Skip to main content

Viruses as Tracers of Fecal Contamination

  • Chapter
  • First Online:

Abstract

In assessments of water quality, determining the source of fecal ­contamination is of paramount importance for mitigating contamination, maintaining­ and restoring healthy ecosystems, and protecting public health. Historically, attention has focused on the use of fecal indicator bacteria (FIB) to indicate the level of fecal contamination, but over the past decade some attention has shifted to the use of pathogenic viruses to determine source(s) of fecal contamination and to assess risks to human health. Initially, viral detection methodologies were used to examine drinking water quality; however, the power of those methodologies has been recognized by those concerned with environmental water quality. Efforts have been made to apply these methods to natural water systems, including recreational waters, stormwater, and shellfishing areas. This chapter addresses the use of viruses in microbial source tracking (MST), specifically the application of quantitative tests for specific types of human pathogenic viruses, and how to choose the most appropriate assay for a particular study. Examples of studies utilizing a range of human pathogenic viruses, concentration and quantification approaches, successful case ­studies, and challenges associated with the use of viral MST methods are discussed.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Abdelzaher, A.M., Wright, M.E., Ortega, C., Solo-Gabriele, H.M., Miller, G., Elmir, S., Newman, X., Shih, P., Bonilla, J.A., Bonilla, T.D., Palmer, C.J., Scott, T., Lukasik, J., Harwood, V.J., McQuaig, S., Sinigalliano, C., Gidley, M., Plano, L.R., Zhu, X., Wang, J.D. and Fleming, L.E. (2010) Presence of pathogens and indicator microbes at a non-point source subtropical recreational marine beach. Appl Environ Microbiol 76, 724–732.

    PubMed  CAS  Google Scholar 

  • Adkins, S.B. (1997) Immunizations: current recommendations. Am Fam Physician 56, 865–874.

    PubMed  Google Scholar 

  • Ahmed, W., A.Goonetilleke and T.Gardner (2010) Human and bovine adenoviruses for the detection of source-specific fecal pollution in coastal waters in Australia. Water Res 44, 4662–4673.

    PubMed  CAS  Google Scholar 

  • Ahmed, W., Goonetilleke, A., Powell, D., Chauhan, K. and Gardner, T. (2009) Comparison of molecular markers to detect fresh sewage in environmental waters. Water Res 43, 4908–4917.

    PubMed  CAS  Google Scholar 

  • Albinana-Gimenez, N., Clemente-Casares, P., Calgua, B., Huguet, J.M., Courtois, S. and Girones, R. (2009) Comparison of methods for concentrating human adenoviruses, polyomavirus JC and noroviruses in source waters and drinking water using quantitative PCR. J Virol Methods 158, 104–109.

    PubMed  CAS  Google Scholar 

  • Alonso, M.C., Rodriguez, J. and Borrego, J.J. (1999) Enumeration and isolation of viral particles from oligotrophic marine environments by tangential flow filtration. Int Microbiol 2, 227–232.

    PubMed  CAS  Google Scholar 

  • American Public Health Association (1998) Standard Methods for the Examination of Water and Wastewater. Maryland. pp. 9.137–9.141: American Public Health Association.

    Google Scholar 

  • Arthur, R.R., Dagostin, S. and Shah, K.V. (1989) Detection of BK virus and JC virus in urine and brain tissue by the polymerase chain reaction. J Clin Microbiol 27, 1174–1179.

    PubMed  CAS  Google Scholar 

  • Barwick, R.S., Levy, D.A., Craun, G.F., Beach, M.J. and Calderon, R.L. (2000) Surveillance for waterborne-disease outbreaks--United States, 1997-1998. MMWR CDC Surveill Summ 49, 1–21.

    PubMed  CAS  Google Scholar 

  • Betancourt, W.Q. and Rose, J.B. (2005) Microbiological assessment of ambient waters and proposed water sources for restoration of a Florida wetland. J Water Health 3, 89–100.

    PubMed  CAS  Google Scholar 

  • Bialasiewicz, S., Whiley, D.M., Lambert, S.B., Nissen, M.D. and Sloots, T.P. (2009) Detection of BK, JC, WU, or KI polyomaviruses in faecal, urine, blood, cerebrospinal fluid and respiratory samples. J Clin Virol 45, 249–254.

    PubMed  CAS  Google Scholar 

  • Bitton, G. (2005) Wastewater Microbiology. Hoboken, N.J.: Wiley, Johns & Sons, Incorporated.

