Intestinal parasites in various animals at a zoo in Malaysia

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1 University of Malaya From the SelectedWorks of Yvonne Lim Ai Lian October 20, 2008 Intestinal parasites in various animals at a zoo in Malaysia Yvonne Lim Ai Lian, University of Malaya Available at:

2 Available online at Veterinary Parasitology 157 (2008) Short communication Intestinal parasites in various animals at a zoo in Malaysia Y.A.L. Lim a, *, R. Ngui a, J. Shukri a, M. Rohela a, H.R. Mat Naim b a Department of Parasitology, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia b Hospital & Veterinary Services, Zoo Negara Malaysia, Ulu Klang Ampang, Kuala Lumpur, Malaysia Received 2 April 2008; received in revised form 11 July 2008; accepted 15 July 2008 Abstract A survey was undertaken to investigate the prevalence of intestinal parasites from different groups of mammals housed in a zoological garden in Malaysia. A total of 197 faecal samples were collected randomly from various primates (99), hoofed mammals (70) and feline (28). It was discovered that 89.3% of feline, 54.5% of primates and 45.7% of hoofed mammals were infected with intestinal parasites. Intestinal parasites found in primates were Balantidium coli (19.2%), Cryptosporidium spp. (14.1%), hookworm (10.1%), Trichuris spp. (5.1%), Ascaris (4.0%) and Blastocystis spp. (2.0%). For hoofed mammals, hookworm had the highest prevalence (34.3%) followed by Trichuris spp. and Cryptosporidium spp. (5.7%). Meanwhile, for feline, Toxocara cati was the most prevalent (64.3%), followed by Cryptosporidium spp. (14.3%), Spirometra spp. (7.1%), and hookworm (3.6%). Animals that were infected were all asymptomatic with low parasite load. Routine monitoring of the presence of parasites in animals kept in the zoo is imperative in assisting zoo management in the formulation and implementation of preventive and control measures against the spread of infectious parasitic diseases among animals within the zoo or to humans. # 2008 Elsevier B.V. All rights reserved. Keywords: Intestinal parasites; Zoo animals; Malaysia 1. Introduction In nature, wild animals live on large areas and have consequently a low genetic resistance against parasitic infections because of low exposure. When herds of these wild animals are kept in captivity in zoological gardens, the problem of parasitic infections can aggravate and pose a serious threat to endangered species, occasionally causing sudden and unexpected local declines in abundance (Muoria et al., 2005). Knowledge of their diseases needs to be gained, especially when bred for re-introduction in the wild. Unfortunately, there have been few detailed and comprehensive studies on the prevalence of the * Corresponding author. Tel.: ; fax: address: limailian@um.edu.my (Y.A.L. Lim). intestinal parasites in animals housed in zoological garden. Occurrence of parasites in animals housed in zoological gardens might vary according to the type of husbandry practices, disease prophylaxis and treatment administered. Intensive husbandry of animals produces conditions which facilitates the spread of parasites. The frequent use of antihelmintics often cause resistant strains to evolve. Moreover, the nutritional status of captive animalscanalsoenhance or diminish their resistance to disease (Geraghty et al., 1982). Therefore, this present study attempts to determine the occurrence and intensity of parasites in wild animals in captivity particularly the feline, hoofed mammals and primates. The finding of this study is essential for the development of a better understanding of the gastrointestinal parasite fauna of these animals and for the /$ see front matter # 2008 Elsevier B.V. All rights reserved. doi: /j.vetpar

