of peripheral CXCL-13 (p = 0.0006) and low levels of cord CXCL-4 and CCL-24 (p = 0.02 and 0.08, respectively). Together the data suggest that low levels of CXCL-4 and CCL-24 coupled with high plasma levels of CXCL-13 and for a lesser extend CXCL-16 represent signatures of PM in the study population. These findings are relevant for understanding the immunopathogenesis of PM and developing new therapeutic or preventive strategies against severe PM outcomes.
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spelling doaj.art-b4dc6c8d01ec4ce8a9590f6de72594cd2023-01-26T05:31:54ZengPublic Library of Science (PLoS)PLoS ONE1932-62032023-01-01181e028061510.1371/journal.pone.0280615Chemokine modulation in microscopic and submicroscopic Plasmodium falciparum malaria infection in women at delivery in Yaoundé, Cameroon.Rosette MegnekouChris Marco Mbianda NanaJean Claude DjontuBernard Marie Zambo BityeBenderli Christine NanaBerenice Kenfack Tekougang ZangueChristiane Josiane DonkeuEstelle EssanguiRodrigue Mbea SalawissReine Ndeumou Medouen Seumko'oLawrence AyongRose Gana Fomban LekeIn pregnancy-associated malaria, chemokines such as CXCL-4, CXCL-13, CXCL-16, and CCL-24 play critical roles in leucocyte trafficking to tissue sites in the infected placenta where inflammatory reactions are active. However, how plasma levels of these chemokines associate with Plasmodium falciparum placental malaria and pregnancy outcomes remains not well understood. The present study analyzed the plasma levels of CXCL-4, CXCL-13, CXCL-16, and CCL-24 chemokines in matched peripheral, placental and cord blood in relation with placental malaria (PM), and with submicroscopic parasitaemia. This was a retrospective case-control study (1:3 ratio) involving samples from 134 women (34 PM+ and 100 PM-) enrolled at delivery at the Marie Reine Health Center in Yaoundé, Cameroon between June 2013 and October 2018. Samples were collected just after delivery and used to diagnose microscopic and submicroscopic Plasmodium falciparum infections. Submicroscopic infections were detected by reverse transcription LAMP whereas chemokine levels were determined by Magnetic Luminex Screening Assay. Overall, PM was associated with increased plasma levels of CXCL-13 and CXCL-16 and low levels of CXCL-4 and CCL-24 in both peripheral and placental blood (0.0002 ≤ p ≤ 0.042). Similarly, CCL-24 levels in peripheral and placental blood samples were significantly lower in submicroscopically infected women compared to healthy controls (p = 0.04 and 0.02, respectively). Maternal hemoglobin levels increased with peripheral plasma levels of CXCL-4 (p = 0.005), CXCL-16 (p = 0.03), and CCL-24 (p = 0.002) while birth weight was lower for babies born from women with high levels of peripheral CXCL-13 (p = 0.0006) and low levels of cord CXCL-4 and CCL-24 (p = 0.02 and 0.08, respectively). Together the data suggest that low levels of CXCL-4 and CCL-24 coupled with high plasma levels of CXCL-13 and for a lesser extend CXCL-16 represent signatures of PM in the study population. These findings are relevant for understanding the immunopathogenesis of PM and developing new therapeutic or preventive strategies against severe PM outcomes.https://doi.org/10.1371/journal.pone.0280615
spellingShingle Rosette Megnekou
Chris Marco Mbianda Nana
Jean Claude Djontu
Bernard Marie Zambo Bitye
Benderli Christine Nana
Berenice Kenfack Tekougang Zangue
Christiane Josiane Donkeu
Estelle Essangui
Rodrigue Mbea Salawiss
Reine Ndeumou Medouen Seumko'o
Lawrence Ayong
Rose Gana Fomban Leke
Chemokine modulation in microscopic and submicroscopic Plasmodium falciparum malaria infection in women at delivery in Yaoundé, Cameroon.
PLoS ONE
title Chemokine modulation in microscopic and submicroscopic Plasmodium falciparum malaria infection in women at delivery in Yaoundé, Cameroon.
title_full Chemokine modulation in microscopic and submicroscopic Plasmodium falciparum malaria infection in women at delivery in Yaoundé, Cameroon.
title_fullStr Chemokine modulation in microscopic and submicroscopic Plasmodium falciparum malaria infection in women at delivery in Yaoundé, Cameroon.
title_full_unstemmed Chemokine modulation in microscopic and submicroscopic Plasmodium falciparum malaria infection in women at delivery in Yaoundé, Cameroon.
title_short Chemokine modulation in microscopic and submicroscopic Plasmodium falciparum malaria infection in women at delivery in Yaoundé, Cameroon.
title_sort chemokine modulation in microscopic and submicroscopic plasmodium falciparum malaria infection in women at delivery in yaounde cameroon
url https://doi.org/10.1371/journal.pone.0280615
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