Changes in the Levels of Chemokines and Cytokines in the Placentas of Women with Plasmodium falciparum Malaria
Abstract
Plasmodium falciparum-infected erythrocytes often are sequestered in the placenta and stimulate the accumulation of maternal mononuclear cells. In this study, the role that chemokines and cytokines play in mediating the inflammatory response was investigated. Placental parasites elicited a statistically significant increase in the levels of interferon (IFN)-gamma, tumor necrosis factor (TNF)-alpha, and interleukin (IL)-10, in plasma collected from the intervillous space. Explants of fetal tissue from malaria-positive placentas also secreted significantly enhanced amounts of IFN-gamma. Culture supernatant of maternal intervillous leukocytes obtained from infected placentas contained significantly higher levels of TNF-alpha, IL-10, monocyte chemotactic protein-1, macrophage inflammatory protein (MIP)-1alpha, MIP-1beta, and IFN-gamma inducible protein-10 than did cultures of white blood cells obtained from uninfected placentas. Taken together, these results show that both fetal and maternal cells secrete inflammatory and immunoregulatory cytokines in response to P. falciparum and suggest that beta-chemokines produced by maternal cells contribute to the accumulation of macrophages in the intervillous space.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Activation of immune cells with upregulation of markers such as CD4+, CD8+ and CD68+ can be observed.
“In addition, activation of immune cells with upregulation of markers such as CD4 + , CD8 + and CD68 + can be observed [121, 123, 124].”
From Current update on malaria in pregnancy: a systematic review (2025) · cites this paper as [123]
PM is associated with inflammatory immune responses, with increased levels of soluble mediators like TNF-α, TNF receptor I, TNF receptor II and IL-10 in peripheral blood.
“PM is associated with inflammatory immune responses [75–79], with increased levels of soluble mediators like TNF-α, TNF receptor I, TNF receptor II and IL-10 in peripheral blood [80,81].”
From Diagnosing malaria in pregnancy: An update (2012) · cites this paper as [76]
Cites
No adjustments are needed for multiple comparisons.
Rothman, K. J. (1990) · Epidemiology · doi:10.1097/00001648-199001000-00010 · Cited by 5,965 · see citing works
Wegmann, T. G., Lin, H., Guilbert, L., & Mosmann, T. R. (1993) · Immunology Today · doi:10.1016/0167-5699(93)90235-d · Cited by 2,852 · see citing works
Baggiolini, M., Dewald, B., & Moser, B. (1997) · Annual Review of Immunology · doi:10.1146/annurev.immunol.15.1.675 · Cited by 2,193 · see citing works
Adherence of <i>Plasmodium falciparum</i> to Chondroitin Sulfate A in the Human Placenta
Fried, M., & Duffy, P. E. (1996) · Science · doi:10.1126/science.272.5267.1502 · Cited by 1,108 · see citing works
The burden of malaria in pregnancy in malaria-endemic areas
Steketee, R., Nahlen, B., Parise, M., & Menendez, C. (2001) · The American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2001.64.28 · Cited by 1,063 · see citing works
Th 1-type immunity is incompatible with successful pregnancy
Raghupathy, R. (1997) · Immunology Today · doi:10.1016/s0167-5699(97)01127-4 · Cited by 994 · see citing works
The Impact of Placental Malaria on Gestational Age and Birth Weight
Menendez, C., Ordi, J., Ismail, M. R., Ventura, P. J., Aponte, J. J., Kahigwa, E., Font, F., & Alonso, P. L. (2000) · The Journal of Infectious Diseases · doi:10.1086/315449 · Cited by 467 · see citing works
The Role of T H 1 and T H 2 Cells in a Rodent Malaria Infection
Taylor-Robinson, A. W., PHILLIPS, R. S., Severn, A., Moncada, S., & Liew, F. Y. (1993) · Science · doi:10.1126/science.8100366 · Cited by 346 · see citing works
Chemokines: signal lamps for trafficking of T and B cells for development and effector function
Kim, C. H., & Broxmeyer, H. E. (1999) · Journal of Leukocyte Biology · doi:10.1002/jlb.65.1.6 · Cited by 338 · see citing works
Placental pathology in malaria: A histological, immunohistochemical, and quantitative study
Ismail, M. R., Ordi, J., Menendez, C., Ventura, P. J., Aponte, J. J., Kahigwa, E., Hirt, R., Cardesa, A., & Alonso, P. L. (2000) · Human Pathology · doi:10.1016/s0046-8177(00)80203-8 · Cited by 328 · see citing works
Fried, M., Muga, R., Misore, A. O., & Duffy, P. E. (1998) · PubMed · Cited by 321 · see citing works
Adhesion of Plasmodium falciparum-infected erythrocytes to hyaluronic acid in placental malaria
Beeson, J. G., Rogerson, S. J., Cooke, B. M., Reeder, J. C., Chai, W., Lawson, A. M., Molyneux, M. E., & Brown, G. V. (2000) · Nature Medicine · doi:10.1038/71582 · Cited by 310 · see citing works
Steketee, R. W., Hightower, A. W., Wirima, J. J., Breman, J. G., Heymann, D. L., & Slutsker, L. (1996) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1996.55.33 · Cited by 303 · see citing works
Massive chronic intervillositis of the placenta associated with malaria infection
Ordi, J., Ismail, M. R., Ventura, P. J., Kahigwa, E., Hirt, R., Cardesa, A., Alonso, P. L., & Menendez, C. (1998) · The American Journal of Surgical Pathology · doi:10.1097/00000478-199808000-00011 · Cited by 265 · see citing works
Fried, M., Muga, R. O., Misore, A. O., & Duffy, P. E. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.160.5.2523 · Cited by 262 · see citing works
Placental pathologic changes in malaria. A histologic and ultrastructural study.
