COINFECTION WITH PLASMODIUM FALCIPARUM AND SCHISTOSOMA HAEMATOBIUM: PROTECTIVE EFFECT OF SCHISTOSOMIASIS ON MALARIA IN SENEGALESE CHILDREN?

VALÉRIE BRIAND Institut de Recherche pour le Développement, Unité de Recherche Santé de la Mère et d’Enfant en Milieu Tropical (Unité 010), Faculté de Pharmacie, Université Paris V, Paris, France; Institut National de la Santé et de la Recherche Médicale, Unité d’Epidemiologie et de Biostatistiques (Unite 472), Villejuif, France

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LAURENCE WATIER Institut de Recherche pour le Développement, Unité de Recherche Santé de la Mère et d’Enfant en Milieu Tropical (Unité 010), Faculté de Pharmacie, Université Paris V, Paris, France; Institut National de la Santé et de la Recherche Médicale, Unité d’Epidemiologie et de Biostatistiques (Unite 472), Villejuif, France

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JEAN-YVES LE HESRAN Institut de Recherche pour le Développement, Unité de Recherche Santé de la Mère et d’Enfant en Milieu Tropical (Unité 010), Faculté de Pharmacie, Université Paris V, Paris, France; Institut National de la Santé et de la Recherche Médicale, Unité d’Epidemiologie et de Biostatistiques (Unite 472), Villejuif, France

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ANDRÉ GARCIA Institut de Recherche pour le Développement, Unité de Recherche Santé de la Mère et d’Enfant en Milieu Tropical (Unité 010), Faculté de Pharmacie, Université Paris V, Paris, France; Institut National de la Santé et de la Recherche Médicale, Unité d’Epidemiologie et de Biostatistiques (Unite 472), Villejuif, France

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MICHEL COT Institut de Recherche pour le Développement, Unité de Recherche Santé de la Mère et d’Enfant en Milieu Tropical (Unité 010), Faculté de Pharmacie, Université Paris V, Paris, France; Institut National de la Santé et de la Recherche Médicale, Unité d’Epidemiologie et de Biostatistiques (Unite 472), Villejuif, France

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Studies with animal models have suggested the possibility of interactions between parasites during concurrent infections and have raised the question of a similar phenomenon in humans. The present survey was undertaken to assess the impact of urinary schistosomiasis on the susceptibility of children to malaria. It was carried out in Senegal between September 2001 and March 2002 among 523 children 3–15 years of age. We tested the association between Plasmodium falciparum densities and the load of Schistosoma haematobium egg excretion using a linear mixed model because data were not independent. After controlling for age, sex, and season, we showed that children lightly infected with S. haematobium (1–9 eggs/10 mL of urine) had lower P. falciparum densities than those not infected (β = −0.34, 95% confidence interval = −0.85, −0.10), suggesting a negative interaction between both parasites.

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  • 1

    Petney TN, Andrews RH, 1998. Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. Int J Parasitol 28 :377–393.

  • 2

    Ashford RW, Craig PS, Oppenheimer SJ, 1992. Polyparasitism on the Kenya coast. 1. Prevalence and association between parasitic infections. Ann Trop Med Parasitol 86 :671–679.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Keiser J, N’Goran EK, Traore M, Lohourignon KL, Singer BH, Lengeler C, Tanner M, Utzinger J, 2002. Polyparasitism with Schistosoma mansoni, geohelminths, and intestinal protozoa in rural Côte d’Ivoire. J Parasitol 88 :461–466.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Christensen NO, Furu P, Kurtzhals J, Odaibo A, 1988. Heterologous synergistic interactions in concurrent experimental infection in the mouse with Schistosoma mansoni, Echinostoma revolutum, Plasmodium yoelii, Babesia microti, and Trypanosoma brucei. Parasitol Res 74 :544–551.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Cox FEG, 2001. Concomitant infections, parasites and immune responses. Parasitology 122 :S23–S38.

  • 6

    Helmby H, Kullberg M, Troye-Blomberg M, 1998. Altered immune responses in mice with concomitant Schistosoma mansoni and Plasmodium chabaudi infections. Infect Immun 66 :5167–5174.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Yoshida A, Maruyama H, Kumagai T, Amano T, Kobayashi F, Zhang M, Himeno K, Ohta N, 2000. Schistosoma mansoni infection cancels the susceptibility to Plasmodium chabaudi through induction of type 1 immune responses in A/J mice. Int Immunol 12 :1117–1125.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Abdel-Wahab MF, Powers KG, Mahmoud SS, Good WC, 1974. Suppression of schistosome granuloma formation by malaria in mice. Am J Trop Med Hyg 23 :915–918.

