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The vectors of Plasmodium knowlesi and other simian malarias Southeast Asia: challenges in malaria elimination

Vythilingam I, Chua TH, Liew JWK, Manin BO, Ferguson HM

Adv Parasitol, 2021;113:131-189.
PMID: 34620382 DOI: 10.1016/bs.apar.2021.08.005

Plasmodium knowlesi, a simian malaria parasite of great public health concern has been reported from most countries in Southeast Asia and exported to various countries around the world. Currently P. knowlesi is the predominant species infecting humans in Malaysia. Besides this species, other simian malaria parasites such as P. cynomolgi and P. inui are also infecting humans in the region. The vectors of P. knowlesi and other Asian simian malarias belong to the Leucosphyrus Group of Anopheles mosquitoes which are generally forest dwelling species. Continual deforestation has resulted in these species moving into forest fringes, farms, plantations and human settlements along with their macaque hosts. Limited studies have shown that mosquito vectors are attracted to both humans and macaque hosts, preferring to bite outdoors and in the early part of the night. We here review the current status of simian malaria vectors and their parasites, knowledge of vector competence from experimental infections and discuss possible vector control measures. The challenges encountered in simian malaria elimination are also discussed. We highlight key knowledge gaps on vector distribution and ecology that may impede effective control strategies.
Fulltext Neonatal melioidosis case reports-Lessons learned

Daim S, Barnad E, Johnny V, Suleiman M, Jikal M, Chua TH, et al.

Clin Case Rep, 2020 Jan;8(1):171-175.
PMID: 31998510 DOI: 10.1002/ccr3.2584

In endemic regions, include melioidosis in the routine differential diagnosis of neonates with respiratory distress, and consider early empirical ceftazidime treatment for neonates with worsening respiratory distress.
The Role of Ecological Linkage Mechanisms in Plasmodium knowlesi Transmission and Spread

Davidson G, Chua TH, Cook A, Speldewinde P, Weinstein P

Ecohealth, 2019 12;16(4):594-610.
PMID: 30675676 DOI: 10.1007/s10393-019-01395-6

Defining the linkages between landscape change, disease ecology and human health is essential to explain and predict the emergence of Plasmodium knowlesi malaria, a zoonotic parasite residing in Southeast Asian macaques, and transmitted by species of Anopheles mosquitos. Changing patterns of land use throughout Southeast Asia, particularly deforestation, are suggested to be the primary drivers behind the recent spread of this zoonotic parasite in humans. Local ecological changes at the landscape scale appear to be increasing the risk of disease in humans by altering the dynamics of transmission between the parasite and its primary hosts. This paper will focus on the emergence of P. knowlesi in humans in Malaysian Borneo and the ecological linkage mechanisms suggested to be playing an important role.
Forest Restoration and the Zoonotic Vector Anopheles balabacensis in Sabah, Malaysia

Davidson G, Speldewinde P, Manin BO, Cook A, Weinstein P, Chua TH

Ecohealth, 2024 Feb 27.
PMID: 38411846 DOI: 10.1007/s10393-024-01675-w

Anthropogenic changes to forest cover have been linked to an increase in zoonotic diseases. In many areas, natural forests are being replaced with monoculture plantations, such as oil palm, which reduce biodiversity and create a mosaic of landscapes with increased forest edge habitat and an altered micro-climate. These altered conditions may be facilitating the spread of the zoonotic malaria parasite Plasmodium knowlesi in Sabah, on the island of Borneo, through changes to mosquito vector habitat. We conducted a study on mosquito abundance and diversity in four different land uses comprising restored native forest, degraded native forest, an oil palm estate and a eucalyptus plantation, these land uses varying in their vegetation types and structure. The main mosquito vector, Anopheles balabacensis, has adapted its habitat preference from closed canopy rainforest to more open logged forest and plantations. The eucalyptus plantations (Eucalyptus pellita) assessed in this study contained significantly higher abundance of many mosquito species compared with the other land uses, whereas the restored dipterocarp forest had a low abundance of all mosquitos, in particular, An. balabacensis. No P. knowlesi was detected by PCR assay in any of the vectors collected during the study; however, P. inui, P. fieldi and P. vivax were detected in An. balabacensis. These findings indicate that restoring degraded natural forests with native species to closed canopy conditions reduces abundance of this zoonotic malarial mosquito vector and therefore should be incorporated into future restoration research and potentially contribute to the control strategies against simian malaria.
Fulltext Assessing seroprevalence and associated risk factors for multiple infectious diseases in Sabah, Malaysia using serological multiplex bead assays

Chan YL, Patterson CL, Priest JW, Stresman G, William T, Chua TH, et al.