3 Y.A.L. Lim et al. / Veterinary Parasitology 157 (2008) prevention of the spread of infectious parasitic diseases among animals within the zoo or to humans. 2. Materials and methods 2.1. Study site This study was conducted at Zoo Negara which is located at Ulu Klang, north-east of Kuala Lumpur. The park was officially opened on 14 November 1963 and has a total of over 5000 animals from 459 species of mammals, birds, reptiles, amphibians and fish coming from South East Asia, Asia, Africa and American continents. Over the years, the zoo has transformed itself into an open concept zoo with over 90% of its animals kept in spacious exhibits with landscape befitting its nature Animals and husbandry (housing) This study covered the various families of animals housed in Zoo Negara (feline, hoofed mammals and primates). Sixteen primates species from four families of primates belonging to New World monkeys (Cedidae), Old World monkeys (Cercopithecidae) and families of the apes (Hylobatidae and Homonidae) were analyzed. Meanwhile, 21 hoofed mammals species and 9 feline species were also analyzed. The hoofed mammals can be subclassified into five families namely; Bovidae, Equidae, Camelidae, Cervidae and Giraffidae. All animals were adults (1 year and above) and they did not have symptoms associated with the parasitic infections. The primates were housed in different cages based on their species either individually or in groups of 2 20 individuals per cage. For hoofed mammals, most of the animals lived either singly or in pairs (not more than three individuals) in a herd with a cement or sandy floor covered by wood shavings or surrounded by iron railing at night and will be placed in open-air exhibition area with sandy and grassy soil at day time. Only the herds of Cervidae families were housed in open-air exhibition areas with sandy and grassy soil both day and night. These herds were exposed to the sun most of the time. All feline were placed in open-air exhibition area with sandy and grassy soil at day time and will be relocated to their cages with a cement floor covered by block stone walls and surrounded by iron railing at night. Animals inside the facilities were cleaned daily with high-pressure pipe water. The outdoor facilities with soil and sand were not cleaned with water but, dung was removed daily except at savannah area Faecal samples collection and examination A total of 197 faecal samples were collected randomly from various animals species and subspecies at Zoo Negara. The samples consisted of faecal samples from feline, hoofed mammals and primates which were 28, 70 and 99, respectively. Collection of faecal samples was carried out in the morning with the assistance of the animal s handlers. All samples were processed and examined by direct wet mount preparation, formalin ethyl acetate concentration technique and permanent stains such as trichrome and Ziehl Neelsen stains. 3. Results A total of 197 faecal samples were collected randomly from 46 species or subspecies (99 primate samples, 70 hoofed mammal samples and 28 feline samples). The overall intestinal parasitic infection in the present study was 56.3% with 34.5% samples positive with helminths and 21.8% positive with protozoa (Table 1). Generally, more feline were infected with at least one intestinal parasite, followed by primates and hoofed mammals. Results indicated that helminthes infections are more common compared to protozoa infections in both hoofed mammals and feline. Occurrence of helminthes and protozoa in feline were 75.0 and 14.3%, respectively. For hoofed mammals, 40.0% of samples collected were positive with helminths and 5.7% with protozoa. However for primates, higher occurrence of protozoa (35.4%) was observed compared to helminthes (19.1%). Table 1 The overall occurrence (%) of intestinal parasitic infections among various animals in Zoo Negara Animals Sample size Helminthes positive (%) Protozoa positive (%) Total Feline (75.0) 4 (14.3) 25 (89.3) Primates (19.1) 35 (35.4) 54 (54.5) Hoofed mammals (40.0) 4 (5.7) 32 (45.7) Total (overall) (34.5) 43 (21.8) 111 (56.3)

