Molecular Surveillance of Cryptosporidium Spp., Giardia Duodenalis, and Enterocytozoon Bieneusi by Genotyping and Subtyping Parasites in Wastewater

Overview

Journal PLoS Negl Trop Dis

Specialties Infectious Diseases
Tropical Medicine

Date 2012 Sep 13

PMID 22970334

Citations 109

Authors

Na Li

Lihua Xiao

Lin Wang

Shuming Zhao

Xukun Zhao

Liping Duan

Meijin Guo

Lili Liu

Yaoyu Feng

Affiliations

Soon will be listed here.

Abstract

Background: Despite their wide occurrence, cryptosporidiosis and giardiasis are considered neglected diseases by the World Health Organization. The epidemiology of these diseases and microsporidiosis in humans in developing countries is poorly understood. The high concentration of pathogens in raw sewage makes the characterization of the transmission of these pathogens simple through the genotype and subtype analysis of a small number of samples.

Methodology/principal Findings: The distribution of genotypes and subtypes of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi in 386 samples of combined sewer systems from Shanghai, Nanjing and Wuhan and the sewer system in Qingdao in China was determined using PCR-sequencing tools. Eimeria spp. were also genotyped to assess the contribution of domestic animals to Cryptosporidium spp., G. duodenalis, and E. bieneusi in wastewater. The high occurrence of Cryptosporidium spp. (56.2%), G. duodenalis (82.6%), E. bieneusi (87.6%), and Eimeria/Cyclospora (80.3%) made the source attribution possible. As expected, several human-pathogenic species/genotypes, including Cryptosporidium hominis, Cryptosporidium meleagridis, G. duodenalis sub-assemblage A-II, and E. bieneusi genotype D, were the dominant parasites in wastewater. In addition to humans, the common presence of Cryptosporidium spp. and Eimeria spp. from rodents indicated that rodents might have contributed to the occurrence of E. bieneusi genotype D in samples. Likewise, the finding of Eimeria spp. and Cryptosporidium baileyi from birds indicated that C. meleagridis might be of both human and bird origins.

Conclusions/significance: The distribution of Cryptosporidium species, G. duodenalis genotypes and subtypes, and E. bieneusi genotypes in urban wastewater indicates that anthroponotic transmission appeared to be important in epidemiology of cryptosporidiosis, giardiasis, and microsporidiosis in the study areas. The finding of different distributions of subtypes between Shanghai and Wuhan was indicative of possible differences in the source of C. hominis among different areas in China.

Citing Articles

Identification of two new genetic loci for high-resolution genotyping of Enterocytozoon bieneusi.

Meng X, Ou Y, Jiang W, Guo Y, Xiao L, Feng Y Parasite. 2025; 32:6.

PMID: 39887113 PMC: 11784105. DOI: 10.1051/parasite/2025002.

Occurrence and Genotypic Identification of spp. and in Bamaxiang Pigs in Bama Yao Autonomous County of Guangxi Province, China.

Yu X, Mu X, Yuan K, Wang S, Li Y, Xu H Animals (Basel). 2024; 14(22).

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Wild sympatric rodents inhabiting pig farm environments may facilitate the spillover of Enterocytozoon bieneusi from pig farms.

Shan F, Meng Q, Wang F, Zhao J, Xu H, Wang N Parasite. 2024; 31:59.

PMID: 39331806 PMC: 11433834. DOI: 10.1051/parasite/2024061.

Wastewater-based intestinal protozoa monitoring in Shanghai, China.

Jiang Y, Yuan Z, Wang Y, Zhang J, Shen Y, Cao J Microbiol Spectr. 2024; 12(11):e0403223.

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Wild rodents in three provinces of China exhibit a wide range of diversity.

Gao Z, Wang H, Hou Q, Qin Y, Qin S, Zhao Q Front Vet Sci. 2024; 11:1427690.

PMID: 39268515 PMC: 11390646. DOI: 10.3389/fvets.2024.1427690.

References

Cama V, Gilman R, Vivar A, Ticona E, Ortega Y, Bern C . Mixed Cryptosporidium infections and HIV. Emerg Infect Dis. 2006; 12(6):1025-8. PMC: 3373040. DOI: 10.3201/eid1206.060015. View

Jiang J, Alderisio K, Xiao L . Distribution of cryptosporidium genotypes in storm event water samples from three watersheds in New York. Appl Environ Microbiol. 2005; 71(8):4446-54. PMC: 1183313. DOI: 10.1128/AEM.71.8.4446-4454.2005. View

Xiao L . Molecular epidemiology of cryptosporidiosis: an update. Exp Parasitol. 2009; 124(1):80-9. DOI: 10.1016/j.exppara.2009.03.018. View

