Abstract
Cryptosporidium spp. are zoonotic intestinal parasites that infect fish, birds, reptiles and mammals. Cryptosporidium spp. are common cause of diarrhea. In this study, a total of 1032 fecal samples were collected from the rectums of sheep and goats. The samples were analyzed using nested polymerase chain reaction (nested PCR) based on the small subunit ribosomal RNA (SSU rRNA) gene of Cryptosporidium spp. The average infection rate of Cryptosporidium spp. was 2.23% (n = 23), and three Cryptosporidium species were identified, namely Cryptosporidium ubiquitum (8/23), Cryptosporidium andersoni (5/23) and Cryptosporidium xiaoi (10/23). Subtyping of C. ubiquitum and C. xiaoi was carried out by DNA sequence analysis of the 60-kDa glycoprotein (gp60) gene. Eight C. ubiquitum isolates were identified as zoonotic subtype XIIa. Nine C. xiaoi isolates were identified as subtypes XXIIIc (n = 1), XXIIIf (n = 3) and XXIIIg (n = 5). Subtype XXIIIg was first found in Chinese sheep. C. ubiquitum subtype XIIa was found in both sheep and goats, suggesting that sheep and goats are important sources of C. ubiquitum infections.
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Data availability
All of the data generated and analyzed during this study are included in this published manuscript. The nucleotide sequences of C. xiaoi for the gp60 gene obtained in this study have been deposited in GenBank, GenBank accession numbers: ON809515—ON809517.
References
Adamu H, Petros B, Zhang G, Kassa H, Amer S, Ye J, Feng Y, Xiao L (2014) Distribution and clinical manifestations of Cryptosporidium species and subtypes in HIV/AIDS patients in Ethiopia. PLoS Negl Trop Dis 8:e2831. https://doi.org/10.1371/journal.pntd.0002831
Alves M, Xiao L, Sulaiman I, Lal AA, Matos O, Antunes F (2003) Subgenotype analysis of Cryptosporidium isolates from humans, cattle, and zoo ruminants in Portugal. J Clin Microbiol 41:2744–2747. https://doi.org/10.1128/jcm.41.6.2744-2747.2003
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 34:142–143. https://doi.org/10.1016/j.eimc.2015.05.010
Dessì G, Tamponi C, Varcasia A, Sanna G, Pipia AP, Carta S, Salis F, Díaz P, Scala A (2020) Cryptosporidium infections in sheep farms from Italy. Parasitol Res 119:4211–4218. https://doi.org/10.1007/s00436-020-06947-2
Díaz P, Quílez J, Prieto A, Navarro E, Pérez-Creo A, Fernández G, Panadero R, López C, Díez-Baños P, Morrondo P (2015) Cryptosporidium species and subtype analysis in diarrhoeic pre-weaned lambs and goat kids from north-western Spain. Parasitol Res 114:4099–4105. https://doi.org/10.1007/s00436-015-4639-0
Fan Y, Huang X, Guo S, Yang F, Yang X, Guo Y, Feng Y, Xiao L, Li N (2021) Subtyping Cryptosporidium xiaoi, a common pathogen in sheep and goats. Pathogens 10:800. https://doi.org/10.3390/pathogens10070800
Fiuza VR, Cosendey RI, Frazão-Teixeira E, Santín M, Fayer R, de Oliveira FC (2011) Molecular characterization of Cryptosporidium in Brazilian sheep. Vet Parasitol 175:360–362. https://doi.org/10.1016/j.vetpar.2010.10.036
Gao H, Wang J, Kang X, Wang P, Wu X, Li Y (2021) Prevalence and risk factors of Cryptosporidium in sheep and goat of China. Chinese Journal of Veterinary Science 41:401–06. https://doi.org/10.16303/j.cnki.1005-4545.2021.02.33
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. https://doi.org/10.1016/j.ejop.2019.03.001
Jezkova J, Horcickova M, Hlaskova L, Sak B, Kvetonova D, Novak J, Hofmannova L, McEvoy J, Kvac M (2016) Cryptosporidium testudinis sp. n., Cryptosporidium ducismarci Traversa, 2010 and Cryptosporidium tortoise genotype III (Apicomplexa: Cryptosporidiidae) in tortoises, Folia Parasitol (Praha), 63.https://doi.org/10.14411/fp.2016.035
Kabir MHB, Ceylan O, Ceylan C, Shehata AA, Bando H, Essa MI, Xuan X, Sevinc F, Kato K (2020) Molecular detection of genotypes and subtypes of Cryptosporidium infection in diarrheic calves, lambs, and goat kids from Turkey. Parasitol Int 79:102163. https://doi.org/10.1016/j.parint.2020.102163
