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First molecular characterization of Cryptosporidium in Yemen

Published online by Cambridge University Press:  01 February 2013

N. A. ALYOUSEFI*
Affiliation:
Department of Parasitology, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia
M. A. K. MAHDY*
Affiliation:
Department of Parasitology, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia Department of Parasitology, Faculty of Medicine, Sana'a University, Sana'a, Yemen
Y. A. L. LIM
Affiliation:
Department of Parasitology, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia
L. XIAO
Affiliation:
Division of Foodborne, Waterborne and Environmental Diseases, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, USA
R. MAHMUD
Affiliation:
Department of Parasitology, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia
*
*Corresponding author: Department of Parasitology, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia. E-mail: [email protected]
*Corresponding author: Department of Parasitology, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia. E-mail: [email protected]

Summary

Cryptosporidium is a protozoan parasite of humans and animals and has a worldwide distribution. The parasite has a unique epidemiology in Middle Eastern countries where the IId subtype family of Cryptosporidium parvum dominates. However, there has been no information on Cryptosporidium species in Yemen. Thus, this study was conducted in Yemen to examine the distribution of Cryptosporidium species and subtype families. Fecal samples were collected from 335 patients who attended hospitals in Sana'a city. Cryptosporidium species were determined by PCR and sequence analysis of the 18 s rRNA gene. Cryptosporidium parvum and C. hominis subtypes were identified based on sequence analysis of the 60 kDa glycoprotein (gp60) gene. Out of 335 samples, 33 (9·9%) were positive for Cryptosporidium. Of them, 97% were identified as C. parvum whilst 1 case (3%) was caused by C. hominis. All 7 C. parvum isolates subtyped belonged to the IIaA15G2R1 subtype. The common occurrence of the zoonotic IIa subtype family of C. parvum highlights the potential occurrence of zoonotic transmission of cryptosporidiosis in Yemen. However, this postulation needs confirmation with future molecular epidemiological studies of cryptosporidiosis in both humans and animals in Yemen.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013