Santin M, Fayer R . Enterocytozoon bieneusi genotype nomenclature based on the internal transcribed spacer sequence: a consensus. J Eukaryot Microbiol. 2009; 56(1):34-8. DOI: 10.1111/j.1550-7408.2008.00380.x. View

Santin M, Fayer R . Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals. Res Vet Sci. 2010; 90(3):363-71. DOI: 10.1016/j.rvsc.2010.07.014. View

Sulaiman I, Fayer R, Yang C, Santin M, Matos O, Xiao L . Molecular characterization of Enterocytozoon bieneusi in cattle indicates that only some isolates have zoonotic potential. Parasitol Res. 2004; 92(4):328-34. DOI: 10.1007/s00436-003-1049-5. View

Feng Y, Zhao X, Chen J, Jin W, Zhou X, Li N . Occurrence, source, and human infection potential of cryptosporidium and Giardia spp. in source and tap water in shanghai, china. Appl Environ Microbiol. 2011; 77(11):3609-16. PMC: 3127622. DOI: 10.1128/AEM.00146-11. View

Savioli L, Smith H, Thompson A . Giardia and Cryptosporidium join the 'Neglected Diseases Initiative'. Trends Parasitol. 2006; 22(5):203-8. DOI: 10.1016/j.pt.2006.02.015. View

Robinson G, Wright S, Elwin K, Hadfield S, Katzer F, Bartley P . Re-description of Cryptosporidium cuniculus Inman and Takeuchi, 1979 (Apicomplexa: Cryptosporidiidae): morphology, biology and phylogeny. Int J Parasitol. 2010; 40(13):1539-48. DOI: 10.1016/j.ijpara.2010.05.010. View

10.

Yong T, Park S, Hwang U, Yang H, Lee K, Min D . Genotyping of Giardia lamblia isolates from humans in China and Korea using ribosomal DNA Sequences. J Parasitol. 2000; 86(4):887-91. DOI: 10.1645/0022-3395(2000)086[0887:GOGLIF]2.0.CO;2. View

11.

Thellier M, Breton J . Enterocytozoon bieneusi in human and animals, focus on laboratory identification and molecular epidemiology. Parasite. 2008; 15(3):349-58. DOI: 10.1051/parasite/2008153349. View

12.

Sogayar M, Yoshida E . Giardia survey in live-trapped small domestic and wild mammals in four regions in the southwest region of the state of São Paulo, Brazil. Mem Inst Oswaldo Cruz. 1995; 90(6):675-8. DOI: 10.1590/s0074-02761995000600002. View

13.

Zhou Y, Lv B, Wang Q, Wang R, Jian F, Zhang L . Prevalence and molecular characterization of Cyclospora cayetanensis, Henan, China. Emerg Infect Dis. 2011; 17(10):1887-90. PMC: 3310644. DOI: 10.3201/eid1710.101296. View

14.

Feng Y, Xiao L . Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev. 2011; 24(1):110-40. PMC: 3021202. DOI: 10.1128/CMR.00033-10. View

15.

Wang K, Li C, Wang J, Tian Y . Cyclospore cayetanensis in Anhui, China. World J Gastroenterol. 2002; 8(6):1144-8. PMC: 4656397. DOI: 10.3748/wjg.v8.i6.1144. View

16.

Carducci A, Verani M, Battistini R, Pizzi F, Rovini E, Andreoli E . Epidemiological surveillance of human enteric viruses by monitoring of different environmental matrices. Water Sci Technol. 2006; 54(3):239-44. DOI: 10.2166/wst.2006.475. View

17.

Vincent V, Scott H, Harvey R, Alali W, Hume M . Novel surveillance of Salmonella enterica serotype Heidelberg epidemics in a closed community. Foodborne Pathog Dis. 2007; 4(3):375-85. DOI: 10.1089/fpd.2007.0025. View

18.

Talebi M, Rahimi F, Katouli M, Mollby R, Pourshafie M . Epidemiological link between wastewater and human vancomycin-resistant Enterococcus faecium isolates. Curr Microbiol. 2008; 56(5):468-73. DOI: 10.1007/s00284-008-9113-0. View

19.

Peng M, Matos O, Gatei W, Das P, Stantic-Pavlinic M, Bern C . A comparison of Cryptosporidium subgenotypes from several geographic regions. J Eukaryot Microbiol. 2002; Suppl:28S-31S. DOI: 10.1111/j.1550-7408.2001.tb00442.x. View

20.

Akinbo F, Okaka C, Omoregie R, Dearen T, Leon E, Xiao L . Molecular epidemiologic characterization of Enterocytozoon bieneusi in HIV-infected persons in Benin City, Nigeria. Am J Trop Med Hyg. 2012; 86(3):441-5. PMC: 3284359. DOI: 10.4269/ajtmh.2012.11-0548. View