Prevalence and genotypes of human noroviruses in tropical urban surface waters and clinical samples in Singapore

Applied and Environmental Microbiology

Volumn 75, Issue 15, 2009, Pages 4984-4992

  Aw, Tiong Gim ^a   Gin, Karina Yew Hoong ^a   Oon, Lynette Lin Ean ^b   Chen, Eileen Xueqin ^b   Woo, Chee Hoe ^c  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b SINGAPORE GENERAL HOSPITAL   (Singapore)

^c Public Utilities Board Singapore   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CLINICAL ISOLATES; CLINICAL REPORTING; CLINICAL SAMPLES; COMPARATIVE ANALYSIS; DNA SEQUENCING; ENVIRONMENTAL ISOLATES; ENVIRONMENTAL WATER SAMPLES; GENOTYPING; GLOBAL EPIDEMIC; NOROVIRUSES; NUCLEOTIDE SEQUENCES; PCR ASSAY; PHYLOGENETIC ANALYSIS; REVERSE TRANSCRIPTION; SINGAPORE; URBAN CATCHMENT; URBAN SURFACE WATERS; WATER ENVIRONMENTS; WATER SAMPLES;

CATCHMENTS; NUCLEIC ACIDS; ULTRAFILTRATION; WATER ANALYSIS;

ENVIRONMENTAL REGULATIONS;

SURFACE WATER; VIRUS DNA;

CATCHMENT; COMPARATIVE STUDY; DISEASE PREVALENCE; DNA; EMERGENCE; EPIDEMIC; GASTROENTERITIS; GENE EXPRESSION; PHYLOGENETICS; POLYMERASE CHAIN REACTION; SURFACE WATER; ULTRAFILTRATION; VIRUS;

ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; EPIDEMIC; ESTUARY; GASTROENTERITIS; GENOTYPE; HUMAN; NONHUMAN; NOROVIRUS; NUCLEOTIDE SEQUENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGAPORE; TROPICS; ULTRAFILTRATION; UNINDEXED SEQUENCE; URBAN AREA; VIRAL GENETICS; VIRUS CAPSID; VIRUS STRAIN; WATER SAMPLING;

CALICIVIRIDAE INFECTIONS; CLUSTER ANALYSIS; EPIDEMIOLOGY, MOLECULAR; GASTROENTERITIS; GENOTYPE; HUMANS; MOLECULAR SEQUENCE DATA; NOROVIRUS; PHYLOGENY; PREVALENCE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY; SINGAPORE; ULTRAFILTRATION; URBAN POPULATION; WATER MICROBIOLOGY;

ASIA; EURASIA; SINGAPORE [SOUTHEAST ASIA]; SOUTHEAST ASIA;

MIRIDAE; NOROVIRUS;

EID: 67651253197     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00489-09     Document Type: Article

References (47)

