Skip to main content

Advertisement

SpringerLink
Log in

Occurrence of Cryptosporidium suis and Cryptosporidium scrofarum on commercial swine farms in the Czech Republic and its associations with age and husbandry practices

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

From 2009 to 2011, the occurrence of Cryptosporidium spp. was investigated on 22 farms in the Czech Republic. A total of 1,620 individual faecal samples of pigs of all age categories (pre-weaned, starters, pre-growers, growers, and sows) were evaluated for presence of Cryptosporidium spp. by standard microscopy and molecular tools. Genotyping was done through PCR amplification and characterization of the SSU rRNA (species-specific protocols) and GP60 loci. Cryptosporidium spp. was found on 16 of 22 farms with a range 0.9–71.4 %. Overall, 194 (12 %) specimens were positive by microscopy and 353 (21.8 %) by PCR. While RFLP and direct sequencing of the PCR-amplified products showed presence of Cryptosporidium suis (142), Cryptosporidium scrofarum (195), Cryptosporidium muris (3) and 13 samples had mixed infections with C. suis and C. scrofarum, species-specific molecular tools identified C. suis (224), C. scrofarum (208), Cryptosporidium parvum subtype IIa A16G1R1b (1), and C. muris (3). In addition, a total of 82 pigs had concurrent infections with C. suis and C. scrofarum. The analysis by age showed that C. suis was primarily detected among pre-weaned, whereas C. scrofarum was mostly detected among starters, especially those weaned at a younger age. Moreover, C. scrofarum never has been detected in animals younger than 6 weeks of age. Also, piglets weaned at 3 weeks of age were twice more likely to be infected with C. scrofarum than piglets weaned at an older age. Pigs raised on straw bedding were more likely to have Cryptosporidium than pigs raised on slats/slurry systems. The infections with different species were not associated with loose faeces or intensity of oocyst shedding, even when comparing different age groups.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Akiyoshi DE, Dilo J, Pearson C, Chapman S, Tumwine J, Tzipori S (2003) Characterization of Cryptosporidium meleagridis of human origin passaged through different host species. Infect Immun 71:1728–1732

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Argenzio RA, Liacos JA, Levy ML, Meuten DJ, Lecce JG, Powell DW (1990) Villous atrophy, crypt hyperplasia, cellular infiltration, and impaired glucose-Na absorption in enteric cryptosporidiosis of pigs. Gastroenterology 98:1129–1140

    PubMed  CAS  Google Scholar 

  • Armson A, Yang R, Thompson J, Johnson J, Reid S, Ryan UM (2009) Giardia genotypes in pigs in Western Australia: prevalence and association with diarrhoea. Exp Parasitol 121:381–383

    Article  PubMed  Google Scholar 

  • Bergeland ME (1977) Necrotic enteritis in nursing piglets. Proc Am Assoc Vet Lab Diagn 20:151–158

    Google Scholar 

  • Budu-Amoako E, Greenwood SJ, Dixon BR, Barkema HW, Hurnik D, Estey C, McClure JT (2012) Occurrence of Giardia and Cryptosporidium in pigs on Prince Edward Island, Canada. Vet Parasitol 184:18–24

    Article  PubMed  Google Scholar 

  • Cama AV, Bern C, Sulaiman IM, Gilman RH, Ticona E, Vivar A, Kawai V, Vargas D, Zhou L, Xiao L (2003) Cryptosporidium species and genotypes in HIV-positive patients in Lima. J Eukaryot Microbiol 50:531–533

    Article  PubMed  Google Scholar 

  • Cama VA, Gilman RH, Vivar A, Ticona E, Ortega Y, Bern C, Xiao L (2006) Mixed Cryptosporidium infections and HIV. Emerg Infect Dis 12:1025–1028

    Article  PubMed  Google Scholar 

  • Chalmers RM, Giles M (2010) Zoonotic cryptosporidiosis in the UK—challenges for control. J Appl Microbiol 109:1487–1497

    Article  PubMed  CAS  Google Scholar 

  • Checkley W, Gilman RH, Epstein LD, Suarez M, Diaz JF, Cabrera L, Black RE, Sterling CR (1997) Asymptomatic and symptomatic cryptosporidiosis: their acute effect on weight gain in Peruvian children. Am J Epidemiol 145:156–163

