Ecological complexity of zoonotic malaria in macaque natural hosts

Abstract Macaques are important reservoirs of zoonotic malaria in Southeast Asia. Although cross-sectional malaria surveys have been conducted in macaques, little is known about intra-host infection dynamics and host variation in susceptibility to infection in these infectious reservoirs. We perform...

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Main Authors: Chaturong Putaporntip, Surasuk Yanmanee, Jidapha Somkuna, Rattanaporn Rojrung, Urassaya Pattanawong, Sunate Karapan, Napaporn Kuamsab, Chew Weng Cheng, Somchai Jongwutiwes
Format: Article
Language:English
Published: Nature Portfolio 2025-02-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-025-86415-y
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author Chaturong Putaporntip
Surasuk Yanmanee
Jidapha Somkuna
Rattanaporn Rojrung
Urassaya Pattanawong
Sunate Karapan
Napaporn Kuamsab
Chew Weng Cheng
Somchai Jongwutiwes
author_facet Chaturong Putaporntip
Surasuk Yanmanee
Jidapha Somkuna
Rattanaporn Rojrung
Urassaya Pattanawong
Sunate Karapan
Napaporn Kuamsab
Chew Weng Cheng
Somchai Jongwutiwes
author_sort Chaturong Putaporntip
collection DOAJ
description Abstract Macaques are important reservoirs of zoonotic malaria in Southeast Asia. Although cross-sectional malaria surveys have been conducted in macaques, little is known about intra-host infection dynamics and host variation in susceptibility to infection in these infectious reservoirs. We performed a longitudinal monitoring of Plasmodium and Hepatocystis infections by microscopy, species-specific polymerase chain reaction (PCR) and targeted amplicon deep sequencing (TADS) in three long-tailed macaques and 20 pig-tailed macaques in two districts of Narathiwat Province, southern Thailand. In total, 104 macaques’ blood samples were obtained during 5 visits with sequential time intervals of 9, 4, 7 and 12 months. Transiently patent Plasmodium infections with low parasite density ( ≤ 1,050 parasites/µL) occurred in 7 pig-tailed macaques, while PCR and TADS diagnosed infections in 45 (43.27%) blood samples with one or more species of parasites, including Plasmodium knowlesi, P. cynomolgi, P. inui, P. fieldi, P. coatneyi, P. aff. coatneyi and Hepatocystis sp. in one long-tailed and 12 pig-tailed macaques. Compared with PCR, TADS additionally detected co-infecting species in 22 of 45 ( 48.89%) samples. Although living in close proximity to other infected macaques, seven macaques were free from infection during the 32-month period. Infections for 4 to 32 months with malaria parasites carrying identical complete mitochondrial genome sequences were reaffirmed in 10 macaques. Potentially new infections were detected transiently or over a long period during the course of the infections while competitive exclusion seemed to occur between Hepatocystis sp. and Plasmodium taxa. Macaques’ Duffy phenotypes did not influence differential susceptibility to Plasmodium infections. These results suggest the ecological complexity of hemoparasite infections in natural reservoirs of zoonotic malaria. The long period of Plasmodium infections in macaques could affect the transmission and control of the disease.
