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Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Research

Impact of placental Plasmodium falciparum malaria infection on the Cameroonian maternal and neonate’s plasma levels of some cytokines known to regulate T cells differentiation and function

Authors: Jean Claude Djontu, Stalone Siewe Siewe, Yolande Delphine Mpeke Edene, Benderli Christine Nana, Edwige Vanessa Chomga Foko, Jude Daiga Bigoga, Rose F. G. Leke, Rosette Megnekou

Published in: Malaria Journal | Issue 1/2016

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Abstract

Background

The impact of placental malaria (PM) infection on the expression profile of some cytokines known to regulate T cell differentiation and function and their influence on birth weight remain unclear. Moreover, there are no reports showing the relationship between PM and IL-27 or IL-28A. This study therefore sought to investigate whether placental P. falciparum infection alters the expression profile of the cytokines IL-28A, IL-27, IL-17E and IL-6 in mothers and their new born.

Methods

In a cross-sectional study conducted between 2013 and 2015 in Yaoundé, Cameroon, peripheral, placental and cord blood samples were collected from 108 women at delivery. Parasitaemia was determined microscopically and haemoglobin levels determined using a Coulter counter. Plasma levels of cytokines (IL-28A, IL-27, IL-17E and IL-6) were measured by Luminex magnetic screening assay.

Results

Malaria parasite density in placenta impression smear associated negatively with maternal haemoglobin level (P < 0.0001) and baby birth weight (P = 0.016). While IL-17E, IL-27 and IL-28A levels were significantly higher in placental and cord plasma than in peripheral (P < 0.0001, < 0.001 and P = 0.026, respectively), an opposite relationship was observed with IL-6 (P = 0.0018). Multivariate analysis confirmed results of univariate analysis where the presence of malaria parasites or pigments in placenta tissue impression smears correlated with decrease levels of maternal IL-17E, IL-27 and IL-28A and neonate levels of IL-28A and IL-17E (0.0001 ≤ P ≤ 0.02). Placental and peripheral parasitaemias also correlated positively with peripheral plasma levels of IL-6 (rs = 0.18, P = 0.05 and rs = 0.17, P = 0.07, respectively). In addition, high maternal haemoglobin level associated with increasing levels of IL-17E, IL-27 and IL-28A in peripheral plasma (0.002 ≤ P ≤ 0.018) and high placental and cord plasma levels of these cytokines associated with increasing birth weight (0.0001 ≤ P ≤ 0.0027).

