Cargando…

The seasonal dynamics and biting behavior of potential Anopheles vectors of Plasmodium knowlesi in Palawan, Philippines

BACKGROUND: A small number of human cases of the zoonotic malaria Plasmodium knowlesi have been reported in Palawan Island, the Philippines. Identification of potential vector species and their bionomics is crucial for understanding human exposure risk in this setting. Here, we combined longitudinal...

Descripción completa

Detalles Bibliográficos
Autores principales: Malijan, Richard Paul B., Mechan, Frank, Braganza, Jessie C., Valle, Kristelle Mae R., Salazar, Ferdinand V., Torno, Majhalia M., Aure, Wilfredo E., Bacay, Brian A., Espino, Fe Esperanza, Torr, Stephen J., Fornace, Kimberly M., Drakeley, Chris, Ferguson, Heather M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8261946/
https://www.ncbi.nlm.nih.gov/pubmed/34233742
http://dx.doi.org/10.1186/s13071-021-04853-9
_version_ 1783719099277246464
author Malijan, Richard Paul B.
Mechan, Frank
Braganza, Jessie C.
Valle, Kristelle Mae R.
Salazar, Ferdinand V.
Torno, Majhalia M.
Aure, Wilfredo E.
Bacay, Brian A.
Espino, Fe Esperanza
Torr, Stephen J.
Fornace, Kimberly M.
Drakeley, Chris
Ferguson, Heather M.
author_facet Malijan, Richard Paul B.
Mechan, Frank
Braganza, Jessie C.
Valle, Kristelle Mae R.
Salazar, Ferdinand V.
Torno, Majhalia M.
Aure, Wilfredo E.
Bacay, Brian A.
Espino, Fe Esperanza
Torr, Stephen J.
Fornace, Kimberly M.
Drakeley, Chris
Ferguson, Heather M.
author_sort Malijan, Richard Paul B.
collection PubMed
description BACKGROUND: A small number of human cases of the zoonotic malaria Plasmodium knowlesi have been reported in Palawan Island, the Philippines. Identification of potential vector species and their bionomics is crucial for understanding human exposure risk in this setting. Here, we combined longitudinal surveillance with a trap-evaluation study to address knowledge gaps about the ecology and potential for zoonotic spillover of this macaque malaria in Palawan Island. METHODS: The abundance, diversity and biting behavior of human-biting Anopheles mosquitoes were assessed through monthly outdoor human landing catches (HLC) in three ecotypes representing different land use (forest edge, forest and agricultural area) across 8 months. Additionally, the host preference and biting activity of potential Anopheles vectors were assessed through comparison of their abundance and capture time in traps baited with humans (HLC, human-baited electrocuting net—HEN) or macaques (monkey-baited trap—MBT, monkey-baited electrocuting net—MEN). All female Anopheles mosquitoes were tested for the presence of Plasmodium parasites by PCR. RESULTS: Previously incriminated vectors Anopheles balabacensis and An. flavirostris accounted for > 95% of anophelines caught in longitudinal surveillance. However, human biting densities were relatively low (An. balabacensis: 0.34–1.20 per night, An. flavirostris: 0–2 bites per night). Biting densities of An. balabacensis were highest in the forest edge, while An. flavirostris was most abundant in the agricultural area. The abundance of An. balabacensis and An. flavirostris was significantly higher in HLC than in MBT. None of the 357 female Anopheles mosquitoes tested for Plasmodium infection were positive. CONCLUSIONS: The relatively low density and lack of malaria infection in Anopheles mosquitoes sampled here indicates that exposure to P. knowlesi in this setting is considerably lower than in neighboring countries (i.e. Malaysia), where it is now the primary cause of malaria in humans. Although anophelines had lower abundance in MBTs than in HLCs, An. balabacensis and An. flavirostris were caught by both methods, suggesting they could act as bridge vectors between humans and macaques. These species bite primarily outdoors during the early evening, confirming that insecticide-treated nets are unlikely to provide protection against P. knowlesi vectors. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-021-04853-9.
format Online
Article
Text
id pubmed-8261946
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-82619462021-07-07 The seasonal dynamics and biting behavior of potential Anopheles vectors of Plasmodium knowlesi in Palawan, Philippines Malijan, Richard Paul B. Mechan, Frank Braganza, Jessie C. Valle, Kristelle Mae R. Salazar, Ferdinand V. Torno, Majhalia M. Aure, Wilfredo E. Bacay, Brian A. Espino, Fe Esperanza Torr, Stephen J. Fornace, Kimberly M. Drakeley, Chris Ferguson, Heather M. Parasit Vectors Research BACKGROUND: A small number of human cases of the zoonotic malaria Plasmodium knowlesi have been reported in Palawan Island, the Philippines. Identification of potential vector species and their bionomics is crucial for understanding human exposure risk in this setting. Here, we combined longitudinal surveillance with a trap-evaluation study to address knowledge gaps about the ecology and potential for zoonotic spillover of this macaque malaria in Palawan Island. METHODS: The abundance, diversity and biting behavior of human-biting Anopheles mosquitoes were assessed through monthly outdoor human landing catches (HLC) in three ecotypes representing different land use (forest edge, forest and agricultural area) across 8 