Abstract
Free-range chickens might mediate the spread of Cryptosporidium oocysts to humans and other animals. Few studies have evaluated the prevalence of Cryptosporidium species in domestic free-range poultry in China. Here, we characterized the prevalence and distribution of species and genotypes of Cryptosporidium in domestic free-range chickens, ducks, and geese in Anhui Province, China. A total of 1910 fresh fecal samples from three poultry species were examined from 18 free-range poultry farms by nested PCR and analysis of the Cryptosporidium SSU rRNA gene. The overall prevalence of Cryptosporidium species was 2.9% (55/1910), with infection rates of 1.3% (11/829) in chickens, 7.3% (36/487) in ducks, and 1.4% (8/594) in geese. C. baileyi (0.6%), C. meleagridis (0.2%), C. galli (0.2%), and C. xiaoi-like genotype (0.2%) were identified in chickens, and only C. baileyi was identified in ducks and geese, with infection rates of 7.4% and 1.3%, respectively. C. baileyi was the most prevalent species. Sequencing of the GP60 gene revealed that the C. meleagridis isolates belonged to the IIIbA26G1R1b subtype. This is the first study to document C. galli and C. xiaoi-like genotype in domestic free-range chickens in China. These findings expand the range of avian hosts known for Cryptosporidium and highlight the need for additional studies to characterize the diversity of Cryptosporidium in avian species.
Similar content being viewed by others
References
Baroudi D, Khelef D, Goucem R, Adjou KT, Adamu H, Zhang H, Xiao L (2013) Common occurrence of zoonotic pathogen Cryptosporidium meleagridis in broiler chickens and turkeys in Algeria. Vet Parasitol 196(3–4):334–340
Cao S, Xu M, Jiang Y, Liu H, Yuan Z, Sun L, Cao J, Shen Y (2020) Prevalence and genetic characterization of Cryptosporidium, Giardia and Enterocytozoon in chickens from Ezhou, Hubei. China Front Vet Sci 7:30
Chen H (2018) Current situation, problems and transformation suggestions of poultry industry in Anhui Province. Guide Chinese Poult 35(3):25–27
de Graaf DC, Vanopdenbosch E, Ortega-Mora LM, Abbassi H, Peeters JE (1999) A review of the importance of cryptosporidiosis in farm animals. Int J Parasitol 29(8):1269–1287
Dong H, Cheng R, Li X, Li J, Chen Y, Ban C, Zhang X, Liu F, Zhang L (2021) Molecular identification of Cryptosporidium spp., Enterocytozoon bieneusi, and Giardia duodenalis in captive pet birds in Henan Province, Central China. J Eukaryot Microbiol 14: e12839.
Eladl AH, Hamed HR, Khalil MR (2014) Consequence of Cryptosporidiosis on the immune response of vaccinated broiler chickens against Newcastle disease and/or avian influenza. Vet Res Commun 38(3):237–347
Elkarim Laatamna A, Holubova N, Sak B, Kvac M (2017) Cryptosporidium meleagridis and C. baileyi (Apicomplexa) in domestic and wild birds in Algeria. Folia Parasitol (Praha) 64: 018.
Elwin K, Hadfield SJ, Robinson G, Chalmers RM (2012) The epidemiology of sporadic human infections with unusual cryptosporidia detected during routine typing in England and Wales, 2000–2008. Epidemiol Infect 140(4):673–678
Ewald MPC, Martins FDC, Caldart ET, Vieira FEG, Yamamura MH, Sasse JP, Barros LD, Freire RL, Navarro IT, Garcia JL (2017) The first study of molecular prevalence and species characterization of Cryptosporidium in free-range chicken (Gallus gallus domesticus) from Brazil. Rev Bras Parasitol Vet 26(4):472–478
Feng Y, Xiao L (2017) Molecular epidemiology of cryptosporidiosis in China. Front Microbiol 8:1701
Feng Y (2018) Genetic diversity and population structure of Cryptosporidium. Trends Parasitol 34:997–1011
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.
Helmy YA, Krücken J, Abdelwhab EM, von Samson-Himmelstjerna G, Hafez HM (2017) Molecular diagnosis and characterization of Cryptosporidium spp. in turkeys and chickens in Germany reveals evidence for previously undetected parasite species. PLoS One 12(6):e0177150.
Hijjawi N, Mukbel R, Yang R, Ryan U (2016) Genetic characterization of Cryptosporidium in animal and human isolates from Jordan. Vet Parasitol 228:116–120
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(6):2243–2251.
