Evaluation of human adenovirus and human polyomavirus as indicators of human sewage contamination in the aquatic environment

Water Research

Volumn 47, Issue 17, 2013, Pages 6750-6761

  Hewitt, Joanne ^a,c   Greening, Gail E ^a   Leonard, Margaret ^b   Lewis, Gillian D ^c  

^a INSTITUTE OF ENVIRONMENTAL SCIENCE AND RESEARCH   (New Zealand)

^b ESR Christchurch Science Centre   (New Zealand)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Environmental waters; Faecal pollution; Human adenovirus; Human polyomavirus; Indicators; Norovirus; Wastewater

Indexed keywords

CONTAMINATION; HEALTH HAZARDS; HEALTH RISKS; INDICATORS (INSTRUMENTS); POLYMERASE CHAIN REACTION; POTABLE WATER; RISK ASSESSMENT; RIVER POLLUTION; SEWAGE; SURFACE WATERS; VIRUSES; WASTEWATER; WASTEWATER TREATMENT; WATER QUALITY;

ENVIRONMENTAL WATER; FAECAL POLLUTIONS; HUMAN ADENOVIRUS; NOROVIRUS; POLYOMAVIRUS;

EFFLUENTS;

RIVER WATER;

ANTHROPOGENIC SOURCE; BIOINDICATOR; DISCHARGE; ESTUARINE CHEMISTRY; FECES; HEALTH RISK; PATHOGEN; POLLUTION MONITORING; POLYMERASE CHAIN REACTION; RISK ASSESSMENT; SURVIVAL; VIRUS; WASTEWATER; WATER QUALITY;

AQUATIC ENVIRONMENT; ARTICLE; HEALTH HAZARD; HUMAN; HUMAN ADENOVIRUS; JC VIRUS; NOROVIRUS; POLLUTION; POLYMERASE CHAIN REACTION; POLYOMA VIRUS; PRIORITY JOURNAL; RISK ASSESSMENT; SEWAGE; WASTE WATER; WATER QUALITY;

HUMAN ADENOVIRUS; NOROVIRUS; POLYOMAVIRUS;

ENVIRONMENTAL WATERS; FAECAL POLLUTION; HUMAN ADENOVIRUS; HUMAN POLYOMAVIRUS; INDICATORS; NOROVIRUS; WASTEWATER;

ADENOVIRUSES, HUMAN; ESTUARIES; HUMANS; POLYOMAVIRUS; RIVERS; SEWAGE; STATISTICS, NONPARAMETRIC; WASTE WATER; WATER MICROBIOLOGY; WATER POLLUTION; WATER PURIFICATION;

EID: 84886091395     PISSN: 00431354     EISSN: 18792448     Source Type: Journal    
DOI: 10.1016/j.watres.2013.09.001     Document Type: Article

References (49)

