Advertisement

Parasitology Research

, Volume 118, Issue 5, pp 1549–1558 | Cite as

Distribution of Cryptosporidium parvum gp60 subtypes in calf herds of Saxony, Germany

  • I. HolzhausenEmail author
  • M. Lendner
  • F. Göhring
  • I. Steinhöfel
  • A. Daugschies
Protozoology - Original Paper

Abstract

Cryptosporidiosis is a common protozoan parasitic infection that causes diarrhoea in neonatal calves. The high shedding of environmentally resistant oocysts facilitates outbreaks of cryptosporidiosis in humans. In total, 58 farms (512 calves) in Germany (Saxony and Brandenburg) were visited three times each. Faecal samples of pre-weaned calves were microscopically examined for oocysts of Cryptosporidium spp. using Heine staining and were scored with regard to their consistency. Overall, 88.9% of calves tested microscopically positive for Cryptosporidium spp. in at least one sample, and the excretion of oocysts was significantly (P < 0.01) associated with a higher faecal score (diarrhoea). After DNA extraction from pooled farm isolates, 47 samples were successfully subtyped by sequence analysis of the 60 kDa glycoprotein gene (gp60). All isolates belonged to subtype family IIa. IIaA15G2R1 was the most common subtype (present on 66% of the farms), followed by IIaA16G3R1 (13%). Subtypes IIaA14G1R1, IIaA14G2R1, IIaA1612R1, IIaA16G2R1, IIaA17G1R1, IIaA17G2R1, IIaA17G4R1 and IIaA19G2R1 were found sporadically. This is the first description of gp60 subtype IIaA17G4R1 in cattle in Germany.

Keywords

Cryptosporidium Calf Germany gp60 subtypes 

Notes

Acknowledgements

The authors would like to thank all members of the Institute of Parasitology, University of Leipzig, for technical and practical support and all employees of the “Core Unit DNA technologies”, University of Leipzig, for sequencing the gp60 nested PCR products.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of animals were followed.

