Prevalence of Cryptosporidium infection in domestic cats from an urban area in Brazil

Luiz da Silveira Neto, Giovanni Widmer, Valéria Marçal Felix de Lima, Marcelo Vasconcelos Meireles, Sandra Valéria Inácio, Marcel Gambin Marques, Ana Elisa Gregui Watanabe Marques, Lucas Vinícius Shigaki de Matos, Mariele Fernanda da Cruz Panegossi, Katia Denise Saraiva Bresciani

Abstract


We investigated the occurrence of Cryptosporidium oocysts shedding by domestic cats in an urban setting. The calculation of minimum sample size was based on an estimated prevalence of 10%, 5% absolute sampling error and a 5% significance level, resulting in 138 cats. A total of 612 owners of 2,290 cats had to be contacted for achieving the minimal sample size. In the end, only 55 owners accepted to participate in this investigation. Stool samples collected from 138 dogs were examined by microscopy using modified Kinyoun acid-fast staining, capture ELISA and nested-PCR followed by sequencing. Samples were considered positive when Cryptosporidium were detected by at least two diagnostic methods. Thirteen samples were positive (9.4%; 95% CI: 4.5 - 14.3). Cryptosporidium amplicons from seven out of the 13 samples were successfully sequenced and shared 99% genetic similarity to Cryptosporidium felis, GenBank access AF112575.1 was found. We concluded that Cryptosporidium infection is common in domestic cats from urban area and veterinary practitioners should guide cat owners to adopt preventive measures against the parasite to reduce the chance of infection in cats and householders.

Keywords


Prevalence; Public Health; Epidemiology; Cryptosporidiosis; Feline.

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References


Alpert, G., Bell, L. M., Kirkpatrick, C. E., Budnick, L. D., Campos, J. M., Friedman, H. M., & Plotkin, S. A. (1986). Outbreak of cryptosporidiosis in a Day-Care Center. Pediatrics, 77(2), 152-157. doi: 10.1203/ 00006450-198504000-01079

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

Bajer, A. (2008). Cryptosporidium and Giardia spp. infections in humans, animals and the environment in Poland. Parasitology Research, 104(1), 1-17. doi: 10.1007/s00436-008-1179-x

Ballweber, L. R., Panuska, C., Huston, C. L., Vasilopulos, R., Pharr, G. T., & Mackin, A. (2009). Prevalence of and risk factors associated with shedding of Cryptosporidium felis in domestic cats of Mississippi and Alabama. Veterinary Parasitology, 160(3-4), 306-310. doi: 10.1016/j.vetpar.2008.11.018

Barbee, S. L., Weber, D. J., Sobsey, M. D., & Rutala, W. A. (1999). Inactivation of Cryptosporidium parvum oocyst infectivity by disinfection and sterilization processes. Gastrointestinal Endoscopy, 49(5), 605-611. doi: 10.1016/S0016-5107(99)70389-5

Beser, J., Toresson, L., Eitrem, R., Krusnell, J. W., & Lebbad, M. (2015). Zoonotic transmission of Cryptosporidium felis in a household. Tropical Medicine & International Health, 18(2014), 170-171. doi: 10.3402/iee.v5.28463

Chalmers, R. M., & Katzer, F. (2013). Looking for Cryptosporidium: the application of advances in detection and diagnosis. Trends in Parasitology, 29(5), 237-251. doi: 10.1016/j.pt.2013.03.001

Chappell, C. L., Okhuysen, P. C., Langer-Curry, R., Widmer, G., Akiyoshi, D. E., Tanriverdi, S., & Tzipori, S. (2006). Cryptosporidium hominis: experimental challenge of healthy adults. American Journal of Tropical Medicine and Hygiene, 75(5), 851-857. doi: 10.4269/ajtmh.2006.75.851

Chappell, C. L, Okhuysen, P. C., Sterling, C. R., & DuPont, H. L. (1996). Cryptosporidium parvum: intensity of infection and oocyst excretion patterns in healthy volunteers. The Journal of Infectious Diseases, 173(1), 232-236. doi: 10.1093/infdis/173.1.232

