Concurrent Infections of Giardia duodenalis, Enterocytozoon bieneusi, and Clostridium difficile in Children during a Cryptosporidiosis Outbreak in a Pediatric Hospital in China

PLoS Neglected Tropical Diseases

Volumn 7, Issue 9, 2013, Pages

  Wang, Lin ^a   Xiao, Lihua ^b   Duan, Liping ^b   Ye, Jianbin ^a,b   Guo, Yaqiong ^a,b   Guo, Meijin ^a   Liu, Lili ^a   Feng, Yaoyu ^a  

^a EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ARTICLE; CHILD; CHINA; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM DIFFICILE INFECTION; CONTROLLED STUDY; CRYPTOSPORIDIOSIS; DIARRHEA; ENTEROCYTOZOON; ENTEROCYTOZOON INFECTION; EPIDEMIC; FEMALE; GENOTYPE; GIARDIA LAMBLIA; GIARDIASIS; HUMAN; INFANT; MAJOR CLINICAL STUDY; MALE; MIXED INFECTION; MOLECULAR DIAGNOSIS; NUCLEOTIDE SEQUENCE; PEDIATRIC HOSPITAL; PHYLOGENY; POLYMERASE CHAIN REACTION; PRESCHOOL CHILD; RISK FACTOR; SCHOOL CHILD; SEQUENCE ANALYSIS; UNINDEXED SEQUENCE;

ADOLESCENT; CHILD; CHILD, PRESCHOOL; CHINA; CLOSTRIDIUM DIFFICILE; COINFECTION; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; DISEASE OUTBREAKS; ENTEROCYTOZOON; FEMALE; GIARDIA LAMBLIA; HOSPITALS, PEDIATRIC; HUMANS; INFANT; INFANT, NEWBORN; MALE; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA;

EID: 84884688162     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002437     Document Type: Article

References (35)

1. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, et al. (2013) Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382: 209-222.
2. Xiao L, (2010) Molecular epidemiology of cryptosporidiosis: an update. Exp Parasitol 124: 80-89.
3. Karanis P, Kourenti C, Smith H, (2007) Waterborne transmission of protozoan parasites: a worldwide review of outbreaks and lessons learnt. J Water Health 5: 1-38.
4. Yoder JS, Beach MJ, (2010) Cryptosporidium surveillance and risk factors in the United States. Exp Parasitol 124: 31-39.
5. Mare A, Man A, Toma F, Szekely E, Lorinczi L, (2007) Re-emergent etiologies: Clostridium difficile. Bacteriol Virusol Parazitol Epidemiol 52: 181-188.
6. Henriques-Gil N, Haro M, Izquierdo F, Fenoy S, del Aguila C, (2010) Phylogenetic approach to the variability of the microsporidian Enterocytozoon bieneusi and its implications for inter- and intrahost transmission. Appl Environ Microbiol 76: 3333-3342.
7. Feng Y, Xiao L, (2011) Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev 24: 110-140.
8. Matos O, Lobo ML, Xiao L, (2012) Epidemiology of Enterocytozoon bieneusi infection in Humans. J Parasitol Res 2012: 981424.
9. Kato H, Ito Y, Akahane T, Izumida S, Yokoyama T, et al. (2010) Typing of Clostridium difficile isolates endemic in Japan by sequencing of slpA and its application to direct typing. J Med Microbiol 59: 556-562.
10. Yong TS, Park SJ, Hwang UW, Yang HW, Lee KW, et al. (2000) Genotyping of Giardia lamblia isolates from humans in China and Korea using ribosomal DNA Sequences. J Parasitol 86: 887-891.
11. Wang R, Zhang X, Zhu H, Zhang L, Feng Y, et al. (2011) Genetic characterizations of Cryptosporidium spp. and Giardia duodenalis in humans in Henan, China. Exp Parasitol 127: 42-45.
12. Wang L, Zhang H, Zhao X, Zhang L, Zhang G, et al. (2013) Zoonotic Cryptosporidium species and Enterocytozoon bieneusi genotypes in HIV-positive patients on antiretroviral therapy. J Clin Microbiol 51: 557-563.
13. Zhang X, Wang Z, Su Y, Liang X, Sun X, et al. (2011) Identification and genotyping of Enterocytozoon bieneusi in China. J Clin Microbiol 49: 2006-2008.
14. Huang H, Wu S, Wang M, Zhang Y, Fang H, et al. (2008) Molecular and clinical characteristics of Clostridium difficile infection in a university hospital in Shanghai, China. Clin Infect Dis 47: 1606-1608.
15. Huang H, Fang H, Weintraub A, Nord CE, (2009) Distinct ribotypes and rates of antimicrobial drug resistance in Clostridium difficile from Shanghai and Stockholm. Clin Microbiol Infect 15: 1170-1173.
16. Yan Q, Zhang J, Chen C, Zhou H, Du P, et al. (2013) Multilocus sequence typing (MLST) analysis of 104 Clostridium difficile strains isolated from China. Epidemiol Infect 141: 195-199.
17. Feng Y, Wang L, Duan L, Gomez-Puerta LA, Zhang L, et al. (2012) Extended outbreak of cryptosporidiosis in a pediatric hospital, China. Emerg Infect Dis 18: 312-314.
18. El-Mahallawy HA, El-Din NH, Salah F, El-Arousy M, El-Naga SA, (2004) Epidemiologic profile of symptomatic gastroenteritis in pediatric oncology patients receiving chemotherapy. Pediatr Blood Cancer 42: 338-342.
19. Carraturo A, Catalani V, Tega L, (2008) Microbiological and epidemiological aspects of rotavirus and enteric adenovirus infections in hospitalized children in Italy. New Microbiol 31: 329-336.
20. Sulaiman IM, Fayer R, Bern C, Gilman RH, Trout JM, et al. (2003) Triosephosphate isomerase gene characterization and potential zoonotic transmission of Giardia duodenalis. Emerg Infect Dis 9: 1444-1452.
21. Lalle M, Pozio E, Capelli G, Bruschi F, Crotti D, et al. (2005) Genetic heterogeneity at the beta-giardin locus among human and animal isolates of Giardia duodenalis and identification of potentially zoonotic subgenotypes. Int J Parasitol 35: 207-213.
22. Caccio SM, Beck R, Lalle M, Marinculic A, Pozio E, (2008) Multilocus genotyping of Giardia duodenalis reveals striking differences between assemblages A and B. Int J Parasitol 38: 1523-1531.
23. Sulaiman IM, Fayer R, Lal AA, Trout JM, Schaefer FW, (2003) Molecular characterization of microsporidia indicates that wild mammals harbor host-adapted Enterocytozoon spp. as well as human-pathogenic Enterocytozoon bieneusi. Appl Environ Microbiol 69: 4495-4501.
24. Santin M, Fayer R, (2009) Enterocytozoon bieneusi genotype nomenclature based on the internal transcribed spacer sequence: a consensus. J Eukaryot Microbiol 56: 34-38.
25. Kato H, Kato N, Watanabe K, Iwai N, Nakamura H, et al. (1998) Identification of toxin A-negative, toxin B-positive Clostridium difficile by PCR. J Clin Microbiol 36: 2178-2182.
26. Wang Q, Zhou Y, Lv B, Fu KD, Chen L, et al. (2009) Prevalence of intestinal parasite infection in Kaifeng city, Henan Province (in Chinese). Chinese J Trop Med 9: 510-514.
27. Sun YR, Xi JW, Yao HX, Xu JL, Wang HL, et al. (2010) The prevalence of intestinal parasites of inpatients in a hospital in Zhengzhou city, Henan Province (in Chinese). Chinese J Trop Med 10: 563-566.
28. Xu LN, Wu GQ, Xi JW, Qi M, Yang N, et al. (2011) Prevalence of intestinal parasitic infection in children in a hospitalized children in Zhengzhou (in Chinese). Chinese J Trop Med 11: 17-22.
29. Jiang ZX, Xu LQ, Yu SH, Li BS, Fang YY, et al. (1997) The epidemiology of giardiasis in China (in Chinese). Chinese J Publ Health 13: 407-408.
30. Aslam S, Hamill RJ, Musher DM, (2005) Treatment of Clostridium difficile-associated disease: old therapies and new strategies. Lancet Infect Dis 5: 549-557.
31. Serdarevic F, Jones RC, Weaver KN, Black SR, Ritger KA, et al. (2012) Multi-pathogen waterborne disease outbreak associated with a dinner cruise on Lake Michigan. Epidemiol Infect 140: 621-625.
32. O'Reilly CE, Bowen AB, Perez NE, Sarisky JP, Shepherd CA, et al. (2007) A waterborne outbreak of gastroenteritis with multiple etiologies among resort island visitors and residents: Ohio, 2004. Clin Infect Dis 44: 506-512.
33. Mach O, Lu L, Creek T, Bowen A, Arvelo W, et al. (2009) Population-based study of a widespread outbreak of diarrhea associated with increased mortality and malnutrition in Botswana, January-March, 2006. Am J Trop Med Hyg 80: 812-818.
34. Smith KE, Stenzel SA, Bender JB, Wagstrom E, Soderlund D, et al. (2004) Outbreaks of enteric infections caused by multiple pathogens associated with calves at a farm day camp. Pediatr Infect Dis J 23: 1098-1104.
35. Lyras D, O'Connor JR, Howarth PM, Sambol SP, Carter GP, et al. (2009) Toxin B is essential for virulence of Clostridium difficile. Nature 458: 1176-1179.