4 156 Y.A.L. Lim et al. / Veterinary Parasitology 157 (2008) It was found that 64.3% of the samples for feline were positive with Toxocara cati and showed the highest occurrence compared to other intestinal parasites. This is followed by Cryptosporidium spp. (14.3%), Spirometra spp. (7.1%) and hookworm (3.6%). All feline were positive with T. cati except for black panther, while only gir lion was detected positive with hookworm. At the same time, Cryptosporidium spp. was the only protozoan species that was found in this study. Meanwhile, Spirometra spp. which belongs to phylum cestode was detected in leopard cat (Table 2). As for primates, further classification was made according to families which can be subdivided into four families belonging to Cercopithecidae, Hominidae, Hylobatidae and Cebidae. Of the 16 species of primates screened for the presence of intestinal parasites, Balantidum coli (19.2%) had the highest prevalence followed by Cryptosporidium spp. (14.1%), hookworm (10.1%), Trichuris spp. (5.1%) and Ascaris spp. (4.0%). Blastocystis spp. (2.1%) showed the lowest occurrence of infection (Table 2). In hoofed mammals, further classification was made according to different families and it was shown that the samples can be subclassified into five families which were Bovidae, Equidae, Camelidae, Giraffidae and Cervidae. The occurrence of hookworm spp. (34.3%) was the highest among different types of intestinal parasites detected from hoofed mammals. The prevalences of Trichuris spp. and Cryptosporidium spp. were similar, 5.7%, respectively. Hookworm infection was the most common in hoofed mammals and Cryptosporidium spp. was the only protozoa detected (Table 2). Generally, different animals have different diversity of intestinal parasitic infection. It was demonstrated that parasitic infections were highest in primates followed by feline and hoofed mammals. 4. Discussion The majority of the animals examined in this study were infected with at least one intestinal parasite species. All the intestinal parasites species identified in this study have previously been described in captive animals housed in zoological garden by other authors, which are known to be pathogenic to both animals and human (animal handlers and visitors). The present study reported that among the infected primates, there was a higher occurrence of protozoa (35.4%) compared to helminthes (19.1%). Observation in a zoological garden at Kenya found otherwise where higher occurrence of helminthes (64.4%) and lowerofprotozoa(17.1%)(munene et al., 1998). In Belgian zoological gardens, high occurrence of nematodes (36.5%) was also detected among captive primates (Goossens et al., 2005). Presence of Balantidium coli, Cryptosporidium spp. and Blastocystis spp. in the present study have also been reported in other zoological studies (Gomez et al., 2000; Goossens, 2005; Levecke, 2007). As for hoofed mammals, similar findings of occurrence of hookworm and Trichuris spp. particularly in zebra and camel was also reported at Dublin Zoological Garden (Geraghty et al., 1982). It has been recorded that Toxocara spp. is the most common roundworm of FelidaeaswellasCanidae(Abe and Yasukawa, 1996) and in this present study, 64.3% of feline were positive for T. cati. Tapeworms also have been found to be common among zoo animals (Chauhan et al., 1973; Sen Gupta, 1974) but only tapeworm Spirometra spp was detected in this study. Occurrence of Cryptosporidium spp. was observed in every group of animals studied. It was found that 11.2% of samples collected from various animals (primates, hoofed mammals and feline) were positive with Cryptosporidium spp. Cryptosporidium spp. is a widespread protozoa considered to be an important cause of gastrointestinal disease in humans and animals as well. Two studies at the same zoo have also detected Cryptosporidium in birds and have indicated a possible association of cryptosporidiosis among birds and their bird handlers (Rohela et al., 2005; Lim et al., 2007). In other parts of the world, artiodactyl ruminants at the Lisbon Zoo, showed a 4% prevalence of cryptosporidiosis (Delgado et al., 2003) and in Barcelona Zoo, 16.7% of primates and 25.8% of herbivores were positive with Cryptosporidium spp. oocysts (Gomez et al., 2000). The