Analysis of adenoviruses and polyomaviruses quantified by qPCR as indicators of water quality in source and drinking-water treatment plants

Water Research

Volumn 43, Issue 7, 2009, Pages 2011-2019

  Albinana Gimenez, Nestor ^a,c   Miagostovich, Marize P ^b   Calgua, Byron ^a   Huguet, Josep M ^c   Matia, Lleonard ^c   Girones, Rosina ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

^c Aigües de Barcelona   (Spain)

Author keywords

Adenovirus; Drinking water; Polyomavirus; qPCR

Indexed keywords

CELL CULTURE; EFFICIENCY; POLYMERASE CHAIN REACTION; QUALITY CONTROL; REMOVAL; VIRUSES; WATER QUALITY; WATER TREATMENT; WATER TREATMENT PLANTS;

ADENOVIRUS; DRINKING WATER TREATMENT PLANTS; HUMAN ADENOVIRUS; LOW CONCENTRATIONS; POLYOMAVIRUS; QPCR; REMOVAL EFFICIENCIES; RIVER WATER SAMPLES; SOURCE WATERS; VIRUS REMOVAL;

POTABLE WATER;

DRINKING WATER; RIVER WATER;

ADSORPTION; BIOASSAY; BIOINDICATOR; DRINKING WATER; GLASS; INFECTIVITY; PATHOGEN; PERFORMANCE ASSESSMENT; POLLUTANT REMOVAL; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; RIVER WATER; STANDARD (REFERENCE); VIRUS; WATER QUALITY; WATER TREATMENT;

ARTICLE; CELL CULTURE; FILTRATION; GENOME; HAZARD ASSESSMENT; HUMAN; HUMAN ADENOVIRUS; NONHUMAN; POLYMERASE CHAIN REACTION; POLYOMA VIRUS; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; VIRAL CONTAMINATION; VIRUS DETECTION; WATER QUALITY; WATER SAMPLING; WATER TREATMENT;

ADENOVIRIDAE; BACTERIA (MICROORGANISMS); HUMAN ADENOVIRUS; JC POLYOMAVIRUS; POLYOMAVIRUS;

EID: 63449110218     PISSN: 00431354     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.watres.2009.01.025     Document Type: Article

References (47)

