Abstract
Severe diarrhea was reported in goat kids in Chungcheongbuk-do, Korea, from 2021 to 2023, and Cryptosporidium infection was suspected. To confirm the cause of this outbreak, fecal samples were collected from goat farms where diarrhea had been reported and analyzed for Cryptosporidium infection using a molecular assay. A total of 65 fecal samples, including 37 from goats with diarrhea and 28 from goats without diarrhea, were collected from six goat farms. Forty-eight of the goats were kids (<2 months) and 17 were adults (>1 year). Cryptosporidium was identified in 53.8% (35/65) of total samples. Overall, 86.5% (32/37) of the diarrheic fecal samples tested positive; however, Cryptosporidium was not detected in any fecal sample from non-diarrheic adult goats. Therefore, cryptosporidiosis was significantly associated with diarrhea in goat kids, and adult goats were not responsible for transmission of Cryptosporidium to them. Phylogenetic analysis and molecular characterization revealed two Cryptosporidium species, namely, C. parvum (n = 28) and C. xiaoi (n = 7). In the C. parvum-positive samples, gp60 gene analysis revealed three zoonotic subtypes—IIaA18G3R1, IIdA15G1, and IIdA16G1. To the best of our knowledge, this study is the first to identify C. parvum IIaA18G3R1 and IIdA16G1 in goats, as well as the first to identify C. xiaoi in goats in Korea. These results suggest that goat kids play an important role as reservoir hosts for different Cryptosporidium species and that continuous monitoring with biosecurity measures is necessary to control cryptosporidiosis outbreaks.
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References
Baroudi D, Hakem A, Adamu H, Amer S, Khelef D, Adjou K, Dahmani H, Chen X, Roellig D, Feng Y (2018) Zoonotic Cryptosporidium species and subtypes in lambs and goat kids in Algeria. Parasit Vectors 11:1–8
Cho E, Yang J, Lee E, Kim S, Cha S, Kim S, Lee M, Han S, Park Y (2013) A waterborne outbreak and detection of Cryptosporidium oocysts in drinking water of an older high-rise apartment complex in Seoul. Korean J Parasitol 51:461–466
Clark DP (1999) New insights into human cryptosporidiosis. Clin Microbiol Rev 12:554–563
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 29:1269–1287
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
Geurden T, Thomas P, Casaert S, Vercruysse J, Claerebout E (2008) Prevalence and molecular characterisation of Cryptosporidium and Giardia in lambs and goat kids in Belgium. Vet Parasitol 155:142–145
Giadinis ND, Papadopoulos E, Lafi SQ, Panousis NK, Papazahariadou M, Karatzias H (2008) Efficacy of halofuginone lactate for the treatment and prevention of cryptosporidiosis in goat kids: an extensive field trial. Small Ruminant Research 76:195–200
Insulander M, Silverlås C, Lebbad M, Karlsson L, Mattsson JG, Svenungsson B (2013) Molecular epidemiology and clinical manifestations of human cryptosporidiosis in Sweden. Epidemiol Infect 141:1009–1020
Ipek DS (2017) Prevalence and molecular characterisation of Cryptosporidium spp. in diarrhoeic pre-weaned goat kids reared under traditional farming system in Diyarbakir, Southeastern Anatolia City, Turkey. Rev Med Vet 168:229–234
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
Karanis P, Plutzer J, Halim NA, Igori K, Nagasawa H, Ongerth J, Liqing M (2007) Molecular characterization of Cryptosporidium from animal sources in Qinghai province of China. Parasitol Res 101:1575–1580
Kaupke A, Michalski MM, Rzeżutka A (2017) Diversity of Cryptosporidium species occurring in sheep and goat breeds reared in Poland. Parasitol Res 116:871–879
Kim J, Lee K, Roh SG, Kim H, Kim JW, So B, Choi E (2022) Clinical cases of zoonotic Cryptosporidium parvum (subtype IIdA15G1) infections in Korean goats. Vet Med 67:156–162
Koinari M, Lymbery AJ, Ryan UM (2014) Cryptosporidium species in sheep and goats from Papua New Guinea. Exp Parasitol 141:134–137
Lange H, Johansen ØH, Vold L, Robertson LJ, Anthonisen IL, Nygard K (2014) Second outbreak of infection with a rare Cryptosporidium parvum genotype in schoolchildren associated with contact with lambs/goat kids at a holiday farm in Norway. Epidemiol Infect 142:2105–2113
Lee S, VanBik D, Kim H, Lee Y, Kim JW, Chae M, Oh S, Goo Y, Kwon O, Kwak D (2016) Multilocus typing of Cryptosporidium spp. in young calves with diarrhea in Korea. Vet Parasitol 229:81–89
Lin Q, Wang X, Chen J, Ding L, Zhao G (2015) Cryptosporidium suis infection in post-weaned and adult pigs in Shaanxi province, northwestern China. Korean J Parasitol 53:113
Ma D, Lee M, Hong S, Cho S, Lee S (2019) Molecular prevalence and genotypes of Cryptosporidium parvum and Giardia duodenalis in patients with acute diarrhea in Korea, 2013–2016. Korean J Parasitol 57:531
Majeed QA, El-Azazy OM, Abdou NM, Al-Aal ZA, El-Kabbany AI, Tahrani LM, 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
Mason RW, Hartley WJ, Tilt L (1981) Intestinal cryptosporidiosis in a kid goat. Aust Vet J 57:386–388
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