Front Public Health, 2022;10:924316.
PMID: 36388287 DOI: 10.3389/fpubh.2022.924316

BACKGROUND: Infectious diseases continue to burden populations in Malaysia, especially among rural communities where resources are limited and access to health care is difficult. Current epidemiological trends of several neglected tropical diseases in these populations are at present absent due to the lack of habitual and efficient surveillance. To date, various studies have explored the utility of serological multiplex beads to monitor numerous diseases simultaneously. We therefore applied this platform to assess population level exposure to six infectious diseases in Sabah, Malaysia. Furthermore, we concurrently investigated demographic and spatial risk factors that may be associated with exposure for each disease.
METHODS: This study was conducted in four districts of Northern Sabah in Malaysian Borneo, using an environmentally stratified, population-based cross-sectional serological survey targeted to determine risk factors for malaria. Samples were collected between September to December 2015, from 919 villages totaling 10,100 persons. IgG responses to twelve antigens of six diseases (lymphatic filariasis- Bm33, Bm14, BmR1, Wb123; strongyloides- NIE; toxoplasmosis-SAG2A; yaws- Rp17 and TmpA; trachoma- Pgp3, Ct694; and giardiasis- VSP3, VSP5) were measured using serological multiplex bead assays. Eight demographic risk factors and twelve environmental covariates were included in this study to better understand transmission in this community.
RESULTS: Seroprevalence of LF antigens included Bm33 (10.9%), Bm14+ BmR1 (3.5%), and Wb123 (1.7%). Seroprevalence of Strongyloides antigen NIE was 16.8%, for Toxoplasma antigen SAG2A was 29.9%, and Giardia antigens GVSP3 + GVSP5 was 23.2%. Seroprevalence estimates for yaws Rp17 was 4.91%, for TmpA was 4.81%, and for combined seropositivity to both antigens was 1.2%. Seroprevalence estimates for trachoma Pgp3 + Ct694 were 4.5%. Age was a significant risk factors consistent among all antigens assessed, while other risk factors varied among the different antigens. Spatial heterogeneity of seroprevalence was observed more prominently in lymphatic filariasis and toxoplasmosis.
CONCLUSIONS: Multiplex bead assays can be used to assess serological responses to numerous pathogens simultaneously to support infectious disease surveillance in rural communities, especially where prevalences estimates are lacking for neglected tropical diseases. Demographic and spatial data collected alongside serosurveys can prove useful in identifying risk factors associated with exposure and geographic distribution of transmission.
Fulltext A Non-severe Coronavirus Disease 2019 Patient With Persistently High Interleukin-6 Level

Hambali NL, Mohd Noh M, Paramasivam S, Chua TH, Hayati F, Payus AO, et al.

Front Public Health, 2020;8:584552.
PMID: 33304877 DOI: 10.3389/fpubh.2020.584552

Interleukin 6 (IL-6) is one of the markers of immune system activation indicating existent infection and inflammation. We present here a case of a 55-year-old male COVID-19 patient with an unusual high level of interleukin 6 (IL-6). Further investigation revealed he had hepatocellular carcinoma (HCC) with underlying hepatitis B. He did not present with respiratory symptoms although a baseline chest x-ray showed changes, and the patient was categorized as Class 3A of COVID-19. Routine investigations proceeded with high-resolution computed tomography and IL-6 to monitor for progression to severe COVID-19. Notably, there was a high IL-6 level but other parameters did not show he was in severe COVID-19. In this report, we conclude that elevated IL-6 level in a COVID-19 patient is not necessarily associated with severe COVID-19.
Genetic diversity of zoonotic malaria parasites from mosquito vector and vertebrate hosts

Wong ML, Ahmed MA, Sulaiman WYW, Manin BO, Leong CS, Quan FS, et al.