References

  1. 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 CrossRefGoogle Scholar
  2. 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 CrossRefGoogle Scholar
  3. Alves M, Xiao L, Antunes F, Matos O (2006) Distribution of Cryptosporidium subtypes in humans and domestic and wild ruminants in Portugal. Parasitol Res 99:287-292.  https://doi.org/10.1007/s00436-006-0164-5 CrossRefGoogle Scholar
  4. Amer S, Honma H, Ikarashi M, Tada C, Fukuda Y, Suyama Y, Nakai Y (2010) Cryptosporidium genotypes and subtypes in dairy calves in Egypt. Vet Parasitol 169:382-386.  https://doi.org/10.1016/j.vetpar.2010.01.017 CrossRefGoogle Scholar
  5. Bacon AL, Farrington SM, Dunlop MG (2000) Sequence interruptions confer differential stability at microsatellite alleles in mismatch repair-deficient cells. Hum Mol Genet 9:2707–2713.  https://doi.org/10.1093/hmg/9.18.2707
  6. Bartels CJM, Holzhauer M, Jorritsma R, Swart WAJM, Lam TJGM (2010) Prevalence, prediction and risk factors of enteropathogens in normal and non-normal faeces of young Dutch dairy calves. Prev Vet Med 93:162–169.  https://doi.org/10.1016/j.prevetmed.2009.09.020 CrossRefGoogle Scholar
  7. Berahmat R, Spotin A, Ahmadpour E, Mahami-Oskouei M, Rezamand A, Aminisani N, Ghojazadeh M, Ghoyounchi R, Mikaeili-Galeh T (2017) Human cryptosporidiosis in Iran: a systematic review and meta-analysis. Parasitol Res 116:1111-1128.  https://doi.org/10.1007/s00436-017-5376-3 CrossRefGoogle Scholar
  8. Broglia A, Reckinger S, Cacció SM, Nöckler K (2008) Distribution of Cryptosporidium parvum subtypes in calves in Germany. Vet Parasitol 154:8-13.  https://doi.org/10.1016/j.vetpar.2008.02.029 CrossRefGoogle Scholar
  9. Brook EJ, Anthony Hart C, French NP, Christley RM (2009) Molecular epidemiology of Cryptosporidium subtypes in cattle in England. Vet J 179:378-382.  https://doi.org/10.1016/j.tvjl.2007.10.023 CrossRefGoogle Scholar
  10. 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.  https://doi.org/10.1016/j.ejop.2014.07.002 CrossRefGoogle Scholar
  11. Chalmers RM, Elwin K, Reilly WJ, Irvine H, Thomas AL, Hunter PR (2002) Cryptosporidium in farmed animals: the detection of a novel isolate in sheep. Int J Parasitol 32:21-26CrossRefGoogle Scholar
  12. Cho Y, Han J, Wang C, Cooper V, Schwartz K, Engelken T, Yoon K (2013) Case-control study of microbiological etiology associated with calf diarrhea. Vet Microbiol 166:375-385.  https://doi.org/10.1016/j.vetmic.2013.07.001. CrossRefGoogle Scholar
  13. Čondlová Š, 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.  https://doi.org/10.1016/j.ejop.2017.12.006 CrossRefGoogle Scholar
  14. DeSilva MB, Schafer S, Kendall Scott M, Robinson B, Hills A, Buser GL, Salis K, Gargano J, Yoder J, Hill V, Xiao L, Roellig D, Hedberg K (2016) Communitywide cryptosporidiosis outbreak associated with a surface water-supplied municipal water system--Baker City, Oregon, 2013. Epidemiol Infect 144:274-284.  https://doi.org/10.1017/S0950268815001831 CrossRefGoogle Scholar
  15. Díaz P, Varcasia A, Pipia AP, Tamponi C, Sanna G, Prieto A, Ruiu A, Spissu P, Díez-Baños P, Morrondo P, Scala A (2018) Molecular characterisation and risk factor analysis of Cryptosporidium spp. in calves from Italy. Parasitol Res 117:3081-3090.  https://doi.org/10.1007/s00436-018-6000-x CrossRefGoogle Scholar
  16. Fayer R, Xiao L (2008) Cryptosporidium and cryptosporidiosis. CRC Press/Taylor & Francis, Boca RatonGoogle Scholar
  17. Fayer R, Santín M, Trout JM, Greiner E (2006) Prevalence of species and genotypes of Cryptosporidium found in 1-2-year-old dairy cattle in the eastern United States. Vet Parasitol 135:105-112.  https://doi.org/10.1016/j.vetpar.2005.08.003 CrossRefGoogle Scholar
