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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.

Matched MeSH terms: Monkey Diseases/epidemiology
Prevalence of parasites in working pig-tailed Macaques (Macaca nemestrina) in Kelantan, Malaysia

Choong SS, Mimi Armiladiana M, Ruhil HH, Peng TL

J Med Primatol, 2019 08;48(4):207-210.
PMID: 31025372 DOI: 10.1111/jmp.12416

BACKGROUND: Coconut is an important commodity in Kelantan, and pig-tailed macaques (Macaca nemestrina) have been traditionally used for coconut-plucking for over a century. Most of these animals were sourced from the wild population, and the parasitic status of these macaques is unknown, plus the impacts caused by these parasites are usually underestimated by the owners.
METHODS: A total of 30 macaques were sampled for blood, faeces and hair plucks to detect parasite.
RESULTS: Out of 21 faecal samples examined, 11 (52%) were determined positive for one or more gastrointestinal parasites, namely Trichostrongylus spp., Strongyloides spp., Anatrichosoma spp., Capillaria spp., Trichuris spp. and Paramphisotomum spp. Filaria was detected in one (3%) of the blood samples. For ectoparasites, only lice, Pedicinus sp., were found in 9 (30%) macaques.
CONCLUSIONS: It is imperative that the parasitic status of these animals be determined so that necessary actions and preventive measures can be implemented to prevent zoonotic transmissions.

Matched MeSH terms: Monkey Diseases/epidemiology*
Occurrence of gastrointestinal nematodes in captive nonhuman primates at Matang Wildlife Centre, Sarawak

Teo SZ, Tuen AA, Madinah A, Aban S, Chong YL

Trop Biomed, 2019 Sep 01;36(3):594-603.
PMID: 33597481

Gastrointestinal nematodes can cause assorted health problems to human and other primates. The status of gastrointestinal nematodes in non-human primates remained less documented in Malaysia. This study aimed to determine the occurrence of gastrointestinal nematodes recovered from the fecal samples of captive non-human primates at the Matang Wildlife Centre (MWC), Sarawak. Fresh fecal samples were collected from 60 non-human primates of six species (i.e. Orangutan, Bornean gibbon, Silvered Leaf monkey, Slow loris, Pig-tailed macaque, and Long-tailed macaque) and processed using simple fecal floatation method and fecal sedimentation method. This study shows high prevalence of nematode infection (>=50%) and co-infection (22 from 45 infected individuals) in all species of captive non-human primates found in MWC, except one individual of young Silvered Leaf monkey was negative for nematode. From these, eight genera of 11 species and one unknown nematode larvae were recovered and among them Oesophagostomum sp., Ascaris sp., and Strongyloides sp. were the most common nematodes infecting the non-human primates. All the Bornean gibbon (n=7) were found to be infected with nematodes. Moreover, Long-tailed macaques at the centre were heavily infected by Ascaris sp. (number of total count, nt = 2132; total mean abundance, MA=113.70). This is the first report of high prevalence nematode infection on multiple species of captive non-human primates in a wildlife centre located in Sarawak. Some of the nematodes are of zoonotic potential. This information is important for health care management, both in-situ and ex-situ conservations of captive and free-ranging nonhuman primates.

Matched MeSH terms: Monkey Diseases/epidemiology
Serological evidence of infection with Tana and Yaba pox viruses among several species of monkey

Downie AW

J Hyg (Lond), 1974 Apr;72(2):245-50.
PMID: 4362411

Sera from cynomolgus monkeys from Malaysia, from Indian rhesus monkeys, from various species of monkeys from Africa and from South America have been examined for neutralizing antibody to Tanapox and Yaba viruses. No antibody was found to either virus in the sera of rhesus monkeys or South American monkeys. A certain proportion of sera from cynomolgus monkeys and various species of African monkey showed antibody to one or other of the viruses, but few of the positive sera showed antibody to both. The results would seem to suggest that infection with the two viruses is endemic in African and Malaysian monkeys but does not occur or is very rare in Indian rhesus and New World monkeys.

