Environmental risk factors and exposure to the zoonotic malaria parasite Plasmodium knowlesi across northern Sabah, Malaysia

a population-based cross-sectional survey

Kimberly M. Fornace, Paddy M. Brock, Tommy R. Abidin, Lynn Grignard, Lou S. Herman, Tock H. Chua, Sylvia Daim, Timothy William, Catriona L.E.B. Patterson, Tom Hall, Matthew J. Grigg, Nicholas M. Anstey, Kevin K.A. Tetteh, Jonathan Cox, Chris J. Drakeley

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Abstract

Background: Land use changes disrupt ecosystems, altering the transmission of vector-borne diseases. These changes have been associated with increasing incidence of zoonotic malaria caused by Plasmodium knowlesi; however, the population-level distributions of infection and exposure remain unknown. We aimed to measure prevalence of serological exposure to P knowlesi and assess associated risk factors.

Methods: We did an environmentally stratified, population-based, cross-sectional survey across households in the Kudat, Kota Marudu, Pitas, and Ranau districts in northern Sabah, Malaysia, encompassing a range of ecologies. Using blood samples, the transmission intensity of P knowlesi and other malaria species was measured by specific antibody prevalence and infection detected using molecular methods. Proportions and configurations of land types were extracted from maps derived from satellite images; a data-mining approach was used to select variables. A Bayesian hierarchical model for P knowlesi seropositivity was developed, incorporating questionnaire data about individual and household-level risk factors with selected landscape factors.

Findings: Between Sept 17, 2015, and Dec 12, 2015, 10 100 individuals with a median age of 25 years (range 3 months to 105 years) were sampled from 2849 households in 180 villages. 5·1% (95% CI 4·8–5·4) were seropositive for P knowlesi, and marked historical decreases were observed in the transmission of Plasmodium falciparum and Plasmodium vivax. Nine Plasmodium spp infections were detected. Age, male sex, contact with macaques, forest use, and raised house construction were positively associated with P knowlesi exposure, whereas residing at higher geographical elevations and use of insecticide were protective. Agricultural and forest variables, such as proportions and fragmentation of land cover types, predicted exposure at different spatial scales from households.

Interpretation: Although few infections were detected, P knowlesi exposure was observed in all demographic groups and was associated with occupational factors. Results suggest that agricultural expansion and forest fragmentation affect P knowlesi exposure, supporting linkages between land use change and P knowlesi transmission.

Funding: UK Medical Research Council, Natural Environment Research Council, Economic and Social Research Council, and Biotechnology and Biosciences Research Council.

Original languageEnglish
Pages (from-to)e179-e186
Number of pages8
JournalThe Lancet Planetary Health
Volume3
Issue number4
Early online date24 Apr 2019
DOIs
Publication statusPublished - Apr 2019

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Plasmodium knowlesi
Malaysia
Zoonoses
Malaria
Parasites
Cross-Sectional Studies
fragmentation
land use
Population
demographic situation
medical research
economic research
Infection
Research
Demography
household survey
biotechnology
social research
Plasmodium vivax
Disease Vectors