  18. Fayer R, Santín M, Trout JM (2007) Prevalence of Cryptosporidium species and genotypes in mature dairy cattle on farms in eastern United States compared with younger cattle from the same locations. Vet Parasitol 145:260-266.  https://doi.org/10.1016/j.vetpar.2006.12.009 CrossRefGoogle Scholar
  19. Feng Y, Ortega Y, He G, Das P, Xu M, Zhang X, Fayer R, Gatei W, Cama V, Xiao L (2007) Wide geographic distribution of Cryptosporidium bovis and the deer-like genotype in bovines. Vet Parasitol 144:1-9.  https://doi.org/10.1016/j.vetpar.2006.10.001 CrossRefGoogle Scholar
  20. Feng Y, Ryan UM, Xiao L (2018) Genetic diversity and population structure of Cryptosporidium. Trends Parasitol 34:997-1011.  https://doi.org/10.1016/j.pt.2018.07.009 CrossRefGoogle Scholar
  21. Follet J, Guyot K, Leruste H, Follet-Dumoulin A, Hammouma-Ghelboun O, Certad G, Dei-Cas E, Halama P (2011) Cryptosporidium infection in a veal calf cohort in France: molecular characterization of species in a longitudinal study. Vet Res 42:116.  https://doi.org/10.1186/1297-9716-42-116 CrossRefGoogle Scholar
  22. Garcia-R JC, French N, Pita A, Velathanthiri N, Shrestha R, Hayman D (2017) Local and global genetic diversity of protozoan parasites: spatial distribution of Cryptosporidium and Giardia genotypes. PLoS Negl Trop Dis 11:e0005736.  https://doi.org/10.1371/journal.pntd.0005736 CrossRefGoogle Scholar
  23. Gargala G, Razakandrainibe R, Costa D, Leméteil D, Dumant Forest C (2017) La cryptosporidiose, une cause de diarrhée aiguë. Revue de la littérature et étude rétrospective des cas dans le département de pédiatrie du CHU de Rouen. Arch Pediatr 24:1344-1349.  https://doi.org/10.1016/j.arcped.2017.10.002 CrossRefGoogle Scholar
  24. Geurden T, Berkvens D, Martens C, Casaert S, Vercruysse JClaerebout E (2007) Molecular epidemiology with subtype analysis of Cryptosporidium in calves in Belgium. Parasitology 134:1981-1987.  https://doi.org/10.1017/S0031182007003460 CrossRefGoogle Scholar
  25. Gillhuber J, Rügamer D, Pfister K, Scheuerle MC (2014) Giardiosis and other enteropathogenic infections: a study on diarrhoeic calves in Southern Germany. BMC Res Notes 7:112.  https://doi.org/10.1186/1756-0500-7-112 CrossRefGoogle Scholar
  26. Glaberman S, Moore JE, Lowery CJ, Chalmers RM, Sulaiman I, Elwin K, Rooney PJ, Millar BC, Dooley JSG, Lal AA, Xiao L (2002) Three drinking-water-associated cryptosporidiosis outbreaks, Northern Ireland. Emerging Infect Dis 8:631-633.  https://doi.org/10.3201/eid0806.010368 CrossRefGoogle Scholar
  27. Göhring F, Möller-Holtkamp P, Daugschies A, Lendner M (2014) Untersuchungen zur Häufigkeit von Cryptosporidium parvum bei Durchfallkälbern und der Einfluss von Koinfektionen auf das Krankheitsgeschehen. Tierärztliche Umschau 4:112-120Google Scholar
  28. Hamnes IS, Gjerde B, Robertson L (2006) Prevalence of Giardia and Cryptosporidium in dairy calves in three areas of Norway. Vet Parasitol 140:204-216.  https://doi.org/10.1016/j.vetpar.2006.03.024 CrossRefGoogle Scholar
  29. Heckler RP, Borges DGL, Bacha FB, Onizuka MKV, Teruya LS, Neves JPL, Leal CRB, Lemos d, Amaral RA, Meireles MV, Borges FA (2015) First genetic identification of Cryptosporidium parvum subtype IIaA14G2R1in beef cattle in Brazil. Prev Vet Med 121:391-394.  https://doi.org/10.1016/j.prevetmed.2015.08.016 CrossRefGoogle Scholar
  30. Heine J (1982) Eine einfache Nachweismethode für Kryptosporidien im Kot. Zentralbl Veterinarmed Reihe B 29:324-327CrossRefGoogle Scholar
  31. 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.  https://doi.org/10.1016/j.vetpar.2016.08.015 CrossRefGoogle Scholar
