Characterization of the infectious reservoir of malaria with an agent-based model calibrated to age-stratified parasite densities and infectiousness

Malaria Journal

Volumn 14, Issue 1, 2015, Pages

  Gerardin, Jaline ^a   Ouédraogo, André Lin ^a,b   McCarthy, Kevin A ^a   Eckhoff, Philip A ^a   Wenger, Edward A ^a  

^a INSTITUTE FOR DISEASE MODELING   (United States)

^b Burkina Faso   (Burkina Faso)

Author keywords

Diagnostics; Drug campaigns; Infectious reservoir; Infectivity; Mechanistic model

Indexed keywords

ANTIMALARIAL AGENT; ARTEMETHER PLUS BENFLUMETOL; DIHYDROARTEMISININ PLUS PIPERAQUINE;

ADAPTIVE IMMUNITY; AGE DISTRIBUTION; ANOPHELES FUNESTUS; ANOPHELES GAMBIAE; ARTICLE; BED NET; CALIBRATION; CASE MANAGEMENT; DISEASE CARRIER; GAMETOCYTE; MALARIA; OOCYST; PARASITE CLEARANCE; PARASITE LOAD; PARASITE PREVALENCE; PARASITE TRANSMISSION; SEASONAL VARIATION; STOCHASTIC MODEL; VECTOR CONTROL; ADOLESCENT; ADULT; AFRICA; AGED; ANIMAL; BIOLOGICAL MODEL; CHILD; HUMAN; INCIDENCE; INFANT; INSECTICIDE TREATED NET; MALARIA, FALCIPARUM; MASS SCREENING; MIDDLE AGED; MOSQUITO; NEWBORN; PARASITOLOGY; PHYSIOLOGY; PLASMODIUM FALCIPARUM; PRESCHOOL CHILD; PREVALENCE; TANZANIA; TRANSMISSION; VERY ELDERLY;

ADOLESCENT; ADULT; AFRICA, WESTERN; AGED; AGED, 80 AND OVER; ANIMALS; ANTIMALARIALS; CHILD; CHILD, PRESCHOOL; CULICIDAE; DISEASE RESERVOIRS; HUMANS; INCIDENCE; INFANT; INFANT, NEWBORN; INSECTICIDE-TREATED BEDNETS; MALARIA, FALCIPARUM; MASS SCREENING; MIDDLE AGED; MODELS, BIOLOGICAL; PLASMODIUM FALCIPARUM; PREVALENCE; TANZANIA;

EID: 84936950719     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/s12936-015-0751-y     Document Type: Article

References (45)

