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Molecular identification of Enterocytozoon bieneusi, Cryptosporidium, and Giardia in Brazilian captive birds

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Abstract

A total of 85 fecal samples from captive birds collected from October 2013 to September 2014 in Uberlândia and Belo Horizonte in the state of Minas Gerais (Brazil) were evaluated for the presence of Enterocytozoon bieneusi, Cryptosporidium, and Giardia by PCR. Of these, three birds were found positive for E. bieneusi (3.5%), two for Cryptosporidium (2.3%), and one for Giardia (1.2%). Two genotypes of E. bieneusi were detected by nucleotide sequence analysis of the ITS region, genotypes D and Peru 6 in a swan goose and in two rock pigeons, respectively. For Cryptosporidium and Giardia, nucleotide sequence analysis of the SSU rRNA identified Cryptosporidium baileyi and Duck genotype in a swan goose and a mandarin duck, respectively, and Giardia duodenalis assemblage A in a toco toucon. Our results demonstrate that human-pathogenic E. bieneusi genotypes D and Peru6 and G. duodenalis assemblage A are present in captive birds in Brazil, corroborating their potential role as a source of human infection and environmental contamination.

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References

  • Abe N, Makino I, Kojima A (2012) Molecular characterization of Giardia psittaci by multilocus sequence analysis. Infect Genet Evol 12:1710–1716

    Article  CAS  PubMed  Google Scholar 

  • Bart A, Wentink-Bonnema EM, Heddema ER, Buijis J, van Gool T (2008) Frequent occurrence of humam-associated microsporidia in fecal droppings of urban pigeons in Amsterdam, the Netherlands. Appl Environ Microbiol 74:7056–7058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berrilli F, D’Alfonso R, Giangaspero A, Marangi M, Brandonisio O, Kaboré Y, Glé C, Cianfanelli C, Lauro R, Di Cave D (2012) Giardia duodenalis genotypes and Cryptosporidium species in humans and domestic animals in Côte d’Ivoire: occurrence and evidence for environmental contamination. Trans R Soc Trop Med Hyg 106:191–195

    Article  PubMed  Google Scholar 

  • Buckholt MA, Lee JH, Tzipori S (2002) Prevalence of Enterocytozoon bieneusi in swine: an 18-month survey at a slaughterhouse in Massachusetts. Appl Environ Microbiol 68:2595–2599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cano L, de Lucio A, Bailo B, Cardona GA, Muadica ASO, Lobo L, Carmena D (2016) Identification and genotyping of Giardia spp. and Cryptosporidium spp. isolates in aquatic birds in the Salburua wetlands, Álava, Northern Spain. Vet Parasitol 221:144–148

    Article  PubMed  Google Scholar 

  • Chelladurai JJ, Clark ME, Kváč M, Holubová N, Khan E, Stenger BL, Giddings CW, McEvoy J (2016) Cryptosporidium galli and novel Cryptosporidium avian genotype VI in North American red-winged blackbirds (Agelaius phoeniceus). Parasitol Res 115:1901–1906

    Article  PubMed  Google Scholar 

  • Current WL, Upton SJ, Haynes TB (1986) The life cycle of Cryptosporidium baileyi n. sp. (Apicomplexa, Cryptosporidiidae) infecting chickens. J Protozool 33:289–296

    Article  CAS  PubMed  Google Scholar 

  • da Cunha MJ, Cury MC, Santín M (2016) Widespread presence of human-pathogenic Enterocytozoon bieneusi genotypes in chickens. Vet Parasitol 217:108–112

    Article  PubMed  Google Scholar 

  • da Silva Fiuza VR, Lopes CW, de Oliveira FC, Fayer R, Santín M (2016) New findings of Enterocytozoon bieneusi in beef and dairy cattle in Brazil. Vet Parasitol 216:46–51

    Article  PubMed  Google Scholar 

  • Erlandsen SL, Weisbrod AR, Knudson LW, Olereich R, Dodge WE, Jakubowski W, Bemrick WJ (1991) Giardiasis in wild and captive bird populations: High prevalence in herons and budgerigars. Int J Environ Health Res 1:132–143

    Article  Google Scholar 

  • Feng Y, Li N, Dearen T, Lobo ML, Matos O, Cama V, Xiao L (2011) Development of a multilocus sequence typing tool for high-resolution genotyping of Enterocytozoon bieneusi. Appl Environ Microbiol 77:4822–4828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galvan-Díaz AL, Magnet A, Fenoy S, Henriques-Gil N, Haro M, Gordo FP, Millán J, Miró J, del Águila C, Izquierdo F (2014) Microsporidia detection and genotyping study of human pathogenic E. bieneusi in animals from Spain. Plos One 9:e92289

    Article  PubMed  PubMed Central  Google Scholar 

  • Gomes RS, Huber F, da Silva S, do Bomfim TCB (2012) Cryptosporidium spp. parasitize exotic birds that are commercialized in markets, commercial aviaries, and pet shops. Parasitol Res 110:1363–1370

