Methods to detect infectious human enteric viruses in environmental water samples

International Journal of Hygiene and Environmental Health

Volumn 214, Issue 6, 2011, Pages 424-436

  Hamza, Ibrahim Ahmed ^a   Jurzik, Lars ^a   Überla, Klaus ^a   Wilhelm, Michael ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Cell culture; Enteric viruses; Infectivity; PCR; Water contamination

Indexed keywords

CAPSID PROTEIN; COLORING AGENT; ENZYME; VIRUS RNA;

ANIMAL; ARTICLE; CHEMISTRY; CULTURE TECHNIQUE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN; IMMUNOMAGNETIC SEPARATION; ISOLATION AND PURIFICATION; MICROBIOLOGY; OXIDATION REDUCTION REACTION; POLYMERASE CHAIN REACTION; VIRUS;

ANIMALS; CAPSID PROTEINS; CELL CULTURE TECHNIQUES; COLORING AGENTS; ENZYMES; FLOW CYTOMETRY; HUMANS; IMMUNOMAGNETIC SEPARATION; MICROSCOPY, FLUORESCENCE; OXIDATION-REDUCTION; POLYMERASE CHAIN REACTION; RNA, VIRAL; VIRUSES; WATER MICROBIOLOGY;

ANIMALIA; MIRIDAE;

EID: 81555197043     PISSN: 14384639     EISSN: 1618131X     Source Type: Journal    
DOI: 10.1016/j.ijheh.2011.07.014     Document Type: Article

References (169)

1. Abad F.X., Pinto R.M., Bosch A. Flow cytometry detection of infectious rotaviruses in environmental and clinical samples. Appl. Environ. Microbiol. 1998, 64:2392-2396.
2. Abad F.X., Pinto R.M., Villena C., Gajardo R., Bosch A. Astrovirus survival in drinking water. Appl. Environ. Microbiol. 1997, 63:3119-3122.
3. Abbaszadegan M., Huber M.S., Gerba C.P., Pepper I.L. Detection of enteroviruses in groundwater with the polymerase chain reaction. Appl. Environ. Microbiol. 1993, 59:1318-1324.
4. Abd El Galil K.H., El Sokkary M.A., Kheira S.M., Salazar A.M., Yates M.V., Chen W., Mulchandani A. Combined immunomagnetic separation-molecular beacon-reverse transcription-PCR assay for detection of hepatitis A virus from environmental samples. Appl. Environ. Microbiol. 2004, 70:4371-4374.
5. Abd El Galil K.H., El Sokkary M.A., Kheira S.M., Salazar A.M., Yates M.V., Chen W., Mulchandani A. Real-time nucleic acid sequence-based amplification assay for detection of hepatitis A virus. Appl. Environ. Microbiol. 2005, 71:7113-7116.
6. Al-Nasrawi K.K., Al Diwan J.K., Al-Hadithi T.S., Saleh A.M. Viral hepatitis E outbreak in Al-Sadr city, Baghdad, Iraq. East Mediterr. Health J. 2010, 16:1128-1132.
7. Ali M.A., Abdel-Dayem T.M.K. Myocarditis: an expected health hazard associated with water resources contaminated with Coxsackie viruses type B. Int. J. Environ. Health Res. 2003, 13:261-270.
8. Ali M.A., Al-Herrawy A.Z., El-Hawaary S.E. Detection of enteric viruses, Giardia and Cryptosporidium in two different types of drinking water treatment facilities. Water Res. 2004, 38:3931-3939.
9. Allain J.P., Hsu J., Pranmeth M., Hanson D., Stassinopoulos A., Fischetti L., Corash L., Lin L. Quantification of viral inactivation by photochemical treatment with amotosalen and UV A light, using a novel polymerase chain reaction inhibition method with preamplification. J. Infect. Dis. 2006, 194:1737-1744.
10. Allander T., Tammi M.T., Eriksson M., Bjerkner A., Tiveljung-Lindell A., Andersson B. Cloning of a human parvovirus by molecular screening of respiratory tract samples. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:12891-12896.
11. Anderson A.D., Heryford A.G., Sarisky J.P., Higgins C., Monroe S.S., Beard R.S., Newport C.M., Cashdollar J.L., Fout G.S., Robbins D.E., Seys S.A., Musgrave K.J., Medus C., Vinje J., Bresee J.S., Mainzer H.M., Glass R.I. A waterborne outbreak of Norwalk-like virus among snowmobilers-Wyoming, 2001. J. Infect. Dis. 2003, 187:303-306.
12. Andorrà I., Esteve-Zarzoso B., Guillamón J.M., Mas A. Determination of viable wine yeast using DNA binding dyes and quantitative PCR. Int. J. Food Microbiol. 2010, 144:257-262.
13. Bae S., Wuertz S. Discrimination of viable and dead fecal Bacteroidales bacteria by quantitative PCR with propidium monoazide. Appl. Environ. Microbiol. 2009, 75:2940-2944.
14. Bae S., Wuertz S. Rapid decay of host-specific fecal Bacteroidales cells in seawater as measured by quantitative PCR with propidium monoazide. Water Res. 2009, 43:4850-4859.
15. Baert L., Wobus C.E., Van Coillie E., Thackray L.B., Debevere J., Uyttendaele M. Detection of murine norovirus 1 by using plaque assay, transfection assay, and real-time reverse transcription-PCR before and after heat exposure. Appl. Environ. Microbiol. 2008, 74:543-546.
