Volume 80, Issue 1
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645


malaria and human immunodeficiency virus (HIV)-1 adversely interact in the context of pregnancy, however little is known regarding the influence of co-infection on the risk of congenital malaria. We aimed to determine the prevalence of placental and congenital malaria and impact of HIV co-infection on trans-placental malaria transmission in 157 parturient women and their infants by microscopy and by quantitative real-time polymerase chain reaction (PCR) in western Kenya. The prevalence of placental and cord blood infections were 17.2% and 0% by microscopy, and 33.1% and 10.8% by PCR. HIV co-infection was associated with a significant increase in placental parasite density ( < 0.05). Cord blood malaria prevalence was increased in co-infected women (odds ratio [OR] = 5.42; 95% confidence interval [CI] = 1.90–15.47) and correlated with placental parasite density (OR = 2.57; 95% CI = 1.80–3.67). A 1-log increase in placental monocyte count was associated with increased risk of congenital infection ( = 0.001) (OR = 48.15; 95% CI = 4.59–505.50). The HIV co-infected women have a significantly increased burden of placental malaria that increases the risk of congenital infection.


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  1. Worrall E, Morel C, Yeung S, Borghi J, Webster J, Hill J, Wiseman V, Mills A, 2007. The economics of malaria in pregnancy—a review of the evidence and research priorities. Lancet Infect Dis 7 : 156–168. [Google Scholar]
  2. Desai M, ter Kuile FO, Nosten F, McGready R, Asamoa K, Brabin B, Newman RD, 2007. Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis 7 : 93–104. [Google Scholar]
  3. Steketee RW, Nahlen BL, Parise ME, Menendez C, 2001. The burden of malaria in pregnancy in malaria-endemic areas. Am J Trop Med Hyg 64 : 28–35. [Google Scholar]
  4. Astagneau P, Steketee RW, Wirima JJ, Khoromana CO, Millet P, 1994. Antibodies to ring-infected erythrocyte surface antigen (Pf155/RESA) protect against P. falciparum parasitemia in highly exposed multigravidas women in Malawi. Acta Trop 57 : 317–325. [Google Scholar]
  5. Brabin B, 1991. An assessment of low birthweight risk in primiparae as an indicator of malaria control in pregnancy. Int J Epidemiol 20 : 276–283. [Google Scholar]
  6. Shulman CE, Graham WJ, Jilo H, Lowe BS, New L, Obiero J, Snow RW, Marsh K, 1996. Malaria is an important cause of anaemia in primigravidae: evidence from a district hospital in coastal Kenya. Trans R Soc Trop Med Hyg 90 : 535–539. [Google Scholar]
  7. Rogerson SJ, Chaiyaroj SC, Ng K, Reeder JC, Brown GV, 1995. Chondroitin sulfate A is a cell-surface receptor for Plasmodium falciparum-infected erythrocytes. J Exp Med 182 : 15–20. [Google Scholar]
  8. Reeder JC, Cowman AF, Davern KM, Beeson JG, Thompson JK, Rogerson SJ, Brown GV, 1999. The adhesion of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate A is mediated by P. falciparum erythrocyte membrane protein 1. Proc Natl Acad Sci USA 96 : 5198–5202. [Google Scholar]
  9. Ricke CH, Staalsoe T, Koram K, Akanmori BD, Riley EM, Theander TG, Hviid L, 2000. Plasma antibodies from malaria-exposed pregnant women recognize variant surface antigens on Plasmodium falciparum-infected erythrocytes in a parity-dependent manner and block parasite adhesion to chondroitin sulphate A. J Immunol 165 : 3309–3316. [Google Scholar]
  10. Fried M, Nosten F, Brockman A, Brabin BJ, Duffy PE, 1998. Maternal antibodies block malaria. Nature 395 : 851–852. [Google Scholar]
  11. Serghides L, Patel SN, Ayi K, Kain KC, 2006. Placental chondroitin sulfate A-binding malarial isolates evade innate phagocytic clearance. J Infect Dis 194 : 133–139. [Google Scholar]
  12. Kraemer SM, Smith JD, 2006. A family affair: var genes, PfEMP1 binding, and malaria disease. Curr Opin Microbiol 9 : 374–380. [Google Scholar]
  13. Galbraith RM, Fox H, Hsi B, Galbraith GMP, Bray RS, Faulk WP, 1980. The human maternofoetal relationship in malaria. II. Histological, ultrastructural and immunopathological studies of the placenta. Trans R Soc Trop Med Hyg 74 : 61–72. [Google Scholar]
