Fievet N, Moussa M, Tami G, Maubert B, Cot M, Deloron P, Chaouat G, 2001. Plasmodium falciparum induces a Th1/Th2 disequilibrium, favoring the Th1-type pathway, in the human placenta. J Infect Dis 183: 1530–1534.
Alemu A, Shiferaw Y, Addis Z, Mathewos B, Birhan W, 2013. Effect of malaria on HIV/AIDS transmission and progression. Parasites & Vectors 6: 18.
Li XX, Zhou XN, 2013. Co-infection of tuberculosis and parasitic diseases in humans: a systematic review. Parasites & Vectors 6: 79.
ter Kuile FO, Parise ME, Verhoeff FH, Udhayakumar V, Newman RD, van Eijk AM, Rogerson SJ, Steketee RW, 2004. The burden of co-infection with human immunodeficiency virus type 1 and malaria in pregnant women in sub-Saharan Africa. Am J Trop Med Hyg 71 (Suppl): 41–54.
Briand V, Badaut C, Cot M, 2009. Placental malaria, maternal HIV infection and infant morbidity. Ann Trop Paediatr 29: 71–83.
Tkachuk AN, Moormann AM, Poore JA, Rochford RA, Chensue SW, Mwapasa V, Meshnick SR, 2001. Malaria enhances expression of CC chemokine receptor 5 on placental macrophages. J Infect Dis 183: 967–972.
van Eijk AM, Ayisi JG, ter Kuile FO, Misore AO, Otieno JA, Rosen DH, Kager PA, Steketee RW, Nahlen BL, 2003. HIV increases the risk of malaria in women of all gravidities in Kisumu, Kenya. AIDS 17: 595–603.
Steketee RW, Wirima JJ, Bloland PB, Chilima B, Mermin JH, Chitsulo L, Breman JG, 1996. Impairment of a pregnant womans acquired ability to limit Plasmodium falciparum by infection with human immunodeficiency virus type-1. Am J Trop Med Hyg 55 (Suppl S): 42–49.
Kfutwah A, Mary JY, Lemen B, Leke R, Rousset D, Barre-Sinoussi F, Nerrienet E, Menu E, Ayouba A, 2009. Plasmodium falciparum infection significantly impairs placental cytokine profile in HIV infected Cameroonian women. PLoS ONE 4: e8114.
Verhoeff FH, Brabin BJ, Hart CA, Chimsuku L, Kazembe P, Broadhead RL, 1999. Increased prevalence of malaria in HIV-infected pregnant women and its implications for malaria control. Trop Med Int Health 4: 5–12.
Kabyemela ER, Muehlenbachs A, Fried M, Kurtis JD, Mutabingwa TK, Duffy PE, 2008. Maternal peripheral blood level of IL-10 as a marker for inflammatory placental malaria. Malar J 7: 26.
Rogerson SJ, Pollina E, Getachew A, Tadesse E, Lema VM, Molyneux ME, 2003. Placental monocyte infiltrates in response to Plasmodium falciparum malaria infection and their association with adverse pregnancy outcomes. Am J Trop Med Hyg 68: 115–119.
Suguitan AL Jr, Leke RG, Fouda G, Zhou A, Thuita L, Metenou S, Fogako J, Megnekou R, Taylor DW, 2003. Changes in the levels of chemokines and cytokines in the placentas of women with Plasmodium falciparum malaria. J Infect Dis 188: 1074–1082.
Moore JM, Chaisavaneeyakorn S, Perkins DJ, Othoro C, Otieno J, Nahlen BL, Shi YP, Udhayakumar V, 2004. Hemozoin differentially regulates proinflammatory cytokine production in human immunodeficiency virus-seropositive and -seronegative women with placental malaria. Infect Immun 72: 7022–7029.
Denoeud-Ndam L, Zannou DM, Fourcade C, Taron-Brocard C, Porcher R, Atadokpede F, Komongui DG, Dossou-Gbete L, Afangnihoun A, Ndam NT, Girard PM, Cot M, 2014. Cotrimoxazole prophylaxis versus mefloquine intermittent preventive treatment to prevent malaria in HIV-infected pregnant women: two randomized controlled trials. J Acquir Immune Defic Syndr 65: 198–206.
