Membrane adsorption with direct cell culture combined with reverse transcription-PCR as a fast method for identifying enteroviruses from sewage

Applied and Environmental Microbiology

Volumn 71, Issue 1, 2005, Pages 72-79

  Papaventsis, D ^a,b,c   Siafakas, N ^a,d   Markoulatos, P ^d   Papageorgiou, G T ^e   Kourtis, C ^e   Chatzichristou, E ^b   Economou, C ^b   Levidiotou, S ^c  

^a HELLENIC PASTEUR INSTITUTE   (Greece)

^b UNIVERSITY OF WEST ATTICA   (Greece)

^c UNIVERSITY OF IOANNINA   (Greece)

^d UNIVERSITY OF THESSALY   (Greece)

^e State General Laboratory of Cyprus   (Cyprus)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULOSE NITRATE MEMBRANE FILTERS; ENTEROVIRUSES; MEMBRANE ADSORPTION; REVERSE TRANSCRIPTION;

ADSORPTION; BIOLOGICAL MEMBRANES; CELLULOSE; EPIDEMIOLOGY; GENETIC ENGINEERING; NITRATES; SEWAGE TREATMENT; VIRUSES;

CELL CULTURE;

PROTEIN VP1; PYROXYLIN;

POLYMERASE CHAIN REACTION;

5' UNTRANSLATED REGION; ARTICLE; CELL CULTURE; CYPRUS; ENTEROVIRUS; ENVIRONMENTAL MONITORING; MEMBRANE FILTER; NONHUMAN; NUCLEOTIDE SEQUENCE; POLIOMYELITIS VIRUS; POLIOMYELITIS VIRUS 2; PUBLIC HEALTH; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEWAGE; SEWAGE TREATMENT; VIRUS ADSORPTION; VIRUS CLASSIFICATION; VIRUS IDENTIFICATION;

5' UNTRANSLATED REGIONS; ADSORPTION; CELL LINE; COLLODION; DNA-BINDING PROTEINS; ENTEROVIRUS; ENVIRONMENTAL MONITORING; HUMANS; MICROPORE FILTERS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT PROTEINS; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SEWAGE; TIME FACTORS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; VIROLOGY; VIRUS CULTIVATION;

ADSORPTION; CELLS; CELLULOSE; GENETIC ENGINEERING; MEMBRANES; NITRATES; SEWAGE TREATMENT; VIRUSES;

ENTEROVIRUS; HUMAN POLIOVIRUS 2; POLIOVIRUS;

EID: 12244262265     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.71.1.72-79.2005     Document Type: Article