Infect Genet Evol, 2019 09;73:26-32.
PMID: 30999059 DOI: 10.1016/j.meegid.2019.04.010

We explored and constructed haplotype network for simian malaria species: Plasmodium knowlesi, P. cynomolgi and P. inui aiming to understand the transmission dynamics between mosquitoes, humans and macaques. Mosquitoes were collected from villages in an area where zoonotic malaria is prevalent. PCR analysis confirmed Anopheles balabacensis as the main vector for macaque parasites, moreover nearly 60% of the mosquitoes harboured more than one Plasmodium species. Fragments of the A-type small subunit ribosomal RNA (SS rRNA) amplified from salivary gland sporozoites, and equivalent sequences obtained from GenBank were used to construct haplotype networks. The patterns were consistent with the presence of geographically distinct populations for P. inui and P. cynomolgi, and with three discrete P. knowlesi populations. This study provides a preliminary snapshot of the structure of these populations, that was insufficient to answer our aim. Thus, collection of parasites from their various hosts and over time, associated with a systematic analysis of a set of genetical loci is strongly advocated in order to obtain a clear picture of the parasite population and the flow between different hosts. This is important to devise measures that will minimise the risk of transmission to humans, because zoonotic malaria impedes malaria elimination.
Fulltext Parasite community structure in sympatric Bornean primates

Frias L, Hasegawa H, Chua TH, Sipangkui S, Stark DJ, Salgado-Lynn M, et al.

Int J Parasitol, 2021 10;51(11):925-933.
PMID: 33862059 DOI: 10.1016/j.ijpara.2021.03.003

Parasites are important components of ecosystems, influencing trophic networks, competitive interactions and biodiversity patterns. Nonetheless, we are not nearly close to disentangling their complex roles in natural systems. Southeast Asia falls within global areas targeted as most likely to source parasites with zoonotic potential, where high rates of land conversion and fragmentation have altered the circulation of wildlife species and their parasites, potentially resulting in altered host-parasite systems. Although the overall biodiversity in the region predicts equally high, or even higher, parasite diversity, we know surprisingly little about wild primate parasites, even though this constitutes the first step towards a more comprehensive understanding of parasite transmission processes. Here, we characterise the gastrointestinal helminth parasite assemblages of a community of Bornean primates living along the Kinabatangan floodplain in Sabah (Malaysian Borneo), including two species endemic to the island. Through parasitological analyses, and by using several measures of parasite infection as proxies for parasite diversity and distribution, we show that (i) most parasite taxonomic groups are not limited to a single host, suggesting a greater flexibility for habitat disturbance, (ii) parasite infracommunities of nocturnal primates differ from their diurnal counterparts, reflecting both phylogenetic and ecological constraints, and (iii) soil-transmitted helminths such as whipworm, threadworm and nodule worm are widespread across the primate community. This study also provides new parasite records for southern pig-tailed macaques (Macaca nemestrina), silvered langurs (Trachypithecus cristatus) and Western tarsiers (Cephalopachus bancanus) in the wild, while adding to the limited records for the other primate species in the community. Given the information gap regarding primate-parasite associations in the region, the information presented here should prove relevant for future studies of parasite biodiversity and infectious disease ecology in Asia and elsewhere.
Fulltext A pinworm's tale: The evolutionary history of Lemuricola (Protenterobius) nycticebi

Frias L, Hasegawa H, Stark DJ, Lynn MS, Nathan SK, Chua TH, et al.

