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Multilocus sequence typing and clonal population genetic structure of Cyclospora cayetanensis in humans

Published online by Cambridge University Press:  12 July 2017

JUNQIANG LI
Affiliation:
College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, China International Joint Research Laboratory for Zoonotic Diseases of Henan, Zhengzhou 450002, China
YANKAI CHANG
Affiliation:
College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, China International Joint Research Laboratory for Zoonotic Diseases of Henan, Zhengzhou 450002, China
KE SHI
Affiliation:
College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, China International Joint Research Laboratory for Zoonotic Diseases of Henan, Zhengzhou 450002, China
RONGJUN WANG
Affiliation:
College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, China International Joint Research Laboratory for Zoonotic Diseases of Henan, Zhengzhou 450002, China
KANDA FU
Affiliation:
Huaihe Hospital of Henan University, Kaifeng 475000, China
SHAN LI
Affiliation:
The PLA No. 155 Central Hospital, Kaifeng 475000, China
JINLING XU
Affiliation:
Henan Province People's Hospital, Zhengzhou 450003, China
LITING JIA
Affiliation:
The Third Affiliated Hospital of Zhengzhou University, Zhengzhou 450052, China
ZHENXIN GUO
Affiliation:
Zhengzhou Children's Hospital, Zhengzhou 450018, China
LONGXIAN ZHANG*
Affiliation:
College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, China International Joint Research Laboratory for Zoonotic Diseases of Henan, Zhengzhou 450002, China
*
*Corresponding author: College of Animal Science and Veterinary Medicine, Henan Agricultural University, 95 Wenhua Road, Zhengzhou 450002, P. R. China. E-mail: zhanglx8999@henau.edu.cn; zhanglx8999@gmail.com

Summary

To investigate the prevalence of Cyclospora cayetanensis in a longitudinal study and to conduct a population genetic analysis, fecal specimens from 6579 patients were collected during the cyclosporiasis – prevalent seasons in two urban areas of central China in 2011–2015. The overall incidence of C. cayetanensis infection was 1·2% (76/6579): 1·6% (50/3173) in Zhengzhou and 0·8% (26/3406) in Kaifeng (P < 0·05), with infections in all age groups (P > 0·05). All the isolates clustered in the C. cayetanensis clade based on the small subunit ribosomal RNA gene sequence phylogenetic analysis. There were 45 specimens positive for all the five C. cayetanensis microsatellite loci, and formed 29 multilocus genotypes (MLGs). The phylogenetic relationships of 54 distinct MLGs (including 25 known reference MLGs), based on the concatenated multilocus sequences, formed three main clusters. A population structure analysis showed that the 79 isolates (including 34 known reference isolates) of C. cayetanensis produced three distinct subpopulations based on allelic profile data. In conclusion, we determined the frequency of C. cayetanensis infection in humans in Henan Province. The clonal population structure of the human C. cayetanensis isolates showed linkage disequilibrium and three distinct subpopulations.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Abanyie, F., Harvey, R. R., Harris, J. R., Wiegand, R. E., Gaul, L., Desvignes-Kendrick, M., Irvin, K., Williams, I., Hall, R. L., Herwaldt, B., Gray, E. B., Qvarnstrom, Y., Wise, M. E., Cantu, V., Cantey, P. T., Bosch, S., DA Silva, A. J., Fields, A., Bishop, H., Wellman, A., Beal, J., Wilson, N., Fiore, A. E., Tauxe, R., Lance, S., Slutsker, L. and Parise, M. and Multistate Cyclosporiasis Outbreak Investigation Team. (2015). 2013 multistate outbreaks of Cyclospora cayetanensis infections associated with fresh produce: focus on the Texas investigations. Epidemiology and Infection 143, 34513458.Google Scholar