Matched MeSH terms: Monkey Diseases/epidemiology*
Gastrointestinal parasites of zoonotic importance observed in the wild, urban, and captive populations of non-human primates in Malaysia

Adrus M, Zainudin R, Ahamad M, Jayasilan MA, Abdullah MT

J Med Primatol, 2019 02;48(1):22-31.
PMID: 30370934 DOI: 10.1111/jmp.12389

BACKGROUND: A study was undertaken to determine gastrointestinal (GI) parasites commonly found in Malaysia's non-human primates (NHP) living in three different types of populations (wild, urban, and captive) and the basis of major GI parasites of zoonotic importance.
METHODS: A total of 308 samples was collected and microscopically screened from the NHP in the wild (n = 163), urban (n = 76), and captive (n = 69) populations. The samples were taken from 12 species of local NHPs.
RESULTS: At least, 44 species of GI parasites comprising of protozoans (seven species), nematodes (26 species), cestodes (five species), trematodes (five species), and pentastomida (one species) were detected. There were no significant differences for the overall prevalence and no great differences in GI parasite species among the wild, urban, and captive NHP populations.
CONCLUSION: The most common GI parasite was Ascaris spp. (49.7%), followed by Oesophagostomum spp. (26.9%), and 31 species discovered in this study are of known public health importance.

Matched MeSH terms: Monkey Diseases/epidemiology*
Fulltext Macacine Herpesvirus 1 in Long-Tailed Macaques, Malaysia, 2009-2011

Lee MH, Rostal MK, Hughes T, Sitam F, Lee CY, Japning J, et al.

Emerg Infect Dis, 2015 Jul;21(7):1107-13.
PMID: 26080081 DOI: 10.3201/eid2107.140162

Macacine herpesvirus 1 (MaHV1; B virus) naturally infects macaques (Macaca spp.) and can cause fatal encephalitis in humans. In Peninsular Malaysia, wild macaques are abundant, and translocation is used to mitigate human-macaque conflict. Most adult macaques are infected with MaHV1, although the risk for transmission to persons who handle them during capture and translocation is unknown. We investigated MaHV1 shedding among 392 long-tailed macaques (M. fascicularis) after capture and translocation by the Department of Wildlife and National Parks in Peninsular Malaysia, during 2009-2011. For detection of MaHV1 DNA, PCR was performed on urogenital and oropharyngeal swab samples. Overall, 39% of macaques were shedding MaHV1 DNA; rates of DNA detection did not differ between sample types. This study demonstrates that MaHV1 was shed by a substantial proportion of macaques after capture and transport and suggests that persons handling macaques under these circumstances might be at risk for exposure to MaHV1.

Matched MeSH terms: Monkey Diseases/epidemiology
Fulltext Phylogeographic Evidence for 2 Genetically Distinct Zoonotic Plasmodium knowlesi Parasites, Malaysia

Yusof R, Ahmed MA, Jelip J, Ngian HU, Mustakim S, Hussin HM, et al.

Emerg Infect Dis, 2016 Aug;22(8):1371-80.
PMID: 27433965 DOI: 10.3201/eid2208.151885

Infections of humans with the zoonotic simian malaria parasite Plasmodium knowlesi occur throughout Southeast Asia, although most cases have occurred in Malaysia, where P. knowlesi is now the dominant malaria species. This apparently skewed distribution prompted an investigation of the phylogeography of this parasite in 2 geographically separated regions of Malaysia, Peninsular Malaysia and Malaysian Borneo. We investigated samples collected from humans and macaques in these regions. Haplotype network analyses of sequences from 2 P. knowlesi genes, type A small subunit ribosomal 18S RNA and cytochrome c oxidase subunit I, showed 2 genetically distinct divergent clusters, 1 from each of the 2 regions of Malaysia. We propose that these parasites represent 2 distinct P. knowlesi types that independently became zoonotic. These types would have evolved after the sea-level rise at the end of the last ice age, which separated Malaysian Borneo from Peninsular Malaysia.

Matched MeSH terms: Monkey Diseases/epidemiology
Fulltext Admixture in Humans of Two Divergent Plasmodium knowlesi Populations Associated with Different Macaque Host Species

Divis PC, Singh B, Anderios F, Hisam S, Matusop A, Kocken CH, et al.