16. Balkin H.B., Margolin A.B. Detection of poliovirus by ICC/qPCR in concentrated water samples has greater sensitivity and is less costly using BGM cells in suspension as compared to monolayers. Virol. J. 2010, 7.
17. Ballester N.A., Fontaine J.H., Margolin A.B. Occurrence and correlations between coliphages and anthropogenic viruses in the Massachusetts Bay using enrichment and ICC-nPCR. J. Water Health 2005, 3:59-68.
18. Barardi C.R.M., Emslie K.R., Vesey G., Williams K.L. Development of a rapid and sensitive quantitative assay for rotavirus based on flow cytometry. J. Virol. Methods 1998, 74:31-38.
19. Begier E.M., Oberste M.S., Landry M.L., Brennan T., Mlynarski D., Mshar P.A., Frenette K., Rabatsky-Ehr T., Purviance K., Nepaul A., Nix W.A., Pallansch M.A., Ferguson D., Cartter M.L., Hadler J.L. An outbreak of concurrent echovirus 30 and coxsackievirus A1 infections associated with sea swimming among a group of travelers to Mexico. Clin. Infect. Dis. 2008, 47:616-623.
20. Belsham G.J., Normann P. Dynamics of picornavirus RNA replication within infected cells. J. Gen. Virol. 2008, 89:485-493.
21. Bertrand I., Maux M., Helmi K., Hoffmann L., Schwartzbrod J., Cauchie H.M. Quantification of Giardia transcripts during in vitro excystation: interest for the estimation of cyst viability. Water Res. 2009, 43:2728-2738.
22. Blackmer F., Reynolds K.A., Gerba C.P., Pepper I.L. Use of integrated cell culture-PCR to evaluate the effectiveness of poliovirus inactivation by chlorine. Appl. Environ. Microbiol. 2000, 66:2267-2268.
23. Boccia D., Tozzi A.E., Cotter B., Rizzo C., Russo T., Buttinelli G., Caprioli A., Marziano M.L., Ruggeri F.M. Waterborne outbreak of Norwalk-like virus gastroenteritis at a tourist resort, Italy. Emerg. Infect. Dis. 2002, 8:563-568.
24. Bofill-Mas S., Albinana-Gimenez N., Clemente-Casares P., Hundesa A., Rodriguez-Manzano J., Allard A., Calvo M., Girones R. Quantification and stability of human adenoviruses and polyomavirus JCPyV in wastewater matrices. Appl. Environ. Microbiol. 2006, 72:7894-7896.
25. Bofill-Mas S., Rodriguez-Manzano J., Calgua B., Carratala A., Girones R. Newly described human polyomaviruses Merkel cell, KI and WU are present in urban sewage and may represent potential environmental contaminants. Virol J 2010, 7:141.
26. Bosch A., Pinto R.M., Comas J., Abad F.X. Detection of infectious rotaviruses by flow cytometry. Methods Mol. Biol. 2004, 268:61-68.
27. Braid M.D., Daniels L.M., Kitts C.L. Removal of PCR inhibitors from soil DNA by chemical flocculation. J. Microbiol. Methods 2003, 52:389-393.
28. Brescia C.C., Griffin S.M., Ware M.W., Varughese E.A., Egorov A.I., Villegas E.N. Cryptosporidium propidium monoazide-PCR, a molecular biology-based technique for genotyping of viable Cryptosporidium oocysts. Appl. Environ. Microbiol. 2009, 75:6856-6863.
29. Brooks H.A., Gersberg R.M., Dhar A.K. Detection and quantification of hepatitis A virus in seawater via real-time RT-PCR. J. Virol. Methods 2005, 127:109-118.
30. Calgua B., Barardi C.R.M., Bofill-Mas S., Rodriguez-Manzano J., Girones R. Detection and quantitation of infectious human adenoviruses and JC polyomaviruses in water by immunofluorescence assay. J. Virol. Methods 2011, 171:1-7.
31. Cantera J.L., Chen W., Yates M.V. Detection of infective poliovirus by a simple, rapid, and sensitive flow cytometry method based on fluorescence resonance energy transfer technology. Appl. Environ. Microbiol. 2010, 76:584-588.
32. Cao J.Y., Wang Y., Song H.Y., Meng Q.L., Sheng L.P., Bian T., Mahemuti W.Q., Yierhali A., Omata M., Bi S.L. Hepatitis A outbreaks in China during 2006: application of molecular epidemiology. Hepatol. Int. 2009, 3:356-363.
33. Carriere M., Pene V., Breiman A., Conti F., Chouzenoux S., Meurs E., Andrieu M., Jaffray P., Grira L., Soubrane O., Sogni P., Calmus Y., Chaussade S., Rosenberg A.R., Podevin P. A novel, sensitive, and specific RT-PCR technique for quantitation of hepatitis C virus replication. J. Med. Virol. 2007, 79:155-160.
34. Casas N., Sunen E. Detection of enteroviruses, hepatitis A virus and rotaviruses in sewage by means of an immunomagnetic capture reverse transcription-PCR assay. Microbiol. Res. 2002, 157:169-175.
35. Chang B., Taguri T., Sugiyama K., Amemura-Maekawa J., Kura F., Watanabe H. Comparison of ethidium monoazide and propidium monoazide for the selective detection of viable Legionella cells. Jpn. J. Infect. Dis. 2010, 63:119-123.