Walter, P. R., GARIN, Y. J. F., & Blot, P. (1982) · PubMed · Cited by 253 · see citing works
Immune Regulation during Pregnancy and Host–Pathogen Interactions in Infectious Abortion
Entrican, G. (2002) · Journal of Comparative Pathology · doi:10.1053/jcpa.2001.0539 · Cited by 225 · see citing works
Moormann, A. M., Sullivan, A. D., Rochford, R. A., Chensue, S. W., Bock, P. J., Nyirenda, T. E., & Meshnick, S. R. (1999) · The Journal of Infectious Diseases · doi:10.1086/315135 · Cited by 208 · see citing works
Maintaining the Immunological Balance in Parasitic Infections: A Role for TGF-β?
Omer, F. M., Kurtzhals, J. A. L., & Riley, E. M. (2000) · Parasitology Today · doi:10.1016/s0169-4758(99)01562-8 · Cited by 200 · see citing works
Sherry, B. A., Alava, G., Tracey, K. J., Martiney, J. A., Cerami, A., & Slater, A. F. G. (1995) · PubMed · Cited by 158 · see citing works
Jokhi, P., King, A., & Loke, Y. W. (1997) · Cytokine · doi:10.1006/cyto.1996.0146 · Cited by 143 · see citing works
Cytokine secretion by human fetal membranes, decidua and placenta at term
Denison, F. C., KELLY, R. W., Calder, A. A., & Riley, S. C. (1998) · Human Reproduction · doi:10.1093/humrep/13.12.3560 · Cited by 140 · see citing works
Malaria Infection during Pregnancy: Intrauterine Growth Retardation and Preterm Delivery in Malawi
Sullivan, A. D., Nyirenda, T. E., Cullinan, T. R., Taylor, T. E., Harlow, S. D., James, S. A., & Meshnick, S. (1999) · The Journal of Infectious Diseases · doi:10.1086/314752 · Cited by 136 · see citing works
Rockett, K. A., Awburn, M. M., Aggarwal, B. B., Cowden, W. B., & Clark, I. A. (1992) · Infection and Immunity · doi:10.1128/iai.60.9.3725-3730.1992 · Cited by 126 · see citing works
Placental malaria. II. A semi‐quantitative investigation of the pathological features
Bulmer, J. N., Rasheed, F. N., Morrison, L., FRANCIS, N., & Greenwood, B. M. (1993) · Histopathology · doi:10.1111/j.1365-2559.1993.tb00111.x · Cited by 115 · see citing works
Fiévet, N., Moussa, M., Tami, G., Maubert, B., Cot, M., Deloron, P., & Chaouat, G. (2001) · The Journal of Infectious Diseases · doi:10.1086/320201 · Cited by 102 · see citing works
Chemokines and innate immunity.
Matsukawa, A., Hogaboam, C. M., Lukacs, N. W., & Kunkel, S. L. (2000) · PubMed · Cited by 95 · see citing works
Ordï, J., Menéndez, C., Ismail, M. R., Ventura, P. J., Palacı́n, A., Kahigwa, E., Fábrega, B. F., Cardesa, A., & Alonso, P. L. (2001) · The Journal of Infectious Diseases · doi:10.1086/319295 · Cited by 92 · see citing works
Troye‐Blomberg, M., Andersson, G., Stoczkowska, M., Shabo, R., Romero, P., Patarroyo, M. E., Wigzell, H., & Perlmann, P. (1985) · The Journal of Immunology · doi:10.4049/jimmunol.135.5.3498 · Cited by 90 · see citing works
Endogenous Interleukin-10 Modulates Proinflammatory Response in Plasmodium falciparum Malaria
Ho, M., Schollaardt, T., Snape, S., Looareesuwan, S., Suntharasamai, P., & White, N. J. (1998) · The Journal of Infectious Diseases · doi:10.1086/515640 · Cited by 88 · see citing works
First trimester human trophoblast expresses both interferon-γ and interferon-γ-receptor
Paulesu, L. R., Romagnoli, R., Cintorino, M., Ricci, M. G., & Garotta, G. (1994) · Journal of Reproductive Immunology · doi:10.1016/0165-0378(94)90013-2 · Cited by 74 · see citing works
Enhanced Plasmodium falciparum merozoite phagocytosis by monocytes from immune individuals
Khusmith, S., Druilhe, P., & Gentilini, M. (1982) · Infection and Immunity · doi:10.1128/iai.35.3.874-879.1982 · Cited by 64 · see citing works
Burgmann, H., Hollenstein, U., Wenisch, C., Thalhammer, F., Looareesuwan, S., & Graninger, W. B. (1995) · Clinical Immunology and Immunopathology · doi:10.1006/clin.1995.1084 · Cited by 60 · see citing works
Galbraith, R. M., Faulk, W. P., Galbraith, G. M. P., Holbrook, T. W., & Bray, R. S. (1980) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/0035-9203(80)90011-5 · Cited by 59 · see citing works
Leopardi, O., Naughten, W., Salvia, L., Colecchia, M., Matteelli, A., Zucchi, A., Shein, A., Muchi, J. A., Carosi, G., & Ghione, M. (1996) · Pathology - Research and Practice · doi:10.1016/s0344-0338(96)80068-9 · Cited by 57 · see citing works
Chaisavaneeyakorn, S., Moore, J. M., Otieno, J. A., Chaiyaroj, S. C., Perkins, D. J., Shi, Y. P., Nahlen, B. L., Lal, A. A., & Udhayakumar, V. (2002) · The Journal of Infectious Diseases · doi:10.1086/338013 · Cited by 55 · see citing works
Tumor Necrosis Factor in Malaria-Induced Abortion
Clark, I. A., & Chaudhri, G. (1988) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1988.39.246 · Cited by 53 · see citing works
