Hostname: page-component-77c89778f8-m42fx Total loading time: 0 Render date: 2024-07-18T11:48:40.496Z Has data issue: false hasContentIssue false
  • English
  • Français

Shedding of Cryptosporidium in calves and dams: evidence of re-infection and shedding of different gp60 subtypes

Published online by Cambridge University Press:  22 July 2019

Sarah Thomson Open the ORCID record for Sarah Thomson [Opens in a new window] ,
Elisabeth A. Innes ,
Nicholas N. Jonsson  and
Frank Katzer
Sarah Thomson
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Edinburgh, EH26 0PZ, UK College of Medical, Veterinary and Life Sciences, University of Glasgow, 464 Bearsden Rd, Glasgow G61 1QH, UK
Elisabeth A. Innes
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Edinburgh, EH26 0PZ, UK
Nicholas N. Jonsson
Affiliation:
College of Medical, Veterinary and Life Sciences, University of Glasgow, 464 Bearsden Rd, Glasgow G61 1QH, UK
Frank Katzer*
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Edinburgh, EH26 0PZ, UK
*
Author for correspondence: Frank Katzer, E-mail: frank.katzer@moredun.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

One of the most common causes of calf diarrhoea is the parasite Cryptosporidium parvum. Two longitudinal studies were carried out on a dairy farm Scotland to determine the prevalence of Cryptosporidium species and subtypes in a group of calves and to determine whether dams were a possible source of calfhood infection. Fecal samples were collected from 25 calves from birth to 12 months in the first year. In the second year, fecal samples were collected from pregnant cows (n = 29) and their calves (n = 30) from birth to 6 months. The samples were tested for Cryptosporidium and speciated. Cryptosporidium parvum-positive samples were subtyped by GP60 fragment analysis. All calves in both studies shed Cryptosporidium during the study period. Cryptosporidium parvum was the predominant species detected in calves ⩽6 weeks of age and at 6 months of age, C. bovis and C. ryanae were detected in calves older than 4 weeks of age but ⩽6 months of age. The prevalence of Cryptosporidium was higher in younger animals than in older animals. GP60 subtyping revealed two subtypes in calves on this farm (IIaA15G2R1 and IIaA19G2R1) that differed in frequency by age. Adult cattle also shed C. parvum, of four gp60 genotypes.

Keywords

C. parvumdam-calf transmissionGP60 subtype
Type
Research Article
Information
Parasitology , Volume 146 , Issue 11 , September 2019 , pp. 1404 - 1413
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, BC (1987) Abomasal cryptosporidiosis in cattle. Veterinary Pathology 24, 235–238.Google Scholar
APHA and SRUC (2014) Veterinary Investigational Diagnosis Analysis (VIDA) Report. https://www.gov.uk/government/publications/veterinary-investigation-diagnosis-analysis. (Accessed 3 July 2019)Google Scholar
Atwill, ER and Pereira, MG (2003) Lack of detectable shedding of Cryptosporidium parvum oocysts by periparturient dairy cattle. Journal of Parasitology 89, 1234–1236. https://doi.org/10.1645/GE-3192RN.Google Scholar
Atwill, ER, Harp, JA, Jones, T, Jardon, PW, Checel, S and Zylstra, M (1998) Evaluation of periparturient dairy cows and contact surfaces as a reservoir of Cryptosporidium parvum for calfhood infection. American Journal of Veterinary Research 59, 1116–1121.Google Scholar
Brook, EJ, Christley, RM, French, NP and Hart, CA (2008) Detection of Cryptosporidium oocysts in fresh and frozen cattle faeces: comparison of three methods. Letters in Applied Microbiology 46, 26–31. https://doi.org/10.1111/j.1472-765X.2007.02257.x.Google Scholar
Brook, EJ, Anthony, HC, French, NP and Christley, RM (2009) Molecular epidemiology of Cryptosporidium subtypes in cattle in England. Veterinary Journal 179, 378–382. https://doi.org/10.1016/j.tvjl.2007.10.023.Google Scholar
Burrells, A, Bartley, PM, Zimmer, IA, Roy, S, Kitchener, AC, Meredith, A, Wright, SE, Innes, EA and Katzer, F (2013) Evidence of the three main clonal Toxoplasma gondii lineages from wild mammalian carnivores in the UK Parasitology, 140, 1–9. https://doi.org/10.1017/S0031182013001169.Google Scholar