Conclusions

Placental malaria downregulates maternal plasma levels of IL-17E, IL-27 and IL-28A and neonates’ plasma levels of IL-17E and IL-28A cytokines, which could help for parasite clearance and increase child birth weight. The study is expected to provide leads that should help identify potential biomarkers for improved birth weight and therapeutic interventions.
Literature
1.
go back to reference Fried M, Duffy PE. Adherence of Plasmodium falciparum to chondroitin sulphate A in the human placenta. Science. 1996;272:1502.CrossRefPubMed Fried M, Duffy PE. Adherence of Plasmodium falciparum to chondroitin sulphate A in the human placenta. Science. 1996;272:1502.CrossRefPubMed
2.
go back to reference Beeson JG, Rogerson SJ, Cooke BM, Reeder JC. Adhesion of Plasmodium falciparum-infected erythrocytes to hyaluronic acid in placental malaria. Nat Med. 2000;6:86–90.CrossRefPubMedPubMedCentral Beeson JG, Rogerson SJ, Cooke BM, Reeder JC. Adhesion of Plasmodium falciparum-infected erythrocytes to hyaluronic acid in placental malaria. Nat Med. 2000;6:86–90.CrossRefPubMedPubMedCentral
3.
go back to reference Davison BB, Cogswell FB, Baskin GB, Falkenstein K, Henson KP, Krogstad D. Placental changes associated with fetal outcome in the Plasmodium coatneyi/rhesus monkey model of malaria in pregnancy. Am J Trop Med Hyg. 2000;63:158–73.PubMed Davison BB, Cogswell FB, Baskin GB, Falkenstein K, Henson KP, Krogstad D. Placental changes associated with fetal outcome in the Plasmodium coatneyi/rhesus monkey model of malaria in pregnancy. Am J Trop Med Hyg. 2000;63:158–73.PubMed
4.
go back to reference Ordi J, Menendez C, Ismail MR, Ventura PJ, Palacin A, Kahigwa E, et al. Placental malaria is associated with cell-mediated inflammatory responses with selective absence of natural killer cells. J Infect Dis. 2001;183:1100–7.CrossRefPubMed Ordi J, Menendez C, Ismail MR, Ventura PJ, Palacin A, Kahigwa E, et al. Placental malaria is associated with cell-mediated inflammatory responses with selective absence of natural killer cells. J Infect Dis. 2001;183:1100–7.CrossRefPubMed
5.
go back to reference Fried M, Muga RO, Misore AO, Duffy PE. Malaria elicits type 1 cytokines in the human placenta: IFN-gama TNF-α associated with pregnancy outcomes. J Immunol. 1998;160:2523–30.PubMed Fried M, Muga RO, Misore AO, Duffy PE. Malaria elicits type 1 cytokines in the human placenta: IFN-gama TNF-α associated with pregnancy outcomes. J Immunol. 1998;160:2523–30.PubMed
6.
go back to reference Kabyemela ER, Muehlenbachs A, Fried M, Kurtis JD, Mutabingwa TK, Duffy PE. Maternal peripheral blood level of IL-10 as a marker for inflammatory placental malaria. Malar J. 2008;7:26.CrossRefPubMedPubMedCentral Kabyemela ER, Muehlenbachs A, Fried M, Kurtis JD, Mutabingwa TK, Duffy PE. Maternal peripheral blood level of IL-10 as a marker for inflammatory placental malaria. Malar J. 2008;7:26.CrossRefPubMedPubMedCentral
7.
go back to reference Agudelo OM, Aristizabal BH, Yanow SK, Arango E, Carmona-Fonseca J, Maestre A. Submicroscopic infection of placenta by Plasmodium produces Th1/Th2 cytokine imbalance, inflammation and hypoxia in women from north–west Colombia. Malar J. 2014;13:122.CrossRefPubMedPubMedCentral Agudelo OM, Aristizabal BH, Yanow SK, Arango E, Carmona-Fonseca J, Maestre A. Submicroscopic infection of placenta by Plasmodium produces Th1/Th2 cytokine imbalance, inflammation and hypoxia in women from north–west Colombia. Malar J. 2014;13:122.CrossRefPubMedPubMedCentral
8.
go back to reference Suguitan AL, Leke RG, Fouda G, Zhou A, Thuita L, Metenou S, Fogako J, Megnekou R, Taylor DW. Changes in the levels of chemokines and cytokines in the placentas of women with Plasmodium falciparum malaria. J Infect Dis. 2003;188(7):1074–82.CrossRefPubMed Suguitan AL, Leke RG, Fouda G, Zhou A, Thuita L, Metenou S, Fogako J, Megnekou R, Taylor DW. Changes in the levels of chemokines and cytokines in the placentas of women with Plasmodium falciparum malaria. J Infect Dis. 2003;188(7):1074–82.CrossRefPubMed
