Volume 75, Issue 5
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645


Pregnancy-associated malaria is one of the leading causes of low birth weight in malaria endemic areas. In this study, 145 parturient women residing in areas endemic for in Lambaréné, Gabon, were recruited into the study after delivery, and the association of maternal infection, inflammatory response, and birth weight was studied. At delivery, 10% (15) of the mothers (12 were positive in both peripheral and placental blood smears, 1 was positive in peripheral blood only, and 2 were positive in placenta blood only) were positive for by microscopy and 23% (30) by real-time polymerase chain reaction (PCR). The level of C-reactive protein (CRP) was significantly elevated in microscopically –positive pregnant women (34 mg/L; 95% CI: 3–458) but not in those with sub-microscopic infections (6 mg/L; 95% CI: 1–40) compared with those free of infection (7 mg/L; 95% CI: 1–43). In a multivariate analysis, the presence of microscopic (adjusted OR = 28.6, 95% CI = 4.8–169.0) or sub-microscopic (adjusted OR = 13.2, 95% CI = 2.4–73.0) infection in pregnant women and age of mothers < 21 years (adjusted OR = 9.7 CI = 1.0–89.7), but not CRP levels, were independent predictors for low birth weight. This finding may have important operational implications and emphasizes the need for appropriate diagnostic methods in studies evaluating the outcome of pregnancy-associated malaria.


Article metrics loading...

The graphs shown below represent data from March 2017
Loading full text...

Full text loading...