References (41)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Meyers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 251:403-410.
2. Altschul, S. F., T. L. Madden, A. Schäffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Anonymous. 2003. Guidelines for environmental surveillance of poliovirus circulation. World Health Organization Department of Vaccines and Biologicals, Geneva, Switzerland.
4. Blomqvist, S., A. L. Bruu, M. Stenvik, and T. Hovi. 2003. Characterization of a recombinant type 3/type 2 poliovirus isolated from a healthy vaccinee and containing a chimeric capsid protein VP1. J. Gen. Virol. 84:573-580.
5. Bottiger, M., and E. Herrstrom. 1992. Isolation of polioviruses from sewage and their characteristics: experience over two decades in Sweden. Scand J. Infect. Dis. 24:151-155.
6. Casas, I., L. Powell, P. E. Klapper, and G. M. Cleator. 1995. New method for the extraction of viral RNA and DNA from cerebrospinal fluid for use in the polymerase chain reaction assay. J. Virol. Methods 53:25-36.
7. Cochi, S. L., H. F. Hull, and N. A. Ward. 1995. To conquer poliomyelitis forever. Lancet 345:1589-1590.
8. Cuervo, N. S., S. Guillot, N. Romanenkova, M. Combiescu, A. Aubert-Combiescu, M. Seghier, V. Caro, R. Crainic, and F. Delpeyroux. 2001. Genomic features of intertypic recombinant Sabin poliovirus strains excreted by primary vaccinees. J. Virol. 75:5740-5751.
9. Furione, M., S. Guillot, D. Otelea, J. Balanant, A. Candrea, and R. Crainic. 1993. Polioviruses with natural recombinant genomes isolated from vaccine-associated paralytic poliomyelitis. Virology 196:199-208.
10. Georgescu, M. M., J. Balanant, A. Macadam, D. Otelea, M. Combiescu, A. A. Combiescu, R. Crainic, and F. Delpeyroux. 1997. Evolution of the Sabin type 1 poliovirus in humans: characterization of strains isolated from patients with vaccine-associated paralytic poliomyelitis. J. Virol. 71:7758-7768.
11. Georgopoulou, A., and P. Markoulatos. 2001. Sabin type 2 polioviruses with intertypic vaccine/vaccine recombinant genomes. Eur. J. Clin. Microbiol. Infect. Dis. 20:792-799.
12. Grabow, W. O., K. L. Botma, J. C. de Villiers, C. G. Clay, and B. Erasmus. 1999. Assessment of cell culture and polymerase chain reaction procedures for the detection of polioviruses in wastewater. Bull. W. H. O. 77:973-980.
13. Guillot, S., V. Caro, N. Cuervo, E. Korotkova, M. Combiescu, A. Persu, A. Aubert-Combiescu, F. Delpeyroux, and R. Crainic. 2000. Natural genetic exchanges between vaccine and wild poliovirus strains in humans. J. Virol. 74:8434-8443.
14. King, A. M. Q., F. Brown, P. Christian, T. Hovi, T. Hyypid, N. J. Knowles, S. M. Lemon, P. D. Minor, A. C. Palmenberg, T. Skern, and G. Stanway. 2000. Picornaviridae, p. 657-673. In M. H. V. Van Regenmortel, C. M. Fauquet, D. H. L. Bishop, C. H. Calisher, E. B. Carsten, M. K. Estes, S. M. Lemon, J. Maniloff, M. A. Mayo, D. J. McGeoch, C. R. Pringle, and R. B. Wickner (ed.), Virus taxonomy. Seventh report of the International Committee for the Taxonomy of Viruses. Academic Press, New York, N.Y.
15. Markoulatos, P., A. Georgopoulou, N. Siafakas, E. Plakokefalos, G. Tzanakaki, and J. Kourea-Kremastinou. 2001. Laboratory diagnosis of common herpesvirus infections of the central nervous system by a multiplex PCR assay. J. Clin. Microbiol. 39:4426-4432.
16. Melnick, J. L. 1996. Enteroviruses: polioviruses, coxsackieviruses, echoviruses and newer enteroviruses, p. 655-712. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Virology, 3rd ed. Lippincott-Raven, Philadelphia, Pa.
17. Metcalf, T. G., J. L. Melnick, and M. K. Estes. 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.
18. Mocé-Llivina, L., J. Jofre, X. Méndez, D. Akkelidou, F. Lucena, and G. T. Papageorgiou. 2002. Counting cytopathogenic virus adsorbed to cellulose nitrate membrane filters as a simple method for counting viruses in raw sewage and sewage effluents. J. Virol. Methods 102:83-92.
19. Moce-Llivina, L., J. Jofre, and M. Muniesa. 2003. Comparison of polyvinylidene fluoride and polyether sulphonate membranes in filtering viral suspensions. J. Virol. Methods 109:99-101.
20. Muir, P., U. Kammerer, K. Korn, M. N. Mulders, T. Pöyry, B. Weissbrich, R. Kandolf, G. M. Cleator, and A. M. van Loon. 1998. Molecular typing of enteroviruses: current Status and future requirements. The European Union Concerted Action on Virus Meningitis and Encephalitis. Clin. Microbiol. Rev. 11:202-227.