  14. Walter PR, Garin Y, Blot P, 1982. Placental pathologic changes in malaria. A histologic and ultrastructural study. Am J Pathol 109 : 330–342. [Google Scholar]
  15. Malhotra I, Mungai P, Muchiri E, Kwiek JJ, Meshnick SR, King CL, 2006. Umbilical cord-blood infections with Plasmodium falciparum malaria are acquired antenatally in Kenya. J Infect Dis 194 : 176–183. [Google Scholar]
  16. Uneke CJ, 2007. Congenital Plasmodium falciparum malaria in sub-Saharan Africa: a rarity or frequent occurrence? Parasitol Res 101 : 835–842. [Google Scholar]
  17. Broen K, Brustoski K, Engelmann I, Luty AJ, 2007. Placental Plasmodium falciparum infection: causes and consequences of in utero sensitization to parasite antigens. Mol Biochem Parasitol 151 : 1–8. [Google Scholar]
  18. Tobian AA, Mehlotra RK, Malhotra I, Wamachi A, Mungai P, Koech D, Ouma J, Zimmerman P, King CL, 2000. Frequent umbilical cord-blood and maternal-blood infections with Plasmodium falciparum, P. malariae, and P. ovale in Kenya. J Infect Dis 182 : 558–563. [Google Scholar]
  19. Xiao LH, 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. [Google Scholar]
  20. Whitworth J, Morgan D, Quigley M, Smith A, Mayanja B, Eotu H, Omoding N, Okongo M, Malamba S, Ojwiya A, 2000. Effect of HIV-1 and increasing immunosuppression on malaria parasitaemia and clinical episodes in adults in rural Uganda: a cohort study. Lancet 356 : 1051–1056. [Google Scholar]
  21. Patnaik P, Jere CS, Miller WC, Hoffman IF, Wirima J, Pendame R, Meshnick SR, Taylor TE, Molyneux ME, Kublin JG, 2005. Effects of HIV-1 serostatus, HIV-1 RNA concentration, and CD4 cell count on the incidence of malaria infection in a cohort of adults in rural Malawi. J Infect Dis 192 : 984–991. [Google Scholar]
  22. Mermin J, Ekwaru JP, Liechty CA, Were W, Downing R, Ransom R, Weidle P, Lule J, Coutinho A, Solberg P, 2006. Effect of co-trimoxazole prophylaxis, antiretroviral therapy, and insecticide-treated bed nets on the frequency of malaria in HIV-1-infected adults in Uganda: a prospective cohort study. Lancet 367 : 1256–1261. [Google Scholar]
  23. French N, Nakiyingi J, Lugada E, Watera C, Whitworth JA, Gilks CF, 2001. Increasing rates of malarial fever with deteriorating immune status in HIV-1-infected Ugandan adults. AIDS 15 : 899–906. [Google Scholar]
  24. Kamya MR, Gasasira AF, Yeka A, Bakyaita N, Nsobya SL, Francis D, Rosenthal PJ, Dorsey G, Havlir D, 2006. Effect of HIV-1 infection on antimalarial treatment outcomes in Uganda: a population-based study. J Infect Dis 193 : 9–15. [Google Scholar]
  25. Abu-Raddad LJ, Patnaik P, Kublin JG, 2006. Dual infection with HIV and malaria fuels the spread of both diseases in sub-Saharan Africa. Science 314 : 1603–1606. [Google Scholar]
  26. Brentlinger PE, Behrens CB, Micek MA, 2006. Challenges in the concurrent management of malaria and HIV in pregnancy in sub-Saharan Africa. Lancet Infect Dis 6 : 100–111. [Google Scholar]
  27. Mwapasa V, Rogerson SJ, Molyneux ME, Abrams ET, Kamwendo DD, Lema VM, Tadesse E, Chaluluka E, Wilson PE, Meshnick SR, 2004. The effect of Plasmodium falciparum malaria on peripheral and placental HIV-1 RNA concentrations in pregnant Malawian women. AIDS 18 : 1051–1059. [Google Scholar]
  28. 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. [Google Scholar]
  29. Ayisi JG, van Eijk AM, Newman RD, ter Kuile FO, Shi YP, Yang C, Kolczak MS, Otieno JA, Misore AO, Kager PA, Lal RB, Steketee RW, Nahlen BL, 2004. Maternal malaria and perinatal HIV transmission, western Kenya. Emerg Infect Dis 10 : 643–652. [Google Scholar]
  30. Brahmbhatt H, Kigozi G, Wabwire-Mangen F, Wabwire-Mangen F, Serwadda D, Sewankambo N, Lutalo T, Wawer MJ, Abramowsky C, Sullivan D, Gray R, 2003. The effects of placental malaria on mother-to-child HIV transmission in Rakai, Uganda. AIDS 17 : 2539–2541. [Google Scholar]
  31. Inion I, Mwanyumba F, Gaillard P, Chohan V, Verhofstede C, Claeys P, Mandaliya K, Van Marck E, Temmerman M, 2003. Placental malaria and perinatal transmission of human immunodeficiency virus type 1. J Infect Dis 188 : 1675–1678. [Google Scholar]
