ASSOCIATION OF SCHISTOSOMA HAEMATOBIUM INFECTION WITH PROTECTION AGAINST ACUTE PLASMODIUM FALCIPARUM MALARIA IN MALIAN CHILDREN

KIRSTEN E. LYKE Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Malaria Research and Training Center, Bandiagara Malaria Project, Department of Epidemiology of Parasitic Diseases, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali

Search for other papers by KIRSTEN E. LYKE in
Current site
Google Scholar
PubMed
Close
,
ALASSANE DICKO Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Malaria Research and Training Center, Bandiagara Malaria Project, Department of Epidemiology of Parasitic Diseases, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali

Search for other papers by ALASSANE DICKO in
Current site
Google Scholar
PubMed
Close
,
ABDOULAYE DABO Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Malaria Research and Training Center, Bandiagara Malaria Project, Department of Epidemiology of Parasitic Diseases, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali

Search for other papers by ABDOULAYE DABO in
Current site
Google Scholar
PubMed
Close
,
LANSANA SANGARE Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Malaria Research and Training Center, Bandiagara Malaria Project, Department of Epidemiology of Parasitic Diseases, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali

Search for other papers by LANSANA SANGARE in
Current site
Google Scholar
PubMed
Close
,
ABDOULAYE KONE Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Malaria Research and Training Center, Bandiagara Malaria Project, Department of Epidemiology of Parasitic Diseases, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali

Search for other papers by ABDOULAYE KONE in
Current site
Google Scholar
PubMed
Close
,
DRISSA COULIBALY Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Malaria Research and Training Center, Bandiagara Malaria Project, Department of Epidemiology of Parasitic Diseases, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali

Search for other papers by DRISSA COULIBALY in
Current site
Google Scholar
PubMed
Close
,
ANDO GUINDO Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Malaria Research and Training Center, Bandiagara Malaria Project, Department of Epidemiology of Parasitic Diseases, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali

Search for other papers by ANDO GUINDO in
Current site
Google Scholar
PubMed
Close
,
KARIM TRAORE Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Malaria Research and Training Center, Bandiagara Malaria Project, Department of Epidemiology of Parasitic Diseases, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali

Search for other papers by KARIM TRAORE in
Current site
Google Scholar
PubMed
Close
,
MODIBO DAOU Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Malaria Research and Training Center, Bandiagara Malaria Project, Department of Epidemiology of Parasitic Diseases, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali

Search for other papers by MODIBO DAOU in
Current site
Google Scholar
PubMed
Close
,
ISSA DIARRA Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Malaria Research and Training Center, Bandiagara Malaria Project, Department of Epidemiology of Parasitic Diseases, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali

Search for other papers by ISSA DIARRA in
Current site
Google Scholar
PubMed
Close
,
MARCELO B. SZTEIN Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Malaria Research and Training Center, Bandiagara Malaria Project, Department of Epidemiology of Parasitic Diseases, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali

Search for other papers by MARCELO B. SZTEIN in
Current site
Google Scholar
PubMed
Close
,
CHRISTOPHER V. PLOWE Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Malaria Research and Training Center, Bandiagara Malaria Project, Department of Epidemiology of Parasitic Diseases, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali

Search for other papers by CHRISTOPHER V. PLOWE in
Current site
Google Scholar
PubMed
Close
, and
OGOBARA K. DOUMBO Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Malaria Research and Training Center, Bandiagara Malaria Project, Department of Epidemiology of Parasitic Diseases, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali

Search for other papers by OGOBARA K. DOUMBO in
Current site
Google Scholar
PubMed
Close
Restricted access

Plasmodium falciparum and Schistosoma haematobium are co-endemic parasitic diseases with worldwide distribution. Evidence suggests interactions occur between helminthic and malaria infections, although it is unclear whether this effect is beneficial or harmful to the host. Malian children 4–14 years of age with asymptomatic S. haematobium infection (SP) (n = 338) were prospectively matched by age, sex, and residence to children without schistosomiasis (SN) (n = 338) who were cleared of occult intestinal parasites, and followed-up for one malaria transmission season (25 weeks). The time to the first clinical malaria infection, incidence of malaria episodes, and parasitemia were recorded. Age associated protection from malaria in children with schistosomiasis was observed. SP children (4–8 years of age) compared with SN children demonstrated delayed time to first clinical malaria infection (74 versus 59 days; P = 0.04), fewer numbers of malaria episodes (1.55 versus 1.81 infections; P = 0.03) and lower geometric mean parasite densities (6,359 versus 9,874 asexual forms/mm3; P = 0.07) at first infection. No association between schistosomiasis and P. falciparum malaria was observed in children 9–14 years of age. We conclude that underlying schistosomiasis is associated with protection against clinical falciparum malaria in an age-dependent manner.