months. Additionally, the host preference and biting activity of potential Anopheles vectors were assessed through comparison of their abundance and capture time in traps baited with humans (HLC, human-baited electrocuting net—HEN) or macaques (monkey-baited trap—MBT, monkey-baited electrocuting net—MEN). All female Anopheles mosquitoes were tested for the presence of Plasmodium parasites by PCR. RESULTS: Previously incriminated vectors Anopheles balabacensis and An. flavirostris accounted for > 95% of anophelines caught in longitudinal surveillance. However, human biting densities were relatively low (An. balabacensis: 0.34–1.20 per night, An. flavirostris: 0–2 bites per night). Biting densities of An. balabacensis were highest in the forest edge, while An. flavirostris was most abundant in the agricultural area. The abundance of An. balabacensis and An. flavirostris was significantly higher in HLC than in MBT. None of the 357 female Anopheles mosquitoes tested for Plasmodium infection were positive. CONCLUSIONS: The relatively low density and lack of malaria infection in Anopheles mosquitoes sampled here indicates that exposure to P. knowlesi in this setting is considerably lower than in neighboring countries (i.e. Malaysia), where it is now the primary cause of malaria in humans. Although anophelines had lower abundance in MBTs than in HLCs, An. balabacensis and An. flavirostris were caught by both methods, suggesting they could act as bridge vectors between humans and macaques. These species bite primarily outdoors during the early evening, confirming that insecticide-treated nets are unlikely to provide protection against P. knowlesi vectors. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-021-04853-9. BioMed Central 2021-07-07 /pmc/articles/PMC8261946/ /pubmed/34233742 http://dx.doi.org/10.1186/s13071-021-04853-9 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Malijan, Richard Paul B.
Mechan, Frank
Braganza, Jessie C.
Valle, Kristelle Mae R.
Salazar, Ferdinand V.
Torno, Majhalia M.
Aure, Wilfredo E.
Bacay, Brian A.
Espino, Fe Esperanza
Torr, Stephen J.
Fornace, Kimberly M.
Drakeley, Chris
Ferguson, Heather M.
The seasonal dynamics and biting behavior of potential Anopheles vectors of Plasmodium knowlesi in Palawan, Philippines
title The seasonal dynamics and biting behavior of potential Anopheles vectors of Plasmodium knowlesi in Palawan, Philippines
title_full The seasonal dynamics and biting behavior of potential Anopheles vectors of Plasmodium knowlesi in Palawan, Philippines
title_fullStr The seasonal dynamics and biting behavior of potential Anopheles vectors of Plasmodium knowlesi in Palawan, Philippines
title_full_unstemmed The seasonal dynamics and biting behavior of potential Anopheles vectors of Plasmodium knowlesi in Palawan, Philippines
title_short The seasonal dynamics and biting behavior of potential Anopheles vectors of Plasmodium knowlesi in Palawan, Philippines
title_sort seasonal dynamics and biting behavior of potential anopheles vectors of plasmodium knowlesi in palawan, philippines
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8261946/
https://www.ncbi.nlm.nih.gov/pubmed/34233742
http://dx.doi.org/10.1186/s13071-021-04853-9
work_keys_str_mv AT malijanrichardpaulb theseasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT mechanfrank theseasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT braganzajessiec theseasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT vallekristellemaer theseasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT salazarferdinandv theseasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT tornomajhaliam theseasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT aurewilfredoe theseasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT bacaybriana theseasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT espinofeesperanza theseasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT torrstephenj theseasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT fornacekimberlym theseasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT drakeleychris theseasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT fergusonheatherm theseasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT malijanrichardpaulb seasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT mechanfrank seasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT braganzajessiec seasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT vallekristellemaer seasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT salazarferdinandv seasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT tornomajhaliam seasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT aurewilfredoe seasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT bacaybriana seasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT espinofeesperanza seasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT torrstephenj seasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT fornacekimberlym seasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT drakeleychris seasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines
AT fergusonheatherm seasonaldynamicsandbitingbehaviorofpotentialanophelesvectorsofplasmodiumknowlesiinpalawanphilippines