Int J Parasitol Parasites Wildl, 2019 Apr;8:25-32.
PMID: 30619706 DOI: 10.1016/j.ijppaw.2018.11.009

Lemuricola (Protenterobius) nycticebi is the only pinworm species known to infect strepsirrhine primates outside Africa, and the only pinworm species yet described in slow lorises. Here, we provided a detailed morphological comparison of female and male worms, and a first description of fourth-stage larvae collected from free-living slow lorises (Nycticebus menagensis) in Sabah, Malaysian Borneo. Using mitochondrial and nuclear markers, we also reconstructed the species' phylogenetic relationship with other pinworms infecting primates. Both morphological and molecular results indicated a distinct association between L. (P.) nycticebi and its host. However, while taxonomy identified this species as a member of the Lemuricola clade and grouped pinworms infecting lemurs and slow lorises together, phylogenetic reconstruction split them, placing L. (P.) nycticebi within the Enterobius clade. Our results suggest that L. (P.) nycticebi may represent a different taxon altogether, and that it is more closely related to pinworm species infecting Old World primates outside Madagascar. Pongobius pongoi (Foitová et al., 2008) n. comb. is also proposed.
Development of allele-specific single-nucleotide polymorphism-based polymerase chain reaction markers in cytochrome oxidase I for the differentiation of Bactrocera papayae and Bactrocera carambolae (Diptera: Tephritidae)

Chua TH, Song BK, Chong YV

J Econ Entomol, 2010 Dec;103(6):1994-9.
PMID: 21309218

Differentiation of Bactrocera papayae Drew & Hancock and Bactrocera carambolae Drew & Hancock (Diptera: Tephritidae) based on morphological characters has often been problematical. We describe here a single-nucleotide polymorphism (SNP)-based polymerase chain reaction (PCR) assay to differentiate between these two species. For detection of SNPs, fragments derived from each species were amplified using two primer pairs, COIF/COIR and UEA7/UEA10, sequenced, and aligned to obtain a contiguous 1,517-bp segment. Two new sets of primers were designed based on the 11 SNPs identified in the region. Results of the SNP-PCR test using any one of these species-specific primer sets indicate that these two species could be differentiated on basis of presence or absence of a band in the gel profile. We also tested the SNP-PCR primers on Bactrocera umbrosa F., Bactrocera cucurbitae Coquillett, Bactrocera latifrons Hendel, and Bactrocera tau (Walker) but did not detect any band in the gel, indicating the likelihood of a false positive for B. papayae is nil. This SNP-PCR method is efficient and useful, especially for immature life stages or when only adult body parts of the two species are available for identification, as encountered often in quarantine work.
Fulltext Comparative evaluation of two commercial real-time PCR kits (QuantiFast™ and abTES™) for the detection of Plasmodium knowlesi and other Plasmodium species in Sabah, Malaysia

Nuin NA, Tan AF, Lew YL, Piera KA, William T, Rajahram GS, et al.

Malar J, 2020 Aug 27;19(1):306.
PMID: 32854695 DOI: 10.1186/s12936-020-03379-2

BACKGROUND: The monkey parasite Plasmodium knowlesi is an emerging public health issue in Southeast Asia. In Sabah, Malaysia, P. knowlesi is now the dominant cause of human malaria. Molecular detection methods for P. knowlesi are essential for accurate diagnosis and in monitoring progress towards malaria elimination of other Plasmodium species. However, recent commercially available PCR malaria kits have unpublished P. knowlesi gene targets or have not been evaluated against clinical samples.
METHODS: Two real-time PCR methods currently used in Sabah for confirmatory malaria diagnosis and surveillance reporting were evaluated: the QuantiFast™ Multiplex PCR kit (Qiagen, Germany) targeting the P. knowlesi 18S SSU rRNA; and the abTES™ Malaria 5 qPCR II kit (AITbiotech, Singapore), with an undisclosed P. knowlesi gene target. Diagnostic accuracy was evaluated using 52 P. knowlesi, 25 Plasmodium vivax, 21 Plasmodium falciparum, and 10 Plasmodium malariae clinical isolates, and 26 malaria negative controls, and compared against a validated reference nested PCR assay. The limit of detection (LOD) for each PCR method and Plasmodium species was also evaluated.
RESULTS: The sensitivity of the QuantiFast™ and abTES™ assays for detecting P. knowlesi was comparable at 98.1% (95% CI 89.7-100) and 100% (95% CI 93.2-100), respectively. Specificity of the QuantiFast™ and abTES™ for P. knowlesi was high at 98.8% (95% CI 93.4-100) for both assays. The QuantiFast™ assay demonstrated falsely-positive mixed Plasmodium species at low parasitaemias in both the primary and LOD analysis. Diagnostic accuracy of both PCR kits for detecting P. vivax, P. falciparum, and P. malariae was comparable to P. knowlesi. The abTES™ assay demonstrated a lower LOD for P. knowlesi of ≤ 0.125 parasites/µL compared to QuantiFast™ with a LOD of 20 parasites/µL. Hospital microscopy demonstrated a sensitivity of 78.8% (95% CI 65.3-88.9) and specificity of 80.4% (95% CI 67.6-89.8) compared to reference PCR for detecting P. knowlesi.
CONCLUSION: The QuantiFast™ and abTES™ commercial PCR kits performed well for the accurate detection of P. knowlesi infections. Although the QuantiFast™ kit is cheaper, the abTES™ kit demonstrated a lower LOD, supporting its use as a second-line referral-laboratory diagnostic tool in Sabah, Malaysia.
Fulltext Defining the ecological and evolutionary drivers of Plasmodium knowlesi transmission within a multi-scale framework