  32. Horčičková M, Čondlová Š, 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 146:1-14.  https://doi.org/10.1017/S0031182018001142 Google Scholar
  33. Hunter PR, Thompson RCA (2005) The zoonotic transmission of Giardia and Cryptosporidium. Int J Parasitol 35:1181-1190.  https://doi.org/10.1016/j.ijpara.2005.07.009 CrossRefGoogle Scholar
  34. Hunter PR, Hughes S, Woodhouse S, Syed Q, Verlander NQ, Chalmers RM, Morgan K, Nichols G, Beeching N, Osborn K (2004) Sporadic cryptosporidiosis case-control study with genotyping. Emerging Infect Dis 10:1241-1249.  https://doi.org/10.3201/eid1007.030582 CrossRefGoogle Scholar
  35. Imre K, Lobo LM, Matos O, Popescu C, Genchi C, Dărăbuş G (2011) Molecular characterisation of Cryptosporidium isolates from pre-weaned calves in Romania: is there an actual risk of zoonotic infections? Vet Parasitol 181:321-324.  https://doi.org/10.1016/j.vetpar.2011.04.042 CrossRefGoogle Scholar
  36. Izzo MM, Kirkland PD, Mohler VL, Perkins NR, Gunn AA, House JK (2011) Prevalence of major enteric pathogens in Australian diary calves with diarrhea. Aust Vet 89:167–173.  https://doi.org/10.1111/j.1751-0813.2011.00692.x
  37. Ježková J, Horčičková M, Hlásková L, Sak B, Květoňová D, Novák J, Hofmannová L, McEvoy J, Kváč M (2016) Cryptosporidium testudinis sp. n., Cryptosporidium ducismarci Traversa, 2010 and Cryptosporidium tortoise genotype III (Apicomplexa: Cryptosporidiidae) in tortoises. Folia Parasitol 63.  https://doi.org/10.14411/fp.2016.035
  38. Joachim A, Eckert E, Petry F, Bialek R, Daugschies A (2003a) Comparison of viability assays for Cryptosporidium parvum oocysts after disinfection. Vet Parasitol 111:47-57CrossRefGoogle Scholar
  39. Joachim A, Krull T, Schwarzkopf J, Daugschies A (2003b) Prevalence and control of bovine cryptosporidiosis in German dairy herds. Vet Parasitol 112:277-288.  https://doi.org/10.1016/S0304-4017(03)00006-2 CrossRefGoogle Scholar
  40. Kaupke A, Rzeżutka A (2015) Emergence of novel subtypes of Cryptosporidium parvum in calves in Poland. Parasitol Res 114:4709-4716.  https://doi.org/10.1007/s00436-015-4719-1 CrossRefGoogle Scholar
  41. Khan A, Shaik JS, Grigg ME (2018) Genomics and molecular epidemiology of Cryptosporidium species. Acta Trop 184:1-14.  https://doi.org/10.1016/j.actatropica.2017.10.023. CrossRefGoogle Scholar
  42. Klintschar M, Wiegand P (2003) Polymerase slippage in relation to the uniformity of tetrameric repeat stretches. Forensic Sci Int 135:163-166.  https://doi.org/10.1016/S0379-0738(03)00201-9 CrossRefGoogle Scholar
  43. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque ASG, Zaidi AKM, Saha D, Alonso PL, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng JB, Omore R, Oundo JO, Hossain A, Das SK, Ahmed S, Qureshi S, Quadri F, Adegbola RA, Antonio M, Hossain MJ, Akinsola A, Mandomando I, Nhampossa T, Acácio S, Biswas K, O'Reilly CE, Mintz ED, Berkeley LY, Muhsen K, Sommerfelt H, Robins-Browne RM, Levine MM (2013) Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the global enteric multicenter study, GEMS). A prospective, case-control study. Lancet 382:209-222.  https://doi.org/10.1016/S0140-6736(13)60844-2 CrossRefGoogle Scholar
  44. Kváč M, Kouba M, Vítovec J (2006) Age-related and housing-dependence of Cryptosporidium infection of calves from dairy and beef herds in South Bohemia, Czech Republic. Vet Parasitol 137:202-209.  https://doi.org/10.1016/j.vetpar.2006.01.027 CrossRefGoogle Scholar
