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Published in: Malaria Journal 1/2018

Open Access 01-12-2018 | Research

Simulation models predict that school-age children are responsible for most human-to-mosquito Plasmodium falciparum transmission in southern Malawi

Authors: Jenna E. Coalson, Lauren M. Cohee, Andrea G. Buchwald, Andrew Nyambalo, John Kubale, Karl B. Seydel, Don Mathanga, Terrie E. Taylor, Miriam K. Laufer, Mark L. Wilson

Published in: Malaria Journal | Issue 1/2018

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Abstract

Background

Malaria persists in some high-transmission areas despite extensive control efforts. Progress toward elimination may require effective targeting of specific human populations that act as key transmission reservoirs.

Methods

Parameterized using molecular-based Plasmodium falciparum infection data from cross-sectional community studies in southern Malawi, a simulation model was developed to predict the proportions of human-to-mosquito transmission arising from (a) children under 5 years old (U5s), (b) school-age children (SAC, 5–15 years), (c) young adults (16–30 years), and (d) adults > 30 years. The model incorporates mosquito biting heterogeneity and differential infectivity (i.e. probability that a blood-fed mosquito develops oocysts) by age and gametocyte density.

Results

The model predicted that SAC were responsible for more than 60% of new mosquito infections in both dry and rainy seasons, even though they comprise only 30% of this southern Malawi population. Young adults were the second largest contributors, while U5s and adults over 30 were each responsible for < 10% of transmission. While the specific predicted values are sensitive to the relative infectiousness of SAC, this group remained the most important contributor to mosquito infections under all realistic estimates.

