Plasmodium vivax: gametócitos e estratégias para o bloqueio de transmissão

Plasmodium vivax: gametocytes and strategies to block transmission

Authors

  • Lorena Pessoa da Costa Silva
  • Glenda Quaresma Ramos

DOI:

https://doi.org/10.34117/bjdv8n9-122

Keywords:

Malária vivax, gametócitos, bloqueio de transmissão, vacinas, drogas

Abstract

A malária é uma doença causada por parasitas do gênero Plasmodium. Considerada um grave problema de saúde pública, a malária está presente em diversos países tropicais e subtropicais, colocando em risco mais da metade da população mundial. Plasmodium vivax é uma das espécies causadoras da malária ao homem e é a das que apresenta maior distribuição geográfica no mundo e, devido a seus aspectos biológicos, tem se tornado um grande desafio em meio a um cenário de eliminação. Os gametócitos são as formas responsáveis pela transmissão do Plasmodium ao vetor, as fêmeas do mosquito Anopheles. Avanços nos estudos da biologia e dinâmica dos gametócitos em P. falciparum, se tornaram possíveis após o estabelecimento de um sistema de cultivo in vitro e modelos experimentais. No entanto, a ausência dessas metodologias para P. vivax tem dificultado o avanço nas pesquisas. Atualmente, diversos estudos e programas tem focado na eliminação da malária e, para alcançar esse sucesso é necessário um conhecimento e compreensão dos estágios envolvidos na transmissão, como os gametócitos. Aqui apresentamos os principais avanços no estudo de gametócitos de P. vivax novas perspectivas no desenvolvimento das ferramentas necessárias para a investigação de agentes para bloquear a transmissão.

References

Arévalo-Herrera, M., Miura, K., Cespedes, N., Echeverry, C., Solano, E., Castellanos, A., Ramirez, J. S., Miranda, A., Kajava, A. V., Long, C., Corradin, G., & Herrera, S. (2021). Immunoreactivity of Sera From Low to Moderate Malaria-Endemic Areas Against Plasmodium vivax rPvs48/45 Proteins Produced in Escherichia coli and Chinese Hamster Ovary Systems. Frontiers in Immunology, 12, 2252. https://doi.org/10.3389/FIMMU.2021.634738/BIBTEX

Arévalo-Herrera, M., Vallejo, A. F., Rubiano, K., Solarte, Y., Marin, C., Castellanos, A., Céspedes, N., & Herrera, S. (2015). Recombinant Pvs48/45 Antigen Expressed in E. coli Generates Antibodies that Block Malaria Transmission in Anopheles albimanus Mosquitoes. PLOS ONE, 10(3), e0119335. https://doi.org/10.1371/JOURNAL.PONE.0119335

Bantuchai, S., Imad, H., & Nguitragool, W. (2022). Plasmodium vivax gametocytes and transmission. Parasitology International, 87, 102497. https://doi.org/10.1016/J.PARINT.2021.102497

Baro, B., Deroost, K., Raiol, T., Brito, M., Almeida, A. C. G., De Menezes-Neto, A., Figueiredo, E. F. G., Alencar, A., Leitão, R., Val, F., Monteiro, W., Oliveira, A., Del Pilar Armengol, M., Ferná Ndez-Becerra, C., Lacerda, M. V, & Del Portillo, H. A. (2017). Plasmodium vivax gametocytes in the bone marrow of an acute malaria patient and changes in the erythroid miRNA profile. https://doi.org/10.1371/journal.pntd.0005365

Bassat, Q. (2011). The Use of Artemether-Lumefantrine for the Treatment of Uncomplicated Plasmodium vivax Malaria. PLOS Neglected Tropical Diseases, 5(12), e1325. https://doi.org/10.1371/JOURNAL.PNTD.0001325