  45. Kváč M, Hromadová N, Květoňová D, Rost M, Sak B (2011) Molecular characterization of Cryptosporidium spp. in pre-weaned dairy calves in the Czech Republic: absence of C. ryanae and management-associated distribution of C. andersoni, C. bovis and C. parvum subtypes. Vet Parasitol 177:378-382.  https://doi.org/10.1016/j.vetpar.2010.11.048 CrossRefGoogle Scholar
  46. Kváč M, Vlnatá G, Ježková J, Horčičková M, Konečný R, Hlásková L, McEvoy J, Sak B (2018) Cryptosporidium occultus sp. n. (Apicomplexa: Cryptosporidiidae) in rats. Eur J Protistol 63:96-104.  https://doi.org/10.1016/j.ejop.2018.02.001 CrossRefGoogle Scholar
  47. Leav BA, Mackay MR, Anyanwu A, O' Connor RM, Cevallos AM, Kindra G, Rollins NC, Bennish ML, Nelson RG, Ward HD (2002) Analysis of sequence diversity at the highly polymorphic Cpgp40/15 locus among Cryptosporidium isolates from human immunodeficiency virus-infected children in South Africa. Infect Immun 70:3881-3890.  https://doi.org/10.1128/IAI.70.7.3881-3890.2002 CrossRefGoogle Scholar
  48. Li F, Wang H, Zhang Z, Li J, Wang C, Zhao J, Hu S, Wang R, Zhang L, Wang M (2016) Prevalence and molecular characterization of Cryptosporidium spp. and Giardia duodenalis in dairy cattle in Beijing, China. Vet Parasitol 219:61-65.  https://doi.org/10.1016/j.vetpar.2016.01.023 CrossRefGoogle Scholar
  49. McKerr C, Adak GK, Nichols G, Gorton R, Chalmers RM, Kafatos G, Cosford P, Charlett A, Reacher M, Pollock KG, Alexander CL, Morton S (2015) An outbreak of Cryptosporidium parvum across England & Scotland Associated with consumption of fresh pre-cut salad leaves, May 2012. PLoS One 10:e0125955.  https://doi.org/10.1371/journal.pone.0125955 CrossRefGoogle Scholar
  50. Naguib D, El-Gohary AH, Roellig D, Mohamed AA, Arafat N, Wang Y, Feng Y, Xiao L (2018) Molecular characterization of Cryptosporidium spp. and Giardia duodenalis in children in Egypt. Parasit Vectors 11:403.  https://doi.org/10.1186/s13071-018-2981-7 CrossRefGoogle Scholar
  51. Ng J, Eastwood K, Durrheim D, Massey P, Walker B, Armson A, Ryan U (2008) Evidence supporting zoonotic transmission of Cryptosporidium in rural New South Wales. Exp Parasitol 119:192-195.  https://doi.org/10.1016/j.exppara.2008.01.010 CrossRefGoogle Scholar
  52. Plutzer J, Karanis P (2009) Genetic polymorphism in Cryptosporidium species: an update. Vet Parasitol 165:187-199.  https://doi.org/10.1016/j.vetpar.2009.07.003 CrossRefGoogle Scholar
  53. Raue K, Heuer L, Böhm C, Wolken S, Epe C, Strube C (2017) 10-year parasitological examination results (2003 to 2012) of faecal samples from horses, ruminants, pigs, dogs, cats, rabbits and hedgehogs. Parasitol Res 116:3315-3330.  https://doi.org/10.1007/s00436-017-5646-0 CrossRefGoogle Scholar
  54. Rieux A, Chartier C, Pors I, Delafosse A, Paraud C (2013a) Molecular characterization of Cryptosporidium isolates from high-excreting young dairy calves in dairy cattle herds in Western France. Parasitol Res 112:3423-3431.  https://doi.org/10.1007/s00436-013-3520-2 CrossRefGoogle Scholar
  55. Rieux A, Chartier C, Pors I, Paraud C (2013b) Dynamics of excretion and molecular characterization of Cryptosporidium isolates in pre-weaned French beef calves. Vet Parasitol 195:169-172.  https://doi.org/10.1016/j.vetpar.2012.12.043 CrossRefGoogle Scholar
  56. Robertson B, Sinclair MI, Forbes AB, Veitch M, Kirk M, Cunliffe D, Willis J, Fairley CK (2002) Case-control studies of sporadic cryptosporidiosis in Melbourne and Adelaide, Australia. Epidemiol Infect 128.  https://doi.org/10.1017/S0950268802006933
  57. Roy SL, DeLong SM, Stenzel SA, Shiferaw B, Roberts JM, Khalakdina A, Marcus R, Segler SD, Shah DD, Thomas S, Vugia DJ, Zansky SM, Dietz V, Beach MJ (2004) Risk factors for sporadic cryptosporidiosis among immunocompetent persons in the United States from 1999 to 2001. J Clin Microbiol 42:2944-2951.  https://doi.org/10.1128/JCM.42.7.2944-2951.2004 CrossRefGoogle Scholar