Author Notes

  • 1

    Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI, 2005. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434 :214–217.

  • 2

    Onah DN, Onyenwe IW, Ihedioha JI, Onwumere OS, 2004. Enhanced survival of rats concurrently infected with Trypanosoma brucei and Strongyloides ratti. Vet Parasitol 119 :165–176.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Yan Y, Inuo G, Akao N, Tsukidate S, Fujita K, 1997. Down-regulation of murine susceptibility to cerebral malaria by inoculation with third-stage larvae of the filarial nematode Brugia pahangi. Parasitology 114 :333–338.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    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
  • 5

    Legesse M, Erko B, Balcha F, 2004. Increased parasitaemia and delayed parasite clearance in Schistosoma mansoni and Plasmodium berghei co-infected mice. Acta Trop 91 :161–166.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    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
  • 7

    Nacher M, Singhasivanon P, Silachamroon U, Treeprasertsuk S, Vannaphan S, Traore B, Gay F, Looareesuwan S, 2001. Helminth infections are associated with protection from malaria-related acute renal failure and jaundice in Thailand. Am J Trop Med Hyg 65 :834–836.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Spiegel A, Tall A, Raphenon G, Trape JF, Druilhe P, 2003. Increased frequency of malaria attacks in subjects co-infected by intestinal worms and Plasmodium falciparum malaria. Trans R Soc Trop Med Hyg 97 :198–199.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    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
  • 10

    Sokhna C, Le Hesran JY, Mbaye PA, Akiana J, Camara P, Diop M, Ly A, Druilhe P, 2004. Increase of malaria attacks among children presenting concomitant infection by Schistosoma mansoni in Senegal. Malar J 3 :43.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Coulibaly D, Diallo DA, Thera MA, Dicko A, Guindo AB, Kone AK, Cissoko Y, Coulibaly S, Djimde A, Lyke K, Doumbo OK, Plowe CV, 2002. Impact of preseason treatment on incidence of falciparum malaria and parasite density at a site for testing malaria vaccines in Bandiagara, Mali. Am J Trop Med Hyg 67 :604–610.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    de Clercq D, Rollinson D, Diarra A, Sacko M, Coulibaly G, Landoure A, Traore M, Southgate VR, Kaukas A, Vercruysse J, 1994. Schistosomiasis in Dogon country, Mali: identification and prevalence of the species responsible for infection in the local community. Trans R Soc Trop Med Hyg 88 :653–656.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Corachan M, Ruiz L, Valls ME, Gascon J, 1992. Schistosomiasis and the Dogon country (Mali). Am J Trop Med Hyg 47 :6–9.

  • 14

    Djimde A, Doumbo OK, Cortese JF, Kayentao K, Doumbo S, Diourte Y, Dicko A, Su XZ, Nomura T, Fidock DA, Wellems TE, Plowe CV, Coulibaly D, 2001. A molecular marker for chloroquine-resistant falciparum malaria. N Engl J Med 344 :257–263.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Diallo DA, Doumbo OK, Plowe CV, Wellems TE, Emanuel EJ, Hurst SA, 2005. Community permission for medical research in developing countries. Clin Infect Dis 41 :255–259.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Chandiwana SK, Woolhouse ME, Bradley M, 1991. Factors affecting the intensity of reinfection with Schistosoma haematobium following treatment with praziquantel. Parasitology 102 :73–83.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    King CL, Medhat A, Malhotra I, Nafeh M, Helmy A, Khaudary J, Ibrahim S, El Sherbiny M, Zaky S, Stupi RJ, Brustoski K, Shehata M, Shata MT, 1996. Cytokine control of parasite-specific anergy in human urinary schistosomiasis. IL-10 modulates lymphocyte reactivity. J Immunol 156 :4715–4721.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Grogan JL, Kremsner PG, Deelder AM, Yazdanbakhsh M, 1998. Antigen-specific proliferation and interferon-gamma and interleukin-5 production are down-regulated during Schistosoma haematobium infection. J Infect Dis 177 :1433–1437.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Briand V, Watier L, Le Hesran JY, Garcia A, Cot M, 2005. Coinfection with Plasmodium falciparum and Schistosoma haematobium: Protective effect of schistosomiasis on malaria in Senegalese children? Am J Trop Med Hyg 72 :702–707.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    von der WT, Honarvar N, Langhorne J, 1996. Gene-targeted mice lacking B cells are unable to eliminate a blood stage malaria infection. J Immunol 156 :2510–2516.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Stevenson MM, Tam MF, 1993. Differential induction of helper T cell subsets during blood-stage Plasmodium chabaudi AS infection in resistant and susceptible mice. Clin Exp Immunol 92 :77–83.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Zwingenberger K, Hohmann A, de Brito MC, Ritter M, 1991. Impaired balance of interleukin-4 and interferon-gamma production in infections with Schistosoma mansoni and intestinal nematodes. Scand J Immunol 34 :243–251.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Golding B, Zaitseva M, Golding H, 1994. The potential for recruiting immune responses toward type 1 or type 2 T cell help. Am J Trop Med Hyg 50 :33–40.