Cai, M, Guo, Y, Pan, B, Li, N, Wang, X, Tang, C, Feng, Y and Xiao, L (2017) Longitudinal monitoring of Cryptosporidium species in pre-weaned dairy calves on five farms in Shanghai, China. Veterinary Parasitology 241, 14–19. https://doi.org/10.1016/j.vetpar.2017.05.005.Google Scholar
Carpenter, C, Fayer, R, Trout, J and Beach, MJ (1999) Chlorine disinfection of recreational water for Cryptosporidium parvum. Emerging Infectious Diseases 5, 579–584.Google Scholar
Chalmers, RM and Davies, AP (2010) Minireview: clinical cryptosporidiosis. Experimental Parasitology 124, 138–146. https://doi.org/10.1016/j.exppara.2009.02.003.Google Scholar
Chalmers, RM and Giles, M (2010) Zoonotic cryptosporidiosis in the UK – challenges for control. Journal of Applied Microbiology 109, 1487–1497. https://doi.org/10.1111/j.1365-2672.2010.04764.x.Google Scholar
Chalmers, RM and Katzer, F (2013) Looking for Cryptosporidium: the application of advances in detection and diagnosis. Trends in Parasitology 29, 237–251. https://doi.org/10.1016/j.pt.2013.03.001.Google Scholar
Chalmers, RM, Smith, RP, Hadfield, SJ, Elwin, K and Giles, M (2011a) Zoonotic linkage and variation in Cryptosporidium parvum from patients in the United Kingdom. Parasitology Research 108, 1321. https://doi.org/10.1007/s00436-010-2199-x.Google Scholar
Chalmers, RM, Smith, R, Elwin, K, Clifton-Hadley, FA and Giles, M (2011b) Epidemiology of anthroponotic and zoonotic human cryptosporidiosis in England and Wales, 2004–2006. Epidemiology and Infection 139, 700–712.Google Scholar
Couto, MC, Lima, MD and Bomfim, TC (2013) New Cryptosporidium parvum subtypes of IIa subfamily in dairy calves from Brazil. Acta Tropica 130C, 117–122. https://doi.org/10.1016/j.actatropica.2013.11.002.Google Scholar
De Graaf, DC, Vanopdenbosch, E, Ortega-Mora, LM, Abbassi, H and Peeters, JE (1999) A review of the importance of cryptosporidiosis in farm animals. International Journal for Parasitology 29, 1269–1287.Google Scholar
Esteban, E and Anderson, BC (1995) Cryptosporidium muris: prevalence, persistency, and detrimental effect on milk production in a drylot dairy. Journal of Dairy Science 78, 1068–1072. https://doi.org/10.3168/jds.S0022-0302(95)76723-6.Google Scholar
Fayer, R, Santin, M and Trout, JM (2008) Cryptosporidium ryanae n. sp. (Apicomplexa: Cryptosporidiidae) in cattle (Bos taurus). Veterinary Parasitology 156, 191–198. https://doi.org/10.1016/j.vetpar.2008.05.024.Google Scholar
Fayer, R, Santin, M and Dargatz, D (2010) Species of Cryptosporidium detected in weaned cattle on cow-calf operations in the United States. Veterinary Parasitology 170, 187–192. https://doi.org/10.1016/j.vetpar.2010.02.040.Google Scholar
Fayer, R (2010) Taxonomy and species delimitation in Cryptosporidium. Experimental Parasitology 124, 90–97. https://doi.org/10.1016/j.exppara.2009.03.005.Google Scholar
Feng, Y, Alderisio, KA, Yang, W, Blancero, LA, Kuhne, WG, Nadareski, CA, Reid, M and Xiao, L (2007) Cryptosporidium genotypes in wildlife from a New York watershed. Applied Environmental Microbiology 73, 6475–6483. https://doi.org/10.1128/AEM.01034-07.Google Scholar
Follet, J, Guyot, K, Leruste, H, Follet-Dumoulin, A, Hammouma-Ghelboun, O, Certad, G, Dei-Cas, E and Halama, P (2011) Cryptosporidium infection in a veal calf cohort in France: molecular characterization of species in a longitudinal study. Veterinary Research 42, 116. https://doi.org/10.1186/1297-9716-42-116.Google Scholar
Grinberg, A, Biggs, PJ, Dukkipati, VS and George, TT (2013) Extensive intra-host genetic diversity uncovered in Cryptosporidium parvum using Next Generation Sequencing. Infection, Genetics and Evolution 15, 18–24. https://doi.org/10.1016/j.meegid.2012.08.017.Google Scholar
Gunn, GJ and Stott, AW (1997) A comparison of economic losses due to calf enteritis and calf pneumonia in Northern Scotland. Epidémiologie et santé animale, 31–32.Google Scholar
Gong, C, Cao, XF, Deng, L, Li, W, Huang, XM, Lan, JC, Xiao, QC, Zhang, ZJ, Feng, F, Zhang, Y, Wang, WB, Guo, P, Wu, KJ and Peng, GN (2017) Epidemiology of Cryptosporidium infection in cattle in China: a review. Parasite 24, 1.Google Scholar
