Hostname: page-component-76fb5796d-22dnz Total loading time: 0 Render date: 2024-04-25T07:38:57.175Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular characterization of Cryptosporidium parvum isolates from human cryptosporidiosis cases in Scotland

Published online by Cambridge University Press:  23 September 2014

A. P. DESHPANDE ,
B. L. JONES ,
L. CONNELLY ,
K. G. POLLOCK ,
S. BROWNLIE  and
C. L. ALEXANDER
A. P. DESHPANDE
Affiliation:
Clinical Microbiology, Greater Glasgow and Clyde NHS, Glasgow, UK
B. L. JONES
Affiliation:
Scottish Microbiology Reference Laboratories, Greater Glasgow and Clyde NHS, Level 5, New Lister Building, Glasgow Royal Infirmary, Alexandra Parade, Glasgow G31 2ER, UK
L. CONNELLY
Affiliation:
Scottish Microbiology Reference Laboratories, Greater Glasgow and Clyde NHS, Level 5, New Lister Building, Glasgow Royal Infirmary, Alexandra Parade, Glasgow G31 2ER, UK
K. G. POLLOCK
Affiliation:
Health Protection Scotland, NHS National Services Scotland, Glasgow, UK
S. BROWNLIE
Affiliation:
Health Protection Scotland, NHS National Services Scotland, Glasgow, UK
C. L. ALEXANDER*
Affiliation:
Scottish Microbiology Reference Laboratories, Greater Glasgow and Clyde NHS, Level 5, New Lister Building, Glasgow Royal Infirmary, Alexandra Parade, Glasgow G31 2ER, UK
*
*Corresponding author: Scottish Microbiology Reference Laboratories, Glasgow Scottish Parasite Diagnostic and Reference Section, Level 5, New Lister Building, Glasgow Royal Infirmary, Alexandra Parade, Glasgow G31 2ER. E-mail: Claire.Alexander@ggc.scot.nhs.uk
Get access Rights & Permissions [Opens in a new window]

Summary

Cryptosporidium parvum (C. parvum) is one of the most prevalent protozoan pathogens responsible for inducing human and animal disease worldwide. In this study, the glycoprotein-60 (gp60) subtyping tool was employed to assess the molecular diversity of C. parvum from human feces throughout Scotland during potential outbreaks. Over a 24-month period, microscopy analysis revealed 1139 positive feces containing Cryptosporidium species with 256 identified by molecular methods specifically as C. parvum. Cryptosporidium parvum was shown to be more prevalent in rural areas of Scotland and subtyping of 87 isolates demonstrated the predominant family as IIa, which occurred in 94% (n = 82) of isolates. The IIaA15G1R1 subtype was most common, being isolated from 47% (n = 41) of Scottish human cases. Non-IIa strains constituted a total of 5 isolates and included subtypes from the IIc, IId and IIg families. This information contributes significantly to existing knowledge and understanding of C. parvum subtypes in Scotland which is vital in assisting with the management of future local and national outbreaks.

Keywords

Cryptosporidium parvummoleculardiversitysubtypesScotlandgp60
Type
Research Article
Information
Parasitology , Volume 142 , Issue 2 , February 2015 , pp. 318 - 325
Check for updates
Copyright
Copyright © Cambridge University Press 2014 

