Veterinary World, EISSN: 2231-0916 RESEARCH ARTICLE

Available at [Link]/Vol.16/December-2023/[Link] Open Access

Prevalence of gastrointestinal parasites in captive mammals at

Khon Kaen Zoo, Thailand
Jirawat Sangpeng1 , Chatanun Eamudomkarn1 , Nuttanan Hongsrichan1 , Atchara Artchayasawat1 ,
Chavin Chaisongkram2 , Kanda Ponsrila2 , Siriwan Kimkamkaew2 , Nonglak Laoprom3 , Thidarut Boonmars1 ,
Paiboon Sithithaworn1 , and Opal Pitaksakulrat1

1. Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand; 2. Department of
Research Conservation and Animal Health, Khon Kaen Zoo, 40280, Thailand; 3. Department of General Science, Faculty
of Science and Engineering, Kasetsart University, Chalermphrakiat Sakon Nakhon Province Campus,
Sakon Nakhon, 47000, Thailand.
Corresponding author: Opal Pitaksakulrat, e-mail: opalpi@[Link]
Co-authors: JS: sjirawat@[Link], CE: chatea@[Link], NH: nuttho@[Link], AA: atchara_a@[Link],
CC: cmzvet@[Link], KP: kanda_plavm16@[Link], SK: bumble-.-bee@[Link], NL: [Link]@[Link],
TB: bthida@[Link], PS: paib_sit@[Link]
Received: 31-07-2023, Accepted: 03-11-2023, Published online: 05-12-2023

doi: [Link]/10.14202/vetworld.2023.2416-2424 How to cite this article: Sangpeng J, Eamudomkarn C,

Hongsrichan N, Artchayasawat A, Chaisongkram C, Ponsrila K, Kimkamkaew S, Laoprom N, Boonmars T, Sithithaworn P,
and Pitaksakulrat O (2023) Prevalence of gastrointestinal parasites in captive mammals at Khon Kaen Zoo, Thailand,
Veterinary World, 16(12): 2416–2424.