1. Ambert-Balay, K., F. Bon, F. Le Guyader, P. Pothier, and E. Kohli. 2005. Characterization of new recombinant noroviruses. J. Clin. Microbiol. 43: 5179-5186.
2. Arnone, R. D., and J. P. Walling. 2007. Waterborne pathogens in urban watersheds. J. Water Health 5:149-162.
3. Atmar, R. L., and M. K. Estes. 2001. Diagnosis of noncultivatable gastroenteritis viruses, the human caliciviruses. Clin. Microbiol. Rev. 14:15-37.
4. Bull, R. A., E. T. V. Tu, C. J. McIver, W. D. Rawlinson, and P. A. White. 2006. Emergence of a new norovirus genotype II. 4 variant associated with global outbreaks of gastroenteritis. J. Clin. Microbiol. 44:327-333.
5. Dey, S. K., T. A. Nguyen, T. G. Phan, O. Nishio, A. F. M. Salim, M. Rahman, F. Yagyu, S. Okitsu, and H. Ushijima. 2007. Molecular and epidemiological trend of norovirus associated gastroenteritis in Dhaka City, Bangladesh. J. Clin. Virol. 40:218-223.
6. Duizer, E., K. J. Schwab, F. H. Neill, R. L. Atmar, M. P. G. Koopmans, and M. K. Estes. 2004. Laboratory efforts to cultivate noroviruses. J. Gen. Virol. 85:79-87.
7. Gray, J. J., J. Green, C. Cunliffe, C. Gallimore, J. V. Lee, K. Neal, and D. W. G. Brown. 1997. Mixed genogroup SRSV infections among a party of canoeists exposed to contaminated recreational water. J. Med. Virol. 52:425-429.
8. Haramoto, E., H. Katayama, K. Oguma, and S. Ohgaki. 2005. Application of cation-coated filter method to detection of noroviruses, enteroviruses, adenoviruses, and torque teno viruses in the Tamagawa River in Japan. Appl. Environ. Microbiol. 71:2403-2411.
9. Haramoto, E., H. Katayama, and S. Ohgaki. 2004. Detection of noroviruses in tap water in Japan by means of a new method for concentrating enteric viruses in large volumes of freshwater. Appl. Environ. Microbiol. 70:2154-2160.
10. Hewitt, J., D. Bell, G. C. Simmons, M. Rivera-Aban, S. Wolf, and G. E. Greening. 2007. Gastroenteritis outbreak caused by waterborne norovirus at a New Zealand ski resort. Appl. Environ. Microbiol. 73:7853-7857.
11. Hill, V. R., A. M. Kahler, N. Jothikumar, T. B. Johnson, D. Hahn, and T. L. Cromeans. 2007. Multistate evaluation of an ultrafiltration-based procedure for simultaneous recovery of enteric microbes in 100-liter tap water samples. Appl. Environ. Microbiol. 73:4218-4225.
12. Ho, E. C. M., P. K. C. Cheng, A. W. L. Lau, A. H. Wong, and W. W. L. Lim. 2007. Atypical norovirus epidemic in Hong Kong during summer of 2006 caused by a new genogroup II/4 variant. J. Clin. Microbiol. 45:2205-2211.
13. Hoebe, C., H. Vennema, A. M. D. Husman, and Y. van Duynhoven. 2004. Norovirus outbreak among primary schoolchildren who had played in a recreational water fountain. J. Infect. Dis. 189:699-705.
14. Husman, A. M. D., P. Bijkerk, W. Lodder, H. van den Berg, W. Pribil, A. Cabaj, P. Gehringer, R. Sommer, and E. Duizer. 2004. Calicivirus inactivation by nonionizing (253.7-nanometer-wavelength [UV]) and ionizing (gamma) radiation. Appl. Environ. Microbiol. 70:5089-5093.
15. Johansen, K., K. Mannerqvist, A. Allard, Y. Andersson, L. G. Burman, L. Dillner, K. O. Hedlund, K. Jonsson, U. Kumlin, T. Leitner, M. Lysen, M. Thorhagen, A. Tiveljung-Lindell, C. Wahlstrom, B. Zweygberg-Wirgart, and A. Widell. 2008. Norovirus strains belonging to the GII. 4 genotype dominate as a cause of nosocomial outbreaks of viral gastroenteritis in Sweden 1997-2005: arrival of new variants is associated with large nationwide epidemics. J. Clin. Virol. 42:129-134.