Moussa, M., Roques, P., Fiévet, N., Menu, E., Maldonado-Estrada, J. G., Brunerie, J., Frydman, R., Fritel, X., Herve, F., & Chaouat, G. (2001) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.2001.01629.x · Cited by 48 · see citing works
Chemokines in host–protozoan-parasite interactions
Brenier‐Pinchart, M., Pelloux, H., Guergour, D., & Ambroise-Thomas, P. (2001) · Trends in Parasitology · doi:10.1016/s1471-4922(01)01902-x · Cited by 45 · see citing works
Dudley, D. J., Edwin, S. S., Dangerfield, A., Waggoner, J. V., & Mitchell, M. D. (1996) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1996.tb00175.x · Cited by 32 · see citing works
Expression of β Chemokines in Explants and Trophoblasts from Early and Term Human Placentae
Moussa, M., Mognetti, B., Dubanchet, S., Menu, E., Chaouat, G., Menu, E., Barré‐Sinoussi, F., Mognetti, B., Roques, P., & Dormont, D. (2001) · American Journal of Reproductive Immunology · doi:10.1034/j.1600-0897.2001.d01-17.x · Cited by 27 · see citing works
Malarial placental infection and low birth weight babies.
Kaushik, A., Sharma, V. K., Sadhna, Kumar, R., & Mitra, R. (1992) · PubMed · Cited by 14 · see citing works
Papadogiannakis, N., Johnsen, S.-A., & Olding, L. B. (1985) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1985.tb00287.x · Cited by 12 · see citing works
Flagged first, then by citations
1 of the 44 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Malaria in pregnancy: pathogenesis and immunity
Rogerson, S. J., Hviid, L., Duffy, P. E., Leke, R. F., & Taylor, D. W. (2007) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(07)70022-1 · Cited by 628 · see citing works
Self-citationter Kuile, F. O., Parise, M. E., Verhoeff, F. H., Udhayakumar, V., Newman, R. D., van Eijk, A. M., Rogerson, S. J., & Steketee, R. W. (2004) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2004.71.41 · Cited by 364 · see citing works
Human malarial disease: a consequence of inflammatory cytokine release
Clark, I. A., Budd, A. C., Alleva, L. M., & Cowden, W. B. (2006) · Malaria Journal · doi:10.1186/1475-2875-5-85 · Cited by 318 · see citing works
Placental Responses to Changes in the Maternal Environment Determine Fetal Growth
Dimasuay, K. G., Boeuf, P., Powell, T. L., & Jansson, T. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00012 · Cited by 258 · see citing works
Cerebrospinal fluid and serum biomarkers of cerebral malaria mortality in Ghanaian children
Armah, H. B., Wilson, N. O., Sarfo, B. Y., Powell, M. D., Bond, V. C., Anderson, W. A., Adjei, A. A., Gyasi, R. K., Tettey, Y., Wiredu, E. K., et al. (2007) · Malaria Journal · doi:10.1186/1475-2875-6-147 · Cited by 239 · see citing works
Malaria in pregnancy: small babies, big problem
Umbers, A. J., Aitken, E. H., & Rogerson, S. J. (2011) · Trends in Parasitology · doi:10.1016/j.pt.2011.01.007 · Cited by 200 · see citing works
Fried, M., & Duffy, P. E. (2017) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a025551 · Cited by 202 · see citing works
Dimasuay, K. G., Aitken, E. H., Rosario, F. J., Njie, M., Glazier, J. D., Rogerson, S. J., Fowkes, F. J. I., Beeson, J. G., Powell, T. L., Jansson, T., et al. (2017) · BMC Medicine · doi:10.1186/s12916-016-0759-3 · Cited by 190 · see citing works
Plasma IP-10, apoptotic and angiogenic factors associated with fatal cerebral malaria in India
Jain, V., Armah, H. B., Tongren, J. E., Ned, R. M., Wilson, N. O., Crawford, S. B., Joel, P. K., Singh, M. P., Nagpal, A. C., Dash, A., et al. (2008) · Malaria Journal · doi:10.1186/1475-2875-7-83 · Cited by 177 · see citing works
Chang, C. C., Crane, M., Zhou, J., Mina, M., Post, J. J., Cameron, B., Lloyd, A. R., Jaworowski, A., French, M. A., & Lewin, S. R. (2013) · Immunological Reviews · doi:10.1111/imr.12063 · Cited by 169 · see citing works
WALKER-ABBEY, A., DJOKAM, R. R. T., ENO, A., LEKE, R. F. G., TITANJI, V. P. K., FOGAKO, J., SAMA, G., THUITA, L. H., BEARDSLEE, E., SNOUNOU, G., et al. (2005) · The American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2005.72.229 · Cited by 132 · see citing works
Self-citationGenomewide Analysis of the Host Response to Malaria in Kenyan Children
Griffiths, M., Shafi, M. J., Popper, S. J., Hemingway, C. A., Kortok, M., Wathen, A., Rockett, K. A., Mott, R., Levin, M., Newton, C. R. J. C., et al. (2005) · The Journal of Infectious Diseases · doi:10.1086/429297 · Cited by 130 · see citing works
Neres, R., Marinho, C. R. F., Gonçalves, L. A., Catarino, M. B., & Penha‐Gonçalves, C. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001608 · Cited by 126 · see citing works
Understanding the role of inflammatory cytokines in malaria and related diseases.