Abstract
Background and Aim: Captive animals are susceptible to parasitic diseases due to the stress and confinement they
experience. In addition, they can serve as reservoirs of zoonotic parasites that have the potential to infect humans. To
investigate this possibility, we estimated the prevalence of gastrointestinal (GI) parasites in captive mammals at Khon Kaen
Zoo, Thailand.
Materials and Methods: One hundred and forty-seven individual mammals (37 primates, 43 carnivores, 62 herbivores, and
5 rodents) were examined for parasitic infections by fecal examination daily for 3 consecutive days using the formalin-ethyl
acetate concentration technique (FECT) and the agar plate culture method.
Results: According to FECT, the overall prevalence of GI parasites was 62.6% (92/147). Within animal groups, the numbers
were as follows: 67.6% (25/37) in primates, 23.3% (10/43) in carnivores, 85.5% (53/62) in herbivores, and 80.0% (4/5)
in rodents. Using the agar plate culture method, 21.43% (27/126) were positive for Strongyloides spp. and hookworm
infections. The GI parasites identified belonged to three categories: protozoa (including Entamoeba histolytica species
complex, Entamoeba coli, Giardia spp., coccidia, and ciliated protozoa), trematodes (minute intestinal flukes and rumen
flukes), and nematodes (strongyle/hookworm, Strongyloides spp., Ascarididae, and Trichuris spp.).
Conclusion: The findings of this study indicate the prevalence of several GI parasites in zoo animals with the potential for
transmission to humans, given the animals’ close proximity to both visitors and animal caretakers.
Keywords: captive mammals, gastrointestinal parasites, zoo, zoonotic parasites.
Introduction Entamoeba dispar complex [5, 6]. Toxoplasma gondii
Zoonotic parasitic diseases can lead to substan- was recently detected in humans working in a zoo [7].
tial health complications for captive animals [1] and Many studies have shown that nematode parasites
those responsible for their care, such as animal keep- can spread from animals to humans in shared habi-
ers. Exposure to contaminated feces, soil, and plants tats [8]. In particular, non-human primates (NHPs)
can put individuals at risk of infection [2, 3]. Helminth have a close phylogenetic relationship with humans
infections in captive wild animals can be fatal [4]. and can share nematodes such as Necator ameri-
Moreover, prolonged captivity can amplify the inter- canus, Ancylostoma duodenale, Ascaris lumbricoides,
action among parasite species, animals, and humans, Strongyloides stercoralis, S. fuelleborni, Trichuris
increasing the chances of transmission. Protozoa with trichiura, and Enterobius vermicularis with nearby
zoonotic potential that have been detected in captive humans [9–12].
animals include Giardia duodenalis, Balantioides coli, Animal reservoirs frequently release zoonotic par-
Cryptosporidium spp., and Entamoeba histolytica/ asites into the environment as oocysts, eggs, and larvae
in feces [13–16]. Humans can become infected with GI
Copyright: Sangpeng, et al. Open Access. This article is distributed parasites by consuming contaminated food and water
under the terms of the Creative Commons Attribution 4.0
International License ([Link] containing oocysts or eggs [17–21]. Moreover, direct
by/4.0/), which permits unrestricted use, distribution, and transmission can occur through contact with the feces of
reproduction in any medium, provided you give appropriate credit
to the original author(s) and the source, provide a link to the reservoir animals that retain infective larval stages [22].
Creative Commons license, and indicate if changes were made. “One Health” is a worldwide philosophy primarily con-
The Creative Commons Public Domain Dedication waiver (http://
[Link]/publicdomain/zero/1.0/) applies to the data
cerned with the overlooked zoonotic transmission of
made available in this article, unless otherwise stated. parasites between animals and humans [23, 24].
Veterinary World, EISSN: 2231-0916 2416
 Available at [Link]/Vol.16/December-2023/[Link]

