Detection and quantification of classic and emerging viruses by skimmed-milk flocculation and PCR in river water from two geographical areas

Water Research

Volumn 47, Issue 8, 2013, Pages 2797-2810

  Calgua, Byron ^a   Fumian, Tulio ^b   Rusiñol, Marta ^a   Rodriguez Manzano, Jesus ^a   Mbayed, Viviana A ^c   Bofill Mas, Silvia ^a   Miagostovich, Marize ^b   Girones, Rosina ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

^c UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Adenovirus; Asfarvirus like virus; Concentration method; Emerging virus; Klassevirus; Merkel cell polyomavirus; Norovirus; Polyomavirus; River water; Rotavirus; Viral indicator

Indexed keywords

CELLS; FLOCCULATION; POLYMERASE CHAIN REACTION; RIVERS; SEWAGE; WATER POLLUTION;

ADENOVIRUS; ASFARVIRUS-LIKE VIRUS; CONCENTRATION METHOD; EMERGING VIRUS; KLASSEVIRUS; MERKEL CELL POLYOMAVIRUS; NOROVIRUSES; POLYOMAVIRUS; RIVER WATER; ROTAVIRUSES; VIRAL INDICATOR;

VIRUSES;

FRESH WATER; RIVER WATER;

BIOINDICATOR; COST-BENEFIT ANALYSIS; DETECTION METHOD; FLOCCULATION; FRESHWATER; GEOGRAPHICAL DISTRIBUTION; MILK; PATHOGEN; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; RIVER WATER; URBAN AREA; VIRUS; WATER QUALITY;

AFRICAN SWINE FEVER VIRUS; ARTICLE; ASFARVIRUS LIKE VIRUS; FLOCCULATION; GEOGRAPHIC DISTRIBUTION; HUMAN ADENOVIRUS; JC VIRUS; KLASSEVIRUS; MERKEL CELL POLYOMAVIRUS; MILK; NOROVIRUS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PICORNAVIRUS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; ROTAVIRUS; UNINDEXED SEQUENCE; URBAN AREA; VIRUS CONCENTRATION; VIRUS DETECTION; WATER SAMPLING;

BARCELONA [CATALONIA]; BRAZIL; CATALONIA; RIO DE JANEIRO [BRAZIL]; SPAIN;

ADENOVIRIDAE; ANIMALIA; HUMAN ADENOVIRUS; NOROVIRUS; POLYOMAVIRUS; ROTAVIRUS;

EID: 84876140181     PISSN: 00431354     EISSN: 18792448     Source Type: Journal    
DOI: 10.1016/j.watres.2013.02.043     Document Type: Article

References (88)