Davidson G, Chua TH, Cook A, Speldewinde P, Weinstein P

Malar J, 2019 Mar 08;18(1):66.
PMID: 30849978 DOI: 10.1186/s12936-019-2693-2

Plasmodium knowlesi is a zoonotic malaria parasite normally residing in long-tailed and pig-tailed macaques (Macaca fascicularis and Macaca nemestrina, respectively) found throughout Southeast Asia. Recently, knowlesi malaria has become the predominant malaria affecting humans in Malaysian Borneo, being responsible for approximately 70% of reported cases. Largely as a result of anthropogenic land use changes in Borneo, vectors which transmit the parasite, along with macaque hosts, are both now frequently found in disturbed forest habitats, or at the forest fringes, thus having more frequent contact with humans. Having access to human hosts provides the parasite with the opportunity to further its adaption to the human immune system. The ecological drivers of the transmission and spread of P. knowlesi are operating over many different spatial (and, therefore, temporal) scales, from the molecular to the continental. Strategies to prevent and manage zoonoses, such as P. knowlesi malaria require interdisciplinary research exploring the impact of land use change and biodiversity loss on the evolving relationship between parasite, reservoir hosts, vectors, and humans over multiple spatial scales.
Fulltext Seasonal and Spatial Dynamics of the Primary Vector of Plasmodium knowlesi within a Major Transmission Focus in Sabah, Malaysia

Wong ML, Chua TH, Leong CS, Khaw LT, Fornace K, Wan-Sulaiman WY, et al.

PLoS Negl Trop Dis, 2015;9(10):e0004135.
PMID: 26448052 DOI: 10.1371/journal.pntd.0004135

BACKGROUND: The simian malaria parasite Plasmodium knowlesi is emerging as a public health problem in Southeast Asia, particularly in Malaysian Borneo where it now accounts for the greatest burden of malaria cases and deaths. Control is hindered by limited understanding of the ecology of potential vector species.
METHODOLOGY/PRINCIPAL FINDINGS: We conducted a one year longitudinal study of P. knowlesi vectors in three sites within an endemic area of Sabah, Malaysia. All mosquitoes were captured using human landing catch. Anopheles mosquitoes were dissected to determine, oocyst, sporozoites and parous rate. Anopheles balabacensis is confirmed as the primary vector of. P. knowlesi (using nested PCR) in Sabah for the first time. Vector densities were significantly higher and more seasonally variable in the village than forest or small scale farming site. However An. balabacensis survival and P. knowlesi infection rates were highest in forest and small scale farm sites. Anopheles balabacensis mostly bites humans outdoors in the early evening between 1800 to 2000 hrs.
CONCLUSIONS/SIGNIFICANCE: This study indicates transmission is unlikely to be prevented by bednets. This combined with its high vectorial capacity poses a threat to malaria elimination programmes within the region.
Fulltext Human exposure to zoonotic malaria vectors in village, farm and forest habitats in Sabah, Malaysian Borneo

Brown R, Chua TH, Fornace K, Drakeley C, Vythilingam I, Ferguson HM

PLoS Negl Trop Dis, 2020 09;14(9):e0008617.
PMID: 32886679 DOI: 10.1371/journal.pntd.0008617

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.
Fulltext Investigating the Contribution of Peri-domestic Transmission to Risk of Zoonotic Malaria Infection in Humans

Manin BO, Ferguson HM, Vythilingam I, Fornace K, William T, Torr SJ, et al.