Clark, I., Alleva, L., Budd, A. C., & Cowden, W. (2008) · Travel Medicine and Infectious Disease · doi:10.1016/j.tmaid.2007.07.002 · Cited by 105 · see citing works
Elevated Levels of IL-10 and G-CSF Associated with Asymptomatic Malaria in Pregnant Women
Wilson, N. O., Bythwood, T., Solomon, W., Jolly, P. E., Yatich, N., Jiang, Y., Shuaib, F. M. B., Adjei, A. A., Anderson, W. A., & Stiles, J. K. (2010) · Infectious Diseases in Obstetrics and Gynecology · doi:10.1155/2010/317430 · Cited by 105 · see citing works
Differential Regulation of β-Chemokines in Children with Plasmodium falciparum Malaria
Ochiel, D. O., Awandare, G. A., KELLER, C. C., Hittner, J. B., Kremsner, P. G., Weinberg, J. B., & Perkins, D. J. (2005) · Infection and Immunity · doi:10.1128/iai.73.7.4190-4197.2005 · Cited by 104 · see citing works
The Structure of a Chondroitin Sulfate-binding Domain Important in Placental Malaria
Higgins, M. K. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.c800086200 · Cited by 99 · see citing works
The Immunology and Pathogenesis of Malaria During Pregnancy
Beeson, J. G., & Duffy, P. E. (2005) · Current topics in microbiology and immunology · doi:10.1007/3-540-29967-x_6 · Cited by 94 · see citing works
Duffy, P. E., & Fried, M. (2005) · Springer eBooks · doi:10.1007/3-540-29088-5_7 · Cited by 86 · see citing works
The role of chemokines in severe malaria: more than meets the eye
Ioannidis, L. J., Nie, C. Q., & Hansen, D. S. (2013) · Parasitology · doi:10.1017/s0031182013001984 · Cited by 84 · see citing works
Muehlenbachs, A., Fried, M., Lachowitzer, J., Mutabingwa, T. K., & Duffy, P. E. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.1.557 · Cited by 81 · see citing works
Conroy, A., Serghides, L., Finney, C., Owino, S. O., Kumar, S., Gowda, D. C., Liles, W. C., Moore, J. M., & Kain, K. C. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004953 · Cited by 81 · see citing works
Diagnosing malaria in pregnancy: An update
Fried, M., Muehlenbachs, A., & Duffy, P. E. (2012) · Expert Review of Anti-infective Therapy · doi:10.1586/eri.12.98 · Cited by 80 · see citing works
Placental Histopathological Changes Associated with Plasmodium vivax Infection during Pregnancy
Souza, R. M., Ataíde, R., Dombrowski, J. G., Ippólito, V., Aitken, E. H., Valle, S. N., Álvarez, J. M., Epiphânio, S., & Marinho, C. R. F. (2013) · PLoS Neglected Tropical Diseases · doi:10.1371/journal.pntd.0002071 · Cited by 79 · see citing works
Maternal peripheral blood level of IL-10 as a marker for inflammatory placental malaria
Kabyemela, E. R., Muehlenbachs, A., Fried, M., Kurtis, J. D., Mutabingwa, T. K., & Duffy, P. E. (2008) · Malaria Journal · doi:10.1186/1475-2875-7-26 · Cited by 79 · see citing works
Malaria in Pregnancy: From Placental Infection to Its Abnormal Development and Damage
Chua, C. L. L., Khoo, S. K. M., Ong, J. L. E., Ramireddi, G. K., Yeo, T. W., & Teo, A. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.777343 · Cited by 90 · see citing works
Innate immunity to malaria—The role of monocytes
Dobbs, K. R., Crabtree, J., & Dent, A. E. (2019) · Immunological Reviews · doi:10.1111/imr.12830 · Cited by 79 · see citing works
Dysregulation of Angiopoietins Is Associated with Placental Malaria and Low Birth Weight
Silver, K., Zhong, K., Leke, R. G. F., Taylor, D. W., & Kain, K. C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009481 · Cited by 76 · see citing works
Self-citationFried, M., Kurtis, J. D., Swihart, B., Pond‐Tor, S., Barry, A., Sidibé, Y., Gaoussou, S., Traoré, M., Keita, S., Mahamar, A., et al. (2017) · Clinical Infectious Diseases · doi:10.1093/cid/cix623 · Cited by 72 · see citing works
MicroReview: The role of Plasmodium falciparum var genes in malaria in pregnancy
Rowe, J. A., & Kyes, S. A. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04256.x · Cited by 72 · see citing works
Modulation of immune responses during HIV–malaria co-infection in pregnancy
Ned, R. M., Moore, J. M., Chaisavaneeyakorn, S., & Udhayakumar, V. (2005) · Trends in Parasitology · doi:10.1016/j.pt.2005.04.010 · Cited by 69 · see citing works