    Google Scholar 

  • Blatchley, E.R., 3rd, Gong, W.L., Alleman, J.E., Rose, J.B., Huffman, D.E., Otaki, M. and Lisle, J.T. (2007) Effects of wastewater disinfection on waterborne bacteria and viruses. Water Environ Res 79, 81–92.

    PubMed  CAS  Google Scholar 

  • Bofill-Mas, S., Formiga-Cruz, M., Clemente-Casares, P., Calafell, F. and Girones, R. (2001) Potential transmission of human polyomaviruses through the gastrointestinal tract after exposure to virions or viral DNA. J Virol 75, 10290–10299.

    PubMed  CAS  Google Scholar 

  • Bofill-Mas, S., Pina, S. and Girones, R. (2000) Documenting the epidemiologic patterns of polyomaviruses in human populations by studying their presence in urban sewage. Appl Environ Microbiol 66, 238–245.

    PubMed  CAS  Google Scholar 

  • Büchen-Osmond, C. (2006a) ICTVdB Management (2006) 00.012.0.03. Norovirus. In: ICTVdB – The Universal Virus Database, version 4 Columbia University, New York, USA http://wwwncbinlmnihgov/ICTVdb/Ictv/fs_indexhtm.

  • Büchen-Osmond, C. (2006b) ICTVdB Management (2006) 00.052.0.01. Enterovirus. In: ICTVdB – The Universal Virus Database, version 4 Columbia University, New York, USA http://wwwncbinlmnihgov/ICTVdb/Ictv/fs_indexhtm.

  • Büchen-Osmond, C. (2006c) ICTVdB Management (2006) 00.052.0.03. Hepatovirus. In: ICTVdB – The Universal Virus Database, version 4 Columbia University, New York, USA http://wwwncbinlmnihgov/ICTVdb/Ictv/fs_indexhtm.

  • Büchen-Osmond, C. (2006d) ICTVdB Management (2006) 00.060.0.03. Rotavirus. In: ICTVdB – The Universal Virus Database, version 4 Columbia University, New York, USA http://wwwncbinlmnihgov/ICTVdb/Ictv/fs_indexhtm.

  • Büchen-Osmond, C. (2006e) Index of Viruses – Adenoviridae (2006). In: ICTVdB – The Universal Virus Database, version 4 Columbia University, New York, USA http://wwwncbinlmnihgov/ICTVdb/Ictv/fs_indexhtm.

  • Büchen-Osmond, C. (2006f) Index of Viruses – Astroviridae (2006). In: ICTVdB – The Universal Virus Database, version 4 Columbia University, New York, USA http://wwwncbinlmnihgov/ICTVdb/Ictv/fs_indexhtm.

  • Büchen-Osmond, C. (2006g) Index of Viruses – Hepevirus (2006). In: ICTVdB - The Universal Virus Database, version 4 Columbia University, New York, USA http://wwwncbinlmnihgov/ICTVdb/Ictv/fs_indexhtm.

  • Burgener, M., Candrian, U. and Gilgen, M. (2003) Comparative evaluation of four large-volume RNA extraction kits in the isolation of viral RNA from water samples. J Virol Methods 108, 165–170.

    PubMed  CAS  Google Scholar 

  • Centers for Disease Control and Prevention (2003) Norovirus Activity-United States, 2002. MMWR 52, 41–45.

    Google Scholar 

  • Chapron, C.D., Ballester, N.A., Fontaine, J.H., Frades, C.N. and Margolin, A.B. (2000) 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 66, 2520–2525.

    PubMed  CAS  Google Scholar 

  • Colford, J.M., Wade, T.J., Schiff, K.C., Wright, C.C., Griffith, J., Sandhu, S.K., Burns, S., Sobsey, M.D., Lovelace, G.L. and Weisberg, S.B. (2007) Water quality indicators and the risk of illness at beaches with nonpoint sources of fecal contamination. Epidemiology 18, 27–35.

    PubMed  Google Scholar 

  • da Silva, A.K., Le Saux, J.C., Parnaudeau, S., Pommepuy, M., Elimelech, M. and Le Guyader, F.S. (2007) Evaluation of removal of noroviruses during wastewater treatment, using real-time reverse transcription-PCR: different behaviors of genogroups I and II. Appl Environ Microbiol 73, 7891–7897.

    PubMed  Google Scholar 

  • Dahling, D.R. and Wright, B.A. (1986) Recovery of viruses from water by a modified flocculation procedure for second-step concentration. Appl Environ Microbiol 51, 1326–1331.

