Environmental surveillance and molecular characterization of human enteric viruses in tropical urban wastewaters

Journal of Applied Microbiology

Volumn 109, Issue 2, 2010, Pages 716-730

  Aw, T G ^a   Gin, K Y H ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

enteric viruses; genotyping; noroviruses; quantitative real time PCR; urban sewage

Indexed keywords

BIODIVERSITY; EFFLUENTS; HEALTH RISKS; POLYMERASE CHAIN REACTION; TROPICS; WASTEWATER RECLAMATION;

ENTERIC VIRUS; GENOTYPING; HUMAN ENTERIC VIRUS; NOROVIRUSES; QUANTITATIVE REAL-TIME PCR; REAL-TIME PCR; SINGAPORE; TROPICAL REGIONS; URBAN SEWAGES; URBAN WASTEWATER;

SEWAGE;

DISEASE PREVALENCE; DISEASE SPREAD; GENOTYPE; HEALTH RISK; HEPATITIS; MOLECULAR ANALYSIS; POLYMERASE CHAIN REACTION; PUBLIC HEALTH; REAL TIME; SURVIVAL; TROPICAL REGION; VIRUS; WASTEWATER;

ARTICLE; ASTROVIRUS; COLIPHAGE; COXSACKIE VIRUS; EFFLUENT; ENTERIC VIRUS; ENTEROVIRUS; GENOTYPE; HEPATITIS A VIRUS; HUMAN ADENOVIRUS; NONHUMAN; NOROVIRUS; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PREVALENCE; REAL TIME POLYMERASE CHAIN REACTION; SEWAGE; SINGAPORE; UNINDEXED SEQUENCE; URBAN AREA; VIRUS CONCENTRATION; VIRUS DETECTION; WASTE WATER; WASTE WATER TREATMENT PLANT;

SINGAPORE [SOUTHEAST ASIA];

ADENOVIRIDAE; ASTROVIRIDAE; COXSACKIEVIRUS; ENTEROVIRUS; HEPATITIS A VIRUS; HUMAN ADENOVIRUS TYPE 41; NOROVIRUS;

EID: 77954464055     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2010.04701.x     Document Type: Article

References (59)