ubiquitous nature of Cryptosporidium in a zoological setup warrants further investigations. Contrastingly, only primates were infected with B. coli (19.2%) and Blastocystis spp. (2.1%) in this study. B. coli was the most prevalent intestinal parasite detected in primates. Similarly, a high prevalence of B. coli (13.0%) infection in primates was observed at Belgian zoological garden (Levecke et al., 2007). In Malaysia and Indonesia, Borneo orang utan and Sumatra orang utan have also been found positive with B. coli (Collet et al., 1986; Kilbourn et al., 2003). Although the occurrence is low, the zoonotic potential of Blastocystis spp. should not be underestimated because Rajah et al. (1999) reported the possibility of these protozoa being

5 Table 2 Occurrence (%) of intestinal parasites in felines, primates and hoofed mammals at Zoo Negara Species N Toxocara cati, Cryptosporidium spp., Spirometra spp., Hookworm, Feline Jungle cat 2 (Felis chaus) 3 3 (100) 1 (33.3) Sumatran tiger 1/2 (P.t. sumatrae) 3 3 (100) 1 (33.3) Indochinese tiger 1/2 3 2 (66.7) 1 (33.3) Pathera tigris corbetti) Malayan tiger 1/2 (P.t. jacksoni) 3 2 (66.7) 1 (33.3) Gir lion 1/2 (P. leo persica) 3 2 (66.7) 1 (33.3) Africa lion 1/2 (P. leo leo) 3 2 (66.7) Leopard cat 2 (Felis bengalensis) 4 2 (50.0) 2 (50.0) Puma 1/2 (Panthera concolor) 4 2 (50.0) Black panther 2 (Panthera onca) 2 Total for feline (64.3) 4 (14.3) 2 (7.1) 1 (3.6) Balantidum coli, Ascaris spp., Trichuris spp., Blastocytis spp., Primates Family Cercopithecidae Stump-tailed macaque (20.0) 1 (20.0) 4 (80.0) Bonnet macaque (25.0) 2 (50.0) 1 (25.0) Long-tailed macaque (25.0) Pig-tailed macaque (12.5) 1 (12.5) 1 (12.5) 1 (12.5) Silvered-leaf monkey (22.2) 2 (22.2) Lion-tailed macaque (14.3) Dusky-leaf monkey (50.0) Hanuman langur (14.3) Olive baboon 2 6 Family Hominidae Sumatra Orang Utan 1/2 3 2 (66.7) 1 (33.3) Borneo Orang Utan 1/2 9 5 (55.6) 4 (44.4) 4 (44.4) Chimpanzee 1/ (36.4) 4 (36.4) Family Hylobatidae White-handed gibbon (16.7) 1 (16.7) Borneo gibbon (50.0) 1 (25.0) Siamang 2 4 Family Cebidae Brown capuchin 2 2 Total for primates (14.1) 1 (10.1) 19 (19.2) 4 (4.0) 5 (5.1) 2 (2.1) Hoofed mammals Family Bovidae Sable antelope (Hippotragus niger) 1/2 4 2 (50.0) 3 (75.0) Y.A.L. Lim et al. / Veterinary Parasitology 157 (2008)

6 158 Table 2 (Continued ) Species N Toxocara cati, Cryptosporidium spp., Spirometra spp., Hookworm, Balantidum coli, Ascaris spp., Trichuris spp., Nilghai 3 2 (66.7) (Boselaphus tragocamelus) 2 Seladang India/Gaur 3 2 (66.7) (Bos gaurus gaurus) 1 Seladang Malaysia 3 2 (66.7) (Bos gaurus hubbacki) 1 Oryx (Oryx dammah) 1/2 4 2 (50.0) Red lechwe (Kobus leche) 1/2 4 2 (50.0) Ankole cattle (Bos taurus) (25.0) 2 (50.0) Nyala (Tragelaphus angasii) 1 3 Serow 2 (Carpricornis sumatraensis) 1 Banteng (Bos javanicus) 1 3 Family Equidae Boehm s zebra 5 1 (20.0) 4 (80.0) (Equus burchellii) 1/2 Horse (Equus caballus) (66.7) Donkey (Equus asinus) (33.3) 1 (33.3) Family Camelidae Camel 5 2 (40.0) 1 (20.0) (Camelus carmelopardalis) 1/2 Guanaco (Lama guanicoe) 1 2 Family Giraffidae Giraffe (Giraffa carmelopardalis) 1/2 4 1 (25.0) 1 (25.0) Family Cervidae Axis deer (Axis - axis) 1 3 Hog deer (Carvus porcinus) 1 3 Sambar deer (Carvus unicolor) 1 3 Barking deer (Muntiacus muntjak) 1 3 Mouse deer 1 3 Total for hoofed mammals 70 4 (5.7) 24 (34.3) 4 (5.7) n = number of positive samples. N = number of samples collected and examined. 1 = grassed/soil enclosure. 2 = concrete enclosure. Blastocytis spp., Y.A.L. Lim et al. / Veterinary Parasitology 157 (2008)

