Norovirus molecular detection in Uruguayan sewage samples reveals a high genetic diversity and GII.4 variant replacement along time

Journal of Applied Microbiology

Volumn 120, Issue 5, 2016, Pages 1427-1435

  Victoria, M ^a   Tort, L F L ^a   Lizasoain, A ^a   Garcia M ^a   Castells, M ^a   Berois, M ^a   Divizia, M ^b   Leite, J P G ^c   Miagostovich, M P ^c   Cristina, J ^a   Colina, R ^a  

^a UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

Genetic diversity; Genotypes; Norovirus; Sewage; Variant replacement

Indexed keywords

BIODIVERSITY; VIRUSES;

GENETICS DIVERSITIES; GENOTYPE; MOLECULAR DETECTION; MOLECULAR EPIDEMIOLOGY; NEW ORLEANS; NOROVIRUSES; ULTRACENTRIFUGATION; URUGUAY; VARIANT REPLACEMENT;

SEWAGE;

DETECTION METHOD; EPIDEMIOLOGY; GASTROENTERITIS; GENETIC VARIATION; GENOTYPE; MOLECULAR ECOLOGY; SEWAGE; VIRUS;

ARTICLE; BACTERIOPHAGE; GENETIC VARIABILITY; MOLECULAR EPIDEMIOLOGY; NONHUMAN; NOROVIRUS; NOROVIRUS GENOTYPE I.3; NOROVIRUS GENOTYPE I.4; NOROVIRUS GENOTYPE I.5; NOROVIRUS GENOTYPE I.6; NOROVIRUS GENOTYPE I.8; NOROVIRUS GENOTYPE II.1; NOROVIRUS GENOTYPE II.13; NOROVIRUS GENOTYPE II.17; NOROVIRUS GENOTYPE II.2; NOROVIRUS GENOTYPE II.4; NOROVIRUS GENOTYPE II.6; NUCLEOTIDE SEQUENCE; PHYLOGENY; PREVALENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEWAGE; ULTRACENTRIFUGATION; URUGUAY; VIRUS CONCENTRATION; VIRUS DETECTION; VIRUS STRAIN; CALICIVIRUS INFECTION; CITY; ENVIRONMENTAL MONITORING; GENETIC VARIATION; GENETICS; GENOTYPE; ISOLATION AND PURIFICATION; POLYMERASE CHAIN REACTION; VIROLOGY;

AUSTRALIA; LOUISIANA; NEW ORLEANS; NEW SOUTH WALES; SYDNEY [NEW SOUTH WALES]; UNITED STATES; URUGUAY;

MIRIDAE; NOROVIRUS;

CAPSID PROTEIN; SEWAGE;

CALICIVIRIDAE INFECTIONS; CAPSID PROTEINS; CITIES; ENVIRONMENTAL MONITORING; GENETIC VARIATION; GENOTYPE; NOROVIRUS; POLYMERASE CHAIN REACTION; SEWAGE; URUGUAY;

EID: 84962650069     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.13058     Document Type: Article

References (34)

