Gastrointestinal parasites in captive wild animals from two Brazilian Zoological Gardens
DOI:
https://doi.org/10.33448/rsd-v11i4.26637Keywords:
Diagnosis; Endoparasites; Mini-FLOTAC; Zoological gardens.Abstract
Keeping animals in zoos is important for the preservation of endangered species. However, captive animals can also be affected by different species of parasites. Herein, we aimed to evaluate the occurrence of gastrointestinal parasites in wild and exotic animals from two zoos in the state of Sergipe, Northeastern Brazil. Fecal samples were obtained by spontaneous defecation of 287 specimens, grouped into mammals (n = 101), birds (n = 99), and reptiles (n = 87). The samples were assessed using two techniques, Mini-FLOTAC and Ziehl-Neelsen, to identify helminths and protozoa, respectively. In total, 60.2% (173/287) of the animals evaluated were positive for some type of gastrointestinal parasite. Among the classes evaluated, mammals (81.1%; 82/101; p-value <0.0001) were mostly affected, followed by birds (56.6%; 56/99) and reptiles (40.2%; 35/87). Furthermore, our findings showed that the parasites Ancylostomatidae and coccidian oocysts were the most abundant among the species. It is important to highlight the first record of some parasites in species in the South America, such as: Ancylostomatidae in Asian Elephant (Elephas maximus) and Brown Bear (Ursus arctos); Toxascaris leonina in Leo (Panthera leo); and Trichostrongyloidea and Ascarididae in Equus quagga burchellii and Lama glama. Taken together, our data showed a high occurrence of gastrointestinal parasites in captive animals, including zoonotic species, which may pose a risk to animal and human public health.
References
Abdisa, T., Hasen, R., Tagesu, T., Regae, G., & Tadese, G (2019).. Poultry Coccidiosis and its Prevention, Control. Schólarena. 2, 1, 1-6.
Abhijith, T. V., Ashokkumar, M., Dencin, R.T ., & George, C. (2018).. Gastrointestinal parasites of Asian elephants (Elephas maximus L. 1789) in south Wayanad forest division, Kerala, India. J Parasit Dis. 42, 3, 382-390. https://doi.org/10.1007/s12639-018-1012-0
Andersen, U. V., Howe, D. K., Olsen, S. N., & Nielsen, M. K. (2013). Recent advances in diagnosing pathogenic equine gastrointestinal helminths: the challenge of prepatent detection. Vet Parasitol. 192, 1-3, 1-9. https://doi.org/10.1016/j.vetpar.2012.11.003
Barbón, A. R., López, J., Jameiska, J., Price, E., Thomasson, A., Whiehead, H., Braun, J., & Stidworthy, M. (2019). Clinical and Pathological Aspect of Systemic Isospora Infection in Blue-crowned Laughing Thrushes (Garrulax courtoisis) at Jersey Zoo. J. Avian Med Surg. 9, 33, 265-277. https://doi.org/10.1647/2018-377
Barbosa, A. S., Pinheiro, J. L., Santos, C. R., Lima, C.S.C.C., Dib, L.V., Echarte, G. V., Augusto, A. M., Bastos, A. C. M. P., Uchôa, C.M.A., Bastos, O.M.P., Santos, F. N., Fonseca, A.B.M., & Amendoeira, M.R.R. (2019). Gastrointestinal Parasites in Captive Animals at the Rio de Janeiro Zoo. Acta Parasitologica, 65, 237-249. https://doi.org/10.2478/s11686-019-00145-6
Barros, L.A ., Sant’Anna, L .X., & Magalhães, B. S. N. (2017). Prevalence of gastrointestinal parasites in wild mammals from Zoological Garden of Rio de Janeiro. R. Bras. Ci. Vet. 24, 4, 179-183. http://dx.doi.org/10.4322/rbcv.2017.034
Betson, M., Alonte, A. J .I., Ancog, R. C., Aquino, A .M .O., Belizario Jr, V .Y., Bordado, A. M. D., Clark, J., Corales, M. C. G., Dacuma, M.G., Divina, B.P., Dixon, M. A., Gourley, S. A., Jimenez, J. R .D., Jones, B .P., Manalo, S. M. P., Prada, J. M., Vliet, A. H. M. V., Whatley, K.C.L., & Paller, V.G.V. (2020). Zoonotic transmission of intestinal helminths in southeast Asia: Implication for controls and elimination. Adv Parasitol. 108, 47-131. https://doi.org/10.1016/bs.apar.2020.01.036
Bowman, D. D., Lynn, R. C., Eberhard, M. L., & Alcaraz, A. (2010). Parastologia Veterinária de Georgis. Tradução de 9ª edição (2008). Elsevier.
