|
|
Received: 24 May 2018 Revised: 17 September 2018 Accepted: 8 October 2018 DOI: 10.1111/jmp.12389
ORIGINAL ARTICLE
Gastrointestinal parasites of zoonotic importance observed in the wild, urban, and captive populations of non-human primates in Malaysia Madinah Adrus1
| Ramlah Zainudin1 | Mariana Ahamad2 | Mohd-Azlan Jayasilan1 |
Mohd Tajuddin Abdullah3 1 Animal Resource Science and Management Programme, Faculty of Resource Science and Technology, Universiti Malaysia Sarawak (UNIMAS), Kota Samarahan, Sarawak, Malaysia 2
Unit of Acarology, Infectious Diseases Research Centre, Institute for Medical Research, Kuala Lumpur, Malaysia
3
Kenyir Research Institute, Universiti Malaysia Terengganu, Kuala Terengganu, Terengganu, Malaysia Correspondence Madinah Adrus, Animal Resource Science and Management Programme, Faculty of Resource Science and Technology, Universiti Malaysia Sarawak (UNIMAS), Kota Samarahan, Sarawak, Malaysia. Email:
[email protected]
Abstract 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. KEYWORDS
emerging infectious diseases, gastrointestinal parasites, infection, non-human primates, zoonotic
1 | I NTRO D U C TI O N
Because of increasing human connectivity and the potential for disease transmission between humans and NHP, further detailed
Parasitisms in non-human primates (NHP) are influenced by both
investigations of parasite ecology in NHP are warranted, especially
biotic and abiotic factors as well as the biology and ecology of the
at the sites that currently do not have information regarding the
parasites.1 Many studies have shown that parasites are frequently
diversity and prevalence of parasites.10 Understanding the evo-
transmitted from wild NHP or those in captivity to humans in a
lutionary and ecological linkage between NHP and their parasites
shared habitat. 2-4 Recent anthropogenic developments have caused
has to be considered because some parasites can be viewed as in-
habitat destruction for human settlements and urbanization, forest
dicators of species that are potentially of imminent threats to NHP
fragmentation, isolated protected areas, and altered NHP natural
conservation.11,12
habitat.
5,6
Thus, these factors increase the connectivity between
Detailed studies on gastrointestinal (GI) parasites in the wild,13-19
Tourists, researchers, animal keepers, rangers,
urban, 20,21 and captive15,17,18,22-24 populations of NHP worldwide
guides, and unintentional human contacts such as poachers, loggers,
have been conducted from previous researches. One similar study
and villagers are important sources of parasite exposure when they
based on the intestinal parasites of free-ranging, semi-captive, and
7,8
humans and NHP.
9
are exposed with captive, wild, and urban NHP. J Med Primatol. 2018;1–10.
captive Pongo abelli in Sumatera, Indonesia, has been conducted but wileyonlinelibrary.com/journal/jmp © 2018 John Wiley & Sons A/S. | 1 Published by John Wiley & Sons Ltd
|
ADRUS et al.
2
none in Malaysia.25 Besides that, little information is known on the 26-28
the animals as laid down by all the relevant wildlife authorities in
There is a
Malaysia as well as the guidelines by the Institutional Animal Care
grave lack of similar studies related to the survey and the prevalence
and Use Committee (IACUC), University of California, Davis, USA, as
of GI parasites in different NHP populations, and most were reported
adopted by the PREDICT Project (No. 16048) Program in Malaysia
on the captivity26-28 and wild populations of NHP.29-31 None of the
and under collaboration between Department of Wildlife and
prevalence of GI parasites in the NHP in Malaysia.
studies were related directly with GI parasites on urban cases except
National Park (DWNP), Malaysia, and Eco-Health Alliance. All pro-
for individual case reports in Malaysia.32,33 Although some basic data
cedures were reviewed and permitted by Malaysian national laws.
on the diversity and prevalence of parasites are available, a limited
For fecal collection, the rules and regulations on wildlife and animal
number of NHP species and/or GI species was investigated.26-31 Such
welfare was taken into consideration.
studies will not only benefit preventive medicine, but also in captive NHP management and conservation of the wild population. In order to obtain more information on the influence of GI parasites
2.2 | Study areas and subjects
on NHP in Malaysia and possible cross-transmission of these parasites,
This study was conducted in nine locations throughout Peninsular
the determination of parasite prevalence of wild, urban, and captive NHP
Malaysia and Malaysian Borneo (Sabah and Sarawak) from February
was investigated as a main objective of this study. We hypothesized that
2012 to June 2013. Each three locations were represented and
there are differences for the overall prevalence of GI parasites of NHP
selected based on three different targeted types of NHP popula-
and there are great differences in the GI parasite species among the wild,
tions. The NHP populations were categorized as wild, urban, and in
urban, and captive populations. This study also presents checklist on the
captivity. The localities were Penang National Park, Kinabatangan
taxonomic identity of the GI parasites, number of individuals of a host
Wildlife Sanctuary, and Bako National Park (wild population);
species infected with a particular parasite species, number of hosts ex-
Langkawi Island, Perak State, and Selangor State (urban population);
amined, and the prevalence of GI parasites in the host species of NHP.
and Taiping Zoo, National Zoo, and Melaka Zoo (captive population; Figure 1). The study sites were selected based on accessibility and
2 | M ATE R I A L S A N D M E TH O DS
initial efforts to investigate possible interaction of wildlife and potential zoonotic disease transmission near the study areas especially for the wild and captive NHP population. As for the urban NHP
2.1 | Humane care guidelines
population, the study sites were selected based on conflict management of human-monkey programs in collaboration with the DWNP,
All sampling procedures and methods conducted complied with
Malaysia. All samples from all three types of population were col-
the rules, regulations, and ethical standards in the treatment of
lected throughout time period, and the samples were not collected
F I G U R E 1 Map of nine localities of the study sites in Malaysia
|
3
ADRUS et al.
based on each season, whereas in Malaysia, there are wet and dry in
Meanwhile, collection of fecal samples from the captive popula-
a year because the main objective of this study did not include the
tion was carried out in the morning with the assistance of the ani-
different seasonality.
mal’s handler (keepers). Fecal samples were collected randomly from the groups of NHP in same cage if the number of NHP more than
2.3 | Sample collection and parasitological analysis
10 individuals while if the NHP in cages for each species was