PLoS Pathog, 2015 May;11(5):e1004888.
PMID: 26020959 DOI: 10.1371/journal.ppat.1004888

Human malaria parasite species were originally acquired from other primate hosts and subsequently became endemic, then spread throughout large parts of the world. A major zoonosis is now occurring with Plasmodium knowlesi from macaques in Southeast Asia, with a recent acceleration in numbers of reported cases particularly in Malaysia. To investigate the parasite population genetics, we developed sensitive and species-specific microsatellite genotyping protocols and applied these to analysis of samples from 10 sites covering a range of >1,600 km within which most cases have occurred. Genotypic analyses of 599 P. knowlesi infections (552 in humans and 47 in wild macaques) at 10 highly polymorphic loci provide radical new insights on the emergence. Parasites from sympatric long-tailed macaques (Macaca fascicularis) and pig-tailed macaques (M. nemestrina) were very highly differentiated (FST = 0.22, and K-means clustering confirmed two host-associated subpopulations). Approximately two thirds of human P. knowlesi infections were of the long-tailed macaque type (Cluster 1), and one third were of the pig-tailed-macaque type (Cluster 2), with relative proportions varying across the different sites. Among the samples from humans, there was significant indication of genetic isolation by geographical distance overall and within Cluster 1 alone. Across the different sites, the level of multi-locus linkage disequilibrium correlated with the degree of local admixture of the two different clusters. The widespread occurrence of both types of P. knowlesi in humans enhances the potential for parasite adaptation in this zoonotic system.

Matched MeSH terms: Monkey Diseases/epidemiology*
[Incidence of diarrhea and antibiotic therapy in cynomolgus monkeys imported for medical use (author's transl)]

Takasaka M, Morota S, Kasono T, Abe M, Honjo S

Jikken Dobutsu, 1973 Jul;22(3):227-36.
PMID: 4204642
Matched MeSH terms: Monkey Diseases/epidemiology*
Fulltext Plasmodium knowlesi: reservoir hosts and tracking the emergence in humans and macaques

Lee KS, Divis PC, Zakaria SK, Matusop A, Julin RA, Conway DJ, et al.

PLoS Pathog, 2011 Apr;7(4):e1002015.
PMID: 21490952 DOI: 10.1371/journal.ppat.1002015

Plasmodium knowlesi, a malaria parasite originally thought to be restricted to macaques in Southeast Asia, has recently been recognized as a significant cause of human malaria. Unlike the benign and morphologically similar P. malariae, these parasites can lead to fatal infections. Malaria parasites, including P. knowlesi, have not yet been detected in macaques of the Kapit Division of Malaysian Borneo, where the majority of human knowlesi malaria cases have been reported. In order to extend our understanding of the epidemiology and evolutionary history of P. knowlesi, we examined 108 wild macaques for malaria parasites and sequenced the circumsporozoite protein (csp) gene and mitochondrial (mt) DNA of P. knowlesi isolates derived from macaques and humans. We detected five species of Plasmodium (P. knowlesi, P. inui, P. cynomolgi, P. fieldi and P. coatneyi) in the long-tailed and pig-tailed macaques, and an extremely high prevalence of P. inui and P. knowlesi. Macaques had a higher number of P. knowlesi genotypes per infection than humans, and some diverse alleles of the P. knowlesi csp gene and certain mtDNA haplotypes were shared between both hosts. Analyses of DNA sequence data indicate that there are no mtDNA lineages associated exclusively with either host. Furthermore, our analyses of the mtDNA data reveal that P. knowlesi is derived from an ancestral parasite population that existed prior to human settlement in Southeast Asia, and underwent significant population expansion approximately 30,000-40,000 years ago. Our results indicate that human infections with P. knowlesi are not newly emergent in Southeast Asia and that knowlesi malaria is primarily a zoonosis with wild macaques as the reservoir hosts. However, ongoing ecological changes resulting from deforestation, with an associated increase in the human population, could enable this pathogenic species of Plasmodium to switch to humans as the preferred host.

Matched MeSH terms: Monkey Diseases/epidemiology*