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spelling doaj-art-49e83ff9bb36496c9faf5d77acd495d52025-08-20T02:48:32ZengNature PortfolioScientific Reports2045-23222025-02-0115111410.1038/s41598-025-86415-yEcological complexity of zoonotic malaria in macaque natural hostsChaturong Putaporntip0Surasuk Yanmanee1Jidapha Somkuna2Rattanaporn Rojrung3Urassaya Pattanawong4Sunate Karapan5Napaporn Kuamsab6Chew Weng Cheng7Somchai Jongwutiwes8Molecular Biology of Malaria and Opportunistic Parasites Research Unit, Department of Parasitology, Faculty of Medicine, Chulalongkorn UniversityMolecular Biology of Malaria and Opportunistic Parasites Research Unit, Department of Parasitology, Faculty of Medicine, Chulalongkorn UniversityMolecular Biology of Malaria and Opportunistic Parasites Research Unit, Department of Parasitology, Faculty of Medicine, Chulalongkorn UniversityMolecular Biology of Malaria and Opportunistic Parasites Research Unit, Department of Parasitology, Faculty of Medicine, Chulalongkorn UniversityMolecular Biology of Malaria and Opportunistic Parasites Research Unit, Department of Parasitology, Faculty of Medicine, Chulalongkorn UniversityDepartment of National Parks, Wildlife and Plant Conservation, Ministry of National Resources and EnvironmentCommunity Public Health Program, Faculty of Health Science and Technology, Southern College of TechnologyDiscovery and Translational Science Department, Leeds Institute of Cardiovascular and Metabolic Medicine, Faculty of Medicine and Health, University of LeedsMolecular Biology of Malaria and Opportunistic Parasites Research Unit, Department of Parasitology, Faculty of Medicine, Chulalongkorn UniversityAbstract Macaques are important reservoirs of zoonotic malaria in Southeast Asia. Although cross-sectional malaria surveys have been conducted in macaques, little is known about intra-host infection dynamics and host variation in susceptibility to infection in these infectious reservoirs. We performed a longitudinal monitoring of Plasmodium and Hepatocystis infections by microscopy, species-specific polymerase chain reaction (PCR) and targeted amplicon deep sequencing (TADS) in three long-tailed macaques and 20 pig-tailed macaques in two districts of Narathiwat Province, southern Thailand. In total, 104 macaques’ blood samples were obtained during 5 visits with sequential time intervals of 9, 4, 7 and 12 months. Transiently patent Plasmodium infections with low parasite density ( ≤ 1,050 parasites/µL) occurred in 7 pig-tailed macaques, while PCR and TADS diagnosed infections in 45 (43.27%) blood samples with one or more species of parasites, including Plasmodium knowlesi, P. cynomolgi, P. inui, P. fieldi, P. coatneyi, P. aff. coatneyi and Hepatocystis sp. in one long-tailed and 12 pig-tailed macaques. Compared with PCR, TADS additionally detected co-infecting species in 22 of 45 ( 48.89%) samples. Although living in close proximity to other infected macaques, seven macaques were free from infection during the 32-month period. Infections for 4 to 32 months with malaria parasites carrying identical complete mitochondrial genome sequences were reaffirmed in 10 macaques. Potentially new infections were detected transiently or over a long period during the course of the infections while competitive exclusion seemed to occur between Hepatocystis sp. and Plasmodium taxa. Macaques’ Duffy phenotypes did not influence differential susceptibility to Plasmodium infections. These results suggest the ecological complexity of hemoparasite infections in natural reservoirs of zoonotic malaria. The long period of Plasmodium infections in macaques could affect the transmission and control of the disease.https://doi.org/10.1038/s41598-025-86415-yNonhuman primate malariaPlasmodium knowlesiPlasmodium cynomolgiPlasmodium inuiPlasmodium coatneyiPlasmodium fieldi
spellingShingle Chaturong Putaporntip
Surasuk Yanmanee
Jidapha Somkuna
Rattanaporn Rojrung
Urassaya Pattanawong
Sunate Karapan
Napaporn Kuamsab
Chew Weng Cheng
Somchai Jongwutiwes
Ecological complexity of zoonotic malaria in macaque natural hosts
Scientific Reports
Nonhuman primate malaria
Plasmodium knowlesi
Plasmodium cynomolgi
Plasmodium inui
Plasmodium coatneyi
Plasmodium fieldi
title Ecological complexity of zoonotic malaria in macaque natural hosts
title_full Ecological complexity of zoonotic malaria in macaque natural hosts
title_fullStr Ecological complexity of zoonotic malaria in macaque natural hosts
title_full_unstemmed Ecological complexity of zoonotic malaria in macaque natural hosts
title_short Ecological complexity of zoonotic malaria in macaque natural hosts
title_sort ecological complexity of zoonotic malaria in macaque natural hosts
topic Nonhuman primate malaria
Plasmodium knowlesi
Plasmodium cynomolgi
Plasmodium inui
Plasmodium coatneyi
Plasmodium fieldi
url https://doi.org/10.1038/s41598-025-86415-y
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