1. Albinana-Gimenez N., Clemente-Casares P., Calgua B., Huguet J.M., Courtois S., Girones R. Comparison of methods for concentrating human adenoviruses, polyomavirus JC and noroviruses in source waters and drinking water using quantitative PCR. Journal of Virological Methods 2009, 158(1-2):104-109.
2. Albinana-Gimenez N., Clemente-Casares P., Bofill-Mas S., Hundesa A., Ribas F., Girones R. Distribution of human polyomaviruses, adenoviruses, and hepatitis E virus in the environment and in a drinking-water treatment plant. Environmental Science & Technology 2006, 40(23):7416-7422.
3. Allander T., Andreasson K., Gupta S., Bjerkner A., Bogdanovic G., Persson M.A.A., Dalianis T., Ramqvist T., Andersson B. Identification of a third human polyomavirus. The Journal of Virology 2007, 81:4130-4136.
4. Allard A., Albinsson B., Wadell G. Rapid typing of human adenoviruses by a general PCR combined with restriction endonuclease analysis. Journal of Clinical Microbiology 2001, 39(2):498-505.
5. Babakir-Mina M., Ciccozzi M., Campitelli L., Aquaro S., Lo Coco A., Perno C.F., Ciotti M. Identification of the novel KI Polyomavirus in paranasal and lung tissues. Journal of Medical Virology 2009, 81:558-561.
6. Barreira D.M., Ferreira M.S., Fumian T.M., Checon R., de Sadovsky A.D., Leite J.P., Miagostovich M.P., Spano L.C. Viral load and genotypes of noroviruses in symptomatic and asymptomatic children in Southeastern Brazil. Journal of Clinical Virology 2010, 47(1):60-64.
7. Berger J.R., Major E.O. Progressive multifocal leukoencephalopathy. Seminars in Neurology 1999, 19(2):l193-1200.
8. Bofill-Mas S., Hundesa A., Calgua B., Rusiñol M., de Motes C.M., Girones R. Cost-effective method for microbial source tracking using specific human and animal viruses. The Journal of Visualized Experiments 2011, 3(58):e2820. 10.3791/2820.
9. Bofill-Mas S., Pilar Clemente-Casares P., Major E.O., Curfman B., Girones R. Analysis of the excreted JC virus strains and their potential oral transmission. Journal of Neurovirology 2003, 9(4):498-507.
10. 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. Applied and Environmental Microbiology 2006, 72(12):7894-7896.
11. Bofill-Mas S., Calgua B., Clemente-Casares P., la Rosa G., Iaconelli M., Muscillo M., Rutjes S., de Roda Husman A.M., Grunert A., Gräber I., Verani M., Carducci A., Calvo M., Wyn-Jones P., Girones R. Quantification of human adenoviruses in European recreational waters. Food and Environmental Virology 2010, 2(2):101-1009.
12. Bofill-Mas S., Formiga-Cruz M., Clemente-Casares P., Calafell F., Girones R. Potential transmisión of human polyomaviruses through the gastrointestinal tract after exposure to virions or viral DNA. Journal of Virology 2001, 75:10290-10299.
13. Bofill-Mas S., Pina S., Girones R. Documenting the epidemiologic patterns of polyomaviruses in human populations by studying their presence in urban sewage. Applied and Environmental Microbiology 2000, 66(1):238-245.
14. 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. Virology Journal 2010, 7(1):141.
15. Brownell M.J., Harwood V.J., Kurz R.C., McQuaig S.M., Lukasik J., Scott T.M. Confirmation of putative stormwater impact on water quality at a Florida beach by microbial source tracking methods and structure of indicator organism populations. Water Research 2007, 41(16):3747-3757.
16. Bull R.A., White P.A. Mechanisms of GII.4 norovirus evolution. Trends in Microbiology 2011, 19(5):233-240.
17. Calgua B., Rodriguez-Manzano J., Hundesa A., Suñen E., Calvo M., Bofill-Mas S., Girones R. New methods for the concentration of viruses from urban sewage using quantitative PCR. Journal of Virological Methods 2013, 187(2):215-221.
