Abstract
Giardiasis is an infection of the small intestine by protozoa of the genus Giardia, which has a wide range of susceptible hosts, including domestic and wild animals and humans. Giardia is a zoonotic agent and represents one of the main human parasites, with high prevalence and great importance in public health. This report aims to describe the parasitism of a non-captive Chital deer (Axis axis) by Giardia duodenalis. The animal, after being rescued by soldiers from the 2nd Platoon of the 2nd Company of the 2nd Battalion of the Environmental Military Police of the State of Santa Catarina, was sent to the Wildlife Studies Center (NEVS) of the University of Western Santa Catarina (UNOESC). During clinical care, an exposed fracture in the left pelvic limb and signs of acute respiratory failure were found. Fecal samples were collected for later parasitological diagnosis. Two techniques were applied: centrifugal flotation with zinc sulfate, to diagnose parasites of the gastrointestinal system, and Baermann, to search for parasitism in the respiratory tract. The investigation revealed the presence of Giardia duodenalis. The animal died on the same day of its arrival due to a cardiorespiratory arrest. The presence of this parasite in an invasive exotic deer species highlights its epidemiological importance, as it can act as a source of infection and spread the disease to humans and other animals.
References
Achaval, F., Clara, M., & Olmos, A. (2007). Mamíferos de la República Oriental del Uruguay (2nd ed.). Montevideo: Zonalibro Industria Gráfica.
Adam, R. D. (2021). Giardia duodenalis: Biology and pathogenesis. Clinical Microbiology Reviews, 34(4), e0002419. http://doi.org/10.1128/CMR.00024-19. PMid:34378955.
Adhikari, J. N., Adhikari, R. B., Bhattarai, B. P., Thapa, T. B., & Ghimire, T. R. (2021). A small-scale coprological survey of the endoparasites in the Himalayan goral Naemorhedus goral (Hardwick, 1825) in Nepal. Biodiversitas (Surakarta), 22(3), 1285-1290. http://doi.org/10.13057/biodiv/d220326.
Ali, R. (2004). The effect of introduced herbivores on vegetation in the Andaman Islands. Current Science, 86(81), 1103-1112. https://www.jstor.org/stable/24109319
Baermann, G. (1917). A simple method for the detection of Ankylostomum (nematode) larvae in soil tests (pp. 41-47). Weltevreden: Geneeskundig Laboratorium. https://www.cabidigitallibrary.org/doi/full/10.5555/19182900349
Bartoš, L., Vaňková, D., Šiler, J., & Losos, S. (1996). Fallow deer tactic to compete over food with red deer. Aggressive Behavior, 22(5), 375-385. http://doi.org/10.1002/(SICI)1098-2337(1996)22:5<375:AID-AB6>3.0.CO;2-I.
Belden, R. C. (1994). Review of exotic ungulates: A case study in Florida. In Proceedings of the Annual Conference Southeastern Association of Fish and Wild Agencies, 48, 78-87. https://seafwa.org/sites/default/files/journalarticles/BELDEN-78-87.pdf
Bengis, R. G., Kock, R. A., & Fischer, J. (2002). Infectious animal diseases: The wildlife/livestock interface. Revue Scientifique et Technique, 21(1), 53-65. http://doi.org/10.20506/rst.21.1.1322. PMid:11974630.
Bentley, A., & Downes, M. C. (1968). Deer in new guinea part 1: Notes on the field identification of certain deer species likely to be encountered in Papua and New Guinea. Papua New Guinea Agricultural Journal, 20, 1-14.
Bowman, D. (2010). Parasitologia veterinária de Georgis (9ª ed.). São Paulo: Elsevier Brasil.
Buret, A. G., Cacciò, S. M., Favennec, L., & Svärd, S. (2020). Update on Giardia: Highlights from the seventh International Giardia and Cryptosporidium Conference. Parasite, 27, 49. http://doi.org/10.1051/parasite/2020047. PMid:32788035.
Cacciò, S. M., & Ryan, U. (2008). Molecular epidemiology of giardiasis. Molecular and Biochemical Parasitology, 160(2), 75-80. http://doi.org/10.1016/j.molbiopara.2008.04.006. PMid:18501440.