Gormley, FJ, Little, CL, Chalmers, RM, Rawal, N and Adak, GK (2011) Zoonotic cryptosporidiosis from petting farms, England and Wales, 1992–2009. Emerging Infectious Diseases 17, 151–152.Google Scholar
Hijjawi, N, Mukbel, R, Yang, R and Ryan, U (2016) Genetic characterization of Cryptosporidium in animal and human isolates from Jordan. Veterinary Parasitology 228, 116–120. https://doi.org/10.1016/j.vetpar.2016.08.015.Google Scholar
Huetink, RE, van der Giessen, JW, Noordhuizen, JP and Ploeger, HW (2001) Epidemiology of Cryptosporidium spp. and Giardia duodenalis on a dairy farm. Veterinary Parasitology 102, 53–67. https://doi.org/10.1016/S0304-4017(01)00514-3.Google Scholar
Imre, K and Darabus, G (2011) Distribution of Cryptosporidium species, genotypes and C. parvum subtypes in cattle in European countries. Scientia Parasitologica 12, 1–9.Google Scholar
Jenkins, M, Trout, J, Higgins, J, Dorsch, M, Veal, D and Fayer, R (2002) Comparison of tests for viable and infectious Cryptosporidium parvum oocysts. Parasitology Research 89, 1–5. https://doi.org/10.1007/s00436-002-0720-6.Google Scholar
Klein, P, Kleinova, T, Volek, Z and Simunek, J (2008) Effect of Cryptosporidium parvum infection on the absorptive capacity and paracellular permeability of the small intestine in neonatal calves. Veterinary Parasitology 152, 53–59. https://doi.org/10.1016/j.vetpar.2007.11.020.Google Scholar
Kvac, M, Hromadova, N, Kvetonova, D, Rost, M and 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. Veterinary Parasitology 177, 378–382. https://doi.org/10.1016/j.vetpar.2010.11.048.Google Scholar
Langkjaer, RB, Vigre, H, Enemark, HL and Maddox-Hyttel, C (2007) Molecular and phylogenetic characterization of Cryptosporidium and Giardia from pigs and cattle in Denmark. Parasitology 134, 339–350. https://doi.org/10.1017/S0031182006001533.Google Scholar
Lorenzo Lorenzo, MJ, Ares-Mazas, E and Villacorta Martinez dM, I (1993) Detection of oocysts and IgG antibodies to Cryptosporidium parvum in asymptomatic adult cattle. Veterinary Parasitology 47, 9–15. https://doi.org/10.1016/0304-4017(93)90171-I.Google Scholar
MSD Animal Health Data Sheet (2012) http://www.noahcompendium.co.uk/?id=-454813&fromsearch=true#iosfirsthighlight (Accessed 3rd July 2019).Google Scholar
Nydam, DV, Wade, SE, Schaaf, SL and Mohammed, HO (2001) Number of Cryptosporidium parvum oocysts or Giardia spp cysts shed by dairy calves after natural infection. American Journal of Veterinary Research 62, 1612–1615.Google Scholar
R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/ (Accessed 3 July 2019).Google Scholar
Ralston, B, Thompson, RC, Pethick, D, McAllister, TA and Olson, ME (2010) Cryptosporidium andersoni in Western Australian feedlot cattle. Australian Veterinary Journal 88, 458–460.Google Scholar
Rieux, A, Chartier, C, Pors, I, Delafosse, A and Paraud, C (2013 a) Molecular characterization of Cryptosporidium isolates from high-excreting young dairy calves in dairy cattle herds in Western France. Parasitology Research 112, 3423–3431. https://doi.org/10.1007/s00436-013-3520-2.Google Scholar
Rieux, A, Paraud, C, Pors, I and Chartier, C (2013 b) Molecular characterization of Cryptosporidium isolates from pre-weaned calves in western France in relation to age. Veterinary Parasitology 197, 7–12. https://doi.org/10.1016/j.vetpar.2013.05.001.Google Scholar
Robertson, LJ, Campbell, A and Smith, HV (1992) Survival of Cryptosporidium parvum oocysts under various environmental pressures. Applied Environmental Microbiology 58, 3494–3500.Google Scholar
Santin, M, Trout, JM, Xiao, L, Zhou, L, Greiner, E and Fayer, R (2004) Prevalence and age-related variation of Cryptosporidium species and genotypes in dairy calves. Veterinary Parasitology 122, 103–117. https://doi.org/10.1016/j.vetpar.2004.03.020.Google Scholar
Santin, M, Trout, JM and Fayer, R (2008) A longitudinal study of cryptosporidiosis in dairy cattle from birth to 2 years of age. Veterinary Parasitology 155, 15–23. https://doi.org/10.1016/j.vetpar.2008.04.018.Google Scholar
