The potential for zoonotic malaria transmission in five areas of Indonesia inhabited by non-human primates

Abstract Background Indonesia is home to many species of non-human primates (NHPs). Deforestation, which is still ongoing in Indonesia, has substantially reduced the habitat of NHPs in the republic. This has led to an intensification of interactions between NHPs and humans, which opens up the possib...

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Main Authors: Dendi Hadi Permana, Hasmiwati, Dwi Anita Suryandari, Ismail Ekoprayitno Rozi, Lepa Syahrani, Wuryantari Setiadi, Nuzulia Irawati, Rizaldi, Suradi Wangsamuda, Yenni Yusuf, Irdayanti, Hijral Aswad, Puji Budi Setia Asih, Din Syafruddin
Format: Article
Language:English
Published: BMC 2023-08-01
Series:Parasites & Vectors
Subjects:
Online Access:https://doi.org/10.1186/s13071-023-05880-4
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author Dendi Hadi Permana
Hasmiwati
Dwi Anita Suryandari
Ismail Ekoprayitno Rozi
Lepa Syahrani
Wuryantari Setiadi
Nuzulia Irawati
Rizaldi
Suradi Wangsamuda
Yenni Yusuf
Irdayanti
Hijral Aswad
Puji Budi Setia Asih
Din Syafruddin
author_facet Dendi Hadi Permana
Hasmiwati
Dwi Anita Suryandari
Ismail Ekoprayitno Rozi
Lepa Syahrani
Wuryantari Setiadi
Nuzulia Irawati
Rizaldi
Suradi Wangsamuda
Yenni Yusuf
Irdayanti
Hijral Aswad
Puji Budi Setia Asih
Din Syafruddin
author_sort Dendi Hadi Permana
collection DOAJ
description Abstract Background Indonesia is home to many species of non-human primates (NHPs). Deforestation, which is still ongoing in Indonesia, has substantially reduced the habitat of NHPs in the republic. This has led to an intensification of interactions between NHPs and humans, which opens up the possibility of pathogen spillover. The aim of the present study was to determine the prevalence of malarial parasite infections in NHPs in five provinces of Indonesia in 2022. Species of the genus Anopheles that can potentially transmit malarial pathogens to humans were also investigated. Methods An epidemiological survey was conducted by capturing NHPs in traps installed in several localities in the five provinces, including in the surroundings of a wildlife sanctuary. Blood samples were drawn aseptically after the NHPs had been anesthetized; the animals were released after examination. Blood smears were prepared on glass slides, and dried blood spot tests on filter paper. Infections with Plasmodium spp. were determined morphologically from the blood smears, which were stained with Giemsa solution, and molecularly through polymerase chain reaction and DNA sequencing using rplU oligonucleotides. The NHPs were identified to species level by using the mitochondrial cytochrome c oxidase subunit I gene and the internal transcribed spacer 2 gene as barcoding DNA markers. Mosquito surveillance included the collection of larvae from breeding sites and that of adults through the human landing catch (HLC) method together with light traps. Results Analysis of the DNA extracted from the dried blood spot tests of the 110 captured NHPs revealed that 50% were positive for Plasmodium, namely Plasmodium cynomolgi, Plasmodium coatneyi, Plasmodium inui, Plasmodium knowlesi and Plasmodium sp. Prevalence determined by microscopic examination of the blood smears was 42%. Species of the primate genus Macaca and family Hylobatidae were identified by molecular analysis. The most common mosquito breeding sites were ditches, puddles and natural ponds. Some of the Anopheles letifer captured through HLC carried sporozoites of malaria parasites that can cause the disease in primates. Conclusions The prevalence of malaria in the NHPs was high. Anopheles letifer, a potential vector of zoonotic malaria, was identified following its collection in Central Kalimantan by the HLC method. In sum, the potential for the transmission of zoonotic malaria in several regions of Indonesia is immense. Graphical Abstract
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spelling doaj.art-37842559ffac4ac490804e387f0268ab2023-11-19T12:31:54ZengBMCParasites & Vectors1756-33052023-08-0116111210.1186/s13071-023-05880-4The potential for zoonotic malaria transmission in five areas of Indonesia inhabited by non-human primatesDendi Hadi Permana0Hasmiwati1Dwi Anita Suryandari2Ismail Ekoprayitno Rozi3Lepa Syahrani4Wuryantari Setiadi5Nuzulia Irawati6Rizaldi7Suradi Wangsamuda8Yenni Yusuf9Irdayanti10Hijral Aswad11Puji Budi Setia Asih12Din Syafruddin13Doctoral Program in Biomedical Science, Faculty of Medicine, University of IndonesiaDepartment of Biology, Faculty of Mathematics and Natural Sciences, University of AndalasDepartment of Biology, Faculty of Medicine, University of IndonesiaNational Research and Innovation Agency (BRIN), Eijkman Research Center for Molecular BiologyNational Research