Regrettably, despite the risk of zoonotic trans- based on eggs’ color, shape, and content or the anatomy
mission, little research has addressed the GI para- of trophozoites, larvae, or other propagules [28, 29].
sites in captive wildlife mammals residing within Agar plate culture technique (APCT)
Thailand’s zoos [25, 26]. In response to this knowl- Strongyloides spp. and hookworms were detected
edge gap, we estimated the prevalence of GI parasites using an APCT. A total of 126 fecal samples (each
across a range of captive mammals at Khon Kaen Zoo. approximately 2 g) were available for examination
Materials and Methods by APCT. Filariform larvae of Strongyloides, hook-
Ethical approval
worms, and free-living adults of Strongyloides were
All animal experiments were approved by the investigated after 4-5 days of culture at room tempera-
Animal Ethics Committee of the Zoological Park ture (27°C–35°C).
Organization of Thailand (No.2301638) and the Statistical analysis
Animal Ethics Committee of the Faculty of Medicine, The percentage of individuals infected with each
Khon Kaen University (AEMDKKU 004/2022). species of parasite was calculated. McNemar’s Chi-
Study period and location square test was used to compare proportions from
The study was conducted from March to June paired samples [30] and to determine whether the
2022 in Khon Kaen Zoo, located in Suan Kwang ability to detect a parasite from a single fecal sample
Mountain in Northeastern Thailand (16° 50’ 42.4” N, was significantly different from that based on samples
102° 53’ 48.1” E). Khon Kaen Zoo was established as from 3 consecutive days. Statistical analysis was con-
an ecotourism and research center for the conservation sidered significant at p < 0.05.
of rare and threatened species. Enclosures typically Results
contain a covered part, with completely or partially
The overall prevalence of GI parasites was 62.6%
finished floors, and an area exposed to the environ-
(92/147) in captive mammals at Khon Kaen Zoo,
ment such as a grassy meadow. The animals are fed
Thailand, according to the FECT. Corresponding val-
daily and the enclosures and grounds are cleaned
ues for different groups of mammals were as follows:
daily, generally in the morning.
primates, 67.6% (25/37); carnivores, 23.3% (10/43);
Sample collection and fecal examination herbivores, 85.5% (53/62); and rodents, 80.0% (4/5)
Fecal samples were collected from 147 indi- (Table-3). In addition, 126 fecal samples were exam-
vidual captive mammals housed in Khon Kaen Zoo ined using the APCT and 21.43% (27/126) were posi-
(37 primates, 43 carnivores, 62 herbivores, and 5 tive for Strongyloides or hookworm (Table-4).
rodents: Table-1). To maximize sensitivity, fecal sam- The prevalence of GI parasites in 69 individual
ples from 3 consecutive days were examined. For 69 animals was determined by examination of fecal sam-
individual animals (10 primates, 29 carnivores, and 30 ples collected on 3 consecutive days. The prevalence
herbivores: Table-2), fecal samples were collected on rates were 55.1% (38/69), 49.28% (34/69), and 52.17%
each of 3 consecutive days. Fresh feces were collected (36/69) based on the 1st-, 2nd-, and 3rd-day examination,
directly from the floor of the enclosures. The sample respectively. One new infected individual was detected
was retrieved from the center of the fecal mass, packed on the 2nd day of examination, and three on the 3rd day
in plastic bags with the name of the host species, and (Table-5). The McNemar test showed no statistically
weighed before being transported in an insulated significant differences between day 2 (p > 0.05) and
box (at approximately 15°C) to the laboratory of the the cumulative 3 consecutive days (p > 0.05). The GI
Parasitology Department, Faculty of Medicine, Khon parasites found in captive primates included Giardia
Kaen University. spp., E. histolytica species complex, Entamoeba coli,
Formalin-ethyl acetate concentration technique minute intestinal trematodes, ciliated protozoa, hook-
(FECT) worm, Strongyloides spp., and Trichuris spp. In car-
All fecal samples were analyzed using the nivores, the GI parasites included ciliated protozoa,
FECT [27] with 3 consecutive days’ examinations of Ascarididae, hookworm, and Strongyloides spp. In
each sample (a total of 354 samples). Two grams of herbivores, the feces yielded E. histolytica species
feces were mixed with 10 mL of 10% formalin solu- complex, E. coli, Giardia spp., coccidia cysts, ciliated
tion, filtered into a 15 mL centrifuge tube using two protozoa, rumen flukes, Ascarididae, Trichuris spp.,
layers of gauze, and centrifuged at 500× g for 5 min. strongyles, and Strongyloides spp. (Figures-1–3).
After removing the supernatant, the debris was mixed Rodents had E. histolytica species complex, hook-
with 3 mL of ethyl acetate solution and 7 mL of 10% worms, Strongyloides spp., and Trichuris spp.
formalin solution and centrifuged at 500 g for 5 min.
Discussion
After removing the supernatant, 1 mL of 10% formalin
solution was added to the sediment. Two drops of the In our study, fecal samples were collected
three aliquots were stained with 1% iodine and exam- directly from the floor of zoo animal enclosures.
ined under a light microscope at 10× and 40× magni- This non-invasive approach eliminates the need
fications (Olympus, Japan). Parasites were identified for chemical or mechanical restraint of the animals,
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Table-1: The numbers of captive mammals from which feces were collected and used for parasite identification in Khon
Kaen Zoo, Thailand.