7 Y.A.L. Lim et al. / Veterinary Parasitology 157 (2008) transmitted to humans or other animals as shown in their study where animal handlers at the zoo were reported to be infected with Blastocystis spp. However, there were no clinical symptoms seen in these animal handlers (Rajah et al., 1999). 5. Conclusion This study indicated the importance of monitoring levels of parasitic infections in zoological garden. The present study has found that 89.3, 54.5 and 45.7% of feline, primates and hoofed mammals were infected with intestinal parasites, respectively. The results of this study showed that even with high standards of husbandry at Zoo Negara coupled with regular faecal examinations by the Veterinary Laboratory there remains a detectable level of parasitic infection. It is felt that if standards were lowered or husbandry or examination levels were relaxed a higher degree of infection would become evident. The intestinal parasites recorded in this study are known to be of human pathogenic importance as potential source for zoonotic transmission between animal and human especially among animal handlers. Conflict of interest statement The authors have no conflicts of interest concerning the work reported in this paper. Acknowledgements The authors are very grateful to the Director of Zoo Negara, Malaysia, Dr Mohamad Ngah for giving permission to collect faecal samples from various animals within the zoo. Special thanks also goes to the veterinarian in charge and all animal keepers for providing guidance and technical assistance during the samples collection. Authors contributions: Lim YAL, Rohela M and Mat Naim HR designed the study protocol; Ngui R and Shukri J carried out the field and laboratory work; Lim YAL, Ngui R and Shukri J drafted the manuscript. All authors read and approved the final manuscript. Lim YAL and Rohela M are guarantors of the paper. References Abe, N., Yasukawa, A., Prevalence of Toxocara spp. Eggs in sandpits of parks in Osaka city, Japan, with notes on the prevention of egg contamination by fence construction. J. Vet. Med. Sci. 59, Chauhan, P.P.S., Bhatia, B.B., Arora, G.S., Agrawal, R.D., Ahluwalia, S.S., A preliminary survey of parasitic infections among mammals and birds at Lucknow and Delhi Zoo. Indian J. Anim. Sci. 43 (2), Collet, J., Galdikas, B.M.F., Sugarjito, J., Jojosudharmo, S.A., Coprological study of parasitism in Orang Utan (Pongo pygmaeus) in Indonesia. J. Med. Primatol. 15, Delgado, E., Fonseca, I.P., Fazendeiro, I., Matos, O., Antunes, F., Cunha, M.B., Cryptosporidium spp. in ruminants at the Lisbon Zoo. J. Zoo Wild Med. 34, Geraghty, V., Mooney, J., Pike, K., A study of parasitic infections in mammals and birds at the Dublin Zoological Garden. Vet. Res. Commun. 5, Gomez, M.S., Torres, J., Gracenea, M., Fernadez-Morán, J., Gonzales- Moreno, O., Further report on Cryptosporidium in Barcelona zoo mammals. Parasitol. Res. 86, Goossens, E., Dorny, P., Boomker, J., Vercammen, F., Vercruysse, J., A 12-month survey of the gastro-intestinal helminths of antelopes, gazelles and giraffids kept at two zoos in Belgium. Vet. Parasitol. 127, Kilbourn, A.M., Karesh, W.B., Wolfe, N.D., Bosi, E.J., Cook, R.A., Andau, M., Health evaluation of free-ragging and semicaptive Orang Utan (Pongo pygmaeus) in Sabah, Malaysia. J. Wildl. Dis. 39, Lim, Y.A.L., Rohela, M., Muhamat Shukri, M., Cryptosporidiosis among birds and bird handlers at Zoo Negara, Malaysia. Southeast Asian J. Trop. Med. Public Health 38 (Suppl. 1), Levecke, B., Dorny, P., Geurden, T., Vercammen, F., Vercruysse, J., Gastrointestinal protozoa in primates of four zoological gardens in Belgium. Vet. Parasitol. 148, Munene, E., Otsyula, M., Mbaabu, D., Mutahi, W.T., Muriuki, S.M.K., Helminth and protozoan gastro-intestinal (GIT) parasites in captive and wild-trapped African non human primates. Vet. Parasitol. 78, Muoria, P.K., Muruthi, P., Rubenstein, D., Oguge, N.O., Munene, E., Cross-sectional survey of gastro-intestinal parasites of Grevy s zebras in southern Samburu, Kenya. Afr. J. Ecol. 43, Rajah, S., Suresh, G.K., Vellayan, J.W., Khairul Anuar, M.A., Init, I., Vennila, R., Saminathan, R., Blastocystis in animal s handlers. Parasitol. Res. 85, Rohela, M., Lim, Y.A.L., Jamaiah, I., Khadijah, P.Y., Laang, S.T., Nazri, M.H., et al., Occurrence of Cryptosporidium oocysts in Wrinkled Hornbill and other birds in the Kuala Lumpur National Zoo. Southeast Asian J. Trop. Med. Public Health 36 (4), Sen Gupta, M.R., A preliminary report on diseases and parasites of zoo animal s birds and reptiles. Indian J. Anim. Health 13,