Experimental Study: The Relationship between Plasmodium falciparum Gametocyte Carriage and Mosquitoes Infectiousness in Two Sympatric Ethnic Groups in Burkina Faso

Main Article Content

Samuel S. Serme
Noëlie H. Bere
Salif Sombie
Amidou Diarra
Desire Kargougou
Benjamin S. Sombie
Moussa Guelbeogo
Ouedraogo N. Issa
Alfred B. Tiono
Edith C. Bougouma
David Modiano
Yves Traore
Issiaka Soulama
Sodiomon B. Sirima

Abstract

Aims: The lower susceptibility of the Fulani to malaria compared to Mossi was previously described in Burkina Faso in West Africa. The mature gametocyte stage of Plasmodium falciparum is known to be the only stage capable of infecting the mosquito though this process is disrupted by the action of immunity and other factors as well. Our study aims to assess the ability of two sympatric ethnic groups known to have different susceptibility to Plasmodium falciparum malaria, to infect mosquitoes through an experimental membrane feeding assay.

Methodology: Study participants were gametocyte carriers aged from 2 to 12 years recruited in the village of Barkoundouba where Fulani and Mossi are living in sympatric. A venous blood was obtained from each participant for direct membrane feeding assay of insectary reared mosquitoes. Blood fed mosquitoes were stored for 7 days with sugar water as the only food source, then dissected for the microscopic detection for oocysts.

Results: A total of 1050 mosquitoes were used for the experimental infections. Eight day after feeding, a total of 897 mosquitoes were dissected, 275 from the Fulani and 622 from the Mossi group. With an average of 43 stomachs examined by experimentation, the mosquito infestation rate was 10.5% in Fulani and 13.2% in Mossi group (p=0.569). The fed mosquito rate was 95 % and 95.6% in Fulani and Mossi ethnic group respectively (p=0.241). The rate of survival mosquitoes after the feeding was 96.5% and 87.5% in Fulani and Mossi ethnic group respectively (p=0.088). The proportion of dissected mosquitoes was 100% and 99.2% in Fulani and Mossi ethnic group respectively (p=0.138) leading to an average oocystic load of 249 in Fulani and 21 in Mossi group. The success rate of DMFA in both groups combined was 57.14%. Indeed, this rate was 33.33% and 66.67% in Fulani and Mossi group respectively.

Conclusion: Our study showed that there is no significant difference found between the two ethnic group with the fed, survival, dissected and the infested mosquitoes rate. However, the average of oocystic load was higher in Fulani than the Mossi group despite the low infection in Fulani group. There is a need to explore the mechanism underlying such difference between the two ethnic groups.

Keywords:
P. falciparum gametocytes, mosquitoes, infectivity, ethnicity, DMFA.

Article Details

How to Cite
S. Serme, S., H. Bere, N., Sombie, S., Diarra, A., Kargougou, D., S. Sombie, B., Guelbeogo, M., N. Issa, O., B. Tiono, A., C. Bougouma, E., Modiano, D., Traore, Y., Soulama, I., & B. Sirima, S. (2020). Experimental Study: The Relationship between Plasmodium falciparum Gametocyte Carriage and Mosquitoes Infectiousness in Two Sympatric Ethnic Groups in Burkina Faso. Advances in Research, 20(5), 1-9. https://doi.org/10.9734/air/2019/v20i530167
Section
Original Research Article

References

Meis J, Wismans P, Jap P, Lensen A, Ponnudurai T: A scanning electron microscopic study of the sporogonic development of Plasmodium falciparum in Anopheles stephensi. Acta Trop. 1992; 50:227-236.

Bradley J, Stone W, Da D, Morlais I, Dicko A, Cohuet A, et al. Predicting the likelihood and intensity of mosquito infection from sex specific Plasmodium falciparum gametocyte density. Elife. 2018; 7:e34463.

Churcher TS, Bousema T, Walker M, Drakeley C, Schneider P, Ouedraogo AL, et al. Predicting mosquito infection from Plasmodium falciparum gametocyte density and estimating the reservoir of infection. Elife. 2013;2:e00626.

Bhatt S, Weiss D, Cameron E, Bisanzio D, Mappin B, Dalrymple U. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526(7572):207-211.

Griffin J, Hollingsworth T, Okell L, Churcher T, White M, Hinsley W, et al. Reducing Plasmodium falciparum malaria transmission in Africa: A model-based evaluation of intervention strategies. PLoS Med. 2010;7(8).