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References

REFERENCES

Abd El Kader, N. M., Blanco, M. A., Ali-Tammam, M., Abd El Ghaffar, A. E. R. B., Osman, A., El Sheikh, N., Rubio, J. M. and de Fuentes, I. (2012). Detection of Cryptosporidium parvum and Cryptosporidium hominis in human patients in Cairo, Egypt. Parasitology Research 110, 161166.CrossRefGoogle ScholarPubMed
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, 303305.CrossRefGoogle ScholarPubMed
Al-Brikan, F., Salem, H., Beeching, N. and Hilal, N. (2008). Multilocus genetic analysis of Cryptosporidium isolates from Saudi Arabia. Journal of the Egyptian Society of Parasitology 38, 645658.Google ScholarPubMed
Al-Shamiri, A., Al-Zubairy, A. and Al-Mamari, R. (2010). The prevalence of Cryptosporidium spp. in children, Taiz District, Yemen. Iranian Journal of Parasitology 5, 2632.Google ScholarPubMed
Al-Shibani, L. A., Azazy, A. A. and El-Taweel, H. A. (2009). Cryptosporidiosis and other intestinal parasites in 3 Yemeni orphanages: prevalence, risk, and morbidity. Journal of the Egyptian Society of Parasitology 39, 327337.Google ScholarPubMed
Alves, M., Xiao, L., Antunes, F. and Matos, O. (2006). Distribution of Cryptosporidium subtypes in humans and domestic and wild ruminants in Portugal. Parasitology Research 99, 287292.CrossRefGoogle ScholarPubMed
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, 27442747.CrossRefGoogle ScholarPubMed
Alyousefi, N. A., Mahdy, M. A. K., Mahmud, R. and Lim, Y. A. L. (2011). Factors associated with high prevalence of intestinal protozoan infections among patients in Sana'a City, Yemen. PLoS One 6, e22044.CrossRefGoogle ScholarPubMed
Broglia, A., Reckinger, S., Cacciò, S. M. and Nöckler, K. (2008). Distribution of Cryptosporidium parvum subtypes in calves in Germany. Veterinary Parasitology 154, 813.CrossRefGoogle ScholarPubMed
Budu-Amoako, E., Greenwood, S., Dixon, B., Sweet, L., Ang, L., Barkema, H. and McClure, J. (2012). Molecular epidemiology of Cryptosporidium and Giardia in humans on Prince Edward Island, Canada: evidence of zoonotic transmission from cattle. Zoonoses and Public Health 59, 424433.CrossRefGoogle ScholarPubMed
Chalmers, R., Elwin, K., Thomas, A., Guy, E. and Mason, B. (2009). Long-term Cryptosporidium typing reveals the aetiology and species-specific epidemiology of human cryptosporidiosis in England and Wales, 2000 to 2003. Eurosurveillance 14. http://www.eurosurveillance.orgCrossRefGoogle ScholarPubMed
Cohen, S., Dalle, F., Gallay, A., Di Palma, M., Bonnin, A. and Ward, H. D. (2006). Identification of Cpgp40/15 Type Ib as the predominant allele in isolates of Cryptosporidium spp. from a waterborne outbreak of gastroenteritis in South Burgundy, France. Journal of Clinical Microbiology 44, 589591.CrossRefGoogle ScholarPubMed
DuPont, H. L., Chappell, C. L., Sterling, C. R., Okhuysen, P. C., Rose, J. B. and Jakubowski, W. (1995). The infectivity of Cryptosporidium parvum in healthy volunteers. New England Journal of Medicine 332, 855859.CrossRefGoogle ScholarPubMed
Eida, A., Eida, M. and El-Desoky, A. (2009). Pathological studies of different genotypes of human Cryptosporidium Egyptian isolates in experimental mice. Journal of the Egyptian Society of Parasitology J39, 975990.Google Scholar
Elwin, K., Hadfield, S.J., Robinson, G., Crouch, N.D. and Chalmers, R.M. (2012). Cryptosporidium viatorum n. sp. (Apicomplexa: Cryptosporidiidae) among travellers returning to Great Britain from the Indian subcontinent, 2007–2011. International Journal for Parasitology 42, 675682.CrossRefGoogle Scholar
Fayer, R. (2010). Taxonomy and species delimitation in Cryptosporidium. Experimental Parasitology 124, 9097.CrossRefGoogle ScholarPubMed
Fayer, R., Morgan, U. and Upton, S. (2000). Epidemiology of Cryptosporidium: transmission, detection and identification. International Journal for Parasitology 30, 13051322.CrossRefGoogle ScholarPubMed
Fayer, R. and Santin, M. (2009). Cryptosporidium xiaoi n. sp. (Apicomplexa: Cryptosporidiidae) in sheep (Ovis aries). Veterinary Parasitology 164, 192200.CrossRefGoogle Scholar