  • 9

    Murray MJ, Murray AB, Murray MB, Murray CJ, 1977. Parotid enlargement, forehead edema, and suppression of malaria as nutritional consequences of ascariasis. Am J Clin Nutr 30 :2117–2121.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Nacher M, Gay F, Singhasivanon P, Krudsood S, Treeprasertsuk S, Mazier D, Vouldoukis I, Looareesuwan S, 2000. Ascaris lumbricoides infection is associated with protection from cerebral malaria. Parasite Immunol 22 :107–113.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Keusch GT, Migasena P, 1982. Biological implications of poly-parasitism. Rev Infect Dis 4 :880–882.

  • 12

    Nacher M, Singhasivanon P, Yimsamran S, Manibunyong W, Thanyavanich N, Wuthisen R, Looareesuwan S, 2002. Intestinal helminth infections are associated with increased incidence of Plasmodium falciparum malaria in Thailand. J Parasitol 88 :55–58.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Le Hesran JY, Akiana J, Ndiaye el HM, Dia M, Senghor P, Konate L, 2004. Severe malaria attack is associated with high prevalence of Ascaris Lumbricoides infection among children in rural Senegal. Trans R Soc Trop Med Hyg 98 :397–399.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Robert V, Dieng H, Lochouran L, Traore SF, Trape JF, Simondon F, Fontenille D, 1998. Malaria transmission in the rural zone of Niakhar, Senegal (French). Trop Med Int Health 3 :667–677.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    WHO, 1998. Guidelines for the Evaluation of Soil-Transmitted Helminthiasis and Schistosomiasis at the Community Level. Geneva: World Health Organization.

    • PubMed
    • Export Citation
  • 16

    McCulloch CE, Searle SR, 2001. Generalized, Linear, and Mixed Models. New York: John Wiley & Sons, Inc.

    • PubMed
    • Export Citation
  • 17

    Mutapi F, Ndhlovu PD, Hagan P, Woolhouse ME, 2000. Anti-schistosome antibody responses in children coinfected with malaria. Parasite Immunol 22 :207–209.

  • 18

    Remoue F, Diallo TO, Angeli V, Hervé M, de Clercq D, Schacht AM, Charrier N, Capron M, Vercruysse J, Ly A, Capron A, Riveau G, 2003. Malaria coinfection in children influences antibodies response to schistosome antigens and inflammatory markers associated with morbidity. Trans R Soc Trop Med Hyg 97 :361–364.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Woolhouse MEJ, Watts CH, Chandiwana SK, 1991. Heterogeneities in transmission rates and the epidemiology of schistosome infection. Proc R Soc Lond B Biol Sci 245 :109–114.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Chandiwana SK, Woolhouse ME, 1991. Heterogeneities in water contacts patterns and the epidemiology of Schistosoma haematobium. Parasitology 103 :363–370.

  • 21

    Etard JF, Audibert M, Dabo A, 1995. Age-acquired resistance and predisposition to reinfection with Schistosoma haematobium after treatment with praziquantel in Mali. Am J Trop Med Hyg 52 :549–558.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Delley V, Bouvier P, Breslow N, Doumbo O, Sagara I, Diakite M, Mauris A, Dolo A, Rougemont A, 2000. What does a single determination of malaria parasite density mean? A longitudinal survey in Mali. Trop Med Int Health 5 :404–412.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Campagne G, Vera C, Barkire H, Tinni A, Tassie JM, Garba A, Sellin B, Chippaux JP, 1999. Preliminary evaluation of usable indicators during a control program for urinary bilharziosis in Niger. Med Trop (Mars) 59 :243–248.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Shankar AH, 2000. Nutritional modulation of malaria morbidity and mortality. J Infect Dis 182 :S616–S635.

  • 25

    Weatherall DJ, Clegg JB, 2002. Genetic variability in response to infection: malaria and after. Genes Immun 3 :331–337.

  • 26

    Allen JE, Maizels RM, 1997. Th1-Th2: reliable paradigm or dangerous dogma? Immunol Today 18 :387–392.

  • 27

    Fallon PG, 2000. Immunopathology of schistosomiasis: a cautionary tale of mice and men. Immunol Today 21 :29–35.

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