Blagborough, A. M., Musiychuk, K., Bi, H., Jones, R. M., Chichester, J. A., Streatfield, S., Sala, K. A., Zakutansky, S. E., Upton, L. M., Sinden, R. E., Brian, I., Biswas, S., Sattabonkot, J., & Yusibov, V. (2016). Transmission blocking potency and immunogenicity of a plant-produced Pvs25-based subunit vaccine against Plasmodium vivax. Vaccine, 34(28), 3252–3259. https://doi.org/10.1016/J.VACCINE.2016.05.007

Bousema, T., Dinglasan, R. R., Morlais, I., Gouagna, L. C., van Warmerdam, T., Awono-Ambene, P. H., Bonnet, S., Diallo, M., Coulibaly, M., Tchuinkam, T., Mulder, B., Targett, G., Drakeley, C., Sutherland, C., Robert, V., Doumbo, O., Touré, Y., Graves, P. M., Roeffen, W., … Churcher, T. S. (2012). Mosquito Feeding Assays to Determine the Infectiousness of Naturally Infected Plasmodium falciparum Gametocyte Carriers. PLoS ONE, 7(8), e42821. https://doi.org/10.1371/journal.pone.0042821

Bousema, T., & Drakeley, C. (2011). Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. In Clinical Microbiology Reviews (Vol. 24, Issue 2, pp. 377–410). Clin Microbiol Rev. https://doi.org/10.1128/CMR.00051-10

Bozdech, Z., Mok, S., Hu, G., Imwong, M., Jaidee, A., Russell, B., Ginsburg, H., Nosten, F., Day, N. P. J., White, N. J., Carlton, J. M., & Preiser, P. R. (2008). The transcriptome of Plasmodium vivax reveals divergence and diversity of transcriptional regulation in malaria parasites. Proceedings of the National Academy of Sciences of the United States of America, 105(42), 16290–16295. https://doi.org/10.1073/pnas.0807404105

Campbell, T. L., de Silva, E. K., Olszewski, K. L., Elemento, O., & Llinás, M. (2010). Identification and Genome-Wide Prediction of DNA Binding Specificities for the ApiAP2 family of regulators from the malaria parasite. PLoS Pathogens, 6(10). https://doi.org/10.1371/journal.ppat.1001165

Canepa, G. E., Molina-Cruz, A., Yenkoidiok-Douti, L., Calvo, E., Williams, A. E., Burkhardt, M., Peng, F., Narum, D., Boulanger, M. J., Valenzuela, J. G., & Barillas-Mury, C. (2018). Antibody targeting of a specific region of Pfs47 blocks Plasmodium falciparum malaria transmission. Npj Vaccines 2018 3:1, 3(1), 1–9. https://doi.org/10.1038/s41541-018-0065-5

Cao, Y., Hart, R. J., Bansal, G. P., & Kumar, N. (2018). Functional conservation of P48/45 proteins in the transmission stages of Plasmodium vivax (Human malaria parasite) and P. berghei (Murine Malaria Parasite). MBio, 9(5). https://doi.org/10.1128/MBIO.01627-18/SUPPL_FILE/MBO004184050SF3.TIF

Douglas, N. M., Simpson, J. A., Phyo, A. P., Siswantoro, H., Hasugian, A. R., Kenangalem, E., Poespoprodjo, J. R., Singhasivanon, P., Anstey, N. M., White, N. J., Tjitra, E., Nosten, F., & Price, R. N. (2013). Gametocyte dynamics and the role of drugs in reducing the transmission potential of plasmodium vivax. Journal of Infectious Diseases, 208(5), 801–812. https://doi.org/10.1093/infdis/jit261

Fabbri, C., Trindade, A. O., Andrade, F. S., Souza, M. F. de, Ríos-Velásquez, C. M., Lacerda, M. V. G. de, Monteiro, W. M., Costa, F. T. M., Amino, R., & Lopes, S. C. P. (2021). Transmission-blocking compound candidates against Plasmodium vivax using P. berghei as an initial screening. Memorias Do Instituto Oswaldo Cruz, 116, e200513. https://doi.org/10.1590/0074-02760200513

Florens, L., Washburn, M. P., Dale Raine, J., Anthony, R. M., Graingerk, M., David Haynes, J., Kathleen Moch, J., Muster, N., Sacci, J. B., Tabb, D. L., Witney, A. A., Wolters, D., Wu, Y., Gardner, M. J., Holderk, A. A., Sinden, R. E., Yates, J. R., & Carucci, D. J. (2002). A proteomic view of the Plasmodium falciparum life cycle.