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

REFERENCES

Abe, N., Matsubayashi, M., Kimata, I. and Iseki, M. (2006). Subgenotype analysis of Cryptosporidium parvum isolates from humans and animals in Japan using the 60-kDa glycoprotein gene sequences. Parasitology Research 99, 303–305.Google Scholar
Akiyoshi, D. E., Tumwine, J. K., Bakeera-Kitaka, S. and Tzipori, S. (2006). Subtype analysis of Cryptosporidium isolates from children in Uganda. Journal of Parasitology 92, 1097–1100.Google Scholar
Alves, M., Xiao, L., Sulaiman, I., Lal, A. A., Matos, O. and Antunes, F. (2003). Subgenotype analysis of Cryptosporidium isolates from humans, cattle and zoo ruminants in Portugal. Journal of Clinical Microbiology 41, 2744–2747.Google Scholar
Bouzid, M., Hunter, P. R., Chalmers, R. M. and Tyler, K. M. (2013). Cryptosporidium pathogenicity and virulence. Clinical Microbiology Review 26, 115–134.Google Scholar
Brook, E. J., Anthony Hart, C., French, N. P. and Christley, R. M. (2009). Molecular epidemiology of Cryptosporidium subtypes in cattle in England. Veterinary Journal 179, 378–382.Google Scholar
Chalmers, R. M. and Davies, A. P. (2010). Minireview: clinical cryptosporidiosis. Experimental Parasitology 124, 138–146.Google Scholar
Chalmers, R. M. and Pollock, K. G. J. (2012). Cryptosporidium in Scotland 2010: reference laboratory data. Health Protection Scotland Weekly Report 46, 33–35.Google Scholar
Chalmers, R. M., Hadfield, S. J., Jackson, C. J., Elwin, K., Xiao, L. and Hunter, P. (2008). Geographic linkage and variation in Cryptosporidium hominis . Emerging Infectious Diseases 14, 496–498.Google Scholar
Chalmers, R. M., Smith, R. P., Hadfield, S. J., Elwin, K. and Giles, M. (2011). Zoonotic linkage and variation in Cryptosopridium parvum from patients in the United Kingdom. Parasitology Research 108, 1321–1325.Google Scholar
Feltus, D. C., Giddings, C. W., Schneck, B. L., Monson, T., Warshauer, D. and McEvoy, J. M. (2006). Evidence supporting zoonotic transmission of Cryptosporidium spp. in Wisconsin. Journal of Clinical Microbiology 44, 4303–4308.Google Scholar
Feng, Y., Torres, E., Li, N., Wanga, L., Bowman, D., and Xiao, L. (2013). Population genetic characterisation of dominant Cryptosporidium parvum subtype IIaA15G2R1. International Journal for Parasitology 43, 1141–1147.Google Scholar
Fournet, N., Deege, M. P., Urbanus, A. T., Nichols, G., Rosner, B. M., Chalmers, R. M., Gorton, R., Pollock, K. G., van der Giessen, J. W., Wever, P. C., Dorigo-Zetsma, J. W., Mulder, B., Mank, T. G., Overdevest, I., Kusters, J. G., van Pelt, W. and Kortbeek, L. M. (2013). Simultaneous increase of Cryptosporidium infections in the Netherlands, the United Kingdom and Germany in late summer season, 2012. Eurosurveillance 18, 1–5. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20348 Google Scholar
Glaberman, S., Moore, J. E., Lowery, C. J., Chalmers, R. M., Sulaiman, I., Elwin, K., Rooney, P. J., Millar, B. C., Dooley, J. S., Lal, A. A. and Xiao, L. (2002). Three drinking-water-associated cryptosporidiosis outbreaks, Northern Ireland. Emerging Infectious Diseases 8, 631–633.Google Scholar
Grinberg, A., Learmonth, J., Kwan, E., Pomroy, W., Lopez Villalobos, N., Gibson, I. and Widmer, G. (2008). Genetic diversity and zoonotic potential of Cryptosporidium parvum causing foal diarrhea. Journal of Clinical Microbiology 46, 2396–2398.Google Scholar
Hadfield, S. J., Robinson, G., Elwin, K. and Chalmers, R. M. (2011). Detection and differentiation of Cryptosporidium spp. in human clinical samples by use of real-time PCR. Journal of Clinical Microbiology 49, 918–924.Google Scholar