    PubMed  CAS  Google Scholar 

  • Dong, Y., Kim, J. and Lewis, G.D. (2009) Evaluation of methodology for detection of human adenoviruses in wastewater, drinking water, stream water and recreational waters. J Appl Microbiol 108, 800–809.

    PubMed  Google Scholar 

  • Dorries, K. (1998) Molecular biology and pathogenesis of human polyomavirus infections. Dev Biol Stand 94, 71–79.

    PubMed  CAS  Google Scholar 

  • Dziuban, E.J., Liang, J.L., Craun, G.F., Hill, V., Yu, P.A., Painter, J., Moore, M.R., Calderon, R.L., Roy, S.L. and Beach, M.J. (2006) Surveillance for waterborne disease and outbreaks associated with recreational water--United States, 2003-2004. MMWR Surveill Summ 55, 1–30.

    PubMed  Google Scholar 

  • Finkbeiner, S.R., Kirkwood, C.D. and Wang, D. (2008) Complete genome sequence of a highly divergent astrovirus isolated from a child with acute diarrhea. Virol J 5, 117.

    PubMed  Google Scholar 

  • Fong, T., Phanikumar, M., Xagoraraki, I. and Rose, J.B. (2010) Quantitative detection of human adenoviruses 1 in waste water and two combined sewer overflows influencing a Michigan river. Appl Environ Microbiol 76(3): 715–723.

    Google Scholar 

  • Fong, T.T., Griffin, D.W. and Lipp, E.K. (2005) Molecular assays for targeting human and bovine enteric viruses in coastal waters and their application for library-independent source tracking. Appl Environ Microbiol 71, 2070–2078.

    PubMed  CAS  Google Scholar 

  • Fong, T.T. and Lipp, E.K. (2005) Enteric viruses of humans and animals in aquatic environments: health risks, detection, and potential water quality assessment tools. Microbiol Mol Biol Rev 69, 357–371.

    PubMed  CAS  Google Scholar 

  • Fuhrman, J.A., Liang, X. Noble, R.T. (2005) Rapid detection of enteroviruses in small volumes of natural waters by real-time quantitative reverse transcriptase PCR. Appl Environ Microbiol 71(8): 4523–4530.

    PubMed  CAS  Google Scholar 

  • Fumian, T.M., Guimaraes, F.R., Pereira Vaz, B.J., da Silva, M.T., Muylaert, F.F., Bofill-Mas, S., Girones, R., Leite, J.P. and Miagostovich, M.P. (2010) Molecular detection, quantification and characterization of human polyomavirus JC from waste water in Rio De Janeiro, Brazil. J Water Health 8, 438–445.

    PubMed  CAS  Google Scholar 

  • Gersberg, R.M., Rose, M.A., Robles-Sikisaka, R. and Dhar, A.K. (2006) Quantitative detection of hepatitis a virus and enteroviruses near the United States-Mexico border and correlation with levels of fecal indicator bacteria. Appl Environ Microbiol 72, 7438–7444.

    PubMed  CAS  Google Scholar 

  • Gilgen, M., Wegmuller, B., Burkhalter, P., Buhler, H.P., Muller, U., Luthy, J. and Candrian, U. (1995) Reverse transcription PCR to detect enteroviruses in surface water. Appl Environ Microbiol 61, 1226–1231.

    PubMed  CAS  Google Scholar 

  • Greenberg, H.B. and Estes, M.K. (2009) Rotaviruses: from pathogenesis to vaccination. Gastroenterology 136, 1939–1951.

    PubMed  CAS  Google Scholar 

  • Gregory, J.B., Litaker, R.W. and Noble, R.T. (2006) Rapid one-step quantitative reverse transcriptase PCR assay with competitive internal positive control for detection of enteroviruses in environmental samples. Appl Environ Microbiol 72, 3960–3967.

    PubMed  CAS  Google Scholar 

  • Gregory, J.B., Webster, L.F., Griffith, J.F. and Stewart, J.R. (2011) Improved detection and quantitation of norovirus from water. Viro Methods 172, (1–2): 38–45.

    PubMed  CAS  Google Scholar 

  • Griffin, D.W., Donaldson, K.A., Paul, J.H. and Rose, J.B. (2003) Pathogenic human viruses in coastal waters. Clin Microbiol Rev 16, 129–143.

