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RefWorks
Reference Manager
BibTeX
Zotero
EndNote
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Insights into Plasmodium vivax Asymptomatic Malaria Infections and Direct Skin-Feeding Assays to Assess Onward Malaria Transmission in the Amazon
Marta Moreno
Marta Moreno
Department of Biology, London School of Hygiene and Tropical Medicine, London, UK;
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Katherine Torres
Katherine Torres
Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Peru;
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Carlos Tong
Carlos Tong
Laboratorio ICEMR-Amazonia, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru;
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Stefano S. García Castillo
Stefano S. García Castillo
Laboratorio de Malaria, Parásitos y Vectores, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru;
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Gabriel Carrasco-Escobar
Gabriel Carrasco-Escobar
Facultad de Salud Pública, Universidad Peruana Cayetano Heredia, Lima, Peru;
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Gerson Guedez
Gerson Guedez
Laboratorio ICEMR-Amazonia, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru;
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Lutecio Torres
Lutecio Torres
Laboratorio ICEMR-Amazonia, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru;
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Manuela Herrera-Varela
Manuela Herrera-Varela
Laboratorio ICEMR-Amazonia, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru;
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Layné Guerra
Layné Guerra
Laboratorio ICEMR-Amazonia, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru;
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Mitchel Guzman-Guzman
Mitchel Guzman-Guzman
Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Peru;
Laboratorio ICEMR-Amazonia, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru;
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Laboratorio ICEMR-Amazonia, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru;
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Daniel Wong
Daniel Wong
Laboratorio ICEMR-Amazonia, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru;
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Roberson Ramirez
Roberson Ramirez
Laboratorio ICEMR-Amazonia, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru;
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Alejandro Llanos-Cuentas
Alejandro Llanos-Cuentas
Facultad de Salud Pública, Universidad Peruana Cayetano Heredia, Lima, Peru;
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Jan E. Conn
Jan E. Conn
Department of Biomedical Sciences, School of Public Health, University at Albany–State University of New York, Albany, New York;
Wadsworth Center, New York State Department of Health, Albany, New York;
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Wadsworth Center, New York State Department of Health, Albany, New York;
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Dionicia Gamboa
Dionicia Gamboa
Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Peru;
Laboratorio de Malaria, Parásitos y Vectores, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru;
Departamento de Ciencias Celulares y Moleculares, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru;
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Laboratorio de Malaria, Parásitos y Vectores, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru;
Departamento de Ciencias Celulares y Moleculares, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru;
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Joseph M. Vinetz
Joseph M. Vinetz
Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Peru;
S Division of Infectious Diseases, Department of Medicine, University of California San Diego, La Jolla, California;
Section of Infectious Diseases, Department of Internal Medicine, Yale School of Medicine, New Haven, Connecticut
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S Division of Infectious Diseases, Department of Medicine, University of California San Diego, La Jolla, California;
Section of Infectious Diseases, Department of Internal Medicine, Yale School of Medicine, New Haven, Connecticut
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ABSTRACT.
Understanding the reservoir and infectivity of Plasmodium gametocytes to vector mosquitoes is crucial to align strategies aimed at malaria transmission elimination. Yet, experimental information is scarce regarding the infectivity of Plasmodium vivax for mosquitoes in diverse epidemiological settings where the proportion of asymptomatically infected individuals varies at a microgeographic scale. We measured the transmissibility of clinical and subclinical P. vivax malaria parasite carriers to the major mosquito vector in the Amazon Basin, Nyssorhynchus darlingi (formerly Anopheles). A total of 105 participants with natural P. vivax malaria infection were recruited from a cohort study in Loreto Department, Peruvian Amazon. Four of 18 asymptomatic individuals with P. vivax positivity by blood smear infected colony-grown Ny. darlingi (22%), with 2.6% (19 of 728) mosquitoes infected. In contrast, 77% (44/57) of symptomatic participants were infectious to mosquitoes with 51% (890 of 1,753) mosquitoes infected. Infection intensity was greater in symptomatic infections (mean, 17.8 oocysts/mosquito) compared with asymptomatic infections (mean, 0.28 oocysts/mosquito), attributed to parasitemia/gametocytemia level. Paired experiments (N = 27) using direct skin-feeding assays and direct membrane mosquito-feeding assays showed that infectivity to mosquitoes was similar for both methods. Longitudinal studies with longer follow-up of symptomatic and asymptomatic parasite infections are needed to determine the natural variations of disease transmissibility.