1. Albinana-Gimenez, N., Clemente-Casares, P., Bofill-Mas, S., Hundesa, A., Ribas, F. Girones, R. (2006) Distribution of human polyomaviruses, adenoviruses, and hepatitis E virus in the environment and in a drinking-water treatment plant. Environ Sci Technol 40, 7416 7422.
2. Allard, A., Albinsson, B. Wadell, G. (2001) Rapid typing of human adenoviruses by a general PCR combined with restriction endonuclease analysis. J Clin Microbiol 39, 498 505.
3. Ang, L.W., Koh, B.K.W., Chan, K.P., Chua, L.T., James, L. Goh, K.T. (2009) Epidemiology and control of hand, foot and mouth disease in Singapore, 2001-2007. Ann Acad Med Singapore 38, 106 112.
4. Arraj, A., Bohatier, J., Aumeran, C., Bailly, J.L., Laveran, H. Traore, O. (2008) An epidemiological study of enteric viruses in sewage with molecular characterization by RT-PCR and sequence analysis. J Water Health 6, 351 358.
5. Aw, T.G., Gin, K.Y.H., Oon, L.L.E., Chen, E.X. Woo, C.H. (2009) Prevalence and genotypes of human noroviruses in tropical urban surface waters and clinical samples in Singapore. Appl Environ Microbiol 75, 4984 4992.
6. Baxter, C.S., Hofmann, R., Templeton, M.R., Brown, M. Andrews, R.C. (2007) Inactivation of adenovirus types 2, 5, and 41 in drinking water by UV light, free chlorine, and monochloramine. J Environ Eng-ASCE 133, 95 103.
7. Bosch, A., Guix, S., Sano, D. Pinto, R.M. (2008) New tools for the study and direct surveillance of viral pathogens in water. Curr Opin Biotechnol 19, 295 301.
8. Bull, R.A., Tu, E.T.V., McIver, C.J., Rawlinson, W.D. White, P.A. (2006) Emergence of a new norovirus genotype II.4 variant associated with global outbreaks of gastroenteritis. J Clin Microbiol 44, 327 333.
9. Chen, C.H., Hsu, B.M. Wan, M.T. (2008) Molecular detection and prevalence of enterovirus within environmental water in Taiwan. J Appl Microbiol 104, 817 823.
10. Clancy, L.E., Craig, M.E., White, P.A. Rawlinson, W.D. (2005) Human enterovirus isolates from an outbreak typed using heteroduplex mobility analysis. J Med Virol 76, 215 222.
11. Costan-Longares, A., Moce-Llivina, L., Avellon, A., Jofre, J. Lucena, F. (2008) Occurrence and distribution of culturable enteroviruses in wastewater and surface waters of north-eastern Spain. J Appl Microbiol 105, 1945 1955.
12. Dey, S.K., Nguyen, T.A., Phan, T.G., Nishio, O., Salim, A.F.M., Rahman, M., Yagyu, F., Okitsu, S. et al. (2007) Molecular and epidemiological trend of norovirus associated gastroenteritis in Dhaka City, Bangladesh. J Clin Virol 40, 218 223.
13. Fong, T.T. Lipp, E.K. (2005) Enteric viruses of humans and animals in aquatic environments: health risks, detection, and potential water quality assessment tools. Microbiol Mol Biol Rev 69, 357 371.
14. Gabbay, Y.B., Leite, J.P.G., Oliveira, D.S., Nakamura, L.S., Nunes, M.R.T., Mascarenhas, J.D.P., Heinemann, M.B. Linhares, A.C. (2007) Molecular epidemiology of astrovirus type 1 in Belem, Brazil, as an agent of infantile gastroenteritis, over a period of 18 years (1982-2000): identification of two possible new lineages. Virus Res 129, 166 174.
15. Gersberg, R.M., Rose, M.A., Robles-Sikisaka, R. Dhar, A.K. (2006) Quantitative detection of hepatitis A virus and enteroviruses near the United States-Mexico border and correlation with levels of fecal indicator bacteria. Appl Environ Microbiol 72, 7438 7444.
16. Guix, S., Caballero, S., Villena, C., Bartolome, R., Latorre, C., Rabella, N., Simo, M., Bosch, A. et al. (2002) Molecular epidemiology of astrovirus infection in Barcelona, Spain. J Clin Microbiol 40, 133 139.
17. Hafliger, D., Gilgen, M., Luthy, J. Hubner, P. (1997) Seminested RT-PCR systems for small round structured viruses and detection of enteric viruses in seafood. Int J Food Microbiol 37, 27 36.
18. Hewitt, J., Bell, D., Simmons, G.C., Rivera-Aban, M., Wolf, S. Greening, G.E. (2007) Gastroenteritis outbreak caused by waterborne norovirus at a New Zealand ski resort. Appl Environ Microbiol 73, 7853 7857.
19. Ho, E.C.M., Cheng, P.K.C., Lau, A.W.L., Wong, A.H. Lim, W.W.L. (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.