Feng, Y., Ortega, Y., He, G., Das, P., Xu, M., Zhang, X., Fayer, R., Gatei, W., Cama, V. and Xiao, L. (2007). Wide geographic distribution of Cryptosporidium bovis and the deer-like genotype in bovines. Veterinary Parasitology 144, 19.CrossRefGoogle ScholarPubMed
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, 918924.CrossRefGoogle ScholarPubMed
Hijjawi, N., Ng, J., Yang, R., Atoum, M. F. M. and Ryan, U. (2010). Identification of rare and novel Cryptosporidium GP60 subtypes in human isolates from Jordan. Experimental Parasitology 125, 161164.CrossRefGoogle ScholarPubMed
Huang, D. B. and White, A. C. (2006). An updated review on Cryptosporidium and Giardia. Gastroenterology Clinics of North America 35, 291314.CrossRefGoogle ScholarPubMed
Iqbal, J., Khalid, N. and Hira, P. R. (2011). Cryptosporidiosis in Kuwaiti children: association of clinical characteristics with Cryptosporidium species and subtypes. Journal of Medical Microbiology 60, 647652.CrossRefGoogle ScholarPubMed
Iqbal, A., Lim, Y. A. L., Surin, J. and Sim, B. L. H. (2012). High diversity of Cryptosporidium subgenotypes identified in Malaysian HIV/AIDS individuals targeting gp60 gene. PLoS One 7, e31139.CrossRefGoogle ScholarPubMed
Johnson, D., Pieniazek, N., Griffin, D., Misener, L. and Rose, J. (1995). Development of a PCR protocol for sensitive detection of Cryptosporidium oocysts in water samples. Applied and Environmental Microbiology 61, 3849.CrossRefGoogle ScholarPubMed
Kjos, S. A., Jenkins, M., Okhuysen, P. C. and Chappell, C. L. (2005). Evaluation of recombinant oocyst protein CP41 for detection of Cryptosporidium-specific antibodies. Clinical and Vaccine Immunology 12, 268272.CrossRefGoogle ScholarPubMed
Lwanga, S. K. and Lemeshow, S. (1991). Sample Size Determination in Health Studies: a Practical Manual. World Health Organization, Geneva, Switzerland.Google Scholar
MacKenzie, W., Hoxie, N., Proctor, M., Gradus, M., Blair, K., Peterson, D., Kazmierczak, J., Addiss, D., Fox, K. and Rose, J. (1994). A massive outbreak in Milwaukee of Cryptosporidium infection transmitted through the public water supply. New England Journal of Medicine 331, 161167.CrossRefGoogle Scholar
Mallon, M., MacLeod, A., Wastling, J., Smith, H., Reilly, B. and Tait, A. (2003). Population structures and the role of genetic exchange in the zoonotic pathogen Cryptosporidium parvum. Journal of Molecular Evolution 56, 407417.CrossRefGoogle ScholarPubMed
Nazemalhosseini-Mojarad, E., Feng, Y. and Xiao, L. (2012). The importance of subtype analysis of Cryptosporidium spp. in epidemiological investigations of human cryptosporidiosis in Iran and other Mideast countries. Gastroenterology and Hepatology from Bed to Bench 5, 6770.Google ScholarPubMed
Nazemalhosseini-Mojarad, E., Haghighi, A., Taghipour, N., Keshavarz, A., Mohebi, S. R., Zali, M. R. and Xiao, L. (2011). Subtype analysis of Cryptosporidium parvum and Cryptosporidium hominis isolates from humans and cattle in Iran. Veterinary Parasitology 179, 250252.CrossRefGoogle ScholarPubMed
Nazemalhosseini Mojarad, E., Keshavarz, A., Taghipour, N., Haghighi, A., Kazemi, B. and Athari, A. (2010). Genotyping of Cryptosporidium spp. in clinical samples: PCR-RFLP analysis of the TRAP-C2 gene. Gastroenterology and Hepatology from Bed to Bench 4, 2933.Google Scholar
Nichols, R. A., Campbell, B. M. and Smith, H. V. (2003). Identification of Cryptosporidium spp. oocysts in United Kingdom noncarbonated natural mineral waters and drinking by using a modified nested PCR-restriction fragment length polymorphism assay. Applied and Environmental Microbiology 69, 41834189.CrossRefGoogle ScholarPubMed
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, 192195.CrossRefGoogle ScholarPubMed
Pangasa, A., Jex, A. R., Nolan, M. J., Campbell, B. E., Haydon, S. R., Stevens, M. A. and Gasser, R. B. (2010). Highly sensitive non-isotopic restriction endonuclease fingerprinting of nucleotide variability in the gp60 gene within Cryptosporidium species, genotypes and subgenotypes infective to humans, and its implications. Electrophoresis 31, 16371647.CrossRefGoogle ScholarPubMed