Holubová N, Zikmundová V, Limpouchová Z, Sak B, Konečný R, Hlásková L, Rajský D, Kopacz Z, McEvoy J, Kváč M (2019) Cryptosporidium proventriculi sp. n. (Apicomplexa: Cryptosporidiidae) in Psittaciformes birds. Eur J Protistol 69:70–87
Iijima Y, Itoh N, Phrompraphai T, Ito Y, Kimura Y, Kameshima S (2018) Molecular prevalence of Cryptosporidium spp. among companion birds kept in pet shops in Japan. Korean J Parasitol 56(3):281–285.
Innes EA, Chalmers RM, Wells B, Pawlowic MC (2020) A one health approach to tackle cryptosporidiosis. Trends Parasitol 36(3):290–303
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(1):452–458
Kassouha M (2014) First detection of Cryptosporidium spp. in broiler chickens in Syria. Basrah J Vet Res 11:253–259
Liao SD, Lu FL, Li PY (1996) Identification of Cryptosporidium spp. and mathematical analysis of their infection status in chickens in Anhui. J Biomath, 11(4):95–101.
Liao C, Wang T, Koehler AV, Fan Y, Hu M, Gasser RB (2018) Molecular investigation of Cryptosporidium in farmed chickens in Hubei Province, China, identifies ‘zoonotic’ subtypes of C. meleagridis. Parasit Vectors 11(1):484.
Li J, Lin X, Zhang L, Qi N, Liao S, Lv M, Wu C, Sun M (2015) Molecular characterization of Cryptosporidium spp. in domestic pigeons (Columba livia domestica) in Guangdong Province, southern China. Parasitol Res 114:2237–2241
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 115(7):2905–2911
Liu A, Gong B, Liu X, Shen Y, Wu Y, Zhang W, Cao J (2020) A retrospective epidemiological analysis of human Cryptosporidium infection in China during the past three decades (1987–2018). PLoS Negl Trop Dis 14(3): e0008146.
Liu X, Zhu H, Meng W, Dong H, Han Q, An Z, Qi M, Ge Y, Wang R (2019) Occurrence of a Cryptosporidium xiaoi-like genotype in peafowl (Pavo cristatus) in China. Parasitol Res 118(12):3555–3559
Morgan UM, Monis PT, Xiao L, Limor J, Sulaiman I, Raidal S, O’Donoghue P, Gasser R, Murray A, Fayer R, Blagburn BL, Lal AA, Thompson RC (2001) Molecular and phylogenetic characterisation of Cryptosporidium from birds. Int J Parasitol 31(3):289–296
Nakamura AA, Meireles MV (2015) Cryptosporidium infections in birds–a review. Rev Bras Parasitol Vet 24(3):253–267
Pavlasek I (1991) Use of glycerine in oocyst detection of Cryptosporidium parvum and C. baileyi in the feces of mammals and birds. Vet Med (praha) 36:255–256
Pavlasek I (2001) Findings of Cryptosporidia in the stomach of chickens and of exotic and wild birds. Veterinarstvi 51:103–108
Qi M, Wang R, Ning C, Li X, Zhang L, Jian F, Sun Y, Xiao L (2011) Cryptosporidium spp. in pet birds: genetic diversity and potential public health significance. Exp Parasitol 128(4):336–340.
Richter D, Wiegand-Tripp G, Burkhardt E, Kaleta EF (1994) Natural infections by Cryptosporidium sp. in farm-raised ducks and geese. Avian Pathol 23:277–286
Ryan U (2010) Cryptosporidium in birds, fish and amphibians. ExpParasitol 124:113–120
Santana BN, Kurahara B, Nakamura AA, da Silva CV, Ferrari ED, da Silva GS, Nagata WB, Meireles MV (2018) Detection and characterization of Cryptosporidium species and genotypes in three chicken production systems in Brazil using different molecular diagnosis protocols. Prev Vet Med 151:73–78
Shahbazi P, Aligolzadeh A, Khordadmehr M, Hashemzadeh Farhang H, Katiraee F (2020) Molecular study and genotyping of Cryptosporidium baileyi and Cryptosporidium parvum from free-range and commercial broiler chickens in Guilan province, Iran. Comp Immunol Microbiol Infect Dis 69:101411.
Soltane R, Guyot K, Dei-Cas E, Ayadi A (2007) Prevalence of Cryptosporidium spp. (Eucoccidiorida: Cryptosporiidae) in seven species of farm animals in Tunisia. Parasite 14:335.
