Prevalence of enteroparasites in primates kept at the Brasília Zoo, Brazil
DOI:
https://doi.org/10.33448/rsd-v12i5.41739Keywords:
Microbiology; Enteroparasites; Primates; Parasitology; Intestinal parasites.Abstract
Parasitic infections are a primary disease affecting wild animals in captivity, which can cause morbidity and even mortality. The study aimed to identify the prevalence of enteroparasites at the Brasília Zoo, Brazil, and their possible risk factors. The research was conducted in 2019, and 37 primates from 19 species participated. Three stool samples were collected from the enclosures and were processed using three parasitological methods: (i) Spontaneous sedimentation, (ii) Rugai, and (iii) Kato-Katz method. Soil samples were collected from five points in each enclosure and processed using the Spontaneous sedimentation method. Water samples were collected from drinking fountains and analyzed for the presence of enteroparasites, using the Spontaneous sedimentation method, and for thermotolerant coliforms and Escherichia coli using the COLILERT microbiological method. The results showed that 54% of the stool samples were positive, mostly for the commensal parasite Entamoeba coli. All soil samples were contaminated, mainly by the pathogenic protozoan Giardia sp. The presence of thermotolerant coliforms was detected in all water samples. This was the first study carried out on the prevalence of intestinal parasites in primates kept at the Brasília Zoo. It is essential for the health and well-being of animals kept in captivity, parasitological monitoring, as the identification of these parasites helps in the treatment and monitoring of infections, in addition to avoiding infections of people who work directly with them.
References
Adrus, M., Zainudin, R., Ahamad, M., Jayasilan, M. A. & Abdullah, M. T. (2019). Gastrointestinal parasites of zoonotic importance observed in the wild, urban, and captive populations of non-human primates in Malaysia. Journal of Medical Primatology, 48: 22– 31. https://doi.org/10.1111/jmp.12389.
Agostini, I., Vanderhoeven, E., Di Bitetti, M.S. & Beldomenico, P.M. (2017). Experimental testing of reciprocal effects of nutrition and parasitism in wild black capuchin monkeys. Scientific Reports, 7, 12778. https://doi.org/10.1038/s41598-017-12803-8.
Alcântara, D. S., Mendonça, I. L., Fernandes Neto, V. P., Carniel, P. G. & Pessoa, F.B. (2016). Estudo coproparasitológico da espécie Cebus libidinosus (macaco-prego). Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 68(6), 1609-1612. https://doi.org/10.1590/1678-4162-9102.
Andrade, M. C. R. (2002). Principais doenças de primatas não-humanos. In: Andrade, A., Pinto, S. C., Oliveira, R.S. Animais de Laboratório: criação e experimentação. Rio de Janeiro: Editora FIOCRUZ.
APHA, (2017). Standard Methods for the examination of water and Wastewater (23rd ed.). Washington DC: American Public Health Association.
Barbosa, A., Pinheiro, J. L., Dos Santos, C. R., De Lima, C., Dib, L. V., Echarte, G. V., Augusto, A. M., Bastos, A., Antunes Uchôa, C. M., Bastos, O., Santos, F. N., Fonseca, A. & Amendoeira, M. (2020). Gastrointestinal Parasites in Captive Animals at the Rio de Janeiro Zoo. Acta parasitologica, 65(1), 237–249. https://doi: 10.2478/s11686-019-00145-6.
Becker, D. J., Streicker, D. G. & Altizer, A. (2018). Using host species traits to understand the consequences of resource provisioning for host–parasite interactions. Journal of Animal Ecolpgy, 87(2), 511–525. https://doi.org/10.1111/1365-2656.12765.
Belova, L. M. & Krylov, M. V. (1998). The distribution of Blastocystis according to different systematic groups of hosts. Parazitologiia, 32(3):268-76.
Bichi, H. M., Suleiman, I. D. & Jayeola, O. A. (2016). Incidence of parasitic infections of nonhuman primates in Kano State Zoological Garden, Nigeria. IOSR Journal of Agriculture and Veterinary Science, 9(4): 39-43. https://doi.org/10.9790/2380-0904023943.
Carmo, A. M. & Salgado, C. A. (2003). Ocorrência de parasitos intestinais em Callithrix sp. (Mammalia, Primates, Callithrichidae). Revista Brasileira de Zoociência, 5, 267-262.