16. Kageyama, T., S. Kojima, M. Shinohara, K. Uchida, S. Fukushi, F. B. Hoshino, N. Takeda, and K. Katayama. 2003. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J. Clin. Microbiol. 41:1548-1557.
17. Kageyama, T., M. Shinohara, K. Uchida, S. Fukushi, F. B. Hoshino, S. Kojima, R. Takai, T. Oka, N. Takeda, and K. Katayama. 2004. Coexistence of multiple genotypes, including newly identified genotypes, in outbreaks of gastroenteritis due to norovirus in Japan. J. Clin. Microbiol. 42:2988-2995.
18. Karim, M. R., and M. W. LeChevallier. 2004. Detection of noroviruses in water: current status and future directions. J. Water Supply Res. Technol. 53:359-380.
19. Kim, S. H., D. S. Cheon, J. Y. Kim, D. H. Lee, W. H. Jheong, Y. J. Heo, H. M. Chung, Y. Jee, and J. S. Lee. 2005. Outbreaks of gastroenteritis that occurred during school excursions in Korea were associated with several waterborne strains of norovirus. J. Clin. Microbiol. 43:4836-4839.
20. Kojima, S., T. Kageyama, S. Fukushi, F. B. Hoshino, M. Shinohara, K. Uchida, K. Natori, N. Takeda, and K. Katayama. 2002. Genogroup-specific PCR primers for detection of Norwalk-like viruses. J. Virol. Methods 100: 107-114.
21. La Rosa, G., S. Fontana, A. Di Grazia, M. Iaconelli, M. Pourshaban, and M. Muscillo. 2007. Molecular identification and genetic analysis of norovirus genogroups I and II in water environments: comparative analysis of different reverse transcription-PCR assays. Appl. Environ. Microbiol. 73:4152-4161.
22. Lee, C., and S.-J. Kim. 2008. The genetic diversity of human noroviruses detected in river water in Korea. Water Res. 42:4477-4484.
23. Lodder, W. J., and A. M. D. Husman. 2005. Presence of noroviruses and other enteric viruses in sewage and surface waters in The Netherlands. Appl. Environ. Microbiol. 71:1453-1461.
24. Lopmam, B. A., M. H. Reacher, Y. van Duijnhoven, F. X. Hanon, D. Brown, and M. Koopmans. 2003. Viral gastroenteritis outbreaks in Europe, 1995-2000. Emerg. Infect. Dis. 9:90-96.
25. Madaeni, S. S. 1999. The application of membrane technology for water disinfection. Water Res. 33:301-308.
26. Maunula, L., I. T. Miettinen, and C. H. von Bonsdorff. 2005. Norovirus outbreaks from drinking water. Emerg. Infect. Dis. 11:1716-1721.
27. Morales-Morales, H. A., G. Vidal, J. Olszewski, C. M. Rock, D. Dasgupta, K. H. Oshima, and G. B. Smith. 2003. Optimization of a reusable hollow-fiber ultrafilter for simultaneous concentration of enteric bacteria, protozoa, and viruses from water. Appl. Environ. Microbiol. 69:4098-4102.
28. Nayak, M. K., G. Balasubramanian, G. C. Sahoo, R. Bhattacharya, J. Vinje, N. Kobayashi, M. C. Sarkar, M. K. Bhattacharya, and T. Krishnan. 2008. Detection of a novel intergenogroup recombinant norovirus from Kolkata, India. Virology 377:117-123.
29. Ng, T. L., P. P. Chan, T. H. Phua, J. P. Loh, R. Yip, C. Wong, C. W. Liaw, B. H. Tan, K. T. Chiew, S. B. Chua, S. Lim, P. L. Ooi, S. K. Chew, and K. T. Goh. 2005. Oyster-associated outbreaks of norovirus gastroenteritis in Singapore. J. Infect. 51:413-418.
30. Nygard, K., M. Torven, C. Ancker, S. B. Knauth, K. O. Hedlund, J. Giesecke, Y. Andersson, and L. Svensson. 2003. Emerging genotype (GGIIb) of norovirus in drinking water, Sweden. Emerg. Infect. Dis. 9:1548-1552.
31. Olszewski, J., L. Winona, and K. H. Oshima. 2005. Comparison of 2 ultra-filtration systems for the concentration of seeded viruses from environmental waters. Can. J. Microbiol. 51:295-303.