Raccurt, C. (2007). Worldwide human zoonotic cryptosporidiosis caused by Cryptosporidium felis. Parasite (Paris, France) 14, 1520.CrossRefGoogle ScholarPubMed
Santin, M., Trout, J. M. and Fayer, R. (2008). A longitudinal study of cryptosporidiosis in dairy cattle from birth to 2 years of age. Veterinary Parasitology 155, 1523.CrossRefGoogle Scholar
Slifko, T. R., Smith, H. V. and Rose, J. B. (2000). Emerging parasite zoonoses associated with water and food. International Journal for Parasitology 30, 13791393.CrossRefGoogle ScholarPubMed
Soba, B. and Logar, J. (2008). Genetic classification of Cryptosporidium isolates from humans and calves in Slovenia. Parasitology 135, 12631270.CrossRefGoogle ScholarPubMed
Stark, D., Al-qassab, S. E., Barratt, J. L. N., Stanley, K., Roberts, T., Marriott, D., Harkness, J. and Ellis, J. T. (2011). Evaluation of multiplex tandem real-time PCR for detection of Cryptosporidium spp., Dientamoeba fragilis, Entamoeba histolytica and Giardia intestinalis in clinical stool samples. Journal of Clinical Microbiology 49, 257262.CrossRefGoogle ScholarPubMed
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, 41174134.CrossRefGoogle 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, 28052809.CrossRefGoogle ScholarPubMed
Tamer, G. S., Turk, M., Dagci, H., Pektas, B., Guy, E. C., Guruz, A. Y. and Uner, A. (2007). The prevalence of cryptosporidiosis in Turkish children, and genotyping of isolates by nested polymerase chain reaction-restriction fragment length polymorphism. Saudi Medical Journal 28, 12431246.Google ScholarPubMed
Thompson, H. P., Dooley, J. S. G., Kenny, J., McCoy, M., Lowery, C. J., Moore, J. E. and Xiao, L. (2007). Genotypes and subtypes of Cryptosporidium spp. in neonatal calves in Northern Ireland. Parasitology Research 100, 619624.CrossRefGoogle ScholarPubMed
Traversa, D. (2010). Evidence for a new species of Cryptosporidium infecting tortoises: Cryptosporidium ducismarci. Parasite and Vectors 3, 21.CrossRefGoogle ScholarPubMed
Trotz-Williams, L., Martin, D., Gatei, W., Cama, V., Peregrine, A., Martin, S., Nydam, D., Jamieson, F. and Xiao, L. (2006). Genotype and subtype analyses of Cryptosporidium isolates from dairy calves and humans in Ontario. Parasitology Research 99, 346352.CrossRefGoogle ScholarPubMed
Waldron, L. S., Dimeski, B., Beggs, P. J., Ferrari, B. C. and Power, M. L. (2011). Molecular epidemiology, spatiotemporal analysis, and ecology of sporadic human cryptosporidiosis in Australia. Applied and Environmental Microbiology 77, 77577765.CrossRefGoogle ScholarPubMed
Weber, R., Bryan, R. T., Bishop, H. S., Wahlquist, S. P., Sullivan, J. J. and Juranek, D. D. (1991). Threshold of detection of Cryptosporidium oocysts in human stool samples: evidence for low sensitivity of current diagnostic methods. Journal of Clinical Microbiology 29, 13231327.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. B. (2008). Molecular epidemiology of Cryptosporidium in humans and cattle in the Netherlands. International Journal for Parasitology 38, 809817.CrossRefGoogle ScholarPubMed
Wu, Z., Nagano, I., Boonmars, T., Nakada, T. and Takahashi, Y. (2003). Intraspecies polymorphism of Cryptosporidium parvum revealed by PCR-restriction fragment length polymorphism (RFLP) and RFLP-single-strand conformational polymorphism analyses. Applied and Environmental Microbiology 69, 47204726.CrossRefGoogle ScholarPubMed
Xiao, L. (2009). Molecular epidemiology of human cryptosporidiosis in developing countries. In Giardia and Cryptosporidium from Molecules to Diseases (ed. Ortega Pierres, G., Cacciò, S., Fayer, R., Mank, T. G., Smith, H. V. and Thompson, R. C. A), pp. 5162. CAB International, Wallingford, UK.CrossRefGoogle Scholar
Xiao, L. (2010). Molecular epidemiology of cryptosporidiosis: an update. Experimental Parasitology 124, 8089.CrossRefGoogle ScholarPubMed