PLoS Negl Trop Dis, 2016 Oct;10(10):e0005064.
PMID: 27741235 DOI: 10.1371/journal.pntd.0005064

In recent years, the primate malaria Plasmodium knowlesi has emerged in human populations throughout South East Asia, with the largest hotspot being in Sabah, Malaysian Borneo. Control efforts are hindered by limited knowledge of where and when people get exposed to mosquito vectors. It is assumed that exposure occurs primarily when people are working in forest areas, but the role of other potential exposure routes (including domestic or peri-domestic transmission) has not been thoroughly investigated.
Fulltext Exposure and infection to Plasmodium knowlesi in case study communities in Northern Sabah, Malaysia and Palawan, The Philippines

Fornace KM, Herman LS, Abidin TR, Chua TH, Daim S, Lorenzo PJ, et al.

PLoS Negl Trop Dis, 2018 Jun;12(6):e0006432.
PMID: 29902171 DOI: 10.1371/journal.pntd.0006432

BACKGROUND: Primarily impacting poor, rural populations, the zoonotic malaria Plasmodium knowlesi is now the main cause of human malaria within Malaysian Borneo. While data is increasingly available on symptomatic cases, little is known about community-level patterns of exposure and infection. Understanding the true burden of disease and associated risk factors within endemic communities is critical for informing evidence-based control measures.
METHODOLOGY/PRINCIPAL FINDINGS: We conducted comprehensive surveys in three areas where P. knowlesi transmission is reported: Limbuak, Pulau Banggi and Matunggung, Kudat, Sabah, Malaysia and Bacungan, Palawan, the Philippines. Infection prevalence was low with parasites detected by PCR in only 0.2% (4/2503) of the population. P. knowlesi PkSERA3 ag1 antibody responses were detected in 7.1% (95% CI: 6.2-8.2%) of the population, compared with 16.1% (14.6-17.7%) and 12.6% (11.2-14.1%) for P. falciparum and P. vivax. Sero-prevalence was low in individuals <10 years old for P. falciparum and P. vivax consistent with decreased transmission of non-zoonotic malaria species. Results indicated marked heterogeneity in transmission intensity between sites and P. knowlesi exposure was associated with agricultural work (OR 1.63; 95% CI 1.07-2.48) and higher levels of forest cover (OR 2.40; 95% CI 1.29-4.46) and clearing (OR 2.14; 95% CI 1.35-3.40) around houses. Spatial patterns of P. knowlesi exposure differed from exposure to non-zoonotic malaria and P. knowlesi exposed individuals were younger on average than individuals exposed to non-zoonotic malaria.
CONCLUSIONS/SIGNIFICANCE: This is the first study to describe serological exposure to P. knowlesi and associated risk factors within endemic communities. Results indicate community-level patterns of infection and exposure differ markedly from demographics of reported cases, with higher levels of exposure among women and children. Further work is needed to understand these variations in risk across a wider population and spatial scale.
Fulltext Phylogenetic analysis of simian Plasmodium spp. infecting Anopheles balabacensis Baisas in Sabah, Malaysia

Chua TH, Manin BO, Daim S, Vythilingam I, Drakeley C

PLoS Negl Trop Dis, 2017 Oct;11(10):e0005991.
PMID: 28968395 DOI: 10.1371/journal.pntd.0005991