20. Hovi, T., Stenvik, M. Rosenlew, M. (1996) Relative abundance of enterovirus serotypes in sewage differs from that in patients: clinical and epidemiological implications. Epidemiol Infect 116, 91 97.
21. Hsu, B.M., Chen, C.H. Wan, M.T. (2007) Genetic diversity of epidemic enterovirus 71 strains recovered from clinical and environmental samples in Taiwan. Virus Res 126, 69 75.
22. Iwai, M., Hasegawa, S., Obara, M., Nakamura, K., Horimoto, E., Takizawa, T., Kurata, T., Sogen, S. et al. (2009) Continuous presence of noroviruses and sapoviruses in raw sewage reflects infections among inhabitants of Toyama, Japan (2006 to 2008). Appl Environ Microbiol 75, 1264 1270.
23. Jothikumar, N., Cromeans, T.L., Hill, V.R., Lu, X., Sobsey, M.D. Erdman, D.D. (2005a) Quantitative real-time PCR assays for detection of human adenoviruses and identification of serotypes 40 and 41. Appl Environ Microbiol 71, 3131 3136.
24. Jothikumar, N., Lowther, J.A., Henshilwood, K., Lees, D.N., Hill, V.R. Vinje, J. (2005b) Rapid and sensitive detection of noroviruses by using TaqMan-based one-step reverse transcription-PCR assays and application to naturally contaminated shellfish samples. Appl Environ Microbiol 71, 1870 1875.
25. Kageyama, T., Kojima, S., Shinohara, M., Uchida, K., Fukushi, S., Hoshino, F.B., Takeda, N. Katayama, K. (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.
26. Ko, G.P., Cromeans, T.L. Sobsey, M.D. (2005) UV inactivation of adenovirus type 41 measured by cell culture mRNA RT-PCR. Water Res 39, 3643 3649.
27. Le Cann, P., Ranarijaona, S., Monpoeho, S., Le Guyader, F. Ferre, V. (2004) Quantification of human astroviruses in sewage using real-time RT-PCR. Res Microbiol 155, 11 15.
28. Lee, C. Kim, S.-J. (2008) The genetic diversity of human noroviruses detected in river water in Korea. Water Res 42, 4477 4484.
29. Lipson, S.M., Walderman, R., Costello, P. Szabo, K. (1988) Sensitivity of rhabdomyosarcoma and guinea pig embryo cell cultures to field isolates of difficult-to-cultivate group A coxsackieviruses. J Clin Microbiol 26, 1298 1303.
30. Meleg, E., Jakab, F., Kocsis, B., Banyai, K., Melegh, B. Szucs, G. (2006) Human astroviruses in raw sewage samples in Hungary. J Appl Microbiol 101, 1123 1129.
31. Metcalf, T.G., Melnick, J.L. Estes, M.K. (1995) Environmental virology: from detection of virus in sewage and water by isolation to identification by molecular biology-a trip of over 50 years. Annu Rev Microbiol 49, 461 487.
32. Muir, P., Kammerer, U., Korn, K., Mulders, M.N., Poyry, T., Weissbrich, B., Kandolf, R., Cleator, G.M. et al. (1998) Molecular typing of enteroviruses: current status and future requirements. Clin Microbiol Rev 11, 202 227.
33. Mustafa, H., Palombo, E.A. Bishop, R.F. (2000) Epidemiology of astrovirus infection in young children hospitalized with acute gastroenteritis in Melbourne, Australia, over a period of four consecutive years, 1995 to 1998. J Clin Microbiol 38, 1058 1062.
34. Myrmel, M., Berg, E.M.M., Grinde, B. Rimstad, E. (2006) Enteric viruses in inlet and outlet samples from sewage treatment plants. J Water Health 4, 197 209.
35. Nadan, S., Walter, J.E., Grabow, W.O.K., Mitchell, D.K. Taylor, M.B. (2003) Molecular characterization of astroviruses by reverse transcriptase PCR and sequence analysis: comparison of clinical and environmental isolates from South Africa. Appl Environ Microbiol 69, 747 753.
36. Nguyen, T.A., Hoang, L., Pham, L.D., Hoang, K.T., Mizuguchi, M., Okitsu, S. Ushijima, H. (2008) Identification of human astrovirus infections among children with acute gastroenteritis in the southern part of Vietnam during 2005-2006. J Med Virol 80, 298 305.
37. Oberste, M.S., Maher, K., Michele, S.M., Belliot, G., Uddin, M. Pallansch, M.A. (2005) Enteroviruses 76, 89, 90 and 91 represent a novel group within the species human enterovirus A. J Gen Virol 86, 445 451.
38. Oh, D.Y., Gaedicke, G. Schreier, E. (2003) Viral agents of acute gastroenteritis in German children: prevalence and molecular diversity. J Med Virol 71, 82 93.
39. Page, R.D.M. (1996) Treeview: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12, 357 358.