36. Chapron C.D., Ballester N.A., Fontaine J.H., Frades C.N., Margolin A.B. Detection of astroviruses, enteroviruses, and adenovirus types 40 and 41 in surface waters collected and evaluated by the information collection rule and an integrated cell culture-nested PCR procedure. Appl. Environ. Microbiol. 2000, 66:2520-2525.
37. Chen N.T., Chang C.W. Rapid quantification of viable legionellae in water and biofilm using ethidium monoazide coupled with real-time quantitative PCR. J. Appl. Microbiol. 2010, 109:623-634.
38. Choi S., Jiang S.C. Real-time PCR quantification of human adenoviruses in urban rivers indicates genome prevalence but low infectivity. Appl. Environ. Microbiol. 2005, 71:7426-7433.
39. Dahling D.R., Berg G., Berman D. BGM, a continuous cell line more sensitive than primary rhesus and African-green kidney-cells for recovery of viruses from water. Health Lab. Sci. 1974, 11:275-282.
40. Dahling D.R., Wright B.A. Optimization of the BGM cell line culture and viral assay procedures for monitoring viruses in the environment. Appl. Environ. Microbiol. 1986, 51:790-812.
41. Demeke T., Adams R.P. The effects of plant polysaccharides and buffer additives on PCR. Biotechniques 1992, 12:332.
42. Divizia M., Gabrieli R., Donia D., Macaluso A., Bosch A., Guix S., Sanchez G., Villena C., Pinto R.M., Palombi L., Buonuomo E., Cenko F., Leno L., Bebeci D., Bino S. Waterborne gastroenteritis outbreak in Albania. Water Sci. Technol. 2004, 50:57-61.
43. Duizer E., Bijkerk P., Rockx B., de Groot A., Twisk F., Koopmans M. Inactivation of caliciviruses. Appl. Environ. Microbiol. 2004, 70:4538-4543.
44. Ehlers M.M., Grabow W.O., Pavlov D.N. Detection of enteroviruses in untreated and treated drinking water supplies in South Africa. Water Res. 2005, 39:2253-2258.
45. El-Senousy W.M., Guix S., Abid I., Pinto R.M., Bosch A. Removal of astrovirus from water and sewage treatment plants, evaluated by a competitive reverse transcription-PCR. Appl. Environ. Microbiol. 2007, 73:164-167.
46. El Hassan M., Braam S.R., Kruyt F.A.E. A real-time RT-PCR assay for the quantitiative determination of adenoviral gene expression in tumor cells. J. Virol. Methods 2006, 133:53-61.
47. Enriquez C.E., Gerba C.P. Concentration of enteric adenovirus 40 from tap, sea and waste water. Water Res. 1995, 29:2554-2560.
48. Fittipaldi M., Rodriguez N.J., Codony F., Adrados B., Penuela G.A., Morato J. Discrimination of infectious bacteriophage T4 virus by propidium monoazide real-time PCR. J. Virol. Methods 2010, 168:228-232.
49. Flekna G., Stefanic P., Wagner M., Smulders F.J., Mozina S.S., Hein I. Insufficient differentiation of live and dead Campylobacter jejuni and Listeria monocytogenes cells by ethidium monoazide (EMA) compromises EMA/real-time PCR. Res. Microbiol. 2007, 158:405-412.
50. Fout G.S., Hill F.W.S., Roberts V.R., Dahling V.D.R., Stetler R.E. ICR Microbial Laboratory Manual 1996, U.S. Environmental Protection Agency, Washington, DC.
51. Frosner G.G., Deinhardt F., Scheid R., Gauss-Muller V., Holmes N., Messelberger V., Siegl G., Alexander J.J. Propagation of human hepatitis A virus in a hepatoma cell line. Infection 1979, 7:303-305.
52. Gantzer C., Maul A., Audic J.M., Schwartzbrod L. Detection of infectious enteroviruses, enterovirus genomes, somatic coliphages, and Bacteroides fragilis phages in treated wastewater. Appl. Environ. Microbiol. 1998, 64:4307-4312.
53. Gerrity D., Ryu H., Crittenden J., Abbaszadegan M. UV inactivation of Adenovirus Type 4 measured by integrated cell culture qPCR. J. Environ. Sci. Health A: Tox. Hazard. Subst. Environ. Eng. 2008, 43:1628-1638.
54. Gilpatrick S.G., Schwab K.J., Estes M.K., Atmar R.L. Development of an immunomagnetic capture reverse transcription-PCR assay for the detection of Norwalk virus. J. Virol. Methods 2000, 90:69-78.
55. Grabow W.O.K. Chapter 1. Overview of health-related water virology. Perspectives in Medical Virology 2007, 1-25. Elsevier. B. Albert (Ed.).
56. Graiver D.A., Saunders S.E., Topliff C.L., Kelling C.L., Bartelt-Hunt S.L. Ethidium monoazide does not inhibit RT-PCR amplification of nonviable avian influenza RNA. J. Virol. Methods 2010, 164:51-54.
57. Grimm A.C., Cashdollar J.L., Williams F.P., Fout G.S. Development of an astrovirus RT-PCR detection assay for use with conventional, real-time, and integrated cell culture/RT-PCR. Can. J. Microbiol. 2004, 50:269-278.
58. Grinde B., Jonassen T.O., Ushijima H. Sensitive detection of group-A rotaviruses by immunomagnetic separation and reverse transcription-polymerase chain-reaction. J. Virol. Methods 1995, 55:327-338.