Rozin A, Schapira D, Braun-Moscovici Y, Nahir AM, 2001. Cotrimoxazole treatment for rheumatoid arthritis. Semin Arthritis Rheum 31: 133–141.
Diallo A, Ndam NT, Moussiliou A, Dos Santos S, Ndonky A, Borderon M, Oliveau S, Lalou R, Le Hesran JY, 2012. Asymptomatic carriage of Plasmodium in urban Dakar: the risk of malaria should not be underestimated. PLoS ONE 7: e31100.
Taylor SM, Mayor A, Mombo-Ngoma G, Kenguele HM, Ouedraogo S, Ndam NT, Mkali H, Mwangoka G, Valecha N, Singh JP, Clark MA, Verweij JJ, Adegnika AA, Severini C, Menegon M, Macete E, Menendez C, Cistero P, Njie F, Affara M, Otieno K, Kariuki S, ter Kuile FO, Meshnick SR, 2014. A quality control program within a clinical trial Consortium for PCR protocols to detect Plasmodium species. J Clin Microbiol 52: 2144–2149.
Moussiliou A, Sissinto-Savi De Tove Y, Doritchamou J, Luty AJ, Massougbodji A, Alifrangis M, Deloron P, Tuikue Ndam N, 2013. High rates of parasite recrudescence following intermittent preventive treatment with sulphadoxine-pyrimethamine during pregnancy in Benin. Malar J 12: 195.
Manyando C, Njunju EM, D'Alessandro U, Van Geertruyden JP, 2013. Safety and efficacy of co-trimoxazole for treatment and prevention of Plasmodium falciparum malaria: a systematic review. PLoS ONE 8: e56916.
Holmes VA, Wallace JM, Gilmore WS, McFaul P, Alexander HD, 2003. Plasma levels of the immunomodulatory cytokine interleukin-10 during normal human pregnancy: a longitudinal study. Cytokine 21: 265–269.
Bostrom S, Ibitokou S, Oesterholt M, Schmiegelow C, Persson JO, Minja D, Lusingu J, Lemnge M, Fievet N, Deloron P, Luty AJ, Troye-Blomberg M, 2012. Biomarkers of Plasmodium falciparum infection during pregnancy in women living in northeastern Tanzania. PLoS ONE 7: e48763.
Wilson NO, Bythwood T, Solomon W, Jolly P, Yatich N, Jiang Y, Shuaib F, Adjei AA, Anderson W, Stiles JK, 2010. Elevated levels of IL-10 and G-CSF associated with asymptomatic malaria in pregnant women. Infect Dis Obstet Gynecol 2010: 317430.
Hygino J, Vieira MM, Kasahara TM, Xavier LF, Blanco B, Guillermo LV, Filho RG, Saramago CS, Lima-Silva AA, Oliveira AL, Guimaraes V, Andrade AF, Bento CA, 2012. The impact of pregnancy on the HIV-1-specific T cell function in infected pregnant women. Clin Immunol 145: 177–188.
Lind A, Brekke K, Pettersen FO, Mollnes TE, Troseid M, Kvale D, 2014. A parameter for IL-10 and TGF-ss mediated regulation of HIV-1 specific T cell activation provides novel information and relates to progression markers. PLoS ONE 9: e85604.
Weissman D, Poli G, Fauci AS, 1994. Interleukin 10 blocks HIV replication in macrophages by inhibiting the autocrine loop of tumor necrosis factor alpha and interleukin 6 induction of virus. AIDS Res Hum Retroviruses 10: 1199–1206.
Oliver BG, Elliott JH, Saphonn V, Vun MC, French MA, Price P, 2010. Interferon-gamma and IL-5 production correlate directly in HIV patients co-infected with Mycobacterium tuberculosis with or without immune restoration disease. AIDS Res Hum Retroviruses 26: 1287–1289.