1. Ahmed W., Wan C., Goonetilleke A., Gardner T. Evaluating sewage-associated JCV and BKV polyomaviruses for sourcing human fecal pollution in a coastal river in Southeast Queensland, Australia. J. Environ. Qual. 2010, 39(5):1743-1750.
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. Environ. Sci. Technol. 2006, 40(23):7416-7422.
3. Albinana-Gimenez N., Miagostovich M.P., Calgua B., Huguet J.M., Matia L., Girones R. Analysis of adenoviruses and polyomaviruses quantified by qPCR as indicators of water quality in source and drinking-water treatment plants. Water Res. 2009, 43(7):2011-2019.
4. Bofill-Mas S., Pina S., Girones R. Documenting the epidemiologic patterns of polyomaviruses in human populations by studying their presence in urban sewage. Appl. Environ. Microbiol. 2000, 66(1):238-245.
5. Bofill-Mas S., Formiga-Cruz M., Clemente-Casares P., Calafell F., Girones R. Potential transmission of human polyomaviruses through the gastrointestinal tract after exposure to virions or viral DNA. J. Virol. 2001, 75(21):10290-10299.
6. 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(12):7894-7896.
7. 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.
8. Boothpur R., Brennan D.C. Human polyoma viruses and disease with emphasis on clinical BK and JC. J. Clin. Virol. 2010, 47(4):306-312.
9. Calgua B., Barardi C.R., 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):1-7.
10. 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.
11. Dalianis T., Hirsch H.H. Human polyomaviruses in disease and cancer. Virology 2013, 437(2):63-72.
12. de Abreu Corrêa A., Carratala A., Barardi C.R., Calvo M., Girones R., Bofill-Mas S. Comparative inactivation of murine norovirus, human adenovirus, and human JC polyomavirus by chlorine in seawater. Appl. Environ. Microbiol. 2012, 78(18):6450-6457.
13. Gerba C.P., Gramos D.M., Nwachuku N. Comparative inactivation of enteroviruses and adenovirus 2 by UV Light. Appl. Environ. Microbiol. 2002, 68(10):5167-5169.
14. Grabow W.O.K. Overview of health-related water virology. Human Viruses in Water 2007, 1-25. Elsevier, Amsterdam, The Netherlands. A. Bosch (Ed.).
15. Greening G.E., Hewitt J., Rivera-Aban M., Croucher D. Molecular epidemiology of norovirus gastroenteritis outbreaks in New Zealand from 2002-2009. J. Med. Virol. 2012, 84(9):1449-1458.
16. Haramoto E., Katayama H., Oguma K., Ohgaki S. Application of cation-coated filter method to detection of noroviruses, enteroviruses, adenoviruses, and torque teno viruses in the Tamagawa River in Japan. Appl. Environ. Microbiol. 2005, 71(5):2403-2411.
17. Haramoto E., Katayama H., Oguma K., Ohgaki S. Quantitative analysis of human enteric adenoviruses in aquatic environments. J. Appl. Microbiol. 2007, 103(6):2153-2159.
18. 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(6):1747-1752.
19. Harrach B., Benkö M., Both G.W., Brown M., Davison A.J., Echavarría M., Hess M., Jones M.S., Kajon A., Lehmkuhl H.D., Mautner V., Mittal S.K., Wadell G. Virus taxonomy: classification and nomenclature of viruses. Ninth Report of the International Committee on Taxonomy of Viruses 2011, 125-141. Elsevier, San Diego, USA. A.M.Q. King, M.J. Adams, E.B. Carstens, E.J. Lefkowitz (Eds.).
20. Harwood V.J., Brownell M., Wang S., Lepo J., Ellender R.D., Ajidahun A., Hellein K.N., Kennedy E., Ye X., Flood C. Validation and field testing of library-independent microbial source tracking methods in the Gulf of Mexico. Water Res. 2009, 43(19):4812-4819.
21. Heim A., Ebnet C., Harste G., Pring-Akerblom P. Rapid and quantitative detection of human adenovirus DNA by real-time PCR. J. Med. Virol. 2003, 70(2):228-239.
22. 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. Appl. Environ. Microbiol. 2002, 68(9):4523-4533.
23. 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(24):7853-7857.
24. Hewitt J., Leonard M., Greening G.E., Lewis G.D. Influence of wastewater treatment process and the population size on human virus profiles in wastewater. Water Res. 2011, 45(18):6267-6276.
25. Hundesa A., Maluquer de Motes C., Bofill-Mas S., Albinana-Gimenez N., Girones R. Identification of human and animal adenoviruses and polyomaviruses for determination of sources of fecal contamination in the environment. Appl. Environ. Microbiol. 2006, 72(12):7886-7893.
