Helminth Parasites in Captive Wildlife in Two Public Zoological Gardens in Southwestern Nigeria

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1 European Journal of Biological Sciences 10 (2): 42-46, 2018 ISSN IDOSI Publications, 2018 DOI: /idosi.ejbs Helminth Parasites in Captive Wildlife in Two Public Zoological Gardens in Southwestern Nigeria 1 2 Ogunyemi Gbemisola, Uwalaka Emmanuel Chibuike, 3 1 Adediran Oyeduntan Adejoju and Adedeji Olufemi Bolarinwa 1 Department of Veterinary, Public Health and Preventive Medicine, University of Ibadan, Nigeria 2 Department of Veterinary Parasitology and Entomology, Micheal Okpara University of Agriculture, Umudike, Nigeria 3 Department of Veterinary Parasitology, University of Ibadan, Nigeria Abstract: A study on helminth parasites on all different classes of animal was conducted at two zoological gardens to determine their presence and zoonotic implications. Fresh faecal samples were collected andprocessed using standard parasitological techniques. These arefloatation method for detection of nematode and cestode eggs, sedimentation method for detection of trematodes and harada-mori culture method for larval culture. Seventy four captive animals were screened. Data obtained were subjected to Chi-square test and a multi-variable adjusted logistic regression as post hoc test with the main outcome measure (RBT test) in bivariate analysis. Out of the 49 animals screened at FUNAAB zoological garden, 22 animals (44.9%) were positive and at OAU zoological garden, 5 animals (20%) were positive out of the 25 animals screened. The general average prevalence of gastro-intestinal helminthes include Nematode Capillariaspp (8.7%), Trichuris spp (11.6%), Strongyloides spp (14.5%), Hookworm (4.3%), Trichostrongylus spp (8.7%), Oesophagostomum spp (1.5%), Pentastomida sp. (11.6%), Syngamus spp (1.5%), Oswaldocruzi spp (2.9%), Physaloptera spp (8.7%), Strongyle (1.5%) and Strongyluris spp (8.7%), Un-identified nematode (5.8%); Cestode - Spirometra spp (5.8%) and Trematode Fasciola spp (2.9%), Un-identified trematode (1.5%). There was significant association between helminth infection and location (OR=4.7, 95%CI: ), class of animals (OR=3.6, 95%CI: ) and feeding habit (OR=5.54, 95%CI: ) of the animals. In conclusion, most of the helminth parasites harboredby the animals have zoonotic importance and thus public health implication. Key words: Public Health Zoonoses Zoos Gastrointestinal Helminths INTRODUCTION These problems may be compounded by poor management in terms of feeding due to the financial In the wild, animals live on wide expanse of land and challenges faced by most zoological gardens in have consequently a low genetic resistance against Nigeria. parasitic infestation because of their low exposure rate [1]. Some authors have worked on helminths in captive When these wild animals are kept under captivity in wildlife in different zoological gardens across the world zoological gardens, the problem of parasitic infestation [3-7]. Some of these works were done within the same can become aggravated and pose a serious threat to study areas as used in this research [4-7] but was done endangered species [1] and humans if zoonotic. Zoonotic either on a particular class of animals or on just one of the parasites pose great public risk that may affect the gardens, none did a comparative analysis of both economic importance of the zoological gardens [2]. zoological gardens used in this research. Corresponding Author: Uwalaka Emmanuel, Department of Veterinary Parasitology and Entomology, Micheal Okpara University of Agriculture, Umudike, Nigeria. Tel:

2 Hence, there is a need to study helminth infestation at two frequently patronized public zoological gardens in south-west Nigeria to identify the various helminth parasites, determine their zoonotic importance and also to estimate the prevalence of gastro-intestinal helminth parasite present at the two zoological gardens. MATERIALS AND METHODS Study Site: The Obafemi Awolowo University (OAU) Zoological Garden located is located in Ile- ife, Osun State. Ile-ife is located on Latitude 7 28' 55" N and Longitude 4 33' 38" E. Federal University of Agriculture Abeokuta (FUNAAB) Zoological Garden is located in Abeokuta, capital city of Ogun State. Abeokuta is located on Latitude: 7 9' 0" North and Longitude: 3 21' 0" East. Approval was obtained from the authorities in charge of the two zoos before sample collection. Collection of faecal samples was between April and May Sample Collection and Examination: Samples were collected from 25 animals at OAU Zoological Garden and from 46 animals at FUNAAB Zoological Garden. Fresh faecal samples (Individual and pooled depending on the housing technique) were collected from each animal at each zoo into labeled sterile sample containers and transported to the Parasitology laboratory in an ice pack container. The samples were analyzed using simple test tube floatation method with saturated solution of sodium chloride as floatation medium as described by Parameshwarappa et al. [8] and sedimentation method. Faeces that were positive for helminth parasites were cultured using harada-mori filter culture as described by Siddiqui and Berk [9]. Identification of ova and larva was done by viewing the microscope at x10 and x40 level of magnification as described by [10]. Statistical Analysis: All data were analysed using Bivariate test and Logistic Regression Model. Statistical significance was set at p<0.05.statistical Package for Social Sciences (SPSS) was the statistical software used. RESULTS At FUNAAB Zoo, 47.83% of the animals screened were positive while 20% of the animals screened at OAU Zoo were positive for helminths. The average percentage positive at the two zoological gardens was 37.50%. Table 1: The prevalence of individual helminth at the two zoological gardens Class of helminth Species N (%) Nematode Capillariaspp 6 (8.7) Trichurisspp 8 (11.6) Strongyloidesspp 10 (14.5) Hook worm 3 (4.3) Trichostrongylusspp 6 (8.7) Oesophagostomumspp 1 (1.5) Syngamusspp 1 (1.5) Pentastomespp, 8 (11.6) Oswaldocruzispp 2 (2.9) Physalopteraspp, 6 (8.7) Strongylurisspp, 6 (8.7) Strongyle 1 (1.5) Un-identified Nematode 4 (5.8) Cestode Fasciolaspp 2 (2.9) Un-identified Trematode 1 (1.5) Trematode Spirometra 4 (5.8) Table 2: Helminth prevalence in the animals as measured by degree of associations between variables and helminth status using bivariate analysis Variables Positive (n)% Negative (n)% 2 x p-value Location O.A.U 5 (18.52) 20 (45.45) F.U.N.A.A.B 22 (81.48) 24 (54.55) Class of Animal Aves 4 (14.81) 22 (50.00) Reptilia 8 (29.63) 12 (27.27) Mammalia 15 (55.56) 10 (22.73) Date of Arrival (7.41) 6 (13.64) (14.81) 12 (27.27) 2011 till date 21 (77.78) 26 (59.09) Source Donated 15 (55.56) 14 (31.82) Purchased 12 (44.44) 30 (68.18) Feeding Habit Herbivore 0 (0.00) 8(18.18) Carnivore 3 (11.11) 12 (27.27) Omnivore 24 (88.89) 24 (54.55) Out of the total population screened at FUNAAB Zoo, 6.52% had single helminth occurrence and 41.30% had multiple helminths occurrence. At OAU Zoo, 12% of the total population screened had single helminth occurrence while 8% had multiple helminths occurrence (Table 1). Comparatively, there was significant correlation between helminth prevalence and location of the zoo (p<0.05), helminth prevalence and class of animal (p<0.05), helminth prevalence to source and feeding habit of the animal (p<0.05). The correlation between helminth prevalence and date of arrival of the animal was insignificant (Table 2). 43