Cite this

Fornace, Kimberly M. ; Brock, Paddy M. ; Abidin, Tommy R. ; Grignard, Lynn ; Herman, Lou S. ; Chua, Tock H. ; Daim, Sylvia ; William, Timothy ; Patterson, Catriona L.E.B. ; Hall, Tom ; Grigg, Matthew J. ; Anstey, Nicholas M. ; Tetteh, Kevin K.A. ; Cox, Jonathan ; Drakeley, Chris J. / Environmental risk factors and exposure to the zoonotic malaria parasite Plasmodium knowlesi across northern Sabah, Malaysia : a population-based cross-sectional survey. In: The Lancet Planetary Health. 2019 ; Vol. 3, No. 4. pp. e179-e186.
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title = "Environmental risk factors and exposure to the zoonotic malaria parasite Plasmodium knowlesi across northern Sabah, Malaysia: a population-based cross-sectional survey",
abstract = "Background: Land use changes disrupt ecosystems, altering the transmission of vector-borne diseases. These changes have been associated with increasing incidence of zoonotic malaria caused by Plasmodium knowlesi; however, the population-level distributions of infection and exposure remain unknown. We aimed to measure prevalence of serological exposure to P knowlesi and assess associated risk factors. Methods: We did an environmentally stratified, population-based, cross-sectional survey across households in the Kudat, Kota Marudu, Pitas, and Ranau districts in northern Sabah, Malaysia, encompassing a range of ecologies. Using blood samples, the transmission intensity of P knowlesi and other malaria species was measured by specific antibody prevalence and infection detected using molecular methods. Proportions and configurations of land types were extracted from maps derived from satellite images; a data-mining approach was used to select variables. A Bayesian hierarchical model for P knowlesi seropositivity was developed, incorporating questionnaire data about individual and household-level risk factors with selected landscape factors. Findings: Between Sept 17, 2015, and Dec 12, 2015, 10 100 individuals with a median age of 25 years (range 3 months to 105 years) were sampled from 2849 households in 180 villages. 5·1{\%} (95{\%} CI 4·8–5·4) were seropositive for P knowlesi, and marked historical decreases were observed in the transmission of Plasmodium falciparum and Plasmodium vivax. Nine Plasmodium spp infections were detected. Age, male sex, contact with macaques, forest use, and raised house construction were positively associated with P knowlesi exposure, whereas residing at higher geographical elevations and use of insecticide were protective. Agricultural and forest variables, such as proportions and fragmentation of land cover types, predicted exposure at different spatial scales from households. Interpretation: Although few infections were detected, P knowlesi exposure was observed in all demographic groups and was associated with occupational factors. Results suggest that agricultural expansion and forest fragmentation affect P knowlesi exposure, supporting linkages between land use change and P knowlesi transmission. Funding: UK Medical Research Council, Natural Environment Research Council, Economic and Social Research Council, and Biotechnology and Biosciences Research Council.",
author = "Fornace, {Kimberly M.} and Brock, {Paddy M.} and Abidin, {Tommy R.} and Lynn Grignard and Herman, {Lou S.} and Chua, {Tock H.} and Sylvia Daim and Timothy William and Patterson, {Catriona L.E.B.} and Tom Hall and Grigg, {Matthew J.} and Anstey, {Nicholas M.} and Tetteh, {Kevin K.A.} and Jonathan Cox and Drakeley, {Chris J.}",
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month = "4",
doi = "10.1016/S2542-5196(19)30045-2",
language = "English",
volume = "3",
pages = "e179--e186",
journal = "The Lancet Planetary Health",
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Fornace, KM, Brock, PM, Abidin, TR, Grignard, L, Herman, LS, Chua, TH, Daim, S, William, T, Patterson, CLEB, Hall, T, Grigg, MJ, Anstey, NM, Tetteh, KKA, Cox, J & Drakeley, CJ 2019, 'Environmental risk factors and exposure to the zoonotic malaria parasite Plasmodium knowlesi across northern Sabah, Malaysia: a population-based cross-sectional survey', The Lancet Planetary Health, vol. 3, no. 4, pp. e179-e186. https://doi.org/10.1016/S2542-5196(19)30045-2

Environmental risk factors and exposure to the zoonotic malaria parasite Plasmodium knowlesi across northern Sabah, Malaysia : a population-based cross-sectional survey. / Fornace, Kimberly M.; Brock, Paddy M.; Abidin, Tommy R.; Grignard, Lynn; Herman, Lou S.; Chua, Tock H.; Daim, Sylvia; William, Timothy; Patterson, Catriona L.E.B.; Hall, Tom; Grigg, Matthew J.; Anstey, Nicholas M.; Tetteh, Kevin K.A.; Cox, Jonathan; Drakeley, Chris J.

In: The Lancet Planetary Health, Vol. 3, No. 4, 04.2019, p. e179-e186.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Environmental risk factors and exposure to the zoonotic malaria parasite Plasmodium knowlesi across northern Sabah, Malaysia

T2 - a population-based cross-sectional survey

AU - Fornace, Kimberly M.

AU - Brock, Paddy M.

AU - Abidin, Tommy R.

AU - Grignard, Lynn

AU - Herman, Lou S.

AU - Chua, Tock H.

AU - Daim, Sylvia

AU - William, Timothy

AU - Patterson, Catriona L.E.B.