Hijjawi, N., Ng, J., Yang, R., Atoum, M. F. and Ryan, U. (2010). Identification of rare and novel Cryptosporidium GP60 subtypes in human isolates from Jordan. Experimental Parasitology 125, 161–164.Google Scholar
Hunter, P. R., Hughes, S., Woodhouse, S., Syed, Q., Verlander, N. Q., Chalmers, R. M., Morgan, K., Nichols, G., Beeching, N. and Osborn, K. (2004). Sporadic cryptosporidiosis case-control study with genotyping. Emerging Infectious Diseases 10, 1241–1249.Google Scholar
Hunter, P. R., Hadfield, S. J., Wilkinson, D., Lake, I. R., Harrison, F. C. and Chalmers, R. M. (2007). Subtypes of Cryptosporidium parvum in humans and disease risk. Emerging Infectious Diseases 13, 82–88.CrossRefGoogle ScholarPubMed
Khan, S. M., Debnath, C., Pramanik, A. K., Xiao, L., Nozaki, T. and Ganguly, S. (2010). Molecular characterization and assessment of zoonotic transmission of Cryptosporidium from dairy cattle in West Bengal, India. Veterinary Parasitology 15, 41–47.Google Scholar
Learmonth, J. J., Ionas, G., Ebbett, K. A. and Kwan, E. S. (2004). Genetic characterization and transmission cycles of Cryptosporidium species isolated from humans in New Zealand. Applied and Environmental Microbiology 70, 3973–3978.Google Scholar
McLauchlin, J., Amar, C., Pedraza-Diaz, S. and Nichols, G. L. (2000). Molecular epidemiological analysis of Cryptosporidium spp. in the United Kingdom: results of genotyping Cryptosporidium spp. in 1,705 fecal samples from humans and 105 fecal samples from livestock animals. Journal of Clinical Microbiology 38, 3984–3990.Google Scholar
Muhid, A., Robertson, I., Ng, J. and Ryan, U. (2011). Prevalence of and management factors contributing to Cryptosporidium sp infection in pre-weaned and post weaned calves in Johor, Malaysia. Experimental Parasitology 127, 534–538.Google Scholar
Ng, J., Eastwood, K., Durrheim, D., Massey, P., Walker, B., Armson, A. and Ryan, U. (2008). Evidence supporting zoonotic transmission of Cryptosporidium in rural New South Wales. Experimental Parasitology 119, 192–195.CrossRefGoogle ScholarPubMed
Ng, J., MacKenzie, B. and Ryan, U. (2010). Longitudinal multi-locus molecular characterisation of sporadic Australian human clinical cases of cryptosporidiosis from 2005–2008. Experimental Parasitology 125, 348–356.Google Scholar
Nichols, R. A. B., Connelly, L., Sullivan, C. B. and Smith, H. V. (2010). Identification of Cryptosporidium species and genotypes in Scottish raw and drinking waters during a one-year monitoring period. Applied Environmental Microbiology 76, 5977–5986.Google Scholar
Pollock, K. G., Ternent, H. E., Mellor, D. J., Chalmers, R. M., Smith, H. V., Ramsay, C. N. and Innocent, G. T. (2010). Spatial and temporal epidemiology of sporadic human cryptosporidiosis in Scotland. Zoonoses and Public Health 57, 487–492.Google Scholar
Pönka, A., Kotilainen, H., Rimhanen-Finne, R., Hokkanen, P., Hänninen, M. L., Kaarna, A., Meri, T. and Kuusi, M. (2009). A foodborne outbreak due to Cryptosporidium parvum in Helsinki. Eurosurveillance 16, 14.Google Scholar
Putignani, L. and Menichella, D. (2010). Global distribution, public health and clinical impact of the protozoan pathogen Cryptosporidium . Interdisciplinary Perspectives on Infectious Diseases 2010, 1–39.Google Scholar
Quilez, J., Torres, E., Chalmers, R. M., Robinson, G., Del Cacho, E. and Sanchez-Acedo, C. (2008 a). Cryptosporidium species and subtype analysis from dairy calves in Spain. Parasitology 135, 1613–1620.Google Scholar
Quilez, J., Torres, E., Chalmers, R. M., Hadfield, S. J., Del Cacho, E. and Sanchez-Acedo, C. (2008 b). Cryptosporidium genotypes and subtypes in lambs and goat kids in Spain. Applied and Environmental Microbiology 74, 6026–6031.Google Scholar