3 Table 3: Particular distribution of helminth identified in animals at OAU Zoo Animal N Helminth identified Guinea fowl 1 Capillariaspp Patas monkey 2 Fasciolaspp Mona monkey 2 Trichurisspp, Capillariaspp, Strongyloidesspp, Trichostrongylusspp, Oesophagostomumspp, Hookworm Table 4: Particular distribution of helminth identified at FUNAAB Zoo Animal N Helminth identified African black eagle 1 Syngamusspp, Strongyloidesspp Robin 2 Trichurisspp Monitor lizard 2 Pentastome, Oswaldocruziaspp, Strongyloidesspp Chameleon 6 Pentastome, Physalopteraspp, Strongylurisspp Patas monkey 6 Strongyloidesspp, Trichostrongylusspp, Hookworm, Spirometraspp, Un-identified larva Mona monkey 3 Strongyloidesspp, Strongylespp, Trichurisspp, Capillariaspp, Hookworm Baboon 3 Trichurisspp, Capillariaspp From the OAU zoo seven different helminth parasites in Africa [17] and infection with were identified from three different species of the captive Strongyloidesfuellebornikellyi occured in the Papua New animals and primates had higher infestations (Table 3). Guinea [18]. It was also reported bymbaya and Udendeye Ten helminth parasites were identified from 7 [15] and Cooper et al. [19] in primates. Trichuristrichuria different species of captive animals at the FUNAAB zoo infects an estimated one billion people worldwide causing (Table 4) % of the parasites detected are capable of morbidity in 220million people and causing an estimated inter-specie transmission. 10,000 deaths per year [19, 20]. Our finding of 11.6 % is similar to that of Mbaya and Udendeye [15], Bezjian et al. DISCUSSION [21] and Dewit et al. [22] in primates. Park and Shin [23] reported Capillariaspp in two Some of the most important and well-known human adult rock patridges in a zoo. Capillaria. philippinensis zoonoses are caused by worm or helminth parasites, is the only species of significance and potentially examples include trichinellosis, cysticercosis, emerging as a zoonotic helminth and is been reported in echinococcosis and schistosomiasis [11]. Others are Indonesia, Japan, Taiwan, India, Iran, Egypt and imported intestinal capillariasis, anisakidosis, eosinophilic cases in Europe [13, 24]. Pentastomida (Tongue worm) enteritis, oesophagostomiasis and gnathostomiasis [12]. occur largely as zoonoses often infecting snakes, lizards, From the total parasites detected in this study, other reptiles and carnivores depending on the specie 62.50% are capable of inter-specie transmission i.e. of [25]. Ayinmode et al. [26] reported it in royal python at immense zoonotic implication. This may eventually the University of Ibadan zoological garden. Bezjian et al. increase with detailed parasite taxonomy. Our finding is [21], Dewit et al. [22] and Mutani et al. [27] reported very similar to report from a study of 60 workers at an Trichostrongylus spp in primates. It is a common helminth Austrian zoo screened for the prevalence of antibodies parasite of ruminants and wild-trapped primates may have against selected zoonotic agents found markers indicating a higher prevalence of this parasite as observed in this that 97% of individuals had been exposed to at least one study due to the contamination of their environment with zoonotic agent [13]. ruminant waste [28]. Oesophagostomumsppis a common According to C.D.C. [14] an estimated million intestinal nematode of primates [29]. Polderman et al. [30] people in the world are infected with hookworm already reported that the parasite is in humans in Northern (Ancylostoma spp. and Necatorspp.). Hookworm Togo and Ghana and it was estimated that in these areas infection is mainly acquired by walking barefoot on over individuals may be infested [12]. Goldberg contaminated soil and or ingestion of larvae [14]. Mbaya and Bursey [31] recorded Strongylurisspp in three and Udendeye [15] reported hookworm infestation in species of African chameleon. While Physalopteraspp captive and free roaming primates. Strongyloidesspp. was recorded in six species of lizards including monitor infects mammals, birds, reptiles and amphibians [16]. lizard by Rataj et al. [32]. Strongyloidesstercoralis is the principal spp. infecting Oswalodocruzia sppwas reported by Goldberg and humans. Infection with a primate parasite Bursey [31] in three species of African Chameleon. (Strongyloidesfuellebornifuelleborni) has been recorded Human ocular sparganosis a disease caused by 44