Coelho, W. M. D., Amarante, A. F. T. do, Soutello, R. V. G. de, Meireles, M. V., & Bresciani, K. D. S. (2009). Ocorrência de parasitos gastrintestinais em amostras fecais de felinos no município de Andradina, São Paulo. Revista Brasileira de Parasitologia Veterinaria, 18(2), 46-49. doi: 10.4322/rbpv .01802010

DuPont, H. L., Chappell, C. L., Sterling, C. R., Okhuysen, P. C., Rose, J. B., & Jakubowski, W. (1995). The Infectivity of Cryptosporidium parvum in Healthy Volunteers. New England Journal of Medicine, 332(13), 855-859. doi: 10.1056/NEJM199503303321304

Elwin, K., Hadfield, S., Robinson, G., & Chalmers, R. M. (2012). The epidemiology of sporadic human infections with unusual cryptosporidia detected during routine typing in England and Wales , 2000 - 2008. Epidemiology and Infection, 140(4), 673-683. doi: 10.1017/S0950268811000860

Fayer, R., Santín, M., Trout, J. M., & Dubey, J. P. (2006). Detection of Cryptosporidium felis and Giardia duodenalis Assemblage F in a cat colony. Veterinary Parasitology, 140(1-2), 44-53. doi: 10.1016/j. vetpar.2006.03.005

Feng, Y., Li, N., Duan, L., & Xiao, L. (2009). Cryptosporidium genotype and subtype distribution in raw wastewater in Shanghai, China: evidence for possible unique Cryptosporidium hominis transmission. Journal of Clinical Microbiology, 47(1), 153-157. doi: 10.1128/JCM.01777-08

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

Funada, M. R., Pena, H. F. J., Soares, R. M., Amaku, M., & Gennari, S. M. (2007). Frequência de parasitos gastrintestinais em cães e gatos atendidos em hospital-escola veterinário da cidade de São Paulo. Arquivo Brasileiro de Medicina Veterinaria e Zootecnia, 59(5), 1338-1340. doi: 10.1590/S0102-09352 007000500038

Gennari, S. M., Kasai, N., Pena, H. F. de 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

Hajdušek, O., Ditrich, O., & Šlapeta, J. (2004). Molecular identification of Cryptosporidium spp. in animal and human hosts from the Czech Republic. Veterinary Parasitology, 122(3), 183-192. doi: 10.1016/j. vetpar.2004.04.005

Hajian-Tilaki, K. (2011). Sample size estimation in epidemiologic studies. Caspian Journal of Internal Medicine, 2(4), 289-298.

Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95-98.

Huber, F., Bomfim, T. C. B., & Gomes, R. S. (2002). Comparação entre infecção por Cryptosporidium sp. e por Giardia sp. em gatos sob dois sistemas de criação. Revista Brasileira de Parasitologia Veterinária, 11(1), 7-12.

Huber, F., Silva, S. da, Bomfim, T. C. B., Teixeira, K. R. S., & Bello, A. R. (2007). Genotypic characterization and phylogenetic analysis of Cryptosporidium sp. from domestic animals in Brazil. Veterinary Parasitology, 150(1-2), 65-74. doi: 10.1016/j.vetpar.2007.08.018

Ito, Y., Itoh, N., Kimura, Y., & Kanai, K. (2016). Molecular detection and characterization of Cryptosporidium spp. among breeding cattery cats in Japan. Parasitology Research, 115(5), 2121-2123. doi: 10.1007/s00436-016-4984-7

Keith, C. L., Radecki, S. V., & Lappin, M. R. (2003). Evaluation of fenbendazole for treatment of Giardia infection in cats concurrently infected with Cryptosporidium parvum. American Journal of Veterinary Research, 64(8), 1027-1029. doi: 10.2460/ajvr.2003.64.1027

Lucca, P. de, De Gaspari, E. N., Bozzoli, L. M., Funada, M. R., Souza Silva, S. O. de, 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/S0036-46652009000600006

Lucio-Forster, A., Griffiths, J. K., Cama, V. A., Xiao, L., & Bowman, D. D. (2010). Minimal zoonotic risk of cryptosporidiosis from pet dogs and cats. Trends in Parasitology, 26(4), 174-179. doi: 10.1016/j.pt. 2010.01.004