Broen, K., Brustoski, K., Engelmann, I., & Luty, A. J. F. (2006) · Molecular and Biochemical Parasitology · doi:10.1016/j.molbiopara.2006.10.001 · Cited by 64 · see citing works
Collantes-Fernández, E., Arrighi, R. B. G., Álvarez‐García, G., Weidner, J. M., Regidor‐Cerrillo, J., Boothroyd, J. C., Ortega‐Mora, L. M., & Barragán, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032123 · Cited by 61 · see citing works
Khunrae, P., Philip, J. M. D., Bull, D. R., & Higgins, M. K. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.08.027 · Cited by 61 · see citing works
Abdallah, M. W., Larsen, N., Grove, J., Bonefeld‐Jørgensen, E. C., Nørgaard‐Pedersen, B., HOUGAARD, D. M., & Mortensen, E. L. (2012) · Cytokine · doi:10.1016/j.cyto.2012.11.015 · Cited by 61 · see citing works
Flanagan, K. L., Halliday, A., Burl, S., Landgraf, K., Jagne, Y. J., Noho‐Konteh, F., Townend, J., Miles, D. J. C., van der Sande, M. A. B., Whittle, H. C., et al. (2009) · European Journal of Immunology · doi:10.1002/eji.200939638 · Cited by 53 · see citing works
Bir, N., Yazdani, S. S., Avril, M., Layez, C., Gysin, J., & Chitnis, C. E. (2006) · Infection and Immunity · doi:10.1128/iai.00481-06 · Cited by 49 · see citing works
Magistrado, P. A., Minja, D., Doritchamou, J., Tuikue Ndam, N., John, D., Schmiegelow, C., Massougbodji, A., Dahlbäck, M., Ditlev, S. B., Pinto, V. V., et al. (2011) · Vaccine · doi:10.1016/j.vaccine.2010.10.080 · Cited by 49 · see citing works
Molecular interactions in the placenta during malaria infection
Mens, P. F., Bojtor, E. C., & Schallig, H. D. F. H. (2010) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2010.05.013 · Cited by 48 · see citing works
Diouf, I., Fiévet, N., Doucouré, S., Ngom, M., Andrieu, M., Mathieu, J.-F., Gaye, A., Thiaw, O. T., & Deloron, P. (2006) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2006.10.001 · Cited by 49 · see citing works
Current update on malaria in pregnancy: a systematic review
Minwuyelet, A., Yewhalaw, D., Siferih, M., & Atenafu, G. (2025) · Tropical Diseases, Travel Medicine and Vaccines · doi:10.1186/s40794-025-00248-1 · Cited by 49 · see citing works
Adégnika, A. A., Köhler, C., Agnandji, S. T., Chai, S. K., Labuda, L. A., Breitling, L. P., Schonkeren, D., Weerdenburg, E. M., Issifou, S., Luty, A. J. F., et al. (2008) · The Journal of Infectious Diseases · doi:10.1086/591057 · Cited by 47 · see citing works
Thévenon, A. D., Zhou, J. A., Megnekou, R., Ako, S., Leke, R. G. F., & Taylor, D. W. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1002293 · Cited by 44 · see citing works
Self-citationde Moraes, L. V., Tadokoro, C. E., Gómez-Conde, I., Olivieri, D. N., & Penha‐Gonçalves, C. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003154 · Cited by 44 · see citing works
Congenital Transmission of Apicomplexan Parasites: A Review
Rojas-Pirela, M., Medina, L., Rojas, M. V., Liempi, A. I., Castillo, C., Pérez-Pérez, E., Guerrero-Muñoz, J., Araneda, S., & Kemmerling, U. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.751648 · Cited by 44 · see citing works
New approaches to pathogenesis of malaria in pregnancy
Rogerson, S. J., & Boeuf, P. (2007) · Parasitology · doi:10.1017/s003118200700011x · Cited by 43 · see citing works
Chêne, A., Briand, V., Ibitokou, S. A., Dechavanne, S., Massougbodji, A., Deloron, P., Luty, A. J. F., Gamain, B., & Fiévet, N. (2014) · Infection and Immunity · doi:10.1128/iai.01922-14 · Cited by 42 · see citing works
Toxoplasma gondii regulates ICAM‐1 mediated monocyte adhesion to trophoblasts
Pfaff, A. W., Georges, S., Abou‐Bacar, A., Letscher‐Bru, V., Klein, J., Mousli, M., & Candolfi, E. (2005) · Immunology and Cell Biology · doi:10.1111/j.1440-1711.2005.01356.x · Cited by 43 · see citing works
Boström, S., Ibitokou, S. A., Oesterholt, M., Schmiegelow, C., Persson, J., Minja, D. T. R., Lusingu, J., Lemnge, M., Fiévet, N., Deloron, P., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048763 · Cited by 41 · see citing works
IFN-gamma and TNF associated with severe falciparum malaria infection in Saudi pregnant women
Nasr, A., Allam, G. A., Hamid, O., & Al-Ghamdi, A. (2014) · Malaria Journal · doi:10.1186/1475-2875-13-314 · Cited by 42 · see citing works