1. Andrade, J.D., Rocha, M.S., Carvalho-Costa, F.A., Fioretti, J.M., Xavier, M.D., Nunes, Z.M., Cardoso, J., Fialho, A.M. et al. (2014) Noroviruses associated with outbreaks of acute gastroenteritis in the State of Rio Grande do Sul, Brazil, 2004-2011. J Clin Virol 61, 345-352.
2. Atmar, R.L., Opekun, A.R., Gilger, M.A., Estes, M.K., Crawford, S.E., Neill, F.H., Ramani, S., Hill, H. et al. (2014) Determination of the 50% human infectious dose for Norwalk virus. J Infect Dis 209, 1016-1022.
3. Boom, R., Sol, C.J., Salimans, M.M., Jansen, C.L., Wertheim-van Dillen, P.M. and van der Noordaa, J. (1990) Rapid and simple method for purification of nucleic acids. J Clin Microbiol 28, 495-503.
4. Boxman, I.L., Tilburg, J.J., Te Loeke, N.A., Vennema, H., Jonker, K., de Boer, E. and Koopmans, M. (2006) Detection of noroviruses in shellfish in the Netherlands. Int J Food Microbiol 108, 391-396.
5. Bull, R.A. and White, P.A. (2011) Mechanisms of GII.4 norovirus evolution. Trends Microbiol 19, 233-240.
6. Chan, M.C., Sung, J.J., Lam, R.K., Chan, P.K., Lee, N.L., Lai, R.W. and Leung, W.K. (2006) Fecal viral load and norovirus-associated gastroenteritis. Emerg Infect Dis 12, 1278-1280.
7. Eden, J.S., Hewitt, J., Lim, K.L., Boni, M.F., Merif, J., Greening, G., Ratcliff, R.M., Holmes, E.C. et al. (2014) The emergence and evolution of the novel epidemic norovirus GII.4 variant Sydney 2012. Virology 450-451, 106-113.
8. Fernández, M.D., Torres, C., Poma, H.R., Riviello-López, G., Martínez, L.C., Cisterna, D.M., Rajal, V.B., Nates, S.V. et al. (2012) Environmental surveillance of norovirus in Argentina revealed distinct viral diversity patterns, seasonality and spatio-temporal diffusion processes. Sci Total Environ 437, 262-269.
9. Fioretti, J.M., Ferreira, M.S., Victoria, M., Vieira, C.B., Xavier Mda, P., Leite, J.P. and Miagostovich, M.P. (2011) Genetic diversity of noroviruses in Brazil. Mem Inst Oswaldo Cruz 106, 942-947.
10. Fioretti, J.M., Bello, G., Rocha, M.S., Victoria, M., Leite, J.P. and Miagostovich, M.P. (2014) Temporal dynamics of norovirus GII.4 variants in Brazil between 2004 and 2012. PLoS ONE 9, e92988.
11. Fumian, T.M., Leite, J.P., Castello, A.A., Gaggero, A., Caillou, M.S. and Miagostovich, M.P. (2010) Detection of rotavirus A in sewage samples using multiplex qPCR and an evaluation of the ultracentrifugation and adsorption-elution methods for virus concentration. J Virol Methods 170, 42-46.
12. Green, K. (2013) Caliciviridae: the noroviruses. In Fields Virology ed. Knipe, D.M., Howley, P.M. et al., pp. 582-608. Philadelphia, PA: Lippincott Williams & Wilkins.
13. Hellmér, M., Paxéus, N., Magnius, L., Enache, L., Arnholm, B., Johansson, A., Bergström, T. and Norder, H. (2014) Detection of pathogenic viruses in sewage provided early warnings of hepatitis A virus and norovirus outbreaks. Appl Environ Microbiol 80, 6771-6781.
14. I.N.E. Instituto Nacional de Estadística (2011) Censos 2011. http://www5.ine.gub.uy/censos2011/index.html. Accessed November 18, 2015.
15. 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.
16. Kitajima, M., Oka, T., Haramoto, E., Takeda, N., Katayama, K. and Katayama, H. (2010) Seasonal distribution and genetic diversity of genogroups I, II, and IV noroviruses in the Tamagawa River, Japan. Environ Sci Technol 44, 7116-7122.
17. Kitajima, M., Haramoto, E., Phanuwan, C., Katayama, H. and Furumai, H. (2012) Molecular detection and genotyping of human noroviruses in influent and effluent water at a wastewater treatment plant in Japan. J Appl Microbiol 112, 605-613.
18. Kremer, J.R., Langlet, J., Skraber, S., Weicherding, P., Weber, B., Cauchie, H.M., De Landtsheer, S., Even, J. et al. (2011) Genetic diversity of noroviruses from outbreaks, sporadic cases and wastewater in Luxembourg 2008-2009. Clin Microbiol Infect 17, 1173-1176.
