Distribution and prevalence of malaria parasites among long-tailed macaques (Macaca fascicularis) in regional populations across Southeast Asia

Abstract

Background: Plasmodium knowlesi and Plasmodium cynomolgi are two malaria parasites naturally transmissible between humans and wild macaque through mosquito vectors, while Plasmodium inui can be experimentally transmitted from macaques to humans. One of their major natural hosts, the long-tailed macaque (Macaca fascicularis), is host to two other species of Plasmodium (Plasmodium fieldi and Plasmodium coatneyi) and is widely distributed in Southeast Asia. This study aims to determine the distribution of wild macaques infected with malarial parasites by examining samples derived from seven populations in five countries across Southeast Asia.Methods: Plasmodium knowlesi, P. cynomolgi, P. coatneyi, P. inui and P. fieldi, were detected using nested PCR assays in DNA samples from 276 wild-caught long-tailed macaques. These samples had been derived from macaques captured at seven locations, two each in the Philippines (n = 68) and Indonesia (n = 70), and one each in Cambodia (n = 54), Singapore (n = 40) and Laos (n = 44). The results were compared with previous studies of malaria parasites in longtailed macaques from other locations in Southeast Asia. Fisher exact test and Chi square test were used to examine the geographic bias of the distribution of Plasmodium species in the macaque populations. Results: Out of 276 samples tested, 177 were Plasmodium-positive, with P. cynomolgi being the most common and widely distributed among all long-tailed macaque populations (53.3 %) and occurring in all populations examined, followed by P. coatneyi (20.4 %), P. inui (12.3 %), P. fieldi (3.4 %) and P. knowlesi (0.4 %). One P. knowlesi infection was detected in a macaque from Laos, representing the first documented case of P. knowlesi in wildlife in Laos. Chi square test showed three of the five parasites (P. knowlesi, P. coatneyi, P. cynomolgi) with significant bias in prevalence towards macaques from Malaysian Borneo, Cambodia, and Southern Sumatra, respectively. Conclusions: The prevalence of malaria parasites, including those that are transmissible to humans, varied among all sampled regional populations of long-tailed macaques in Southeast Asia. The new discovery of P. knowlesi infection in Laos, and the high prevalence of P. cynomolgi infections in wild macaques in general, indicate the strong need of public advocacy in related countries.

Malaria parasites in macaques in Thailand: stump-tailed macaques (Macaca arctoides) are new natural hosts for Plasmodium knowlesi, Plasmodium inui, Plasmodium coatneyi and Plasmodium fieldi

“…A complex nature of Plasmodium spp. infections was observed among the wild macaques studied, which is similar to the results of previous studies on wild macaques in Peninsular Malaysia, Malaysian Borneo, Thailand, Singapore, Laos, Cambodia and the Philippines [34,42,43,44,45,46]. The DNA samples were each collected at single time points and the PCR results may not re ect the actual prevalence or the total number of species of Plasmodium present in each host since it has been observed that the parasitaemia of malaria parasites uctuate over time within a host [2].…”

Ancestry, Plasmodium cynomolgi prevalence and rhesus macaque admixture in cynomolgus macaques (Macaca fascicularis) bred for export in Chinese breeding farms

“…Because these parasites’ infections in humans are likely to originate from close proximity between humans and wild macaques, a thorough understanding of the distribution of the zoonotic malaria parasite in nature is essential in the control and prevention of malaria disease in countries and regions under high risk. Recent studies have shown that P. cynomolgi is one of the most common malarial parasites among wild cynomolgus macaques and is uniformly and widely distributed throughout cynomolgus macaque populations in Southeast Asia . Infections in experimentally infected rhesus macaques result in much more severe clinical manifestations than in cynomolgus macaques .…”

“…Recent studies have shown that P. cynomolgi is one of the most common malarial parasites among wild cynomolgus macaques and is uniformly and widely distributed throughout cynomolgus macaque populations in Southeast Asia. 38,[42][43][44] Infections in experimentally infected rhesus macaques result in much more severe clinical manifestations than in cynomolgus macaques. 36 Furthermore, previous studies reported a significantly higher count of parasites in rhesus macaques than in cynomolgus macaques within the same duration after infection.…”

Primate Infectious Disease Ecology: Insights and Future Directions at the Human-Macaque Interface

“…They also revealed that P. knowlesi, previously hypothesized as having been transmitted to humans via anopheline vectors from overlapping macaque populations, was derived from an ancestral malarial parasite that existed before humans came to Southeast Asia. Since then, high prevalence of P. knowlesi has been detected among free-living macaques at vegetation mosaics and forest fragments in other parts of Southeast Asia, including Indonesia, Cambodia, Laos, and Vietnam (Huffman et al 2013b;Zhang et al 2016). Malaria is now widely recognized as being a threat at human-primate interfaces (Singh et al 2004).…”