26. Imperiale M.J., Major E.O. Polyomaviruses. Fields Virology 2007, 2263-2298. Lippincott, Williams and Wilkins, Philadelphia, PA. D.M. Knipe, P.M. Howley (Eds.).
27. Kageyama T., Kojima S., Shinohara M., Uchida K., Fukushi S., Hoshino F.B., Takeda N., Katayama K. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J. Clin. Microbiol. 2003, 41(4):1548-1557.
28. Kirs M., Harwood V.J., Fidler A.E., Gillespie P.A., Fyfe W.R., Blackwood A.D., Cornelisen C.D. Source tracking faecal contamination in an urbanised and a rural waterway in the Nelson-Tasman region, New Zealand. N.Z. J. Mar. Freshwater Res. 2011, 45(1):43-58.
29. La Rosa G., Fratini M., Della Libera S., Iaconelli M., Muscillo M. Emerging and potentially emerging viruses in water environments. Ann. Dell'Istituto Super. Sanita 2012, 48(4):397-406.
30. Le Guyader F.S., Atmar R.L. Viruses in shellfish. Human Viruses in Water. Perspectives in Medical Virology 2007, 205-226. Elsevier, Amsterdam, The Netherlands. A. Bosch (Ed.).
31. Lee C., Kim S.J. Molecular detection of human enteric viruses in urban rivers in Korea. J. Microbiol. Biotechnol. 2008, 18(6):1156-1163.
32. Lopman B., Gastanaduy P., Park G.W., Hall A.J., Parashar U.D., Vinje J. Environmental transmission of norovirus gastroenteritis. Curr. Opin. Virol. 2012, 2(1):96-102.
33. McQuaig S.M., Scott T.M., Harwood V.J., Farrah S.R., Lukasik J.O. Detection of human-derived fecal pollution in environmental waters by use of a PCR-based human polyomavirus assay. Appl. Environ. Microbiol. 2006, 72(12):7567-7574.
34. 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. Appl. Environ. Microbiol. 2009, 75(11):3379-3388.
35. McQuaig S., Griffith J., Harwood V.J. The association of fecal indicator bacteria with human viruses and microbial source tracking markers at coastal beaches impacted by nonpoint source pollution. Appl. Environ. Microbiol. 2012, 78(18):6423-6432.
36. Miagostovich M.P., Ferreira F.F., Guimaraes 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. Appl. Environ. Microbiol. 2008, 74(2):375-382.
37. Nwachuku N., Gerba C.P., Oswald A., Mashadi F.D. Comparative inactivation of adenovirus serotypes by UV light disinfection. Appl. Environ. Microbiol. 2005, 71(9):5633-5636.
38. Payment P., Locas A. Pathogens in water: value and limits of correlation with microbial indicators. Ground Water 2011, 49(1):4-11.
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. Appl. Environ. Microbiol. 1998, 64(9):3376-3382.
40. R Development Core Team. R: a Language and Environment for Statistical Computing 2011, R Foundation for Statistical Computing, Vienna, Austria, URL:. http://www.R-project.org/.
41. Savichtcheva O., Okabe S. Alternative indicators of fecal pollution: relations with pathogens and conventional indicators, current methodologies for direct pathogen monitoring and future application perspectives. Water Res. 2006, 40(13):2463-2476.
42. Sidhu J.P., Toze S.G. Human pathogens and their indicators in biosolids: a literature review. Environ. Int. 2009, 35(1):187-201.
43. Teunis P.F., Moe C.L., Liu P., S E.M., Lindesmith L., Baric R.S., Le Pendu J., Calderon R.L. Norwalk virus: how infectious is it?. J. Med. Virol. 2008, 80(8):1468-1476.
44. Till D., McBride G., Ball A., Taylor K., Pyle E. Large-scale freshwater microbiological study: rationale, results and risks. J. Water Health 2008, 6(4):443-460.
45. Williamson W.M., Ball A., Wolf S., Hewitt J., Lin S., Scholes P., Ambrose V., Robson B., Greening G.E. Enteric viruses in New Zealand drinking-water sources. Water Sci. Technol. 2011, 63(8):1744-1751.
46. Wold W.S.M., Horwitz M.S. Adenoviruses. Fields Virology 2007, 2395-2436. Lippincott Williams & Wilkins, Philadephia, PA, USA. D.M. Knipe, P.M. Howley (Eds.).
47. Wolf S., Hewitt J., Greening G.E. Viral multiplex quantitative PCR assays for tracking sources of fecal contamination. Appl. Environ. Microbiol. 2010, 76(5):1388-1394.
48. Wyn-Jones A.P., Carducci A., Cook N., D'Agostino M., Divizia M., Fleischer J., Gantzer C., Gawler A., Girones R., Holler C., Husman A.M., Kay D., Kozyra I., Lopez-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 Res. 2011, 45(3):1025-1038.
49. Xagoraraki I., Kuo D.H., Wong K., Wong M., Rose J.B. Occurrence of human adenoviruses at two recreational beaches of the great lakes. Appl. Environ. Microbiol. 2007, 73(24):7874-7881.