Abstract
This study screened 151 pet-derived fecal specimens randomly collected from four commercial markets in northeast China for the presence of Cryptosporidium by genus-specific nested PCRs of the small subunit rRNA gene. Of these, 14 specimens (9.3 %) from nine species of birds, two types of rodents, and a hedgehog were positive for Cryptosporidium. Sequence analysis on the PCR-positive isolates facilitated identification of three Cryptosporidium species (C. baileyi, C. galli, and C. ubiquitum) and two Cryptosporidium genotypes (ferret genotype and avian genotype V). The study birds were affected predominantly with bird-specific C. baileyi (Atlantic canary, budgerigar, crested myna, rock dove, and silky fowl), C. galli (Chinese hwamei), and Cryptosporidium avian genotype V (Fischer’s lovebird and rosy-faced lovebird). Cryptosporidium ferret genotype previously considered rodent-adapted was identified in three specimens from budgerigar, chipmunk, and red squirrel. Two specimens collected from common hill myna and hedgehog were positive for C. ubiquitum. The species of birds that can be colonized by Cryptosporidium were extended. Moreover, the data expanded the host range of Cryptosporidium ferret genotype and C. ubiquitum, especially the birds. The carriage of zoonotic C. ubiquitum in small caged pets is of public health importance.
References
Abe N, Iseki M (2003) Identification of genotypes of Cryptosporidium parvum isolates from ferrets in Japan. Parasitol Res 89(5):422–424
Abe N, Iseki M (2004) Identification of Cryptosporidium isolates from cockatiels by direct sequencing of the PCR-amplified small subunit ribosomal RNA gene. Parasitol Res 92(6):523–526
Abe N, Makino I (2010) Multilocus genotypic analysis of Cryptosporidium isolates from cockatiels, Japan. Parasitol Res 106(6):1491–1497
Abe N, Matsubara K (2015) Molecular identification of Cryptosporidium isolates from exotic pet animals in Japan. Vet Parasitol 209(3-4):254–257
Abu Samra N, Jori F, Xiao L, Rikhotso O, Thompson PN (2013) Molecular characterization of Cryptosporidium species at the wildlife/livestock interface of the Kruger National Park, South Africa. Comp Immunol Microbiol Infect Dis 36(3):295–302
Azami M, Moghaddam DD, Salehi R, Salehi M (2007) The identification of Cryptosporidium species (protozoa) in Ifsahan, Iran by PCR-RFLP analysis of the 18S rRNA gene. Mol Biol (Mosk) 41(5):934–939
Bjorkman C, Lindstrom L, Oweson C, Ahola H, Troell K, Axen C (2015) Cryptosporidium infections in suckler herd beef calves. Parasitology 142(8):1108–1114
Blanco MA, de Lucio A, Fuentes I, Carmena D (2016) Cryptosporidium ubiquitum in Venezuela: first report in a paediatric patient with acute diarrhoea. Enferm Infecc Microbiol Clin 34(2):142–143
Connelly L, Craig BH, Jones B, Alexander CL (2013) Genetic diversity of Cryptosporidium spp. within a remote population of Soay Sheep on St. Kilda Islands, Scotland. Appl Environ Microbiol 79(7):2240–2246
Curtiss JB, Leone AM, Wellehan JF Jr, Emerson JA, Howerth EW, Farina LL (2015) Renal and cloacal cryptosporidiosis (Cryptosporidium avian genotype V) in a major mitchell’s cockatoo (Lophochroa leadbeateri). J Zoo Wildl Med 46(4):934–937
Ditrich O, Palkovic L, Sterba J, Prokopic J, Loudova J, Giboda M (1991) The first finding of Cryptosporidium baileyi in man. Parasitol Res 77(1):44–47
Dyachenko V, Kuhnert Y, Schmaeschke R, Etzold M, Pantchev N, Daugschies A (2010) Occurrence and molecular characterization of Cryptosporidium spp. genotypes in European hedgehogs (Erinaceus europaeus L.) in Germany. Parasitology 137(2):205–216
Enemark HL et al (2002) Molecular characterization of Danish Cryptosporidium parvum isolates. Parasitology 125(pt 4):331–341
Fayer R et al (2002) Temporal variability of Cryptosporidium in the Chesapeake Bay. Parasitol Res 88(11):998–1003
Fayer R, Santin M, Macarisin D (2010) Cryptosporidium ubiquitum n. sp. in animals and humans. Vet Parasitol 172(1-2):23–32
Feng Y (2010) Cryptosporidium in wild placental mammals. Exp Parasitol 124(1):128–137
Feng Y et al (2011) Occurrence, source, and human infection potential of Cryptosporidium and Giardia spp. in source and tap water in shanghai, China. Appl Environ Microbiol 77(11):3609–3616
Feng Y et al (2012) Common occurrence of a unique Cryptosporidium ryanae variant in zebu cattle and water buffaloes in the buffer zone of the Chitwan National Park, Nepal. Vet Parasitol 185(2-4):309–314
Galvan AL et al (2014) A year-long study of Cryptosporidium species and subtypes in recreational, drinking and wastewater from the central area of Spain. Sci Total Environ 468–469:368–375
Gomez-Couso H et al (2012) Presence and molecular characterisation of Giardia and Cryptosporidium in alpacas (Vicugna pacos) from Peru. Vet Parasitol 187(3-4):414–420