4 Spirometraspphas been reported in South America [33], 3. Mir A.Q, Dua K, Singla L.D, Sharma S, Singh M.P Central Europe [34] and Asia [35]. Fascioliasis caused by 2016.Prevalence of parasitic infection in captive wild Fasciola hepatica and Fasciolagiganticalocalize in the animals in Bir Moti Bagh mini zoo (Deer Park), Patiala, biliary ducts of the definitive hosts. Migrating immature Punjab. Veterinary World, 9(6): F. hepatica flukes in humans have been mainly reported 4. Adeniyi, I.C., O.A. Morenikeji and B.O. Emikpe, in blood vessels, lung, subcutaneous tissue and The prevalence of gastro-intestinal parasites of ventricles of the brain, they have also been recovered carnivores in university zoological gardens in South from the anterior chamber of a patient in Iran [36]. West Nigeria. Journal of Veterinary Medicine and Fasciolaspp may also encyst on vegetations and await Animal Health, 7(4): consumption by an unwitting animal [37]. This may be 5. Adetunji, V.E., Prevalence of gastro-intestinal among the many reasons why it was found at the OAU parasites in primates and their keepers from two zoo patas monkeys whose enclosure has trees and other zoological gardens in Ibadan, Nigeria. Sokoto Journal forms of vegetation. of Veterinary Sciences, 12(2): Feeding habits may account for the high infestation 6. Sam-Wobo, S.O., N.P. Innocent, I. Oyatogun, of the animals, allowing for cross specie infestations and O.A. Surakat and H. Mogaji, Status of immense zoonotic implications. The high prevalence of helminths in birds kept in Zoological Park, Abeokuta, nematodes may also be due to the nature of their direct Nigeria. Journal of Entomology and Zoology Studies, life cycle and survival in the environment. These factors 5(6): need to be considered for critical control and prevention 7. Egbetade A., O. Akinkuotu, O. Jayeola, A. Niniola, N. of helminthes in captive wildlife and public health. Emmanuel, E. Olugbogi and S. Onadeko CONCLUSION Gastrointestinal helminths of resident wildlife at the Federal University of Agriculture Zoological Park, Abeokuta. Sokoto Journal of Veterinary Sciences, Conclusively, this research has shown that these 12(3): captive anials in our zoological gardens carry some 8. Parameshwarappa, K.D., C. Chandrakanth and parasites and can also serve as potential zoonotic hazard B. Sunil, The prevalence of intestinal parasitic to occupationally exposed individuals and visitors, infestations and the evaluation of difference therefore, our wildlife species need to be consistently concentrations techniques of the stool examination. monitored and screened for control of helminth parasites J. Clin. Diagn. Res., 4662: and thus averting public health implications. 9. Siddiqui, A.A. and S.L. Berk, Diagnosis of Strongyloides Stercoralis infection. Clin Infect Dis., ACKNOWLEDGEMENT 33: Soulsby, E.J.L., Helminthes, Arthropods and Gratitude to the managements of the two University Protozoa of Domesticated Animals, 6th Edition. ELBS Zoos (OAU and FUNAAB), technical staffs in and Bailliere Tindall & Cassel Ltd, London, pp: theparasitology laboratory of the Department of 11. Robinson, M.W. and J.P. Dalton, Zoonotic Veterinary microbiology and parasitology and Dr. TA helminth infections with particular emphasis on Jarikre for his inputs in the manuscript. fasciolosis and other trematodiases. Phil Trans R Soc. B., 364(1530): REFERENCES 12. Mccarthy, J. and T.A. Moore, Emerging helminth zoonoses. Int J Parasitol, 30(12): Lim, Y.A.L., R. Ngui, J. Shukr, M. Rohela and 13. Juncker-Voss, M., L.H. Pros, H. Lussy, U. Enzenberg, H.R. Matnaim, Intestinal parasites in various H. Auer, H. Lassnig, M. Muller and N. Nowotny, animals at a zoo in Malaysia. Veterinary Parasitology, Screening for antibodies against zoonoses 157: among employees of the Zoological Garden of 2. Anon, Health Topics: Zoonoses. Vienna. Schonbrunn, Austria. Berliner und topics/zoonoses/en/parameshwarappa, MunchenerTierarztlicheWochenschrift, 117: K.D., C. Chandrakanth, B. Sunil, The prevalence 14. Center For Disease Control and Prevention (C.D.C., of intestinal parasitic infections and the evaluation of 2013). Global Health -Division of Parasitic Diseases different concentration techniques of the stool and Malaria. Available from: examination. J. ClinDiagn Res., 6(7):

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