40. Papaventsis, D., Siafakas, N., Markoulatos, P., Papageorgiou, G.T., Kourtis, C., Chatzichristou, E., Economou, C. Levidiotou, S. (2005) Membrane adsorption with direct cell culture combined with reverse transcription-PCR as a fast method for identifying enteroviruses from sewage. Appl Environ Microbiol 71, 72 79.
41. Parshionikar, S.U., Willian-True, S., Fout, G.S., Robbins, D.E., Seys, S.A., Cassady, J.D. Harris, R. (2003) Waterborne outbreak of gastroenteritis associated with a norovirus. Appl Environ Microbiol 69, 5263 5268.
42. Petrinca, A.R., Donia, D., Pierangeli, A., Gabrieli, R., Degener, A.M., Bonanni, E., Diaco, L., Cecchini, G. et al. (2009) Presence and environmental circulation of enteric viruses in three different wastewater treatment plants. J Appl Microbiol 106, 1608 1617.
43. Pina, S., Puig, M., Lucena, F., Jofre, J. Girones, R. (1998) Viral pollution in the environment and in shellfish: human adenovirus detection by PCR as an index of human viruses. Appl Environ Microbiol 64, 3376 3382.
44. Pina, S., Buti, M., Jardi, R., Clemente-Casares, P., Jofre, J. Girones, R. (2001) Genetic analysis of hepatitis A virus strains recovered from the environment and from patients with acute hepatitis. J Gen Virol 82, 2955 2963.
45. Robertson, B.H. Nicholson, J.K.A. (2005) New microbiology tools for public health and their implications. Annu Rev Public Health 26, 281 302.
46. Robertson, B.H., Jansen, R.W., Khanna, B., Totsuka, A., Nainan, O.V., Siegl, G., Widell, A., Margolis, H.S. et al. (1992) Genetic relatedness of hepatitis A virus strains recovered from different geographical regions. J Gen Virol 73, 1365 1377.
47. Sapkal, G.N., Bondre, V.P., Fulmali, P.V., Patil, P., Gopalkrishna, V., Dadhania, V., Ayachit, V.M., Gangale, D. et al. (2009) Enteroviruses in patients with acute encephalitis, Uttar Pradesh, India. Emerg Infect Dis 15, 295 298.
48. Savichtcheva, O. Okabe, S. (2006) Alternative indicators of fecal pollution: relations with pathogens and conventional indicators, current methodologies for direct pathogen monitoring and future application perspectives. Water Res 40, 2463 2476.
49. Schmidt, N.J., Ho, H.H. Lennette, E.H. (1975) Propagation and isolation of group A coxsackieviruses in RD cells. J Clin Microbiol 2, 183 185.
50. Shieh, Y.S.C., Wait, D., Tai, L. Sobsey, M.D. (1995) Methods to remove inhibitors in sewage and other fecal wastes for enterovirus detection by the polymerase chain reaction. J Virol Methods 54, 51 66.
51. Shieh, Y.S.C., Baric, R.S. Sobsey, M.D. (1997) Detection of low levels of enteric viruses in metropolitan and airplane sewage. Appl Environ Microbiol 63, 4401 4407.
52. Symonds, E.M., Griffin, D.W. Breitbart, M. (2009) Eukaryotic viruses in wastewater samples from the United States. Appl Environ Microbiol 75, 1402 1409.
53. Tu, E.T.V., Bull, R.A., Greening, G.E., Hewitt, J., Lyon, M.J., Marshall, J.A., McIver, C.J., Rawlinson, W.D. et al. (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.
54. Ueki, Y., Sano, D., Watanabe, T., Akiyama, K. Omura, T. (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.
55. +) and Somatic Coliphage in Water by Single Agar Layer (SAL) Procedure No. EPA 821-R-01-029.
56. Wong, M., Xagoraraki, I. Rose, J.B. (2007) Recent advances and future needs in environmental virology. In Human Viruses in Water ed Bosch, A. pp. 259 284
57. Wyn-Jones, A.P. Sellwood, J. (2001) Enteric viruses in the aquatic environment. J Appl Microbiol 91, 945 962.
58. Yee, E.L., Palacio, H., Atmar, R.L., Shah, U., Kilborn, C., Faul, M., Gavagan, T.E., Feigin, R.D. et al. (2007) Widespread outbreak of norovirus gastroenteritis among evacuees of hurricane Katrina residing in a large "megashelter" in Houston, Texas: lessons learned for prevention. Clin Infect Dis 44, 1032 1039.
59. Yeo, D.S.Y., Seah, S.G.K., Chew, J.S.W., Lim, E.A.S., Liaw, J.C.W., Loh, J.P. Tan, B.H. (2007) Molecular identification of coxsackievirus A24 variant, isolated from an outbreak of acute hemorrhagic conjunctivitis in Singapore in 2005. Arch Virol 152, 2005 2016.