Moon S, Kwak W, Lee S, Kim W, Oh J, Youn S (2013) Epidemiological characteristics of the first water-borne outbreak of cryptosporidiosis in Seoul, Korea. J Korean Med Sci 28:983–989
Nazemalhosseini-Mojarad E, Haghighi A, Taghipour N, Keshavarz A, Mohebi SR, Zali MR, Xiao L (2011) Subtype analysis of Cryptosporidium parvum and Cryptosporidium hominis isolates from humans and cattle in Iran. Vet Parasitol 179:250–252
Papanikolopoulou V, Baroudi D, Guo Y, Wang Y, Papadopoulos E, Lafi SQ, Abd El-Tawab MM, Diakou A, Giadinis ND, Feng Y (2018) Genotypes and subtypes of Cryptosporidium spp. in diarrheic lambs and goat kids in northern Greece. Parasitol Int 67:472–475
Park J, Guk S, Han E, Shin E, Kim J, Chai J (2006) Genotype analysis of Cryptosporidium spp. prevalent in a rural village in Hwasun-gun, Republic of Korea. Korean J Parasitol 44:27
Quílez J, Torres E, Chalmers RM, Hadfield SJ, Del Cacho E, Sánchez-Acedo C (2008) Cryptosporidium genotypes and subtypes in lambs and goat kids in Spain. Appl Environ Microbiol 74:6026–6031
Rhee JK, Seu YS, Park BK (1991) Isolation and identification of Cryptosporidium from various animals in Korea. III. Identification of Cryptosporidium baileyi from Korean chicken. Korean J Parasitol 29:315–324
Rieux A, Paraud C, Pors I, Chartier C (2013) Molecular characterization of Cryptosporidium spp. in pre-weaned kids in a dairy goat farm in western France. Vet Parasitol 192:268–272
Santín M (2013) Clinical and subclinical infections with Cryptosporidium in animals. N Z Vet J 61:1–10
Sayers GM, Dillon MC, Connolly E, Thornton L, Hyland E, Loughman E, O’Mahony MA, Butler KM (1996) Cryptosporidiosis in children who visited an open farm. Commun Dis Rep CDR Rev 6:140
Sevinç F, ŞİMŞEK A, Uslu U (2005) Massive Cryptosporidium parvum infection associated with an outbreak of diarrhoea in neonatal goat kids. Turk J Vet Anim Sci 29:1317–1320
Song J, Kim C, Chang S, Abdelkader TS, Han J, Kim T, Oh H, Lee JM, Kim D, Kim J (2015) Detection and molecular characterization of Cryptosporidium spp. from wild rodents and insectivores in South Korea. Korean J Parasitol 53:737
Sulaiman IM, Hira PR, Zhou L, Al-Ali FM, Al-Shelahi FA, Shweiki HM, Iqbal J, Khalid N, Xiao L (2005) Unique endemicity of cryptosporidiosis in children in Kuwait. J Clin Microbiol 43:2805–2809
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027
Taylan-Ozkan A, Yasa-Duru S, Usluca S, Lysen C, Ye J, Roellig DM, Feng Y, Xiao L (2016) Cryptosporidium species and Cryptosporidium parvum subtypes in dairy calves and goat kids reared under traditional farming systems in Turkey. Exp Parasitol 170:16–20
Thamsborg SM, Jørgensen RJ, Henriksen SA (1990) Cryptosporidiosis in kids of dairy goats. Vet Rec 127:627–628
Tzanidakis N, Sotiraki S, Claerebout E, Ehsan A, Voutzourakis N, Kostopoulou D, Stijn C, Vercruysse J, Geurden T (2014) Occurrence and molecular characterization of Giardia duodenalis and Cryptosporidium spp. in sheep and goats reared under dairy husbandry systems in Greece. Parasite 21:45
Utaaker KS, Chaudhary S, Kifleyohannes T, Robertson LJ (2021) Global goat! Is the expanding goat population an important reservoir of Cryptosporidium? Front Vet Sci 8:648500
Vieira LS, Silva M, Tolentino A, Lima JD, Silva AC (1997) Outbreak of cryptosporidiosis in dairy goats in Brazil. Vet Rec 140:427–428
Acknowledgements
The authors would like to express their sincere appreciation to Mr. Suk-Geun Mo for his help with goat fecal sampling.
Funding
This study was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. 2021R1F1A1061795); the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry, and Fisheries (IPET) through the Agriculture, Food, and Rural Affairs Convergence Technologies Program for Educating Creative Global Leader, funded by the Ministry of Agriculture, Food, and Rural Affairs (MAFRA) (grant number: 320005-4); and “Regional Innovation Strategy (RIS)” through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (MOE) (2021RIS-001).
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AYK, WKL, and SHL conceptualized the study. AYK, BA, SL, SK, and SHL performed sampling and molecular experiments. AYK, KDM, SML, DK, and SHL analyzed the data. AYK, DK, and SHL contributed to the manuscript. SHL supervised the study. All authors read and approved the final manuscript.
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The requirement for ethical review and approval was waived as this study focused on animal fecal samples. The study was performed for the purpose of diagnosis in goats. Animal contact during the examination was minimal, consistent with routine physical examination procedures, and was conducted with appropriate handling under the supervision of licensed veterinarians. None of the treatments were harmful or detrimental to animal welfare.
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Kim, AY., Alkathiri, B., Lee, S. et al. Outbreak of severe diarrhea due to zoonotic Cryptosporidium parvum and C. xiaoi in goat kids in Chungcheongbuk-do, Korea. Parasitol Res 122, 2045–2054 (2023). https://doi.org/10.1007/s00436-023-07904-5
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DOI: https://doi.org/10.1007/s00436-023-07904-5