Updating estimates of Plasmodium knowlesi malaria risk in response to changing land use patterns across Southeast Asia

Background Plasmodium knowlesi is a zoonotic parasite that causes malaria in humans. The pathogen has a natural host reservoir in certain macaque species and is transmitted to humans via mosquitoes of the Anopheles Leucosphyrus Group. The risk of human P. knowlesi infection varies across Southeast Asia and is dependent upon environmental factors. Understanding this geographic variation in risk is important both for enabling appropriate diagnosis and treatment of the disease and for improving the planning and evaluation of malaria elimination. However, the data available on P. knowlesi occurrence are biased towards regions with greater surveillance and sampling effort. Predicting the spatial variation in risk of P. knowlesi malaria requires methods that can both incorporate environmental risk factors and account for spatial bias in detection. Methods & Results We extend and apply an environmental niche modelling framework as implemented by a previous mapping study of P. knowlesi transmission risk which included data up to 2015. We reviewed the literature from October 2015 through to March 2020 and identified 264 new records of P. knowlesi, with a total of 524 occurrences included in the current study following consolidation with the 2015 study. The modelling framework used in the 2015 study was extended, with changes including the addition of new covariates to capture the effect of deforestation and urbanisation on P. knowlesi transmission. Discussion Our map of P. knowlesi relative transmission suitability estimates that the risk posed by the pathogen is highest in Malaysia and Indonesia, with localised areas of high risk also predicted in the Greater Mekong Subregion, The Philippines and Northeast India. These results highlight areas of priority for P. knowlesi surveillance and prospective sampling to address the challenge the disease poses to malaria elimination planning.

[1]  C. Drakeley,et al.  Simian malaria: a narrative review on emergence, epidemiology and threat to global malaria elimination. , 2023, The Lancet. Infectious diseases.

[2]  K. Lindblade,et al.  Is there evidence of sustained human-mosquito-human transmission of the zoonotic malaria Plasmodium knowlesi? A systematic literature review , 2022, Malaria journal.

[3]  R. Hod,et al.  The Role of Human Behavior in Plasmodium knowlesi Malaria Infection: A Systematic Review , 2022, International journal of environmental research and public health.

[4]  G. Milanez,et al.  Quantification of the misidentification of Plasmodium knowlesi as Plasmodium malariae by microscopy: an analysis of 1569 P. knowlesi cases , 2021, Malaria journal.

[5]  R. Culleton,et al.  Malaria elimination in Malaysia and the rising threat of Plasmodium knowlesi , 2020, Journal of physiological anthropology.

[6]  K. Battle,et al.  Global maps of travel time to healthcare facilities , 2020, Nature Medicine.

[7]  R. Moon,et al.  Cross-species reactivity of antibodies against Plasmodium vivax blood-stage antigens to Plasmodium knowlesi , 2020, PLoS neglected tropical diseases.

[8]  J. Longbottom,et al.  Quantifying geographic accessibility to improve efficiency of entomological monitoring , 2020, PLoS neglected tropical diseases.

[9]  Bo Kong,et al.  Landscape ecology development supported by geospatial technologies: A review , 2019, Ecol. Informatics.

[10]  J. Cox,et al.  Environmental risk factors and exposure to the zoonotic malaria parasite Plasmodium knowlesi across northern Sabah, Malaysia: a population-based cross-sectional survey , 2019, The Lancet. Planetary health.

[11]  B. Goossens,et al.  Long-Tailed Macaque Response to Deforestation in a Plasmodium knowlesi-Endemic Area , 2019, EcoHealth.

[12]  T. Yeo,et al.  Plasmodium knowlesi Malaria in Sabah, Malaysia, 2015–2017: Ongoing Increase in Incidence Despite Near-elimination of the Human-only Plasmodium Species , 2019, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[13]  A. Cook,et al.  The Role of Ecological Linkage Mechanisms in Plasmodium knowlesi Transmission and Spread , 2019, EcoHealth.