59. Hamza I.A., Jurzik L., Stang A., Sure K., Uberla K., Wilhelm M. Detection of human viruses in rivers of a densly-populated area in Germany using a virus adsorption elution method optimized for PCR analyses. Water Res. 2009, 43:2657-2668.
60. Hamza I.A., Jurzik L., Uberla K., Wilhelm M. Evaluation of pepper mild mottle virus, human picobirnavirus and Torque teno virus as indicators of fecal contamination in river water. Water Res. 2011, 45:1358-1368.
61. Hamza I.A., Jurzik L., Wilhelm M., Uberla K. Detection and quantification of human bocavirus in river water. J. Gen. Virol. 2009, 90:2634-2637.
62. Haramoto E., Kitajima M., Katayama H., Ohgaki S. Real-time PCR detection of adenoviruses, polyomaviruses, and torque teno viruses in river water in Japan. Water Res. 2010, 44:1747-1752.
63. Harley D., Harrower B., Lyon M., Dick A. A primary school outbreak of pharyngoconjunctival fever caused by adenovirus type 3. Commun. Dis. Intell. 2001, 25:9-12.
64. Hashimoto S., Sakakibara N., Kumai H., Nakai M., Sakuma S., Chiba S., Fujinaga K. Fastidious human adenovirus type 40 can propagate efficiently and produce plaques on a human cell line, A549, derived from lung carcinoma. J. Virol. 1991, 65:2429-2435.
65. Hauri A.M., Schimmelpfennig M., Walter-Domes M., Letz A., Diedrich S., Lopez-Pila J., Schreier E. An outbreak of viral meningitis associated with a public swimming pond. Epidemiol. Infect. 2005, 133:291-298.
66. Hewitt J., Bell D., Simmons G.C., Rivera-Aban M., Wolf S., Greening G.E. Gastroenteritis outbreak caused by waterborne norovirus at a New Zealand ski resort. Appl. Environ. Microbiol. 2007, 73:7853-7857.
67. Hoebe C., Vennema H., Husman A.M.D., van Duynhoven Y. Norovirus outbreak among primary schoolchildren who had played in a recreational water fountain. J. Infect. Dis. 2004, 189:699-705.
68. Hovi T., Roivainen M., Blomqvist S. Chapter 4. Enteroviruses with special reference to poliovirus and poliomyelitis eradication. Perspectives in Medical Virology 2007, 69-89. Elsevier. B. Albert (Ed.).
69. Hwang Y.C., Leong O.M., Chen W., Yates M.V. Comparison of a reporter assay and immunomagnetic separation real-time reverse transcription-PCR for the detection of enteroviruses in seeded environmental water samples. Appl. Environ. Microbiol. 2007, 73:2338-2340.
70. Hwang Y.-C., Chen W., Yates M.V. Use of fluorescence resonance energy transfer for rapid detection of enteroviral infection in vivo. Appl. Environ. Microbiol. 2006, 72:3710-3715.
71. Jeffery K., Aarons E. Diagnostic approaches. Principles and Practice of Clinical Virology 2009, 1-27. John Wiley & Sons. A.J. Zuckerman, J.E.B. Barry, D. Schoub, P.D. Griffiths, P. Mortimer (Eds.).
72. Jiang S.C. Human adenoviruses in water: occurrence and health implications: a critical review. Environ. Sci. Technol. 2006, 40:7132-7140.
73. Jiang Y.J., Liao G.Y., Zhao W., Sun M.B., Qian Y., Bian C.X., Jiang S.D. Detection of infectious hepatitis A virus by integrated cell culture/strand-specific reverse transcriptase-polymerase chain reaction. J. Appl. Microbiol. 2004, 97:1105-1112.
74. Jones E.L., Gaither M., Kramer A., Gerba C.P. An analysis of water quality in the Colorado River, 2003-04; an investigation into recurring outbreaks of norovirus among rafters. Wilderness Environ. Med. 2009, 20:6-13.
75. Jothikumar N., Cliver D.O., Mariam T.W. Immunomagnetic capture PCR for rapid concentration and detection of hepatitis A virus from environmental samples. Appl. Environ. Microbiol. 1998, 64:504-508.
76. Kim K., Katayama H., Kitajima M., Tohya Y., Ohgaki S. Development of a real-time RT-PCR assay combined with ethidium monoazide treatment for RNA viruses and its application to detect viral RNA after heat exposure. Water Sci. Technol. 2011, 63:502-507.
77. Ko G., Cromeans T.L., Sobsey M.D. Detection of infectious adenovirus in cell culture by mRNA reverse transcription-PCR. Appl. Environ. Microbiol. 2003, 69:7377-7384.
78. Ko G., Cromeans T.L., Sobsey M.D. UV inactivation of adenovirus type 41 measured by cell culture mRNA RT-PCR. Water Res. 2005, 39:3643-3649.
79. Kobayashi H., Oethinger M., Tuohy M.J., Hall G.S., Bauer T.W. Distinction between intact and antibiotic-inactivated bacteria by real-time PCR after treatment with propidium monoazide. J. Orthop. Res. 2010, 28:1245-1251.
80. Kok T.W., Pryor T., Payne L. Comparison of rhabdomyosarcoma, buffalo green monkey kidney epithelial, A549 (human lung epithelial) cells and human embryonic lung fibroblasts for isolation of enteroviruses from clinical samples. J. Clin. Virol. 1998, 11:61-65.