  1. Ramsay S, 2003. Preventing malaria in pregnancy. Lancet Infect Dis 3 : 4. [Google Scholar]
  2. Bray RS, Anderson MJ, 1979. Falciparum malaria and pregnancy. Trans R Soc Trop Med Hyg 73 : 427–431. [Google Scholar]
  3. Bouyou-Akotet MK, Ionete-Collard DE, Mabika-Manfoumbi M, Kendjo E, Matsiegui PB, Mavoungou E, Kombila M, 2003. Prevalence of Plasmodium falciparum infection in pregnant women in Gabon. Malar J 2 : 18. [Google Scholar]
  4. Tako EA, Zhou A, Lohoue J, Leke R, Taylor DW, Leke RF, 2005. Risk factors for placental malaria and its effect on pregnancy outcome in Yaounde, Cameroon. Am J Trop Med Hyg 72 : 236–242. [Google Scholar]
  5. Shi YP, Sayed U, Qari SH, Roberts JM, Udhayakumar V, Oloo AJ, Hawley WA, Kaslow DC, Nahlen BL, Lal AA, 1996. Natural immune response to the C-terminal 19-kilodalton domain of Plasmodium falciparum merozoite surface protein 1. Infect Immun 64 : 2716–2723. [Google Scholar]
  6. Oeuvray C, Theisen M, Rogier C, Trape JF, Jepsen S, Druilhe P, 2000. Cytophilic immunoglobulin responses to Plasmodium falciparum glutamate-rich protein are correlated with protection against clinical malaria in Dielmo, Senegal. Infect Immun 68 : 2617–2620. [Google Scholar]
  7. Adam I, Ali DM, Elbashir MI, 2004. Manifestations of falciparum malaria in pregnant women of Eastern Sudan. Saudi Med J 25 : 1947–1950. [Google Scholar]
  8. Steketee RW, Wirima JJ, Slutsker L, Heymann DL, Breman JG, 1996. The problem of malaria and malaria control in pregnancy in sub-Saharan Africa. Am J Trop Med Hyg 55 : 2–7. [Google Scholar]
  9. Okoko BJ, Enwere G, Ota MO, 2003. The epidemiology and consequences of maternal malaria: A review of immunological basis. Acta Trop 87 : 193–205. [Google Scholar]
  10. McCormick MC, 1985. The contribution of low birth weight to infant mortality and childhood morbidity. N Engl J Med 312 : 82–90. [Google Scholar]
  11. Menendez C, 1995. Malaria during pregnancy: a priority area of malaria research and control. Parasitol Today 11 : 178–183. [Google Scholar]
  12. 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]
  13. Brabin BJ, 1983. An analysis of malaria in pregnancy in Africa. Bull World Health Organ 61 : 1005–1016. [Google Scholar]
  14. Guyatt HL, Snow RW, 2004. Impact of malaria during pregnancy on low birth weight in sub-Saharan Africa. Clin Microbiol Rev 17 : 760–769. [Google Scholar]
  15. Whitty CJ, Edmonds S, Mutabingwa TK, 2005. Malaria in pregnancy. BJOG 112 : 1189–1195. [Google Scholar]
  16. Fried M, Duffy PE, 1996. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 272 : 1502–1504. [Google Scholar]
  17. Lekana Douki JB, Traore B, Costa FT, Fusai T, Pouvelle B, Sterkers Y, Scherf A, Gysin J, 2002. Sequestration of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate A, a receptor for maternal malaria: monoclonal antibodies against the native parasite ligand reveal pan-reactive epitopes in placental isolates. Blood 100 : 1478–1483. [Google Scholar]
  18. Torre D, Speranza F, Giola M, Matteelli A, Tambini R, Biondi G, 2002. Role of Th1 and Th2 cytokines in immune response to uncomplicated Plasmodium falciparum malaria. Clin Diagn Lab Immunol 9 : 348–351. [Google Scholar]
  19. Bates MD, Quenby S, Takakuwa K, Johnson PM, Vince GS, 2002. Aberrant cytokine production by peripheral blood mononuclear cells in recurrent pregnancy loss? Hum Reprod 17 : 2439–2444. [Google Scholar]
  20. Kemp K, Kurtzhals JA, Akanmori BD, Adabayeri V, Goka BQ, Behr C, Hviid L, 2002. Increased levels of soluble CD30 in plasma of patients with Plasmodium falciparum malaria. Clin Diagn Lab Immunol 9 : 720–722. [Google Scholar]
  21. Graninger W, Thalhammer F, Hollenstein U, Zotter GM, Kremsner PG, 1992. Serum protein concentrations in Plasmodium falciparum malaria. Acta Trop 52 : 121–128. [Google Scholar]
  22. Ghezzi F, Franchi M, Raio L, Di Naro E, Bossi G, D’Eril GV, Bolis P, 2002. Elevated amniotic fluid C-reactive protein at the time of genetic amniocentesis is a marker for preterm delivery. Am J Obstet Gynecol 186 : 268–273. [Google Scholar]