    Article  PubMed  CAS  Google Scholar 

  • Chen F, Huang K (2007) Prevalence and phylogenetic analysis of Cryptosporidium in pigs in eastern China. Zoonoses Publ Health 54:393–400

    Article  CAS  Google Scholar 

  • Chen Z, Mi R, Yu H, Shi Y, Huang Y, Chen Y, Zhou P, Cai Y, Lin J (2011) Prevalence of Cryptosporidium spp. in pigs in Shanghai, China. Vet Parasitol 181:113–119

    PubMed  Google Scholar 

  • Ebeid M, Mathis A, Pospischil A, Deplazes P (2003) Infectivity of Cryptosporidium parvum genotype I in conventionally reared piglets and lambs. Parasitol Res 90:232–235

    PubMed  CAS  Google Scholar 

  • Enemark HL, Ahrens P, Bille-Hansen V, Heegaard PM, Vigre H, Thamsborg SM, Lind P (2003) Cryptosporidium parvum: infectivity and pathogenicity of the ‘porcine’ genotype. Parasitology 126:407–416

    Article  PubMed  CAS  Google Scholar 

  • Fayer R (2008) General biology. In: Fayer R, Xiao L (eds) Cryptosporidium and cryptosporidiosis, 2nd edn. CRC and IWA, Boca Raton, pp 1–42

    Google Scholar 

  • Fayer R (2010) Taxonomy and species delimitation in Cryptosporidium. Exp Parasitol 124:90–97

    Article  PubMed  Google Scholar 

  • Featherstone CA, Marshall JA, Giles M, Sayers AR, Pritchard GC (2010) Cryptosporidium infection in pigs in East Anglia. Vet Rec 166:51–52

    Article  PubMed  CAS  Google Scholar 

  • Guselle NJ, Appelbee AJ, Olson ME (2003) Biology of Cryptosporidium parvum in pigs: from weaning to market. Vet Parasitol 113:7–18

    Article  PubMed  CAS  Google Scholar 

  • Hadfield SJ, Robinson G, Elwin K, Chalmers RM (2011) Detection and differentiation of Cryptosporidium spp. in human clinical samples by use of real-time PCR. J Clin Microbiol 49:918–924

    Article  PubMed  CAS  Google Scholar 

  • Hamnes IS, Gjerde BK, Robertson LJ (2006) Occurrence of Cryptosporidium and Giardia in suckling piglets in Norway. Vet Parasitol 140:204–216

    Article  PubMed  Google Scholar 

  • Hamnes IS, Gjerde BK, Forberg T, Robertson LJ (2007) Occurrence of Cryptosporidium and Giardia in suckling piglets in Norway. Vet Parasitol 144:222–233

    Article  PubMed  Google Scholar 

  • Jeníková M, Němejc K, Sak B, Květoňová D, Kváč M (2011) New view on the age-specificity of pig Cryptosporidium by species-specific primers for distinguishing Cryptosporidium suis and Cryptosporidium pig genotype II. Vet Parasitol 176:120–125

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Johnson J, Buddle R, Reid S, Armson A, Ryan UM (2008) Prevalence of Cryptosporidium genotypes in pre- and post-weaned pigs in Australia. Exp Parasitol 119:418–421

    Article  PubMed  CAS  Google Scholar 

  • Kennedy GA, Kreitner GL, Strafuss AC (1977) Cryptosporidiosis in three pigs. J Am Vet Med Assoc 170:348–350

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Kváč M, Hanzlíková D, Sak B, Květoňová D (2009a) Prevalence and age-related infection of Cryptosporidium suis, C. muris and Cryptosporidium pig genotype II in pigs on a farm complex in the Czech Republic. Vet Parasitol 160:319–322

    Article  PubMed  Google Scholar 

  • Kváč M, Květoňová D, Sak B, Ditrich O (2009b) Cryptosporidium pig genotype II in immunocompetent man. Emerg Infect Dis 15:982–983

    Article  PubMed  Google Scholar 

  • Kváč M, Sak B, Hanzlíková D, Kotilová J, Květoňová D (2009c) Molecular characterization of Cryptosporidium isolates from pigs at slaughterhouses in South Bohemia, Czech Republic. Parasitol Res 104:425–428

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Kváč M, Kestřánová M, Pinková M, Květoňová D, Kalinová J, Wagnerová P, Kotková M, Vítovec J, Ditrich O, McEvoy J, Stenger B, Sak B (2013) Cryptosporidium scrofarum n. sp. (Apicomplexa: Cryptosporidiidae) in domestic pigs (Sus scrofa). Vet Parasitol 191:218–227