81. Koonjul P.K., Brandt W.F., Farrant J.M., Lindsey G.G. Inclusion of polyvinylpyrrolidone in the polymerase chain reaction reverses the inhibitory effects of polyphenolic contamination of RNA. Nucleic Acids Res. 1999, 27:915-916.
82. Koroglu M., Yakupogullari Y., Otlu B., Ozturk S., Ozden M., Ozer A., Sener K., Durmaz R. A waterborne outbreak of epidemic diarrhea due to group A rotavirus in Malatya, Turkey. New Microbiol. 2011, 34:17-24.
83. Kreader C.A. Relief of amplification inhibition in PCR with bovine serum albumin or T4 gene 32 protein. Appl. Environ. Microbiol. 1996, 62:1102-1106.
84. Kuhn R.C., Rock C.M., Oshima K.H. Effects of pH and magnetic material on immunomagnetic separation of Cryptosporidium oocysts from concentrated water samples. Appl. Environ. Microbiol. 2002, 68:2066-2070.
85. Lee H.K., Jeong Y.S. Comparison of total culturable virus assay and multiplex integrated cell culture-PCR for reliability of waterborne virus detection. Appl. Environ. Microbiol. 2004, 70:3632-3636.
86. Lee C., Lee S.H., Han E., Kim S.J. Use of cell culture-PCR assay based on combination of A549 and BGMK cell lines and molecular identification as a tool to monitor infectious adenoviruses and enteroviruses in river water. Appl. Environ. Microbiol. 2004, 70:6695-6705.
87. Lee C.S., Lee J.H., Kwon K.S. Outbreak of hepatitis A in Korean military personnel. Int. J. Infect. Dis. 2008, 12:E88.
88. Lee S.H., Lee C., Lee K.W., Cho H.B., Kim S.J. The simultaneous detection of both enteroviruses and adenoviruses in environmental water samples including tap water with an integrated cell culture-multiplex-nested PCR procedure. J. Appl. Microbiol. 2005, 98:1020-1029.
89. Leland D.S., Ginocchio C.C. Role of cell culture for virus detection in the age of technology. Clin. Microbiol. Rev. 2007, 20:49-78.
90. Leung W.K., To K.F., Chan p.K., Wu A.K., Lee N., Yuen K.Y., Sung J.J. Enteric involvement of severe acute respiratory syndrome assoicated coronavirus infection. Gastroenterology 2003, 125:1011-1017.
91. Levine R.L., Williams J.A., Stadtman E.R., Shacter E. Carbonyl assays for determination of oxidatively modified proteins. Oxygen Radicals in Biological Systems, Pt C 1994, pp. 346-357.
92. Li D., Gu A.Z., He M., Shi H.-C., Yang W. UV inactivation and resistance of rotavirus evaluated by integrated cell culture and real-time RT-PCR assay. Water Res. 2009, 43:3261-3269.
93. Li D., Gu A.Z., Yang W., He M., Hu X.H., Shi H.C. An integrated cell culture and reverse transcription quantitative PCR assay for detection of infectious rotaviruses in environmental waters. J. Microbiol. Methods 2010, 82:59-63.
94. Li D., He M., Jiang S.C. Detection of infectious adenoviruses in environmental waters by fluorescence-activated cell sorting assay. Appl. Environ. Microbiol. 2010, 76:1442-1448.
95. Li J.W., Xin Z.T., Wang X.W., Zheng J.L., Chao F.H. Mechanisms of inactivation of hepatitis a virus by chlorine. Appl. Environ. Microbiol. 2002, 68:4951-4955.
96. Li Y., Pan Z., Ji Y., Peng T., Archard L.C., Zhang H. Enterovirus replication in valvular tissue from patients with chronic rheumatic heart disease. Eur. Heart J. 2002, 23:567-573.
97. Lin W.T., Luo J.F., Guo Y. Comparison and characterization of microbial communities in sulfide-rich wastewater with and without propidium monoazide treatment. Curr. Microbiol. 2011, 62:374-381.
98. Lindesmith L., Moe C., Marionneau S., Ruvoen N., Jiang X., Lindblad L., Stewart P., LePendu J., Baric R. Human susceptibility and resistance to Norwalk virus infection. Nat. Med. 2003, 9:548-553.
99. Manzara S., Muscillo M., La Rosa G., Marianelli C., Cattani P., Fadda G. Molecular identification and typing of enteroviruses isolated from clinical specimens. J. Clin. Microbiol. 2002, 40:4554-4560.
100. Markwell D.D., Shortridge K.F. Possible waterborne transmission and maintenance of influenza viruses in domestic ducks. Appl. Environ. Microbiol. 1982, 43:110-115.
101. Mattison K., Bidawid S. Analytical methods for food and environmental viruses. Food Environ. Virol. 2009, 1:107-122.
102. Maunula L., Kalso S., Von Bonsdorff C.H., Ponka A. Wading pool water contaminated with both noroviruses and astroviruses as the source of a gastroenteritis outbreak. Epidemiol. Infect. 2004, 132:737-743.
103. Maunula L., Klemola P., Kauppinen A., Soderberg K., Nguyen T., Pitkanen T., Kaijalainen S., Simonen M.L., Miettinen I.T., Lappalainen M., Laine J., Vuento R., Kuusi M., Roivainen M. Enteric viruses in a large waterborne outbreak of acute gastroenteritis in Finland. Food Environ. Virol. 2009, 1:31-36.