Cavallero, S., El Sherif, R. A., Pizzarelli, A., El Fituri, A. A., El Showhdi, M., Benmosa, F., & D'Amelio, S. (2019). Occurrence of Anisakis and Hysterothylacium Nematodes in Atlantic Chub Mackerels from Libyan Coasts. Helminthologia, 56(4), 347–352. https://doi.org/10.2478/helm-2019-0034.
Daszak, P., Cunningham, A. A. & Hyatt, A. D. (2000). Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science, 287(5452), 443-9. https://doi.org/10.1126/science.287.5452.443.
Diniz, L. S. M. (1997). Primatas em Cativeiro – Manejo e Problemas Veterinários. Editora Ícone, São Paulo.
Fagiolini, M., Lia, R. P., Laricchiuta, P., Cavicchio, P., Mannella, R., Cafarchia, C., Otranto, D., Finotello, R., & Perrucci, S. (2010). Gastrointestinal parasites in mammals of two Italian Zoological gardens. Journal of Zoo and Wildlife Medicine, 41(4), 662–670. http://www.jstor.org/stable/40962311.
Fernandes, M. L. B., Gouveia, R. L., Lucena, L. F., Rodrigues, M. da S., Silva, A. K. P. & Silva, N. M. P. da R. (2021). Estudo de balneabilidade em quatro praias do arquipélago de Fernando de Noronha baseado em análise de coliformes totais. Research, Society and Development, 10(11), e302101119784. https://doi.org/10.33448/rsd-v10i11.19784.
Ferreira da Silva, M. T., Aquim, E. C., de Sousa, T. P. R., Gomes, N. R. de S., de Vasconcelos, A. R. O., Andrade Silveira, C. C. de O., Junior Costa, F. M., & Evangelista, L. S. de M. (2018). Occurrence of Intestinal Parasites in Alouatta caraya of the Zoobotanical Park of Teresina, Piauí, Brazil. Acta Scientiae Veterinariae, 46, 5. https://doi.org/10.22456/1679-9216.87478.
Fia, R., Tadeu, H. C., Menezes, J. P. C., Fia, F. R. L. & Oliveira, L. F. C. (2015). Qualidade da água de um ecossistema lótico urbano. Revista Brasileira de Recursos Hídricos, 20(1): 267-275. https://doi.org/10.21168/rbrh.v20n1.p267-275.
FJZB. Fundação Jardim Zoológico de Brasília. http://www.zoo.df.gov.br/index.php/2015-04-30-13-43-03/nossahistori.
Gillespie, T. R., Lonsdorf, E. V., Canfield, E. P., Meyer, D. J., Nadler, Y., Raphael, J., Pusey, A. E., Pond, J., Pauley, J., Milengeya, T., Travis, D. A. (2010). Demographic and ecological effects on patterns of parasitism in eastern chimpanzees (Pantroglodytes schweinfurthii) in Gombe National Park, Tanzania. American journal of physical anthropology, 143(4), 534–544. https://doi.org/10.1002/ajpa.21348.
Goossensa, E., Dornya, P., Boomkerd, J., & Vercammen, F. (2005). A 12-month survey of the gastro-intestinal helminths of antílopes, gazelles and giraffes kept at two zoos in Belgum. Veterinary Parasitology, 127(3-4), 303–312. https://doi.org/10.1016/j.vetpar.2004.10.013.
Hunter, P. R., & Thompson, R. C. (2005). The zoonotic transmission of Giardia and Cryptosporidium. International journal for parasitology, 35(11-12), 1181–1190. https://doi.org/10.1016/j.ijpara.2005.07.009.
Johnston, K. L., Wu, B., Guimarães, A., Ford, L., Slatko, B. E. & Taylor, M. J. (2010). Lipoprotein biosynthesis as a target for anti-Wolbachia treatment of filarial nematodes. Parasites & vectors, 3, 99. https://doi.org/10.1186/1756-3305-3-99.
Kashid, K. P., Shrikhande, G. B., & Bhojne, G. R. (2002). Incidence of gastrointestinal helminths in captive wild animal sat diferente localions. Zoos’ Print Journal, 18(3), 1053-1054.
Lasprilla, M., Ocampo, M., & López, G. (2009). Identificación de huevos de nematodos en carnívoros y primates ubicados en el Zoológico Santa Fe de Medellín, mediante método coprológico directo y de flotación. Revista Spei Domus, 5, 30-36.