18. Calgua B., Mengewein A., Grunert A., Bofill-Mas S., Clemente-Casares P., Hundesa A., Wyn-Jones A.P., López-Pila J.M., Girones R. Development and application of a one-step low cost procedure to concentrate viruses from seawater samples. Journal of Virological Methods 2008, 153(2):79-83.
19. Cantalupo P.G., Calgua B., Zhao G., Hundesa A., Wier A.D., Katz J.P., Grabe M., Hendrix R.W., Girones R., Wang D., Pipas J.M. Raw sewage harbors diverse viral populations. MBio 2011, 2(5):1-11.
20. Colford J.M., Wade T.J., Schiff K.C., Wright C.C., Griffith J.F., Sandhu S.K., Burns S., Sobsey M., Lovelace G., Weisberg S.B. Water quality indicators and the risk of illness at beaches with nonpoint sources of fecal contamination. Epidemiology 2007, 18(1):27-35.
21. de Roda Husman A.M., Lodder W.J., Rutjes S.A., Schijven J.F., Teunis P.F. Long-term inactivation study of three enteroviruses in artificial surface and groundwaters using PCR and cell culture. Applied and Environmental Microbiology 2009, 75(4):1050-1057.
22. Directive 2006/7/EC of the European Parliament and of the Council of 15 February 2006 concerning the management of bathing water quality and repealing Directive 76/160/EEC.
23. Feng H., Shuda M., Chang Y., Moore P.S. Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 2008, 319:1096-1100.
24. Ferreira M.S., Victoria M., Carvalho-Costa F.A., Vieira C.B., Xavier M.P., Fioretti J.M., Andrade J., Volotão E.M., Rocha M., Leite J.P., Miagostovich M.P. Surveillance of norovirus infections in the state of Rio De Janeiro, Brazil 2005-2008. Journal of Medical Virology 2010, 82(8):1442-1448.
25. Finkbeiner S.R., Allred A.F., Tarr P.I., Klein E.J., Kirkwood C.D., Wang D. Metagenomic analysis of human diarrhea: viral detection and discovery. Plos Pathogens 2008, 4(2):e1000011.
26. Fong T.T., Lipp E.K. Enteric viruses of humans and animals in aquatic environments: health risks, detection and potential water quality assessment tools. Microbiology and Molecular Biology Reviews 2005, 69(2):357-371.
27. Foulongne V., Sauvage V., Hebert C., Dereure O., Cheval J., Gouilh M.A., Pariente K., Segondy M., Burguière A., Manuguerra J.C., Caro V., Eloit M. Human skin microbiota: high diversity of DNA viruses identified on the human skin by high throughput sequencing. PLoS One 2012, 7(6):e38499.
28. Foulongne V., Kluger N., Dereure O., Brieu N., Guillot B., Segondy M. Merkel cell polyomavirus and Merkel cell carcinoma, France. Emerging Infectious Diseases 2008, 14(9):1491-1493.
29. Frisque R.J., Bream G.L., Cannella M.T. Human polyomavirus JC virus genome. Journal of Virology 1984, 51(2):458-469.
30. ® vaccine in Rio de Janeiro, Brazil. Water Research 2011, 45:5755-5763.
31. Fumian T.M., Guimarães F.R., Pereira Vaz B.J., da Silva M.T., Muylaert F.F., Bofill-Mas S., Girones R., Leite J.P., Miagostovich M.P. Molecular detection, quantification and characterization of human polyomavirus JC from waste water in Rio De Janeiro, Brazil. Journal of Water and Health 2010, 8(3):438-445.
32. Gallimore C.I., Taylor C., Gennery A.R., Cant A.J., Galloway A., Iturriza-Gomara M., Gray J.J. Environmental monitoring for gastroenteric viruses in a pediatric primary immunodeficiency unit. Journal of Clinical Microbiology 2006, 44(2):395-399.
33. Gantzer C., Maul A., Audic J.M., Schwartzbrod L. Detection of infectious enteroviruses, enterovirus genomes, somatic coliphages and Bacteroides fragilis phages in treated wastewater. Applied and Environmental Microbiology 1998, 64:4307-4312.
34. Gaynor A.M., Nissen M.D., Whiley D.M., Mackay I.M., Lambert S.B., Wu G., Brennan D.C., Storch G.A., Sloots T.P., Wang D. Identification of a novel polyomavirus from patients with acute respiratory tract infections. Plos Pathogens 2007, 3:595-604.