104. Mirzaei H., Regnier F. Affinity chromatographic selection of carbonylated proteins followed by identification of oxidation sites using tandem mass spectrometry. Anal. Chem. 2005, 77:2386-2392.
105. Monceyron C., Grinde B. Detection of hepatitis-a virus in clinical and environmental-samples by immunomagnetic separation and PCR. J. Virol. Methods 1994, 46:157-166.
106. Morris R. Detection of enteroviruses: an assessment of ten cell lines. Water Sci. Technol. 1985, 17:81-88.
107. Murrin K., Slade J. Rapid detection of viable enteroviruses in water by tissue culture and semi-nested polymerase chain reaction. Water Sci. Technol. 1997, 35:429-432.
108. Myrmel M., Rimstad E., Wasteson Y. Immunomagnetic separation of a Norwalk-like virus (genogroup I) in artificially contaminated environmental water samples. Int. J. Food Microbiol. 2000, 62:17-26.
109. Nocker A., Cheung C.Y., Camper A.K. Comparison of propidium monoazide with ethidium monoazide for differentiation of live vs dead bacteria by selective removal of DNA from dead cells. J. Microbiol. Methods 2006, 67:310-320.
110. Nocker A., Richter-Heitmann T., Montijn R., Schuren F., Kort R. Discrimination between live and dead cells in bacterial communities from environmental water samples analyzed by 454 pyrosequencing. Int. Microbiol. 2010, 13:59-65.
111. Nocker A., Sossa K.E., Camper A.K. Molecular monitoring of disinfection efficacy using propidium monoazide in combination with quantitative PCR. J. Microbiol. Methods 2007, 70:252-260.
112. Nogva H.K., Dromtorp S.M., Nissen H., Rudi K. Ethidium monoazide for DNA-based differentiation of viable and dead bacteria by 5'-nuclease PCR. Biotechniques 2003, 34:804.
113. Nuanualsuwan S., Cliver D.O. Pretreatment to avoid positive RT-PCR results with inactivated viruses. J. Virol. Methods 2002, 104:217-225.
114. Nuanualsuwan S., Cliver D.O. Capsid functions of inactivated human picornaviruses and feline calicivirus. Appl. Environ. Microbiol. 2003, 69:350-357.
115. Okamoto H., Akahane Y., Ukita M., Fukuda M., Tsuda F., Miyakawa Y., Mayumi M. Fecal excretion of a nonenveloped DNA virus (TTV) associated with posttransfusion non-A-G hepatitis. J. Med. Virol. 1998, 56:128-132.
116. Pan Y., Breidt F. Enumeration of viable Listeria monocytogenes cells by real-time PCR with propidium monoazide and ethidium monoazide in the presence of dead cells. Appl. Environ. Microbiol. 2007, 73:8028-8031.
117. Parshionikar S., Laseke I., Fout G.S. Use of propidium monoazide in reverse transcriptase PCR to distinguish between infectious and noninfectious enteric viruses in water samples. Appl. Environ. Microbiol. 2010, 76:4318-4326.
118. Pina S., Puig M., Lucena F., Jofre J., Girones R. Viral pollution in the environment and in shellfish: human adenovirus detection by PCR as an index of human viruses. Appl. Environ. Microbiol. 1998, 64:3376-3382.
119. Pinto R.M., Diez J.M., Bosch A. Use of the colonic-carcinoma cell-line caco-2 for in-vivo amplification and detection of enteric viruses. J. Med. Virol. 1994, 44:310-315.
120. Pintó R.M., Saiz J.-C. Chapter 3. Enteric hepatitis viruses. Perspectives in Medical Virology 2007, 39-67. Elsevier. B. Albert (Ed.).
121. Podewils L.J., Blevins L.Z., Hagenbuch M., Itani D., Burns A., Otto C., Blanton L., Adams S., Monroe S.S., Beach M.J., Widdowson M. Outbreak of norovirus illness associated with a swimming pool. Epidemiol. Infect. 2007, 135:827-833.
122. Prinja S., Kumar S., Reddy G.M., Ratho R.K., Kumar R. Investigation of viral hepatitis E outbreak in a town in Haryana. J. Commun. Dis. 2008, 40:249-254.
123. Rasanen S., Lappalainen S., Kaikkonen S., Hamalainen M., Salminen M., Vesikari T. Mixed viral infections causing acute gastroenteritis in children in a waterborne outbreak. Epidemiol. Infect. 2010, 1-8.
124. Reed L.J., Muench H. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 1938, 27:493-495.
125. Reynolds K.A. Integrated cell culture/PCR for detection of enteric viruses in environmental samples. Methods Mol. Biol. 2004, 268:69-78.
126. Reynolds K.A., Gerba C.P., Pepper I.L. Detection of infectious enteroviruses by an integrated cell culture-PCR procedure. Appl. Environ. Microbiol. 1996, 62:1424-1427.
127. Ridinger D.N., Spendlove R.S., Barnett B.B., George D.B., Roth J.C. Evaluation of cell-lines and immunofluorescence and plaque-assay procedures for quantifying reoviruses in sewage. Appl. Environ. Microbiol. 1982, 43:740-746.
128. Riera-Montes M., Brus Sjolander K., Allestam G., Hallin E., Hedlund K.O., Lofdahl M. Waterborne norovirus outbreak in a municipal drinking-water supply in Sweden. Epidemiol. Infect. 2011, 1-8.