1. World Health Organization. World malaria report 2013. Geneva: WHO; 2013. p. 1-286.
2. WHO Malaria Policy Advisory Committee and Secretariat. Malaria Policy Advisory Committee to the WHO: conclusions and recommendations of sixth biannual meeting (September 2014). Malar J. 2015;14:137.
3. Cotter C, Sturrock HJ, Hsiang MS, Liu J, Phillips AA, Hwang J, et al. The changing epidemiology of malaria elimination: new strategies for new challenges. Lancet. 2013;382:900-11.
4. Ochola LB, Vounatsou P, Smith T, Mabaso MLH, Newton CRJC. The reliability of diagnostic techniques in the diagnosis and management of malaria in the absence of a gold standard. Lancet Infect Dis. 2006;6:582-8.
5. Bousema T, Okell L, Felger I, Drakeley C. Asymptomatic malaria infections: detectability, transmissibility and public health relevance. Nat Rev Microbiol. 2014;12:833-40.
6. Jeffery GM, Eyles DE. Infectivity to mosquitoes of Plasmodium falciparum as related to gametocyte density and duration of infection. Am J Trop Med Hyg. 1955;4:781-9.
7. Da DF, Churcher TS, Yerbanga RS, Yaméogo B, Sangaré I, Ouédraogo JB, et al. Experimental study of the relationship between Plasmodium gametocyte density and infection success in mosquitoes: implications for the evaluation of malaria transmission-reducing interventions. Exp Parasitol. 2015;149(C):74-83.
8. Young MD, Hardman NF, Burgess RW, Frohne WC, Sabrosky CW. The infectivity of native malarias in South Carolina to Anopheles quadrimaculatus. Am J Trop Med Hyg. 1948;1:303-11.
9. Bousema T, Drakeley C. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev. 2011;24:377-410.
10. Drakeley CJ, Bousema JT, Akim INJ, Teelen K, Roeffen W, Lensen AH, et al. Transmission-reducing immunity is inversely related to age in Plasmodium falciparum gametocyte carriers. Parasite Immunol. 2006;28:185-90.
11. Greenwood BM. Asymptomatic malaria infections-do they matter? Parasitol Today. 1987;3:206-14.
12. Okell LC, Bousema T, Griffin JT, Ouédraogo AL, Ghani AC, Drakeley CJ. Factors determining the occurrence of submicroscopic malaria infections and their relevance for control. Nat Commun. 2012;3:1237.
13. 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.
14. Ouédraogo AL, Gonçalves BP, Gnémé A, Wenger EA, Guelbeogo MW, Ouédraogo A, et al. Dynamics of the human infectious reservoir for malaria determined by mosquito feeding assays and ultra-sensitive malaria diagnosis in Burkina Faso. J Infect Dis. 2015: in press.
15. Epidemiological Modeling Software. www.idmod.org/software.
16. Eckhoff PA. Malaria parasite diversity and transmission intensity affect development of parasitological immunity in a mathematical model. Malar J. 2012;11:419.
17. Eckhoff P. Mathematical models of within-host and transmission dynamics to determine effects of malaria interventions in a variety of transmission settings. Am J Trop Med Hyg. 2013;88:817-27.
18. Eckhoff P. P. falciparum infection durations and infectiousness are shaped by antigenic variation and innate and adaptive host immunity in a mathematical model. PLoS One. 2012;7:e44950.
19. McCarthy KA, Wenger EA, Huynh GH, Eckhoff PA. Calibration of an intrahost malaria model and parameter ensemble evaluation of a pre-erythrocytic vaccine. Malar J. 2015;14:6.
20. Molineaux L, Gramiccia G. The Garki project: research on the epidemiology and control of malaria in the Sudan Savanna of West Africa. Geneva: World Health Organization; 1980.
21. Smith T, Charlwood JD, Kihonda J, Mwankusye S, Billingsley P, Meuwissen J, et al. Absence of seasonal variation in malaria parasitaemia in an area of intense seasonal transmission. Acta Trop. 1993;54:55-72.
22. Rogier C, Tall A, Diagne N, Fontenille D, Spiegel A, Trape JF. Plasmodium falciparum clinical malaria: lessons from longitudinal studies in Senegal. Parassitologia. 1999;41:255-9.
23. Trape JF, Rogier C, Konate L, Diagne N, Bouganali H, Canque B, et al. The Dielmo project: a longitudinal study of natural malaria infection and the mechanisms of protective immunity in a community living in a holoendemic area of Senegal. Am J Trop Med Hyg. 1994;51:123-37.
24. Collins WE, Jeffery GM. A retrospective examination of sporozoite- and trophozoite-induced infections with Plasmodium falciparum: development of parasitologic and clinical immunity during primary infection. Am J Trop Med Hyg. 1999;61:4-19.