  • 24

    Cooper PJ, Chico ME, Sandoval C, Espinel I, Guevara A, Kennedy MW, Urban JF Jr, Griffin GE, Nutman TB, 2000. Human infection with Ascaris lumbricoides is associated with a polarized cytokine response. J Infect Dis 182 :1207–1213.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    La Flamme AC, Scott P, Pearce EJ, 2002. Schistosomiasis delays lesion resolution during Leishmania major infection by impairing parasite killing by macrophages. Parasite Immunol 24 :339–345.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Graham AL, Lamb TJ, Read AF, Allen JE, 2005. Malaria-filaria coinfection in mice makes malarial disease more severe unless filarial infection achieves patency. J Infect Dis 191 :410–421.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Sabin EA, Araujo MI, Carvalho EM, Pearce EJ, 1996. Impairment of tetanus toxoid-specific Th1-like immune responses in humans infected with Schistosoma mansoni. J Infect Dis 173 :269–272.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Cooper PJ, Chico M, Sandoval C, Espinel I, Guevara A, Levine MM, Griffin GE, Nutman TB, 2001. Human infection with Ascaris lumbricoides is associated with suppression of the interleukin-2 response to recombinant cholera toxin B subunit following vaccination with the live oral cholera vaccine CVD 103-HgR. Infect Immun 69 :1574–1580.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Viana IR, Sher A, Carvalho OS, Massara CL, Eloi-Santos SM, Pearce EJ, Colley DG, Gazzinelli G, Correa-Oliveira R, 1994. Interferon-gamma production by peripheral blood mononuclear cells from residents of an area endemic for Schistosoma mansoni. Trans R Soc Trop Med Hyg 88 :466–470.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Zwingenberger K, Irschick E, Siqueira Vergetti JG, Correia Dacal AR, Janssen-Rosseck R, Bienzle U, Huber C, Feldmeier H, 1989. Release of interleukin 2 and gamma interferon by peripheral mononuclear cells in human Schistosoma mansoni infection normalizes after chemotherapy. Scand J Immunol 30 :463–471.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Borkow G, Leng Q, Weisman Z, Stein M, Galai N, Kalinkovich A, Bentwich Z, 2000. Chronic immune activation associated with intestinal helminth infections results in impaired signal transduction and anergy. J Clin Invest 106 :1053–1060.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Kamal SM, Bianchi L, Al Tawil A, Koziel M, El Sayed KK, Peter T, Rasenack JW, 2001. Specific cellular immune response and cytokine patterns in patients coinfected with hepatitis C virus and Schistosoma mansoni. J Infect Dis 184 :972–982.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    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
  • 34

    Nyakeriga AM, Troye-Blomberg M, Dorfman JR, Alexander ND, Back R, Kortok M, Chemtai AK, Marsh K, Williams TN, 2004. Iron deficiency and malaria among children living on the coast of Kenya. J Infect Dis 190 :439–447.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Oppenheimer SJ, Gibson FD, Macfarlane SB, Moody JB, Harrison C, Spencer A, Bunari O, 1986. Iron supplementation increases prevalence and effects of malaria: report on clinical studies in Papua New Guinea. Trans R Soc Trop Med Hyg 80 :603–612.

    • PubMed
    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 79 79 11
Full Text Views 290 4 0
PDF Downloads 85 6 0
 
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save