  58. Ryan U, Paparini A, Monis P, Hijjawi N (2016) It's official - Cryptosporidium is a gregarine: what are the implications for the water industry? Water Res 105:305-313.  https://doi.org/10.1016/j.watres.2016.09.013 CrossRefGoogle Scholar
  59. Santín M, Trout JM, Xiao L, Zhou L, Greiner E, Fayer R (2004) Prevalence and age-related variation of Cryptosporidium species and genotypes in dairy calves. Vet Parasitol 122:103-117.  https://doi.org/10.1016/j.vetpar.2004.03.020 CrossRefGoogle Scholar
  60. 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.  https://doi.org/10.1016/j.vetpar.2008.04.018 CrossRefGoogle Scholar
  61. Shivley CB, Lombard JE, Urie NJ, Kopral CA, Santín M, Earleywine TJ, Olson JD, Garry FB (2018) Preweaned heifer management on US dairy operations: part VI. Factors associated with average daily gain in preweaned dairy heifer calves. J Dairy Sci 101:9245–9258.  https://doi.org/10.3168/jds.2017-14022
  62. Smith RP, Clifton-Hadley FA, Cheney T, Giles M (2014) Prevalence and molecular typing of Cryptosporidium in dairy cattle in England and Wales and examination of potential on-farm transmission routes. Vet Parasitol 204:111-119.  https://doi.org/10.1016/j.vetpar.2014.05.022 CrossRefGoogle Scholar
  63. Stensvold CR, Ethelberg S, Hansen L, Sahar S, Voldstedlund M, Kemp M, Hartmeyer GN, Otte E, Engsbro AL, Nielsen HV, Mølbak K (2015) Cryptosporidium infections in Denmark, 2010-2014. Dan Med J 62:A5086Google Scholar
  64. Strong WB, Gut J, Nelson RG (2000) Cloning and sequence analysis of a highly polymorphic Cryptosporidium parvum gene encoding a 60-kilodalton glycoprotein and characterization of its 15- and 45-kilodalton zoite surface antigen products. Infect Immun 68:4117-4134.  https://doi.org/10.1128/IAI.68.7.4117-4134.2000 CrossRefGoogle Scholar
  65. 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.  https://doi.org/10.1128/JCM.43.6.2805-2809.2005 CrossRefGoogle Scholar
  66. Taha S, Elmalik K, Bangoura B, Lendner M, Mossaad E, Daugschis A (2017) Molecular characterization of bovine Cryptosporidium isolated from diarrheic calves in the Sudan. Parasitol Res 110:2971-2979.  https://doi.org/10.1007/s00436-017-5606-8 CrossRefGoogle Scholar
  67. 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.  https://doi.org/10.1016/j.exppara.2016.06.014 CrossRefGoogle Scholar
  68. Thomson S, Hamilton CA, Hope JC, Katzer F, Mabbott NA, Morrison LJ, Innes EA (2017) Bovine cryptosporidiosis: impact, host-parasite interaction and control strategies. Vet Res 48:394.  https://doi.org/10.1186/s13567-017-0447-0 CrossRefGoogle Scholar
  69. Trotz-Williams LA, Jarvie BD, Martin SW, Leslie KE, Peregrine AS (2005) Prevalence of Cryptosporidium parvum infection in southwestern Ontario and its association with diarrhea in neonatal dairy calves. Can Vet J 46:349-351Google Scholar
  70. 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.  https://doi.org/10.1007/s00436-006-0157-4 CrossRefGoogle Scholar
  71. Valenzuela O, González-Díaz M, Garibay-Escobar A, Burgara-Estrella A, Cano M, Durazo M, Bernal RM, Hernandez J, Xiao L (2014) Molecular characterization of Cryptosporidium spp. in children from Mexico. PLoS One 9:e96128.  https://doi.org/10.1371/journal.pone.0096128 CrossRefGoogle Scholar
  72. Waldron LS, Dimeski B, Beggs PJ, Ferrari BC, Power ML (2011a) Molecular epidemiology, spatiotemporal analysis, and ecology of sporadic human cryptosporidiosis in Australia. Appl Environ Microbiol 77:7757-7765.  https://doi.org/10.1128/AEM.00615-11 CrossRefGoogle Scholar