9.
go back to reference Raghupathy R. Th1-type immunity is incompatible with successful pregnancy. Immunol Today. 1997;18:478–82.CrossRefPubMed Raghupathy R. Th1-type immunity is incompatible with successful pregnancy. Immunol Today. 1997;18:478–82.CrossRefPubMed
10.
go back to reference Megnekou R, Djontu JC, Bigoga JD, Lissom A, Magagoum SH. Role of some biomarkers in malaria in women living in Yaoundé, Cameroun. Acta Trop. 2015;181:97–102.CrossRef Megnekou R, Djontu JC, Bigoga JD, Lissom A, Magagoum SH. Role of some biomarkers in malaria in women living in Yaoundé, Cameroun. Acta Trop. 2015;181:97–102.CrossRef
11.
go back to reference Megnekou R, Djontu JC, Bigoga JD, Medou FM, Tenou S, Lissom A. Impact of placental Plasmodium falciparum malaria on the profile of some oxidative stress biomarkers in women living in Yaoundé, Cameroon. PLoS ONE. 2015;10:e0134633.CrossRefPubMedPubMedCentral Megnekou R, Djontu JC, Bigoga JD, Medou FM, Tenou S, Lissom A. Impact of placental Plasmodium falciparum malaria on the profile of some oxidative stress biomarkers in women living in Yaoundé, Cameroon. PLoS ONE. 2015;10:e0134633.CrossRefPubMedPubMedCentral
12.
go back to reference Lucas S, Ghilardi N, Li J, de Sauvage FJ. IL-27 regulates IL-12 responsiveness of naive 27CD4+ T cells through Stat1-dependant and independent mechanisms. Proc Natl Acad Sci USA. 2003;100:15047–52.CrossRefPubMedPubMedCentral Lucas S, Ghilardi N, Li J, de Sauvage FJ. IL-27 regulates IL-12 responsiveness of naive 27CD4+ T cells through Stat1-dependant and independent mechanisms. Proc Natl Acad Sci USA. 2003;100:15047–52.CrossRefPubMedPubMedCentral
13.
go back to reference Takeda A, Hamano S, Yamanaka Hanada AT, Ishibashi T, Mak TW, et al. Cutting edge: role of IL-27/WSX-1 signaling for induction of T-bet through activation of STAT1 during initial Th1commitment. J Immunol. 2003;170:4886–90.CrossRefPubMed Takeda A, Hamano S, Yamanaka Hanada AT, Ishibashi T, Mak TW, et al. Cutting edge: role of IL-27/WSX-1 signaling for induction of T-bet through activation of STAT1 during initial Th1commitment. J Immunol. 2003;170:4886–90.CrossRefPubMed
14.
go back to reference Kamiya S, Owaki T, Morishima N, Fukai F, Mizuguchi J, Yoshimoto T. An indispensable role for STAT1 in IL-27-induced T-bet expression but not proliferation of naive CD4+ T cells. J Immunol. 2004;173:3871–7.CrossRefPubMed Kamiya S, Owaki T, Morishima N, Fukai F, Mizuguchi J, Yoshimoto T. An indispensable role for STAT1 in IL-27-induced T-bet expression but not proliferation of naive CD4+ T cells. J Immunol. 2004;173:3871–7.CrossRefPubMed
15.
go back to reference Stumhofer JS, Wilson EH, Huang E, Tato CM, Johnson LM, Villarino AV, et al. Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat Immunol. 2006;7:937–45.CrossRefPubMed Stumhofer JS, Wilson EH, Huang E, Tato CM, Johnson LM, Villarino AV, et al. Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat Immunol. 2006;7:937–45.CrossRefPubMed
16.
go back to reference Tomohiro Y, Takayuki Y, Koubun Y, Junichiro M, Kenji N. IL-27 Suppresses Th2 cell development and Th2 cytokines production from polarized Th2 cells: a novel therapeutic way for Th2-mediated allergic inflammation. J Immunol. 2007;179:4415–23.CrossRef Tomohiro Y, Takayuki Y, Koubun Y, Junichiro M, Kenji N. IL-27 Suppresses Th2 cell development and Th2 cytokines production from polarized Th2 cells: a novel therapeutic way for Th2-mediated allergic inflammation. J Immunol. 2007;179:4415–23.CrossRef
17.
go back to reference Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N, et al. Conversion of peripheral CD4 + CD25- naive T cells to CD4+ CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med. 2003;198:1875–86.CrossRefPubMedPubMedCentral Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N, et al. Conversion of peripheral CD4 + CD25- naive T cells to CD4+ CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med. 2003;198:1875–86.CrossRefPubMedPubMedCentral