21. pro cleavage site: evidence for high genomic diversity and long-term endemicity of distinct genotypes. J. Gen. Virol. 81:803-812.
22. Oberste, M. S., K. Maher, D. R. Kilpatrick, M. R. Flemister, B. A. Brown, and M. A. Pallansch. 1999. Typing of human enteroviruses by partial sequencing of VP1. J. Clin. Microbiol. 37:1288-1293.
23. Oherste, M. S., K. Maher, D. R. Kilpatrick, and M. A. Pallansch. 1999. Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J. Virol. 73:1941-1948.
24. Oberste, M. S., W. A. Nix, K. Maher, and M. A. Pallansch. 2003. Improved molecular identification of enteroviruses by RT-PCR and amplicon sequencing. J. Clin. Virol. 26:375-377.
25. Pallin, R., A. P. Wyn-Jones, B. M. Place, and N. F. Lightfoot. 1997. The detection of enteroviruses in large volume concentrates of recreational waters by the polymerase chain reaction. J. Virol. Methods 67:57-67.
26. Papageorgiou, G. T., L. Moce-Llivina, C. G. Christodoulou, F. Lucena, D. Akkelidou, E. Ioannou, and J. Jofre. 2000. A simple methodological approach for counting and identifying cytopathogenic viruses adsorbed to cellulose nitrate membrane filters. Appl. Environ. Microbiol. 66:194-198.
27. Patriarca, P. A. 1994. Polio outbreaks: a tale of torment. Lancet 344:630-631.
28. Puig, M., J. Jofre, F. Lucena, A. Allard, G. Wadell, and G. Girones. 1994. Detection of adenoviruses and enteroviruses in polluted waters by nested PCR amplification. Appl. Environ. Microbiol. 60:2963-2970.
29. Reynolds, K. A., C. P. Gerba, and I. L. Pepper. 1996. Detection of infectious enteroviruses by an integrated cell culture-PCR procedure. Appl. Environ. Microbiol. 62:1424-1427.
30. Rusin, P., C. Enriquez, D. Johnson, and C. Gerba. 2000. Enteric viruses, p. 472-484. In R. Maier, I. Pepper, and C. Gerba (ed.), Environmental microbiology, 1st ed. Academic Press, London, United Kingdom.
31. Shieh, Y. S., R. S. Baric, and M. D. Sobsey. 1997. Detection of low levels of enteric viruses in metropolitan and airplane sewage. Appl. Environ. Microbiol. 63:4401-4407.
32. Siafakas, N., A. Georgopoulou, P. Markoulatos, and N. Spyrou. 2000. Isolation of polioviruses and other enteroviruses in south Greece between 1994 and 1998. J. Clin. Lab. Anal. 14:157-163.
33. Siafakas, N., A. Georgopoulou, P. Markoulatos, N. Spyrou, and G. Stanway. 2001. Molecular detection and identification of an enterovirus during an outbreak of aseptic meningitis. J. Clin. Lab. Anal. 15:87-93.
34. Siafakas, N., P. Markoulatos, G. Stanway, G. Tzanakaki, and J. Kourea-Kremastinou. 2001. A reliable RT-PCR/RFLP assay for the molecular classification of enterovirus reference and wild type strains to either of the two genetic clusters on the basis of the 5′-UTR. Mol. Cell. Probes 16:209-216.
35. Siafakas, N., P. Markoulatos, C. Vlachos, G. Stanway, G. Tzanakaki, and J. Kourea-Kreraastinou. 2003. Molecular sub-grouping of enterovirus reference and wild type strains into distinct genetic clusters using a simple RFLP assay. Mol. Cell. Probes. 17:113-123.
36. Stanway, G. 1990. Structure, function and evolution of picornaviruses. J. Gen. Virol. 71:2483-2501.
37. Tambini, G., J. K. Andrus, E. Marques, J. Boshell, M. Pallansch, C. A. deq Uadros, and O. Kew. 1993. Direct detection of wild poliovirus circulation by stool surveys of healthy children and analysis of community wastewater. J. Infect. Dis. 168:1510-1514.
38. Thoelen, I., E. Moës, P. Lemey, S. Mostmans, E. Wolants, A. M. Lindberg, A. M. Vandamme, and M. Van Ranst. 2004. Analysis of the serotype and genotype correlation of VP1 and the 5′ noncoding region in an epidemiological survey of the human enterovirus B species. J. Clin. Microbiol. 42:963-971.
39. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
40. Van der Avoort, H. G., J. H. Reimerink, A. Ras, M. N. Mulders, and A. M. Van Loon. 1995. Isolation of epidemic poliovirus from sewage during the 1992-3 type 3 outbreak in The Netherlands. Epidemiol. Infect. 114:481-491.
41. Yang, C.-F., T. Naguib, S.-J. Yang, E. Nasr, J. Jorba, N. Ahmed, R. Campagnoli, H. van der Avoort, H. Shimizu, T. Yoneyama, T. Miyamura, M. Pallansch, and O. Kew. 2003. Circulation of endemic type 2 vaccine-derived poliovirus in Egypt from 1983 to 1993. J. Virol. 77:8366-8377.