Humans frequently exposed to a range of non-human primate malaria parasite species through the bites of Anopheles dirus mosquitoes in South-central Vietnam

Parasites & Vectors, Jul 2015

Background Recent studies have described natural human infections of the non-human primate parasites Plasmodium knowlesi and Plasmodium cynomolgi. In Southeast Asia, mosquitoes of the Anopheles leucosphyrus group bite both humans and monkeys in the forest and thus offer a possible route for Plasmodium species to bridge the species barrier. In this study we analysed the species composition of malarial sporozoites infecting the salivary glands of Anopheles dirus in order to determine their potential role as bridge vectors of Plasmodium parasites from monkeys to humans. Methods Mosquitoes were collected in the forest and forest fringe area of Khanh Phu commune by human-baited landing collection. Anopheles species were determined on the basis of morphologic features. Sporozoite-infected salivary glands were applied to filter paper and dried in an ambient atmosphere, before storage in closed vials at 4–6 °C. Detection and identification of Plasmodium species in salivary glands were carried out by nested-PCR of the small subunit ribosomal RNA gene. Results Six species of Plasmodium parasites were detected by PCR, of which P. vivax was the most common, followed by P. knowlesi, P. inui, P. cynomolgi, P. coatneyi and P. falciparum. Twenty-six of the 79 sporozoite infected mosquitoes showed multiple infections, most of which were a combination of P. vivax with one or more of the non-human primate Plasmodium species. Conclusions These results suggest that humans overnighting in this forest are frequently inoculated with both human and non-human primate malaria parasites, leading to a situation conducive for the emergence of novel zoonotic malaria.

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Humans frequently exposed to a range of non-human primate malaria parasite species through the bites of Anopheles dirus mosquitoes in South-central Vietnam

Maeno et al. Parasites & Vectors Humans frequently exposed to a range of non-human primate malaria parasite species through the bites of Anopheles dirus mosquitoes in South-central Vietnam Yoshimasa Maeno 0 1 Nguyen Tuyen Quang 1 3 Richard Culleton 1 2 Satoru Kawai 1 6 Gaku Masuda 1 5 Shusuke Nakazawa 1 4 Ron P. Marchand 1 3 0 Department of Virology and Parasitology, Fujita Health University School of Medicine , 1-98 Kutsukake, Toyoake, Aichi 470-1192 , Japan 1 Pf = P. falciparum , Pv = P. vivax, Pk = P. knowlesi, Pct = P. coatneyi, Pcy = P. cynomolgi, Pin = P. inui 2 Malaria Unit, Institute of Tropical Medicine, Nagasaki University , Nagasaki, Nagasaki , Japan 3 Khanh Phu Malaria Research Unit, Medical Committee Netherlands-Viet Nam , Nha Trang, Khanh Hoa province , Viet Nam 4 Department of Protozoology, Institute of Tropical Medicine, Nagasaki University , Nagasaki, Nagasaki , Japan 5 The Graduate School of Global Environmental Studies, Kyoto University , Kyoto, Kyoto , Japan 6 Laboratory of Tropical Medicine and Parasitology, Dokkyo Medical University , Mibu, Tochigi , Japan Background: Recent studies have described natural human infections of the non-human primate parasites Plasmodium knowlesi and Plasmodium cynomolgi. In Southeast Asia, mosquitoes of the Anopheles leucosphyrus group bite both humans and monkeys in the forest and thus offer a possible route for Plasmodium species to bridge the species barrier. In this study we analysed the species composition of malarial sporozoites infecting the salivary glands of Anopheles dirus in order to determine their potential role as bridge vectors of Plasmodium parasites from monkeys to humans. Methods: Mosquitoes were collected in the forest and forest fringe area of Khanh Phu commune by human-baited landing collection. Anopheles species were determined on the basis of morphologic features. Sporozoite-infected salivary glands were applied to filter paper and dried in an ambient atmosphere, before storage in closed vials at 4-6 °C. Detection and identification of Plasmodium species in salivary glands were carried out by nested-PCR of the small subunit ribosomal RNA gene. Results: Six species of Plasmodium parasites were detected by PCR, of which P. vivax was the most common, followed by P. knowlesi, P. inui, P. cynomolgi, P. coatneyi and P. falciparum. Twenty-six of the 79 sporozoite infected mosquitoes showed multiple infections, most of which were a combination of P. vivax with one or more of the non-human primate Plasmodium species. Conclusions: These results suggest that humans overnighting in this forest are frequently inoculated with both human and non-human primate malaria parasites, leading to a situation conducive for the emergence of novel zoonotic malaria. Sporozoites; Anopheles dirus; Plasmodium vivax; Plasmodium falciparum; Plasmodium knowlesi; Plasmodium cynomolgi; Plasmodium coatneyi; Plasmodium inui - Background Six malaria parasite species, Plasmodium falciparum, Plasmodium vivax, Plasmodium malariae, Plasmodium ovale wallikeri, Plasmodium ovale curtisi and Plasmodium knowlesi cause disease in humans. In Southeast Asia 13 species of Plasmodium parasites are found in non-human primates [1]. One of these, P. knowlesi, is now a well-known threat to human health in multiple countries in the region [2–6]. Recently, the first naturally acquired human infection of Plasmodium cynomolgi was described from the east coast of Peninsular Malaysia [7]. Little is known regarding the ability of other non-human primate Plasmodium parasites, besides P. knowlesi and P. cynomolgi, to infect humans, though Plasmodium inui, Plasmodium eylesi, Plasmodium schwetzi and others have been recorded as possessing the ability to infect humans as a result of experimental infection [8–16]. Malaria parasites have the ability to switch hosts [17], indeed, it is now thought that of the six species that commonly infect humans, at least three, P. falciparum, P. vivax and P. knowlesi were originally parasites of nonhuman primates that jumped the species barrier to man. Zoonotic malaria infections can only occur when the vectors of non-human malaria parasites come into contact with people. Members of the Anopheles dirus complex are known to be important vectors of human Plasmodium parasites in the forests of Southeast Asia, and An. dirus (Species A) has previously been shown to vector P. knowlesi in Vietnam [6, 18, 19]. In order to assess the risk of potential zoonotic infections with nonhuman primate parasites, we assayed the malaria parasite species composition of sporozoites residing in the salivary glands of forest-caught An. dirus mosquitoes. Here we report the occurrence of P. inui, P. cynomolgi and Plasmodium coatneyi in the salivary glands of humanbiting An. dirus mosquitoes in Vietnam. Methods Parasites Positive control genomic DNA (gDNA) for P. falciparum was obtained from 3D7-9A in vitro cultured parasites, whilst P. vivax and P. malariae gDNA was extracted from (...truncated)


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Yoshimasa Maeno, Nguyen Quang, Richard Culleton, Satoru Kawai, Gaku Masuda, Shusuke Nakazawa, Ron Marchand. Humans frequently exposed to a range of non-human primate malaria parasite species through the bites of Anopheles dirus mosquitoes in South-central Vietnam, Parasites & Vectors, 2015, pp. 376, 8, DOI: 10.1186/s13071-015-0995-y