Gasser O, Brander C, Wolbers M, Brown NV, Rauch A, Gunthard HF, Battegay M, Hess C, 2013. Expansion of interferon-gamma-secreting HIV-specific T cells during successful antiretroviral therapy. HIV Med 14: 241–246.
Faye A, Pornprasert S, Mary JY, Dolcini G, Derrien M, Barre-Sinoussi F, Chaouat G, Menu E, 2007. Characterization of the main placental cytokine profiles from HIV-1-infected pregnant women treated with anti-retroviral drugs in France. Clin Exp Immunol 149: 430–439.
Ned RM, Moore JM, Chaisavaneeyakorn S, Udhayakumar V, 2005. Modulation of immune responses during HIV-malaria co-infection in pregnancy. Trends Parasitol 21: 284–291.
Chaisavaneeyakorn S, Moore JM, Otieno J, Chaiyaroj SC, Perkins DJ, Shi YP, Nahlen BL, Lal AA, Udhayakumar V, 2002. Immunity to placental malaria. III. Impairment of interleukin(IL)-12, not IL-18, and interferon-inducible protein-10 responses in the placental intervillous blood of human immunodeficiency virus/malaria-coinfected women. J Infect Dis 185: 127–131.
Moore JM, Ayisi J, Nahlen BL, Misore A, Lal AA, Udhayakumar V, 2000. Immunity to placental malaria. II. Placental antigen-specific cytokine responses are impaired in human immunodeficiency virus-infected women. J Infect Dis 182: 960–964.
Derrien M, Faye A, Dolcini G, Chaouat G, Barre-Sinoussi F, Menu E, 2005. Impact of the placental cytokine-chemokine balance on regulation of cell-cell contact-induced human immunodeficiency virus type 1 translocation across a trophoblastic barrier in vitro. J Virol 79: 12304–12310.
Xiao L, Owen SM, Rudolph DL, Lal RB, Lal AA, 1998. Plasmodium falciparum antigen-induced human immunodeficiency virus type 1 replication is mediated through induction of tumor necrosis factor- alpha. J Infect Dis 177: 437–445.
Montaner LJ, Griffin P, Gordon S, 1994. Interleukin-10 inhibits initial reverse transcription of human immunodeficiency virus type 1 and mediates a virostatic latent state in primary blood-derived human macrophages in vitro. J Gen Virol 75: 3393–3400.
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We investigated the circulating plasma levels of Th1- (Interleukin-2 [IL-2], tumor necrosis factor-α [TNF-α], interferon-gamma [IFN-γ]) and Th2-type (IL-4, IL-5, IL-10) cytokines in human immunodeficiency virus (HIV)-infected pregnant women living in a malaria-endemic area. We analyzed samples from 200 pregnant women included in the prevention of pregnancy-associated malaria in HIV-infected women: cotrimoxazole prophylaxis versus mefloquine (PACOME) clinical trial who were followed until delivery. Cytokine concentrations were measured by flow cytometry-based multiplex bead array. Significantly elevated levels of IL-10 and lower levels of TNF-α were observed at delivery compared with inclusion (P = 0.005). At inclusion, the presence of circulating IFN-γ, a higher CD4+ T cell count and having initiated intermittent preventive treatment of malaria with sulfadoxine pyrimethamine (SP-IPTp) were all associated with a lower likelihood of Plasmodium falciparum infection. At delivery, the inverse relationship between the presence of infection and circulating IFN-γ persisted, although there was a positive association between the likelihood of infection and the presence of circulating TNF-α. Initiation of antiretroviral therapy was associated with elevated IL-5 production. Consistent with our own and others' observations in HIV seronegative subjects, this study shows circulating IL-10 to be a marker of infection with P. falciparum during pregnancy even in HIV-infected women, although plasma IFN-γ may be a marker of anti-malarial protection in such women.
Financial support: The PACOME trial received funding from SIDACTION (research grant no. AI19-3-01528).
Disclosure: The funding sources had no involvement in the design, collection, analysis, and interpretation of data, writing of the manuscript or decision to publish.
