Relationships between human adenoviruses and faecal indicator organisms in European recreational waters

Water Research

Volumn 46, Issue 13, 2012, Pages 4130-4141

  Wyer, Mark D ^a   Wyn Jones, A Peter ^a   Kay, David ^a   Au Yeung, Ho Kong Christopher ^b   Gironés, Rosina ^c   López Pila, Juan ^d   de Roda Husman, Ana Maria ^e   Rutjes, Saskia ^e   Schneider, Oliver ^f  

^a ABERYSTWYTH UNIVERSITY   (United Kingdom)

^b PUBLIC HEALTH WALES   (United Kingdom)

^c UNIVERSITY OF BARCELONA   (Spain)

^d UMWELTBUNDESAMT   (Germany)

^e NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^f Landesgesundheitsamt   (Germany)

Author keywords

E. coli; Faecal indicator organisms; Human adenovirus; Intestinal enterococci; Logistic regression; Recreational water quality

Indexed keywords

ESCHERICHIA COLI; WATER QUALITY;

E. COLI; FAECAL INDICATOR ORGANISMS; HUMAN ADENOVIRUS; INTESTINAL ENTEROCOCCI; LOGISTIC REGRESSIONS; RECREATIONAL WATER QUALITY;

REGRESSION ANALYSIS;

FRESH WATER; SEA WATER; VIRUS DNA;

BIOINDICATOR; DISEASE INCIDENCE; FECAL COLIFORM; MOLECULAR ANALYSIS; POLLUTION EXPOSURE; POOL; RECREATIONAL ACTIVITY; REGRESSION ANALYSIS; VIRUS; WATER QUALITY;

ARTICLE; BACTERIAL SURVIVAL; CELL COUNT; COLIPHAGE; CONCENTRATION (PARAMETERS); CONTINGENCY TABLE; ENTEROCOCCUS; ESCHERICHIA COLI; EUROPE; FECAL INDICATOR ORGANISM; HUMAN ADENOVIRUS; MICROORGANISM; NONHUMAN; PRIORITY JOURNAL; RECREATIONAL WATER QUALITY; VIRUS DETECTION; WATER QUALITY;

EUROPE;

ESCHERICHIA COLI; HUMAN ADENOVIRUS;

EID: 84862764435     PISSN: 00431354     EISSN: 18792448     Source Type: Journal    
DOI: 10.1016/j.watres.2012.04.008     Document Type: Article

References (54)