Smith, R. P., Chalmers, R. M., Mueller-Doblies, D., Clifton-Hadley, F. A., Elwin, K., Watkins, J., Paiba, G. A., Hadfield, S. J. and Giles, M. (2010). Investigation of farms linked to human patients with cryptosporidiosis in England and Wales. Preventative Veterinary Medicine 94, 9–17.Google Scholar
Soba, B. and Logar, J. (2008). Genetic classification of Cryptosporidium isolates from humans and calves in Slovenia. Parasitology 135, 1263–1270.CrossRefGoogle ScholarPubMed
Standards for Microbiology Investigations; Staining Procedures TP 39. http://www.hpa.org.uk/ProductsServices/MicrobiologyPathology/UKStandardsForMicrobiologyInvestigations/TermsOfUseForSMIs/AccessToUKSMIs/SMITestProcedures/ Google Scholar
Strong, W. B., Gut, J. and Nelson, R. G. (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. Infection and Immunity 68, 4117–4134.Google Scholar
Sulaiman, I. M., Hira, P. R., Zhou, L., Al-Ali, F. M., Al-Shelahi, F. A., Shweiki, H. M., Iqbal, J., Khalid, N. and Xiao, L. (2005). Unique endemicity of cryptosporidiosis in children in Kuwait. Journal of Clinical Microbiology 43, 2805–2809.CrossRefGoogle ScholarPubMed
Thompson, H. P., Dooley, J. S., Kenny, J., McCoy, M., Lowery, C. J., Moore, J. E. and Xiao, L. (2007). Genotypes and subtypes of Cryptosporidium species in neonatal calves in Northern Ireland. Parasitology Research 100, 619–624.Google Scholar
Trotz-Williams, L. A., Martin, D. S., Gatei, W., Cama, V., Peregrine, A. S., Martin, S. W., Nydam, D. V., Jamieson, F. and Xiao, L. (2006). Genotype and subtype analyses of Cryptosporidium isolates from dairy calves and humans in Ontario. Parasitology Research 99, 346–352.Google Scholar
Vojdani, J. D., Beuchat, L. R. and Tauxe, R. V. (2008). Juice-associated outbreaks of human illness in the United States 1995–2005. Journal of Food Protection 71, 356–64.Google Scholar
Wang, R., Wang, H., Sun, Y., Zhang, L., Jian, F., Qi, M., Ning, C. and Xiao, L. (2011). Characteristics of Cryptosporidium transmission in preweaned dairy cattle in Henan, China. Journal of Clinical Microbiology 49, 1077–1082.CrossRefGoogle ScholarPubMed
Wielinga, P. R., de Vries, A., van der Goot, T. H., Mank, T., Mars, M. H., Kortbeek, L. M. and van der Giessen, J. W. (2008). Molecular epidemiology of Cryptosporidium in humans and cattle in The Netherlands. International Journal of Parasitology 38, 809–817.CrossRefGoogle ScholarPubMed
Xiao, L. (2010). Molecular epidemiology of cryptosporidiosis: an update. Experimental Parasitology 124, 80–89.Google Scholar
Xiao, L. and Feng, Y. (2008). Zoonotic cryptosporidiosis. FEMS Immunology and Medical Microbiology 52, 309–323.Google Scholar
Xiao, L., Zhou, L., Santin, M., Yang, W. and Fayer, R. (2007). Distribution of Cryptosporidium parvum subtypes in calves in eastern United States. Parasitology Research 100, 701–706.Google Scholar
Yoshida, H., Matsuo, M., Miyoshi, T., Uchino, K., Nakaguchi, H., Fukumoto, T., Teranaka, Y. and Tanaka, T. (2007). An outbreak of cryptosporidiosis suspected to be related to contaminated food October 2006, Sakai City Japan. Japanese Journal of Infectious Diseases 60, 405–407.Google Scholar
Zintl, A., Proctor, A. F., Read, C., Dewaal, T., Shanaghy, N., Fanning, S. and Mulcahy, G. (2009). The prevalence of Cryptosporidium species and subtypes in human faecal samples in Ireland. Epidemiology and Infection 137, 270–277.Google Scholar
Zintl, A., Ezzaty-Mirashemi, M., Chalmers, R. M., Elwin, K., Mulcahy, G., Lucy, F. E. and De Waal, T. (2011). Longitudinal and spatial distribution of GP60 subtypes in human cryptosporidiosis cases in Ireland. Epidemiology and Infection 139, 1945–1955.CrossRefGoogle ScholarPubMed