Bhandari, D., Tandukar, S., Parajuli, H., Thapa, P., Chaudhary, P., Shrestha, D., Shah, P. K., Sherchan, J. B. and Sherchand, J. B. (2015). Cyclospora infection among school children in Kathmandu, Nepal: prevalence and associated risk factors. Tropical Medicine and Health 43, 211216.CrossRefGoogle ScholarPubMed
Buckee, C. O. and Gupta, S. (2010). Modelling malaria population structure and its implications for control. Modelling Parasite Transmission and Control 673, 112126.Google Scholar
Döller, P. C., Dietrich, K., Filipp, N., Brockmann, S., Dreweck, C., Vonthein, R., Wagner-Wiening, C. and Wiedenmann, A. (2002). Cyclosporiasis outbreak in Germany associated with the consumption of salad. Emerging Infectious Diseases 8, 992–924.Google Scholar
Earl, D. A. and von Holdt, B. M. (2012). Structure harvester: a website and program for visualizing structure output and implementing the Evanno method. Conservation Genetics Resources 4, 359361.Google Scholar
Eberhard, M. L., Ortega, Y. R., Hanes, D. E., Nace, E. K., Do, R. Q., Robl, M. G., Won, K. Y., Gavidia, C., Sass, N. L., Mansfield, K., Gozalo, A., Griffiths, J., Gilman, R., Sterling, C. R. and Arrowood, M. J. (2000). Attempts to establish experimental Cyclospora cayetanensis infection in laboratory animals. Journal of Parasitology 86, 577582.Google Scholar
Gatei, W., Das, P., Dutta, P., Sen, A., Cama, V., Lal, A. A. and Xiao, L. (2007). Multilocus sequence typing and genetic structure of Cryptosporidium hominis from children in Kolkata, India. Infection, Genetics and Evolution 7, 197205.Google Scholar
Giangaspero, A., Marangi, M., Koehler, A. V., Papini, R., Normanno, G., Lacasella, V., Lonigro, A. and Gasser, R. B. (2015). Molecular detection of Cyclospora in water, soil, vegetables and humans in southern Italy signals a need for improved monitoring by health authorities. International Journal of Food Microbiology 211, 95100.CrossRefGoogle ScholarPubMed
Guo, Y., Roellig, D. M., Li, N., Tang, K., Frace, M., Ortega, Y., Arrowood, M. J., Feng, Y., Qvarnstrom, Y., Wang, L., Moss, D. M., Zhang, L. and Xiao, L. (2016). Multilocus sequence typing tool for Cyclospora cayetanensis . Emerging Infectious Diseases 22, 14641467.Google Scholar
Haubold, B. and Hudson, R. R. (2000). LIAN 3.0: detecting linkage disequilibrium in multilocus data. Bioinformatics 16, 847849.CrossRefGoogle ScholarPubMed
Kaminsky, R. G., Lagos, J., Raudales Santos, G. and Urrutia, S. (2016). Marked seasonality of Cyclospora cayetanensis infections: ten-year observation of hospital cases, Honduras. BMC Infectious Diseases 16, 66.CrossRefGoogle ScholarPubMed
Karim, M. R., Wang, R., He, X., Zhang, L., Li, J., Rume, F. I., Dong, H., Qi, M., Jian, F., Zhang, S., Sun, M., Yang, G., Zou, F., Ning, C. and Xiao, L. (2014). Multilocus sequence typing of Enterocytozoon bieneusi in nonhuman primates in China. Veterinary Parasitology 200, 1323.Google Scholar
Khan, A., Fux, B., Su, C., Dubey, J. P., Darde, M. L., Ajioka, J. W., Rosenthal, B. M. and Sibley, L. D. (2007). Recent transcontinental sweep of Toxoplasma gondii driven by a single monomorphic chromosome. Proceedings of the National Academy of Sciences 104, 1487214877.Google Scholar
Legua, P. and Seas, C. (2013). Cystoisospora and cyclospora . Current Opinion in Infectious Diseases 26, 479483.CrossRefGoogle ScholarPubMed
Li, G., Xiao, S., Zhou, R., Li, W. and Wadeh, H. (2007). Molecular characterization of Cyclospora-like organism from dairy cattle. Parasitology Research 100, 955961.Google Scholar
Li, W., Wan, Q., Yu, Q., Yang, Y., Tao, W., Jiang, Y. and Xiao, L. (2016). Genetic variation of mini- and microsatellites and a clonal structure in Enterocytozoon bieneusi population in foxes and raccoon dogs and population differentiation of the parasite between fur animals and humans. Parasitology Research 115, 28992904.CrossRefGoogle Scholar
Librado, P. and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 14511452.CrossRefGoogle ScholarPubMed
