The genetic diversity of Cryptosporidium spp. in Apodemus spp. (striped field mouse, yellow-necked mouse and wood mouse) from 16 European countries was examined by PCR/sequencing of isolates from 437 animals. Overall, 13.7% (60/437) of animals were positive for Cryptosporidium by PCR. Phylogenetic analysis of small-subunit rRNA, Cryptosporidium oocyst wall protein and actin gene sequences showed the presence of Cryptosporidium ditrichi (22/60), Cryptosporidium apodemi (13/60), Cryptosporidium apodemus genotype I (8/60), Cryptosporidium apodemus genotype II (9/60), Cryptosporidium parvum (2/60), Cryptosporidium microti (2/60), Cryptosporidium muris (2/60) and Cryptosporidium tyzzeri (2/60). At the gp60 locus, novel gp60 families XVIIa and XVIIIa were identified in Cryptosporidium apodemus genotype I and II, respectively, subtype IIaA16G1R1b was identified in C. parvum, and subtypes IXaA8 and IXcA6 in C. tyzzeri. Only animals infected with C. ditrichi, C. apodemi, and Cryptosporidium apodemus genotypes shed oocysts that were detectable by microscopy, with the infection intensity ranging from 2000 to 52,000 oocysts per gram of faeces. None of the faecal samples was diarrheic in the time of the sampling.

Department of Biology and Medical Parasitology Wroclaw Medical University Poland

Department of Parasitology Institute of Genetics and Microbiology University of Wrocław Poland

Faculty of Agriculture University of South Bohemia in České Budějovice Czech Republic; Institute of Parasitology Biology Centre of the Czech Academy of Sciences České Budějovice Czech Republic

Institute of Parasitology Biology Centre of the Czech Academy of Sciences České Budějovice Czech Republic

Microbiological Sciences Department North Dakota State University Fargo USA

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Alves M, Xiao LH, 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, 10.1128/JCM.41.6.2744-2747.2003. PubMed DOI PMC

Backhans A, Jacobson M, Hansson I, Lebbad M, Lambertz ST, Gammelgard E, Saager M, Akande O, Fellstrom C, 2013. Occurrence of pathogens in wild rodents caught on Swedish pig and chicken farms. Epidemiol. Infect 141, 1885–1891, 10.1017/S0950268812002609. PubMed DOI PMC

Bajer A, Bednarska M, Pawelczyk A, Behnke JM, Gilbert FS, Sinski E, 2002. Prevalence and abundance of Cryptosporidium parvum and Giardia spp. in wild rural rodents from the Mazury Lake District region of Poland. Parasitology 125, 21–34. PubMed

Bednarska M, Bajer A, Sinski E, Girouard AS, Tamang L, Graczyk TK, 2007. Fluorescent in situ hybridization as a tool to retrospectively identify Cryptosporidium parvum and Giardia lamblia in samples from terrestrial mammalian wildlife. Parasitol. Res 100, 455–460, 10.1007/s00436-006-0276-y. PubMed DOI

Bouzid M, Hunter PR, Chalmers RM, Tyler KM, 2013. Cryptosporidium pathogenicity and virulence. Clin. Microbiol. Rev 26, 115–134, 10.1128/Cmr.00076-12. PubMed DOI PMC

Castro-Hermida JA, Garcia-Presedo I, Gonzalez-Warleta M, Mezo M, 2011. Prevalence of Cryptosporidium and Giardia in roe deer (Capreolus capreolus) and wild boars (Sus scrofa) in Galicia (NW, Spain). Vet. Parasitol 179, 216–219, 10.1016/j.vetpar.2011.02.023. PubMed DOI

Cavalier-Smith T, 2014. Gregarine site-heterogeneous 18S rDNA trees, revision of gregarine higher classification, and the evolutionary diversification of Sporozoa. Eur. J. Protistol 50, 472–495, 10.1016/j.ejop.2014.07.002. PubMed DOI

Chalmers RM, Sturdee AP, Bull SA, Miller A, Wright SE, 1997. The prevalence of Cryptosporidium parvum and C. muris in Mus domesticus, Apodemus sylvaticus and Clethrionomys glareolus in an agricultural system. Parasitol. Res 83, 478–482. PubMed

Crawshaw GJ, Mehren KG, 1987. Cryptosporidiosis in zoo and wild animals., Erkrankungen der Zootiere. Verhandlungsbericht des 29 Internationalen Symposiums Uber die Erkrankungen der Zootiere. Akademie-Verlag, Berlin, Cardiff, pp. 353–362.