    Google Scholar 

  • Langkjaer RB, Vigre H, Enemark HL, Maddox-Hyttel C (2007) Molecular and phylogenetic characterization of Cryptosporidium and Giardia from pigs and cattle in Denmark. Parasitology 134:339–350

    Article  PubMed  CAS  Google Scholar 

  • Maddox-Hyttel C, Langkjaer RB, Enemark HL, Vigre H (2006) Cryptosporidium and Giardia in different age groups of Danish cattle and pigs—occurrence and management associated risk factors. Vet Parasitol 141:48–59

    Article  PubMed  Google Scholar 

  • McCarthy S, Ng J, Gordon C, Miller R, Wyber A, Ryan UM (2008) Prevalence of Cryptosporidium and Giardia species in animals in irrigation catchments in the southwest of Australia. Exp Parasitol 118:596–599

    Article  PubMed  Google Scholar 

  • Miláček P, Vítovec J (1985) Differential staining of Cryptosporidia by aniline–carbol–methyl violet and tartrazine in smears from faeces and scrapings of intestinal mucosa. Folia Parasitol 32:50

    PubMed  Google Scholar 

  • Mišič Z, Katič-Radivojevič S, Kulišič Z (2003) Cryptosporidium infections in nursing, weaning and post-weaned piglets and sows in the Belgrade district. Acta Vet (Belograd) 5–6:361–366

    Google Scholar 

  • Moon HW, Bemrick WJ (1981) Fecal transmission of calf cryptosporidia between calves and pigs. Vet Pathol 18:248–255

    PubMed  CAS  Google Scholar 

  • Moon HW, Schwartz A, Welch MJ, McCann PP, Runnels PL (1982) Experimental fecal transmission of human cryptosporidia to pigs, and attempted treatment with an ornithine decarboxylase inhibitor. Vet Pathol 19:700–707

    Article  PubMed  CAS  Google Scholar 

  • Morgan UM, Sargent KD, Deplazes P, Forbes DA, Spano F, Hertzberg H, Elliot A, Thompson RC (1998) Molecular characterization of Cryptosporidium from various hosts. Parasitology 117:31–37

    Article  PubMed  CAS  Google Scholar 

  • Morgan UM, Buddle R, Armson A, Elliot A, Thompson RCA (1999) Molecular and biological characterisation of Cryptosporidium in pigs. Aust Vet J 77:44–47

    Article  PubMed  CAS  Google Scholar 

  • Němejc K, Sak B, Květoňová D, Hanzal V, Jeníková M, Kváč M (2012) The first report on Cryptosporidium suis and Cryptosporidium pig genotype II in Eurasian wild boars (Sus scrofa) (Czech Republic). Vet Parasitol 184:122–125

    Article  PubMed  Google Scholar 

  • Nguyen ST, Fukuda Y, Tada C, Sato R, Huynh VV, Nguyen DT, Nakai Y (2012a) Molecular characterization of Cryptosporidium in pigs in central Vietnam. Parasitol Res. doi:10.1007/s00436-012-3124-2

  • Nguyen ST, Honma H, Geurden T, Ikarash M, Fukuda Y, Huynh VV, Nguyen DT, Nakai Y (2012b) Prevalence and risk factors associated with Cryptosporidium oocysts shedding in pigs in Central Vietnam. Res Vet Sci 93:848–852

    Article  PubMed  Google Scholar 

  • Paoletti B, Giangaspero A, Gatti A, Iorio R, Cembalo D, Milillo P, Traversa D (2009) Immunoenzymatic analysis and genetic detection of Cryptosporidium parvum in lambs from Italy. Exp Parasitol 122:349–352

    Article  PubMed  CAS  Google Scholar 

  • Plutzer J, Karanis P (2009) Genetic polymorphism in Cryptosporidium species: an update. Vet Parasitol 165:187–199

    Article  PubMed  CAS  Google Scholar 

  • Quílez J, Sánchez-Acedo C, Clavel A, del Cacho E, López-Bernad F (1996) Comparison of an acid-fast stain and a monoclonal antibody-based immunofluorescence reagent for the detection of Cryptosporidium oocysts in faecal specimens from cattle and pigs. Vet Parasitol 67:75–81

