Fig 1 - available from: Malaria Journal
This content is subject to copyright. Terms and conditions apply.
Map of Kalimantan, Indonesia, showing areas (red) where human Plasmodium knowlesi infection was found in Barito Utara, Central Kalimantan (obtained from http://commons.wikimedia.org/ wiki/File: Lokasi Kalimantan Tengah Kabupaten Barito Utara.svg)
Source publication
Background:
The Indonesian archipelago is endemic for malaria. Although Plasmodium falciparum and P. vivax are the most common causes for malaria cases, P. malariae and P. ovale are also present in certain regions. Zoonotic case of malaria had just became the attention of public health communities after the Serawak study in 2004. However, zoonotic...
Citations
... Given this requirement, continued surveillance and mitigation of P. knowlesi throughout at-risk regions of Indonesia will be important. Between the period of 2015 and 2020, a small number of studies have identified substantial numbers of P. knowlesi infections within Indonesia [68][69][70], particularly within northern Sumatra [56,71,72], a region identified as a valuable target for surveillance effort in the 2015 model [31]. Despite this, the Indonesian region of Kalimantan on the island of Borneo still has a relative scarcity of occurrence data given its high predicted transmission suitability and the number of P. knowlesi cases reported in adjacent areas of Malaysia. ...
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.
... Emergence of Plasmodium knowlesi infections has been linked to changes in land cover and land use . While sporadic cases have been reported across Southeast Asia, including in Indonesia (Setiadi et al., 2016 ), the Philippines (Fornace et al., 2018 ), Vietnam (Maeno et al., 2015 ), Brunei (Koh et al., 2019 ) and Myanmar (Ghinai et al., 2017 ), the majority of P. knowlesi cases are found in East Malaysia (Borneo) with hotspots in the states of Sabah and Sarawak (Jeyaprakasam et al., 2020 ), areas that have seen extensive deforestation and landscape modification. In Sabah, human prevalence of P. knowlesi infection has recently been shown to be specifically associated with recent loss of intact forest, agricultural activities, and fragmentation across multiple localised spatial scales Fornace et al., 2019b. ...
Zoonotic disease dynamics in wildlife hosts are rarely quantified at macroecological scales due to the lack of systematic surveys. Non-human primates (NHPs) host Plasmodium knowlesi, a zoonotic malaria of public health concern and the main barrier to malaria elimination in Southeast Asia. Understanding of regional P. knowlesi infection dynamics in wildlife is limited. Here, we systematically assemble reports of NHP P. knowlesi and investigate geographic determinants of prevalence in reservoir species. Meta-analysis of 6322 NHPs from 148 sites reveals that prevalence is heterogeneous across Southeast Asia, with low overall prevalence and high estimates for Malaysian Borneo. We find that regions exhibiting higher prevalence in NHPs overlap with human infection hotspots. In wildlife and humans, parasite transmission is linked to land conversion and fragmentation. By assembling remote sensing data and fitting statistical models to prevalence at multiple spatial scales, we identify novel relationships between P. knowlesi in NHPs and forest fragmentation. This suggests that higher prevalence may be contingent on habitat complexity, which would begin to explain observed geographic variation in parasite burden. These findings address critical gaps in understanding regional P. knowlesi epidemiology and indicate that prevalence in simian reservoirs may be a key spatial driver of human spillover risk.
... Within the last three decades, deforestation for agriculture, mining, and resettlement has substantially reduced the habitat of NHPs in the western part of Indonesia, including the islands of Sumatra, Java, Kalimantan (the Indonesian part of Borneo), Sulawesi, Bali, and the Lesser Sunda Islands [12]. This has led to the intensification of interactions between NHPs and humans in many parts of Indonesia and thus opened up the possibility of pathogen spillover from NHPs, and other wild animals, to humans, as evidenced by reports of cases of zoonotic malaria in Sumatra and Kalimantan [13][14][15]. The aim of the present study was to determine the prevalence of malarial parasite infections in NHPs in five provinces of Indonesia in 2022. ...