and Innovation Agency (BRIN), Eijkman Research Center for Molecular BiologyNational Research and Innovation Agency (BRIN), Eijkman Research Center for Molecular BiologyDepartment of Biology, Faculty of Mathematics and Natural Sciences, University of AndalasDepartment of Biology, Faculty of Mathematics and Natural Sciences, University of AndalasDepartment of Parasitology, Faculty of Medicine, University of HasanuddinDepartment of Parasitology, Faculty of Medicine, University of HasanuddinDepartment of Parasitology, Faculty of Medicine, University of HasanuddinDepartment of Parasitology, Faculty of Medicine, University of HasanuddinNational Research and Innovation Agency (BRIN), Eijkman Research Center for Molecular BiologyNational Research and Innovation Agency (BRIN), Eijkman Research Center for Molecular BiologyAbstract Background Indonesia is home to many species of non-human primates (NHPs). Deforestation, which is still ongoing in Indonesia, has substantially reduced the habitat of NHPs in the republic. This has led to an intensification of interactions between NHPs and humans, which opens up the possibility of pathogen spillover. The aim of the present study was to determine the prevalence of malarial parasite infections in NHPs in five provinces of Indonesia in 2022. Species of the genus Anopheles that can potentially transmit malarial pathogens to humans were also investigated. Methods An epidemiological survey was conducted by capturing NHPs in traps installed in several localities in the five provinces, including in the surroundings of a wildlife sanctuary. Blood samples were drawn aseptically after the NHPs had been anesthetized; the animals were released after examination. Blood smears were prepared on glass slides, and dried blood spot tests on filter paper. Infections with Plasmodium spp. were determined morphologically from the blood smears, which were stained with Giemsa solution, and molecularly through polymerase chain reaction and DNA sequencing using rplU oligonucleotides. The NHPs were identified to species level by using the mitochondrial cytochrome c oxidase subunit I gene and the internal transcribed spacer 2 gene as barcoding DNA markers. Mosquito surveillance included the collection of larvae from breeding sites and that of adults through the human landing catch (HLC) method together with light traps. Results Analysis of the DNA extracted from the dried blood spot tests of the 110 captured NHPs revealed that 50% were positive for Plasmodium, namely Plasmodium cynomolgi, Plasmodium coatneyi, Plasmodium inui, Plasmodium knowlesi and Plasmodium sp. Prevalence determined by microscopic examination of the blood smears was 42%. Species of the primate genus Macaca and family Hylobatidae were identified by molecular analysis. The most common mosquito breeding sites were ditches, puddles and natural ponds. Some of the Anopheles letifer captured through HLC carried sporozoites of malaria parasites that can cause the disease in primates. Conclusions The prevalence of malaria in the NHPs was high. Anopheles letifer, a potential vector of zoonotic malaria, was identified following its collection in Central Kalimantan by the HLC method. In sum, the potential for the transmission of zoonotic malaria in several regions of Indonesia is immense. Graphical Abstracthttps://doi.org/10.1186/s13071-023-05880-4Zoonotic malariaNon-human primatesPlasmodium speciesInfectionAnophelesMalaria vector
spellingShingle Dendi Hadi Permana
Hasmiwati
Dwi Anita Suryandari
Ismail Ekoprayitno Rozi
Lepa Syahrani
Wuryantari Setiadi
Nuzulia Irawati
Rizaldi
Suradi Wangsamuda
Yenni Yusuf
Irdayanti
Hijral Aswad
Puji Budi Setia Asih
Din Syafruddin
The potential for zoonotic malaria transmission in five areas of Indonesia inhabited by non-human primates
Parasites & Vectors
Zoonotic malaria
Non-human primates
Plasmodium species
Infection
Anopheles
Malaria vector
title The potential for zoonotic malaria transmission in five areas of Indonesia inhabited by non-human primates
title_full The potential for zoonotic malaria transmission in five areas of Indonesia inhabited by non-human primates
title_fullStr The potential for zoonotic malaria transmission in five areas of Indonesia inhabited by non-human primates
title_full_unstemmed The potential for zoonotic malaria transmission in five areas of Indonesia inhabited by non-human primates
title_short The potential for zoonotic malaria transmission in five areas of Indonesia inhabited by non-human primates
title_sort potential for zoonotic malaria transmission in five areas of indonesia inhabited by non human primates
topic Zoonotic malaria
Non-human primates
Plasmodium species
Infection
Anopheles
Malaria vector
url https://doi.org/10.1186/s13071-023-05880-4
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