    PubMed  Google Scholar 

  • Griffin, D.W., Gibson, C.J., 3rd, Lipp, E.K., Riley, K., Paul, J.H., 3rd and Rose, J.B. (1999) Detection of viral pathogens by reverse transcriptase PCR and of microbial indicators by standard methods in the canals of the Florida Keys. Appl Environ Microbiol 65, 4118–4125.

    PubMed  CAS  Google Scholar 

  • Guttman-Bass, N. and Nasser, A. (1984) Simultaneous concentration of four enteroviruses from tap, waste, and natural waters. Appl Environ Microbiol 47, 1311–1315.

    PubMed  CAS  Google Scholar 

  • Hamza, I.A., Jurzik, L., Stang, A., Sure, K., Uberla, K. and Wilhelm, M. (2009) 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 43, 2657–2668.

    PubMed  CAS  Google Scholar 

  • Haramoto, E., Katayama, H., Oguma, K., Yamashita, H., Tajima, A., Nakajima, H. and Ohgaki, S. (2006) Seasonal profiles of human noroviruses and indicator bacteria in a wastewater treatment plant in Tokyo, Japan. Water Sci Technol 54, 301–308.

    PubMed  CAS  Google Scholar 

  • Haramoto, E., Kitajima, M., Katayama, H. and Ohgaki, S. (2010) Real-time PCR detection of adenoviruses, polyomaviruses, and torque teno viruses in river water in Japan. Water Res 44, 1747–1752.

    PubMed  CAS  Google Scholar 

  • Havelaar, A.H., Pot-Hogeboom, W.M., Furuse, K., Pot, R. and Hormann, M.P. (1990) F-specific RNA bacteriophages and sensitive host strains in faeces and wastewater of human and animal origin. J Appl Bacteriol 69, 30–37.

    PubMed  CAS  Google Scholar 

  • He, J. and Jiang, S. (2005) Quantification of enterococci and human adenoviruses in environmental samples by real-time PCR. Appl Env Micro 71, 2250–2255.

    CAS  Google Scholar 

  • Hijnen, W.A., Beerendonk, E.F. and Medema, G.J. (2006) Inactivation credit of UV radiation for viruses, bacteria and protozoan (oo)cysts in water: a review. Water Res 40, 3–22.

    PubMed  CAS  Google Scholar 

  • Hirsch, H.H. and Steiger, J. (2003) Polyomavirus BK. Lancet Infect Dis 3, 611–623.

    PubMed  Google Scholar 

  • Hogan, T.F., Padgett, B.L., Walker, D.L., Borden, E.C. and McBain, J.A. (1980) Rapid detection and identification of JC virus and BK virus in human urine by using immunofluorescence microscopy. J Clin Microbiol 11, 178–183.

    PubMed  CAS  Google Scholar 

  • Hsu, B.M., Chen, C.H. and Wan, M.T. (2008) Prevalence of enteroviruses in hot spring recreation areas of Taiwan. FEMS Immunol Med Microbiol 52, 253–259.

    PubMed  CAS  Google Scholar 

  • Hundesa, A., Maluquer de Motes, C., Albinana-Gimenez, N., Rodriguez-Manzano, J., Bofill-Mas, S., Sunen, E. and Rosina Girones, R. (2009) Development of a qPCR assay for the quantification of porcine adenoviruses as an MST tool for swine fecal contamination in the environment. J Virol Methods 158, 130–135.

    PubMed  CAS  Google Scholar 

  • Hundesa, A., Maluquer de Motes, C., Bofill-Mas, S., Albinana-Gimenez, N. and Girones, R. (2006) Identification of human and animal adenoviruses and polyomaviruses for determination of sources of fecal contamination in the environment. Appl Environ Microbiol 72, 7886–7893.

    PubMed  CAS  Google Scholar 

  • Jiang, S., Noble, R. and Chu, W. (2001) Human adenoviruses and coliphages in urban runoff-impacted coastal waters of Southern California. Appl Environ Microbiol 67, 179–184.

    PubMed  CAS  Google Scholar 

  • Jiang, S.C. (2006) Human adenoviruses in water: occurrence and health implications: a critical review. Environ Sci Technol 40, 7132–7140.

    PubMed  CAS  Google Scholar 

  • Jiang, S.C. and Chu, W. (2004) PCR detection of pathogenic viruses in southern California urban rivers. J Appl Microbiol 97, 17–28.

    PubMed  CAS  Google Scholar 

  • Jiang, S.C., Chu, W. and He, J.W. (2007a) Seasonal detection of human viruses and coliphage in Newport Bay, California. Appl Environ Microbiol 73, 6468–6474.