Cacciò, S. M., Lalle, M., & Svärd, S. G. (2018). Host specificity in the Giardia duodenalis species complex. Infection, Genetics and Evolution, 66, 335-345. http://doi.org/10.1016/j.meegid.2017.12.001. PMid:29225147.
Certad, G., Viscogliosi, E., Chabé, M., & Cacciò, S. M. (2017). Pathogenic mechanisms of Cryptosporidium and Giardia. Trends in Parasitology, 33(7), 561-576. http://doi.org/10.1016/j.pt.2017.02.006. PMid:28336217.
Chalkowski, K., Lepczyk, C. A., & Zohdy, S. (2018). Parasite ecology of invasive species: Conceptual framework and new hypotheses. Trends in Parasitology, 34(8), 655-663. http://doi.org/10.1016/j.pt.2018.05.008. PMid:29935995.
Chang, Y., Li, J., & Zhang, L. (2023). Genetic diversity and molecular diagnosis of Giardia. Infection, Genetics and Evolution, 113, 105482. http://doi.org/10.1016/j.meegid.2023.105482. PMid:37451417.
Clout, M. N., & Russell, J. C. (2008). The invasion ecology of mammals: A global perspective. Wildlife Research, 35(3), 180-184. http://doi.org/10.1071/WR07091.
Coffey, C. M., Collier, S. A., Gleason, M. E., Yoder, J. S., Kirk, M. D., Richardson, A. M., Fullerton, K. E., & Benedict, K. M. (2021). Evolving epidemiology of reported giardiasis cases in the United States, 1995-2016. Clinical Infectious Diseases, 72(5), 764-770. http://doi.org/10.1093/cid/ciaa128. PMid:32047932.
Cripps, J. K., Pacioni, C., Scroggie, M. P., Woolnough, A. P., & Ramsey, D. S. L. (2019). Introduced deer and their potential role in disease transmission to livestock in Australia. Mammal Review, 49(1), 60-77. http://doi.org/10.1111/mam.12142.
Davis, N. E., Bennett, A., Forsyth, D. M., Bowman, D. M., Lefroy, E. C., Wood, S. W., Woolnough, A. P., West, P., Hampton, J. O., & Johnson, C. N. (2016). A systematic review of the impacts and management of introduced deer (family Cervidae) in Australia. Wildlife Research, 43(6), 515-532. http://doi.org/10.1071/WR16148.
De Vos, A., Manville, R. H., & van Gelder, R. G. (1956). Introduced mammals and their influence on native biota (1st ed.). New York: New York Zoology Society. http://doi.org/10.5962/p.203412.
Debárbora, V. N., Nava, S., Cirignoli, S. M., Guglielmone, A. A., & Poi, A. S. G. (2012). Ticks (Acari: Ixodidae) parasitizing endemic and exotic wild mammals in the Esteros del Iberá wetlands, Argentina. Systematic and Applied Acarology, 17(3), 243-250. http://doi.org/10.11158/saa.17.3.3.
Duckworth, J. W., Kumar, N. S., Anwarul Islam, M., Sagar Baral, H., & Timmins, R. (2015). Axis axis. In International Union for Conservation of Nature and Natural Resources (Ed.), IUCN Red List of Threatened Species: e.T41783A22158006. Gland: IUCN.
Einarsson, E., Ma’ayeh, S., & Svärd, S. G. (2016). An up-date on Giardia and giardiasis. Current Opinion in Microbiology, 34, 47-52. http://doi.org/10.1016/j.mib.2016.07.019. PMid:27501461.
Etges, M. F., Martínez-Lanfranco, J. A., & Guadagnin, D. L. (2023). Spread risk assessment of invasive axis deer using bioclimatic niche models. Biological Invasions, 25(2), 485-498. http://doi.org/10.1007/s10530-022-02928-x.
Faas, C. J., & Weckerly, F. W. (2010). Habitat interference by axis deer on white‐tailed deer. The Journal of Wildlife Management, 74(4), 698-706. http://doi.org/10.2193/2009-135.
Fantinatti, M., Bello, A. R., Fernandes, O., & Da-Cruz, A. M. (2016). Identification of Giardia lamblia assemblage E in humans points to a new anthropozoonotic cycle. The Journal of Infectious Diseases, 214(8), 1256-1259. http://doi.org/10.1093/infdis/jiw361. PMid:27511898.