Conclusions

These results suggest that U5 children play a small role compared to SAC in maintaining P. falciparum transmission in southern Malawi. Models that assume biting homogeneity overestimate the importance of U5s. To reduce transmission, interventions will need to reach more SAC and young adults. This publicly available model can be used by others to estimate age-specific transmission contributions in epidemiologically similar sites with local parameter estimates of P. falciparum prevalence and bed net use.
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Literature
2.
go back to reference Wilson ML, Walker ED, Mzilahowa T, Mathanga DP, Taylor TE. Malaria elimination in Malawi: research needs in highly endemic, poverty-stricken contexts. Acta Trop. 2012;121:218–26.CrossRefPubMed Wilson ML, Walker ED, Mzilahowa T, Mathanga DP, Taylor TE. Malaria elimination in Malawi: research needs in highly endemic, poverty-stricken contexts. Acta Trop. 2012;121:218–26.CrossRefPubMed
3.
go back to reference Mathanga DP, Walker ED, Wilson ML, Ali D, Taylor TE, Laufer MK. Malaria control in Malawi: current status and directions for the future. Acta Trop. 2012;121:212–7.CrossRefPubMed Mathanga DP, Walker ED, Wilson ML, Ali D, Taylor TE, Laufer MK. Malaria control in Malawi: current status and directions for the future. Acta Trop. 2012;121:212–7.CrossRefPubMed
4.
go back to reference Noor AM, Kinyoki DK, Mundia CW, Kabaria CW, Mutua JW, Alegana VA, et al. The changing risk of Plasmodium falciparum malaria infection in Africa: 2000–10: a spatial and temporal analysis of transmission intensity. Lancet. 2014;383:1739–47.CrossRefPubMedPubMedCentral Noor AM, Kinyoki DK, Mundia CW, Kabaria CW, Mutua JW, Alegana VA, et al. The changing risk of Plasmodium falciparum malaria infection in Africa: 2000–10: a spatial and temporal analysis of transmission intensity. Lancet. 2014;383:1739–47.CrossRefPubMedPubMedCentral
5.
go back to reference WHO. World malaria report 2015. Geneva: World Health Organization; 2015. WHO. World malaria report 2015. Geneva: World Health Organization; 2015.
6.
go back to reference Murray CJL, Ortblad KF, Guinovart C, Lim SS, Wolock TM, Roberts DA, et al. Global, regional, and national incidence and mortality for HIV, tuberculosis, and malaria during 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2014;384:1005–70.CrossRefPubMedPubMedCentral Murray CJL, Ortblad KF, Guinovart C, Lim SS, Wolock TM, Roberts DA, et al. Global, regional, and national incidence and mortality for HIV, tuberculosis, and malaria during 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2014;384:1005–70.CrossRefPubMedPubMedCentral
7.
go back to reference Walldorf JA, Cohee LM, Coalson JE, Bauleni A, Nkanaunena K, Kapito-Tembo A, et al. School-age children are a reservoir of malaria infection in Malawi. PLoS ONE. 2015;10:e0134061.CrossRefPubMedPubMedCentral Walldorf JA, Cohee LM, Coalson JE, Bauleni A, Nkanaunena K, Kapito-Tembo A, et al. School-age children are a reservoir of malaria infection in Malawi. PLoS ONE. 2015;10:e0134061.CrossRefPubMedPubMedCentral
8.
go back to reference Coalson JE, Walldorf JA, Cohee LM, Ismail MD, Mathanga D, Joice R, et al. High prevalence of Plasmodium falciparum gametocyte infections in school-age children using sensitive molecular detection: patterns and predictors of risk from a cross-sectional study in southern Malawi. Malar J. 2016;15:527.CrossRefPubMedPubMedCentral Coalson JE, Walldorf JA, Cohee LM, Ismail MD, Mathanga D, Joice R, et al. High prevalence of Plasmodium falciparum gametocyte infections in school-age children using sensitive molecular detection: patterns and predictors of risk from a cross-sectional study in southern Malawi. Malar J. 2016;15:527.CrossRefPubMedPubMedCentral
9.
