Low occurrence of Cryptosporidium canis in feces of dogs seroreactive for Leishmania spp.
DOI:
https://doi.org/10.5433/1679-0359.2022v43n4p1823Keywords:
Cryptosporidiosis, Epidemiology, Leishmaniasis, One health, Zoonosis.Abstract
In this study, we investigated the occurrence and characterized molecularly Cryptosporidium oocysts in feces of dogs seroreactive for Leishmania spp. We hypothesized that the clinical staging of canine visceral leishmaniasis (CVL) influences the occurrence and intensity of Cryptosporidium spp. oocyst shedding in feces from the canine host due to the immunosuppression induced by Leishmania infantum. Fecal samples from 101 dogs with anti-Leishmania spp. antibodies detected by Dual-Path Platform (DPP®) immunochromatographic test (Biomanguinhos) and/or enzyme-linked immunosorbent assay (Biomanguinhos) were concentrated by the centrifuge-sedimentation method in water-ethyl acetate. The sediments were submitted to the technique of negative staining with malachite green and observed under an optical microscope (400× magnification). The occurrence was 0.99% (95 confidence interval 0.00%-2.93%). A single Cryptosporidium oocyst was found in one of the samples examined by microscopy, and the result was confirmed by nested-PCR. The amplicon sequence showed 100% genetic identity with Cryptosporidium canis. The dog presented the following clinical signs suggestive of CVL: cachexia, generalized alopecia, pale colored gingival mucosa, splenomegaly, and onychogryphosis. We conclude that there is no evidence that the oligosymptomatic and symptomatic clinical staging of dogs seroreactive for Leishmania spp. influenced the occurrence and intensity of C. canis oocyst shedding in the canine host.Downloads
References
Almeida, B. F. M., Narciso, L. G., Bosco, A. M., Pereira, P. P., Braga, E. T., Avanço, S. V., Marcondes, M., & Ciarlini, P. C. (2013). Neutrophil dysfunction varies with the stage of canine visceral leishmaniosis. Veterinary Parasitology, 196(1-2), 6-12. doi: 10.1016/j.vetpar.2013.02.016
Alves, M. E. M., Martins, F. D. C., Bräunig, P., Pivoto, F. L., Sangioni, L. A., & Vogel, F. S. F. (2018). Molecular detection of Cryptosporidium spp. and the occurrence of intestinal parasites in fecal samples of naturally infected dogs and cats. Parasitology Research, 117(9), 3033-3038. doi: 10.1007/s00436-018-5986-4
Asano, K., Suzuki, K., Matsumoto, T., Sakai, T., & Asano, R. (2004). Prevalence of dogs with intestinal parasites in Tochigi, Japan in 1979, 1991 and 2002. Veterinary Parasitology, 120(3), 243-248. doi: 10. 1016/j.vetpar.2004.01.009
Assis, D. C., Resende, D. V., Cabrine-Santos, M., Correia, D., & Oliveira-Silva, M. B. (2013). Prevalence and genetic characterization of Cryptosporidium spp. and Cystoisospora belli in HIV-infected patients. Revista do Instituto de Medicina Tropical, 55(3), 149-154. doi: 10.1590/S0036-46652013000300002
Bresciani, K. D. S., Amarante, A. F. T., Lima, V. M. F., Marcondes, M., Feitosa, F. L. F., Táparo, Serrano, A. C. M., Ishizaki, M. N., Tome, R. O., Perri, S. H. V., & Meireles, M. V. (2008). Infecções por Cryptosporidium spp. em cães de Araçatuba, Brasil. Veterinária e Zootecnia, 15(3), 466-468. https://rvz. emnuvens.com.br/rvz/article/view/396/213
Cui, Z., Dong, H., Wang, R., Jian, F., Zhang, S., Ning, C., & Zhang, L. (2018). A canine model of experimental infection with Cryptosporidium canis. Experimental Parasitology, 195(12), 19-23. doi: 10.1016/j. exppara.2018.09.019
Ederli, B. B., Ederli, N. B., Oliveira, F. C. R., Quirino, C. R., & Carvalho, C. B. (2008). Fatores de risco associados à infecção por Cryptosporidium spp. em cães domiciliados na cidade de Campos dos Goytacazes, Estado do Rio de Janeiro, Brasil. Revista Brasileira de Parasitologia Veterinária, 17(1), 260-266. https://rbpv.org.br/download/17supl.12008/Protozool014
el-Ahraf, A., Tacal, J. V., Sobih, M., Amin, M., Lawrence, W., & Wilcke, B. W. (1991). Prevalence of cryptosporidiosis in dogs and human beings in San Bernardino County, California. Journal of the American Veterinary Medical Association, 198(4), 631-634.