Čondlová S, Horčičková M, Sak B, Květoňová D, Hlásková L, Konečný R, Stanko M, McEvoy J, Kváč M, 2018. Cryptosporidium apodemi sp. n. and Cryptosporidium ditrichi sp. n. (Apicomplexa: Cryptosporidiidae) in Apodemus spp. Eur. J. Protistol 63, 1–12, 10.1016/j.ejop.2017.12.006. PubMed DOI

Danišová O, Valenčáková A, Stanko M, Luptaková L, Hatalová E, Canady A, 2017. Rodents as a reservoir of infection caused by multiple zoonotic species/genotypes of C. parvum, C. hominis, C. suis, C. scrofarum, and the first evidence of C. muskrat genotypes I and II of rodents in Europe. Acta Trop 172, 29–35, 10.1016/j.actatropica.2017.04.013. PubMed DOI

de Bellocq JG, Baird SJE, Albrechtova J, Sobekova K, Piálek J, 2015. Murine Cytomegalovirus Is Not Restricted to the House Mouse Mus musculus domesticus: Prevalence and Genetic Diversity in the European House Mouse Hybrid Zone. J. Virol 89, 406–414, 10.1128/Jvi.02466-14. PubMed DOI PMC

Del Coco VF, Cordoba MA, Bilbao G, de Almeida Castro AP, Basualdo JA, Fayer R, Santin M, 2014. Cryptosporidium parvum GP60 subtypes in dairy cattle from Buenos Aires, Argentina. Res. Vet. Sci 96, 311–314, 10.1016/j.rvsc.2013.12.010. PubMed DOI

Fayer R, 2007. General Biology, in: Fayer R, Xiao L (Eds.), Cryptosporidium and cryptosporidiosis, 2 ed CRC Press, Boca Raton, FL, pp. 1–42.

Fayer R, Gasbarre L, Pasquali P, Canals A, Almeria S, Zarlenga D, 1998. Cryptosporidium parvum infection in bovine neonates: dynamic clinical, parasitic and immunologic patterns. Int. J. Parasitol 28, 49–56. PubMed

Fayer R, Santín M, Xiao L, 2005. Cryptosporidium bovis n. sp. (Apicomplexa: Cryptosporidiidae) in cattle (Bos taurus). J. Parasitol 91, 624–629, 10.1645/GE-3435. PubMed DOI

Graczyk TK, Cranfield MR, Fayer R, 1998. Oocysts of Cryptosporidium from snakes are not infectious to ducklings but retain viability after intestinal passage through a refractory host. Vet. Parasitol 77, 33–40. PubMed

Graczyk TK, Fayer R, Cranfield MR, 1996. Cryptosporidium parvum is not transmissible to fish, amphibians, or reptiles. J. Parasitol 82, 748–751. PubMed

Hajdušek O, Ditrich O, Šlapeta J, 2004. Molecular identification of Cryptosporidium spp. in animal and human hosts from the Czech Republic. Vet. Parasitol 122, 183–192, 10.1016/j.vetpar.2004.04.005. PubMed DOI

Hikosaka K, Nakai Y, 2005. A novel genotype of Cryptosporidium muris from large Japanese field mice, Apodemus speciosus. Parasitol. Res 97, 373–379, 10.1007/s00436-005-1459-7. PubMed DOI

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, 10.1007/s00436-016-4967-8. PubMed DOI PMC

Horčičková M, Čondlová S, Holubová N, Sak B, Květoňová D, Hlásková L, Konečný R, Sedláček F, Clark M, Giddings C, McEvoy J, Kváč M, 2018. Diversity of Cryptosporidium in common voles and description of Cryptosporidium alticolis sp. n. and Cryptosporidium microti sp. n. (Apicomplexa: Cryptosporidiidae). Parasitology, 1–14, 10.1017/S0031182018001142. PubMed DOI PMC

Imre K, Luca C, Costache M, Sala C, Morar A, Morariu S, Ilie MS, Imre M, Darabus G, 2013. Zoonotic Cryptosporidium parvum in Romanian newborn lambs (Ovis aries). Vet. Parasitol 191, 119–122, 10.1016/j.vetpar.2012.08.020. PubMed DOI

Iseki M, Maekawa T, Moriya K, Uni S, Takada S, 1989. Infectivity of Cryptosporidium muris (strain RN 66) in various laboratory animals. Parasitol. Res 75, 218–222. PubMed