Hajdusek O, Ditrich O, Slapeta J (2004) Molecular identification of Cryptosporidium spp. in animal and human hosts from the Czech Republic. Vet Parasitol 122(3):183–192
Hamidinejat H, Jalali MH, Jafari RA, Nourmohammadi K (2014) Molecular determination and genotyping of Cryptosporidium spp. in fecal and respiratory samples of industrial poultry in Iran. Asian Pac J Trop Med 7(7):517–520
Kimura A, Suzuki Y, Matsui T (2004) Identification of the Cryptosporidium isolate from chickens in Japan by sequence analyses. J Vet Med Sci 66(7):879–881
Krawczyk AI et al (2015) Presence of zoonotic agents in engorged ticks and hedgehog faeces from Erinaceus europaeus in (sub) urban areas. Parasit Vectors 8:210
Li J et al (2015a) Molecular characterization of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi in captive wildlife at Zhengzhou zoo, China. J Eukaryot Microbiol 62(6):833–839
Li W et al (2015b) Prevalence and genetic characteristics of Cryptosporidium, Enterocytozoon bieneusi and Giardia duodenalis in cats and dogs in Heilongjiang province, China. Vet Parasitol 208(3-4):125–134
Lv C et al (2009) Cryptosporidium spp. in wild, laboratory, and pet rodents in China: prevalence and molecular characterization. Appl Environ Microbiol 75(24):7692–9699
Molloy SF et al (2010) Identification of a high diversity of Cryptosporidium species genotypes and subtypes in a pediatric population in Nigeria. Am J Trop Med Hyg 82(4):608–613
Murakoshi F et al (2013) Detection and genotyping of Cryptosporidium spp. in large Japanese field mice, Apodemus speciosus. Vet Parasitol 196(1-2):184–188
Nakamura AA, Meireles MV (2015) Cryptosporidium infections in birds—a review. Rev Bras Parasitol Vet 24(3):253–267
Nakamura AA, Simoes 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(1-2):47–51
Ng J, Pavlasek I, Ryan U (2006) Identification of novel Cryptosporidium genotypes from avian hosts. Appl Environ Microbiol 72(12):7548–7553
Nichols RA, Connelly L, Sullivan CB, Smith HV (2010) Identification of Cryptosporidium species and genotypes in Scottish raw and drinking waters during a one-year monitoring period. Appl Environ Microbiol 76(17):5977–5986
Nolan MJ, Jex AR, Koehler AV, Haydon SR, Stevens MA, Gasser RB (2013) Molecular-based investigation of Cryptosporidium and Giardia from animals in water catchments in southeastern Australia. Water Res 47(5):1726–1740
Paz e Silva FM, Lopes RS, Bresciani KD, Amarante AF, Araujo JP Jr (2014) High occurrence of Cryptosporidium ubiquitum and Giardia duodenalis genotype E in sheep from Brazil. Acta Parasitol 59(1):193–196
Plutzer J, Karanis P (2009) Genetic polymorphism in Cryptosporidium species: an update. Vet Parasitol 165(3-4):187–199
Qi M et al (2011) Cryptosporidium spp. in pet birds: genetic diversity and potential public health significance. Exp Parasitol 128(4):336–340
Qi M et al (2015) Zoonotic Cryptosporidium spp. and Enterocytozoon bieneusi in pet chinchillas (Chinchilla lanigera) in China. Parasitol Int 64(5):339–341
Ruecker NJ et al (2012) Molecular and phylogenetic approaches for assessing sources of Cryptosporidium contamination in water. Water Res 46(16):5135–5150
Ryan U (2010) Cryptosporidium in birds, fish and amphibians. Exp Parasitol 124(1):113–120
Ryan U, Fayer R, Xiao L (2014) Cryptosporidium species in humans and animals: current understanding and research needs. Parasitology 141(13):1667–1685
Sangster L et al (2016) Detection and molecular characterisation of Cryptosporidium parvum in British European hedgehogs (Erinaceus europaeus). Vet Parasitol 217:39–44
Slapeta J (2013) Cryptosporidiosis and Cryptosporidium species in animals and humans: a thirty colour rainbow? Int J Parasitol 43(12-13):957–970
Stenger BL et al (2015) North American tree squirrels and ground squirrels with overlapping ranges host different Cryptosporidium species and genotypes. Infect Genet Evol 36:287–293
Xiao L (2010) Molecular epidemiology of cryptosporidiosis: an update. Exp Parasitol 124(1):80–89
Xiao L, Fayer R (2008) Molecular characterisation of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. Int J Parasitol 38(11):1239–1255
Zhang XX, Zhang NZ, Zhao GH, Zhao Q, Zhu XQ (2015) Prevalence and genotyping of Cryptosporidium infection in pet parrots in north China. Biomed Res Int 2015:549798
Acknowledgments
We gratefully acknowledge the financial support from the Young Talents’ Project of Northeast Agricultural University (no. 14QC19) and the University Nursing Program for Young Scholars with Creative Talents in Heilongjiang Province (no. UNPYSCT-2015008).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Li, Q., Li, L., Tao, W. et al. Molecular investigation of Cryptosporidium in small caged pets in northeast China: host specificity and zoonotic implications. Parasitol Res 115, 2905–2911 (2016). https://doi.org/10.1007/s00436-016-5076-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-016-5076-4