Stensvold CR, Beser J, Axén C, Lebbad M (2014) High applicability of a novel method for gp60-based subtyping of Cryptosporidium meleagridis. J Clin Microbiol 52:2311–2319
Thamsborg SM, Roepstorff A, Larsen MM (1999) Integrated and biological control of parasites in organic and conventional production systems. Vet Parasitol 84(3–4):169–186
Wang K, Gazizova A, Wang Y, Zhang K, Zhang Y, Chang Y, Cui Y, Zhang Y, Zhang S, Zhang L (2019) First detection of Cryptosporidium spp. in migratory whooper swans (Cygnus cygnus) in China. Microorganisms 8(1):6.
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
Wang R, Jian F, Sun Y, Hu Q, Zhu J, Wang F, Ning C, Zhang L, Xiao L (2010) Large-scale survey of Cryptosporidium spp. in chickens and Pekin ducks (Anas platyrhynchos) in Henan, China: prevalence and molecular characterization. Avian Pathol 39(6):447–451.
Wang R, Wang F, Zhao J, Qi M, Ning C, Zhang L, Xiao L (2012) Cryptosporidium spp. in quails (Coturnix coturnix japonica) in Henan, China: molecular characterization and public health significance. Vet Parasitol 187(3–4):534–537.
Wang T, Fan Y, Koehler AV, Ma G, Li T, Hu M, Gasser RB (2017) First survey of Cryptosporidium, Giardia and Enterocytozoon in diarrhoeic children from Wuhan, China. Infect Genet Evol 51:127–131
Wei JZ, Li PY, He CS, Zhu QY, Xie JG (2003) Investigation on infectious condition of chicken Cryptosporidium in a private farm of Anhui Province. Chin J Vet Sci 23(5):472–473
Xiao LH, Escalante L, Yang CF, Sulaiman I, Escalante AA, Montali RJ, Fayer R, Lal AA (1999) Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Appl Environ Microbiol 65:1578–1583
Yang W, Chen P, Villegas EN, Landy RB, Kanetsky C, Cama V, Dearen T, Schultz CL, Orndorff KG, Prelewicz GJ, Brown MH, Young KR, Xiao L (2008) Cryptosporidium source tracking in the Potomac River watershed. Appl Environ Microbiol 74:6495–6504
Yang Z, Zhao W, Wang J, Ren G, Zhang W, Liu A (2018) Molecular detection and genetic characterizations of Cryptosporidium spp. in farmed foxes, minks, and raccoon dogs in northeastern China. Parasitol Res 117(1):169–175.
Zhang W, Wang R, Yang F, Zhang L, Cao J, Zhang X, Ling H, Liu A, Shen Y (2013) Distribution and genetic characterizations of Cryptosporidium spp. in pre-weaned dairy calves in Northeastern China’s Heilongjiang Province. PLoS One 8(1): e54857.
Zhao W, Zhou HH, Ma TM, Cao J, Lu G, Shen YJ (2019) PCR-based detection of Cryptosporidium spp. and Enterocytozoon bieneusi in farm-raised and free-ranging geese (Anser anser f. domestica) from Hainan Province of China: natural infection rate and the species or genotype distribution. Front Cell Infect Microbiol 9:416.
Zhou L, Kassa H, Tischler ML, Xiao L (2004) Host-adapted Cryptosporidium spp. in Canada geese (Branta canadensis). Appl Environ Microbiol 70(7):4211–4215.
Acknowledgements
We thank the staff on the farms for their assistance with this study. We thank Liwen Bianji, Edanz Editing China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.
Funding
This work was supported by the Anhui Provincial Natural Science Foundation (1808085MC84, and 1908085QC116), and the school-level talent project of Anhui Science and Technology University (dkwd201702).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval
This study was approved by the Animal Care and Welfare Committee of Anhui Science and Technology University, Fengyang, China. All the fecal samples from the domestic chickens, ducks, and geese were collected with the permission of the cattle owners.
Competing interests
The authors declare no competing interests.
Additional information
Section Editor: Yaoyu Feng
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Gong, Z., Kan, Zz., Huang, Jm. et al. Molecular prevalence and characterization of Cryptosporidium in domestic free-range poultry in Anhui Province, China. Parasitol Res 120, 3519–3527 (2021). https://doi.org/10.1007/s00436-021-07191-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-021-07191-y