Malaria in Pregnancy and the Newborn
Rogerson, S. J. (2009) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-0981-7_12 · Cited by 40 · see citing works
Impact of Pregnancy-Associated Malaria on Infant Malaria Infection in Southern Benin
Borgella, S., Fiévet, N., Huynh, B.-T., Ibitokou, S. A., Hounguevou, G., Affedjou, J., Sagbo, J.-C., Houngbégnon, P., Guézo-Mévo, B., Massougbodji, A., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0080624 · Cited by 39 · see citing works
Megnekou, R., Djontu, J. C., Bigoga, J. D., Medou, F. M., Tenou, S., & Lissom, A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0134633 · Cited by 38 · see citing works
Self-citationFetal responses during placental malaria modify the risk of low birth weight
Kabyemela, E. R., Fried, M., Kurtis, J. D., Mutabingwa, T. K., & Duffy, P. E. (2008) · Infection and Immunity · doi:10.1128/iai.00964-07 · Cited by 37 · see citing works
Kidima, W. B. (2015) · BioMed Research International · doi:10.1155/2015/451735 · Cited by 37 · see citing works
Muehlenbachs, A., Nabasumba, C., McGready, R., Turyakira, E., Tumwebaze, B., Dhorda, M., Nyehangane, D., Nalusaji, A., Nosten, F., Guerin, P. J., et al. (2012) · Malaria Journal · doi:10.1186/1475-2875-11-150 · Cited by 35 · see citing works
Ndeserua, R., Juma, A., Mosha, D., & Chilongola, J. O. (2015) · African Health Sciences · doi:10.4314/ahs.v15i3.15 · Cited by 33 · see citing works
Kumar, S. B., Exten, C. L., Milner, D. A., Ramirez, N. C., Ackerman, W. E., Mwapasa, V., Turner, A. N., & Kwiek, J. J. (2012) · AIDS · doi:10.1097/qad.0b013e3283519b00 · Cited by 35 · see citing works
CXC ligand 9 response to malaria during pregnancy is associated with low-birth-weight deliveries
Dong, S., Kurtis, J. D., Pond-Tor, S., Kabyemela, E., Duffy, P. E., & Fried, M. (2012) · Infection and Immunity · doi:10.1128/iai.00220-12 · Cited by 32 · see citing works
Bayoumi, N. K., Bakhet, K. H., Mohmmed, A. A., Eltom, A., Elbashir, M. I., Mavoungou, E., & Adam, I. (2008) · Journal of Tropical Pediatrics · doi:10.1093/tropej/fmn062 · Cited by 32 · see citing works
Circulating Monocytes, Tissue Macrophages, and Malaria
Özarslan, N., Robinson, J. F., & Gaw, S. L. (2019) · Journal of Tropical Medicine · doi:10.1155/2019/3720838 · Cited by 32 · see citing works
Fucosylated Chondroitin Sulfate Inhibits Plasmodium falciparum Cytoadhesion and Merozoite Invasion
Bastos, M. F., Albrecht, L., Kozlowski, E. O., Lopes, S. C. P., Blanco, Y. C., Carlos, B. C., Castiñeiras, C., Vicente, C. P., WERNECK, C. C., Wunderlich, G., et al. (2014) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00686-13 · Cited by 31 · see citing works
Tomlinson, A., Semblat, J., Gamain, B., & Chêne, A. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.624126 · Cited by 29 · see citing works
Cytokine signatures of Plasmodium vivax infection during pregnancy and delivery outcomes
Dobaño, C., Bardají, A., Arévalo-Herrera, M., Martínez-Espinosa, F. E., Bôtto-Menezes, C., Padilla, N., Menegon, M., Kochar, S., Kochar, S. K., Unger, H., et al. (2020) · PLOS Neglected Tropical Diseases · doi:10.1371/journal.pntd.0008155 · Cited by 28 · see citing works
Djontu, J. C., Siewe, S. S., Edene, Y. D. M., Nana, B. C., Foko, E. V. C., Bigoga, J. D., Leke, R. F. G., & Megnekou, R. (2016) · Malaria Journal · doi:10.1186/s12936-016-1611-0 · Cited by 27 · see citing works
Self-citationMolecular Principles of Intrauterine Growth Restriction in Plasmodium Falciparum Infection
Seitz, J., Prieto, D. M. M., Fávaro, R. R., Schneider, H., & Markert, U. R. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00098 · Cited by 29 · see citing works
Maestre, A., & Carmona‐Fonseca, J. (2014) · The Journal of Infection in Developing Countries · doi:10.3855/jidc.3777 · Cited by 27 · see citing works
Costa, F. T. M., Avril, M., Nogueira, P. A., & Gysin, J. (2006) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2006001200003 · Cited by 29 · see citing works
Complement Activation in Placental Malaria
McDonald, C. R., Tran, V., & Kain, K. C. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.01460 · Cited by 25 · see citing works