Grüring, C., Moon, R. W., Lim, C., Holder, A. A., Blackman, M. J., & Duraisingh, M. T. (2014). Human red blood cell-adapted Plasmodium knowlesi parasites: a new model system for malaria research. Cellular Microbiology, 16(5), 612–620. https://doi.org/10.1111/CMI.12275

Handayani, S., Chiu, D. T., Tjitra, E., Kuo, J. S., Lampah, D., Kenangalem, E., Renia, L., Snounou, G., Price, R. N., Anstey, N. M., & Russell, B. (2009). High Deformability of Plasmodium vivax–Infected Red Blood Cells under Microfluidic Conditions. The Journal of Infectious Diseases, 199(3), 445. https://doi.org/10.1086/596048

Hisaeda, H., Stowers, A. W., Tsuboi, T., Collins, W. E., Sattabongkot, J. S., Suwanabun, N., Torii, M., & Kaslow, D. C. (2000). Antibodies to malaria vaccine candidates Pvs25 and Pvs28 completely block the ability of plasmodium vivax to infect mosquitoes. Infection and Immunity, 68(12), 6618–6623. https://doi.org/10.1128/IAI.68.12.6618-6623.2000/ASSET/FB77FF75-5B09-47A3-95A1-3BE649E295B2/ASSETS/GRAPHIC/II1201025005.JPEG

Kafsack, B. F. C., Rovira-Graells, N., Clark, T. G., Bancells, C., Crowley, V. M., Campino, S. G., Williams, A. E., Drought, L. G., Kwiatkowski, D. P., Baker, D. A., Cortés, A., & Llinás, M. (2014). A transcriptional switch underlies commitment to sexual development in malaria parasites. Nature, 507(7491), 248–252. https://doi.org/10.1038/nature12920

Kobylinski, K. C., Ubalee, R., Ponlawat, A., Nitatsukprasert, C., Phasomkulsolsil, S., Wattanakul, T., Tarning, J., Na-Bangchang, K., McCardle, P. W., Davidson, S. A., & Richardson, J. H. (2017). Ivermectin susceptibility and sporontocidal effect in Greater Mekong Subregion Anopheles. Malaria Journal, 16(1), 1–13. https://doi.org/10.1186/S12936-017-1923-8/FIGURES/8

Kocken, C. H. M., Ozwara, H., Van der Wel, A., Beetsma, A. L., Mwenda, J. M., & Thomas, A. W. (2002). Plasmodium knowlesi provides a rapid in vitro and in vivo transfection system that enables double-crossover gene knockout studies. Infection and Immunity, 70(2), 655–660. https://doi.org/10.1128/IAI.70.2.655-660.2002/ASSET/45399389-8B21-495D-A2E1-B01D207CC37D/ASSETS/GRAPHIC/II0221022003.JPEG

Kosasih, A., Koepfli, C., Dahlan, M. S., Hawley, W. A., Baird, J. K., Mueller, I., Lobo, N. F., & Sutanto, I. (2021). Gametocyte carriage of Plasmodium falciparum (pfs25) and Plasmodium vivax (pvs25) during mass screening and treatment in West Timor, Indonesia: a longitudinal prospective study. Malaria Journal, 20(1), 177. https://doi.org/10.1186/s12936-021-03709-y

Leba, L.-J., Musset, L., Pelleau, S., Estevez, Y., Birer, C., Briolant, S., Witkowski, B., Ménard, D., Delves, M. J., Legrand, E., Duplais, C., & Popovici, J. (2015). Use of Plasmodium falciparum culture-adapted field isolates for in vitro exflagellation-blocking assay. Malaria Journal, 14(1), 234. https://doi.org/10.1186/s12936-015-0752-x