go back to reference Buchwald A, Walldorf J, Cohee L, Coalson J, Chimbiya N, Bauleni A, et al. Bed net use among school-aged children after a universal bed net campaign in Malawi. Malar J. 2016;15:127.CrossRefPubMedPubMedCentral Buchwald A, Walldorf J, Cohee L, Coalson J, Chimbiya N, Bauleni A, et al. Bed net use among school-aged children after a universal bed net campaign in Malawi. Malar J. 2016;15:127.CrossRefPubMedPubMedCentral
10.
go back to reference Muirhead-Thomson RC. The malarial infectivity of an African village population to mosquitoes (Anopheles gambiae): a random xenodiagnostic survey. Am J Trop Med Hyg. 1957;6:971–9.CrossRefPubMed Muirhead-Thomson RC. The malarial infectivity of an African village population to mosquitoes (Anopheles gambiae): a random xenodiagnostic survey. Am J Trop Med Hyg. 1957;6:971–9.CrossRefPubMed
11.
go back to reference Gamage-Mendis AC, Rajakaruna J, Carter R, Mendis KN. Infectious reservoir of Plasmodium vivax and Plasmodium falciparum malaria in an endemic region of Sri Lanka. Am J Trop Med Hyg. 1991;45:479–87.CrossRefPubMed Gamage-Mendis AC, Rajakaruna J, Carter R, Mendis KN. Infectious reservoir of Plasmodium vivax and Plasmodium falciparum malaria in an endemic region of Sri Lanka. Am J Trop Med Hyg. 1991;45:479–87.CrossRefPubMed
12.
go back to reference Githeko AK, Brandling-Bennett AD, Beier M, Atieli F, Owaga M, Collins FH. The reservoir of Plasmodium falciparum malaria in a holoendemic area of western Kenya. Trans R Soc Trop Med Hyg. 1992;86:355–8.CrossRefPubMed Githeko AK, Brandling-Bennett AD, Beier M, Atieli F, Owaga M, Collins FH. The reservoir of Plasmodium falciparum malaria in a holoendemic area of western Kenya. Trans R Soc Trop Med Hyg. 1992;86:355–8.CrossRefPubMed
13.
go back to reference Boudin C, Olivier M, Molez J-F, Chiron J-P, Ambroise-Thomas P. High human malarial infectivity to laboratory-bred Anopheles gambiae in a village in Burkina Faso. Am J Trop Med Hyg. 1993;48:700–6.CrossRefPubMed Boudin C, Olivier M, Molez J-F, Chiron J-P, Ambroise-Thomas P. High human malarial infectivity to laboratory-bred Anopheles gambiae in a village in Burkina Faso. Am J Trop Med Hyg. 1993;48:700–6.CrossRefPubMed
14.
go back to reference Drakeley C, Akim N, Sauerwein R, Greenwood B, Targett G. Estimates of the infectious reservoir of Plasmodium falciparum malaria in The Gambia and in Tanzania. Trans R Soc Trop Med Hyg. 2000;94:472–6.CrossRefPubMed Drakeley C, Akim N, Sauerwein R, Greenwood B, Targett G. Estimates of the infectious reservoir of Plasmodium falciparum malaria in The Gambia and in Tanzania. Trans R Soc Trop Med Hyg. 2000;94:472–6.CrossRefPubMed
15.
go back to reference Bonnet S, Gouagna LC, Paul RE, Safeukui I, Meunier JY, Boudin C. Estimation of malaria transmission from humans to mosquitoes in two neighbouring villages in south Cameroon: evaluation and comparison of several indices. Trans R Soc Trop Med Hyg. 2003;97:53–9.CrossRefPubMed Bonnet S, Gouagna LC, Paul RE, Safeukui I, Meunier JY, Boudin C. Estimation of malaria transmission from humans to mosquitoes in two neighbouring villages in south Cameroon: evaluation and comparison of several indices. Trans R Soc Trop Med Hyg. 2003;97:53–9.CrossRefPubMed
16.
go back to reference Gaye A, Bousema T, Libasse G, Ndiath MO, Konaté L, Jawara M, et al. Infectiousness of the human population to Anopheles arabiensis by direct skin feeding in an area hypoendemic for malaria in Senegal. Am J Trop Med Hyg. 2015;92:648–52.CrossRefPubMedPubMedCentral Gaye A, Bousema T, Libasse G, Ndiath MO, Konaté L, Jawara M, et al. Infectiousness of the human population to Anopheles arabiensis by direct skin feeding in an area hypoendemic for malaria in Senegal. Am J Trop Med Hyg. 2015;92:648–52.CrossRefPubMedPubMedCentral
17.
go back to reference 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 ultrasensitive malaria diagnosis in Burkina Faso. J Infect Dis. 2016;213:90–9.CrossRefPubMed 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 ultrasensitive malaria diagnosis in Burkina Faso. J Infect Dis. 2016;213:90–9.CrossRefPubMed