32. Page, R. D. M. 1996. TREEVIEW: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12:357-358.
33. Parshionikar, S. U., S. Willian-True, G. S. Fout, D. E. Robbins, S. A. Seys, J. D. Cassady, and R. Harris. 2003. Waterborne outbreak of gastroenteritis associated with a norovirus. Appl. Environ. Microbiol. 69:5263-5268.
34. Phan, T. G., K. Kaneshi, Y. Ueda, S. Nakaya, S. Nishimura, A. Yamamoto, K. Sugita, S. Takanashi, S. Okitsu, and H. Ushijima. 2007. Genetic heterogeneity, evolution, and recombination in noroviruses. J. Med. Virol. 79: 1388-1400.
35. Rose, J. B., and S. L. Molloy. 2007. Globalization effects on water quality: monitoring the impact on and control of waterborne disease, p. 92-119. In W. W. Taylor, M. G. Schechter, and L. G. Wolfson (ed.), Globalization: effects on fisheries resources. Cambridge University Press, New York, NY.
36. Shin, G. A., and M. D. Sobsey. 2008. Inactivation of norovirus by chlorine disinfection of water. Water Res. 42:4562-4568.
37. Shin, G. A., and M. D. Sobsey. 2003. Reduction of Norwalk virus, poliovirus 1, and bacteriophage MS2 by ozone disinfection of water. Appl. Environ. Microbiol. 69:3975-3978.
38. Thurston-Enriqueza, J. A., C. N. Haas, J. Jacangelo, and C. P. Gerba. 2005. Inactivation of enteric adenovirus and feline calicivirus by ozone. Water Res. 39:3650-3656.
39. Tu, E. T. V., R. A. Bull, G. E. Greening, J. Hewitt, M. J. Lyon, J. A. Marshall, C. J. McIver, W. D. Rawlinson, and P. A. White. 2008. Epidemics of gastroenteritis during 2006 were associated with the spread of norovirus GII.4 variants 2006a and 2006b. Clin. Infect. Dis. 46:413-420.
40. Ueki, Y., D. Sano, T. Watanabe, K. Akiyama, and T. Omura. 2005. Norovirus pathway in water environment estimated by genetic analysis of strains from patients of gastroenteritis, sewage, treated wastewater, river water and oysters. Water Res. 39:4271-4280.
41. U.S. Environmental Protection Agency. 2005. Drinking water contaminant candidate list 2; final notice. Fed. Regist. 70:9071-9077.
42. van den Berg, H., W. Lodder, W. van der Poel, H. Vennema, and A. M. D. Husman. 2005. Genetic diversity of noroviruses in raw and treated sewage water. Res. Microbiol. 156:532-540.
43. Vinje, J., R. A. Hamidjaja, and M. D. Sobsey. 2004. Development and application of a capsid VP1 (region D) based reverse transcription PCR assay for genotyping of genogroup I and II noroviruses. J. Virol. Methods 116:109-117.
44. Vinje, J., and P. G. Koopmans. 1996. Molecular detection and epidemiology of small round-structured viruses in outbreaks of gastroenteritis in The Netherlands. J. Infect. Dis. 174:610-615.
45. Webby, R. J., K. S. Carville, M. D. Kirk, G. Greening, R. M. Ratcliff, S. K. Crerar, K. Dempsey, M. Sarna, R. Stafford, M. Patel, and G. Hall. 2007. Internationally distributed frozen oyster meat causing multiple outbreaks of norovirus infection in Australia. Clin. Infect. Dis. 44:1026-1031.
46. Widdowson, M. A., A. Sulka, S. N. Bulens, R. S. Beard, S. S. Chaves, R. Hammond, E. D. P. Salehi, E. Swanson, J. Totaro, R. Woron, P. S. Mead, J. S. Bresee, S. S. Monroe, and R. I. Glass. 2005. Norovirus and foodborne disease, United States, 1991-2000. Emerg. Infect. Dis. 11:95-102.
47. Zheng, D. P., T. Ando, R. L. Fankhauser, R. S. Beard, R. I. Glass, and S. S. Monroe. 2006. Norovirus classification and proposed strain nomenclature. Virology 346:312-323.