35. Girones R., Ferrús M.A., Alonso J.L., Rodriguez-Manzano J., Calgua B., Corrêa Ade A., Hundesa A., Carratala A., Bofill-Mas S. Molecular detection of pathogens in water-the pros and cons of molecular techniques. Water Research 2010, 44(15):4325-4339.
36. Glass R.I., Parashar U.D., Estes M.K. Norovirus gastroenteritis. The New England Journal of Medicine 2009, 361(18):1776-1785.
37. Greninger A.L., Holtz L., Kang G., Ganem D., Wang D., De Risi J.L. Serological evidence of human klassevirus infection. Clinical and Vaccine Immunology 2010, 17(10):1584-1588.
38. Greninger A.L., Runckel C., Chiu C.Y., Haggerty T., Parsonnet J., Ganem D., De Risi J.L. The complete genome of klassevirus - a novel picornavirus in pediatric stool. Virology Journal 2009, 6:82.
39. Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 2010, 59(3):307-321.
40. Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symposium Series 1999, 41:95-98.
41. Han T.H., Kim C.H., Chung J.Y., Park S.H., Hwang E.S. Klassevirus infection in children, South Korea. Emerging Infectious Diseases 2010, 16(10):1623-1625.
42. Haramoto E., Katayama H., Ohgaki S. Detection of noroviruses in tap water in Japan by means of a new method for concentrating enteric viruses in large volumes of freshwater. Applied and Environmental Microbiology 2004, 70:2154-2160.
43. Hernroth B.E., Conden-Hansson A.C., Rehnstam-Holm A.S., Girones R., Allard A.K. Environmental factors influencing human viral pathogens and their potential indicator organisms in the blue mussel, Mytilus edulis: the first Scandinavian report. Applied and Environmental Microbiology 2002, 68(9):4523-4533.
44. Holtz L.R., Finkbeiner S.R., Zhao G., Kirkwood C.D., Girones R., Pipas J.M., Wang D. Klassevirus 1, a previously undescribed member of the family Picornaviridae, is globally widespread. Virology Journal 2009, 6:86.
45. ISO 19458 Water Quality-Sampling for Microbiological Analysis. Guidance on Planning Water Sampling Regimes, on Sampling Procedures for Microbiological Analysis and on Transport, Handling and Storage of Samples until Analysis Begins 2006.
46. Iturriza Gómara M., Wong C., Blome S., Desselberger U., Gray J. Molecular characterization of VP6 genes of human rotavirus isolates: correlation of genogroups with subgroups and evidence of independent segregation. Journal of Virology 2002, 76(13):6596-6601.
47. Jothikumar N., Lowther J.A., Henshilwood K., Lees D., Hill V.R., Vinjé J. Rapid and sensitive detection of noroviruses by using TaqMan-Based One-Step Reverse Transcription-PCR assays and application to naturally contaminated shellfish samples. Applied and Environmental Microbiology 2006, 71(4):1870-1875.
48. Katayama H., Shimasaki A., Ohgaki S. Development of a virus concentration method and its application to detection of enterovirus and Norwalk virus from coastal seawater. Applied and Environmental Microbiology 2002, 68:1033-1039.
49. Khan M.A., Bass D.M. Viral infections: new and emerging. Current Opinion in Gastroenterology 2010, 26(1):26-30.
50. Kitamura T., Aso Y., Kuniyoshi N., Hara K., Yogo Y. High incidence of urinary JC virus excretion in non-immunosuppressed older patients. Journal of Infectious Diseases 1990, 161:1128-1133.
51. Koo H.L., Ajami N., Atmar R.L., DuPont H.L. Noroviruses: the leading cause of gastroenteritis worldwide. Discovery Medicine 2010, 10(50):61-70.
52. Koralnik I.J., Boden D., Mai V.X., Lord C.I., Letvin N.L. JC virus DNA load in patients with and without progressive multifocal leukoencephalopathy. Neurology 1999, 52:253-260.
53. Lambertini E., Spencer S.K., Bertz P.D., Loge F.J., Kieke B.A., Borchardt M.A. Concentration of enteroviruses, adenoviruses, and noroviruses from drinking water by use of glass wool filters. Applied and Environmental Microbiology 2008, 74(10):2990-2996.