Authors' addresses: Samad A. Ibitokou, Centre d'étude et de Recherche sur le Paludisme Associé à la Grossesse et à l'enfance (CERPAGE), Faculté des Sciences de la Santé, Université d'Abomey-Calavi, Benin, E-mail: ibitokou_samad@yahoo.fr (current address: University of Texas Medical Branch, Department of Internal Medicine, Division of Infectious Disease, Galveston, TX). Lise Denoeud-Ndam, Michel Cot, Adrian J.F. Luty, and Nicaise Tuikue Ndam, Institut de Recherche pour le Développement, UMR 216, Mère et enfant face aux Infections Tropicales, Paris, France, E-mails: lisedenoeud@yahoo.fr, michel.cot@ird.fr, adrian.luty@ird.fr, and nicaise.ndam@ird.fr. Sèm Ezinmegnon, Rodolphe Ladékpo, and Achille Massougbodji, Centre d'étude et de Recherche sur le Paludisme Associé à la Grossesse et à l'enfance (CERPAGE), Faculté des Sciences de la Santé, Université d'Abomey-Calavi, Benin, E-mails: e25sem@yahoo.fr, ladekpo@yahoo.fr, and massougbodjiachille@yahoo.fr. Djimon-Marcel Zannou, Faculté des Sciences de la Santé, Université d'Abomey-Calavi, Benin, E-mail: djmzannou@yahoo.fr. Pierre-Marie Girard, Service des Maladies Infectieuses et Tropicales, Hôpital Saint-Antoine, Paris, France, E-mail: pierre-marie.girard@sat.aphp.fr.
Fievet N, Moussa M, Tami G, Maubert B, Cot M, Deloron P, Chaouat G, 2001. Plasmodium falciparum induces a Th1/Th2 disequilibrium, favoring the Th1-type pathway, in the human placenta. J Infect Dis 183: 1530–1534.
Alemu A, Shiferaw Y, Addis Z, Mathewos B, Birhan W, 2013. Effect of malaria on HIV/AIDS transmission and progression. Parasites & Vectors 6: 18.
Li XX, Zhou XN, 2013. Co-infection of tuberculosis and parasitic diseases in humans: a systematic review. Parasites & Vectors 6: 79.
ter Kuile FO, Parise ME, Verhoeff FH, Udhayakumar V, Newman RD, van Eijk AM, Rogerson SJ, Steketee RW, 2004. The burden of co-infection with human immunodeficiency virus type 1 and malaria in pregnant women in sub-Saharan Africa. Am J Trop Med Hyg 71 (Suppl): 41–54.
Briand V, Badaut C, Cot M, 2009. Placental malaria, maternal HIV infection and infant morbidity. Ann Trop Paediatr 29: 71–83.
Tkachuk AN, Moormann AM, Poore JA, Rochford RA, Chensue SW, Mwapasa V, Meshnick SR, 2001. Malaria enhances expression of CC chemokine receptor 5 on placental macrophages. J Infect Dis 183: 967–972.
van Eijk AM, Ayisi JG, ter Kuile FO, Misore AO, Otieno JA, Rosen DH, Kager PA, Steketee RW, Nahlen BL, 2003. HIV increases the risk of malaria in women of all gravidities in Kisumu, Kenya. AIDS 17: 595–603.
Steketee RW, Wirima JJ, Bloland PB, Chilima B, Mermin JH, Chitsulo L, Breman JG, 1996. Impairment of a pregnant womans acquired ability to limit Plasmodium falciparum by infection with human immunodeficiency virus type-1. Am J Trop Med Hyg 55 (Suppl S): 42–49.
Kfutwah A, Mary JY, Lemen B, Leke R, Rousset D, Barre-Sinoussi F, Nerrienet E, Menu E, Ayouba A, 2009. Plasmodium falciparum infection significantly impairs placental cytokine profile in HIV infected Cameroonian women. PLoS ONE 4: e8114.
Verhoeff FH, Brabin BJ, Hart CA, Chimsuku L, Kazembe P, Broadhead RL, 1999. Increased prevalence of malaria in HIV-infected pregnant women and its implications for malaria control. Trop Med Int Health 4: 5–12.