Koinari M, Lymbery AJ, Ryan UM (2014) Cryptosporidium species in sheep and goats from Papua New Guinea. Exp Parasitol 141:134–137. https://doi.org/10.1016/j.exppara.2014.03.021
Li N, Xiao L, Alderisio K, Elwin K, Cebelinski E, Chalmers R, Santin M, Fayer R, Kvac M, Ryan U, Sak B, Stanko M, Guo Y, Wang L, Zhang L, Cai J, Roellig D, Feng Y (2014) Subtyping Cryptosporidium ubiquitum, a zoonotic pathogen emerging in humans. Emerg Infect Dis 20:217–224. https://doi.org/10.3201/eid2002.121797
Li P, Cai J, Cai M, Wu W, Li C, Lei M, Xu H, Feng L, Ma J, Feng Y, Xiao L (2016) Distribution of Cryptosporidium species in Tibetan sheep and yaks in Qinghai. China, Vet Parasitol 215:58–62. https://doi.org/10.1016/j.vetpar.2015.11.009
Li W, Wang K, Tang L, Chen M, Li H, Kan Z, Gu Y (2019) Molecular characterization of Cryptosporidium species in sheep and goats in Anhui Province and neighboring provinces. Chinese J Schistosomiasis Control 31:474–78+85. https://doi.org/10.16250/j.32.1374.2018043
Majeed QAH, El-Azazy OME, Abdou NMI, Al-Aal ZA, El-Kabbany AI, Tahrani LMA, AlAzemi MS, Wang Y, Feng Y, Xiao L (2018) Epidemiological observations on cryptosporidiosis and molecular characterization of Cryptosporidium spp. in sheep and goats in Kuwait. Parasitol Res 117:1631–1636. https://doi.org/10.1007/s00436-018-5847-1
Maurya PS, Rakesh RL, Pradeep B, Kumar S, Kundu K, Garg R, Ram H, Kumar A, Banerjee PS (2013) Prevalence and risk factors associated with Cryptosporidium spp. infection in young domestic livestock in India. Trop Anim Health Prod 45:941–946. https://doi.org/10.1007/s11250-012-0311-1
Mi R, Wang X, Huang Y, Zhou P, Liu Y, Chen Y, Chen J, Zhu W, Chen Z (2014) Prevalence and molecular characterization of Cryptosporidium in goats across four provincial level areas in China. PLoS ONE 9:e111164. https://doi.org/10.1371/journal.pone.0111164
Mi R, Wang X, Huang Y, Mu G, Zhang Y, Jia H, Zhang X, Yang H, Wang X, Han X, Chen Z (2018) Sheep as a potential source of zoonotic cryptosporidiosis in China. Appl Environ Microbiol 84:e00868-18. https://doi.org/10.1128/aem.00868-18
Morgan-Ryan UM, Fall A, Ward LA, Hijjawi N, Sulaiman I, Fayer R, Thompson RC, Olson M, Lal A, Xiao L (2002) Cryptosporidium hominis n. sp. (Apicomplexa: Cryptosporidiidae) from Homo sapiens. J Eukaryot Microbiol 49:433–440. https://doi.org/10.1111/j.1550-7408.2002.tb00224.x
Pritchard GC, Marshall JA, Giles M, Chalmers RM, Marshall RN (2007) Cryptosporidium parvum infection in orphan lambs on a farm open to the public. Vet Rec 161:11–14. https://doi.org/10.1136/vr.161.1.11
Ryan UM, Feng Y, Fayer R, Xiao L (2021) Taxonomy and molecular epidemiology of Cryptosporidium and Giardia - a 50 year perspective (1971–2021). Int J Parasitol 51:1099–1119. https://doi.org/10.1016/j.ijpara.2021.08.007
Santín M (2013) Clinical and subclinical infections with Cryptosporidium in animals. N Z Vet J 61:1–10. https://doi.org/10.1080/00480169.2012.731681
Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM (2011) Foodborne illness acquired in the United States–major pathogens. Emerg Infect Dis 17:7–15. https://doi.org/10.3201/eid1701.p11101
Wang Y, Feng Y, Cui B, Jian F, Ning C, Wang R, Zhang L, Xiao L (2010) Cervine genotype is the major Cryptosporidium genotype in sheep in China. Parasitol Res 106:341–347. https://doi.org/10.1007/s00436-009-1664-x
Wang R, Li G, Cui B, Huang J, Cui Z, Zhang S, Dong H, Yue D, Zhang L, Ning C, Wang M (2014) Prevalence, molecular characterization and zoonotic potential of Cryptosporidium spp. in goats in Henan and Chongqing. China, Exp Parasitol 142:11–16. https://doi.org/10.1016/j.exppara.2014.04.001
Xiao L, Singh A, Limor J, Graczyk TK, Gradus S, Lal A (2001) Molecular characterization of Cryptosporidium oocysts in samples of raw surface water and wastewater. Appl Environ Microbiol 67:1097–1101. https://doi.org/10.1128/aem.67.3.1097-1101.2001