  32. 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 : 41–54. [Google Scholar]
  33. Farcas GA, Zhong KJY, Mazzulli T, Kain KC, 2004. Evaluation of the RealArt Malaria LC real-time PCR assay for malaria diagnosis. J Clin Microbiol 42 : 636–638. [Google Scholar]
  34. Malhotra I, Dent A, Mungai P, Muchiri E, King CL, 2005. Real-time quantitative PCR for determining the burden of Plasmodium falciparum parasites during pregnancy and infancy. J Clin Microbiol 43 : 3630–3635. [Google Scholar]
  35. Beier JC, Oster CN, Onyango FK, Bales JD, Sherwood JA, Perkins PV, Chumo DK, Koech DV, Whitmire RE, Roberts CR, 1994. Plasmodium falciparum incidence relative to entomologic inoculation rates at a site proposed for testing malaria vaccines in western Kenya. Am J Trop Med Hyg 50 : 529–536. [Google Scholar]
  36. Adazu K, Lindblade KA, Rosen DH, Odhiambo F, Ofware P, Kwach J, Van Eijk AM, Decock KM, Amornkul P, Karanja D, Vulule JM, Slutsker L, 2005. Health and demographic surveillance in rural western Kenya: a platform for evaluating interventions to reduce morbidity and mortality from infectious diseases. Am J Trop Med Hyg 73 : 1151–1158. [Google Scholar]
  37. 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. [Google Scholar]
  38. Moore JM, Nahlen BL, Misore A, Lal AA, Udhayakumar V, 1999. Immunity to placental malaria. I. Elevated production of interferon-gamma by placental blood mononuclear cells is associated with protection in an area with high transmission of malaria. J Infect Dis 179 : 1218–1225. [Google Scholar]
  39. Othoro C, Moore JM, Wannemuehler K, Nahlen BL, Otieno J, Slutsker L, Lal AA, Shi YP, 2006. Evaluation of various methods of maternal placental blood collection for immunology studies. Clin Vaccine Immunol 13 : 568–574. [Google Scholar]
  40. Moore JM, Nahlen B, Ofulla AV, Caba J, Ayisi J, Oloo A, Misore A, Nahmias AJ, Lal AA, Udhayakumar V, 1997. A simple perfusion technique for isolation of maternal intervillous blood mononuclear cells from human placentae. J Immunol Methods 209 : 93–104. [Google Scholar]
  41. 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. [Google Scholar]
  42. Abrams ET, Brown H, Chensue SW, Turner GD, Tadesse E, Lema VM, Molyneux ME, Rochford R, Meshnick SR, Roerson SJ, 2003. Host response to malaria during pregnancy: placental monocyte recruitment is associated with elevated beta chemokine expression. J Immunol 170 : 2759–2764. [Google Scholar]
  43. Chaisavaneeyakorn S, Lucchi N, Abramowsky C, Othoro C, Chaiyoroj SC, Shi YP, Nahlen BL, Peterson DS, Moore JM, Udhayakumar V, 2005. Immunohistological characterization of macrophage migration inhibitory factor expression in Plasmodium falciparum-infected placentas. Infect Immun 73 : 3287–3293. [Google Scholar]
  44. Fried M, Muga RO, Misore AO, Duffy PE, 1998. Malaria elicits type 1 cytokines in the human placenta: IFN-gamma and TNF-alpha associated with pregnancy outcomes. J Immunol 160 : 2523–2530. [Google Scholar]
  45. Rogerson SJ, Brown HC, Pollina E, Pollina E, Abrams ET, Tadesse E, Lema VM, Molyneux ME, 2003. Placental tumor necrosis factor alpha but not gamma interferon is associated with placental malaria and low birth weight in Malawian women. Infect Immun 71 : 267–270. [Google Scholar]
  46. Ordi J, Menendez C, Ismail MR, Ventura PJ, Palacin A, Kahigwa E, Ferrer B, Cardesa A, Alonso PL, 2001. Placental malaria is associated with cell-mediated inflammatory responses with selective absence of natural killer cells. J Infect Dis 183 : 1100–1107. [Google Scholar]
  47. Diouf I, Fievet N, Doucoure S, Ngom M, Andrieu M, Mathieu JF, Gaye A, Thiaw OT, Deloron P, 2006. IL-12 producing monocytes and IFN-gamma and TNF-alpha producing T-lymphocytes are increased in placentas infected by Plasmodium falciparum. J Reprod Immunol 73 : 152–162. [Google Scholar]

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  • Received : 13 Jun 2008
  • Accepted : 11 Sep 2008

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