- Supplemental Materials (PDF 179 KB)
Author Notes
These authors contributed equally to this work.
Financial support: This research was funded by NIH National Institute of Allergy and Infectious Diseases (NIAID) (U19AI089681) to J. M. V. and was funded in part by NIH-NIAID (R01AI110112) to J. E. C.
Authors’ addresses: Marta Moreno, Department of Infection Biology, London School of Hygiene & Tropical Medicine, London, UK, E-mail: marta.moreno@lshtm.ac.uk. Katherine Torres, Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Peru, E-mail: katherine.torres.f@upch.pe. Carlos Tong, Gerson Guedez, Lutecio Torres, Manuela Herrera-Varela, Layné Guerra, Mitchel Guzman, Daniel Wong, and Roberson Ramirez, Laboratorio ICEMR-Amazonia, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru, E-mails: ctong32@gmail.com, gersonerick@hotmail.es, eddie.torres.t@upch.pe, manuelahv82@gmail.com, laygueva.12@gmail.com, guzman.mitch@gmail.com, danielantonio@outlook.com.pe, and roberson.ramirez.s@upch.pe. Stefano S. García Castillo, Laboratorio de Malaria, Parásitos y Vectores, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru, E-mail: stefano.garcia.c@upch.pe. Gabriel Carrasco-Escobar and Alejandro Llanos-Cuentas, Department of Epidemiology, University of California San Diego, La Jolla, CA, E-mails: gabriel.carrasco@upch.pe and alejandro.llanos.c@upch.pe. Jan E. Conn, Department of Biomedical Sciences, School of Public Health, University at Albany–State University of New York, Albany, NY, and Wadsworth Center, New York State Department of Health, Albany, NY, E-mail: jan.conn@health.ny.gov. Dionicia Gamboa, Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Peru, Laboratorio de Malaria, Parásitos y Vectores, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru, and Departamento de Ciencias Celulares y Moleculares, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru, E-mail: dionigamboa@yahoo.com. Joseph M. Vinetz, Division of Infectious Diseases, Department of Medicine, University of California San Diego, La Jolla, CA, Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Peru, and Section of Infectious Diseases, Department of Internal Medicine, Yale School of Medicine, New Haven, CT, E-mail: joseph.vinetz@yale.edu.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization , 2020. World Malaria Report. Geneva, Switzerland: WHO.
-
2.
Krotoski WA, 1989. The hypnozoite and malarial relapse. Prog Clin Parasitol 1: 1–19.
-
3.
Adams JH, Mueller I, 2017. The biology of Plasmodium vivax. Cold Spring Harb Perspect Med 7: a025585.
-
4.
Bousema T, Drakeley C, 2011. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev 24: 377–410.
-
5.
Vallejo AF, García J, Amado-Garavito AB, Arévalo-Herrera M, Herrera S, 2016. Plasmodium vivax gametocyte infectivity in sub-microscopic infections. Malar J 15: 48.
-
6.
Collins KA et al., 2020. A Plasmodium vivax experimental human infection model for evaluating efficacy of interventions. J Clin Invest 130: 2920–2927.
-
7.
Smalley ME, Brown J, Bassett NM, 1981. The rate of production of Plasmodium falciparum gametocytes during natural infections. Trans R Soc Trop Med Hyg 75: 318–319.
-
8.
Schneider P, Greischar MA, Birget PLG, Repton C, Mideo N, Reece SE, 2018. Adaptive plasticity in the gametocyte conversion rate of malaria parasites. PLoS Pathog 14: e1007371.
-
9.
Lefèvre T, Vantaux A, Dabiré KR, Mouline K, Cohuet A, 2013. Non-genetic determinants of mosquito competence for malaria parasites. PLoS Pathog 9: e1003365.
-
10.
Tadesse FG, Meerstein-Kessel L, Gonçalves BP, Drakeley C, Ranford-Cartwright L, Bousema T, 2019. Gametocyte sex ratio: the key to understanding Plasmodium falciparum transmission? Trends Parasitol 35: 226–238.
-
11.
Boyd MF, Stratman-Thomas WK, Kitchen SF, 1935. On the relative susceptibility of Anopheles quadrimaculatus to Plasmodium vivax and Plasmodium falciparum .Am J Trop Med Hyg 15: 485–493.
-
12.
