Gastrointestinal Helminths in Large Felines from a Zoo in Malaysia

The study was conducted at the zoo which covers 110 acres of land and is occupied by a total of 5,317 animals from 476 species of mammals, amphibians, fishes, birds, and reptiles. This study involved 10 large felines which consist of five pumas (Puma concolor), three African lions (Panthera leo), a spotted leopard (Panthera pardus), and a black panther (Panthera onca). All animals were adults aged more than one year old, and individual data is recorded in Table I. All animals did not show any clinical signs associated with parasitic infections such as diarrhoea and had good body condition scores.

The animals were mainly housed in two different locations inside the zoo. The pumas were housed in the Mammalian Kingdom section which was located further north compared to the other species in this study which were housed in the Carnivores section and located in the centre of the zoo. Every day after the animals were released into the exhibition area, the night holding facilities were cleaned with a high-pressure water pipe. In the exhibition area the faeces was removed once every two days. The large felines in the zoo were fed once daily in the evening when the animals return to their holding facilities after visiting hours. Their diet consists of mainly poultry meat and beef, and there are livestock reared for feeding purposes to the carnivorous animals in the zoo. Other than that, the pumas are sometimes fed with white rats once every week.

A total of 10 faecal samples (one faeces per animal) were collected according to individual animals listed in Table I. Some of the animals are kept together in one cage, therefore before sample collection, with help from the zoo management team, the animals (pumas and African lions) were kept separately for this purpose. Sample collections were conducted in the morning, after the animals were released into the exhibition area and before the cages were cleaned. All samples were subjected to simple floatation technique by using salt solution (Sodium Nitrate, specific gravity= 1.30) and formalin–ether sedimentation technique.

In general, the fecal consistency was well-formed faeces for all fecal samples without any sign of diarrhea. All animals in the present study were infected with nematodes (n= 10), while cestode infection (10 %; n=1/10) and protozoan infection (10 %; n=1/10) were also observed. Half (n=5/10) of the large felines had mixed infections with Toxocara spp. and Ancylostoma spp. All five pumas were infected with Toxocara cati (n = 5/5, 100%) (95% CI: 46.29-98.13) (Supplementary Fig. 1) and one of the pumas suffered from mixed infection with Ancylostoma spp. (n = 1/4, 20%), Oxyuris spp. (n = 1/4, 20%), and Isospora-like oocyst (n = 1/4, 20%) (CI: 1.32-78.05). All three African lions had mixed infections with Toxascaris leonina (n = 3/3, 100%) and Ancylostoma spp. (n = 3/3, 100%) (CI: 30.99-96.82) (Supplementary Fig. 2). The spotted leopard was infected with Toxocara cati (n = 1/1, 100%) while the black panther was suffering from mixed infection with Toxocara cati (n = 1/1, 100%) and a Spirometra spp. (n = 1/1, 100%) (CI: 54.62-89.22).

This is the first documentation of gastrointestinal parasite infection involving large captive felines maintained in a zoo. A previous survey on intestinal parasites of various animals in a Malaysian zoo was described by Lim et al. (2008). The carnivores examined in the present study were infected with at least one gastrointestinal parasite and all identified species have been previously described in captive carnivores. Among these gastrointestinal parasites, two of the identified species (Toxocara cati and Ancylostoma spp.) possess zoonotic potential and can be a source of transmission between animals and humans. In general, Toxocara sp. is known to cause visceral larval migrans and ocular larval migrans (Magnaval, 2001) while Ancylostoma spp. causes cutaneous larval migrans in humans (Bowman, 2010). In comparison with the previous work done in the same zoo in 2008 (Lim et al., 2008), the pumas’ parasite infection changed from single infection with Toxocara cati to mixed infection with Ancylostoma spp., Oxyuris spp., and Isospora sp. eggs. For African lions, the gastrointestinal parasite infection changed from single infection with Toxocara cati to having mixed infection with Toxascaris leonina and Ancylostoma spp. Other than that, the black panther had no gastrointestinal parasites detected previously, but currently suffers from mixed infection with Toxocara cati and Spirometra sp. There are various factors that could contribute to the differences between the 2008 research and this present work. Firstly, the method used for processing and examining the samples were different. In the previous work, direct wet mount was used where small amounts of faeces and only normal saline were used as a medium to examine the presence of gastrointestinal eggs or oocysts. In the present work, simple floatation technique was used as eggs will float in a salt solution which could increase the chances of finding parasite eggs. However, for trematode egg identification the formalin

*No deworming regime stated in the health record.

ether sedimentation techniques were similar for both studies. The most common determinants for differences in prevalence are management practices, animal food source, and other factors (Javaregowda, 2016; Rokib ur Raja et al., 2014). The large felines in the present work harboured gastrointestinal parasites most likely as a result of high environmental contamination as they are kept intensively which increases the chances of parasite infective stages to be abundant in a confined area. Despite proper attention to feeding and maintenance of hygiene, animals that are kept in captivity or in confined areas are prone to different parasitic infections (Lim et al., 2008). In the zoo, the holding cages are cleaned daily while faeces in the exhibition area will be removed once every two days. However, this is not always the case as faeces could be present in the exhibition area for longer than two days. This situation might contribute to the occurrence of gastrointestinal parasite infection that may persist in the environment and lead to constant infection of the animals. Parasitic diseases often represent a major concern in zoo animals for the high environmental contamination and constitutes one of the major problems causing mortality in these animals (Fagiolini et al., 2010). Mortality in these animals might result from changes in the integrity of the host enterocytes (Sheppard, 1974) caused by the gastrointestinal parasites. This causes interference with both intestinal digestion and absorption (Stein and Marquard, 1973) which leads to changes in the architecture of the intestinal villi (Fernando and McCraw, 1973). Subsequently, this leads to increased flow of tissue fluid and blood into the intestinal lumen (Bailey, 1994) thus resulting in the clinical sign of diarrhoea, leaving the host susceptible to secondary bacterial invasion (Li et al., 1996).

The results of this study showed that even with regular faecal examination performed in the zoo, there is still a presence of detectable levels of parasitic infection in these large felines. Other than that, the majority of parasite species detected in this study are known to be zoonotic and transmission to humans is a significant risk. Proper parasite control of the environment as well as food and water sources is important together with providing better quality food with vitamins and minerals as supplements and identifying procedures to diminish the risk of infection (Borghare et al., 2009).

We are grateful to the Director of the zoo for giving permission to collect fecal samples from these large felines. We also want to thanks veterinarian on duty and all animal keepers in their guidance and assistance during sampling.

There is supplementary material associated with this article. Access the material online at: https://dx.doi.org/10.17582/journal.pjz/20190917030922

Authors have declared no conflict of interest.