Malkin, E. M., Durbin, A. P., Diemert, D. J., Sattabongkot, J., Wu, Y., Miura, K., Long, C. A., Lambert, L., Miles, A. P., Wang, J., Stowers, A., Miller, L. H., & Saul, A. (2005). Phase 1 vaccine trial of Pvs25H: a transmission blocking vaccine for Plasmodium vivax malaria. Vaccine, 23(24), 3131–3138. https://doi.org/10.1016/J.VACCINE.2004.12.019

Malleret, B., Li, A., Zhang, R., Tan, K. S. W., Suwanarusk, R., Claser, C., Cho, J. S., Koh, E. G. L., Chu, C. S., Pukrittayakamee, S., Ng, M. L., Ginhoux, F., Ng, L. G., Lim, C. T., Nosten, F., Snounou, G., Rénia, L., & Russell, B. (2015). Plasmodium vivax: restricted tropism and rapid remodeling of CD71-positive reticulocytes. Blood, 125(8), 1314. https://doi.org/10.1182/BLOOD-2014-08-596015

Mayor, A., & Alano, P. (2015). Bone marrow reticulocytes: a Plasmodium vivax affair? Blood, 125(8), 1203–1205. https://doi.org/10.1182/BLOOD-2014-12-614123

McCaffery, J. N., Fonseca, J. A., Singh, B., Cabrera-Mora, M., Bohannon, C., Jacob, J., Arévalo-Herrera, M., & Moreno, A. (2019). A multi-stage plasmodium vivax malaria vaccine candidate able to induce long-lived antibody responses against blood stage parasites and robust transmission-blocking activity. Frontiers in Cellular and Infection Microbiology, 9(MAY), 135. https://doi.org/10.3389/FCIMB.2019.00135/BIBTEX

Miles, A. P., Zhang, Y., Saul, A., & Stowers, A. W. (2002). Large-Scale Purification and Characterization of Malaria Vaccine Candidate Antigen Pvs25H for Use in Clinical Trials. Protein Expression and Purification, 25(1), 87–96. https://doi.org/10.1006/PREP.2001.1613

Miura, K., Tachibana, M., Takashima, E., Morita, M., Kanoi, B. N., Nagaoka, H., Baba, M., Torii, M., Ishino, T., & Tsuboi, T. (2019). Malaria transmission-blocking vaccines: wheat germ cell-free technology can accelerate vaccine development. Https://Doi.Org/10.1080/14760584.2019.1674145, 18(10), 1017–1027. https://doi.org/10.1080/14760584.2019.1674145

Moon, R. W., Hall, J., Rangkuti, F., Ho, Y. S., Almond, N., Mitchell, G. H., Pain, A., Holder, A. A., & Blackman, M. J. (2013). Adaptation of the genetically tractable malaria pathogen Plasmodium knowlesi to continuous culture in human erythrocytes. Proceedings of the National Academy of Sciences of the United States of America, 110(2), 531–536. https://doi.org/10.1073/PNAS.1216457110/SUPPL_FILE/PNAS.201216457SI.PDF

Nacher, M., Silachamroon, U., Singhasivanon, P., Wilairatana, P., Phumratanaprapin, W., Fontanet, A., & Looareesuwan, S. (2004). Comparison of artesunate and chloroquine activities against Plasmodium vivax gametocytes. Antimicrobial Agents and Chemotherapy, 48(7), 2751–2752. https://doi.org/10.1128/AAC.48.7.2751-2752.2004

Painter, H. J., Campbell, T. L., & Llinás, M. (2011). The Apicomplexan AP2 family: Integral factors regulating Plasmodium development. Molecular and Biochemical Parasitology, 176(1), 1–7. https://doi.org/10.1016/j.molbiopara.2010.11.014