1. Abbaszadegan M., Monterio P., Nwachuku N., Alum A., and Ryu H. Removal of adenovirus, calicivirus, and bacteriophages by conventional drinking water treatment. Journal of Environmental Science and Health Part A 43 (2008) 171-177
2. Albinana-Gimenez N., Clemente-Casares P., Bofill-Mas S., Hundesa A., Ribas F., and Girones R. Distribution of human polyomaviruses, adenoviruses and hepatitis E virus in the environment and in a drinking-water treatment plant. Environmental Science and Technology 40 (2006) 7416-7422
3. Albinana-Gimenez, N., Clemente-Casares, P., Calgua, B., Courtois, S., Huguet, J.M., Girones, R. Comparison of methods for the quantification of human adenoviruses, polyomavirus JC and norovirus in source and drinking water. Journal of Virological Methods, in press.
4. Ali M.A., Al-Herrawy A.Z., and El Hawaary S.E. Detection of enteric viruses, Giardia and Cryptosporidium in two different types of drinking water treatment facilities. Water Research 38 (2004) 3931-3939
5. Allard A., Albinsson B., and Wadell G. Rapid typing of human adenoviruses by a general PCR combined with transcription endonuclease analysis. Journal of Clinical Microbiology 39 (2001) 498-505
6. AWWA. Water Treatment: Principles and Practices of Water Supply Operations. second ed. (1995), American Water Works Association, Denver
7. Berger J.R., Kaszovita B., Donovan P.J., and Dickinson G. Progressive multifocal leukoencephalopathy associated with human immunodeficiency virus infection. Annals of Internal Medicine 107 (1987) 78-87
8. Bofill-Mas S., Albinana-Gimenez N., Clemente-Casares P., Hundesa A., Rodiguez-Manzano J., Allard A., Calvo M., and Girones R. Quantification and stability of human adenoviruses and polyomavirus JCPyV in wastewater matrices. Applied and Environmental Microbiology 72 12 (2006) 7894-7896
9. Bofill-Mas S., Formiga-Cruz M., Clemente-Casares P., Calafell F., and Girones R. Potential transmission of human polyomaviruses through the intestinal tract after exposure of virions or viral DNA. Journal of Virology 75 21 (2001) 10290-10299
10. Bofill-Mas S., Pina S., and Girones R. Documenting the epidemiologic patterns of polyomaviruses in human populations studying their presence in urban sewage. Applied and Environmental Microbiology 66 (2000) 238-245
11. Brandt C.D., Kim H.W., Vargosko A.J., Jeffries B.C., Arrobio J.O., Rindge B., Parrott R.H., and Chanock R.M. Infections in 18,000 infants and children in a controlled study of respiratory tract disease. I. Adenovirus pathogenicity in relation to serologic type and illness syndrome. American Journal of Epidemiology 90 6 (1969) 484-500
12. Calgua, B., Mengewein, A., Grünert, A., Bofill-Mas, S., Clemente-Casares, P., Hundesa, A., Wyn-Jones, A.P., López-Pila, J.M., Girones, R, 2008. Development and application of a one-step low cost procedure to concentrate viruses from seawater samples. Journal of Virological Methods, Journal of Virological Methods 153 (2), 79-83.
13. Cho H.B., Lee S.H., Cho J.C., and Kim S.J. Detection of adenoviruses and enteroviruses in tap water and river water by reverse transcription multiplex PCR. Canadian Journal of Microbiology 46 5 (2000) 412-424
14. Choi S., and Jiang S.C. Real-time PCR quantification of human adenoviruses in urban rivers indicates genome prevalence but low infectivity. Applied and Environmental Microbiology 71 11 (2005) 7426-7433
15. Enam S., Del Valle L., Lara C., Gan D.D., Ortiz-Hidalgo C., Palazzo J.P., and Khalili K. Association of human polyomavirus JCV with colon cancer: evidence for interaction of viral T-antigen and beta-catenin. Cancer Research 62 23 (2002) 7093-7101
16. Formiga-Cruz M., Allard A.K., Conden-Hansson A.C., Hensilwood H., Hernroth B.E., Jofre J., Lees D.N., Lucena F., Papapetropoulou R.E., Rangdale A., Tsibouxi A., Vantarakis A., and Girones R. Evaluation of potential indicators of viral contamination in shellfish with applicability to diverse geographical areas. Applied and Environmental Microbiology 69 (2003) 1556-1563
17. Formiga-Cruz M., Tofiño-Quesada G., Bofill-Mas S., Lees D.N., Henshilwood K., Allard A.K., Conden-Hansson A.C., Hernroth B.E., Vantarakis A., Tsibouxi A., Papapetropoulou M., Furones M.D., and Girones R. Distribution of human virus contamination in shellfish from different growing areas in Greece, Spain, Sweden and the United Kingdom. Applied and Environmental Microbiology 68 12 (2002) 5990-5998
18. Gerba C.P., Goyal S.M., LaBelle R.L., Cech I., and Bodgan G.F. Failure of indicator bacteria to reflect the occurrence of enteroviruses in marine waters. American Journal of Public Health 69 11 (1979) 1116-1119
19. Haramoto E., Katayama H., Oguma K., and Ohgaki S. Application of cation-coated filter method to detection of noroviruses, enteroviruses adenoviruses and torque teno viruses in the Tamagawa River in Japan. Applied and Environmental Microbiology 71 5 (2005) 2403-2411
20. Haramoto E., Katayama H., Oguma K., and Ohgaki S. Quantitative analysis of human enteric adenoviruses in aquatic environments. Journal of Applied Microbiology 103 (2007) 2153-2159
21. He J., and Jiang S. Quantification of enterococci and human adenoviruses in environmental samples by real-time PCR. Applied and Environmental Microbiology 71 5 (2005) 2250-2255