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
... Emergence of Plasmodium knowlesi infections has been linked to LULCC . While sporadic cases have been reported across Southeast Asia, including in Indonesia (Setiadi et al., 2016 ), the Philippines (Fornace et al., 2018 ), Vietnam (Maeno et al., 2015 ), Brunei (Koh et al., 2019 ) and Myanmar (Ghinai et al., 2017 ), the majority of P. knowlesi cases are found in East Malaysia (Borneo) with hotspots in the states of Sabah and Sarawak (Jeyaprakasam et al., 2020 ), areas that have seen extensive deforestation and landscape modification. In Sabah, human prevalence of P. knowlesi infection has recently been shown to be specifically associated with recent loss of intact forest, agricultural activities and fragmentation across multiple localised spatial scales Fornace et al., 2019bFornace et al., , 2016. ...
In wildlife and humans, parasite infection has been linked to land conversion and fragmented habitat. However, zoonotic disease dynamics in wildlife hosts are rarely quantified at macroecological scales due to the lack of systematic surveys. Non-human primates (NHPs) host Plasmodium knowlesi, a zoonotic malaria with increasing public health impact and the main barrier to malaria elimination in Southeast Asia. Understanding of regional P. knowlesi infection dynamics in wildlife is limited. Here, we systematically assemble reports of NHP P. knowlesi and investigate how landscape impacts prevalence. Meta-analysis of 6322 NHPs from 148 sites highlights that prevalence is heterogeneous across Southeast Asia, with low overall prevalence and high estimates for Malaysian Borneo. Broadly, we find that regions exhibiting higher prevalence in NHPs overlap with human infection hotspots. By assembling remote sensing data and fitting generalised linear mixed models to prevalence at multiple spatial scales, we identify novel relationships between P. knowlesi in NHPs and forested landscapes. Preliminary evidence suggests that higher prevalence may be contingent on habitat complexity, which might explain geographic variation in parasite burden. Findings address critical gaps in understanding P. knowlesi epidemiology and indicate that prevalence in simian reservoirs may be a key spatial driver of human spillover risk.
... Pigs (Sus spp.) and macaques (Macaca spp.) host high pathogen loads and are known to carry several diseases, including brucellosis, leptospirosis, Nipah, tuberculosis and Japanese encephalitis (discussed further in Section V.5). These species also share high rates of immune similarity with humans, with recent evidence of simian malaria outbreaks in Central Kalimantan, Indonesia (Lee et al., 2011;Barrios-Garcia & Ballari, 2012;Setiadi et al., 2016) acting as disease reservoirs and providing considerable potential for zoonotic disease transfer to humans (Plowright et al., 2017;Shah et al., 2018;Gibb et al., 2020). ...
In many disturbed terrestrial landscapes, a subset of native generalist vertebrates thrives. The population trends of these disturbance-tolerant species may be driven by multiple factors, including habitat preferences, foraging opportunities (including crop raiding or human refuse), lower mortality when their predators are persecuted (the 'human shield' effect) and reduced competition due to declines of disturbance-sensitive species. A pronounced elevation in the abundance of disturbance-tolerant wildlife can drive numerous cascading impacts on food webs, biodiversity, vegetation structure and people in coupled human-natural systems. There is also concern for increased risk of zoonotic disease transfer to humans and domestic animals from wildlife species with high pathogen loads as their abundance and proximity to humans increases. Here we use field data from 58 landscapes to document a supra-regional phenomenon of the hyperabundance and community dominance of Southeast Asian wild pigs and macaques. These two groups were chosen as prime candidates capable of reaching hyperabundance as they are edge adapted, with gregarious social structure, omnivorous diets, rapid reproduction and high tolerance to human proximity. Compared to intact interior forests, population densities in degraded forests were 148% and 87% higher for wild boar and macaques, respectively. In landscapes with >60% oil palm coverage, wild boar and pig-tailed macaque estimated abundances were 337% and 447% higher than landscapes with <1% oil palm coverage, respectively, suggesting marked demographic benefits accrued by crop raiding on calorie-rich food subsidies. There was extreme community dominance in forest landscapes with >20% oil palm cover where two pig and two macaque species accounted for >80% of independent camera trap detections, leaving <20% for the other 85 mammal species >1 kg considered. Establishing the population trends of pigs and macaques is imperative since they are linked to cascading impacts on the fauna and flora of local forest ecosystems, disease and human health, and economics (i.e., crop losses). The severity of potential negative cascading effects may motivate control efforts to achieve ecosystem integrity, human health and conservation objectives. Our review concludes that the rise of native generalists can be mediated by specific types of degradation, which influences the ecology and conservation of natural areas, creating both positive and detrimental impacts on intact ecosystems and human society.