Common name Species Number of individuals

Primate
Chimpanzee Pan troglodytes 4
Bornean Orangutan Pongo pygmaeus 3
Red‑shanked Douc Langur Pygathrix nemaeus 3
Hamadryas baboon Papio hamadryas 3
Ring‑tailed Lemur Lemur catta 8
Tenasserim Lutung Trachypithecus barbei 1
Common Squirrel Monkey Saimiri sciureus 3
Bengal Slow Loris Nycticebus bengalensis 1
Geoffoy’s Marmoset Callithrix geoffroyi 4
Common Marmoset Callithrix jacchus 6
Golden‑handed Tamarin Saguinus midas 1
Total 37
Carnivore
White Lion Panthera leo 2
Lion Panthera leo 4
Malayan Sun Bear Helarctos malayanus 2
Asiatic Black Bear Ursus thibetanus 4
Binturong Arctictis binturong 4
White Tiger Panthera tigris 1
Indo‑Chinese Tiger Panthera tigris corbetti 2
Leopard Cat Prionailurus bengalensis 5
Spotted Hyaena Crocuta crocuta 3
Tanuki Nyctereutes procyonoides viverrinus 4
Small‑clawed Otter Aonyx cinereus 2
Asiatic Jackal Canis aureus 4
Common Palm Civet Paradoxurus hermaphroditus 1
Ferret Mustela putorius furo 2
Meerkat Suricata suricatta 1
Fennec fox Vulpes zerda 1
South American Fur Seal Arctocephalus australis 1
Total 43
Herbivore
Red Kangaroo Macropus rufus 2
white Bennett's Wallaby Macropus rufogriseus 1
Pygmy Hippopotamus Choeropsis liberiensis 5
Southern White Rhinoceros Ceratotherium simum simum 1
Oryx Oryx gazella 2
Springbok Antidorcas marsupialis 1
Barasingha Rucervus duvaucelii 3
Barbary Sheep Ammotragus lervia 3
Ankole‑Watusi Bos taurus indicus 7
Common Barking Deer Muntiacus muntjak 5
Hog Deer Axis porcinus 16
Nyala Tragelaphus angasii 1
Dromedary Camel Camelus dromedarius 1
Nilgai Boselaphus tragocamelus 1
Chinese Serow Capricornis milneedwardsii 1
Burchell’s Zebra Equus quagga burchellii 2
Giraffe Giraffa camelopardalis 2
Spotted Deer Axis axis 1
Rusa Deer Rusa timorensis 2
Elephant Elephas maximus 1
Brow‑Antlered Deer Rucervus eldii thamin 3
Sika Deer Cervus nippon 1
Total 62
Rodentia
Malayan Porcupine Hystrix brachyura 2
Capybara Hydrochoerus hydrochaeris 3
Total 5
All samples 147

thus reducing stress and not affecting their wel- infected) among captive mammals at Khon Kaen Zoo
fare [31, 32]. The significant finding of a considerable raises concerns. Comparable prevalence values have
range of GI parasitic infections (62.6% of animals been reported from zoo populations in other countries,
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Table-2: The numbers of captive mammals from which feces were collected on each of 3 consecutive days and used for
parasite identification in Khon Kaen Zoo, Thailand.

Common name Species Number of individual

Primate
Bornean Orangutan Pongo pygmaeus 3
Red‑shanked Douc Langur Pygathrix nemaeus 1
Ring‑tailed Lemur Lemur catta 3
Tenasserim Lutung Trachypithecus barbei 1
Common Marmoset Callithrix jacchus 1
Golden‑handed Tamarin Saguinus midas 1
Total 10
Carnivore
White Lion Panthera leo 1
Lion Panthera leo 4
Malayan Sun Bear Helarctos malayanus 2
Asiatic Black Bear Ursus thibetanus 4
Binturong Arctictis binturong 1
White Tiger Panthera tigris 1
Indo‑Chinese Tiger Panthera tigris corbetti 2
Leopard Cat Prionailurus bengalensis 1
Spotted Hyaena Crocuta crocuta 3
Tanuki Nyctereutes procyonoides viverrinus 4
Asiatic Jackal Canis aureus 4
Common Palm Civet Paradoxurus hermaphroditus 1
South American Fur Seal Arctocephalus australis 1
Total 29
Herbivore
Red Kangaroo Macropus rufus 2
White Bennett’s Wallaby Macropus rufogriseus 1
Pygmy Hippopotamus Choeropsis liberiensis 1
Southern White Rhinoceros Ceratotherium simum simum 1
Oryx Oryx gazella 2
Springbok Antidorcas marsupialis 1
Ankole‑Watusi Bos taurus indicus 7
Common Barking Deer Muntiacus muntjak 5
Hog Deer Axis porcinus 2
Nyala Tragelaphus angasii 1
Dromedary Camel Camelus dromedarius 1
Nilgai Boselaphus tragocamelus 1
Chinese Serow Capricornis milneedwardsii 1
Burchell’s Zebra Equus quagga burchellii 1
Giraffe Giraffa camelopardalis 2
Elephant Elephas maximus 1
Total 30
All samples 69