Faust, E. C., D’antonio, J. S., Odom, V., Miller, M. J., Peres, C., Sawitz, W., Thomen, L. F., Toble, J., & Walker, J. H. (1938). A critical study of clinical laboratory technics for the diagnosis of protozoan cysts and helminth eggs in feces. The American Journal of Tropical Medicine and Hygiene, s1-18(2), 169-183. http://doi.org/10.4269/ ajtmh.1938.s1-18.169.
García-Presedo, I., Pedraza-Díaz, S., González-Warleta, M., Mezo, M., Gómez-Bautista, M., Ortega-Mora, L. M., & Castro-Hermida, J. A. (2013). The first report of Cryptosporidium bovis, C. ryanae and Giardia duodenalis sub-assemblage A-II in roe deer (Capreolus capreolus) in Spain. Veterinary Parasitology, 197(3-4), 658-664. http://doi.org/10.1016/j.vetpar.2013.07.002. PMid:23890824.
Garcia-R, J. C., Ogbuigwe, P., Pita, A. B., Velathanthiri, N., Knox, M. A., Biggs, P. J., French, N. P., & Hayman, D. T. (2021). First report of novel assemblages and mixed infections of Giardia duodenalis in human isolates from New Zealand. Acta Tropica, 220, 105969. http://doi.org/10.1016/j.actatropica.2021.105969. PMid:34029530.
Grubb, P. (2005). Order Artiodactyla. In D. E. Wilson & D. M. Reeder (Eds.), Mammal species of the world: A taxonomic and geographic reference (1st ed., pp. 637-722). Baltimore: Johns Hopkins University Press.
Hamnes, I. S., Gjerde, B., Robertson, L., Vikøren, T., & Handeland, K. (2006). Prevalence of Cryptosporidium and Giardia in free-ranging wild cervids in Norway. Veterinary Parasitology, 141(1-2), 30-41. http://doi.org/10.1016/j. vetpar.2006.05.004. PMid:16797126.
Hatcher, M. J., Dick, J. T., & Dunn, A. M. (2012). Disease emergence and invasions. Functional Ecology, 26(6), 1275-1287. http://doi.org/10.1111/j.1365-2435.2012.02031.x. PMid:32313353.
Higuera, A., Muñoz, M., López, M. C., Reyes, P., Urbano, P., Villalobos, O., & Ramírez, J. D. (2020). Development of a multilocus sequence typing scheme for Giardia intestinalis. Genes, 11(7), 764. http://doi.org/10.3390/ genes11070764. PMid:32650382.
Holsback, L., Cardoso, M. J. L., Fagnani, R., & Patelli, T. H. C. (2013). Natural infection by endoparasites among free-living wild animals. Revista Brasileira de Parasitologia Veterinária, 22(2), 302-306. http://doi.org/10.1590/ S1984-29612013005000018. PMid:23778826.
Horlock-Roberts, K., Reaume, C., Dayer, G., Ouellet, C., Cook, N., & Yee, J. (2017). Drug-free approach to study the unusual cell cycle of Giardia intestinalis. MSphere, 2(5), e00384-16. http://doi.org/10.1128/mSphere.00384-16. PMid:28959734.
Huaman, J. L., Pacioni, C., Forsyth, D. M., Pople, A., Hampton, J. O., Helbig, K. J., & Carvalho, T. G. (2021). Evaluation of haemoparasite and Sarcocystis infections in Australian wild deer. International Journal for Parasitology. Parasites and Wildlife, 15, 262-269. http://doi.org/10.1016/j.ijppaw.2021.06.006. PMid:34277336.
Huaman, J. L., Helbig, K. J., Carvalho, T. G., Doyle, M., Hampton, J., Forsyth, D. M., Pople, A. R., & Pacioni, C. (2023). A review of viral and parasitic infections in wild deer in Australia with relevance to livestock and human health. Wildlife Research, 50(9), 593-602. http://doi.org/10.1071/WR22118.