BACKGROUND: Anopheles balabacensis of the Leucospyrus group has been confirmed as the primary knowlesi malaria vector in Sabah, Malaysian Borneo for some time now. Presently, knowlesi malaria is the only zoonotic simian malaria in Malaysia with a high prevalence recorded in the states of Sabah and Sarawak.
METHODOLOGY/PRINCIPAL FINDINGS: Anopheles spp. were sampled using human landing catch (HLC) method at Paradason village in Kudat district of Sabah. The collected Anopheles were identified morphologically and then subjected to total DNA extraction and polymerase chain reaction (PCR) to detect Plasmodium parasites in the mosquitoes. Identification of Plasmodium spp. was confirmed by sequencing the SSU rRNA gene with species specific primers. MEGA4 software was then used to analyse the SSU rRNA sequences and bulid the phylogenetic tree for inferring the relationship between simian malaria parasites in Sabah. PCR results showed that only 1.61% (23/1,425) of the screened An. balabacensis were infected with one or two of the five simian Plasmodium spp. found in Sabah, viz. Plasmodium coatneyi, P. inui, P. fieldi, P. cynomolgi and P. knowlesi. Sequence analysis of SSU rRNA of Plasmodium isolates showed high percentage of identity within the same Plasmodium sp. group. The phylogenetic tree based on the consensus sequences of P. knowlesi showed 99.7%-100.0% nucleotide identity among the isolates from An. balabacensis, human patients and a long-tailed macaque from the same locality.
CONCLUSIONS/SIGNIFICANCE: This is the first study showing high molecular identity between the P. knowlesi isolates from An. balabacensis, human patients and a long-tailed macaque in Sabah. The other common simian Plasmodium spp. found in long-tailed macaques and also detected in An. balabacensis were P. coatneyi, P. inui, P. fieldi and P. cynomolgi. The high percentage identity of nucleotide sequences between the P. knowlesi isolates from the long-tailed macaque, An. balabacensis and human patients suggests a close genetic relationship between the parasites from these hosts.
Fulltext Effect of different habitat types on abundance and biting times of Anopheles balabacensis Baisas (Diptera: Culicidae) in Kudat district of Sabah, Malaysia

Chua TH, Manin BO, Vythilingam I, Fornace K, Drakeley CJ

Parasit Vectors, 2019 Jul 25;12(1):364.
PMID: 31345256 DOI: 10.1186/s13071-019-3627-0

BACKGROUND: We investigated the effect of five common habitat types on the diversity and abundance of Anopheles spp. and on the biting rate and time of Anopheles balabacensis (currently the only known vector for Plasmodium knowlesi in Sabah) at Paradason village, Kudat, Sabah. The habitats were forest edge, playground area, longhouse, oil palm plantation and shrub-bushes area. Sampling of Anopheles was done monthly using the human landing catch method in all habitat types for 14 months (October 2013 to December 2014, excluding June 2014). The Anopheles species were morphologically identified and subjected to PCR assay for the detection of Plasmodium parasites. Generalised linear mixed models (GLMM) were applied to test the variation in abundance and biting rates of An. balabacensis in different habitat types.
RESULTS: A total of 1599 Anopheles specimens were collected in the village, of which about 90% were An. balabacensis. Anopheles balabacensis was present throughout the year and was the dominant Anopheles species in all habitat types. The shrub bushes habitat had the highest Anopheles species diversity while forest edge had the greatest number of Anopheles individuals caught. GLMM analysis indicated that An. balabacensis abundance was not affected by the type of habitats, and it was more active during the early and late night compared to predawn and dawn. PCR assay showed that 1.61% of the tested An. balabacensis were positive for malaria parasites, most of which were caught in oil palm estates and infected with one to two Plasmodium species.
CONCLUSIONS: The identification of infected vectors in a range of habitats, including agricultural and farming areas, illustrates the potential for humans to be exposed to P. knowlesi outside forested areas. This finding contributes to a growing body of evidence implicating environmental changes due to deforestation, expansion of agricultural and farming areas, and development of human settlements near to forest fringes in the emergence of P. knowlesi in Sabah.
Fulltext A new paradigm for Aedes spp. surveillance using gravid ovipositing sticky trap and NS1 antigen test kit

Lau SM, Chua TH, Sulaiman WY, Joanne S, Lim YA, Sekaran SD, et al.