Milozzi, C. B., Gabriela, C. E., Mudry, M. D., Navone, G. T. (2012). Intestinal parasites of Alouatta caraya (Primates, Ceboidea): preliminary study in semi-captivity and in the wild in Argentina. Mastozoología neotropical, 19(2), 163-178. http://www.scielo.org.ar/scielo.php?script=sci_arttext&pid=S0327-93832012000200006&lng=es&tlng=en.
Muller, G. C. K., Krambeck, A., Hirano, Z. M. B. & Silva-Filho, H. H. (2000). Levantamento preliminar de endoparasitas do tubo digestivo de bugios Alouatta guariba clamitans. Neotropical Primates, 8(3), 107-108.
Nath, B. G., Isalm, I. & Chakraborty, A. (2012) Prevalence of parasitic infection in captive non-human primates of Assam State Zoo, India. Veterinary World, 5(10), 614-616, https://doi.org/10.5455/vetworld.2012.614-616.
Neves, D. P. (2016). Parasitologia humana. (13a ed.). Atheneu.
Nunn, C. L. & Altizer, S. M. (2005). The global mammal parasite database: An online resource for infectious disease records in wild primates. Evolutionary Anthropology, 14: 1-2. https://doi.org/10.1002/evan.20041.
OMS. (2008) Organização Mundial de Saúde Animal. Código Sanitário de Animais Terrestres. Zoonoses transmissíveis por primatas não humanos. São Paulo: OIE.
Parkar, U., Traub, R. J., Vitali, S., Elliot, A., Levecke, B., Robertson, I., Geurden, T., Steele, J., Drake, B., & Thompson, R. C. (2010). Molecular characterization of Blastocystis isolates from zoo animals and their animal-keepers. Veterinary parasitology, 169(1-2), 8–17. https://doi.org/10.1016/j.vetpar.2009.12.03.
Parr, N. A., Fedigan, L. M., & Kutz, S. J. (2013). A coprological survey of parasites in white-faced capuchins (Cebus capucinus) from Sector Santa Rosa, ACG, Costa Rica. Folia primatologica; international journal of primatology, 84(2), 102–114. https://doi.org/10.1159/000348287.
Rey, L. (2008). Parasitologia: parasitos e doenças parasitárias do homem nas Américas e na África, (3a ed.), Guanabara-Koogan.
Rodrigues, T. C., Santana, I. S. F., Lemos, L. Q., Silva, M. S., Prado, I. S., Rêgo, C. O., Soares, M. S., Queiroz, T. S., Tomazi, L., Nishiyama, P. B., Silva, M. B.., & Fraga, R. E. (2021). Adaptação das técnicas parasitológicas de identificação para quantificação de parasitos gastrintestinais em primatas. Research, Society and Development, 10(12), e462101220706. https://doi.org/10.33448/rsd-v10i12.20706.
Santa Cruz, A. C. M., Borda, J. T., Patiño, E. M., Gómez, L. & Zunino, G. E. (2000). Habitat fragmentationnand parasitism in howler monkeys (Alouatta caraya). Neotropical primates, 8, 146-148.
Schurer, J. M., Ramirez, V., Kyes, P., Tanee, T., Patarapadungkit, N., Thamsenanupap, P., Trufan, S., Grant, E. T., Garland-Lewis, G., Kelley, S., Nueaitong, H., Kyes, R. C., & Rabinowitz, P. (2019). Long-Tailed Macaques (Macaca fascicularis) in Urban Landscapes: Gastrointestinal Parasitism and Barriers for Healthy Coexistence in Northeast Thailand. The American journal of tropical medicine and hygiene, 100(2), 357–364. https://doi.org/10.4269/ajtmh.18-0241.
Shehani U. F., Preethi V. U. & Saminda P. F. (2022). Effect of urbanization on zoonotic gastrointestinal parasite prevalence in endemic toque macaque (Macaca sinica) from different climatic zones in Sri Lanka, International Journal for Parasitology: Parasites and Wildlife, 17, 100-109. https://doi.org/10.1016/j.ijppaw.2021.12.007.
Shen, S. S., Qu, X. Y., Zhang, W. Z., Li, J., & Lv, Z. Y. (2019). Infection against infection: parasite antagonism against parasites, viruses and bacteria. Infectious Diseases of Poverty, 8, 49. https://doi.org/10.1186/s40249-019-0560-6.
Silva, A. S., Gressler, L. T., Lara, V. M., Monteiro, S. G. & Carregaro, A. B. (2009). Protozoários gastrintestinais em bugios (Alouatta sp.) mantidos em cativeiro. Ciência Animal Brasileira / Brazilian Animal Science, 10(2), 669–672. https://revistas.ufg.br/vet/article/view/1382.