Karim, M. R., Li, J., Rume, F. I., Sumon, S. M. R., Selim, A. S. M., Hoda, N., & Zhang, L. (2021). Occurrence and molecular characterization of Cryptosporidium spp. and Giardia duodenalis among captive mammals in the Bangladesh National Zoo. Parasitology International, 84, 102414. http://doi.org/10.1016/j.parint.2021.102414. PMid:34182122.
Lalle, M., di Regalbono, A. F., Poppi, L., Nobili, G., Tonanzi, D., Pozio, E., & Cacciò, S. M. (2007). A novel Giardia duodenalis assemblage A subtype in fallow deer. The Journal of Parasitology, 93(2), 426-428. http://doi.org/10.1645/GE-983R.1. PMid:17539431.
Lallo, M. A., Pereira, A., Araújo, R., Favorito, S. E., Bertolla, P., & Bondan, E. F. (2009). Ocorrência de Giardia, Cryptosporidium e microsporídios em animais silvestres em área de desmatamento no Estado de São Paulo, Brasil. Ciência Rural, 39(5), 1465-1470. http://doi.org/10.1590/S0103-84782009005000085.
Long, J. L. (2003). Introduced mammals of the world: Their history, distribution and influence. Victoria: CSIRO Publishing. http://doi.org/10.1071/9780643090156.
Mares, M. A., & Ojeda, R. A. (1984). Faunal commercialization and conservation in South America. Bioscience, 34(9), 580-584. http://doi.org/10.2307/1309601.
Mertins, J. W., Mortenson, J. A., Bernatowicz, J. A., & Hall, P. B. (2011). Bovicola tibialis (Phthiraptera: Trichodectidae): Occurrence of an exotic chewing louse on cervids in North America. Journal of Medical Entomology, 48(1), 1-12. http://doi.org/10.1603/ME10057. PMid:21337942.
Mohanty, N. P., Harikrishnan, S., Sivakumar, K., & Vasudevan, K. (2016). Impact of invasive spotted deer (Axis axis) on tropical island lizard communities in the Andaman archipelago. Biological Invasions, 18(1), 9-15. http://doi.org/10.1007/s10530-015-1006-0.
Monteiro, S. G. (2017). Parasitologia na medicina veterinária (2ª ed.). Rio de Janeiro: Roca.
Moriarty, A. J. (2004). Wild deer herds in Australia’s urban fringe: Issues, management and politics. In D. Lunney & S. Burgin (Eds.), Urban wildlife: More than meets the eye (pp. 179-185). Mosman: Royal Zoological Society of New South Wales. http://doi.org/10.7882/FS.2004.095.
Novillo, A., & Ojeda, R. A. (2008). The exotic mammals of Argentina. Biological Invasions, 10(8), 1333-1344. http://doi.org/10.1007/s10530-007-9208-8.
Nowak, R. M. (1999). Walker’s mammals of the world (1st ed.). Baltimore: Johns Hopkins University Press. http://doi.org/10.56021/9780801857898.
Patz, J. A., Graczyk, T. K., Geller, N., & Vittor, A. Y. (2000). Effects of environmental change on emerging parasitic diseases. International Journal for Parasitology, 30(12-13), 1395-1405. http://doi.org/10.1016/S0020- 7519(00)00141-7. PMid:11113264.
Poulin, R. (2017). Invasion ecology meets parasitology: Advances and challenges. International Journal for Parasitology. Parasites and Wildlife, 6(3), 361-363. http://doi.org/10.1016/j.ijppaw.2017.03.006. PMid:30951572.
Preuss, J. F., Posser, E., Albrecht, L. B., Silva, V. P., & Bandiera, F. C. (2020). First record of the exotic species Axis axis (Erxleben, 1777) (Artiodactyla, Cervidae) in the state of Santa Catarina, southern Brazil. Check List, 16(5), 1139-1142. http://doi.org/10.15560/16.5.1139.
Reis, L. L., Lima, D. C. S., Silva, T. R. R., Braga, F. C. O., Nava, A. F. D., & Vicente, A. C. P. (2023). Circulation of Giardia duodenalis in domestic and wild animals from Amazon region: A systematic review. Acta Tropica, 237, 106708. http://doi.org/10.1016/j.actatropica.2022.106708. PMid:36195184.