Abeles SR, Chuquiyauri R, Tong C, Vinetz JM, 2013. Human host-derived cytokines associated with Plasmodium vivax transmission from acute malaria patients to Anopheles darlingi mosquitoes in the Peruvian Amazon. Am J Trop Med Hyg 88: 1130–1137.
-
13.
Meibalan E, Marti M, 2017. Biology of malaria transmission. Cold Spring Harb Perspect Med 7: a025452.
-
14.
Bennink S, Kiesow MJ, Pradel G, 2016. The development of malaria parasites in the mosquito midgut. Cell Microbiol 18: 905–918.
-
15.
Bradley J et al., 2018. Predicting the likelihood and intensity of mosquito infection from sex specific Plasmodium falciparum gametocyte density. eLife 7: e34463.
-
16.
Bansal GP, Weinstein CS, Kumar N, 2016. Insight into phagocytosis of mature sexual (gametocyte) stages of Plasmodium falciparum using a human monocyte cell line. Acta Trop 157: 96–101.
-
17.
Clayton AM, Dong Y, Dimopoulos G, 2014. The Anopheles innate immune system in the defense against malaria infection. J Innate Immunol 6: 169–181.
-
18.
Molina-Cruz A, Zilversmit MM, Neafsey DE, Hartl DL, Barillas-Mury C, 2016. Mosquito vectors and the globalization of Plasmodium falciparum malaria. Annu Rev Genet 50: 447–465.
-
19.
Kiattibutr K et al., 2017. Infectivity of symptomatic and asymptomatic Plasmodium vivax infections to a southeast Asian vector, Anopheles dirus. Int J Parasitol 47: 163–170.
-
20.
Bousema T et al., 2012. Mosquito feeding assays to determine the infectiousness of naturally infected Plasmodium falciparum gametocyte carriers. PLoS One 7: e42821.
-
21.
Andolina C et al., 2021. Sources of persistent malaria transmission in a setting with effective malaria control in eastern Uganda: a longitudinal, observational cohort study. Lancet Infect Dis 21: 1568–1578.
-
22.
Muirhead-Thomson RC, 1957. The malarial infectivity of an African village population to mosquitoes (Anopheles gambiae): a random xenodiagnostic survey. Am J Trop Med Hyg 6: 971–979.
-
23.
Bonnet S, Gouagna C, Safeukui I, Meunier JY, Boudin C, 2000. Comparison of artificial membrane feeding with direct skin feeding to estimate infectiousness of Plasmodium falciparum gametocyte carriers to mosquitoes. Trans R Soc Trop Med Hyg 94: 103–106.
-
24.
Diallo M et al., 2008. Evaluation and optimization of membrane feeding compared to direct feeding as an assay for infectivity. Malar J 7: 248.
-
25.
Sattabongkot J, Maneechai N, Phunkitchar V, Eikarat N, Khuntirat B, Sirichaisinthop J, Burge R, Coleman RE, 2003. Comparison of artificial membrane feeding with direct skin feeding to estimate the infectiousness of Plasmodium vivax gametocyte carriers to mosquitoes. Am J Trop Med Hyg 69: 529–535.
-
26.
Rosas-Aguirre A, Guzman-Guzman M, Gamboa D, Chuquiyauri R, Ramirez R, Manrique P, Carrasco-Escobar G, Puemape C, Llanos-Cuentas A, Vinetz JM, 2017. Micro-heterogeneity of malaria transmission in the Peruvian Amazon: a baseline assessment underlying a population-based cohort study. Malar J 16: 312.
-
27.
Rovira-Vallbona E, Contreras-Mancilla JJ, Ramirez R, Guzmán-Guzmán M, Carrasco-Escobar G, Llanos-Cuentas A, Vinetz JM, Gamboa D, Rosanas-Urgell A, 2017. Predominance of asymptomatic and sub-microscopic infections characterizes the Plasmodium gametocyte reservoir in the Peruvian Amazon. PLoS Negl Trop Dis 11: e0005674.
-
28.
Lin JT, Saunders DL, Meshnick SR, 2014. The role of submicroscopic parasitemia in malaria transmission: what is the evidence? Trends Parasitol 30: 183–190.
-
29.
Recker M, Bull PC, Buckee CO, 2018. Recent advances in the molecular epidemiology of clinical malaria. F1000Research 7: 1159.
-
30.
Ministerio de Salud del Perú (MINSA) , 2010. Norma Técnica de Salud para el Control de Calidad del Diagnóstico Microscópico de Malaria. Lima, Peru: MINSA.
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