  23. Malek A, Bersinger NA, Di Santo S, Mueller MD, Sager R, Schneider H, Ghezzi F, Karousou E, Passi A, De Luca G, Raio L, 2005. C-reactive protein production in term human placental tissue. Placenta 27 : 619–625. [Google Scholar]
  24. Ramharter M, Grobusch MP, Kiessling G, Adegnika AA, Moller U, Agnandji ST, Kramer M, Schwarz N, Kun JF, Oyakhirome S, Issifou S, Borrmann S, Lell B, Mordmuller B, Kremsner PG, 2005. Clinical and parasitological characteristics of puerperal malaria. J Infect Dis 191 : 1005–1009. [Google Scholar]
  25. Kassberger F, Birkenmaier A, Khattab A, Kremsner PG, Klinkert MQ, 2002. PCR typing of Plasmodium falciparum in matched peripheral, placental and umbilical cord blood. Parasitol Res 88 : 1073–1079. [Google Scholar]
  26. Mayengue PI, Rieth H, Khattab A, Issifou S, Kremsner PG, Klinkert MQ, Ntoumi F, 2004. Sub-microscopic Plasmodium falciparum infections and multiplicity of infection in matched peripheral, placental and umbilical cord blood samples from Gabonese women. Trop Med Int Health 9 : 949–958. [Google Scholar]
  27. Walker-Abbey A, Djokam RR, Eno A, Leke RF, Titanji VP, Fogako J, Sama G, Thuita LH, Beardslee E, Snounou G, Zhou A, Taylor DW, 2005. Malaria in pregnant Cameroonian women: The effect of age and gravidity on sub-microscopic and mixed-species infections and multiple parasite genotypes. Am J Trop Med Hyg 72 : 229–235. [Google Scholar]
  28. Singer LM, Newman RD, Diarra A, Moran AC, Huber CS, Stennies G, Sirima SB, Konate A, Yameogo M, Sawadogo R, Barnwell JW, Parise ME, 2004. Evaluation of a malaria rapid diagnostic test for assessing the burden of malaria during pregnancy. Am J Trop Med Hyg 70 : 481–485. [Google Scholar]
  29. Ntoumi F, Contamin H, Rogier C, Bonnefoy S, Trape JF, Mercereau-Puijalon O, 1995. Age-dependent carriage of multiple Plasmodium falciparum merozoite surface antigen-2 alleles in asymptomatic malaria infections. Am J Trop Med Hyg 52 : 81–88. [Google Scholar]
  30. Snounou G, Bourne T, Jarra W, Viriyakosol S, Brown KN, 1992. Identification and quantification of rodent malaria strains and species using gene probes. Parasitology 105 : 21–27. [Google Scholar]
  31. Andrews L, Andersen RF, Webster D, Dunachie S, Walther RM, Bejon P, Hunt-Cooke A, Bergson G, Sanderson F, Hill AV, Gilbert SC, 2005. Quantitative real-time polymerase chain reaction for malaria diagnosis and its use in malaria vaccine clinical trials. Am J Trop Med Hyg 73 : 191–198. [Google Scholar]
  32. 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]
  33. Swan H, Sloan L, Muyombwe A, Chavalitshewinkoon-Petmitr P, Krudsood S, Leowattana W, Wilairatana P, Looareesuwan S, Rosenblatt J, 2005. Evaluation of a real-time polymerase chain reaction assay for the diagnosis of malaria in patients from Thailand. Am J Trop Med Hyg 73 : 850–854. [Google Scholar]
  34. Mankhambo L, Kanjala M, Rudman S, Lema VM, Rogerson SJ, 2002. Evaluation of the OptiMAL rapid antigen test and species-specific PCR to detect placental Plasmodium falciparum infection at delivery. J Clin Microbiol 40 : 155–158. [Google Scholar]
  35. Wildling E, Winkler S, Kremsner PG, Brandts C, Jenne L, Wernsdorfer WH, 1995. Malaria epidemiology in the province of Moyen Ogoov, Gabon. Trop Med Parasitol 46 : 77–82. [Google Scholar]
  36. Sylla EH, Kun JF, Kremsner PG, 2000. Mosquito distribution and entomological inoculation rates in three malaria-endemic areas in Gabon. Trans R Soc Trop Med Hyg 94 : 652–656. [Google Scholar]
  37. Borrmann S, Oyakhirome S, Esser G, Trinkle C, Issifou S, Grobusch MP, Krishna S, Kremsner PG, 2004. Short report: Evaluation of a simple and inexpensive photometric device for the measurement of hemoglobin. Am J Trop Med Hyg 71 : 691–692. [Google Scholar]
  38. Planche T, Krishna S, Kombila M, Engel K, Faucher JF, Ngou-Milama E, Kremsner PG, 2001. Comparison of methods for the rapid laboratory assessment of children with malaria. Am J Trop Med Hyg 65 : 599–602. [Google Scholar]