129. Rigonan A.S., Mann L., Chonmaitree T. Use of monoclonal antibodies to identify serotypes of enterovirus isolates. J. Clin. Microbiol. 1998, 36:1877-1881.
130. Rigotto C., Victoria M., Moresco V., Kolesnikovas C.K., Correa A.A., Souza D.S., Miagostovich M.P., Simoes C.M., Barardi C.R. Assessment of adenovirus, hepatitis A virus and rotavirus presence in environmental samples in Florianopolis, South Brazil. J. Appl. Microbiol. 2010, 109:1979-1987.
131. Rodriguez R.A., Gundy P.M., Gerba C.P. Comparison of BGM and PLC/PRC/5 cell lines for total culturable viral assay of treated sewage. Appl. Environ. Microbiol. 2008, 74:2583-2587.
132. Rudi K., Moen B., Dromtorp S.M., Holck A.L. Use of ethidium monoazide and PCR in combination for quantification of viable and dead cells in complex samples. Appl. Environ. Microbiol. 2005, 71:1018-1024.
133. Rule Wigginton K., Menin L., Montoya J.P., Kohn T. Oxidation of virus proteins during UV(254) and singlet oxygen mediated inactivation. Environ. Sci. Technol. 2010, 44:5437-5443.
134. Sano D., Pinto R.M., Omura T., Bosch A. Detection of oxidative damages on viral capsid protein for evaluating structural integrity and infectivity of human norovirus. Environ. Sci. Technol. 2010, 44:808-812.
135. Sarguna P., Rao A., Sudha Ramana K.N. Outbreak of acute viral hepatitis due to hepatitis E virus in Hyderabad. Indian J. Med. Microbiol. 2007, 25:378-382.
136. Sartorius B., Andersson Y., Velicko I., De Jong B., Lofdahl M., Hedlund K.O., Allestam G., Wangsell C., Bergstedt O., Horal P., Ulleryd P., Soderstrom A. Outbreak of norovirus in Vastra Gotaland associated with recreational activities at two lakes during August 2004. Scand. J. Infect. Dis. 2007, 39:323-331.
137. Sauch J.F., Flanigan D., Galvin M.L., Berman D., Jakubowski W. Propidium iodide as an indicator of giardia cyst viability. Appl. Environ. Microbiol. 1991, 57:3243-3247.
138. Scarcella C., Carasi S., Cadoria F., Macchi L., Pavan A., Salamana M., Alborali G.L., Losio M.M., Boni P., Lavazza A., Seyler T. An outbreak of viral gastroenteritis linked to municipal water supply, Lombardy, Italy, June 2009. Euro Surveill. 2009, 1:4.
139. Schriewer A., Wehlmann A., Wuertz S. Improving qPCR efficiency in environmental samples by selective removal of humic acids with DAX-8. J. Microbiol. Methods 2011, 85:16-21.
140. Schwab K. Chapter 2. Waterborne gastroenteritis viruses. Perspectives in Medical Virology 2007, 27-38. Elsevier. B. Albert (Ed.).
141. Sedmak G., Bina D., Macdonald J., Couillard L. Nine-year study of the occurrence of culturable viruses in source water for two drinking water treatment plants and the influent and effluent of a Wastewater Treatment Plant in Milwaukee, Wisconsin (August 1994 through July 2003). Appl. Environ. Microbiol. 2005, 71:1042-1050.
142. Shieh Y.C., Wong C.I., Krantz J.A., Hsu F.C. Detection of naturally occurring enteroviruses in waters using direct RT-PCR and integrated cell culture-RT-PCR. J. Virol. Methods 2008, 149:184-189.
143. Simonet J., Gantzer C. Degradation of the poliovirus 1 genome by chlorine dioxide. J. Appl. Microbiol. 2006, 100:862-870.
144. Simonet J., Gantzer C. Inactivation of poliovirus 1 and F-specific RNA phages and degradation of their genomes by UV irradiation at 254 nanometers. Appl. Environ. Microbiol. 2006, 72:7671-7677.
145. Sinclair R.G., Jones E.L., Gerba C.P. Viruses in recreational water-borne disease outbreaks: a review. J. Appl. Microbiol. 2009, 107:1769-1780.
146. Singh G., Vajpayee P., Khatoon I., Jyoti A., Dhawan A., Gupta K.C., Shanker R. Chromium oxide nano-particles induce stress in bacteria: probing cell viability. J. Biomed. Nanotechnol. 2011, 7:166-167.
147. Siqueira A.A., Santelli A., Alencar L.R., Dantas M.P., Dimech C.P.N., Carmo G.M.I., Santos D.A., Alves R.M.S., Lucena M.B.F., Morais M., Assis R.M.S., Fialho A., Mascarenhas J.D.P., Costa M., Linhares A.C., Leite J.P.G., Araujo W.N., Hatch D.L. Outbreak of acute gastroenteritis in young children with death due to rotavirus genotype G9 in Rio Branco, Brazilian Amazon region, 2005. Int. J. Infect. Dis. 2010, 14:E898-E903.
148. Smith E.M., Gerba C.P. Development of a method for detection of human rotavirus in water and sewage. Appl. Environ. Microbiol. 1982, 43:1440-1450.
149. Spinner M.L., Di Giovanni G.D. Detection and identification of mammalian reoviruses in surface water by combined cell culture and reverse transcription-PCR. Appl. Environ. Microbiol. 2001, 67:3016-3020.