Penna-Coutinho, J., da Silva Araújo, M., Campos Aguiar, A. C., Sá, P. M., Rios, C. T., Medeiros, J. F., Pereira, D. B., Boechat, N., & Krettli, A. U. (2021). MEFAS, a hybrid of artesunate-mefloquine active against asexual stages of Plasmodium vivax in field isolates, inhibits malaria transmission. International Journal for Parasitology: Drugs and Drug Resistance, 17, 150–155. https://doi.org/10.1016/J.IJPDDR.2021.09.003

Pereira-Silva, J. W., Martins-Campos, K. M., Sabrina dos Reis Martins, E., de Souza Menezes, A., Guimarães Lacerda, M. V., Costa Pessoa, F. A., & Ríos-Velásquez, C. M. (2021). Long-lasting infectivity of Plasmodium vivax present in malarial patient blood to Anopheles aquasalis. Experimental Parasitology, 108064. https://doi.org/10.1016/j.exppara.2021.108064

Pinilla, Y. T., C. P. Lopes, S., S. Sampaio, V., Andrade, F. S., Melo, G. C., Orfanó, A. S., Secundino, N. F. C., Guerra, M. G. V. B., Lacerda, M. V. G., Kobylinski, K. C., Escobedo-Vargas, K. S., López-Sifuentes, V. M., Stoops, C. A., Baldeviano, G. C., Tarning, J., Vasquez, G. M., Pimenta, P. F. P., & Monteiro, W. M. (2018). Promising approach to reducing Malaria transmission by ivermectin: Sporontocidal effect against Plasmodium vivax in the South American vectors Anopheles aquasalis and Anopheles darlingi. PLOS Neglected Tropical Diseases, 12(2), e0006221. https://doi.org/10.1371/JOURNAL.PNTD.0006221

Ponsa, N., Sattabongkot, J., Kittayapong, P., Eikarat, N., & Coleman, R. E. (2003). Transmission-blocking activity of tafenoquine (WR-238605) and artelinic acid against naturally circulating strains of plasmodium vivax in Thailand. American Journal of Tropical Medicine and Hygiene, 69(5), 542–547. https://doi.org/10.4269/ajtmh.2003.69.542

Popovici, J., Vantaux, A., Primault, L., Samreth, R., Piv, E. P., Bin, S., Kim, S., Lek, D., Serre, D., & Menard, D. (2018). Therapeutic and transmission-blocking efficacy of dihydroartemisinin/ piperaquine and chloroquine against Plasmodium vivax Malaria, Cambodia. Emerging Infectious Diseases, 24(8), 1516–1519. https://doi.org/10.3201/eid2408.170768

Pukrittayakamee, S, Imwong, M., Singhasivanon, P., Stepniewska, K., Day, N., & White, N. J. (2008). Effects of different antimalarial drugs on gametocyte carriage in P. vivax malaria. Am J Trop Med Hyg, 79(3), 378–384.

Pukrittayakamee, Sasithon, Chotivanich, K., Chantra, A., Clemens, R., Looareesuwan, S., & White, N. J. (2004). Activities of Artesunate and Primaquine against Asexual- and Sexual-Stage Parasites in Falciparum Malaria. Antimicrobial Agents and Chemotherapy, 48(4), 1329–1334. https://doi.org/10.1128/AAC.48.4.1329-1334.2004

Qiu, Y., Zhao, Y., Liu, F., Ye, B., Zhao, Z., Thongpoon, S., Roobsoong, W., Sattabongkot, J., Cui, L., Fan, Q., & Cao, Y. (2020). Evaluation of Plasmodium vivax HAP2 as a transmission-blocking vaccine candidate. Vaccine, 38(13), 2841–2848. https://doi.org/10.1016/J.VACCINE.2020.02.011

Ramjanee, S., Robertson, J. S., Franke-Fayard, B., Sinha, R., Waters, A. P., Janse, C. J., Wu, Y., Blagborough, A. M., Saul, A., & Sinden, R. E. (2007). The use of transgenic Plasmodium berghei expressing the Plasmodium vivax antigen P25 to determine the transmission-blocking activity of sera from malaria vaccine trials. Vaccine, 25(5), 886–894. https://doi.org/10.1016/J.VACCINE.2006.09.035