1. 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, 39:498-505.
2. Adams M.H. Bacteriophages 1959, Inter-science, New York, p. 592.
3. Aslan A., Xagoraki I., Simmons F.J., Rose J.B., Dorevitch S. Occurrence of adenovirus and other enteric viruses in limited-contact freshwater recreational areas and bathing waters. Journal of Applied Microbiology 2011, 111:1250-2161.
4. Bofill-Mas S., Caluga B., Clemente-Casares P., La Rosa G., Iaconelli M., Muscillo M., de Roda Husman A.M., Grunert A., Gräber I., Verani M., Carducci A., Calvo M., Wyn-Jones A.P., Girones R. Quantification of human adenovirus in European recreational waters. Food and Environmental Virology 2010, 2(2):101-109.
5. Bucardo F., Karlsson B., Nordgren J., Paniagua M., González A., Amador J.J., Espinoza F., Svensson L. Mutated G4P[8] rotavirus associated with a nationwide outbreak of gastroenteritis in Nicaragua in 2005. Journal of Clinical Microbiology 2007, 45(3):990-997.
6. Caluga B., Mengewein A., Grunert A., Bofill-Mas S., Clemente-Casares P., Hundesa A., Wyn-Jones A.P., Lòpez-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, 153:79-83.
7. Council of the European Union (CEU) 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 2006.
8. Contreras-Coll N., Lucena F., Mooijman K., Havelaar A., Pierz V., Boque M., Gawler A., Höller C., Lambiri M., Mirolo G., Moreno B., Niemi M., Sommer R., Valentin B., Wiedenmann A., Young V., Jofre J. Occurrence and levels of indicator bacteriophages in bathing waters throughout Europe. Water Research 2002, 36(20):4963-4974.
9. 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.
10. Enriquez C.E., Hurst C.J., Gerba C.P. Survival of the enteric adenoviruses 40 and 41 in tap, sea and wastewater. Water Research 1995, 29:2548-2553.
11. Fleisher J.M., Kay D., Salmon R.L., Jones F., Wyer M.D., Godfree A.F. Marine waters contaminated with domestic sewage: nonenteric illnesses associated with bather exposure in the United Kingdom. American Journal of Public Health 1996, 86(9):1228-1234.
12. Gerba C.P., Goyal S.M., LaBelle R.L., Cech I., Bodgan G.F. Failure of indicator bacteria to reflect the occurrence of enteroviruses in marine waters. American Journal of Public Health 1979, 69:1116-1119.
13. Gray J.J., Green J., Gallimore C., Lee J.V., Neal K., Brown D.W.G. Mixed genotype SRSV infections among a party of canoeists exposed to contaminated recreational water. Journal of Medical Virology 1997, 52:425-429.
14. Harley D., Harrower B., Lyon M., Dick A. A primary school outbreak of pharyngoconjunctival fever caused by adenovirus type 3. Communicable Diseases Intelligence 2001, 25(1):9-12.
15. 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. Epidemiology and Infection 2005, 133(2):291-298.
16. Havelaar A.H., van Olphen M., Drost Y. F-specific RNA bacteriophage are adequate model organisms for enteric viruses in fresh water. Applied and Environmental Microbiology 1993, 59(9):2956-2962.
17. Hijnen W.A.M., Beerendonk E.F., Medema G.J. Inactivation credit of UV radiation for viruses, bacteria and protozoan (oo)cysts in water: a review. Water Research 2006, 40:3-22.
18. Hoebe C.J.P.A., Vennema H., de Roda Husman A.M., van Duynhoven Y.T.H.P. Norovirus outbreak among primary school children who had played in a recreational water fountain. Journal of Infectious Diseases 2004, 189:699-705.
19. Iijima Y., Tanaka S., Ohishi H. Multiple outbreaks of gastroenteritis due to a single strain of genotype GII/4 norovirus in Kobe, Japan: risk factors for norovirus spread in health care settings. Japanese Journal of Infectious Diseases 2008, 61(5):419-422.
20. Inlow M. Prediction Confidence Intervals after Logistic Regression. StataCorp 1999, http://www.stata.com/support/faqs/stat/prep.html.
21. International Standard, ISO 7899-1 (cor 1: 2000). Water Quality-Detection and Enumeration of Intestinal Enterococci-part 1: Miniaturized Method (Most Probable Number) for Surface and Waste Water 1998, International Organization for Standardization, Geneva, Switzerland, p. 19.
22. International Standard, ISO 9308-3 (cor 1: 2000). Water Quality-detection and Enumeration of Escherichia coli and Coliform Bacteria -Part 3: Miniaturized Method (Most Probable Number) for the Detection and Enumeration of E. coli in Surface and Waste Water 1998, International Organization for Standardization, Geneva, Switzerland, p. 20.
23. International Standard, ISO 7899-2 Water Quality-detection and Enumeration of Intestinal Enterococci-Part 2: Membrane Filtration Method 2000, International Organization for Standardization, Geneva, Switzerland, p. 7.
24. International Standard, ISO 9308-1 (cor 1: 2007). Water Quality-detection and Enumeration of Escherichia coli and Coliform Bacteria in Surface and Waste Water-Part 1: Membrane Filtration Method 2000, International Organization for Standardization, Geneva, Switzerland, p. 10.
25. International Standard, ISO 10705-2 Water Quality-detection and Enumeration of Bacteriophages-Part 2: Enumeration of Somatic Coliphages 2000, International Organization for Standardization, Geneva, Switzerland, p. 16.
26. Joiner B., Cryer J., Ryan B.F. Minitab Handbook 2004, Brooks Cole, p. 505. fifth ed.
27. Joyce E., Rueedi J., Cronin A., Pedley S., Tellam J., Greswell R. Fate and Transport of Phage and Viruses in UK Permotriassic Sandstone Aquifers. Science Report - SC03021/SR 2007, Environment Agency, p. 81.