Brasil, (1996. Infecções oportunistas por parasitas em AIDS: técnicas de diagnóstico, 1th ed. Ministério da Saúde, Brasília 17pp.
Capasso, M., Maurelli, M. P., Ianniello, D., Alves, L. C., Amadesi, A., Laricchiuta, P., Silvestre, P., Campolo, M., Cringoli, G., & Rinaldi, L. (2019). Use of Mini-FLOTAC and Fill-FLOTAC for rapidly diagnosing parasitic infections in zoo mammals. Rev Bras Parasitol Vet. 28, 1, 168-171. https://doi.org/10.1590/s1984-296120180087
Carrera-Játiva, P. D., Morgan, E. R., Barrows, M., & Wronski, T., (2018). Gastrointestinal Parasites in Captive and Free-Ranging Bird and Potential Cross-Transmision in a Zoo Environment. J. of Zoo and Wildlife Medicine. 49, 1, 116-128. https://doi.org/10.1638/2016-0279r1.1
Conde, D. A. (2013).. The Role of Zoos. Zoo conservation biology. 2, 207-215. https://www.researchgate.net/publication/259863205
Cordón, G. P., Prados, A. H., Moreno, M. S., Pontes, A., Osuna, A., & Rosales, M.J. (2009). Intestinal and heamatic parasitesm in the birds of the Almuñecar (Granada, Spain) ornithological garden. Vet Parasitol. 165, 3-4, 361-366. https://doi.org/10.1016/j.vetpar.2009.07.027
Cringoli, G., Maurelli, M. P., Levecke, B., Bosco, A., Vercruysse, J., Utzinger, J., & Rinaldi, L., (2017). The Mini-FLOTAC technique for the diagnosis of helminth and protozoan infections in humans and animals. Nature Protocols. 12, 1723-1732. http://dx.doi.org/10.1038/nprot.2017.067
Cringoli, G., Rinaldi, L., Maurelli, M. P., & Utzinger, J., (2010). FLOTAC: new multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nature Protocols. 5, 3, 503-515. doi: https://doi.org/10.1038/nprot.2009.235
Foil, L. D., & Gorham, J. R. (2000). Mechanical Transmission of Disease Agents by Arthropods. Medical Entomology. 461-514. http://dx.doi.org/10.1007/978-94-011-6472-6_12
Frezza, T .F., Sani, A. A., Souza, G. T .R., & Santos, L. C. (2021).. Helmintos parasitos de répteis e anfíbios no estado de São Paulo, Brasil. Interfaces Científicas – Saúde e Ambiente. 8, 3, 32-59. https://doi.org/10.17564/2316-3798.2021v8n3p32-59
Gomes, M. P. I., Osorio, M. R., & Maza, F. A. (1993). Parasitation of falconiform, stingiform and passeriform (corvidae) by helminths in Spain. Research and Review in Parasitology. 53, (3-4), 129-135.
Henriksen, S. A., & Pohlenz, J. F .L., (1981).. Satining of Cryptosporidium by a modified Ziehl- Neelsen technique. Acta Vet. Scan. 22, 594–596.
Holsback, L., Cardoso, M. J. L., Fagnani, R., & Patelli, T. H. C. (2013). Natural infection by endoparasites among free-living wild animals. Rev. Bras. Parasitol. Vet., 22, 2, 302-306. https://doi.org/10.1590/s1984-29612013005000018
Ilic, T., Becskei, Z., Gajic, B., Ozvegy, J., Stepanovic, P., Nenadovic, K., & Dimitrijeviic, S. (2018). Prevalence of endoparasitic infections of birds in zoo gardens in Serbia. Acta Parasitol. 63, 1, 134-146. https://doi.org/10.1515/ap-2018-0015
Instituto Brasileiro de Geografia e Estatística, (2021). Cidades e Estados – Sergipe. https://www.ibge.gov.br/cidades-e-estados/se/aracaju.html [Accessed 21 November 2021).