Xiao L, Fayer R, Ryan U, Upton SJ (2004) Cryptosporidium taxonomy: recent advances and implications for public health. Clin Microbiol Rev 17:72–97. https://doi.org/10.1128/cmr.17.1.72-97.2004
Yang, J (2018) 'Investigation on Cryptosporidium infections of cattle, goats and sheep in part areas of Ningxia', Northwest A&F University
Ye J, Xiao L, Wang Y, Wang L, Amer S, Roellig DM, Guo Y, Feng Y (2013) Periparturient transmission of Cryptosporidium xiaoi from ewes to lambs. Vet Parasitol 197:627–633. https://doi.org/10.1016/j.vetpar.2013.07.021
Zahedi A, Bolland SJ, Oskam CL, Ryan U (2021) Cryptosporidium abrahamseni n sp (Apicomplexa: Cryptosporidiiae) from red-eye tetra (Moenkhausia sanctaefilomenae). Exp Parasitol 223:108089. https://doi.org/10.1016/j.exppara.2021.108089
Zhang Z, Chen D, Zou Y, Hou J, Sun L, Li Z, Yang J, Zou F, Zhu X (2020) First report of Cryptosporidium spp. infection and risk factors in black-boned goats and black-boned sheep in China. Parasitol Res 119:2813–2819. https://doi.org/10.1007/s00436-020-06781-6
Zhong Z, Tu R, Ou H, Yan G, Dan J, Xiao Q, Wang Y, Cao S, Shen L, Deng J, Zuo Z, Ma X, Zhou Z, Liu H, Yu S, Ren Z, Hu Y, Peng G (2018) Occurrence and genetic characterization of Giardia duodenalis and Cryptosporidium spp from adult goats in Sichuan Province. China. PLoS One 13:e0199325. https://doi.org/10.1371/journal.pone.0199325
Zhu W, Mi R, Wang J, Wang C, Huang Y, Zhang H, Jia H, Zhang X, Han X, Chen Z (2018) Detection and actin sequence analysis of Cryptosporidium infection in sheep and goats in Tengzhou Shandong Province. Chinese J Animal Infect Dis 26:69–75. https://doi.org/10.1128/AEM.00868-18
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We thank Let Pub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.
Funding
This research was funded by the National Natural Science Foundation of China (U1904203), and the Leading talents of the Thousand Talents Program of Central China (19CZ0122). The sponsors played no role in study design, in the collection, analysis, or interpretation of the data, in writing the report, or in the decision to submit the article for publication.
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Longxian Zhang contributed to the conception and design of the experiments. Jiashu Lang, Han Han and Heping Dong performed the experiments. Ziyang Qin and Huikai Qin helped in interpretation of data. Yin Fu and Junchen Zhang collected fecal samples. Junqiang Li, Xiaoying Li, Guanghui Zhao and Jinfeng Zhao interpreted the results and drafted the manuscript. All of the authors read and approved the final version of the manuscript.
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This study was conducted in accordance with the Chinese Laboratory Animal Administration Act of 1988. The research protocol was reviewed and approved by the Research Ethics Committee of Henan Agricultural University. Permission was obtained from farm owners before the collection of animal fecal samples.
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Key findings
• The infection rate of Cryptosporidium spp. was 2.23% in sheep and goats.
• Cryptosporidium ubiquitum, Cryptosporidium andersoni and Cryptosporidium xiaoi were identified in sheep and goats.
• Cryptosporidium ubiquitum subtype XIIa, and C. xiaoi subtypes XXIIIc, XXIIIf and XXIIIg were found in this study.
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Lang, J., Han, H., Dong, H. et al. Molecular characterization and prevalence of Cryptosporidium spp. in sheep and goats in western Inner Mongolia, China. Parasitol Res 122, 537–545 (2023). https://doi.org/10.1007/s00436-022-07756-5
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DOI: https://doi.org/10.1007/s00436-022-07756-5