19. Kroneman, A., Verhoef, L., Harris, J., Vennema, H., Duizer, E., van Duynhoven, Y., Gray, J., Iturriza, M. et al. (2008) Analysis of integrated virological and epidemiological reports of norovirus outbreaks collected within the Foodborne Viruses in Europe network from 1 July 2001 to 30 June 2006. J Clin Microbiol 46, 2959-2965.
20. Mans, J., Netshikweta, R., Magwalivha, M., Van Zyl, W.B. and Taylor, M.B. (2013) Diverse norovirus genotypes identified in sewage-polluted river water in South Africa. Epidemiol Infect 141, 303-313.
21. Patel, M.M., Widdowson, M.A., Glass, R.I., Akazawa, K., Vinjé, J. and Parashar, U.D. (2008) Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg Infect Dis 14, 1224-1231.
22. Patel, M.M., Hall, A.J., Vinjé, J. and Parashar, U.D. (2009) Noroviruses: a comprehensive review. J Clin Virol 44, 1-8.
23. Pina, S., Jofre, J., Emerson, S.U., Purcell, R.H. and Girones, R. (1998) Characterization of a strain of infectious hepatitis E virus isolated from sewage in an area where hepatitis E is not endemic. Appl Environ Microbiol 64, 4485-4488.
24. Raboni, S.M., Damasio, G.A., Ferreira, C.E., Pereira, L.A., Nogueira, M.B., Vidal, L.R., Cruz, C.R. and Almeida, S.M. (2014) Acute gastroenteritis and enteric viruses in hospitalised children in southern Brazil: aetiology, seasonality and clinical outcomes. Mem Inst Oswaldo Cruz 109, 428-435.
25. Rajal, V.B., McSwain, B.S., Thompson, D.E., Leutenegger, C.M., Kildare, B.J. and Wuertz, S. (2007) Validation of hollow fiber ultrafiltration and real-time PCR using bacteriophage PP7 as surrogate for the quantification of viruses from water samples. Water Res 41, 1411-1422.
26. Rajko-Nenow, P., Waters, A., Keaveney, S., Flannery, J., Tuite, G., Coughlan, S., O'Flaherty, V. and Doré, W. (2013) Norovirus genotypes present in oysters and in effluent from a wastewater treatment plant during the seasonal peak of infections in Ireland in 2010. Appl Environ Microbiol 79, 2578-2587.
27. Romani, S., Mohebbi, S.R., Hosseini, S.M., Azimzadeh, P., Vahedi, M., Derakhshan, F. and Zali, M.R. (2012) Prevalence of norovirus infection in children and adults with acute gastroenteritis, Tehran, Iran, 2008-2009. Food Environ Virol 4, 1-5.
28. Siebenga, J.J., Vennema, H., Zheng, D.P., Vinjé, J., Lee, B.E., Pang, X.L., Ho, E.C., Lim, W. et al. (2009) Norovirus illness is a global problem: emergence and spread of norovirus GII.4 variants, 2001-2007. J Infect Dis 200, 802-812.
29. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28, 2731-2739.
30. Tran, T.N., Trainor, E., Nakagomi, T., Cunliffe, N.A. and Nakagomi, O. (2013) Molecular epidemiology of noroviruses associated with acute sporadic gastroenteritis in children: global distribution of genogroups, genotypes and GII.4 variants. J Clin Virol 56, 185-193.
31. Victoria, M., Fumian, T.M., Rocha, M.S., Dalmao, F., Leite, J.P., Girones, R. and Miagostovich, M.P. (2014a) Gastroenteric virus dissemination and influence of rainfall events in urban beaches in Brazil. J Appl Microbiol 117, 1210-1218.
32. Victoria, M., Tort, L.F., García, M., Lizasoain, A., Maya, L., Leite, J.P., Miagostovich, M.P., Cristina, J. et al. (2014b) Assessment of gastroenteric viruses from wastewater directly discharged into Uruguay River, Uruguay. Food Environ Virol 6, 116-124.
33. Vinjé, J. (2014) Advances in laboratory methods for detection and typing of norovirus. J Clin Microbiol 53, 373-381.
34. Zheng, D.P., Ando, T., Fankhauser, R.L., Beard, R.S., Glass, R.I. and Monroe, S.S. (2006) Norovirus classification and proposed strain nomenclature. Virology 346, 312-323.