Sà, J. M., Cannon, M. V., Caleon, R. L., Wellems, T. E., & Serre, D. (2020). Single-cell transcription analysis of Plasmodium vivax blood-stage parasites identifies stage- and species-specific profiles of expression. PLOS Biology, 18(5), e3000711. https://doi.org/10.1371/JOURNAL.PBIO.3000711

Salazar Alvarez, L. C., Vera Lizcano, O., da Silva Barros, D. K. A., Baia-da-Silva, D. C., Monteiro, W. M., Pimenta, P. F. P., de Lacerda, M. V. G., Costa, F. T. M., & Lopes, S. C. P. (2021). Plasmodium vivax Gametocytes Adherence to Bone Marrow Endothelial Cells. Frontiers in Cellular and Infection Microbiology, 11, 357. https://doi.org/10.3389/FCIMB.2021.614985/BIBTEX

Sattabongkot, J., Tsuboi, T., Hisaeda, H., Tachibana, M., Suwanabun, N., Rungruang, T., Cao, Y. M., Stowers, A. W., Sirichaisinthop, J., Coleman, R. E., & Torii, M. (2003). BLOCKING OF TRANSMISSION TO MOSQUITOES BY ANTIBODY TO PLASMODIUM VIVAX MALARIA VACCINE CANDIDATES PVS25 AND PVS28 DESPITE ANTIGENIC POLYMORPHISM IN FIELD ISOLATES. The American Journal of Tropical Medicine and Hygiene, 69(5), 536–541. https://doi.org/10.4269/AJTMH.2003.69.536

Schäfer, C., Roobsoong, W., Kangwanrangsan, N., Bardelli, M., Rawlinson, T. A., Dambrauskas, N., Trakhimets, O., Parthiban, C., Goswami, D., Reynolds, L. M., Kennedy, S. Y., Flannery, E. L., Murphy, S. C., Sather, D. N., Draper, S. J., Sattabongkot, J., Mikolajczak, S. A., & Kappe, S. H. I. (2020). A Humanized Mouse Model for Plasmodium vivax to Test Interventions that Block Liver Stage to Blood Stage Transition and Blood Stage Infection. IScience, 23(8), 101381. https://doi.org/10.1016/J.ISCI.2020.101381

Sinha, A., Hughes, K. R., Modrzynska, K. K., Otto, T. D., Pfander, C., Dickens, N. J., Religa, A. A., Bushell, E., Graham, A. L., Cameron, R., Kafsack, B. F. C., Williams, A. E., Llinás, M., Berriman, M., Billker, O., & Waters, A. P. (2014). A cascade of DNA-binding proteins for sexual commitment and development in Plasmodium. Nature, 507(7491), 253–257. https://doi.org/10.1038/nature12970

Tachibana, M., Sato, C., Otsuki, H., Sattabongkot, J., Kaneko, O., Torii, M., & Tsuboi, T. (2012). Plasmodium vivax gametocyte protein Pvs230 is a transmission-blocking vaccine candidate. Vaccine, 30(10), 1807–1812. https://doi.org/10.1016/J.VACCINE.2012.01.003

Tachibana, M., Wu, Y., Iriko, H., Muratova, O., MacDonald, N. J., Sattabongkot, J., Takeo, S., Otsuki, H., Torii, M., & Tsuboi, T. (2011). N-terminal prodomain of Pfs230 synthesized using a cell-free system is sufficient to induce complement-dependent malaria transmission-blocking activity. Clinical and Vaccine Immunology, 18(8), 1343–1350. https://doi.org/10.1128/CVI.05104-11/ASSET/A11E6A26-57FA-40D0-907C-5D18460608FA/ASSETS/GRAPHIC/ZCD9990941930006.JPEG

Theisen, M., Jore, M. M., & Sauerwein, R. (2017). Towards clinical development of a Pfs48/45-based transmission blocking malaria vaccine. Http://Dx.Doi.Org/10.1080/14760584.2017.1276833, 16(4), 329–336. https://doi.org/10.1080/14760584.2017.1276833