Knight, A., Ewen, J. G., Brekke, P., & Santure, A. W., (2018). Chapter Two – The Evolutionary Biology, Ecology and Epidemiology of Coccidia of Passerine Brids. Advances in Parasitology. 99, 35-60. https://doi.org/10.1016/bs.apar.2018.01.001
Kvapil, P., Kastelic, M., Dovc, E., Cizek, P., Lima, N., & Strus, S. (2017). An eight-year survey of the intestinal parasites of carnivores, hoofed mammals, primates, ratites and reptiles in the Ljubljana zoo in Sovenia. Folia Parasitol (Praha). 21, 64, 1-6. https://doi.org/10.14411/fp.2017.013
Li, J., Wang, Z., Karim, M. R, & Zhang, L. (2020). Detection of human intestinal protozoan parasites in vegetables and fruits: a review. Parasit vectors. 13, 1, 1-19 https://doi.org/10.1186/s13071-020-04255-3
Lim, Y., Ngui, R., Shukri, J., Rohela, M., & Naim, H. R. M. (2008). Intestinal parasites in various animals at a zoo in Malaysia. Vet Parasitol. 157.1-2, 154-159. https://doi.org/10.1016/j.vetpar.2008.07.015
Lozano, J., Almeida, C., Victório, A. C., Melo, P., Rodrigues, J. P., Rinaldi, L., Cringoli, G., Gomes, L., Oliveira, M., Paz-Silva, A., & Carvalho, L.M., (2021). Implementation of Mini-FLOTAC in Routine Diagnosis of Coccidia and Helminth Infections in Domestic and Exotic Birds. Veterinary Sciences. 8, 8, 1-12. https://doi.org/10.3390/vetsci8080160
Melo, Y. J. O., Ferraz, H.T., Oliveira, R.A., & Aguiar, P.T.B. (2019). Ovos de helmintos encontrados em fezes de aves silvestres. Centro Científico Conhecer, 16, 29, 1129-1148. DOI: 10.18677/EnciBio_2019A94
Melo, Y. J. O., Ferraz, H. T., Saturino, K. C., Silva, T. D. P., Braga, I .A., Meirelles-Bartoli, R. B., & Ramos, D. G. S. (2021). Gastrointestinal parasites in captive and free-living wild birds in Goiania Zoo. Brazilian Journal of Biology. 82, 1-8. https://doi.org/10.1590/1519-6984.240386
Mewius, A., Lusa, E. R., Pertille, J. G., Dos Reis, T. D., Pletsch, J. A., & França, R. T. (2021). Endoparasites in group of wild animals raised in captivity. Pesq. Vet. Bras. 41, 1-7. https://doi.org/10.1590/1678-5150-PVB-6758
Morezzi, B. B., ALVES, I. S.; Kawanichi, L.A., Bergamo, M. C. S., Pirasol, M. G.; Santos, M. I., Vieira, F.P . R., & Camargo, H.B., (2021). Enriquecimento ambiental em zoológicos. PubVet, 15, 5, 1-9. https://doi.org/10.31533/pubvet.v15n05a813.1-9
Nath, T. C., Eom, K. S., Choe, S., Hm, S., Islam, S., Ndosi, B.A., Kang, Y., Bia, M. M., Kim, S., Eamudomkarn, C., Jeon, H.K., Park, H., & Lee, D. (2021). Insight into One Health Approach: Endoparasite Infections in Captive Wildlife in Bangladesh. Pathogens, 10, 2, 1-14. https://doi.org/10.3390/pathogens10020250
Oliveira, I .M. S., Carmo, I. B., Cruz, J. H. S., Santos, M. J., & Farias, L. A. (2017). A importância dos endoparasiticidas e ectoparasiticidas em animais domésticos – Revisão. Pub Vet, 11, 03, 281-284. http://dx.doi.org/10.22256/PUBVET.V11N3.281-284
Otegbade, A. C., & Morenikeji, O. A., (2014). Gastrointestinal parasites of birds in zoological gardens in south-west Nigeria. Trop. Biomed. 31, 1, 54-62. https://pubmed.ncbi.nlm.nih.gov/24862045/
Papini, R., Girivetto, M., Marangi, M., Mancianti, F., & Giangaspero, (2012). A. Endoparasite infections in pet and zoo birds in Italy. Scientific World Journal. 2012, 1-9. https://doi.org/10.1100/2012/253127
Papini, R., Manetti, C., & Mancianti, F. (2011). Coprological survey in pet reptiles in Italy. Vet Rec. 169, 8, 1-4. https://doi.org/10.1136/vr.d4398