Elliot, A., Morgan, U. M., & Thompson, R. C. A. (1999). Improved staining method for detecting Cryptosporidium oocysts in stools using malachite green. The Journal of General and Applied Microbiology, 45(3), 139-142. doi: 10.2323/jgam.45.139
Fayer, R. (2008). General biology. In R. Fayer, & L. Xiao (Orgs.), Cryptosporidium and Cryptosporidiosis (2nd ed., Cap. 1, pp. 1-42). CRC Press.
Fayer, R., Morgan, U., & Upton, S. J. (2000). Epidemiology of Cryptosporidium: transmission, detection and identification. International Journal for Parasitology, 30(12-13), 1305-1322. doi: 10.1016/s0020-7519 (00)00135-1
Fayer, R., Trout, J. M., Morgan, U. M., Lal, A. A., & Dubey, J. P. (2001). Cryptosporidium canis n. sp. from domestic dogs. The Journal of Parasitology, 87(6), 1415-1422. doi: 10.1645/0022-3395(2001)087 [1415:CCNSFD]2.0.CO;2
Feng, Y., Ryan, U. M., & Xiao, L. (2018). Genetic diversity and population structure of Cryptosporidium. Trends in Parasitology, 34(11), 997-1011. doi: 10.1016/j.pt.2018.07.009
Frizzo, C., Schmidt, A. P., Wagner, G., & Müller, G. A. (2016). Intestinal parasites present in canine fecal samples collected in Rural Areas of municipalities in the Midwest of Santa Catarina, Brazil. Revista de Patologia Tropical, 45(2), 227. doi: 10.5216/rpt.v45i2.41774
Gennari, S. M., Kasai, N., Pena, H. F. J., & Cortez, A. (1999). Ocorrência de protozoários e helmintos em amostras de fezes de cães e gatos da cidade de São Paulo. Brazilian Journal of Veterinary Research and Animal Science, 36(2), 87-91. doi: 10.1590/S1413-95961999000200006
Gonçalves, A. A. M., Leite, J. C., Resende, L. A., Mariano, R. M. da S., Silveira, P., Melo, O. A. de O., Jr., Ribeiro, H. S., Oliveira, D. S. de, Soares, D. F., Santos, T. A. P., Marques, A. F., Galdino, A. S., Martins, O. A., Fº., Dutra, W. O., Silveira-Lemos, D. da, & Giunchetti, R. C. (2019). An overview of immunotherapeutic approaches against Canine Visceral Leishmaniasis: What has been tested on dogs and a new perspective on improving treatment efficacy. Frontiers in Cellular and Infection Microbiology, 9(12), 427. doi: 10.3389/fcimb.2019.00427
González-Díaz, M., Urrea-Quezada, A., Villegas-Gómez, I., Durazo, M., Garibay-Escobar, A., Hernández, J., Lihua, X., & Valenzuela, O. (2016). Cryptosporidium canis in two Mexican toddlers. In Pediatric Infectious Disease Journal, 35(11), 1265-1266. doi: 10.1097/INF.0000000000001287
Huber, F., Bomfim, T. C. B., & Gomes, R. S. (2005). Comparison between natural infection by Cryptosporidium sp., Giardia sp. in dogs in two living situations in the West Zone of the municipality of Rio de Janeiro. Veterinary Parasitology, 130(1-2), 69-72. doi: 10.1016/j.vetpar.2005.03.012
Itoh, N., Tanaka, H., Iijima, Y., Kameshima, S., & Kimura, Y. (2019). Molecular prevalence of Cryptosporidium spp. in breeding kennel dogs. Korean Journal of Parasitology, 57(2), 197-200. doi: 10. 3347/kjp.2019.57.2.197
Jian, F., Qi, M., He, X., Wang, R., Zhang, S., Dong, H., & Zhang, L. (2014). Occurrence and molecular characterization of Cryptosporidium in dogs in Henan Province, China. BMC Veterinary Research, 10(26), 10-13. doi: 10.1186/1746-6148-10-26
Koutinas, A. F., & Koutinas, C. K. (2014). Pathologic mechanisms underlying the clinical findings in canine leishmaniosis due to Leishmania infantum/chagasi. Veterinary Pathology, 51(2), 527-538. doi: 10.1177/ 0300985814521248
Lallo, M. A., & Bondan, E. F. (2006). Prevalência de Cryptosporidium sp. em cães de instituições da cidade de São Paulo. Revista de Saúde Pública, 40(1), 120-125. doi: 10.1590/S0034-89102006000100019
Laurenti, M. D., Santana Leandro, M. V. de, Tomokane, T. Y., De Lucca, H. R. L., Aschar, M., Souza, C. S. F., Silva, R. M., Marcondes, M., Matta, V. L. R. da. (2014). Comparative evaluation of the DPP® CVL rapid test for canine serodiagnosis in area of visceral leishmaniasis. Veterinary Parasitology, 205(3-4), 444-450. doi: 10.1016/j.vetpar.2014.09.002