AU - Hall, Tom

AU - Grigg, Matthew J.

AU - Anstey, Nicholas M.

AU - Tetteh, Kevin K.A.

AU - Cox, Jonathan

AU - Drakeley, Chris J.

PY - 2019/4

Y1 - 2019/4

N2 - Background: Land use changes disrupt ecosystems, altering the transmission of vector-borne diseases. These changes have been associated with increasing incidence of zoonotic malaria caused by Plasmodium knowlesi; however, the population-level distributions of infection and exposure remain unknown. We aimed to measure prevalence of serological exposure to P knowlesi and assess associated risk factors. Methods: We did an environmentally stratified, population-based, cross-sectional survey across households in the Kudat, Kota Marudu, Pitas, and Ranau districts in northern Sabah, Malaysia, encompassing a range of ecologies. Using blood samples, the transmission intensity of P knowlesi and other malaria species was measured by specific antibody prevalence and infection detected using molecular methods. Proportions and configurations of land types were extracted from maps derived from satellite images; a data-mining approach was used to select variables. A Bayesian hierarchical model for P knowlesi seropositivity was developed, incorporating questionnaire data about individual and household-level risk factors with selected landscape factors. Findings: Between Sept 17, 2015, and Dec 12, 2015, 10 100 individuals with a median age of 25 years (range 3 months to 105 years) were sampled from 2849 households in 180 villages. 5·1% (95% CI 4·8–5·4) were seropositive for P knowlesi, and marked historical decreases were observed in the transmission of Plasmodium falciparum and Plasmodium vivax. Nine Plasmodium spp infections were detected. Age, male sex, contact with macaques, forest use, and raised house construction were positively associated with P knowlesi exposure, whereas residing at higher geographical elevations and use of insecticide were protective. Agricultural and forest variables, such as proportions and fragmentation of land cover types, predicted exposure at different spatial scales from households. Interpretation: Although few infections were detected, P knowlesi exposure was observed in all demographic groups and was associated with occupational factors. Results suggest that agricultural expansion and forest fragmentation affect P knowlesi exposure, supporting linkages between land use change and P knowlesi transmission. Funding: UK Medical Research Council, Natural Environment Research Council, Economic and Social Research Council, and Biotechnology and Biosciences Research Council.

AB - Background: Land use changes disrupt ecosystems, altering the transmission of vector-borne diseases. These changes have been associated with increasing incidence of zoonotic malaria caused by Plasmodium knowlesi; however, the population-level distributions of infection and exposure remain unknown. We aimed to measure prevalence of serological exposure to P knowlesi and assess associated risk factors. Methods: We did an environmentally stratified, population-based, cross-sectional survey across households in the Kudat, Kota Marudu, Pitas, and Ranau districts in northern Sabah, Malaysia, encompassing a range of ecologies. Using blood samples, the transmission intensity of P knowlesi and other malaria species was measured by specific antibody prevalence and infection detected using molecular methods. Proportions and configurations of land types were extracted from maps derived from satellite images; a data-mining approach was used to select variables. A Bayesian hierarchical model for P knowlesi seropositivity was developed, incorporating questionnaire data about individual and household-level risk factors with selected landscape factors. Findings: Between Sept 17, 2015, and Dec 12, 2015, 10 100 individuals with a median age of 25 years (range 3 months to 105 years) were sampled from 2849 households in 180 villages. 5·1% (95% CI 4·8–5·4) were seropositive for P knowlesi, and marked historical decreases were observed in the transmission of Plasmodium falciparum and Plasmodium vivax. Nine Plasmodium spp infections were detected. Age, male sex, contact with macaques, forest use, and raised house construction were positively associated with P knowlesi exposure, whereas residing at higher geographical elevations and use of insecticide were protective. Agricultural and forest variables, such as proportions and fragmentation of land cover types, predicted exposure at different spatial scales from households. Interpretation: Although few infections were detected, P knowlesi exposure was observed in all demographic groups and was associated with occupational factors. Results suggest that agricultural expansion and forest fragmentation affect P knowlesi exposure, supporting linkages between land use change and P knowlesi transmission. Funding: UK Medical Research Council, Natural Environment Research Council, Economic and Social Research Council, and Biotechnology and Biosciences Research Council.

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