  39. Dati F, Schumann G, Thomas L, Aguzzi F, Baudner S, Bienvenu J, Blaabjerg O, Blirup-Jensen S, Carlstrom A, Petersen PH, Johnson AM, Milford-Ward A, Ritchie RF, Svendsen PJ, Whicher J, 1996. Consensus of a group of professional societies and diagnostic companies on guidelines for interim reference ranges for 14 proteins in serum based on the standardization against the IFCC/BCR/CAP Reference Material (CRM 470). International Federation of Clinical Chemistry. Community Bureau of Reference of the Commission of the European Communities. College of American Pathologists. Eur J Clin Chem Clin Biochem 34 : 517–520. [Google Scholar]
  40. Borrmann S, Binder RK, Adegnika AA, Missinou MA, Issifou S, Ramharter M, Wernsdorfer WH, Kremsner PG, 2002. Reassessment of the resistance of Plasmodium falciparum to chloroquine in Gabon: Implications for the validity of tests in vitro vs. in vivo. Trans R Soc Trop Med Hyg 96 : 660–663. [Google Scholar]
  41. Ramharter M, Wernsdorfer WH, Kremsner PG, 2004. In vitro activity of quinolines against Plasmodium falciparum in Gabon. Acta Trop 90 : 55–60. [Google Scholar]
  42. Saute F, Menendez C, Mayor A, Aponte J, Gomez-Olive X, Dgedge M, Alonso P, 2002. Malaria in pregnancy in rural Mozambique: The role of parity, sub-microscopic and multiple Plasmodium falciparum infections. Trop Med Int Health 7 : 19–28. [Google Scholar]
  43. Mockenhaupt FP, Rong B, Till H, Eggelte TA, Beck S, Gyasi-Sarpong C, Thompson WN, Bienzle U, 2000. Sub-microscopic Plasmodium falciparum infections in pregnancy in Ghana. Trop Med Int Health 5 : 167–173. [Google Scholar]
  44. Achidi EA, Kuoh AJ, Minang JT, Ngum B, Achimbom BM, Motaze SC, Ahmadou MJ, Troye-Blomberg M, 2005. Malaria infection in pregnancy and its effects on haemoglobin levels in women from a malaria endemic area of Fako Division, South West Province, Cameroon. J Obstet Gynaecol 25 : 235–240. [Google Scholar]
  45. van den Borne BE, Landewe RB, Rietveld JH, Goei The HS, Griep EN, Breedveld FC, Dijkmans BA, 1999. Chloroquine therapy in patients with recent-onset rheumatoid arthritis: The clinical response can be predicted by the low level of acute-phase reaction at baseline. Clin Rheumatol 18 : 369–372. [Google Scholar]
  46. Di Naro E, Ghezzi F, Raio L, Romano F, Mueller MD, McDougall J, Cicinelli E, 2003. C-reactive protein in vaginal fluid of patients with preterm premature rupture of membranes. Acta Obstet Gynecol Scand 82 : 1072–1079. [Google Scholar]
  47. Chen SU, Ko TM, Hwa HL, Lu PJ, Ho HN, Yang YS, 2001. Maternal serum C-reactive protein level does not change significantly after fetal reduction: It could be used as an indicator of chorioamnionitis. J Assist Reprod Genet 18 : 336–340. [Google Scholar]
  48. Yoon BH, Romero R, Shim JY, Shim SS, Kim CJ, Jun JK, 2003. C-reactive protein in umbilical cord blood: A simple and widely available clinical method to assess the risk of amniotic fluid infection and funisitis. J Matern Fetal Neonatal Med 14 : 85–90. [Google Scholar]
  49. Mwanyumba F, Inion I, Gaillard P, Mandaliya K, Praet M, Temmerman M, 2003. Placental inflammation and perinatal outcome. Eur J Obstet Gynecol Reprod Biol 108 : 164–170. [Google Scholar]
  50. Luxemburger C, McGready R, Kham A, Morison L, Cho T, Chongsuphajaisiddhi T, White NJ, Nosten F, 2001. Effects of malaria during pregnancy on infant mortality in an area of low malaria transmission. Am J Epidemiol 154 : 459–465. [Google Scholar]
  51. Singh N, Mehra RK, Srivastava N, 2001. Malaria during pregnancy and infancy, in an area of intense malaria transmission in central India. Ann Trop Med Parasitol 95 : 19–29. [Google Scholar]
  52. WHO Expert Committee on Malaria. 2000. World Health Organ Tech Rep Ser 892 : i74. [Google Scholar]

Data & Media loading...

  • Received : 22 Feb 2006
  • Accepted : 26 Jul 2006

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error