Omer, S. A., Franco‐Jarava, C., Noureldien, A., Omer, M., Abdelrahim, M., Molina, I., & Adam, I. (2021) · Malaria Journal · doi:10.1186/s12936-021-03580-x · Cited by 27 · see citing works
Sarr, D., Oliveira, L. J., Russ, B. N., Owino, S. O., Middii, J. D., Mwalimu, S., Ambasa, L., Almutairi, F., VULULE, J. M., Rada, B., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.682668 · Cited by 25 · see citing works
Derrien, M., Faye, A., Dolcini, G. L., Chaouat, G., Barré‐Sinoussi, F., & Menu, E. (2005) · Journal of Virology · doi:10.1128/jvi.79.19.12304-12310.2005 · Cited by 24 · see citing works
Genesis of placental sequestration in malaria and possible targets for drugs for placental malaria
Clark, R. L. (2019) · Birth Defects Research · doi:10.1002/bdr2.1496 · Cited by 27 · see citing works
A brief review on features of falciparum malaria during pregnancy
Manirakiza, A., Serdouma, E., Ngbalé, R. N., Moussa, S., Gondjé, S., Degana, R. M., Bata, G. G. B., Moyen, J. M., Delmont, J. P., Grésenguet, G., et al. (2017) · Journal of Public Health in Africa · doi:10.4081/jphia.2017.668 · Cited by 22 · see citing works
Rodrigues-Duarte, L., Pandya, Y., Neres, R., & Penha‐Gonçalves, C. (2018) · Infection and Immunity · doi:10.1128/iai.00708-17 · Cited by 20 · see citing works
Peripheral Blood Cell Signatures of Plasmodium falciparum Infection during Pregnancy
Ibitokou, S. A., Oesterholt, M., Brutus, L., Borgella, S., Agbowaï, C., Ezinmègnon, S., Lusingu, J., Schmiegelow, C., Massougbodji, A., Deloron, P., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0049621 · Cited by 20 · see citing works
Pastor‐Fernández, I., Collantes-Fernández, E., Jiménez-Pelayo, L., Ortega‐Mora, L. M., & Horcajo, P. (2021) · Frontiers in Veterinary Science · doi:10.3389/fvets.2020.634458 · Cited by 20 · see citing works
Malaria during pregnancy in endemic areas: A lens for examining maternal–fetal conflict
Abrams, E. T., & Meshnick, S. R. (2009) · American Journal of Human Biology · doi:10.1002/ajhb.20919 · Cited by 20 · see citing works
Dobaño, C., Berthoud, T. K., Manaca, M. N., Nhabomba, A. J., Guinovart, C., Aguilar, R., Barbosa, A., Groves, P., Rodríguez, M. H., Jiménez, A., et al. (2018) · Malaria Journal · doi:10.1186/s12936-018-2317-2 · Cited by 20 · see citing works
Suguitan, A. L., Gowda, D. C., Fouda, G. G., Thuita, L. W., Zhou, A., Djokam, R., Metenou, S., Leke, R. G. F., & Taylor, D. W. (2004) · Infection and Immunity · doi:10.1128/iai.72.9.5267-5273.2004 · Cited by 20 · see citing works
Self-citationKane, E. G., & Taylor-Robinson, A. W. (2011) · Malaria Research and Treatment · doi:10.4061/2011/764845 · Cited by 19 · see citing works
Gbédandé, K., Carpio, V. H., & Stephens, R. (2020) · Immunological Reviews · doi:10.1111/imr.12835 · Cited by 19 · see citing works
Ibitokou, S. A., Boström, S., Brutus, L., Ndam, N. T., Vianou, B., Agbowaï, C., Zin, M. A., Huynh, B.-T., Massougbodji, A., Deloron, P., et al. (2014) · Clinical and Vaccine Immunology · doi:10.1128/cvi.00009-14 · Cited by 18 · see citing works
Role of some biomarkers in placental malaria in women living in Yaoundé, Cameroon
Megnekou, R., Djontu, J. C., Bigoga, J. D., Lissom, A., & Magagoum, S. H. (2014) · Acta Tropica · doi:10.1016/j.actatropica.2014.10.007 · Cited by 17 · see citing works
Self-citationKfutwah, A. K. W., Mary, J., Lemen, B., LEKE, R. J. I., Rousset, D., Barré‐Sinoussi, F., Nerrienet, E., Menu, E., Ayouba, A., & for the ANRS 1267 study team (2009) · PLoS ONE · doi:10.1371/journal.pone.0008114 · Cited by 18 · see citing works
Self-citationPornprasert, S., Faye, A., Mary, J., Dolcini, G. L., Leechanachai, P., Chaouat, G., Ngo‐Giang‐Huong, N., Barré‐Sinoussi, F., & Menu, E. (2005) · Placenta · doi:10.1016/j.placenta.2005.10.010 · Cited by 14 · see citing works
Thévenon, A. D., Leke, R. G. F., Suguitan, A. L., Zhou, J. A., & Taylor, D. W. (2009) · Infection and Immunity · doi:10.1128/iai.01069-08 · Cited by 14 · see citing works
Self-citationYeo, K. T., Embury, P., Anderson, T., Mungai, P., Malhotra, I. J., King, C. L., Kazura, J. W., & Dent, A. E. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1801024 · Cited by 14 · see citing works