    Article  PubMed  Google Scholar 

  • Ryan UM, Xiao L (2009) Molecular epidemiology and typing of nonhuman isolates of Cryptosporidium. In: Ortega-Pierres MG, Cacciò SM, Fayer R, Mank TG, Smith HV, Thompson RCA (eds) Giardia and Cryptosporidium: from molecules to disease. CABI, Oxfordshire, pp 65–80

    Chapter  Google Scholar 

  • Ryan UM, Samarasinghe B, Read C, Buddle JR, Robertson ID, Thompson RC (2003) Identification of a novel Cryptosporidium genotype in pigs. Appl Environ Microbiol 69:3970–3974

    Article  PubMed  CAS  Google Scholar 

  • Ryan UM, Monis P, Enemark HL, Sulaiman I, Samarasinghe B, Read C, Buddle R, Robertson I, Zhou L, Thompson RC, Xiao L (2004) Cryptosporidium suis n. sp. (Apicomplexa: Cryptosporidiidae) in pigs (Sus scrofa). J Parasitol 90:769–773

    Article  PubMed  CAS  Google Scholar 

  • Ryan UM, Read C, Hawkins P, Warnecke M, Swanson P (2005a) Genotypes of Cryptosporidium from Sydney water catchment areas. J Appl Microbiol 98:1221–1229

    Article  PubMed  CAS  Google Scholar 

  • Ryan UM, Bath C, Robertson I, Read C, Elliot A, McInnes L, Traub R, Besier B (2005b) Sheep may not be an important zoonotic reservoir for Cryptosporidium and Giardia parasites. Appl Env Microbiol 71:4992–4997

    Article  CAS  Google Scholar 

  • Sanford SE (1987) Enteric cryptosporidial infection in pigs: 184 cases (1081–1985). J Am Vet Med Assoc 190:695–698

    PubMed  CAS  Google Scholar 

  • Santín M, Zarlenga DS (2009) A multiplex polymerase chain reaction assay to simultaneously distinguish Cryptosporidium species of veterinary and public health concern in cattle. Vet Parasitol 166:32–37

    Article  PubMed  Google Scholar 

  • Santín M, Trout JM, Fayer R (2007) Prevalence and molecular characterization of Cryptosporidium and Giardia species and genotypes in sheep in Maryland. Vet Parasitol 146:17–24

    Article  PubMed  Google Scholar 

  • Santín M, Trout JM, Fayer R (2008) A longitudinal study of cryptosporidiosis in dairy cattle from birth to 2 years of age. Vet Parasitol 155:15–23

    Article  PubMed  Google Scholar 

  • Schad GA, Duffy CH, Leiby DA, Murrell KD, Zirkle EW (1987) Trichinella spiralis in an agricultural ecosystem: transmission under natural and experimentally modified on-farm conditions. J Parasitol 73:95–102

    Article  PubMed  CAS  Google Scholar 

  • Smith HV (2008) Cryptosporidiosis. In: OIE Biological Standards Commission (ed) OIE manual of diagnostic tests and vaccines for terrestrial animals, 6th edn. Office International des Epizooties, Paris, pp 1192–1215

    Google Scholar 

  • Smith HV, Cacciò SM, Cook N, Nichols RAB, Tait A (2007) Cryptosporidium and Giardia as foodborne zoonoses. Vet Parasitol 149:29–40

    Article  PubMed  CAS  Google Scholar 

  • Suárez-Luengas L, Clavel A, Quílez J, Goñi-Cepero MP, Torres E, Sánchez-Acedo C, del Cacho E (2007) Molecular characterization of Cryptosporidium isolates from pigs in Zaragoza (northeastern Spain). Vet Parasitol 148:231–235

    Article  PubMed  Google Scholar 

  • Thompson PB, Brewer J, Brewer EE (1996) Swine care handbook. National Pork Board, Des Moines, p 34

    Google Scholar 

  • Tzipori S, Angus KW, Gray EW, Campbell I, Allan F (1981) Diarrhea in lambs experimentally infected with Cryptosporidium isolated from calves. Am J Vet Res 42:1400–1404

    PubMed  CAS  Google Scholar 

  • Tzipori S, Smith M, Makin T, Halpin C (1982) Enterocolitis in piglets caused by Cryptosporidium sp. purified from calf faeces. Vet Parasitol 11:121–126