MacLeod, A., Tweedie, A., Welburn, S. C., Maudlin, I., Turner, C. M. and Tait, A. (2000). Minisatellite marker analysis of Trypanosoma brucei: reconciliation of clonal, panmictic, and epidemic population genetic structures. Proceedings of the National Academy of Sciences 97, 1344213447.Google 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.Google Scholar
Morrison, L. J., Mallon, M. E., Smith, H. V., MacLeod, A., Xiao, L. and Tait, A. (2008). The population structure of the Cryptosporidium parvum population in Scotland: a complex picture. Infection, Genetics and Evolution 8, 121129.CrossRefGoogle ScholarPubMed
Orozco-Mosqueda, G. E., Martínez-Loya, O. A. and Ortega, Y. R. (2014). Cyclospora cayetanensis in a pediatric hospital in Morelia, México. The American Journal of Tropical Medicine and Hygiene 91, 537540.Google Scholar
Ortega, Y. R. and Sanchez, R. (2010). Update on Cyclospora cayetanensis, a food-borne and waterborne parasite. Clinical Microbiology Reviews 23, 218234.Google Scholar
Ortega, Y. R., Sterling, C. R., Gilman, R. H., Cama, V. A. and Diaz, F. (1993). Cyclospora species – a new protozoan pathogen of humans. New England Journal of Medicine 328, 13081312.Google Scholar
Ozdamar, M., Hakko, E. and Turkoglu, S. (2010). High occurrence of cyclosporiasis in Istanbul, Turkey, during a dry and warm summer. Parasites & Vectors 3, 39.Google Scholar
Plutzer, J. and Karanis, P. (2016). Neglected waterborne parasitic protozoa and their detection in water. Water Research 101, 318332.CrossRefGoogle ScholarPubMed
Pritchard, J. K., Stephens, M. and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945959.Google Scholar
Su, X., Hayton, K. and Wellems, T. E. (2007). Genetic linkage and association analyses for trait mapping in Plasmodium falciparum . Nature Reviews Genetics 8, 497506.Google Scholar
Sulaiman, I. M., Ortega, Y., Simpson, S. and Kerdahi, K. (2014). Genetic characterization of human-pathogenic Cyclospora cayetanensis parasites from three endemic regions at the 18S ribosomal RNA locus. Infection, Genetics and Evolution 22, 229234.CrossRefGoogle ScholarPubMed
Tanriverdi, S., Markovics, A., Arslan, M. O., Itik, A., Shkap, V. and Widmer, G. (2006). Emergence of distinct genotypes of Cryptosporidium parvum in structured host populations. Applied and Environmental Microbiology 2, 25072513.CrossRefGoogle Scholar
Tibayrenc, M. and Ayala, F. J. (2002). The clonal theory of parasitic protozoa: 12 years on. Trends in Parasitology 18, 405410.Google Scholar
Tibayrenc, M. and Ayala, F. J. (2014). Cryptosporidium, Giardia, Cryptococcus, Pneumocystis genetic variability: cryptic biological species or clonal near-clades? PLoS Pathogens 10, e1003908.CrossRefGoogle ScholarPubMed
Wan, Q., Xiao, L., Zhang, X., Li, Y., Lu, Y., Song, M. and Li, W. (2016). Clonal evolution of Enterocytozoon bieneusi populations in swine and genetic differentiation in subpopulations between isolates from swine and humans. PLoS Neglected Tropical Diseases 10, e0004966.Google Scholar
Wang, R., Jian, F., Zhang, L., Ning, C., Liu, A., Zhao, J., Feng, Y., Qi, M., Wang, H., Lv, C., Zhao, G. and Xiao, L. (2012). Multilocus sequence subtyping and genetic structure of Cryptosporidium muris and Cryptosporidium andersoni . PLoS ONE 7, e43782.Google Scholar
Wang, R., Zhang, L., Axén, C., Bjorkman, C., Jian, F., Amer, S., Liu, A., Feng, Y., Li, G., Lv, C., Zhao, Z., Qi, M., Dong, H., Wang, H., Sun, Y., Ning, C. and Xiao, L. (2014). Cryptosporidium parvum IId family: clonal population and dispersal from Western Asia to other geographical regions. Scientific Reports 4, 4208.Google Scholar
Zhou, Y., Lv, B., Wang, Q., Wang, R., Jian, F., Zhang, L., Ning, C., Fu, K., Wang, Y., Qi, M., Yao, H., Zhao, J., Zhang, X., Sun, Y., Shi, K., Arrowood, M. J. and Xiao, L. (2011). Prevalence and molecular characterization of Cyclospora cayetanensis, Henan, China. Prevalence 17, 18871890.Google Scholar
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