54. Lodder W.J., van den Berg H., Rutjes S.A., de Roda Husman A.M. Presence of enteric viruses in source waters for drinking water production in the Netherlands. Applied and Environmental Microbiology 2010, 76(17):5965-5971.
55. Loh J., Zhao G., Presti R.M., Holtz L.R., Finkbeiner S.R., Droit L., Villasana Z., Todd C., Pipas J.M., Calgua B., Girones R., Wang D., Virgin H.W. Detection of novel sequences related to african Swine Fever virus in human serum and sewage. The Journal of Virology 2009, 83(24):13019-13025.
56. Löytynoja A., Goldman N. An algorithm for progressive multiple alignment of sequences with insertions. Proceedings of the National Academy of Sciences of the United States of America 2005 26, 102(30):10557-10562.
57. McQuaig S.M., Scott T.M., Harwood V.J., Farrah S.R., Lukasik J.O. Detection of human-drived fecal pollution in environmental waters by use of a PCR-based human polyomavirus assay. Applied and Environmental Microbiology 2006, 72(12):7567-7574.
58. McQuaig S.M., Scott T.M., Lukasik J.O., Paul J.H., Harwood V.J. Quantification of human polyomaviruses JC Virus and BK Virus by TaqMan quantitative PCR and comparison to other water quality indicators in water and fecal samples. Applied and Environmental Microbiology 2009, 75(11):3379-3388.
59. Miagostovich M.P., Ferreira F.F., Guimarães F.R., Fumian T.M., Diniz-Mendes L., Luz S.L., Silva L.A., Leite J.P. Molecular detection and characterization of gastroenteritis viruses occurring naturally in the stream waters of Manaus, central Amazonia, Brazil. Applied and Environmental Microbiology 2008, 74(2):375-382.
60. Moens U., Ludvigsen M., Van Ghelue M. Human Polyomaviruses in Skin Diseases 2011, Pathology Research International, 123491.
61. Pal A., Sirota L., Maudru T., Peden K., Lewis A.M. Real-time PCR assays for the detection of virus-specific DNA in simples with mixed populations of polyomaviruses. Journal of Virological Methods 2006, 135(1):32-42.
62. Pallin R., Wyn-Jones A.P., Place B.M., Lightfoot N.F. The detection of enteroviruses in large volume concentrates of recreational waters by the polymerase chain reaction. Journal of Virological Methods 1997, 67:57-67.
63. Parashar U.D., Burton A., Lanata C., Boschi-Pinto C., Shibuya K., Steele D., Birmingham M., Glass R.I. Global mortality associated with rotavirus disease among children in 2004. Journal of Infection Disease 2009, 1:200.
64. Patel M.M., Widdowson M.A., Glass R.I., Akazawa K., Vinjé J., Parashar U.D. Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerging Infectious Diseases 2008, 14(8):1224-1231.
65. Pina S., Puig M., Lucena F., Jofre J., Girones R. Viral pollution in the environment and shellfish: human adenovirus detection by PCR as an index of human viruses. Applied and Environmental. Microbiology 1998, 64:3376-3382.
66. Posada D. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 2008, 25:1253-1256.
67. Prado T., Silva D.M., Guilayn W.C., Rose T.L., Gaspar A.M., Miagostovich M.P. Quantification and molecular characterization of enteric viruses detected in effluents from two hospital wastewater treatment plants. Water Research 2011, 45(3):1287-1297.
68. Puig M., Jofre J., Lucena F., Allard A., Wadell G., Girones R. Detection of adenoviruses and enteroviruses in polluted waters by nested PCR amplification. Applied and Environmental Microbiology 1994, 60:2963-2970.
69. Pusch D., Oh D.Y., Wolf S., Dumke R., Schröter-Bobsin U., Höhne M., Röske I., Schreier E. Detection of enteric viruses and bacterial indicators in German environmental waters. Archives of Virology 2005, 150(5):929-947.