... Within the last 3 decades deforestation for agricultural, mining and human resettlement activities has substantially reduced the habitat of NHPs in the western part of Indonesia, including the islands of Sumatra, Java, Kalimantan (Indonesian part of Borneo), Sulawesi, Bali and the lesser Sunda islands [12]. This situation has intensi ed interaction between human and NHPs in many parts of Indonesia and thus open the possibility of pathogen spill over from NHPs and other wild animal to human as evidenced by reports of zoonotic malaria cases in Sumatra and Kalimantan [13][14][15]. The present study aims to determine the prevalence of malaria parasite infection among the NHPs in four provinces of Indonesia during the period of 2022 through the capture and release of wild ...
... Plasmodium knowlesi the most common cause of zoonotic malaria was only found West Sumatra and Central Java. The ndings are not in accordance with reports of zoonotic malaria cases previously in Aceh and Kalimantan [13][14][15]. In Sabang, Aceh, zoonotic malaria cases were reported to be caused by P, knowlesi [15,27] but this study found out no P. knowlesi infection among the Macaque examined. ...
Background
Indonesia is home for many species of non-human primate (NHP). The current deforestation has substantially reduced the habitat of the NHPs and intensifies interaction with human being and thus open the possibility of pathogen spill over. The present study aims to determine the prevalence of malaria parasite infection among the NHPs in five provinces of Indonesia during the period of 2022 through the capture and release of wild NHPs using a trap installed in several localities surrounding the sanctuary that border the human settlement. The potential Anopheles sp. mosquito that may transmit the pathogen to human was also explored.
Methods
Epidemiologic surveys were conducted through the capture and release of wild NHPs using a trap installed in several localities surrounding the wildlife sanctuary that border the human settlement. Captured NHP was anesthetized and blood samples were aseptically drawn using phlebotomy to make blood smear and dried blood spot (DBS) on filter paper. Infection of the captured NHPs with malaria was determined using light microscopy on Giemsa-stained blood smears and PCR amplification and DNA sequencing of the amplicons using the rPLU oligos. The species of the NHP was determined using the barcoding DNA markers, mitochondrial DNA (mtDNA) Cytochrome Oxidase Subunit I (COI) and Internal transcribed spacer 2 (ITS2) gene of the nuclear ribosomal DNA. Mosquito surveillance included larval collection on breeding sites and adult collection using human landing catch (HLC) and light traps.
Results
Analysis of the DNA extracted from the DBS of the 110 captured NHPs, revealed positive Plasmodium, namely P. cynomolgi, P.coatneyi, P. inui, P. knowlesi and Plasmodium sp. at the prevalence rate of 42% and 50% by microscopy and PCR, respectively. Molecular analysis on the captured NHPs identified several species of Macaca sp. and Hylobates sp. Mosquito surveillance identified several common breeding sites such as ditch, piddle, and natural ponds. Anopheles letifer was found during HLC carried sporozoites of primate malaria.