Jacobson C, Williams A, Yang R, Ryan U, Carmichael I, Campbell AJ, Gardner GE, 2016. Greater intensity and frequency of Cryptosporidium and Giardia oocyst shedding beyond the neonatal period is associated with reductions in growth, carcase weight and dressing efficiency in sheep. Vet. Parasitol 228, 42–51, 10.1016/j.vetpar.2016.08.003. PubMed DOI

Jenkins MB, Liotta JL, Lucio-Forster A, Bowman DD, 2010. Concentrations, viability, and distribution of Cryptosporidium genotypes in lagoons of swine facilities in the Southern Piedmont and in coastal plain watersheds of Georgia. Appl. Environ. Microbiol 76, 5757–5763, 10.1128/AEM.00434-10. PubMed DOI PMC

Jiang J, Alderisio KA, Xiao L, 2005. Distribution of Cryptosporidium genotypes in storm event water samples from three watersheds in New York. Appl. Environ. Microbiol 71, 4446–4454, 10.1128/AEM.71.8.4446-4454.2005. PubMed DOI PMC

Kulis-Malkowska K, 2007. [The impact of nematode invasions on the pattern of Cryptosporidium parvum infection in wild rodents]. Wiad Parazytol 53, 251–252. PubMed

Kváč M, Hofmannová L, Hlásková L, Květoňová D, Vitovec J, McEvoy J, Sak B, 2014a. Cryptosporidium erinacei n. sp. (Apicomplexa: Cryptosporidiidae) in hedgehogs. Vet. Parasitol 201, 9–17, 10.1016/j.vetpar.2014.01.014. PubMed DOI

Kváč M, Kestřánová M, Květoňová D, Kotková M, Ortega Y, McEvoy J, Sak B, 2012. Cryptosporidium tyzzeri and Cryptosporidium muris originated from wild West-European house mice (Mus musculus domesticus) and East-European house mice (Mus musculus musculus) are non-infectious for pigs. Exp. Parasitol 131, 107–110, 10.1016/j.exppara.2012.03.016. PubMed DOI

Kváč M, McEvoy J, Loudová M, Stenger B, Sak B, Květoňová D, Ditrich O, Rašková V, Moriarty E, Rost M, Macholán M, Piálek J, 2013. Coevolution of Cryptosporidium tyzzeri and the house mouse (Mus musculus). Int. J. Parasitol 43, 805–817, 10.1016/j.ijpara.2013.04.007. PubMed DOI PMC

Kváč M, McEvoy J, Stenger B, Clark M, 2014b. Cryptosporidiosis in other vertebrates, in: Cacciò SM, Widmer G (Eds.), Cryptosporidium: Parasite and Disease, 1st ed Springer, Wien, pp. 237–326.

Kváč M, Ondráčková Z, Květoňová D, Sak B, Vítovec J, 2007. Infectivity and pathogenicity of Cryptosporidium andersoni to a novel host, southern multimammate mouse (Mastomys coucha). Vet. Parasitol 143, 229–233, 10.1016/j.vetpar.2006.08.031. PubMed DOI

Li N, Xiao L, Alderisio K, Elwin K, Cebelinski E, Chalmers R, Santin M, Fayer R, Kváč 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, 10.3201/eid2002.121797. PubMed DOI PMC

Li X, Pereira M, Larsen R, Xiao C, Phillips R, Striby K, McCowan B, Atwill ER, 2015. Cryptosporidium rubeyi n. sp. (Apicomplexa: Cryptosporidiidae) in multiple Spermophilus ground squirrel species. Int. J. Parasitol. Parasites Wildl 4, 343–350, 10.1016/j.ijppaw.2015.08.005. PubMed DOI PMC

Lv C, Zhang L, Wang R, Jian F, Zhang S, Ning C, Wang H, Feng C, Wang X, Ren X, Qi M, Xiao L, 2009. Cryptosporidium spp. in wild, laboratory, and pet rodents in china: prevalence and molecular characterization. Appl. Environ. Microbiol 75, 7692–7699. PubMed PMC

Miláček P, Vítovec J, 1985. Differential staining of cryptosporidia by aniline-carbol-methyl violet and tartrazine in smears from feces and scrapings of intestinal mucosa. Folia Parasitol 32, 50. PubMed

Murakoshi F, Fukuda Y, Matsubara R, Kato Y, Sato R, Sasaki T, Tada C, Nakai Y, 2013. Detection and genotyping of Cryptosporidium spp. in large Japanese field mice, Apodemus speciosus. Vet. Parasitol 196, 184–188, 10.1016/j.vetpar.2013.02.011. PubMed DOI