18.
go back to reference Gonçalves BP, Kapulu MC, Sawa P, Guelbéogo WM, Tiono AB, Grignard L, et al. Examining the human infectious reservoir for Plasmodium falciparum malaria in areas of differing transmission intensity. Nat Commun. 2017;8:1133.CrossRefPubMedPubMedCentral Gonçalves BP, Kapulu MC, Sawa P, Guelbéogo WM, Tiono AB, Grignard L, et al. Examining the human infectious reservoir for Plasmodium falciparum malaria in areas of differing transmission intensity. Nat Commun. 2017;8:1133.CrossRefPubMedPubMedCentral
19.
go back to reference Carnevale P, Frézil J, Bosseno M, Le Pont F, Lancien J. Etude de l’aggressivité d’Anopheles gambiae A en fonction de l’âge et du sexe des subjets humains. Bull World Health Organ. 1978;56:147–54.PubMedPubMedCentral Carnevale P, Frézil J, Bosseno M, Le Pont F, Lancien J. Etude de l’aggressivité d’Anopheles gambiae A en fonction de l’âge et du sexe des subjets humains. Bull World Health Organ. 1978;56:147–54.PubMedPubMedCentral
20.
go back to reference 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.CrossRef 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.CrossRef
21.
go back to reference Stone W, Gonçalves BP, Bousema T, Drakeley C. Assessing the infectious reservoir of falciparum malaria: past and future. Trends Parasitol. 2015;31:287–96.CrossRefPubMed Stone W, Gonçalves BP, Bousema T, Drakeley C. Assessing the infectious reservoir of falciparum malaria: past and future. Trends Parasitol. 2015;31:287–96.CrossRefPubMed
22.
go back to reference Muirhead-Thomson RC. The distribution of anopheline mosquito bites among different age groups: a new factor in malaria epidemiology. BMJ. 1951;1:1114–7.CrossRefPubMedPubMedCentral Muirhead-Thomson RC. The distribution of anopheline mosquito bites among different age groups: a new factor in malaria epidemiology. BMJ. 1951;1:1114–7.CrossRefPubMedPubMedCentral
23.
go back to reference Bruce MC, Macheso A, Kelly-Hope LA, Nkhoma S, McConnachie A, Molyneux ME. Effect of transmission setting and mixed species infections on clinical measures of malaria in Malawi. PLoS ONE. 2008;3:e2775.CrossRefPubMedPubMedCentral Bruce MC, Macheso A, Kelly-Hope LA, Nkhoma S, McConnachie A, Molyneux ME. Effect of transmission setting and mixed species infections on clinical measures of malaria in Malawi. PLoS ONE. 2008;3:e2775.CrossRefPubMedPubMedCentral
24.
go back to reference Churcher TS, Bousema T, Walker M, Drakeley C, Schneider P, Ouédraogo AL, et al. Predicting mosquito infection from Plasmodium falciparum gametocyte density and estimating the reservoir of infection. Elife. 2013;2:e00626.CrossRefPubMedPubMedCentral Churcher TS, Bousema T, Walker M, Drakeley C, Schneider P, Ouédraogo AL, et al. Predicting mosquito infection from Plasmodium falciparum gametocyte density and estimating the reservoir of infection. Elife. 2013;2:e00626.CrossRefPubMedPubMedCentral
25.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
26.
go back to reference Johnston GL, Smith DL, Fidock DA. Malaria’s missing number: calculating the human component of R0 by a within-host mechanistic model of Plasmodium falciparum infection and transmission. PLoS Comput Biol. 2013;9:e1003025.CrossRefPubMedPubMedCentral Johnston GL, Smith DL, Fidock DA. Malaria’s missing number: calculating the human component of R0 by a within-host mechanistic model of Plasmodium falciparum infection and transmission. PLoS Comput Biol. 2013;9:e1003025.CrossRefPubMedPubMedCentral
27.
go back to reference National Statistical Office. 2008 population and housing census: preliminary report. 2008 (September). National Statistical Office. 2008 population and housing census: preliminary report. 2008 (September).
28.