Conclusion
The findings indicate a high prevalence of primate malaria infection among the NHPs and in certain areas the Anopheles sp. vector that potentially transmit zoonotic malaria such as An. letifer were identified during HLC. Overall, the zoonotic malaria transmission in several areas is immense.
... Several studies have been demonstrated human P. knowlesi infection cases in both Central and South Kalimantan Provinces [13,15,17]. Human P. knowlesi-infected case in South Kalimantan was firstly reported by Figtree and team in 2010 [15], then followed by Ompusunggu and team (2015) [17] in Central and South Kalimantan. ...
... Human P. knowlesi-infected case in South Kalimantan was firstly reported by Figtree and team in 2010 [15], then followed by Ompusunggu and team (2015) [17] in Central and South Kalimantan. The latest publication by Setiadi and team (2016) [13] also discovered the human P. knowlesi infection case in Central Kalimantan Province. Ompusunggu and team in 2015 were discovered three positive P. knowlesi in humans among 287 investigated samples [17]. ...
Human invasion in the forest domain results in close contact between humans and macaques which may increase the potential transmission of zoonotic diseases, including malaria. Primate-to-human cross-species transmission of infectious agents has become a focus of significant scientific interest over the years. This present study aims to identify malaria parasites among macaques in Central and South Kalimantan Provinces, Indonesia. Whole blood of macaques was served as sample and collected from macaques in four sites (Pulang Pisau and Palangkaraya in Central Kalimantan, Tanah Laut and Banjar in South Kalimantan). Malaria parasite species identification was conducted by using microscopy gold standard assessment and Nested Polymerase Chain Reaction (Nested PCR) using specific primer sets against Plasmodium knowlesi, Plasmodium cynomolgi, and Plasmodium inui. A total of 224 macaques had successfully been trapped, of these 215 (96%) were Macaca fascicularis and 9 (4%) were Macaca nemestrina. Out of 224 whole blood samples tested, 49% were Plasmodium positive, with P. inui (57.3%), P. cynomolgi (16.3%), and P. knowlesi (9.9%), both single or mixed infections. With the increasing of humans and macaques contact being reported in Indonesia, particularly in Kalimantan Provinces as a result of deforestation, the cross-species transmission of malaria becomes a significant health issue to be considered. Moreover, discovering many cases of Plasmodium positive macaques in Kalimantan also increases the potential transmission to humans due to contact between both species. Consequently, appropriate malaria excellent surveillance and diagnostic capacity should be significantly improved to support malaria elimination strategy.
... A third report involved PCR analysis of 287 filter paper dried blood spots from malaria patients in Central and South Kalimantan, three of which (1.1%) were positive for P. knowlesi [116]. A fourth report in 2016 of P. knowlesi was the case of a 60-year-old man working at a coal mining site in Central Kalimantan [117]. ...
Kalimantan is a part of Indonesia, which occupies the southern three-quarters of the island of Borneo, sharing a border with the Malaysian states of Sabah and Sarawak. Although most areas of Kalimantan have low and stable transmission of Plasmodium falciparum and Plasmodium vivax, there are relatively high case numbers in the province of East Kalimantan. Two aspects of malaria endemicity in Kalimantan differentiate it from the rest of Indonesia, namely recent deforestation and potential exposure to the zoonotic malaria caused by Plasmodium knowlesi that occurs in relatively large numbers in adjacent Malaysian Borneo. In the present review, the history of malaria and its current epidemiology in Kalimantan are examined, including control and eradication efforts over the past two centuries, mosquito vector prevalence, anti-malarial use and parasite resistance, and the available data from case reports of knowlesi malaria and the presence of conditions which would support transmission of this zoonotic infection.
... Although there is a significant burden of knowlesi malaria in both Sabah and Sarawak, including severe and fatal cases 6,[17][18][19][20] , data relating to the prevalence and clinical sequelae of this infection in humans in Indonesian Borneo are sparse. Only 12 confirmed cases have been reported to date [21][22][23][24][25] and all of these are from South and Central Kalimantan rather than the provinces of West and North Kalimantan bordering Malaysian Borneo. Most data relating to P. knowlesi in Indonesia come from the approximately 400 cases found in Sumatra 26 and Aceh 27 provinces. ...