Lucca, P. de, Gaspari, E. N., Bozzoli, L. M., Funada, M. R., Silva, S. O. S., Iuliano, W., & Soares, R. M. (2009). Molecular characterization of Cryptosporidium spp. from HIV infected patients from an urban area of Brazil. Revista do Instituto de Medicina Tropical de São Paulo, 51(6), 341-343. doi: 10.1590/S00 36-46652009000600007
Mac Kenzie, W. R., Hoxie, N. J., Proctor, M. E., Gradus, M. S., Blair, K. A., Peterson, D. E., Kazmierczak, J. J., Addiss, D. G., Fox, K. R., Rose, J. B., & Davis, J. B. (1994). A massive outbreak in Milwaukee of Cryptosporidium infection transmitted through the public water supply. The New England Journal of Medicine, 331(3), 161-167. doi: 10.1056/NEJM199407213310304
Mancianti, F., Gramiccia, M., Gradoni, L., & Pieri, S. (1988). Studies on canine leishmaniasis control. 1. Evolution of infection of different clinical forms of canine leishmaniasis following antimonial treatment. Transactions of the Royal Society of Tropical Medicine and Hygiene, 82(4), 566-567. doi: 10.1016/0035-9203(88)90510-X
Meloni, B. P., & Thompson, R. C. A. (1996). Simplified methods for obtaining purified oocysts from mice and for growing Cryptosporidium parvum in vitro. The Journal of Parasitology, 82(5), 757-762.
Miambo, R. D., Laitela, B., Malatji, M. P., Afonso, S. M. S., Pondja, A., Jr., Lindh, J., & Mukaratirwa, S. (2019). Prevalence of Giardia and Cryptosporidium in young livestock and dogs in Magude district of Maputo Province, Mozambique. Onderstepoort Journal of Veterinary Research, 86(1), 1-6. doi: 10.4102/ ojvr.v86i1.1709
Miller, D. L., Liggett, A., Radi, Z. A., & Branch, L. O. (2003). Gastrointestinal cryptosporidiosis in a puppy. Veterinary Parasitology, 115(3), 199-204. doi: 10.1016/S0304-4017(03)00237-1
Ministério da Saúde (2014). Manual de vigilância e controle da leishmaniose visceral. Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Brasília, DF: Ministério da Saúde.
Olabanji, G. M., Maikai, B. V., & Otolorin, G. R. (2016). Prevalence and risk factors associated with faecal shedding of Cryptosporidium oocysts in dogs in the Federal Capital Territory, Abuja, Nigeria. Veterinary Medicine International, 2016(1), 4591238. doi: 10.1155/2016/4591238
Palmer, C. S., Traub, R. J., Robertson, I. D., Devlin, G., Rees, R., & Thompson, R. C. A. (2008). Determining the zoonotic significance of Giardia and Cryptosporidium in Australian dogs and cats. Veterinary Parasitology, 154(1-2), 142-147. doi: 10.1016/j.vetpar.2008.02.031
Peixoto, H. M., Oliveira, M. R. F., & Romero, G. A. S. (2015). Serological diagnosis of canine visceral leishmaniasis in Brazil: systematic review and meta-analysis. Tropical Medicine and International Health, 20(3), 334-352. doi: 10.1111/tmi.12429
Poot, J., Rogers, M. E., Bates, P. A., & Vermeulen, A. (2005). Detailed analysis of an experimental challenge model for Leishmania infantum (JPC strain) in dogs. Veterinary Parasitology, 130(1-2), 41-53. doi: 10. 1016/j.vetpar.2005.03.002
Reis, A. B., Martins-Filho, O. A., Teixeira-Carvalho, A., Giunchetti, R. C., Carneiro, C. M., Mayrink, W. Taguri, L. W., Corrêa-Oliveira, R. (2009). Systemic and compartmentalized immune response in canine visceral leishmaniasis. Veterinary Immunology and Immunopathology, 128(1-3), 87-95. doi: 10.1016/j. vetimm.2008.10.307
Santos, F. A. G., Yamamura, M. H., Vidotto, O., & Camargo, P. L. (2007). Ocorrência de parasitos gastrintestinais em cães (Canis familiaris) com diarreia aguda oriundos da região metropolitana de Londrina, Estado do Paraná, Brasil. Semina: Ciências Agrárias, 28(2), 257. doi: 10.5433/1679-0359.2007 v28n2p257