Nakamura AA, Meireles MV, 2015. Cryptosporidium infections in birds--a review. Rev. Bras. Parasitol. Vet 24, 253–267, 10.1590/S1984-29612015063. PubMed DOI

Ng-Hublin JS, Singleton GR, Ryan U, 2013. Molecular characterization of Cryptosporidium spp. from wild rats and mice from rural communities in the Philippines. Infect. Genet. Evol 16, 5–12, 10.1016/j.meegid.2013.01.011. PubMed DOI

Ng JS, Eastwood K, Walker B, Durrheim DN, Massey PD, Porigneaux P, Kemp R, McKinnon B, Laurie K, Miller D, Bramley E, Ryan U, 2012. Evidence of Cryptosporidium transmission between cattle and humans in northern New South Wales. Exp. Parasitol 130, 437–441, 10.1016/j.exppara.2012.01.014. PubMed DOI

Papanikolopoulou V, Baroudi D, Guo Y, Wang Y, Papadopoulos E, Lafi SQ, Abd El-Tawab MM, Diakou A, Giadinis ND, Feng Y, Xiao L, 2018. Genotypes and subtypes of Cryptosporidium spp. in diarrheic lambs and goat kids in northern Greece. Parasitol. Int 67, 472–475, 10.1016/j.parint.2018.04.007. PubMed DOI

Pedraza-Diaz S, Amar C, Iversen AM, Stanley PJ, McLauchlin J, 2001. Unusual Cryptosporidium species recovered from human faeces: first description of Cryptosporidium felis and Cryptosporidium ‘dog type’ from patients in England. J. Med. Microbiol 50, 293–296. PubMed

Perec-Matysiak A, Bunkowska-Gawlik K, Zalesny G, Hildebrand J, 2015. Small rodents as reservoirs of Cryptosporidium spp. and Giardia spp. in south-western Poland. Ann. Agr. Env. Med 22, 1–5, 10.5604/12321966.1141359. PubMed DOI

Petersen HH, Jianmin W, Katakam KK, Mejer H, Thamsborg SM, Dalsgaard A, Olsen A, Enemark HL, 2015. Cryptosporidium and Giardia in Danish organic pig farms: Seasonal and age-related variation in prevalence, infection intensity and species/genotypes. Vet. Parasitol 214, 29–39, 10.1016/j.vetpar.2015.09.020. PubMed DOI

Prediger J, Horčičková M, Hofmannová L, Sak B, Ferrari N, Mazzamuto MV, Romeo C, Wauters LA, McEvoy J, Kváč M, 2017. Native and introduced squirrels in Italy host different Cryptosporidium spp. Eur. J. Protistol 61, 64–75, 10.1016/j.ejop.2017.09.007. PubMed DOI

Ren X, Zhao J, Zhang L, Ning C, Jian F, Wang R, Lv C, Wang Q, Arrowood MJ, Xiao L, 2012. Cryptosporidium tyzzeri n. sp. (Apicomplexa: Cryptosporidiidae) in domestic mice (Mus musculus). Exp. Parasitol 130, 274–281, 10.1016/j.exppara.2011.07.012. PubMed DOI

Rhee JK, Yook SY, Park BK, 1995. Oocyst production and immunogenicity of Cryptosporidium muris (strain MCR) in mice. Korean J. Parasitol 33, 377–382. PubMed

Ryan U, Xiao L, 2014. Taxonomy and Molecular Taxonomy, in: Cacciò SM, Widmer G (Eds.), Cryptosporidium: parasite and disease, 1 ed Springer, pp. 3–42.

Sak B, Petrzelkova KJ, Květoňová D, Mynářová A, Pomajbíková K, Modrý D, Cranfield MR, Mudakikwa A, Kváč M, 2014. Diversity of microsporidia, Cryptosporidium and Giardia in mountain gorillas (Gorilla beringei beringei) in Volcanoes National Park, Rwanda. PLoS One 9, e109751, 10.1371/journal.pone.0109751. PubMed DOI PMC

Saki J, Foroutan-Rad M, Asadpouri R, 2016 Molecular Characterization of Cryptosporidium spp. in Wild Rodents of Southwestern Iran Using 18s rRNA Gene Nested-PCR-RFLP and Sequencing Techniques. J. Trop. Med 2016, 6834206, 10.1155/2016/6834206. PubMed DOI PMC