The simian parasite Plasmodium knowlesi is the predominant species causing human malaria infection, including hospitalisations for severe disease and death, in Malaysian Borneo. By contrast, there have been only a few case reports of knowlesi malaria from Indonesian Borneo. This situation seems paradoxical since both regions share the same natural macaque hosts and Anopheles mosquito vectors, and therefore have a similar epidemiologically estimated risk of infection. To determine whether there is a true cross-border disparity in P. knowlesi prevalence, we conducted a community-based malaria screening study using PCR in Kapuas Hulu District, West Kalimantan. Blood samples were taken between April and September 2019 from 1000 people aged 6 months to 85 years attending health care facilities at 27 study sites within or close to jungle areas. There were 16 Plasmodium positive samples by PCR, five human malarias (two Plasmodium vivax , two Plasmodium ovale and one Plasmodium malariae ) and 11 in which no species could be definitively identified. These data suggest that, if present, simian malarias including P. knowlesi are rare in the Kapuas Hulu District of West Kalimantan, Indonesian Borneo compared to geographically adjacent areas of Malaysian Borneo. The reason for this discrepancy, if confirmed in other epidemiologically similar regions of Indonesian Borneo, warrants further studies targeting possible cross-border differences in human activities in forested areas, together with more detailed surveys to complement the limited data relating to monkey hosts and Anopheles mosquito vectors in Indonesian Borneo.
... It is transmitted to its major natural host, Macaca fascicularis, mostly by mosquitoes of the Anopheles leucosphyrus group, and was thought to be confined to macaque monkeys until the first report of a human infection in Malaysia on April 9, 1965 [14]. It is now responsible for the majority of malaria cases in Malaysia [15][16][17][18][19][20][21][22][23][24][25][26][27][28]. It is suspected that in neighboring countries, including Indonesia, the transmission of P. knowlesi is underestimated due to limited access to high-standard microscopic skills and molecular diagnosis tools [21,29]. ...
... In the same year, another case of P. knowlesi was reported from the same province [16]. Again, in Kalimantan, three (n = 3) cases were positive for P. knowlesi out of 287 malaria cases during the 2013-2014 period: a 28-year-old man and a 50-year-old man were from Central Kalimantan Province and a 28-year-old pregnant woman was from South Kalimantan Province [17,18]. ...
... In North Sumatra province, 377 cases of P. knowlesi were collected in 2015 [22]. A total of 111 Table 1 Plasmodium knowlesi confirmed cases in Indonesia a n = 1 case described in [18] was defined at the same place and date as [17] b n = 19 cases described in [21] were defined at the same place and date as [20] Article 15:258 aggregated cases occurred in this Aceh province between 2015 and 2018 [24]. Aceh and North Sumatra provinces may be considered as the hotspots of Indonesian P. knowlesi (Fig. 2). ...
Background
The Indonesian Republic plans to relocate its capital from Jakarta to East Kalimantan, Borneo Island, in the next few years. This relocation may be associated with deforestation, decreased biodiversity, and an increased risk of emerging zoonotic infections, including Plasmodium knowlesi malaria. The Malaysian part of Borneo Island is one of the main hotspots of P. knowlesi malaria.
Methods
Considering this risk, we evaluated the transmission dynamics of P. knowlesi in the Indonesian Archipelago based on a literature search and extensive review of data from the Indonesian Ministry of Health.
Results
We report that 545 P. knowlesi cases were documented in Indonesia, mainly in the Aceh and North Sumatra provinces, with 95% of these occurring in the last 4 years.
Conclusions
The main P. knowlesi vectors are present in the area of the future capital, requiring strengthened surveillance to reduce the risk of emerging cases in a rapidly growing population.