go back to reference Killeen GF, Smith TA, Ferguson HM, Mshinda H, Abdulla S, Lengeler C, et al. Preventing childhood malaria in Africa by protecting adults from mosquitoes with insecticide-treated nets. PLoS Med. 2007;4:e229.CrossRefPubMedPubMedCentral Killeen GF, Smith TA, Ferguson HM, Mshinda H, Abdulla S, Lengeler C, et al. Preventing childhood malaria in Africa by protecting adults from mosquitoes with insecticide-treated nets. PLoS Med. 2007;4:e229.CrossRefPubMedPubMedCentral
29.
go back to reference Rantala A-M, Taylor SM, Trottman PA, Luntamo M, Mbewe B, Maleta K, et al. Comparison of real-time PCR and microscopy for malaria parasite detection in Malawian pregnant women. Malar J. 2010;9:269.CrossRefPubMedPubMedCentral Rantala A-M, Taylor SM, Trottman PA, Luntamo M, Mbewe B, Maleta K, et al. Comparison of real-time PCR and microscopy for malaria parasite detection in Malawian pregnant women. Malar J. 2010;9:269.CrossRefPubMedPubMedCentral
30.
go back to reference Alano P. Molecular approaches to monitor parasite genetic complexity in the transmission of Plasmodium falciparum malaria. Parassitologia. 2005;47:199–203.PubMed Alano P. Molecular approaches to monitor parasite genetic complexity in the transmission of Plasmodium falciparum malaria. Parassitologia. 2005;47:199–203.PubMed
31.
go back to reference Mwingira F, Genton B, Kabanywanyi ANM, Felger I. Comparison of detection methods to estimate asexual Plasmodium falciparum parasite prevalence and gametocyte carriage in a community survey in Tanzania. Malar J. 2014;13:433.CrossRefPubMedPubMedCentral Mwingira F, Genton B, Kabanywanyi ANM, Felger I. Comparison of detection methods to estimate asexual Plasmodium falciparum parasite prevalence and gametocyte carriage in a community survey in Tanzania. Malar J. 2014;13:433.CrossRefPubMedPubMedCentral
32.
go back to reference Wampfler R, Mwingira F, Javati S, Robinson L, Betuela I, Siba P, et al. Strategies for detection of Plasmodium species gametocytes. PLoS ONE. 2013;8:e76316.CrossRefPubMedPubMedCentral Wampfler R, Mwingira F, Javati S, Robinson L, Betuela I, Siba P, et al. Strategies for detection of Plasmodium species gametocytes. PLoS ONE. 2013;8:e76316.CrossRefPubMedPubMedCentral
33.
go back to reference Drakeley CJ, Secka I, Correa S, Greenwood BM, Targett GAT. Host haematological factors influencing the transmission of Plasmodium falciparum gametocytes to Anopheles gambiae s.s. mosquitoes. Trop Med Int Health. 1999;4:131–8.CrossRefPubMed Drakeley CJ, Secka I, Correa S, Greenwood BM, Targett GAT. Host haematological factors influencing the transmission of Plasmodium falciparum gametocytes to Anopheles gambiae s.s. mosquitoes. Trop Med Int Health. 1999;4:131–8.CrossRefPubMed
34.
go back to reference Tchuinkam T, Mulder B, Dechering K, Stoffels H, Verhave JP, Cot M, et al. Experimental infections of Anopheles gambiae with Plasmodium falciparum of naturally infected gametocyte carriers in Cameroon: factors influencing the infectivity to mosquitoes. Trop Med Parasitol. 1993;44:271–6.PubMed Tchuinkam T, Mulder B, Dechering K, Stoffels H, Verhave JP, Cot M, et al. Experimental infections of Anopheles gambiae with Plasmodium falciparum of naturally infected gametocyte carriers in Cameroon: factors influencing the infectivity to mosquitoes. Trop Med Parasitol. 1993;44:271–6.PubMed
35.
go back to reference Toure YT, Doumbo O, Toure A, Bagayoko M, Diallo M, Dolo A, et al. Gametocyte infectivity by direct mosquito feeds in an area of seasonal malaria transmission: implications for Bancoumana, Mali as a transmission-blocking vaccine site. Am J Trop Med Hyg. 1998;59:481–6.CrossRefPubMed Toure YT, Doumbo O, Toure A, Bagayoko M, Diallo M, Dolo A, et al. Gametocyte infectivity by direct mosquito feeds in an area of seasonal malaria transmission: implications for Bancoumana, Mali as a transmission-blocking vaccine site. Am J Trop Med Hyg. 1998;59:481–6.CrossRefPubMed
36.
go back to reference Draper CC. Observations on the infectiousness of gametocytes in hyperendemic malaria. Trans R Soc Trop Med Hyg. 1953;47:160–5.CrossRefPubMed Draper CC. Observations on the infectiousness of gametocytes in hyperendemic malaria. Trans R Soc Trop Med Hyg. 1953;47:160–5.CrossRefPubMed