Tsuboi, T., Kaslow, D. C., Gozar, M. M. G., Tachibana, M., Cao, Y. M., & Torii, M. (1998). Sequence polymorphism in two novel Plasmodium vivax ookinete surface proteins, Pvs25 and Pvs28, that are malaria transmission-blocking vaccine candidates. Molecular Medicine, 4(12), 772–782. https://doi.org/10.1007/BF03401770/FIGURES/4

Vallejo, A. F., Rubiano, K., Amado, A., Krystosik, A. R., Herrera, S., & Arévalo-Herrera, M. (2016). Optimization of a Membrane Feeding Assay for Plasmodium vivax Infection in Anopheles albimanus. PLoS Neglected Tropical Diseases, 10(6). https://doi.org/10.1371/journal.pntd.0004807

Venugopal, K., Hentzschel, F., Valkiūnas, G., & Marti, M. (2020). Plasmodium asexual growth and sexual development in the haematopoietic niche of the host. In Nature Reviews Microbiology (Vol. 18, Issue 3, pp. 177–189). Nature Research. https://doi.org/10.1038/s41579-019-0306-2

Vera, O., De Brito, P. B., Albrecht, L., Martins-Campos, K. M., Pimenta, P. F. P., Monteiro, W. M., Lacerda, M. V. G., Lopes, S. C. P., & Costa, F. T. M. (2015). Purification methodology for viable and infective Plasmodium vivax gametocytes that is compatible with transmission-blocking assays. Antimicrobial Agents and Chemotherapy, 59(10), 6638–6641. https://doi.org/10.1128/AAC.01136-15

Wampfler, R., Hofmann, N. E., Karl, S., Betuela, I., Kinboro, B., Lorry, L., Silkey, M., Robinson, L. J., Mueller, I., & Felger, I. (2017). Effects of liver-stage clearance by Primaquine on gametocyte carriage of Plasmodium vivax and P. falciparum. PLOS Neglected Tropical Diseases, 11(7), e0005753. https://doi.org/10.1371/JOURNAL.PNTD.0005753

Westenberger, S. J., McClean, C. M., Chattopadhyay, R., Dharia, N. V., Carlton, J. M., Barnwell, J. W., Collins, W. E., Hoffman, S. L., Zhou, Y., Vinetz, J. M., & Winzeler, E. A. (2010). A Systems-Based Analysis of Plasmodium vivax Lifecycle Transcription from Human to Mosquito. PLOS Neglected Tropical Diseases, 4(4), e653. https://doi.org/10.1371/JOURNAL.PNTD.0000653

World Health Organization. (2020). WHO World Malaria Report 2020. In Malaria report 2020.

World malaria report 2021. (n.d.).

Wu, Y., Ellis, R. D., Shaffer, D., Fontes, E., Malkin, E. M., Mahanty, S., Fay, M. P., Narum, D., Rausch, K., Miles, A. P., Aebig, J., Orcutt, A., Muratova, O., Song, G., Lambert, L., Zhu, D., Miura, K., Long, C., Saul, A., … Durbin, A. P. (2008). Phase 1 Trial of Malaria Transmission Blocking Vaccine Candidates Pfs25 and Pvs25 Formulated with Montanide ISA 51. PLOS ONE, 3(7), e2636. https://doi.org/10.1371/JOURNAL.PONE.0002636

Yoeli, M. (1938). Note on the experimental infection of Anopheles elutus with Plasmodium falciparum by feeding through a prepared animal membrane. Rivista Di Malariologia, 17, 62–66.

Published

2022-09-12

How to Cite

Silva, L. P. da C., & Ramos, G. Q. (2022). Plasmodium vivax: gametócitos e estratégias para o bloqueio de transmissão: Plasmodium vivax: gametocytes and strategies to block transmission. Brazilian Journal of Development, 8(9), 62266–62280. https://doi.org/10.34117/bjdv8n9-122

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