Snak, A., Agostini, K. M., Lenzi, P. F., Montanucci, C. R., Delgado, L. E. & Zabott, M. V. (2022). Perfil parasitológico de mamíferos silvestres cativos. Veterinária E Zootecnia, 24(1), 193–200. https://rvz.emnuvens.com.br/rvz/article/view/719.
Snak, A., Lenzi, P. F., Agostini, K. M., Delgado, L. E., Montanucci, C. R., & Zabott, M. V. (2014). Análises coproparasitológicas de aves silvestres cativas. Ciência Animal Brasileira, 15(4), 502–507. https://doi.org/10.1590/1089-6891v15i425797.
Souza, J. R, J. C., Greinert, J. A., Baad, R., Rode, G., Heinig, J. R, A. & Hirano, Z. M. B. (2005). Levantamento de parasitas intestinais de bugios-ruivos (Alouatta guariba clamitans) mantidos em cativeiro no Centro de Pesquisa Biológicas de Indaial, Projeto Bugio, SC. In: XI Congresso Brasileiro de Primatologia, PUC-RS, Porto Alegre.
Souza, L. H. N., Arruda, R. O. M., Rosini, E. F. & Pontes, D. D. (2019). Diagnóstico da qualidade ambiental dos lagos e nascentes do zoológico de Guarulhos, município de Guarulhos–SP. Revista Geociências-UNG-Ser, 18(1): 12-18. http://dx.doi.org/10.33947/1981-7428-v18n1-4078.
Stensvold, C. R., Alfellani, M. A., Nørskov-Lauritsen, S., Prip, K., Victory, E. L., Maddox-Hyttel, C., Nielsen, H. V., & Clark, C. G. (2009). Subtype distribution of Blastocystis isolates from synanthropic and zoo animals and identification of a new subtype. International Journal for Parasitology, 39(4), 473-479. https://doi.org/10.1016/j.ijpara.2008.07.006.
Stoner, K.E. & González Di Pierro, A.M. (2006). Intestinal Parasitic Infections in Alouatta Pigra in Tropical Rainforest in Lacandona, Chiapas, Mexico: Implications for Behavioral Ecology and Conservation. In: Estrada, A., Garber, P.A., Pavelka, M.S.M., Luecke, L. (eds) New Perspectives in the Study of Mesoamerican Primates. Developments in Primatology: Progress and Prospects. Springer, Boston, MA. https://doi.org/10.1007/0-387-25872-8_10.
Stuart, M. D., Strier, K. B. & Pierberg, S. M. A. (1993). Coprological survey of parasites of wild muriquis, Brachyteles arachnoids, and brown Howling monkeys, Alouatta fusca. Helminthological Society of Washington, 60, 111-115.
Stuart, M., Pendergast, V., Rumfelt, S., Pierberg, S., Greenspan, L., Glander, K. & Clarke, M. (1998). Parasites of Wild Howlers (Alouatta spp.). International Journal of Primatology, 19, 493–512. https://doi.org/10.1023/A:1020312506375.
Viney, M. E., & Lok, J. B. (2007). Strongyloides spp. WormBook:the online review of C. elegans biology. 1–15. https://doi.org/10.1895/wormbook.1.141.1
Whitney, R. A. (1974). Metazoan Parasites of Nonhuman Primates. The Bulletin of the Society of Pharmacological and Environmental Pathologists, 2(1), 15-19. doi:10.1177/019262337400200106.
Zhou, S., Harbecke, D. & Streit, A. (2019). From the feces to the genome: a guideline for the isolation and preservation of Strongyloides stercoralis in the field for genetic and genomic analysis of individual worms. Parasites Vectors, 12, 496. https://doi.org/10.1186/s13071-019-3748-5.
Zimmer, K., Dräger, K. G., Klawonn, W., & Hess, R. G. (1999). Contribution to the diagnosis of Johne's disease in cattle. Comparative studies on the validity of Ziehl-Neelsen staining, faecal culture and a commercially available DNA-Probe test in detecting Mycobacterium paratuberculosis in faeces from cattle. Zentralblatt fur Veterinarmedizin. Reihe B. Journal of veterinary medicine. Series, 46(2), 137–140. https://doi.org/10.1111/j.0931-1793.1999.00214.x.
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