150. Straub T.M., Honer zu Bentrup K., Orosz-Coghlan P., Dohnalkova A., Mayer B.K., Bartholomew R.A., Valdez C.O., Bruckner-Lea C.J., Gerba C.P., Abbaszadegan M., Nickerson C.A. In vitro cell culture infectivity assay for human noroviruses. Emerg. Infect. Dis. 2007, 13:396-403.
151. Tallon L.A., Love D.C., Moore Z.S., Sobsey M.D. Recovery and sequence analysis of hepatitis a virus from springwater implicated in an outbreak of acute viral hepatitis. Appl. Environ. Microbiol. 2008, 74:6158-6160.
152. Tani N., Dohi Y., Kurumatani N., Yonemasu K. Seasonal distribution of adenoviruses, enteroviruses and reoviruses in urban river water. Microbiol. Immunol. 1995, 39:577-580.
153. ter Waarbeek H.L., Dukers-Muijrers N.H., Vennema H., Hoebe C.J. Waterborne gastroenteritis outbreak at a scouting camp caused by two norovirus genogroups: GI and GII. J. Clin. Virol. 2010, 47:268-272.
154. Terletskaia-Ladwig E., Meier S., Hahn R., Leinmuller M., Schneider F., Enders M. A convenient rapid culture assay for the detection of enteroviruses in clinical samples: comparison with conventional cell culture and RT-PCR. J. Med. Microbiol. 2008, 57:1000-1006.
155. Teunis P.F.M., Lodder W.J., Heisterkamp S.H., de Roda Husman A.M. Mixed plaques: Statistical evidence how plaque assays may underestimate virus concentrations. Water Res. 2005, 39:4240-4250.
156. Vesper S., McKinstry C., Hartmann C., Neace M., Yoder S., Vesper A. Quantifying fungal viability in air and water samples using quantitative PCR after treatment with propidium monoazide (PMA). J. Microbiol. Methods 2008, 72:180-184.
157. Villena C., Gabrieli R., Pinto R.M., Guix S., Donia D., Buonomo E., Palombi L., Cenko F., Bino S., Bosch A., Divizia M. A large infantile gastroenteritis outbreak in Albania caused by multiple emerging rotavirus genotypes. Epidemiol. Infect. 2003, 131:1105-1110.
158. Wang L., Li Y., Mustapha A. Detection of viable Escherichia coli O157:H7 by ethidium monoazide real-time PCR. J. Appl. Microbiol. 2009, 107:1719-1728.
159. Wei Z.P., Feng J.H., Lin H.Y., Mullapudi S., Bishop E., Tous G.I., Casas-Finet J., Hakki F., Strouse R., Schenerman M.A. Identification of a single tryptophan residue as critical for binding activity in a humanized monoclonal antibody against respiratory syncytial virus. Anal. Chem. 2007, 79:2797-2805.
160. Werber D., Lausevic D., Mugosa B., Vratnica Z., Ivanovic-Nikolic L., Zizic L., Alexandre-Bird A., Fiore L., Ruggeri F.M., Di Bartolo I., Battistone A., Gassilloud B., Perelle S., Nitzan Kaluski D., Kivi M., Andraghetti R., Pollock K.G. Massive outbreak of viral gastroenteritis associated with consumption of municipal drinking water in a European capital city. Epidemiol. Infect. 2009, 137:1713-1720.
161. WHO Guidelines for Drinking-Water Quality. Recommendations 2008, vol. 1. 3rd ed.
162. Wolf S., Rivera-Aban M., Greening G.E. Long-range reverse transcription as a useful tool to assess the genomic integrity of norovirus. Food Environ. Virol. 2009, 1:129-136.
163. Wyn-Jones A.P., Sellwood J. Enteric viruses in the aquatic environment. J. Appl. Microbiol. 2001, 91:945-962.
164. Yang W., Gu A.Z., Zeng S.Y., Li D., He M., Shi H.C. Development of a combined immunomagnetic separation and quantitative reverse transcription-PCR assay for sensitive detection of infectious rotavirus in water samples. J. Microbiol. Methods 2011, 84:447-453.
165. Yeats J., Smuts H., Serfontein C.J., Kannemeyer J. Investigation into a school enterovirus outbreak using PCR detection and serotype identification based on the 5'non-coding region. Epidemiol. Infect. 2005, 133:1123-1130.
166. Yeh H.-Y., Hwang Y.-C., Yates M.V., Mulchandani A., Chen W. Detection of hepatitis A virus by using a combined cell culture-molecular beacon assay. Appl. Environ. Microbiol. 2008, 74:2239-2243.
167. Yeh H.Y., Yates M.V., Mulchandani A., Chen W. Visualizing the dynamics of viral replication in living cells via Tat peptide delivery of nuclease-resistant molecular beacons. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:17522-17525.
168. Yoder J.S., Blackburn B.G., Craun G.F., Hill V., Levy D.A., Chen N., Lee S.H., Calderon R.L., Beach M.J. Surveillance for waterborne-disease outbreaks associated with recreational water-United States, 2001-2002. MMWR Surveill. Summ. 2004, 53:1-22.
169. Yoder J.S., Hlavsa M.C., Craun G.F., Hill V.R., Yu P.A., Hicks L.A., Alexander N.T., Calderon R.L., Roy S.L., Beach M.J. Surveillance for waterborne disease and outbreaks associated with recreational water use and other aquatic facility-associated health events-United States, 2005-2006. MMWR Surveill. Summ. 2008, 57:1-29.