Patra, G., Efimova, M. A., Sahara, A., Al-Abodi, H., Borthakur, S., & Ghosh, S. (2019). Prevalence of endoparasitic fauna of various species of birds in North-Eastern region of India. Biological Rhythm Research. 52, 2021, 882-894. https://doi.org/10.1080/09291016.2019.1608725
Rostami, A., Riahi, S. M., Omrani, V. F., Wang, T., Hofmman, A., Mirzapour, A., Foroutan, M., Fakhri, Y., Macpherson, C.N.L., & Gasser, R.B. (2020). Global Prevalence Estimative of Toxascaris leonine Infection in Dogs and Cats. Pathogens. 9, 6, 1-14. https://doi.org/10.3390/pathogens9060503
Ryan, U., & Zahedi, A. (2019). Molecular epidemiology of giardiasis from a veterinary perspective. Adv Parasitol. 106, 209-254. https://doi.org/10.1016/bs.apar.2019.07.002
Ryan, U., Zahedi, A., & Paparini. A. (2016). Cryptosporidium in humans and animals-a one health approach to prophylaxis. Parasites Immunol. 38, 9, 535-547. https://doi.org/10.1111/pim.12350
Santos, P. M. S., Silva, S. G. N., Fonseca, C. F., & Oliveira, J .B. (2015). Parasites of birds and mammals in captivity in Pernambuco state, Brazil. Pesq. Vet. Bras. 35, 9, 788-794. https://doi.org/10.1590/S0100-736X2015000900004
Schaper, L., Hutton, P., & McGraw, K .J. (2021). Bird-freeder cleaning lowers disease severity in rural but not urban bird. Scientific Reports, 11, 12835, 1-8. https://doi.org/10.1038/s41598-021-92117-y
Seguel, M., & Gottdenker., (2017). The diversity and impact of hookworm infections in Wildlife. International Journal for Parasitology: Parasites and Wildlife. 6, 3, 177-194. https://dx.doi.org/10.1016%2Fj.ijppaw.2017.03.007
Smith, H. V., Robertson, L. J., & Ongerth, J. E., (1995). Cryptosporidiosis and giardiasis: the impact of waterborne transmission. J. Water. SRT - AQUA 44, 258–274.
Spratt, D. M. (2015). Species of Angiostrongylus (Nematoda: Metastrongyloidea) in wildlife: A review. Int J Parasitol Parastes Wildl. 9, 4, 178-189. https://doi.org/10.1016/j.ijppaw.2015.02.006
Taylor, M. A., Coop, R .L., & Wall, R. L. (2017). Parasitologia Veterinária. Tradução da 4ª edição. Editora Guanabara Koogan.
Thompson, R. C. A., Kutz, S., & Smith, A. (2009). Parasites zoonoses and wildlife: emerging issues. Int Environ Res Public Health. 6, 2, 678-693. https://doi.org/10.3390/ijerph6020678
Tiddi, B., Pfoh, R., & Agostini, I. (2019). The impacto f food provisioning on parasite infection in wild black capuchin monkeys: a network approach. Primates. 60, 3, 297-306. https://doi.org/10.1007/s10329-018-00711-y
Vizcaychipi, K. A., Rinas, M., Irazu, L., Miyagi, A., Arguelles, C. F., & DeMatteo, K. E. (2016). Neotropical Zoonotic Parasites in Bush Dogs (Sopeothos venaticus) from Upper Paraná Atlantic Forests in Misiones, Argentina. Vector Borne Zoonotic Dis. 16, 10, 664-672. https://doi.org/10.1089/vbz.2015.1929
Wyrobisz, A., Kowai, J., & Nosal, P. (2016). Insight into species diversity of the Trichostrongylidae Leiper, 1912 (Nematoda: Stongylida) in ruminants. J Helminthol. 90, 6, 639-646. https://doi.org/10.1017/s0022149x15001017
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Copyright (c) 2022 Igo Gonçalves dos Santos; Aksa Ingrid Vieira Batista; Weslania Souza Inacio da Silva; Manuel Benicio Oliveira Neto; Sofia Cerqueira Schettino; Matheus Resende Oliveira; Rafael Antonio Nascimento Ramos; Leucio Câmara Alves; Márcio Bezerra-Santos; Victor Fernando Santana Lima
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