Parasit Vectors, 2017 Mar 21;10(1):151.
PMID: 28327173 DOI: 10.1186/s13071-017-2091-y

BACKGROUND: Dengue remains a serious public health problem in Southeast Asia and has increased 37-fold in Malaysia compared to decades ago. New strategies are urgently needed for early detection and control of dengue epidemics.
METHODS: We conducted a two year study in a high human density dengue-endemic urban area in Selangor, where Gravid Ovipositing Sticky (GOS) traps were set up to capture adult Aedes spp. mosquitoes. All Aedes mosquitoes were tested using the NS1 dengue antigen test kit. All dengue cases from the study site notified to the State Health Department were recorded. Weekly microclimatic temperature, relative humidity (RH) and rainfall were monitored.
RESULTS: Aedes aegypti was the predominant mosquito (95.6%) caught in GOS traps and 23% (43/187 pools of 5 mosquitoes each) were found to be positive for dengue using the NS1 antigen kit. Confirmed cases of dengue were observed with a lag of one week after positive Ae. aegypti were detected. Aedes aegypti density as analysed by distributed lag non-linear models, will increase lag of 2-3 weeks for temperature increase from 28 to 30 °C; and lag of three weeks for increased rainfall.
CONCLUSION: Proactive strategy is needed for dengue vector surveillance programme. One method would be to use the GOS trap which is simple to setup, cost effective (below USD 1 per trap) and environmental friendly (i.e. use recyclable plastic materials) to capture Ae. aegypti followed by a rapid method of detecting of dengue virus using the NS1 dengue antigen kit. Control measures should be initiated when positive mosquitoes are detected.
Fulltext Evaluation of electric nets as means to sample mosquito vectors host-seeking on humans and primates

Hawkes F, Manin BO, Ng SH, Torr SJ, Drakeley C, Chua TH, et al.

Parasit Vectors, 2017 Jul 18;10(1):338.
PMID: 28720113 DOI: 10.1186/s13071-017-2277-3

BACKGROUND: Plasmodium knowlesi is found in macaques and is the only major zoonotic malaria to affect humans. Transmission of P. knowlesi between people and macaques depends on the host species preferences and feeding behavior of mosquito vectors. However, these behaviours are difficult to measure due to the lack of standardized methods for sampling potential vectors attracted to different host species. This study evaluated electrocuting net traps as a safe, standardised method for sampling P. knowlesi vectors attracted to human and macaque hosts. Field experiments were conducted within a major focus on P. knowlesi transmission in Malaysian Borneo to compare the performance of human (HENET) or macaque (MENET) odour-baited electrocuting nets, human landing catches (HLC) and monkey-baited traps (MBT) for sampling mosquitoes. The abundance and diversity of Anopheles sampled by different methods were compared over 40 nights, with a focus on the P. knowlesi vector Anopheles balabancensis.
RESULTS: HLC caught more An. balabacensis than any other method (3.6 per night). In contrast, no An. balabacensis were collected in MBT collections, which generally performed poorly for all mosquito taxa. Anopheles vector species including An. balabacensis were sampled in both HENET and MENET collections, but at a mean abundance of less than 1 per night. There was no difference between HENET and MENET in the overall abundance (P = 0.05) or proportion (P = 0.7) of An. balabacensis. The estimated diversity of Anopheles species was marginally higher in electrocuting net than HLC collections, and similar in collections made with humans or monkey hosts.
CONCLUSIONS: Host-baited electrocuting nets had moderate success for sampling known zoonotic malaria vectors. The primary vector An. balabacensis was collected with electrocuting nets baited both with humans and macaques, but at a considerably lower density than the HLC standard. However, electrocuting nets were considerably more successful than monkey-baited traps and representatively characterised anopheline species diversity. Consequently, their use allows inferences about relative mosquito attraction to be meaningfully interpreted while eliminating confounding factors due to trapping method. On this basis, electrocuting net traps should be considered as a useful standardised method for investigating vector contact with humans and wildlife reservoirs.

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