Kabyemela ER, Muehlenbachs A, Fried M, Kurtis JD, Mutabingwa TK, Duffy PE, 2008. Maternal peripheral blood level of IL-10 as a marker for inflammatory placental malaria. Malar J 7: 26.
Rogerson SJ, Pollina E, Getachew A, Tadesse E, Lema VM, Molyneux ME, 2003. Placental monocyte infiltrates in response to Plasmodium falciparum malaria infection and their association with adverse pregnancy outcomes. Am J Trop Med Hyg 68: 115–119.
Suguitan AL Jr, Leke RG, Fouda G, Zhou A, Thuita L, Metenou S, Fogako J, Megnekou R, Taylor DW, 2003. Changes in the levels of chemokines and cytokines in the placentas of women with Plasmodium falciparum malaria. J Infect Dis 188: 1074–1082.
Moore JM, Chaisavaneeyakorn S, Perkins DJ, Othoro C, Otieno J, Nahlen BL, Shi YP, Udhayakumar V, 2004. Hemozoin differentially regulates proinflammatory cytokine production in human immunodeficiency virus-seropositive and -seronegative women with placental malaria. Infect Immun 72: 7022–7029.
Denoeud-Ndam L, Zannou DM, Fourcade C, Taron-Brocard C, Porcher R, Atadokpede F, Komongui DG, Dossou-Gbete L, Afangnihoun A, Ndam NT, Girard PM, Cot M, 2014. Cotrimoxazole prophylaxis versus mefloquine intermittent preventive treatment to prevent malaria in HIV-infected pregnant women: two randomized controlled trials. J Acquir Immune Defic Syndr 65: 198–206.
Rozin A, Schapira D, Braun-Moscovici Y, Nahir AM, 2001. Cotrimoxazole treatment for rheumatoid arthritis. Semin Arthritis Rheum 31: 133–141.
Diallo A, Ndam NT, Moussiliou A, Dos Santos S, Ndonky A, Borderon M, Oliveau S, Lalou R, Le Hesran JY, 2012. Asymptomatic carriage of Plasmodium in urban Dakar: the risk of malaria should not be underestimated. PLoS ONE 7: e31100.
Taylor SM, Mayor A, Mombo-Ngoma G, Kenguele HM, Ouedraogo S, Ndam NT, Mkali H, Mwangoka G, Valecha N, Singh JP, Clark MA, Verweij JJ, Adegnika AA, Severini C, Menegon M, Macete E, Menendez C, Cistero P, Njie F, Affara M, Otieno K, Kariuki S, ter Kuile FO, Meshnick SR, 2014. A quality control program within a clinical trial Consortium for PCR protocols to detect Plasmodium species. J Clin Microbiol 52: 2144–2149.
Moussiliou A, Sissinto-Savi De Tove Y, Doritchamou J, Luty AJ, Massougbodji A, Alifrangis M, Deloron P, Tuikue Ndam N, 2013. High rates of parasite recrudescence following intermittent preventive treatment with sulphadoxine-pyrimethamine during pregnancy in Benin. Malar J 12: 195.
Manyando C, Njunju EM, D'Alessandro U, Van Geertruyden JP, 2013. Safety and efficacy of co-trimoxazole for treatment and prevention of Plasmodium falciparum malaria: a systematic review. PLoS ONE 8: e56916.
Holmes VA, Wallace JM, Gilmore WS, McFaul P, Alexander HD, 2003. Plasma levels of the immunomodulatory cytokine interleukin-10 during normal human pregnancy: a longitudinal study. Cytokine 21: 265–269.
Bostrom S, Ibitokou S, Oesterholt M, Schmiegelow C, Persson JO, Minja D, Lusingu J, Lemnge M, Fievet N, Deloron P, Luty AJ, Troye-Blomberg M, 2012. Biomarkers of Plasmodium falciparum infection during pregnancy in women living in northeastern Tanzania. PLoS ONE 7: e48763.