Table-3: The overall prevalence of GI parasites in captive and oocysts, capacity for passive oral transmission, and
mammals according to the FECT.
lack of requirement for intermediate hosts [5, 6]. Most
Type Number Parasite parasite infections in wild animals are asymptomatic
of animals positive (%) [39], but stress from captivity can make them symptom-
Primate 37 25 (67.6) atic, resulting in severe clinical symptoms of diarrhea
Carnivore 43 10 (23.3) [40–42]. We detected Giardia spp., E. histolytica species
Herbivore 62 53 (85.5) complex, hookworms, Strongyloides spp., Ascarididae,
Rodents 5 4 (80.0)
Total 147 92 (62.6) and Trichuris spp., all of which have the potential for
transmission in the zoo environment. GI parasites can
GI=Gastrointestinal, FECT=Formalin‑ethyl acetate
concentration technique spread to animal keepers, who may not always be
aware of the risk [43–45]. Prevention of transmission
such as Nepal (19.5%) [33], Malaysia (56.3%) [34], requires a multifaceted approach encompassing suit-
and Bangladesh (60.5%) [35]. Higher prevalence has able medications, food-handling practices, and height-
been reported in some cases, such as 68.3% in the Rio ened sanitation to enhance animal and worker welfare.
de Janeiro Zoo [36], 72.5% in Spain [5], and 71.8% Contaminated food and water are the major sources of
and 74.2% in Brazil [37, 38]. GI parasite infections and are likely the transmission
Identifying protozoans within the captive animal routes of infections that we detected in this study.
in our study reveals the potential for easy transmission The quantity of stool samples adequate to
among hosts due to the environmental resilience of cysts detect intestinal parasites in epidemiologic research
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a b c d

e f g h i j
Figure-1: Figures of gastrointestinal parasites in fecal samples of captive primates. (a) Giardia spp. (40×); (b) Entamoeba
histolytica species complex (40×); (c) Entamoeba coli (40×); (d) Minute intestinal trematode (40×); (e) Ciliated protozoa
(40×); (f) Hookworm (40×); (g) Strongyloides spp. (40×); (h) Trichuris spp. (40×); (i) Hookworm rhabditiform larva
(40×); and (j) Strongyloides spp. rhabditiform larva (40×). Red arrow = Prominent genital primordium.

Table-4: The prevalence of GI parasites in captive mammals according to the APCT.

Types Number Strongyloides spp. (%) Hookworm (%) Mixed infection (%)
Primate 21 4 (19.0) 4 (19.0) 4 (19.0)
Carnivore 38 ‑ 3 (7.9) ‑
Herbivore 62 3 (4.9) 7 (11.3) ‑
Rodent 5 2 (40.0) ‑ ‑
Total 126 9 (7.1) 14 (11.1) 4 (3.2)
GI=Gastrointestinal, APCT=Agar plate culture technique