18.
go back to reference Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature. 2006;441:235–8.CrossRefPubMed Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature. 2006;441:235–8.CrossRefPubMed
19.
go back to reference Dolgachev V, Petersen BC, Budelsky AL, Berlin AA, Lukacs NW. Pulmonary IL-17E (IL-25) production and IL-17RB + myeloid cell-derived Th2 cytokine production are dependent upon stem cell factor-induced responses during chronic allergic pulmonary disease. J Immunol. 2009;183:5705–15.CrossRefPubMed Dolgachev V, Petersen BC, Budelsky AL, Berlin AA, Lukacs NW. Pulmonary IL-17E (IL-25) production and IL-17RB + myeloid cell-derived Th2 cytokine production are dependent upon stem cell factor-induced responses during chronic allergic pulmonary disease. J Immunol. 2009;183:5705–15.CrossRefPubMed
20.
go back to reference Terrier B, Bièche I, Maisonobe T, Laurendeau I, Rosenzwajg M, Kahn JE, Diemert MC, et al. IL-25: a cytokine linking eosinophils and adaptative immunity in Churg-Strauss syndrome. Blood. 2010;116:4523–31.CrossRefPubMed Terrier B, Bièche I, Maisonobe T, Laurendeau I, Rosenzwajg M, Kahn JE, Diemert MC, et al. IL-25: a cytokine linking eosinophils and adaptative immunity in Churg-Strauss syndrome. Blood. 2010;116:4523–31.CrossRefPubMed
21.
go back to reference Wong CK, Li PW, Lam CW. Intracellular JNK, p38 MAPK and NF-kB regulate IL-25 induced release of cytokines and chemokines from costimulated T helper lymphocytes. Immunol Lett. 2007;112:82–91.CrossRefPubMed Wong CK, Li PW, Lam CW. Intracellular JNK, p38 MAPK and NF-kB regulate IL-25 induced release of cytokines and chemokines from costimulated T helper lymphocytes. Immunol Lett. 2007;112:82–91.CrossRefPubMed
22.
go back to reference Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK, et al. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol. 2003;4:69–77.CrossRefPubMed Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK, et al. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol. 2003;4:69–77.CrossRefPubMed
23.
go back to reference Meager A, Visvalingam K, Dilger P, Bryan D, Wadhwa M. Biological activity of interleukins-28 and -29: comparison with type I interferons. Cytokine. 2005;31:109–18.CrossRefPubMed Meager A, Visvalingam K, Dilger P, Bryan D, Wadhwa M. Biological activity of interleukins-28 and -29: comparison with type I interferons. Cytokine. 2005;31:109–18.CrossRefPubMed
24.
go back to reference Lauterbach H, Bathke B, Gilles Traidl-Hoffmann C, Luber CA, Fejer G, et al. Mouse CD8α+ DCs and human BDCA3+ DCs are major producers of IFN-λ in response to poly IC. J Exp Med. 2010;207:2703–17.CrossRefPubMedPubMedCentral Lauterbach H, Bathke B, Gilles Traidl-Hoffmann C, Luber CA, Fejer G, et al. Mouse CD8α+ DCs and human BDCA3+ DCs are major producers of IFN-λ in response to poly IC. J Exp Med. 2010;207:2703–17.CrossRefPubMedPubMedCentral
25.
go back to reference Koltsida O, Hausding M, Stavropoulos A, Koch S, Tzelepis G, Ubel C, et al. IL-28A (IFN-λ2) modulates lung DC function to promote Th1 immune skewing and suppress allergic airway disease. EMBO Mol Med. 2011;3:348–56.CrossRefPubMedPubMedCentral Koltsida O, Hausding M, Stavropoulos A, Koch S, Tzelepis G, Ubel C, et al. IL-28A (IFN-λ2) modulates lung DC function to promote Th1 immune skewing and suppress allergic airway disease. EMBO Mol Med. 2011;3:348–56.CrossRefPubMedPubMedCentral
26.
go back to reference Hunter CA. New IL-12-family members: IL-23 and IL-27, cytokines with divergent functions. Nat Rev Immunol. 2005;5:521–31.CrossRefPubMed Hunter CA. New IL-12-family members: IL-23 and IL-27, cytokines with divergent functions. Nat Rev Immunol. 2005;5:521–31.CrossRefPubMed
27.
go back to reference Megnekou R, Lissom A, Bigoga JD, Djontu JC. Effects of pregnancy-associated malaria on T cell cytokines in Cameroonian Women. Scandin J Immunol. 2015;84:504–14. Megnekou R, Lissom A, Bigoga JD, Djontu JC. Effects of pregnancy-associated malaria on T cell cytokines in Cameroonian Women. Scandin J Immunol. 2015;84:504–14.