25. Ouedraogo AL, Roeffen W, Luty AJF, de Vlas SJ, Nebie I, Ilboudo-Sanogo E, et al. Naturally acquired immune responses to Plasmodium falciparum sexual stage antigens Pfs48/45 and Pfs230 in an area of seasonal transmission. Infect Immun. 2011;79:4957-64.
26. Raftery AE, Bao L. Estimating and projecting trends in HIV/AIDS generalized epidemics using incremental mixture importance sampling. Biometrics. 2010;66:1162-73.
27. Eckhoff PA. A malaria transmission-directed model of mosquito life cycle and ecology. Malar J. 2011;10:303.
28. Central Intelligence Agency (CIA). The world factbook. Washington, DC: Central Intelligence Agency; 2014.
29. Carnevale P, Frézil JL, Bosseno MF, Le Pont F, Lancien J. [The aggressiveness of Anopheles gambiae A in relation to the age and sex of the human subjects] (in French). Bull World Health Organ. 1978;56:147-54.
30. Port GR, Boreham PFL, Bryan JH. The relationship of host size to feeding by mosquitoes of the Anopheles gambiae Giles complex (Diptera: Culicidae). Bull Entomol Res. 1980;70:133-44.
31. Smith T, Maire N, Dietz K, Killeen GF, Vounatsou P, Molineaux L, et al. Relationship between the entomologic inoculation rate and the force of infection for Plasmodium falciparum malaria. Am J Trop Med Hyg. 2006;75:11-8.
32. Gerardin J, Eckhoff P, Wenger EA. Mass campaigns with antimalarial drugs: a modelling comparison of artemether-lumefantrine and DHA-piperaquine with and without primaquine as tools for malaria control and elimination. BMC Infect Dis. 2015;15:144.
33. Tarning J, Zongo I, Somé FA, Rouamba N, Parikh S, Rosenthal PJ, et al. Population pharmacokinetics and pharmacodynamics of piperaquine in children with uncomplicated falciparum malaria. Clin Pharmacol Ther. 2009;91:497-505.
34. Churcher TS, Trape JF, Cohuet A. Human-to-mosquito transmission efficiency increases as malaria is controlled. Nat Commun. 2015;6:6054.
35. Nafo-Traore F, Judd EJ, Okwo-Bele J-M. Protecting vulnerable groups in malaria-endemic areas in Africa through accelerated deployment of insecticide-treated nets. In: A joint WHO-UNICEF statement volume 57. Geneva: WHO/UNICEF; 2005. p. 1-2.
36. Brie¨t OJ, Penny MA. Repeated mass distributions and continuous distribution of long-lasting insecticidal nets: modelling sustainability of health benefits from mosquito nets, depending on case management. Malar J. 2013;12:401.
37. The WorldWide Antimalarial Resistance Network (WWARN) DP Study Group. The effect of dosing regimens on the antimalarial efficacy of dihydroartemisinin-piperaquine: a pooled analysis of individual patient data. PLoS Med. 2013;10:e1001564.
38. Tiono AB, Ouédraogo A, Ogutu B, Diarra A, Coulibaly S, Gansané A, et al. A controlled, parallel, cluster-randomized trial of community-wide screening and treatment of asymptomatic carriers of Plasmodium falciparum in Burkina Faso. Malar J. 2013;12:79.
39. Daniels RF, Schaffner SF, Wenger EA, Proctor JL, Chang H-H, Wong W, et al. Modeling malaria genomics reveals transmission decline and rebound in Senegal. Proc Natl Acad Sci USA. 2015, epub ahead of print 10.1073/pnas.1505691112.
40. Smalley ME, Sinden RE. Plasmodium falciparum gametocytes: their longevity and infectivity. Parasitology. 1977;74:1-8.
41. Baker DA. Malaria gametocytogenesis. Mol Biochem Parasitol. 2010;172:57-65.
42. Bousema T, Sutherland CJ, Churcher TS, Mulder B, Gouagna LC, Riley EM, et al. Human immune responses that reduce the transmission of Plasmodium falciparum in African populations. Int J Parasitol. 2011;41:293-300.
43. Schneider P, Bousema JT, Gouagna LC, Otieno S, van de Vegte-Bolmer M, Omar SA, et al. Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am J Trop Med Hyg. 2007;76:470-4.
44. Walker M, Basáñez M-G, Ouédraogo A, Hermsen C, Bousema T, Churcher TS. Improving statistical inference on pathogen densities estimated by quantitative molecular methods: malaria gametocytaemia as a case study. BMC Bioinformatics. 2015;16:5.
45. Bousema T, Dinglasan RR, Morlais I, Gouagna LC, van Warmerdam T, Awono-Ambene PH, et al. Mosquito feeding assays to determine the infectiousness of naturally infected Plasmodium falciparum gametocyte carriers. PLoS One. 2012;7, e42821.