Richardson, M. L., & Demarais, S. (1992). Parasites and condition of coexisting populations of white-tailed and exotic deer in south-central Texas. Journal of Wildlife Diseases, 28(3), 485-489. http://doi.org/10.7589/0090-3558-28.3.485. PMid:1512889.
Riemann, H., Zaman, M. R., Ruppanner, R., Aalund, O., Jorgensen, J. B., Worsaae, H., & Behymer, D. (1979). Paratuberculosis in cattle and free-living exotic deer. Journal of the American Veterinary Medical Association, 174(8), 841-843. PMid:500426.
Romero, J. A., Medellín, R. A., & de Ita, A. O. (2008). Animales exóticos en México: Una amenaza para la biodiversidad (1st ed.). México: Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, Universidad Nacional Autónoma de México y Secretaría de Medio Ambiente y Recursos Naturales.
Ryan, U., & Cacciò, S. M. (2013). Zoonotic potential of Giardia. International Journal for Parasitology, 43(12-13), 943-956. http://doi.org/10.1016/j.ijpara.2013.06.001. PMid:23856595.
Santin, M. (2020). Cryptosporidium and Giardia in ruminants. The Veterinary Clinics of North America. Food Animal Practice, 36(1), 223-238. http://doi.org/10.1016/j.cvfa.2019.11.005. PMid:32029186.
Santin, M., & Fayer, R. (2015). Enterocytozoon bieneusi, Giardia, and Cryptosporidium infecting white‐tailed deer. The Journal of Eukaryotic Microbiology, 62(1), 34-43. http://doi.org/10.1111/jeu.12155. PMid:25066778.
Schaller, G. B. (1967). The deer and the tiger: A study of wildlife in India (1st ed.). Chicago: University of Chicago Press.
Seabolt, M. H., Roellig, D. M., & Konstantinidis, K. T. (2022). Genomic comparisons confirm Giardia duodenalis sub-assemblage AII as a unique species. Frontiers in Cellular and Infection Microbiology, 12, 1010244. http:// doi.org/10.3389/fcimb.2022.1010244. PMid:36325462.
Smith, K. F., Acevedo‐Whitehouse, K., & Pedersen, A. B. (2009). The role of infectious diseases in biological conservation. Animal Conservation, 12(1), 1-12. http://doi.org/10.1111/j.1469-1795.2008.00228.x.
Song, Y., Li, W., Liu, H., Zhong, Z., Luo, Y., Wei, Y., Fu, W., Ren, Z., Zhou, Z., Deng, L., Cheng, J., & Peng, G. (2018). First report of Giardia duodenalis and Enterocytozoon bieneusi in forest musk deer (Moschus berezovskii) in China. Parasites & Vectors, 11(1), 204. http://doi.org/10.1186/s13071-018-2681-3.
Sponchiado, J., Melo, G. L., & Cáceres, N. C. (2011). First record of the invasive alien species Axis axis (Erxleben, 1777) (Artiodactyla: Cervidae) in Brazil. Biota Neotropica, 11(3), 403-406. http://doi.org/10.1590/S1676-06032011000300032.
Stephens, R. M., Alldredge, A. W., & Phillips, G. E. (2003). Aggressive interactions of Rocky Mountain elk, Cervus elaphus nelsoni, during the calving season toward mule deer, Odocoileus hemionus, in central Colorado. Canadian Field Naturalist, 117(2), 316-317. http://doi.org/10.22621/cfn.v117i2.807.
Sulaiman, I. M., Fayer, R., Lal, A. A., Trout, J. M., Schaefer III, F. W., & Xiao, L. (2003). Molecular characterization of microsporidia indicates that wild mammals harbor host-adapted Enterocytozoon spp. as well as humanpathogenic Enterocytozoon bieneusi. Applied and Environmental Microbiology, 69(8), 4495-4501. http://doi.org/10.1128/AEM.69.8.4495-4501.2003. PMid:12902234.
Taylor, M. A., Coop, R. L., & Wall, R. L. (2017). Parasitologia veterinária. Rio de Janeiro: Guanabara Koogan.
This work is licensed under a Creative Commons Attribution 4.0 International License.
Copyright (c) 2024 Jackson Fábio Preuss, Clóvis Junior Chimin Chafes, Andréia Buzatti