McDonald, C. R., Weckman, A. M., Conroy, A. L., Olwoch, P., Natureeba, P., Kamya, M. R., Havlir, D. V., Dorsey, G., & Kain, K. C. (2019) · Scientific Reports · doi:10.1038/s41598-019-43191-w · Cited by 14 · see citing works
Megnekou, R., Staalsøe, T., & Hviid, L. (2013) · Malaria Journal · doi:10.1186/1475-2875-12-387 · Cited by 14 · see citing works
Self-citationStructural insights into chondroitin sulfate binding in pregnancy-associated malaria
Khunrae, P., & Higgins, M. K. (2010) · Biochemical Society Transactions · doi:10.1042/bst0381337 · Cited by 14 · see citing works
Davison, B. B., Kaack, M. B., Rogers, L. B., Rasmussen, K. K., Rasmussen, T., Henson, E. W., Montenegro, S., Henson, M. C., Mzwaek, F., & Krogstad, D. J. (2005) · The Journal of Infectious Diseases · doi:10.1086/430004 · Cited by 13 · see citing works
Ibitokou, S. A., Denoeud‐Ndam, L., Ezinmègnon, S., Ladékpo, R., Zannou, D.-M., Massougbodji, A., Girard, P., Cot, M., Luty, A. J. F., & Ndam, N. T. (2015) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.14-0653 · Cited by 13 · see citing works
Kirosingh, A. S., Delmastro, A. C., Kakuru, A., van der Ploeg, K., Bhattacharya, S., Press, K. D., Ty, M., de la Parte, L., Kizza, J., Muhindo, M. K., et al. (2023) · EBioMedicine · doi:10.1016/j.ebiom.2023.104772 · Cited by 12 · see citing works
Chua, C. L. L., Brown, G. V., Hamilton, J. A., Molyneux, M. E., Rogerson, S. J., & Boeuf, P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0064127 · Cited by 13 · see citing works
Dibua, U. M. E., Badger-Emeka, L. I., & Ugonabo, J. A. (2013) · International Journal of Medicine and Medical Sciences · doi:10.5897/ijmms2013.0903 · Cited by 13 · see citing works
Pregnancy-associated malaria: Effects of cytokine and chemokine expression
Sánchez, K., & Spencer, L. M. (2022) · Travel Medicine and Infectious Disease · doi:10.1016/j.tmaid.2022.102282 · Cited by 12 · see citing works
Sarr, D., Bracken, T. C., Owino, S. O., Cooper, C. A., Smith, G., Nagy, T., & Moore, J. M. (2015) · Placenta · doi:10.1016/j.placenta.2015.04.007 · Cited by 12 · see citing works
Effects of Pregnancy‐associated Malaria on T Cell Cytokines in Cameroonian Women
Megnekou, R., Lissom, A., Bigoga, J. D., & Djontu, J. C. (2015) · Scandinavian Journal of Immunology · doi:10.1111/sji.12286 · Cited by 12 · see citing works
Self-citationImpact of oxidative stress in response to malarial infection during pregnancy
Chandrashekhar, V., Punnath, K., Dayanand, K. K., Kakkilaya, S. B., Jayadev, P., Kumari, S., Achur, R. N., & Gowda, D. C. (2022) · Tropical parasitology · doi:10.4103/tp.tp_18_20 · Cited by 11 · see citing works
- Authors
- Suguitan, Jr., Leke, R. G. F., Fouda, G., Zhou, A., Thuita, L., Metenou, S., Fogako, J., Megnekou, R., & Taylor, D. W.
- Affiliations
- Université de Yaoundé I (CM)
- Georgetown University (US)
- Venue
- The Journal of Infectious Diseases
- Publisher
- Oxford University Press (OUP)
- Published
- 2003-10
- Volume
- 188
- Issue
- 7
- Pages
- 1074-7082
- ISSN
- 0022-1899 (ISSN-L)
- 1537-6613
- OpenAlex
- W2096731679
- Cited by
- 161
- References
- 44
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 5 · 2023: 5 · 2022: 5 · 2021: 9 · 2020: 8 · 2019: 7 · 2018: 5 · 2017: 5 · 2016: 5 · 2015: 11 · 2014: 8 · 2013: 10 · 2012: 13
- FWCI
- 8.12
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Infectious Diseases (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Public Health Service (U01A1 43888)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Keywords
- Plasmodium falciparum, malaria in pregnancy, placenta, chemokines, cytokines, interferon-gamma, TNF-α, IL-10, MCP-1, macrophage inflammatory protein-1alpha, macrophage inflammatory protein-1β, CXCL10, fetal tissue, placental inflammation, macrophage accumulation, immune regulation
- MeSH terms
- Adult, Animals, Cameroon, Enzyme-Linked Immunosorbent Assay, Female, Fetus, Hematocrit, Humans, Immunohistochemistry, Leukocyte Count, Placenta, Plasmodium falciparum, Pregnancy, Pregnancy Complications, Parasitic, Cytokines, Malaria, Falciparum, Parasitemia, Chemokines
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review