37.
go back to reference Graves PM, Burkot TR, Carter R, Cattani JA, Lagog M, Parker J, et al. Measurement of malarial infectivity of human populations to mosquitoes in the Madang area, Papua New Guinea. Parasitology. 1988;96(Pt 2):251–63.CrossRefPubMed Graves PM, Burkot TR, Carter R, Cattani JA, Lagog M, Parker J, et al. Measurement of malarial infectivity of human populations to mosquitoes in the Madang area, Papua New Guinea. Parasitology. 1988;96(Pt 2):251–63.CrossRefPubMed
38.
go back to reference Haji H, Smith T, Charlwood JD, Meuwissen JH. Absence of relationships between selected human factors and natural infectivity of Plasmodium falciparum to mosquitoes in an area of high transmission. Parasitology. 1996;113:425–31.CrossRefPubMed Haji H, Smith T, Charlwood JD, Meuwissen JH. Absence of relationships between selected human factors and natural infectivity of Plasmodium falciparum to mosquitoes in an area of high transmission. Parasitology. 1996;113:425–31.CrossRefPubMed
39.
go back to reference Coleman RE, Kumpitak C, Ponlawat A, Phunkitchar V, Rachapaew N, Zollner G. Infectivity of asymptomatic Plasmodium-infected human populations to Anopheles dirus mosquitoes in Western Thailand. J Med Entomol. 2004;41:201–8.CrossRefPubMed Coleman RE, Kumpitak C, Ponlawat A, Phunkitchar V, Rachapaew N, Zollner G. Infectivity of asymptomatic Plasmodium-infected human populations to Anopheles dirus mosquitoes in Western Thailand. J Med Entomol. 2004;41:201–8.CrossRefPubMed
40.
go back to reference Muirhead-Thomson R. Low gametocyte thresholds of infection of Anopheles with Plasmodium falciparum: a significant factor in malaria epidemiology. BMJ. 1954;1:68–70.CrossRefPubMedPubMedCentral Muirhead-Thomson R. Low gametocyte thresholds of infection of Anopheles with Plasmodium falciparum: a significant factor in malaria epidemiology. BMJ. 1954;1:68–70.CrossRefPubMedPubMedCentral
41.
go back to reference Ouédraogo AL, Bousema T, Schneider P, de Vlas SJ, Ilboudo-Sanogo E, Cuzin-Ouattara N, et al. Substantial contribution of submicroscopical Plasmodium falciparum gametocyte carriage to the infectious reservoir in an area of seasonal transmission. PLoS ONE. 2009;4:e8410.CrossRefPubMedPubMedCentral Ouédraogo AL, Bousema T, Schneider P, de Vlas SJ, Ilboudo-Sanogo E, Cuzin-Ouattara N, et al. Substantial contribution of submicroscopical Plasmodium falciparum gametocyte carriage to the infectious reservoir in an area of seasonal transmission. PLoS ONE. 2009;4:e8410.CrossRefPubMedPubMedCentral
42.
go back to reference 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.PubMed 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.PubMed
43.
go back to reference Mulder B, Tchuinkam T, Dechering K, Verhave JP, Carnevale P, Meuwissen JHET, et al. Malaria transmission-blocking activity in experimental infections of Anopheles gambiae from naturally infected Plasmodium falciparum gametocyte carriers. Trans R Soc Trop Med Hyg. 1994;88:121–5.CrossRefPubMed Mulder B, Tchuinkam T, Dechering K, Verhave JP, Carnevale P, Meuwissen JHET, et al. Malaria transmission-blocking activity in experimental infections of Anopheles gambiae from naturally infected Plasmodium falciparum gametocyte carriers. Trans R Soc Trop Med Hyg. 1994;88:121–5.CrossRefPubMed
Metadata
Title
Simulation models predict that school-age children are responsible for most human-to-mosquito Plasmodium falciparum transmission in southern Malawi
Authors
Jenna E. Coalson
Lauren M. Cohee
Andrea G. Buchwald
Andrew Nyambalo
John Kubale
Karl B. Seydel
Don Mathanga
Terrie E. Taylor
Miriam K. Laufer
Mark L. Wilson
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2018
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-018-2295-4

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