28.
go back to reference Kimura D, Mivakoda M, Kimura K, Honma K, Hara H, Yoshida H, et al. Interleukin -27—Producing CD4 (+) T cells regulate protective immunity during malaria parasite infection. Immunity. 2016;44:672–82.CrossRefPubMed Kimura D, Mivakoda M, Kimura K, Honma K, Hara H, Yoshida H, et al. Interleukin -27—Producing CD4 (+) T cells regulate protective immunity during malaria parasite infection. Immunity. 2016;44:672–82.CrossRefPubMed
29.
go back to reference Rogerson JS, Hviid L, Duffy EP, Leke FGR, Taylor DW. Malaria in pregnancy: pathogenesis and immunity. Lancet. 2007;7:105–15.CrossRefPubMed Rogerson JS, Hviid L, Duffy EP, Leke FGR, Taylor DW. Malaria in pregnancy: pathogenesis and immunity. Lancet. 2007;7:105–15.CrossRefPubMed
30.
go back to reference Bennett WA, Lagoo-Deenadayalan S, Whitworth NS, Stopple JA, Barber WH, Hale E, et al. First trimester human chorionic villi express both immunoregulatory and inflammatory cytokines: a role for interleukin-10 in regulating the cytokine network of pregnancy. Am J Reprod Immunol. 1999;41:70–8.CrossRefPubMed Bennett WA, Lagoo-Deenadayalan S, Whitworth NS, Stopple JA, Barber WH, Hale E, et al. First trimester human chorionic villi express both immunoregulatory and inflammatory cytokines: a role for interleukin-10 in regulating the cytokine network of pregnancy. Am J Reprod Immunol. 1999;41:70–8.CrossRefPubMed
31.
go back to reference Lin H, Mosmann TR, Guilbert L, Tuntipopipat S, Wegmann TG. Synthesis of T helper2-type cytokines at the maternal foetal interface. J Immunol. 1993;151:4562–73.PubMed Lin H, Mosmann TR, Guilbert L, Tuntipopipat S, Wegmann TG. Synthesis of T helper2-type cytokines at the maternal foetal interface. J Immunol. 1993;151:4562–73.PubMed
32.
go back to reference Kabyemela ER, Fried M, Kurtis JD, Mutabingwa KT, Duffy PE. Fetal responses during placental malaria modify the risk of low birth weight. Infect Immun. 2008;76:1527–34.CrossRefPubMedPubMedCentral Kabyemela ER, Fried M, Kurtis JD, Mutabingwa KT, Duffy PE. Fetal responses during placental malaria modify the risk of low birth weight. Infect Immun. 2008;76:1527–34.CrossRefPubMedPubMedCentral
33.
go back to reference Wilkinson A, Pedersen S, Urassa M, Michael D, Andreasen A, Todd J, et al. Elevated umbilical cord cytokines are related to birth size in HIV-exposed and unexposed Infants. FASEB J. 2015;29:403–5. Wilkinson A, Pedersen S, Urassa M, Michael D, Andreasen A, Todd J, et al. Elevated umbilical cord cytokines are related to birth size in HIV-exposed and unexposed Infants. FASEB J. 2015;29:403–5.
34.
go back to reference Chêne A, Briand V, Ibitoukou S, Dechayvanne S, Massougbodii A, Deloron P, et al. Placental cytokine and chemokine profiles reflect pregnancy outcomes in women exposed to Plasmodium falciparum infection. Infect Immun. 2014;82:3783–9.CrossRefPubMedPubMedCentral Chêne A, Briand V, Ibitoukou S, Dechayvanne S, Massougbodii A, Deloron P, et al. Placental cytokine and chemokine profiles reflect pregnancy outcomes in women exposed to Plasmodium falciparum infection. Infect Immun. 2014;82:3783–9.CrossRefPubMedPubMedCentral
35.
go back to reference Ibitokou S, Oesterholt M, Brutus L, Borgelle S, Agbowai C, Ezinmègnon S, et al. Peripheral blood cell signatures of Plasmodium falciparum infection during pregnancy. PLoS ONE. 2012;7:e49621.CrossRefPubMedPubMedCentral Ibitokou S, Oesterholt M, Brutus L, Borgelle S, Agbowai C, Ezinmègnon S, et al. Peripheral blood cell signatures of Plasmodium falciparum infection during pregnancy. PLoS ONE. 2012;7:e49621.CrossRefPubMedPubMedCentral
36.
go back to reference Yin Z, Dai J, Deng J, Sheikh F, Natalia M, Shih T, et al. Type III IFNs are produced by and stimulate human plasmacytoid dendritic cells1. J Immunol. 2012;189:2735–45.CrossRefPubMedPubMedCentral Yin Z, Dai J, Deng J, Sheikh F, Natalia M, Shih T, et al. Type III IFNs are produced by and stimulate human plasmacytoid dendritic cells1. J Immunol. 2012;189:2735–45.CrossRefPubMedPubMedCentral