Ma, P., & Soave, R. (1983). Three-step stool examination for cryptosporidiosis in 10 homosexual men with protracted watery diarrhea. The Journal of Infectious Diseases, 147(5), 824-828. doi: 10.1093/infdis/ 147.5.824

Marks, S. L., Hanson, T. E., & Melli, A. C. (2004). Comparison of direct immunofluorescence, modified acid-fast staining, and enzyme immunoassay techniques for detection of Cryptosporidium spp in naturally exposed kittens. Journal of the American Veterinary Medical Association, 225(10), 1549-1553. doi: 10.2460/javma.2004.225.1549

Meloni, B. P., & Thompson, R. C. (1996). Simplified methods for obtaining purified oocysts from mice and for growing Cryptosporidium parvum in vitro. The Journal of Parasitology, 82(5), 757-762. doi: 10. 2307/3283888

Méndez-Hermida, F., Ares-Mazás, E., McGuigan, K. G., Boyle, M., Sichel, C., & Fernández-Ibáñez, P. (2007). Disinfection of drinking water contaminated with Cryptosporidium parvum oocysts under natural sunlight and using the photocatalyst TiO2. Journal of Photochemistry and Photobiology B: Biology, 88(2-3), 105-111. doi: 10.1016/j.jphotobiol.2007.05.004

Moreira, A. S., Babtista, C. T., Brasil, C. L., Valente, J. S. S., Bruhn, F. R. P., & Pereira, D. I. B. (2018). Risk factors and infection due to Cryptosporidium spp. in dogs and cats in southern Rio Grande do Sul. Brazlian Journal of Veterinary Parasitology, 27(1), 112-117. doi: 10.1590/s1984-296120180012

Neira, O, P., Muñoz, S, N., & Rosales L, M. J. (2010). Infección por Cryptosporidium parvum en una mujer embarazada, inmunocompetente, con riesgo ocupacional. Revista Chilena de Infectología, 27(4), 345-349. doi: 10.4067/S0716-10182010000500011

Oates, S. C., Miller, M. A., Hardin, D., Conrad, P. A., Melli, A., Jessup, D. A.,… Miller, W. A. (2012). Prevalence, environmental loading, and molecular characterization of Cryptosporidium and Giardia isolates from domestic and wild animals along the central California coast. Applied and Environmental Microbiology, 78(24), 8762-8772. doi: 10.1128/AEM.02422-12

Overgaauw, P. A. M., van Zutphen, L., Hoek, D., Yaya, F. O., Roelfsema, J., Pinelli, E.,… Kortbeek, L. M. (2009). Zoonotic parasites in fecal samples and fur from dogs and cats in The Netherlands. Veterinary Parasitology, 163(1-2), 115-122. doi: 10.1016/j.vetpar.2009.03.044

Pedraza-Diaz, S., Amar, C., Iversen, A. M., Stanley, P. J., & McLauchlin, J. (2001). Unusual Cryptosporidium species recovered from human faeces: First description of Cryptosporidium felis and Cryptosporidium “dog type” from patients in England. Journal of Medical Microbiology, 50(3), 293-296. doi: 10.1099/0022-1317-50-3-293

Pereira, C. R. A., & Ferreira, A. P. (2012). Ocorrência e fatores de risco da criptosporidiose em felinos de companhia de idosos. Revista Brasileira de Geriatria e Gerontologia, 15(4), 681-691. doi: 10.1590/S1 809-98232012000400009

Pivoto, F. L., Lopes, L. F. D., Vogel, F. S. F., Botton, S. A., & Sangioni, L. A. (2013). Ocorrência de parasitos gastrointestinais e fatores de risco de parasitismo em gatos domésticos urbanos de Santa Maria, RS, Brasil. Ciência Rural, 43(8), 1453-1458. doi: 10.1590/S0103-84782013000800018

Ragozo, A. M. A., Muradian, V., Silva, J. C. R. e, Caravieri, R., Amajoner, V. R., Magnabosco, C., & Gennari, S. M. (2002). Ocorrência de parasitos gastrintestinais em fezes de gatos das cidades de São Paulo e Guarulhos. Brazilian Journal of Veterinary Research and Animal Science, 39(5), 244-246. doi: 10.1590/S1413-95962002000500005

