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Environmental and spatial risk factors for the larval habitats of Plasmodium knowlesi vectors in Sabah, Malaysian Borneo.

ABSTRACT: Land-use changes, such as deforestation and agriculture, can influence mosquito vector populations and malaria transmission. These land-use changes have been linked to increased incidence in human cases of the zoonotic malaria Plasmodium knowlesi in Sabah, Malaysian Borneo. This study investigates whether these associations are partially driven by fine-scale land-use changes creating more favourable aquatic breeding habitats for P. knowlesi anopheline vectors. Using aerial remote sensing data, we developed a sampling frame representative of all land use types within a major focus of P. knowlesi transmission. From 2015 to 2016 monthly longitudinal surveys of larval habitats were collected in randomly selected areas stratified by land use type. Additional remote sensing data on environmental variables, land cover and landscape configuration were assembled for the study site. Risk factor analyses were performed over multiple spatial scales to determine associations between environmental and spatial variables and anopheline larval presence. Habitat fragmentation (300 m), aspect (350 m), distance to rubber plantations (100 m) and Culex larval presence were identified as risk factors for Anopheles breeding. Additionally, models were fit to determine the presence of potential larval habitats within the areas surveyed and used to generate a time-series of monthly predictive maps. These results indicate that land-use change and topography influence the suitability of larval habitats, and may partially explain the link between P. knowlesi incidence and deforestation. The predictive maps, and identification of the spatial scales at which risk factors are most influential may aid spatio-temporally targeted vector control interventions.

SUBMITTER: Byrne I

PROVIDER: S-EPMC8175559 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The zoonotic malaria parasite, Plasmodium knowlesi, is now a substantial public health problem in Malaysian Borneo. Current understanding of P. knowlesi vector bionomics and ecology in Sabah comes from a few studies near the epicentre of human cases in one district, Kudat. These have incriminated Anopheles balabacensis as the primary vector, and suggest that human exposure to vector biting is peri-domestic as well as in forest environments. To address the limited understanding of vector ecology and human exposure risk outside of Kudat, we performed wider scale surveillance across four districts in Sabah with confirmed transmission to investigate spatial heterogeneity in vector abundance, diversity and infection rate. Entomological surveillance was carried out six months after a cross-sectional survey of P. knowlesi prevalence in humans throughout the study area; providing an opportunity to investigate associations between entomological indicators and infection. Human-landing catches were performed in peri-domestic, farm and forest sites in 11 villages (3-4 per district) and paired with estimates of human P. knowlesi exposure based on sero-prevalence. Anopheles balabacensis was present in all districts but only 6/11 villages. The mean density of An. balabacensis was relatively low, but significantly higher in farm (0.094/night) and forest (0.082/night) than peri-domestic areas (0.007/night). Only one An. balabacensis (n = 32) was infected with P. knowlesi. Plasmodium knowlesi sero-positivity in people was not associated with An. balabacensis density at the village-level however post hoc analyses indicated the study had limited power to detect a statistical association due low vector density. Wider scale sampling revealed substantial heterogeneity in vector density and distribution between villages and districts. Vector-habitat associations predicted from this larger-scale surveillance differed from those inferred from smaller-scale studies in Kudat; highlighting the importance of local ecological context. Findings highlight potential trade-offs between maximizing temporal versus spatial breadth when designing entomological surveillance; and provide baseline entomological and epidemiological data to inform future studies of entomological risk factors for human P. knowlesi infection.

Project description:BackgroundPlasmodium knowlesi is a significant cause of human malaria in Sarawak, Malaysian Borneo. Only one study has been previously undertaken in Sarawak to identify vectors of P. knowlesi, where Anopheles latens was incriminated as the vector in Kapit, central Sarawak. A study was therefore undertaken to identify malaria vectors in a different location in Sarawak.MethodsMosquitoes found landing on humans and resting on leaves over a 5-day period at two sites in the Lawas District of northern Sarawak were collected and identified. DNA samples extracted from salivary glands of Anopheles mosquitoes were subjected to nested PCR malaria-detection assays. The small subunit ribosomal RNA (SSU rRNA) gene of Plasmodium was sequenced, and the internal transcribed spacer 2 (ITS2) and mitochondrial cytochrome c oxidase subunit 1 (cox1) gene of the mosquitoes were sequenced from the Plasmodium-positive samples for phylogenetic analysis.ResultsTotals of 65 anophelines and 127 culicines were collected. By PCR, 6 An. balabacensis and 5 An. donaldi were found to have single P. knowlesi infections while 3 other An. balabacensis had either single, double or triple infections with P. inui, P. fieldi, P. cynomolgi and P. knowlesi. Phylogenetic analysis of the Plasmodium SSU rRNA gene confirmed 3 An. donaldi and 3 An. balabacensis with single P. knowlesi infections, while 3 other An. balabacensis had two or more Plasmodium species of P. inui, P. knowlesi, P. cynomolgi and some species of Plasmodium that could not be conclusively identified. Phylogenies inferred from the ITS2 and/or cox1 sequences of An. balabacensis and An. donaldi indicate that they are genetically indistinguishable from An. balabacensis and An. donaldi, respectively, found in Sabah, Malaysian Borneo.ConclusionsPreviously An. latens was identified as the vector for P. knowlesi in Kapit, central Sarawak, Malaysian Borneo, and now An. balabacensis and An. donaldi have been incriminated as vectors for zoonotic malaria in Lawas, northern Sarawak.

Project description:BackgroundMalaria parasites such as Plasmodium knowlesi, P. inui, and P. cynomolgi are spread from macaques to humans through the Leucosphyrus Group of Anopheles mosquitoes. It is crucial to know the distribution of these vectors to implement effective control measures for malaria elimination. Plasmodium knowlesi is the most predominant zoonotic malaria parasite infecting humans in Malaysia.MethodsVector data from various sources were used to create distribution maps from 1957 to 2021. A predictive statistical model utilizing logistic regression was developed using significant environmental factors. Interpolation maps were created using the inverse distance weighted (IDW) method and overlaid with the corresponding environmental variables.ResultsBased on the IDW analysis, high vector abundances were found in the southwestern part of Sarawak, the northern region of Pahang and the northwestern part of Sabah. However, most parts of Johor, Sabah, Perlis, Penang, Kelantan and Terengganu had low vector abundance. The accuracy test indicated that the model predicted sampling and non-sampling areas with 75.3% overall accuracy. The selected environmental variables were entered into the regression model based on their significant values. In addition to the presence of water bodies, elevation, temperature, forest loss and forest cover were included in the final model since these were significantly correlated. Anopheles mosquitoes were mainly distributed in Peninsular Malaysia (Titiwangsa range, central and northern parts), Sabah (Kudat, West Coast, Interior and Tawau division) and Sarawak (Kapit, Miri, and Limbang). The predicted Anopheles mosquito density was lower in the southern part of Peninsular Malaysia, the Sandakan Division of Sabah and the western region of Sarawak.ConclusionThe study offers insight into the distribution of the Leucosphyrus Group of Anopheles mosquitoes in Malaysia. Additionally, the accompanying predictive vector map correlates well with cases of P. knowlesi malaria. This research is crucial in informing and supporting future efforts by healthcare professionals to develop effective malaria control interventions.

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Environmental and spatial risk factors for the larval habitats of Plasmodium knowlesi vectors in Sabah, Malaysian Borneo.

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