Coinfection with Plasmodium Falciparum and Schistosoma Haematobium: Additional Evidence of the Protective Effect of Schistosomiasis on Malaria in Senegalese Children

Overview

Journal Am J Trop Med Hyg

Specialty Tropical Medicine

Date 2013 Dec 11

PMID 24323515

Citations 33

Authors

Magali Lemaitre

Laurence Watier

Valerie Briand

Andre Garcia

Jean Yves Le Hesran

Michel Cot

Affiliations

Soon will be listed here.

Abstract

Parasitic infections are associated with high morbidity and mortality in developing countries. Several studies focused on the influence of helminth infections on malaria but the nature of the biological interaction is under debate. Our objective was to undertake a study to explore the influence of the measure of excreted egg load caused by Schistosoma haematobium on Plasmodium falciparum parasite densities. Ten measures of malaria parasite density and two measures of schistosomiasis egg urinary excretion over a 2-year follow-up period on 178 Senegalese children were considered. A linear mixed-effect model was developed to take data dependence into account. This work showed that children with a light S. haematobium infection (1-9 eggs/mL of urine) presented lower P. falciparum parasite densities than children not infected by S. haematobium (P < 0.04). Possible changes caused by parasite coinfections should be considered in the anti-helminth treatment of children and in malaria vaccination development.

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References

Brutus L, Watier L, Hanitrasoamampionona V, Razanatsoarilala H, Cot M . Confirmation of the protective effect of Ascaris lumbricoides on Plasmodium falciparum infection: results of a randomized trial in Madagascar. Am J Trop Med Hyg. 2008; 77(6):1091-5. View

Arinola O . Complement factors and circulating immune complexes in children with urinary schistosomiasis and asymptomatic malaria. Afr J Med Med Sci. 2005; 34(1):9-13. View

Yoshida A, Maruyama H, Kumagai T, Amano T, Kobayashi F, Zhang M . Schistosoma mansoni infection cancels the susceptibility to Plasmodium chabaudi through induction of type 1 immune responses in A/J mice. Int Immunol. 2000; 12(8):1117-25. DOI: 10.1093/intimm/12.8.1117. View

Wilson S, Vennervald B, Kadzo H, Ireri E, Amaganga C, Booth M . Hepatosplenomegaly in Kenyan schoolchildren: exacerbation by concurrent chronic exposure to malaria and Schistosoma mansoni infection. Trop Med Int Health. 2007; 12(12):1442-9. DOI: 10.1111/j.1365-3156.2007.01950.x. View

Adegnika A, Kremsner P . Epidemiology of malaria and helminth interaction: a review from 2001 to 2011. Curr Opin HIV AIDS. 2012; 7(3):221-4. DOI: 10.1097/COH.0b013e3283524d90. View

Boel M, Carrara V, Rijken M, Proux S, Nacher M, Pimanpanarak M . Complex Interactions between soil-transmitted helminths and malaria in pregnant women on the Thai-Burmese border. PLoS Negl Trop Dis. 2010; 4(11):e887. PMC: 2982827. DOI: 10.1371/journal.pntd.0000887. View

Cox F . Concomitant infections, parasites and immune responses. Parasitology. 2001; 122 Suppl:S23-38. DOI: 10.1017/s003118200001698x. View

Diallo T, Remoue F, Gaayeb L, Schacht A, Charrier N, De Clerck D . Schistosomiasis coinfection in children influences acquired immune response against Plasmodium falciparum malaria antigens. PLoS One. 2010; 5(9):e12764. PMC: 2939900. DOI: 10.1371/journal.pone.0012764. View

Robert V, Dieng H, Lochouran L, Traore S, Trape J, Simondon F . [Malaria transmission in the rural zone of Niakhar, Senegal]. Trop Med Int Health. 1998; 3(8):667-77. DOI: 10.1046/j.1365-3156.1998.00288.x. View

10.

Lyke K, Dicko A, Dabo A, Sangare L, Kone A, Coulibaly D . Association of Schistosoma haematobium infection with protection against acute Plasmodium falciparum malaria in Malian children. Am J Trop Med Hyg. 2005; 73(6):1124-30. PMC: 2738948. View

11.

CHRISTENSEN N, Furu P, Kurtzhals J, Odaibo A . Heterologous synergistic interactions in concurrent experimental infection in the mouse with Schistosoma mansoni, Echinostoma revolutum, Plasmodium yoelii, Babesia microti, and Trypanosoma brucei. Parasitol Res. 1988; 74(6):544-51. DOI: 10.1007/BF00531632. View

12.

Zeger S, Liang K . Longitudinal data analysis for discrete and continuous outcomes. Biometrics. 1986; 42(1):121-30. View

13.

Wiria A, Prasetyani M, Hamid F, Wammes L, Lell B, Ariawan I . Does treatment of intestinal helminth infections influence malaria? Background and methodology of a longitudinal study of clinical, parasitological and immunological parameters in Nangapanda, Flores, Indonesia (ImmunoSPIN Study). BMC Infect Dis. 2010; 10:77. PMC: 2859773. DOI: 10.1186/1471-2334-10-77. View

14.

Diallo T, Remoue F, Schacht A, Charrier N, Dompnier J, Pillet S . Schistosomiasis co-infection in humans influences inflammatory markers in uncomplicated Plasmodium falciparum malaria. Parasite Immunol. 2005; 26(8-9):365-9. DOI: 10.1111/j.0141-9838.2004.00719.x. View

15.

Sokhna C, Le Hesran J, Mbaye P, Akiana J, Camara P, Diop M . Increase of malaria attacks among children presenting concomitant infection by Schistosoma mansoni in Senegal. Malar J. 2004; 3:43. PMC: 538284. DOI: 10.1186/1475-2875-3-43. View

16.

Brutus L, Watier L, Briand V, Hanitrasoamampionona V, Razanatsoarilala H, Cot M . Parasitic co-infections: does Ascaris lumbricoides protect against Plasmodium falciparum infection?. Am J Trop Med Hyg. 2006; 75(2):194-8. View

17.

Garcia A, Dieng A, Rouget F, Migot-Nabias F, Le Hesran J, Gaye O . Role of environment and behaviour in familial resemblances of Plasmodium falciparum infection in a population of Senegalese children. Microbes Infect. 2004; 6(1):68-75. DOI: 10.1016/j.micinf.2003.09.021. View

18.

Knowles S . The effect of helminth co-infection on malaria in mice: a meta-analysis. Int J Parasitol. 2011; 41(10):1041-51. DOI: 10.1016/j.ijpara.2011.05.009. View

19.

Mutapi F, Ndhlovu P, Hagan P, Woolhouse M . Anti-schistosome antibody responses in children coinfected with malaria. Parasite Immunol. 2000; 22(4):207-9. DOI: 10.1046/j.1365-3024.2000.00288.x. View

20.

Nacher M . Interactions between worms and malaria: good worms or bad worms?. Malar J. 2011; 10:259. PMC: 3192711. DOI: 10.1186/1475-2875-10-259. View