Silverlas, C and Blanco-Penedo, I (2013) Cryptosporidium spp. in calves and cows from organic and conventional dairy herds. Epidemiology and Infection 141, 529–539. https://doi.org/10.1017/S0950268812000830.Google Scholar
Silverlas, C, Naslund, K, Bjorkman, C and Mattsson, JG (2010) Molecular characterisation of Cryptosporidium isolates from Swedish dairy cattle in relation to age, diarrhoea and region. Veterinary Parasitology 169, 289–295. https://doi.org/10.1016/j.vetpar.2010.01.003.Google Scholar
Smith, RP, Clifton-Hadley, FA, Cheney, T and Giles, M (2014) Prevalence and molecular typing of Cryptosporidium in dairy cattle in England and Wales and examination of potential on-farm transmission routes. Veterinary Parasitology 204, 111–119. https://doi.org/10.1016/j.vetpar.2014.05.022.Google Scholar
Sulaiman, IM, Hira, PR, Zhou, L, Al-Ali, FM, Al-Shelahi, FA, Shweiki, HM, Iqbal, J, Khalid, N and Xiao, L (2005) Unique endemicity of cryptosporidiosis in children in Kuwait. Journal of Clinical Microbiology 43, 2805–2809. https://doi.org/10.1128/JCM.43.6.2805-2809.2005.Google Scholar
Sweeny, JPA, Ryan, UM, Robertson, ID, Yang, R, Bell, K and Jacobson, C (2011a) Longitudinal investigation of protozoan parasites in meat lamb farms in southern Western Australia. Preventive Veterinary Medicine 101, 192–203. https://doi.org/10.1016/j.prevetmed.2011.05.016.Google Scholar
Sweeny, JPA, Ryan, UM, Robertson, ID and Jacobson, C (2011b) Cryptosporidium and Giardia associated with reduced lamb carcase productivity. Veterinary Parasitology 182, 127–139. https://doi.org/10.1016/j.vetpar.2011.05.050.Google Scholar
Thomson, S, Innes, EA, Jonsson, NN and Katzer, F (2016) A multiplex PCR test to identify four common cattle-adapted Cryptosporidium species. Parasitology Open 2, 9. https://doi.org/10.1017/pao.2016.2.Google Scholar
Thomson, S, Hamilton, CA, Hope, JC, Katzer, F, Mabbott, NA, Morrison, LJ and Innes, EA (2017) Bovine cryptosporidiosis: impact, host-parasite interaction and control strategies. Veterinary Research 48, 42. https://doi.org/10.1186/s13567-017-0447-0.Google Scholar
Tzipori, S and Ward, H (2002) Cryptosporidiosis: biology, pathogenesis and disease. Microbes and Infection 4, 1047–1058.Google Scholar
Tzipori, S, Smith, M, Halpin, C, Angus, KW, Sherwood, D and Campbell, I (1983) Experimental cryptosporidiosis in calves: clinical manifestations and pathological findings. Veterinary Record 112, 116–120.Google Scholar
Weir, SC, Pokorny, NJ, Carreno, RA, Trevors, JT and Lee, H (2002) Efficacy of common laboratory disinfectants on the infectivity of Cryptosporidium parvum oocysts in cell culture. Applied Environmental Microbiology 68, 2576–2579.Google Scholar
Wells, B, Shaw, H, Hotchkiss, E, Gilray, J, Ayton, R, Green, J, Katzer, F, Wells, A and Innes, E (2015) Prevalence, species identification and genotyping Cryptosporidium from livestock and deer in a catchment in the Cairngorms with a history of a contaminated public water supply. Parasites and Vectors 8, 66. https://dx.doi.org/10.1186%2Fs13071-015-0684-x.Google Scholar
Wells, B, Thomson, S, Ensor, H, Innes, EA and Katzer, F (2016) Development of a sensitive method to extract and detect low numbers of Cryptosporidium oocysts from adult cattle faecal samples. Veterinary Parasitology 227, 26–29. https://doi.org/10.1016/j.vetpar.2016.07.018.Google Scholar
Xiao, L and Feng, Y (2009) Zoonotic cryptosporidiosis. FEMS Immunology and Medical Microbiology 52, 309–323. https://dx.doi.org/10.1111/j.1574-695X.2008.00377.x.Google Scholar
Xiao, L, Escalante, L, Yang, C, Sulaiman, I, Escalante, AA, Montali, RJ, Fayer, R and Lal, AA (1999) Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Applied and Environmental Microbiology 65, 1578–1583.Google Scholar
Zahedi, A, Paparini, A, Jian, F, Robertson, I and Ryan, U (2016) Public health significance of zoonotic Cryptosporidium species in wildlife: critical insights into better drinking water management. International Journal for Parasitology: Parasites and Wildlife 5, 88–109. https://dx.doi.org/10.1016%2Fj.ijppaw.2015.12.001.Google Scholar