    Article  PubMed  Google Scholar 

  • Haro M, Henriques-Gil N, Fenoy S, Izquierdo F, Alonso F, Del Aguila C (2006) Detection and genotyping of Enterocytozoon bieneusi in pigeons. J Eukaryot Microbiol 53:S58–S60

    Article  PubMed  Google Scholar 

  • Holsback L, Cardoso MJ, Fagnani R, Patelli TH (2013) Natural infection by endoparasites among free-living wild animals. Rev Bras Parasitol Vet 22:302–306

    Article  PubMed  Google Scholar 

  • Holubová N, Sak B, Horčičková M, Hlásková L, Květoňová D, Menchaca S, McEvoy J, Kváč M (2016) Cryptosporidium avium n. sp. (Apicomplexa: Cryptosporidiidae) in birds. Parasitol Res 115:2243–2251

    Article  PubMed  Google Scholar 

  • Hopkins RM, Meloni BP, Groth DM, Wetherall JD, Reynoldson JA, Thompson RCA (1997) Ribosomal RNA sequencing reveals differences between the genotypes of Giardia isolates recovered from humans and dogs living in the same locality. J Parasitol 83:44–51

    Article  CAS  PubMed  Google Scholar 

  • Huber F, da Silva S, Bonfim TCB, Teixeira KRS, Bello AR (2007) Genotypic characterization and phylogenetic analysis of Cryptosporidium sp. from domestic animals in Brazil. Vet Parasitol 150:65–74

    Article  CAS  PubMed  Google Scholar 

  • Jellison KL, Distel DL, Hemond HF, Schauer DB (2004) Phylogenetic analysis of the hypervariable region of the 18S rRNA gene of Cryptosporidium oocysts in feces of Canada geese (Branta canadensis): evidence for five novel genotypes. Appl Environ Microbiol 70:452–458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kasicková D, Sak B, Kvác M, Ditrich O (2009) Sources of potentially infectious human microsporidia: molecular characterization of microsporidia isolates from exotic birds in the Czech Republic, prevalence study and importance of birds in epidemiology of the human microsporidial infections. Vet Parasitol 165:125–130

    Article  PubMed  Google Scholar 

  • Lallo MA, Calábria P, Milanelo L (2012) Encephalitozoon and Enterocytozoon (Microsporidia) spores in stool from pigeons and exotic birds. Vet Parasitol 190:418–422

    Article  PubMed  Google Scholar 

  • Li Q, Li L, Tao W, Jiang Y, Wan Q, Lin Y, Li W (2016) Molecular investigation of Cryptosporidium in small caged pets in northeast China: host specificity and zoonotic implications. Parasitol Res 15:2905–2911

    Article  Google Scholar 

  • Lobo ML, Xiao L, Cama V, Magalhaes N, Antunes F, Matos O (2006) Identification of potentially human-pathogenic Enterocytozoon bieneusi genotypes in various birds. Appl Environ Microbiol 72:7380–7382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Majewska AC, Taddeus KG, Słodkowicz-Kowalska A, Tamang L, Jędrzejewski S, Zduniak P, Solarczyk P, Nowosad A, Nowosad P (2009) The role of free-ranging, captive, and domestic birds of Western Poland in environmental contamination with Cryptosporidium parvum oocysts and Giardia lamblia cysts. Parasitol Res 104:1093–1099

    Article  PubMed  Google Scholar 

  • McLauchlin J, Pedraza-Díaz S, Amar-Hoetzeneder C, Nichols GL (1999) Genetic characterization of Cryptosporidium strains from 218 patients with diarrhea diagnosed as having sporadic cryptosporidiosis. J Clin Microbiol 37:3153–3158

    CAS  PubMed  PubMed Central  Google Scholar 

  • McRoberts KM, Meloni BP, Morgan UM, Marano R, Binz N, Eriandsen SL, Halse SA, Thompson RC (1996) Morphological and molecular characterization of Giardia isolated from the straw-necked ibis (Threskiornis spinicollis) in Western Australia. J Parasitol 82:711–718

    Article  CAS  PubMed  Google Scholar 

  • Müller MG, Kinne J, Schuster RK, Walochnik J (2008) Outbreak of microsporidiosis caused by Enterocytozoon bieneusi in falcons. Vet Parasitol 152:67–78

    Article  PubMed  Google Scholar 

  • Nakamura AA, Meireles MV (2015) Cryptosporidium in birds - a review. Braz J Vet Parasitol 24:253–267

    Article  Google Scholar 

  • Nakamura AA, Simões DC, Antunes RG, da Silva DC, Meireles MV (2009) Molecular characterization of Cryptosporidium spp. from fecal samples of birds kept in captivity in Brazil. Vet Parasitol 166:47–51