RBM P: The global malaria action plan for a malaria free world. WHO Press, Geneva, Switzerland. 2008;91.

Modiano D, Petrarca V, Sirima B, Bosman A, Nebié I, Diallo D, et al. Plasmodium falciparum malaria in sympatric ethnic groups of Burkina Faso, West Africa. Parassitologia. 1995;37(2-3):255-259.

Modiano D, Chiucchiuini A, Vincenzo P, Sirima B, Gaia L, Roggero M, et al. Interethnic differences in the humoral response to non-repetitive regions of the Plasmodium falciparum circumsporozoite protein. Am J Trop Med Hyg. 1999;61:663-667.

Nebie I, Diarra A, Ouedraogo A, et al. Humoral responses to Plasmodium falciparum blood-stage antigens and association with incidence of clinical malaria in children living in an area of seasonal malaria transmission in Burkina Faso, West Africa. Infect Immun. 2008; 76:759-766.

Ouédraogo AL, Guelbéogo WM, Cohuet A, Morlais I, King JG, Gon-çalves BP, et al. A protocol for mem-brane feeding assays to determine the infectiousness of P. falciparum naturally infected individuals to Anopheles gambiae. Malaria World Journal. 2013;4:16.

Ponnudurai T, Lensen A, Van Gemert G, Bensink M, Bolmer M, Meuwissen J. Feeding behaviour and sporozoite ejection by infected Anopheles Stephensì. Trans R Soc Trop Med Hyg. 1991;85:175-180.

Drakeley CJ, Akim INJ, Sauerwein BR, Greenwood BM, Targett GAT. Estimates of the infectious reservoir of P. falciparum malaria in the Gambia and in Tanzania. Trans R Soc Trop Med Hyg. 2000;94:472-476.

Awono-Ambene H, Diawara L, Robert V: Comparison of direct and membrane feeding methods to infect Anopheles arabkiensis with Plasmodium falciparum. Am J Trop Med Hyg. 2001;64:32- 34.

Ponnudurai T, Lensen AH, Van Gemert G, Bensink M, Bolmer M, Meuwissen J. Infectivity of cultured Plasmodium falciparum gametocytes to mosquitoes. Parasitology. 1989;98 Pt 2:165-173.

Boudin C, Lyannaz J, Bosseno M, Chaize J, Carnevale P. Production of sporozoites of human Plasmodium in Bobo-Dioulasso (Burkina Faso). Ann Soc Belg Med Trop (Mars). 1989; 69(1):3-23.

Smalley: Plasmodium falciparum gametogenesis In vitro. Nature. 1976; 2M:271-272.

Jensen JB. Observations on gametogenesis in Plasmodium falciprum from continuous culture.] Protozol. 1979; 26:129-132.

Rutledge LCD, Tantichareon JGB. Factors affecting the infection of anophelines with human malaria in Thailand. Trans Roy Soc Trop Med Hyg. 1969;63:613-619.

Boudin C, Van DKM, Tchuinkam T, Gouagna C, Bonnet S, Safeukui I, et al. Parasite Plasmodium falciparum transmission blocking immunity under conditions of low and high endemicity in Cameroon. Immunol Lett. 2004;26:105-110.

Schneider P, Bousema J, Gouagna L, Otieno S, Van de Vegte-Bolmer M, Omar S. Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am J Trop Med Hyg. 2007;76:470-474.

Mendes A, Awono-Ambene P, Nsango S, Cohuet A, Fontenille D, Kafatos F, et al. Infection intensity-dependent responses of Anopheles gambiae to the African malaria parasite Plasmodium falciparum. Infect Immun. 2011;79:4708-4715.

Bousema T, Dinglasan R, Morlais I, Gouagna L, Van WT, Awono-Ambene P, et al. A Mosquito feeding assays to determine the infectiousness of naturally infected Plasmodium falciparum gametocyte carriers. PLoS One. 2012;7:e42821.

Paul RE, Bonnet S, Boudin C, Tchuinkam T, Robert V. Aggregation in malaria parasites places limits on mosquito infection rates. Infect Genet Evol. 2007; 7:577-586.

Bousema T, Griffin J, Sauerwein R, Smith D, Churcher T, Takken W, et al. Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Med. 2012; 9:e1001165.