Wilson NO, Bythwood T, Solomon W, Jolly P, Yatich N, Jiang Y, Shuaib F, Adjei AA, Anderson W, Stiles JK, 2010. Elevated levels of IL-10 and G-CSF associated with asymptomatic malaria in pregnant women. Infect Dis Obstet Gynecol 2010: 317430.
Hygino J, Vieira MM, Kasahara TM, Xavier LF, Blanco B, Guillermo LV, Filho RG, Saramago CS, Lima-Silva AA, Oliveira AL, Guimaraes V, Andrade AF, Bento CA, 2012. The impact of pregnancy on the HIV-1-specific T cell function in infected pregnant women. Clin Immunol 145: 177–188.
Lind A, Brekke K, Pettersen FO, Mollnes TE, Troseid M, Kvale D, 2014. A parameter for IL-10 and TGF-ss mediated regulation of HIV-1 specific T cell activation provides novel information and relates to progression markers. PLoS ONE 9: e85604.
Weissman D, Poli G, Fauci AS, 1994. Interleukin 10 blocks HIV replication in macrophages by inhibiting the autocrine loop of tumor necrosis factor alpha and interleukin 6 induction of virus. AIDS Res Hum Retroviruses 10: 1199–1206.
Oliver BG, Elliott JH, Saphonn V, Vun MC, French MA, Price P, 2010. Interferon-gamma and IL-5 production correlate directly in HIV patients co-infected with Mycobacterium tuberculosis with or without immune restoration disease. AIDS Res Hum Retroviruses 26: 1287–1289.
Gasser O, Brander C, Wolbers M, Brown NV, Rauch A, Gunthard HF, Battegay M, Hess C, 2013. Expansion of interferon-gamma-secreting HIV-specific T cells during successful antiretroviral therapy. HIV Med 14: 241–246.
Faye A, Pornprasert S, Mary JY, Dolcini G, Derrien M, Barre-Sinoussi F, Chaouat G, Menu E, 2007. Characterization of the main placental cytokine profiles from HIV-1-infected pregnant women treated with anti-retroviral drugs in France. Clin Exp Immunol 149: 430–439.
Ned RM, Moore JM, Chaisavaneeyakorn S, Udhayakumar V, 2005. Modulation of immune responses during HIV-malaria co-infection in pregnancy. Trends Parasitol 21: 284–291.
Chaisavaneeyakorn S, Moore JM, Otieno J, Chaiyaroj SC, Perkins DJ, Shi YP, Nahlen BL, Lal AA, Udhayakumar V, 2002. Immunity to placental malaria. III. Impairment of interleukin(IL)-12, not IL-18, and interferon-inducible protein-10 responses in the placental intervillous blood of human immunodeficiency virus/malaria-coinfected women. J Infect Dis 185: 127–131.
Moore JM, Ayisi J, Nahlen BL, Misore A, Lal AA, Udhayakumar V, 2000. Immunity to placental malaria. II. Placental antigen-specific cytokine responses are impaired in human immunodeficiency virus-infected women. J Infect Dis 182: 960–964.
Derrien M, Faye A, Dolcini G, Chaouat G, Barre-Sinoussi F, Menu E, 2005. Impact of the placental cytokine-chemokine balance on regulation of cell-cell contact-induced human immunodeficiency virus type 1 translocation across a trophoblastic barrier in vitro. J Virol 79: 12304–12310.
Xiao L, Owen SM, Rudolph DL, Lal RB, Lal AA, 1998. Plasmodium falciparum antigen-induced human immunodeficiency virus type 1 replication is mediated through induction of tumor necrosis factor- alpha. J Infect Dis 177: 437–445.
Montaner LJ, Griffin P, Gordon S, 1994. Interleukin-10 inhibits initial reverse transcription of human immunodeficiency virus type 1 and mediates a virostatic latent state in primary blood-derived human macrophages in vitro. J Gen Virol 75: 3393–3400.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 30 | 30 | 10 |
Full Text Views | 321 | 89 | 0 |
PDF Downloads | 101 | 29 | 0 |