    Article  CAS  PubMed  Google Scholar 

  • Nakamura AA, Homem CG, da Silva AMJ, Meireles MV (2014) Diagnosis of gastric cryptosporidiosis in birds using a duplexreal-time PCR assay. Vet Parasitol 205:7–13

    Article  CAS  PubMed  Google Scholar 

  • O’Donoghue PJ (1995) Cryptosporidium and cryptosporidiosis in man and animals. Int J Parasitol 25:139–195

    Article  PubMed  Google Scholar 

  • Papini R, Girivetto M, Marangi M, Mancianti F, Giangaspero A (2012) Endoparasite infection in pet and zoo Birds in Italy. Sci World J 2012:1–9

    Article  Google Scholar 

  • Pirestani M, Sadraei J, Forouzandeh M (2013) Molecular characterization and genotyping of human related microsporidia in free-ranging and captive pigeons of Tehran, Iran. Infect Genet Evol 20:495–499

    Article  CAS  PubMed  Google Scholar 

  • Reboredo-Fernández A, Ares-Mazás E, Caccio SM, Gómez-Couso H (2015) Occurrence of Giardia and Cryptosporidium in wild birds in Galicia (Northwest Spain). Parasitology 142:917–925

    Article  PubMed  Google Scholar 

  • Ryan U (2010) Cryptosporidium in birds, fish and amphibians. Exp Parasitol 124:113–120

    Article  PubMed  Google Scholar 

  • Ryan U, Caccio SM (2013) Zoonotic potential of Giardia. Int J Parasitol 43:943–956

    Article  CAS  PubMed  Google Scholar 

  • Ryan UM, Xiao L, Read C, Sulaiman IM, Monis P, Lal AA, Fayer R, Pavlásek I (2003) A redescription of Cryptosporidium galli Pavlasek, 1999 (Apicomplexa: Cryptosporidiidae) from birds. J Parasitol 89:809–813

    Article  CAS  PubMed  Google Scholar 

  • Ryan U, Fayer R, Xiao L (2014) Cryptosporidium species in humans and animals: current understanding and research needs. Parasitology 141:1667–1685

    Article  PubMed  Google Scholar 

  • Santín M (2015) Enterocytozoon bieneusi. In: Xiao L, Ryan U (eds) Biology of Foodborne Parasites, 1st edn. CRC Press, Boca Raton, pp 149–174

    Google Scholar 

  • Santín M, Fayer R (2011) Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals. Res Vet Sci 90:363–371

    Article  PubMed  Google Scholar 

  • Sevá AP, Funada MR, Richtzenhain L, Guimarães MB, Souza SO, Allegretti L, Sinhorini JA, Duarte VV, Soares M (2011) Genotyping of Cryptosporidium spp. from free-living wild birds from Brazil. Vet Parasitol 175:27–32

    Article  Google Scholar 

  • Slavin D (1955) Cryptosporidium meleagridis (sp. nov.). J Comp Pathol 65:262–266

    Article  CAS  PubMed  Google Scholar 

  • Sréter T, Varga I (2000) Cryptosporidiosis in birds—a review. Vet Parasitol 87:261–279

    Article  PubMed  Google Scholar 

  • Stodkowicz-Kowalska A, Graczyk TK, Nowosad A, Majewska AC (2013) First detection of microsporidia in raised pigeons in Poland. Ann Agric Environ Med 20:13–15

    Google Scholar 

  • Wang L, Xue X, Li J, Zhou Q, Yu Y, Du A (2014) Cryptosporidiosis in broiler chickens in Zhejiang Province, China: molecular characterization of oocysts detected in fecal samples. Parasite 21:36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao L (2010) Molecular epidemiology of cryptosporidiosis: an update. Exp Parasitol 124:80–88

    Article  CAS  PubMed  Google Scholar 

  • Xiao L, Morgan U, Limor J, Escalante A, Arrowood M, Shulaw W, Thompson RC, Fayer R, Lal AA (1999) Genetic diversity within Cryptosporidium parvum and related Cryptosporidium species. Appl Environ Microbiol 65:3386–33918

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao W, Yu S, Yang Z, Zhang Y, Zhang L, Wang R, Zhang W, Yang F, Liu F (2016) Genotyping of Enterocytozoon bieneusi (Microsporidia) isolated from various birds in China. Infec Genet Evol 40:151–154

    Article  CAS  Google Scholar 

  • Zhou L, Kassa H, Tischler ML, Xiao L (2004) Host-adapted Cryptosporidium spp. in Canada geese (Branta canadensis). Appl Environ Microbiol 70:4211–4215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This study was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), process number 99999.009537/2014-07.

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Correspondence to Mónica Santín.

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da Cunha, M.J.R., Cury, M.C. & Santín, M. Molecular identification of Enterocytozoon bieneusi, Cryptosporidium, and Giardia in Brazilian captive birds. Parasitol Res 116, 487–493 (2017). https://doi.org/10.1007/s00436-016-5309-6

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