Satoh M, Hikosaka K, Sasaki T, Suyama Y, Yanai T, Ohta M, Nakai Y, 2003. Characteristics of a novel type of bovine Cryptosporidium andersoni. Appl. Environ. Microbiol 69, 691–692. PubMed PMC

Song J, Kim CY, Chang SN, Abdelkader TS, Han J, Kim TH, Oh H, Lee JM, Kim DS, Kim JT, Oh HS, Hur M, Suh JH, Park JH, 2015. Detection and molecular characterization of Cryptosporidium spp. from wild rodents and insectivores in South Korea. Korean J. Parasitol 53, 737–743, 10.3347/kjp.2015.53.6.737. PubMed DOI PMC

Spano F, Putignani L, McLauchlin J, Casemore DP, Crisanti A, 1997. PCR-RFLP analysis of the Cryptosporidium oocyst wall protein (COWP) gene discriminates between C. wrairi and C. parvum, and between C. parvum isolates of human and animal origin. FEMS Microbiology Letters 150, 209–217. PubMed

Stenger BL, Clark ME, Kváč M, Khan E, Giddings CW, Prediger J, McEvoy JM, 2015. North American tree squirrels and ground squirrels with overlapping ranges host different Cryptosporidium species and genotypes. Infect. Genet. Evol 36, 287–293, 10.1016/j.meegid.2015.10.002. PubMed DOI

Striepen B, 2013. Parasitic infections: Time to tackle cryptosporidiosis. Nature 503, 189–191. PubMed

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. PubMed PMC

Sulaiman IM, Lal AA, Xiao LH, 2002. Molecular phylogeny and evolutionary relationships of Cryptosporidium parasites at the actin locus. J. Parasitol 88, 388–394, 10.1645/0022-3395(2002)088[0388:MPAERO]2.0.CO;2. PubMed DOI

Torres J, Gracenea M, Gomez MS, Arrizabalaga A, Gonzalez-Moreno O, 2000. The occurrence of Cryptosporidium parvum and C. muris in wild rodents and insectivores in Spain. Vet. Parasitol 92, 253–260. PubMed

Trotz-Williams LA, Martin DS, Gatei W, Cama V, Peregrine AS, Martin SW, Nydam DV, Jamieson F, Xiao L, 2006. Genotype and subtype analyses of Cryptosporidium isolates from dairy calves and humans in Ontario. Parasitol. Res 99, 346–352. PubMed

Tůmová E, Skřivan M, Marounek M, Pavlásek I, Ledvinka Z, 2002. Performance and oocyst shedding in broiler chickens orally infected with Cryptosporidium baileyi and Cryptosporidium meleagridis. Avian Dis 46, 203–207, 10.1637/0005-2086(2002)046[0203:PAOSIB]2.0.CO;2. PubMed DOI

Vetterling JM, Jervis HR, Merrill TG, Sprinz H, 1971. Cryptosporidium wrairi sp. n. from the guinea pig Cavia porcellus, with an emendation of the genus. J. Protozool 18, 243–247. PubMed

Webster JP, Macdonald DW, 1995a. Cryptosporidiosis reservoir in wild brown rats (Rattus norvegicus) in the UK. Epidemiol. Infect 115, 207–209. PubMed PMC

Webster JP, Macdonald DW, 1995b. Parasites of wild brown rats (Rattus norvegicus) on UK farms. Parasitology 111, 247–255. PubMed

Wielinga PR, de VA, van der Goot TH, Mank T, Mars MH, Kortbeek LM, van der Giessen JW, 2008. Molecular epidemiology of Cryptosporidium in humans and cattle in The Netherlands. Int. J. Parasitol 38, 809–817. PubMed

Xiao L, Escalante L, Yang C, 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. PubMed PMC

Xiao L, Moore JE, Ukoh U, Gatei W, Lowery CJ, Murphy TM, Dooley JS, Millar BC, Rooney PJ, Rao JR, 2006. Prevalence and identity of Cryptosporidium spp. in pig slurry. Appl. Environ. Microbiol 72, 4461–4463, 10.1128/AEM.00370-06. PubMed DOI PMC

Xiao L, Ryan UM, Graczyk TK, Limor J, Li L, Kombert M, Junge R, Sulaiman IM, Zhou L, Arrowood MJ, Koudela B, Modrý D, Lal AA, 2004. Genetic diversity of Cryptosporidium spp. in captive reptiles. Appl. Environ. Microbiol 70, 891–899. PubMed PMC

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