[14]  J. Cox,et al.  Predictive analysis across spatial scales links zoonotic malaria to deforestation , 2019, Proceedings of the Royal Society B.

[15]  N. Day,et al.  Asymptomatic Natural Human Infections With the Simian Malaria Parasites Plasmodium cynomolgi and Plasmodium knowlesi , 2018, The Journal of infectious diseases.

[16]  C. Groves Primate taxonomy , 2018, The International Encyclopedia of Biological Anthropology.

[17]  J. Cox,et al.  Exposure and infection to Plasmodium knowlesi in case study communities in Northern Sabah, Malaysia and Palawan, The Philippines , 2018, PLoS neglected tropical diseases.

[18]  W. Hawley,et al.  Malaria elimination in Indonesia: halfway there. , 2018, The Lancet. Global health.

[19]  W. Hawley,et al.  Two clusters of Plasmodium knowlesi cases in a malaria elimination area, Sabang Municipality, Aceh, Indonesia , 2018, Malaria Journal.

[20]  T. Yeo,et al.  Age-Related Clinical Spectrum of Plasmodium knowlesi Malaria and Predictors of Severity , 2018, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[21]  P. Brey,et al.  First case of human infection with Plasmodium knowlesi in Laos , 2018, PLoS neglected tropical diseases.

[22]  K. Battle,et al.  A global map of travel time to cities to assess inequalities in accessibility in 2015 , 2018, Nature.

[23]  J. Cox,et al.  Individual-level factors associated with the risk of acquiring human Plasmodium knowlesi malaria in Malaysia: a case-control study , 2017, The Lancet. Planetary health.

[24]  C. Sutherland,et al.  Contribution of Plasmodium knowlesi to Multispecies Human Malaria Infections in North Sumatera, Indonesia , 2017, The Journal of infectious diseases.

[25]  B. Greenhouse,et al.  Malaria risk factor assessment using active and passive surveillance data from Aceh Besar, Indonesia, a low endemic, malaria elimination setting with Plasmodium knowlesi, Plasmodium vivax, and Plasmodium falciparum , 2016, Malaria Journal.

[26]  Samir Bhatt,et al.  Estimating Geographical Variation in the Risk of Zoonotic Plasmodium knowlesi Infection in Countries Eliminating Malaria , 2016, PLoS neglected tropical diseases.

[27]  I. Vythilingam,et al.  Current status of Plasmodium knowlesi vectors: a public health concern? , 2016, Parasitology.

[28]  Nick Golding,et al.  Predicting the geographical distributions of the macaque hosts and mosquito vectors of Plasmodium knowlesi malaria in forested and non-forested areas , 2016, Parasites & Vectors.

[29]  C. Sutherland,et al.  Molecular identification of human plasmodium knowlesi infections in North Sumatera, Indonesia , 2016 .

[30]  J. Cox,et al.  Plasmodium knowlesi transmission: integrating quantitative approaches from epidemiology and ecology to understand malaria as a zoonosis , 2016, Parasitology.

[31]  J. Cox,et al.  Asymptomatic and Submicroscopic Carriage of Plasmodium knowlesi Malaria in Household and Community Members of Clinical Cases in Sabah, Malaysia , 2015, The Journal of infectious diseases.

[32]  J. Townsend,et al.  Mapping Disease Transmission Risk: Enriching Models Using Biogeography and Ecology , 2015, Emerging Infectious Diseases.

[33]  Peter M. Atkinson,et al.  An effective approach for gap-filling continental scale remotely sensed time-series , 2014, ISPRS journal of photogrammetry and remote sensing : official publication of the International Society for Photogrammetry and Remote Sensing.

[34]  C. Justice,et al.  High-Resolution Global Maps of 21st-Century Forest Cover Change , 2013, Science.

[35]  Y. D. Sharma,et al.  Discordance in drug resistance-associated mutation patterns in marker genes of Plasmodium falciparum and Plasmodium knowlesi during coinfections. , 2013, The Journal of antimicrobial chemotherapy.