70. R: A Language and Environment for Statistical Computing 2008, R Development Core Team. http://www.R-project.org.
71. Rosario K., Nilsson C., Lim Y.W., Ruan Y., Breitbart M. Metagenomic analysis of viruses in reclaimed water. Environmental. Microbiology 2009, 11:2806-2820.
72. Schael I.P., Gonzalez R., Salinas B. Severity and age of rotavirus diarrhea, but not socioeconomic conditions, are associated with rotavirus seasonality in Venezuela. Journal of Medical Virology 2009, 81:562-567.
73. Schowalter R.M., Pastrana D.V., Pumphrey K.A., Moyer A.L., Buck C.B. Merkel cell polyomavirus and two previously unknown polyomaviruses are chronically shed from human skin. Cell Host & Microbe 2010, 7(6):509-515.
74. Shan T., Wang C., Cui L., Yu Y., Delwart E., Zhao W., Zhu C., Lan D., Dai X., Hua X. Picornavirus salivirus/klassevirus in children with diarrhea, China. Emerging Infectious Diseases 2010, 16(8):1303-1305.
75. Sobsey M.D., Wallis C., Henderson M., Melnick J.L. Concentration of enteroviruses from large volumes of water. Applied Microbiology 1973, 26(4):529-534.
76. USEPA Water Quality Standards for Coastal and Great Lakes Recreation Waters 2004, vol. 69. p. 220.
77. van den Berg H., Lodder W., van der Poel W., Vennema H., de Roda Husman A.M. Genetic diversity of noroviruses in raw and treated sewage water. Research in Microbiology 2005, 156:532-540.
78. Vega E., Vinjé J. Novel GII.12 norovirus strain, United States, 2009-2010. Emerging Infectious Diseases 2011, 17(8):1516-1518.
79. Vennema H., de Bruin E., Koopmans M. Rational optimization of generic primers used for Norwalk-like virus detection by reverse transcriptase polymerase chain reaction. Journal of Clinical Virology 2002, 25(2):233-235.
80. Verzani J. Using R for Introductory Statistics 2004, Chapman & Hall/CRC.
81. Victoria M., Guimarães F.R., Fumian T.M., Ferreira F.F., Vieira C.B., Shubo T., Leite J.P., Miagostovich M.P. One year monitoring of norovirus in a sewage treatment plant in Rio de Janeiro, Brazil. Journal of Water and Health 2010, 8(1):158-1565.
82. Vilaginès P., Sarrette B., Husson G., Vilaginès R. Glass wool for virus concentration at ambient water pH level. Water Science and Technology 1993, 27:299-306.
83. Weber T., Trebst C., Frye S., Cinque P., Vago L., Sindic C.J., Schulz-Schaeffer W.J., Kretzschmar H.A., Enzensberger W., Hunsmann G., Luke W. Analysis of the systemic and intrathecal humoral immune response in progressive multifocal leukoencephalopathy. Journal of Infection Diseases 1997, 176:250-254.
84. WHO Guidelines for Safe Recreational Water Environments. Coastal and Freshwaters 2003, vol. 1. World Health Organisation, Geneva, 219.
85. Wieland U., Mauch C., Kreuter A., Krieg T., Pfister H. Merkel cell polyomavirus DNA in persons without merkel cell carcinoma. Emerging Infectious Diseases 2009, 15(9):1496-1498.
86. Wyn-Jones A.P., Carducci A., Cook N., D'Agostino M., Divizia M., Fleischer J., Gantzer C., Gawler A., Girones R., Höller C., de Roda Husman A.M., Kay D., Kozyra I., López-Pila J., Muscillo M., Nascimento M.S., Papageorgiou G., Rutjes S., Sellwood J., Szewzyk R., Wyer M. Surveillance of adenoviruses and noroviruses in European recreational waters. Water Research 2011, 45(3):1025-1038.
87. Yousry T.A., Major E.O., Ryschkewitsch C., Fahle G., Fischer S., Hou J., Curfman B., Miszkiel K., Mueller-Lenke N., Sanchez E., Barkhof F., Radue E.W., Jager H.R., Clifford D.B. Evaluation of patients treated with natalizumab for progressive multifocal. The New England Journal of Medicine 2006, 354:924-933.
88. Zeng S.Q., Halkosalo A., Salminen M., Szakal E.D., Puustinen L., Vesikari T. One-step quantitative RT-PCR for the detection of rotavirus in acute gastroenteritis. Journal of Virological Methods 2008, 153:238-240.