22. Herbold K., Flehming B., and Botzenhart K. Comparison of ozone inactivation, in flowing water, of Hepatitis A virus, Poliovirus 1 and indicator organisms. Applied and Environmental Microbiology 55 11 (1989) 2949-2953
23. Hernroth B.E., Conden-Hansson A.C., Rehnstam-Holm A.S., Girones R., and 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 68 9 (2002) 4523-4533
24. Hori R., Murai Y., Tsuneyama K., Abdel-Aziz H.O., Nomoto K., Takahashi H., Cheng C.M., Kuchina T., Harman B.V., and Takano Y. Detection of JC virus DNA sequences in colorectal cancers in Japan. Virchows Archives 447 4 (2005) 723-730
25. IAWPRC study group of water virology. The health significance of viruses in water. Water Research 17 (1983) 121-132
26. Ito K., Inoue S., Hiraku Y., and Kawanishi S. Mechanism of site-specific DNA damage induced by ozone. Mutation Research 585 (2005) 60-70
27. Katayama H., Haramoto E., Oguma K., Yamashita H., Tajima A., Nakajima H., and Ohgaki S. One-year monthly quantitative survey of noroviruses, enteroviruses, and adenoviruses in wastewater collected from six plants in Japan. Water Research 42 (2008) 1441-1448
28. Lambertini E., Spencer S.K., Bertz P.D., Loge F.J., Kieke B.A., and Borchardt M.A. Concentration of enteroviruses, adenoviruses and noroviruses from drinking water with glass wool filters. Applied and Environmental Microbiology 74 10 (2008) 2990-2996
29. LeChevallier M.W., and Au K.-K. Water Treatment and Pathogen Control: Process Efficiency in Achieving Safe Drinking Water (2004), World Health Organization and IWA, Geneva
30. Lee C., Lee S.H., Han E., and 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 70 11 (2004) 6695-6705
31. Lipp E.K., Farrah S.A., and Rose J.B. Assessment of microbiological fecal pollution and human enteric pathogens in a coastal community. Marine Pollution Bulletin 42 4 (2001) 286-293
32. Major E.O., Amemiya K., Tornatore C.S., Houff S.A., and Berger J.R. Pathogenesis and molecular biology of progressive multifocal leukoencephalopathy, the JC virus-induced demyelinating disease of the human brain. Clinical Microbiology Reviews 5 (1992) 49-73
33. Mi B., Eaton C.L., Kim J.H., Colvin C.K., Lozier J.C., and Maiñas B.J. Removal of biological and non-biological viral surrogates by spiral-wound reverse osmosis membrane elements with intact and compromised integrity. Water Research 38 (2004) 3821-3832
34. Pal A., Sirota L., Maudru T., Peden K., and Lewis A.M. Real-time PCR assays for the detection of virus-specific DNA in samples with mixed populations of polyomaviruses. Journal of Virological Methods 135 1 (2006) 32-42
35. Pina S., Puig M., Lucena F., Jofre J., and Girones R. Viral pollution in the environment and shellfish: human adenovirus detection by PCR as an index of human viruses. Applied and Environmental Microbiology 64 (1998) 3376-3382
36. Puig M., Jofre J., Lucena F., Allard A., Wadell G., and Girones R. Detection of adenoviruses and enteroviruses in polluted waters by nested PCR amplification. Applied and Environmental Microbiology 60 8 (1994) 2963-2970
37. Shah K.V. Polyomaviruses. In: Fields B.N., Knipe D.M., and Howley P.M. (Eds). Fields Virology. third ed. (1995), Raven Publishers, Philadelphia, PA 1997-2005
38. Stewart P.L., Fuller S.D., and Burnett R.M. Difference imaging of adenovirus-bridging the resolution gap between X-ray crystallography and electron-microscopy. EMBO Journal 12 (1993) 2589-2599
39. Thompson S.S., Jackson J.L., Suva-Castillo M., Yanko W.A., El Jack Z., Kuo J., Chen C.L., Williams F.P., and Schnurr D.P. Detection of infectious human adenoviruses in tertiary-treated and ultraviolet-disinfected wastewater. Water and Environmental Research 75 2 (2003) 163-170
40. Thurston-Enriquez J.A., Haas C.N., Jacangelo J., and Gerba C.P. Inactivation of enteric adenovirus and feline calicivirus by ozone. Water Research 39 (2005) 3650-3656
41. Tree J.A., Adams M.R., and Lees D.N. Chlorination of indicator bacteria and viruses in primary sewage effluent. Applied and Environmental Microbiology 69 (2003) 2038-2043
42. Van Heerden J., Ehlers M.M., Heim A., and Grabow W.O.K. Prevalence, quantification and typing of adenoviruses detected in river and treated drinking water in South Africa. Journal of Applied Microbiology 99 (2005) 234-242
43. Vilaginès P., Sarrette B., Husson G., and Vilagines R. Glass wool for virus concentration at ambient water pH level. Water Science and Technology 27 (1993) 299-306
44. Wadell G., Allard A., Svensson L., and Uhnoo I. Enteric adenoviruses. In: Farthing M. (Ed). Viruses and the Gut, Proceedings of the Ninth BSG·SK&F International Workshop (1988), Swan Press Ltd., London, U.K. 71-78
45. Wold W.S.M., and Horwitz M.S. Adenoviruses. In: Knipe D.M., and Howley P.M. (Eds). Fields Virology. seventh ed. (2007), Lippincott Williams & Wilkins, Philadelphia, PA 2395-2436
46. World Health Organization. Emerging Issues in Water and Infectious Disease. Available from: (2003). http://www.who.int/water_sanitation_health/emerging/emerging.pdf
47. Yokoyama T., Murai K., Murozuka T., Wakisaka A., Tanifuji M., Fujii N., and Tomono T. Removal of small non-enveloped viruses by nanofiltration. Vox Sanguinis 86 (2004) 225-229