[36]  Balbir Singh,et al.  Human Infections and Detection of Plasmodium knowlesi , 2013, Clinical Microbiology Reviews.

[37]  A. Tatem,et al.  High Resolution Population Distribution Maps for Southeast Asia in 2010 and 2015 , 2013, PloS one.

[38]  R. Hijmans,et al.  Cross-validation of species distribution models: removing spatial sorting bias and calibration with a null model. , 2012, Ecology.

[39]  Robert P. Anderson,et al.  Ecological Niches and Geographic Distributions (MPB-49) , 2011 .

[40]  David L. Smith,et al.  Modelling the global constraints of temperature on transmission of Plasmodium falciparum and P. vivax , 2011, Parasites & Vectors.

[41]  Steven J. Phillips,et al.  The art of modelling range‐shifting species , 2010 .

[42]  Damien Sulla-Menashe,et al.  MODIS Collection 5 global land cover: Algorithm refinements and characterization of new datasets , 2010 .

[43]  Kim-Sung Lee,et al.  Morphological features and differential counts of Plasmodium knowlesi parasites in naturally acquired human infections , 2009, Malaria Journal.

[44]  J. Barnwell,et al.  Plasmodium knowlesi: finally being recognized. , 2009, The Journal of infectious diseases.

[45]  P. Potapov,et al.  Mapping the World's Intact Forest Landscapes by Remote Sensing , 2008 .

[46]  J Elith,et al.  A working guide to boosted regression trees. , 2008, The Journal of animal ecology.

[47]  W. Cohen,et al.  MODIS tasselled cap: land cover characteristics expressed through transformed MODIS data , 2007 .

[48]  T. Hastie,et al.  Variation in demersal fish species richness in the oceans surrounding New Zealand: an analysis using boosted regression trees , 2006 .

[49]  A. Townsend Peterson,et al.  Novel methods improve prediction of species' distributions from occurrence data , 2006 .

[50]  J. Fleagle Primate Taxonomy.Smithsonian Series in Comparative Evolutionary Biology. ByColin Groves.Washington (DC): Smithsonian Institution Press. $65.00. viii + 350 p; ill.; index. ISBN: 1–56098–872‐X. 2001. , 2002 .

[51]  J. Friedman Greedy function approximation: A gradient boosting machine. , 2001 .

[52]  G. De’ath,et al.  CLASSIFICATION AND REGRESSION TREES: A POWERFUL YET SIMPLE TECHNIQUE FOR ECOLOGICAL DATA ANALYSIS , 2000 .

[53]  W. Keydel,et al.  Shuttle Radar Topography Mission , 2000 .

[54]  E. Alpert,et al.  Experimental mosquito-transmission of Plasmodium knowlesi to man and monkey. , 1968, The American journal of tropical medicine and hygiene.

[55]  W. Stewart Ministry , 1962 .

[56]  R. Vignon HEALTH ORGANIZATION , 1925, Techniques hospitalieres, medico-sociales et sanitaires.

[57]  C. Drakeley,et al.  Epidemiology of the zoonotic malaria Plasmodium knowlesi in changing landscapes. , 2021, Advances in parasitology.

[58]  N. Anstey,et al.  Clinical management of Plasmodium knowlesi malaria. , 2021, Advances in parasitology.

[59]  Gao Qi,et al.  Global technical strategy for malaria 2016–2030 , 2015 .

[60]  Olfn Khuh Wr Grzqordg,et al.  Recent advances in the management of Plasmodium knowlesi infection , 2014 .

[61]  William K. Reisen,et al.  Landscape epidemiology of vector-borne diseases. , 2010, Annual review of entomology.

[62]  Steven J. Phillips,et al.  Sample selection bias and presence-only distribution models: implications for background and pseudo-absence data. , 2009, Ecological applications : a publication of the Ecological Society of America.

[63]  W. Collins,et al.  Primate malarias. , 1974, Advances in veterinary science and comparative medicine.