Satoh, M., Matsubara-Nihei, Y., Sasaki, T., & Nakai, Y. (2006). Characterization of Cryptosporidium canis isolated in Japan. Parasitology Research, 99(6), 746-748. doi: 10.1007/s00436-006-0216-x
Savioli, L., Smith, H., & Thompson, A. (2006). Giardia and Cryptosporidium join the “Neglected Diseases Initiative.” Trends in Parasitology, 22(5), 203-208. doi: 10.1016/j.pt.2006.02.015
Sevá, A. P., Funada, M. R., Souza, S. O., Nava, A., Richtzenhain, L. J., & Soares, R. M. (2010). Occurrence and molecular characterization of Cryptosporidium spp. isolated from domestic animals in a rural area surrounding Atlantic dry forest fragments in Teodoro Sampaio municipality, State of São Paulo, Brazil. Revista Brasileira de Parasitologia Veterinária, 19(4), 249-253. doi: 10.1590/s1984-296120100004000 11
Shukla, R., Giraldo, P., Kraliz, A., Finnigan, M., & Sanchez, A. L. (2006). Cryptosporidium spp. and other zoonotic enteric parasites in a sample of domestic dogs and cats in the Niagara region of Ontario. The Canadian Veterinary Journal = La Revue Veterinaire Canadienne, 47(12), 1179-1184. https://www.ncbi. nlm.nih.gov/pmc/articles/PMC1636587/pdf/cvj47pg1179.pdf
Silva, K. L. O., Melo, L. M., Perosso, J., Oliveira, B. B., Santos, P. S. P. dos, Eugênio, F. de R., & Lima, V. M. F. de. (2013). CD95 (FAS) and CD178 (FASL) induce the apoptosis of CD4+ and CD8+ cells isolated from the peripheral blood and spleen of dogs naturally infected with Leishmania spp. Veterinary Parasitology, 197(3-4), 470-476. doi: 10.1016/j.vetpar.2013.07.012
Taghipour, A., Olfatifar, M., Bahadory, S., Godfrey, S. S., Abdoli, A., Khatami, A., Javanmar, E., & Shahrivar, F. (2020). The global prevalence of Cryptosporidium infection in dogs: a systematic review and meta-analysis. Veterinary Parasitology, 281(3), 109093. doi: 10.1016/j.vetpar.2020.109093
Tangtrongsup, S., Scorza, A. V., Reif, J. S., Ballweber, L. R., Lappin, M. R., & Salman, M. D. (2020). Seasonal distributions and other risk factors for Giardia duodenalis and Cryptosporidium spp. infections in dogs and cats in Chiang Mai, Thailand. Preventive Veterinary Medicine, 174(1), 104820. doi: 10.1016/j. prevetmed.2019.104820
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., & Higgins, D. G. (1997). The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25(24), 4876-4882. doi: 10.1093/nar/25.24.4876
Thompson, R. C. A., Palmer, C. S., & O’Handley, R. (2008). The public health and clinical significance of Giardia and Cryptosporidium in domestic animals. Veterinary Journal, 177(1), 18-25. doi: 10.1016/j.tvjl. 2007.09.022
Toepp, A. J., & Petersen, C. A. (2020). The balancing act: immunology of leishmaniosis. Research in Veterinary Science, 130(6), 19-25. doi: 10.1016/j.rvsc.2020.02.004
Turnwald, G. H., Barta, O., Taylor, H. W., Kreeger, J., Coleman, S. U., & Pourciau, S. S. (1988). Cryptosporidiosis associated with immunosuppression attributable to distemper in a pup. Journal of the American Veterinary Medical Association, 192(1), 79-81.
Willard, M. D., & Bouley, D. (1999). Cryptosporidiosis, coccidiosis, and total colonic mucosal collapse in an immunosuppressed puppy. Journal of the American Animal Hospital Association, 35(5), 405-409. doi: 10.5326/15473317-35-5-405
Xiao, L., Alderisio, K., Limor, J., Royer, M., & Lal, A. A. (2000). Identification of species and sources of Cryptosporidium oocysts in storm waters with a small-subunit rRNA-based diagnostic and genotyping tool. Applied and Environmental Microbiology, 66(12), 5492-5498. doi: 10.1128/AEM.66.12.5492-5498. 2000
Xiao, L., Cama, V. A., Cabrera, L., Ortega, Y., Pearson, J., & Gilman, R. H. (2007). Possible transmission of Cryptosporidium canis among children and a dog in a household. Journal of Clinical Microbiology, 45(6), 2014-2016. doi: 10.1128/JCM.00503-07
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