38.
go back to reference Kastelein RA, Hunter CA, Cua DJ. Discovery and biology of IL-23 and IL-27: related but functionally distinct regulators of inflammation. Annu Rev Immunol. 2007;25:221–42.CrossRefPubMed Kastelein RA, Hunter CA, Cua DJ. Discovery and biology of IL-23 and IL-27: related but functionally distinct regulators of inflammation. Annu Rev Immunol. 2007;25:221–42.CrossRefPubMed
39.
go back to reference Veldhoen M, Hocking RJ, Atkins CJ, Locksley RM, Stockinger B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity. 2006;24:179–89.CrossRefPubMed Veldhoen M, Hocking RJ, Atkins CJ, Locksley RM, Stockinger B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity. 2006;24:179–89.CrossRefPubMed
40.
go back to reference Boström S, Ibitokou S, Oesterholt M, Schmiegelow C, Persson JO, Minja D, et al. Biomarkers of Plasmodium falciparum infection during pregnancy in women living in north-eastern Tanzania. PLoS ONE. 2012;7:e48763.CrossRefPubMedPubMedCentral Boström S, Ibitokou S, Oesterholt M, Schmiegelow C, Persson JO, Minja D, et al. Biomarkers of Plasmodium falciparum infection during pregnancy in women living in north-eastern Tanzania. PLoS ONE. 2012;7:e48763.CrossRefPubMedPubMedCentral
41.
go back to reference Fievet N, Moussa M, Tami G, Maubert B, Cot M, Deloron P, et al. Plasmodium falciparum induces a Th1/Th2 disequilibrium, favouring the Th1-type pathway, in the human placenta. J Infect Dis. 2001;183:1530–4.CrossRefPubMed Fievet N, Moussa M, Tami G, Maubert B, Cot M, Deloron P, et al. Plasmodium falciparum induces a Th1/Th2 disequilibrium, favouring the Th1-type pathway, in the human placenta. J Infect Dis. 2001;183:1530–4.CrossRefPubMed
42.
go back to reference Mc Donald CR, Tan V, Kain KC. Complement activation in placental malaria. Front Microbial. 2015;6:1–9. Mc Donald CR, Tan V, Kain KC. Complement activation in placental malaria. Front Microbial. 2015;6:1–9.
43.
go back to reference Taylor-Robinson AW, Smith EC. A dichotomous role for nitric oxide in protection against blood stage malaria infection. Immunol Let. 1999;67:1–9.CrossRef Taylor-Robinson AW, Smith EC. A dichotomous role for nitric oxide in protection against blood stage malaria infection. Immunol Let. 1999;67:1–9.CrossRef
44.
go back to reference Rogerson SJ, Pollina E, Getachew A, Tadesse E, Lema VM, Molyneux ME. Placental monocyte infiltrates in response to Plasmodium falciparum malaria infection and their association with adverse pregnancy outcomes. Am J Trop Med Hyg. 2003;68:115–9.PubMed Rogerson SJ, Pollina E, Getachew A, Tadesse E, Lema VM, Molyneux ME. Placental monocyte infiltrates in response to Plasmodium falciparum malaria infection and their association with adverse pregnancy outcomes. Am J Trop Med Hyg. 2003;68:115–9.PubMed
45.
go back to reference Megnekou R, Staalsoe T, Hviid L. Cytokine response to pregnancy-associated recrudescence of Plasmodium berghei infection in mice with pre-existing immunity to malaria. Malar J. 2013;12:387.CrossRefPubMedPubMedCentral Megnekou R, Staalsoe T, Hviid L. Cytokine response to pregnancy-associated recrudescence of Plasmodium berghei infection in mice with pre-existing immunity to malaria. Malar J. 2013;12:387.CrossRefPubMedPubMedCentral
Metadata
Title
Impact of placental Plasmodium falciparum malaria infection on the Cameroonian maternal and neonate’s plasma levels of some cytokines known to regulate T cells differentiation and function
Authors
Jean Claude Djontu
Stalone Siewe Siewe
Yolande Delphine Mpeke Edene
Benderli Christine Nana
Edwige Vanessa Chomga Foko
Jude Daiga Bigoga
Rose F. G. Leke
Rosette Megnekou
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2016
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-016-1611-0

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