Robertson, L. J., Campbell, A. T., & Smith, H. V. (1992). Survival of Cryptosporidium parvum oocysts under various environmental pressures. Applied and Environmental Microbiology, 58(11), 3494-3500. doi: 0099-2240/92/113494-07$02.00/0

Rochelle, P. A., Upton, S. J., Montelone, B. A., & Woods, K. (2005). The response of Cryptosporidium parvum to UV light. Trends in Parasitology, 21(2), 81-87. doi: 10.1016/j.pt.2004.11.009

Ryan, U., Hijjawi, N., & Xiao, L. (2018). Foodborne cryptosporidiosis. International Journal for Parasitology, 48(1), 1-12. doi: 10.1016/j.ijpara.2017.09.004

Samie, A., Tsipa, M. A., & Bessong, P. (2013). The epidemiology of Cryptosporidium in cats and dogs in the Thohoyandou region, South Africa. African Journal of Microbiology Research, 7(21), 2510-2518. doi: 10.5897/AJMR12.1391

Sargent, K. D., Morgan, U. M., Elliot, A, & Thompson, R. C. (1998). Morphological and genetic characterisation of Cryptosporidium oocysts from domestic cats. Veterinary Parasitology, 77(4), 221-227. doi: 10.1016/S0304-4017(98)00122-8

Smith, H. V., & Nichols, R. A. B. (2010). Cryptosporidium: Detection in water and food. Experimental Parasitology, 124(1), 61-79. doi: 10.1016/j.exppara.2009.05.014

Thomaz, A., Meireles, M. V., Soares, R. M., Pena, H. F. J., & Gennari, S. M. (2007). Molecular identification of Cryptosporidium spp. from fecal samples of felines, canines and bovines in the state of São Paulo, Brazil. Veterinary Parasitology, 150(4), 291-296. doi: 10.1016/j.vetpar.2007.09.023

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

Tiangtip, R., & Jongwutiwes, S. (2002). Molecular analysis of Cryptosporidium species isolated from HIV-infected patients in Thailand. Tropical Medicine & International Health, 7(4), 357-364. doi: 10.1046/j. 1365-3156.2002.00855.x

Tzipori, S., & Widmer, G. (2008). A hundred-year retrospective on cryptosporidiosis. Trends in Parasitology, 24(4), 184-189. doi: 10.1016/j.pt.2008.01.002

Wang, R., Zhang, X., Zhu, H., Zhang, L., Feng, Y., Jian, F.,… Xiao, L. (2011). Genetic characterizations of Cryptosporidium spp. and Giardia duodenalis in humans in Henan, China. Experimental Parasitology, 127(1), 42-45. doi: 10.1016/j.exppara.2010.06.034

Xiao, L., Escalante, L., Yang, C., Sulaiman, I., Escalante, A. A., Montali, R. J.,… Lal, A. A. (1999a). Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Applied and Environmental Microbiology, 65(4), 1578-1583. Retrieved from http://www.ncbi.nlm.nih. gov/pubmed/10103253

Xiao, L., & Fayer, R. (2008). Molecular characterisation of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. International Journal for Parasitology, 38(11), 1239-1255. doi: 10.1016/j.ijpara.2008.03.006

Xiao, L., Fayer, R., Ryan, U. M., & Upton, S. J. (2004). Cryptosporidium taxonomy: recent advances and implications for Public Health. Clinical Microbiology Reviews, 17(1), 72-97. doi: 10.1128/CMR.17.1.72

Xiao, L., Morgan, U. M., Limor, J., Escalante, A., Arrowood, M., Shulaw, W.,… Lal, A. A. (1999b). Genetic diversity within Cryptosporidium parvum and related Cryptosporidium species. Applied and Environmental Microbiology, 65(8), 3386-3391. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/ 10427023




DOI: http://dx.doi.org/10.5433/1679-0359.2020v41n6p2677

Semina: Ciênc. Agrár.
Londrina - PR
E-ISSN 1679-0359
DOI: 10.5433/1679-0359
E-mail: semina.agrarias@uel.br
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