  73. Waldron LS, Ferrari BC, Cheung-Kwok-Sang C, Beggs PJ, Stephens N, Power ML (2011b) Molecular epidemiology and spatial distribution of a waterborne cryptosporidiosis outbreak in Australia. Appl Environ Microbiol 77:7766-7771.  https://doi.org/10.1128/AEM.00616-11 CrossRefGoogle Scholar
  74. Waltner-Toews D, Martin SW, Meek AH (1986) The effect of early calfhood health status on survivorship and age at first calving. Can J Vet Res 50:314-317Google Scholar
  75. Weber SE, Lippuner C, Corti S, Deplazes P, Hässig M (2016) Klinische Epidemiologie der Kälber- Cryptosporidiose. Schweiz Arch Tierheilkd 158:341-350.  https://doi.org/10.17236/sat00062. CrossRefGoogle Scholar
  76. Wielinga PR, de VA, van der Goot, Tjeerd H, Mank T, Mars MH, Kortbeek LM, van der Giessen, Joke WB (2008) Molecular epidemiology of Cryptosporidium in humans and cattle in the Netherlands. Int J Parasitol 38:809-817.  https://doi.org/10.1016/j.ijpara.2007.10.014 CrossRefGoogle Scholar
  77. Windeyer MC, Leslie KE, Godden SM, Hodgins DC, Lissemore KD, LeBlanc SJ (2014) Factors associated with morbidity, mortality, and growth of dairy heifer calves up to 3 months of age. Prev Vet Med 113:231-240.  https://doi.org/10.1016/j.prevetmed.2013.10.019 CrossRefGoogle Scholar
  78. Xiao L (2010) Molecular epidemiology of cryptosporidiosis: an update. Exp Parasitol 124:80-89.  https://doi.org/10.1016/j.exppara.2009.03.018 CrossRefGoogle Scholar
  79. Xiao L, Feng Y (2017) Molecular epidemiologic tools for waterborne pathogens Cryptosporidium spp. and Giardia duodenalis. Food Waterborne Parasitol 8-9:14-32.  https://doi.org/10.1016/j.fawpar.2017.09.002 CrossRefGoogle Scholar
  80. Xiao L, Morgan UM, Limor J, Escalante A, Arrowood M, Shulaw W, Thompson RC, Fayer R, Lal AA (1999) Genetic diversity within Cryptosporidium parvum and related Cryptosporidium species. Appl Environ Microbiol 65:3386-3391Google Scholar
  81. Xiao L, Zhou L, Santin M, Yang W, Fayer R (2007) Distribution of Cryptosporidium parvum subtypes in calves in eastern United States. Parasitol Res 100:701-706.  https://doi.org/10.1007/s00436-006-0337-2 CrossRefGoogle Scholar
  82. Zahedi A, Durmic Z, Gofton AW, Kueh S, Austen J, Lawson M, Callahan L, Jardine J, Ryan U (2017a) Cryptosporidium homai n. sp. (Apicomplexa: Cryptosporidiiae) from the guinea pig (Cavia porcellus). Vet Parasitol 245:92-101.  https://doi.org/10.1016/j.vetpar.2017.08.014 CrossRefGoogle Scholar
  83. Zahedi A, Gofton AW, Jian F, Paparini A, Oskam C, Ball A, Robertson I, Ryan U (2017b) Next generation sequencing uncovers within-host differences in the genetic diversity of Cryptosporidium gp60 subtypes. Int J Parasitol 47:601-607.  https://doi.org/10.1016/j.ijpara.2017.03.003 CrossRefGoogle Scholar
  84. Zahedi A, Monis P, Gofton AW, Oskam CL, Ball A, Bath A, Bartkow M, Robertson I, Ryan U (2018) Cryptosporidium species and subtypes in animals inhabiting drinking water catchments in three states across Australia. Water Res 134:327-340.  https://doi.org/10.1016/j.watres.2018.02.005 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • I. Holzhausen
    • 1
    • 2
    Email author
  • M. Lendner
    • 1
  • F. Göhring
    • 1
    • 2
  • I. Steinhöfel
    • 3
  • A. Daugschies
    • 1
    • 2
  1. 1.Institute of Parasitology, Centre for Infectious DiseasesUniversity of LeipzigLeipzigGermany
  2. 2.Albrecht - Daniel - Thaer - Institute for Agricultural Sciences e.V.University of LeipzigLeipzigGermany
  3. 3.Saxon State Office for EnvironmentAgriculture and GeologyKöllitschGermany

Personalised recommendations