28. Kay D., Fleisher J.M., Salmon R.L., Jones F., Wyer M.D., Godfree A.F., Zelenauch-Jacquotte Z., Shore R. Predicting the likelihood of gastroenteritis from sea bathing - results from randomized exposure. The Lancet 1994, 344(8927):905-909.
29. Kay D., Bartram J., Prüss A., Ashbolt N., Wyer M.D., Fleisher J.M., Fewtrell L., Rogers A., Rees G. Derivation of numerical values for the World Health Organization guidelines for recreational waters. Water Research 2004, 38(5):1296-1304.
30. Laverick M.A., Wyn-Jones A.P., Carter M.J. Quantitative RT-PCR for the enumeration of noroviruses (Norwalk-like viruses) in water and sewage. Letters in Applied Microbiology 2004, 39:127-136.
31. 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. Applied and Environmental Microbiology 2004, 70:6695-6705.
32. Lipp E.K., Farrah S.A., Rose J.B. Assessment and impact of microbial fecal pollution and human enteric pathogens in a coastal community. Marine Pollution Bulletin 2001, 42:286-329.
33. Maunula L., Kalso S., von Bonsdorff C.-H., Pönkä A. Wading pool water contaminated with both noroviruses and astroviruses as the source of a gastroenteritis outbreak. Epidemiology and Infection 2004, 132(4):737-743.
34. Medema G.J., van Asperen I.A., Kokman-Houweling J.M., Nooitgedagt A., van de Laar M.J.W., Havelaar A.H. The relationship between health effects in triathletes and microbiological quality of freshwater. Water Science and Technology 1995, 31(5-6):19-26.
35. 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.
36. Mitchell G., Namdeo A., Kay D. A new disease-burden method for estimating the impact of outdoor air quality on human health. Science of the Total Environment 2000, 246(2-3):153-163.
37. Nwachuku N., Gerba C.P. Health risks of enteric viral infections in children. Reviews in Environmental Contamination and Toxicology 2006, 186:1-56.
38. Papapetropolou M., Vantarakis A.C. Detection of adenovirus outbreak at a municipal swimming pool by nested PCR amplification. Journal of Infection 1995, 36:101-103.
39. 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. Applied and Environmental Microbiology 1998, 64:3376-3382.
40. Rutjes S.A., Lodder W.J., Lodder-Verschoor F., van den Berg H.H.J.L., Vennema H., Duizer E., Koopsmans M., de Roda Husman A.M. Sources of hepatitis E virus genotype 3 in the Netherlands. Emerging Infectious Diseases 2009, 15(3):381-387.
41. Rzeżutka A., Cook N. Survival of human enteric viruses in the environment and food. FEMS Microbiology Reviews 2004, 28:441-453.
42. Sarguna P., Rao A., Sudha Ramana K.N. Outbreak of acute viral hepatitis due to hepatitis E virus in Hyderabad. Indian Journal of Medical Microbiology 2007, 25(4):378-382.
43. Sinclair R.G., Jones E.L., Gerba C.P. Viruses in recreational water-borne disease outbreaks: a review. Journal of Applied Microbiology 2009, 107(6):1769-1780.
44. Sinton L.W., Hall C.H., Lynch P.A., Davis-Colley R.J. Sunlight inactivation of fecal indicator bacteria and bacteriophages from waste stabilization pond effluent in fresh and saline waters. Applied and Environmental Microbiology 2002, 68(3):1122-1131.
45. SPSS SPSS 16.0 Brief Guide 2007, SPSS Inc., Chicago, p. 217.
46. Thurston-Enriquez J.A., Haas C.N., Jacangelo J., Gerba C.P. Inactivation of feline calicivirus and adenovirus type 40 by UV radiation. Applied and Environmental Microbiology 2003, 69:577-582.
47. Vasl R., Fattal B., Katzenelson E., Shuval H. Survival of enteroviruses and bacterial indicator organisms in the Sea. Viruses and Wastewater Treatment 1981, 113-116. Pergamon Press. M. Goddard, M. Butler (Eds.).
48. Wong M., Kumar Lekha, Jenkins T.M., Xagoraraki I., Phanikumar M.S., Rose J.B. Evaluation of public ealth risks at recreational beaches in Lake Michigan via detection of enteric viruses and a human-specific bacteriological marker. Water Research 2009, 43:1137-1149.
49. World Health Organization (WHO) Guidelines for Safe Recreational Water Environments Volume 1: Coastal and Freshwaters 2003, World Health Organization, Geneva, p. 219.
50. Wyer M.D., Fleisher J.M., Gough J., Kay D., Merrett H. An investigation into parametric relationships between enterovirus and faecal indicator organisms in the coastal waters of England and Wales. Water Research 1995, 29(8):1863-1868.
51. Wyer M.D., Kay D., Fleisher J.M., Salmon R.L., Jones F., Godfree A.F., Jackson G., Rogers R. An experimental health related classification for marine waters. Water Research 1999, 33(3):715-722.
52. 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., Kozyra I., López-Pila J., Muscillo M., São José Nascimento M., Papageorgiou G., Rutjes S., Sellwood J., Szewzyk R., Wyer M.D., Kay D. Surveillance of adenoviruses and noroviruses in European recreational waters. Water Research 2011, 45:1025-1038.
53. Zar J.H. Biostatistical Analysis 1998, Prentice Hall, p. 929. fourth ed.
54. Zhang Y., Tan X.J., Wang H.Y., Yan D.M., Zhu S.L., Wang D.Y., Ji F., Wang X.J., Gao Y.J., Chen L., An H.Q., Li D.X., Wang S.W., Xu A.Q., Wang Z.J., Xu W.B. An outbreak of hand, foot, and mouth disease associated with subgenotype C4 of human enterovirus 71 in Shandong, China. Journal of Clinical Virology 2009, 44(4):262-267.