    Article  PubMed  CAS  Google Scholar 

  • Vítovec J, Koudela B (1992) Pathogenesis of intestinal cryptosporidiosis in conventional and gnotobiotic piglets. Vet Parasitol 43:25–36

    Article  PubMed  Google Scholar 

  • Vítovec J, Hamadejová K, Landová L, Kváč M, Květoňová D, Sak B (2006) Prevalence and pathogenicity of Cryptosporidium suis in pre- and post-weaned pigs. J Vet Med B 53:239–243

    Article  Google Scholar 

  • Wang R, Qiu S, Jian F, Zhang S, Shen Y, Zhang L, Ning C, Cao J, Qi M, Xiao L (2010) Prevalence and molecular identification of Cryptosporidium spp. in pigs in Henan, China. Parasitol Res 107:1489–1494

    Article  PubMed  Google Scholar 

  • Wieler LH, Ilieff A, Herbst W, Bauer C, Wieler E, Bauerfeind R, Failing K, Klos H, Wengert D, Bajer G, Zahner H (2001) Prevalence of enteropathogens in suckling and weaned piglets with diarrhoea in southern Germany. J Vet Med B 48:151–159

    Article  CAS  Google Scholar 

  • Xiao L (2010) Molecular epidemiology of cryptosporidiosis: an update. Exp Parasitol 124:80–89

    Article  PubMed  CAS  Google Scholar 

  • Xiao L, Herd RP, Bowman GL (1994) Prevalence of Cryptosporidium and Giardia infections on two Ohio pig farms with different management systems. Vet Parasitol 52:331–336

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Xiao L, Bern C, Arrowood M, Sulaiman I, Zhou L, Kawai V, Vivar A, Lal AA, Gilman RH (2002) Identification of the Cryptosporidium pig genotype in a human patient. J Infec Dis 185:1846–1848

    Article  Google Scholar 

  • Xiao L, Lal AA, Jiang J (2004) Detection and differentiation of Cryptosporidium oocysts in water by PCR-RFLP. Meth Molec Biol 268:163–176

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Xiao S, An W, Chen Z, Zhang D, Yu J, Yang M (2012) Occurrences and genotypes of Cryptosporidium oocysts in river network of southern-eastern China. Parasitol Res 110:1701–1709

    Article  PubMed  Google Scholar 

  • Yatswako S, Faleke OO, Gulumbe ML, Daneji AI (2007) Cryptosporidium oocysts and Balantidium coli cysts in pigs reared semi-intensively in Zuru, Nigeria. Pak J Biol Sci 10:3435–3439

    Article  PubMed  CAS  Google Scholar 

  • Zintl A, Neville D, Maguire D, Fanning S, Mulcahy G, Smith HV, De Waal T (2007) Prevalence of Cryptosporidium species in intensively farmed pigs in Ireland. Parasitology 134:1575–1582

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This study was funded by projects of the Ministry of Education, Youth and Sports of the Czech Republic (LH11061 and MSM 6007665806) and project of the Grant Agency of University of South Bohemia (022/2010/Z). The authors thank to all farmers involved in the project for providing data and biology material for our research. The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.

Author information

Authors and Affiliations

  1. Faculty of Agriculture, University of South Bohemia in České Budějovice, Studentská 13, 370 05, České Budějovice, Czech Republic

    Karel Němejc, Naděžda Kernerová & Martin Kváč

  2. Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, v.v.i., Branišovská 31, 370 05, České Budějovice, Czech Republic

    Bohumil Sak, Dana Květoňová & Martin Kváč

  3. Faculty of Economics, University of South Bohemia in České Budějovice, Studentská 13, 370 05, České Budějovice, Czech Republic

    Michael Rost

  4. Division of Parasitic Diseases, Centers for Disease Control and Prevention, Atlanta, GA, USA

    Vitaliano A. Cama

Authors
  1. Karel Němejc
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bohumil Sak
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dana Květoňová
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Naděžda Kernerová
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michael Rost
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Vitaliano A. Cama
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Martin Kváč
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin Kváč.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Němejc, K., Sak, B., Květoňová, D. et al. Occurrence of Cryptosporidium suis and Cryptosporidium scrofarum on commercial swine farms in the Czech Republic and its associations with age and husbandry practices. Parasitol Res 112, 1143–1154 (2013). https://doi.org/10.1007/s00436-012-3244-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-012-3244-8

Keywords

Search

Navigation