Table-5: The frequency of detection of GI parasites in improve the detection of organisms such as E. histo-
captive mammals on 3 consecutive days according to the
FECT.
lytica/E. dispar [51, 52]. Collection of fecal samples
in the zoo is quite easy due to the high compliance
Type/ Number Parasite positive New individual of organization, routine cleaning, and regular use of
day on each day (%) discovery
anthelmintic treatments.
Mammal A previous study by Moustafa [53] showed that
Day 1 69 38 (55.07) ‑
Day 2 69 34 (49.28) 1
using three consecutive daily examinations, sensitiv-
Day 3 69 36 (52.17) 3 ity of the agar plate method increased from 70.3%
Total 69 42 (60.87) 4 to 96.2%. Another study revealed a significantly
GI=Gastrointestinal, FECT=Formalin‑ethyl acetate higher cumulative positive rate of S. stercoralis from
concentration technique 13.3% to 22% by examining fecal samples daily for
3 consecutive days [54]. Repeated fecal examinations
is still uncertain [46]. Parasites can produce eggs or clearly increase the evaluation of the prevalence of
cysts intermittently, which means that a single fecal strongyloidiasis, which is an important disease in
examination may not detect all cases. Although tra- humans.
ditional fecal examination techniques, including However, the findings of this study imply that
the APCT, FECT, Baermann technique, and direct the prevalence of GI parasites acquired through a sin-
smear, have been the main reference procedures for gle stool examination using the FECT technique could
diagnosing strongyloidiasis, these techniques have be equally reliable when compared to the results from
low sensitivity and are unreliable due to irregular the analysis of fecal samples collected over 3 consecu-
larval excretion in humans [47, 48] and the high tive days. Importantly, it should be noted that the par-
fluctuation in larval excretion from animals [49]. asites identified in this investigation potentially have
Hence, examination of fecal samples collected on the capacity for zoonotic transmission due to their
multiple days could improve the accuracy of detect- hosts’ close proximity to humans.
ing parasites, making it possible to provide adequate One limitation of this study was the problem
treatment in a timely manner. It is typically recom- of fecal collection from known individuals of herd
mended to examine stool samples collected on 3 animals such as many herbivores. It can be diffi-
different days [50], an approach demonstrated to cult to identify the feces of each animal in a group,
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a b c d

e f g
Figure-2: Figures of gastrointestinal parasites in fecal samples of captive carnivores. (a) Ciliated protozoa (40×); (b-d)
Ascarididae (40×); (e) Hookworm (40×); (f) Strongyloides spp. (40×); and (g) Hookworm rhabditiform larva (40×).

a b c d e f

g h i j k l
Figure-3: Figures of gastrointestinal parasites in fecal samples of captive herbivores. (a) Entamoeba histolytica species
complex (60×); (b) Entamoeba coli (40×); (c) Giardia spp. (40×); (d) Coccidia cyst (60×); (e) Ciliated protozoa (40×);
(f) Rumen fluke (40×); (g) Ascarididae (40×); (h) Trichuris spp. (40×); (i) Strongyle (40×); (j) Strongyloides spp. (40×);
(k) Strongyle rhabditiform larva (40×); and (l) Strongyloides spp. rhabditiform larva (40×). Red arrow = prominent genital
primordium.

particularly if they are free-ranging or have access provide information on the prevalence of parasitic
to shared feeding and watering areas. In these cir- infection in captive mammals and hence inform zoo
cumstances, the collection process can be time-con- management to improve animal welfare and health.
suming and labor-intensive, especially when dealing It is important to minimize the dangers of zoonotic
with a large group. Furthermore, this procedure may infections to tourists, researchers, animal keepers,
induce stress among the animals, leading to potential and veterinarians.
alterations in their behavior and defecation patterns.
Conclusion
Finally, variations might increase as some animals
defecate more frequently or in different locations To the best of our knowledge, this study is the
than others, consequently challenging the accuracy first to investigate the prevalence of GI parasites
of individual fecal collection to reflect the overall in captive mammals kept in the Khon Kaen Zoo
herd prevalence. The results from this study will (includes NHPs, carnivores, herbivores, and rodents)
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