    PubMed  CAS  Google Scholar 

  • Jiang, S.C., Chu, W., Olson, B.H., He, J.W., Choi, S., Zhang, J., Le, J.Y. and Gedalanga, P.B. (2007b) Microbial source tracking in a small southern California urban watershed indicates wild animals and growth as the source of fecal bacteria. Appl Microbiol Biotechnol 76, 927–934.

    PubMed  CAS  Google Scholar 

  • Jimenez-Clavero, M.A., Escribano-Romero, E., Mansilla, C., Gomez, N., Cordoba, L., Roblas, N., Ponz, F., Ley, V. and Saiz, J.C. (2005) Survey of bovine enterovirus in biological and environmental samples by a highly sensitive real-time reverse transcription-PCR. Appl Environ Microbiol 71, 3536–3543.

    PubMed  CAS  Google Scholar 

  • Katayama, H., Haramoto, E., Oguma, K., Yamashita, H., Tajima, A., Nakajima, H. and Ohgaki, S. (2008) One-year monthly quantitative survey of noroviruses, enteroviruses, and adenoviruses in wastewater collected from six plants in Japan. Water Res 42, 1441–1448.

    PubMed  CAS  Google Scholar 

  • Katayama, H., Shimasaki, A. and Ohgaki, S. (2002) Development of a virus concentration method and its application to detection of enterovirus and norwalk virus from coastal seawater. Appl Environ Microbiol 68(3): 1033–1039.

    PubMed  CAS  Google Scholar 

  • Khalil, S.M. and Stoner, G.L. (2001) Human Polyomaviruses: Molecular and Clinical Perspectives. New York: Wiley-Liss Inc.

    Google Scholar 

  • Khetsuriani, N., Lamonte-Fowlkes, A., Oberst, S. and Pallansch, M.A. (2006) Enterovirus surveillance-United States, 1970-2005. MMWR Surveill Summ 55, 1–20.

    PubMed  Google Scholar 

  • Kramer, M.H., Herwaldt, B.L., Craun, G.F., Calderon, R.L. and Juranek, D.D. (1996) Surveillance for waterborne-disease outbreaks--United States, 1993-1994. MMWR CDC Surveill Summ 45, 1–33.

    PubMed  CAS  Google Scholar 

  • Kuniholm, M.H., Purcell, R.H., McQuillan, G.M., Engle, R.E., Wasley, A. and Nelson, K.E. (2009) Epidemiology of Hepatitis E Virus in the United States: Results from the Third National Health and Nutrition Examination Survey, 1988-1994. J Infect Dis 200, 48–56.

    PubMed  Google Scholar 

  • Kunitake, T., Kitamura, T., Guo, J., Taguchi, F., Kawabe, K. and Yogo, Y. (1995) Parent-to-child transmission is relatively common in the spread of the human polyomavirus JC virus. J Clin Microbiol 33, 1448–1451.

    PubMed  CAS  Google Scholar 

  • Lee, G. and Lee, C. (2008) Molecular detection and characterization of human enteroviruses in Korean surface water. J Microbiol 46, 319–324.

    PubMed  CAS  Google Scholar 

  • Lee, S.H., Lee, C., Lee, K.W., Cho, H.B. and Kim, S.J. (2005) 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 98, 1020–1029.

    PubMed  CAS  Google Scholar 

  • Lee, S.H., Levy, D.A., Craun, G.F., Beach, M.J. and Calderon, R.L. (2002) Surveillance for waterborne-disease outbreaks--United States, 1999-2000. MMWR Surveill Summ 51, 1–47.

    PubMed  CAS  Google Scholar 

  • Lee, T.W. and Kurtz, J.B. (1982) Human astrovirus serotypes. J Hyg (Lond) 89, 539–540.

    CAS  Google Scholar 

  • Lemarchand, K., Masson, L. and Brousseau, R. (2004) Molecular biology and DNA microarray technology for microbial quality monitoring of water. Crit Rev Microbiol 30, 145–172.

    PubMed  CAS  Google Scholar 

  • Leskinen, S., Brownell, M., Lim, D. and Harwood, V.J. (2010) Hollow-Fiber ultrafiltration and PCR detection of human-associated genetic markers from various types of surface water in Florida. Appl Env Micro 76, 4116–7.

    CAS  Google Scholar 

  • Levy, D.A., Bens, M.S., Craun, G.F., Calderon, R.L. and Herwaldt, B.L. (1998) Surveillance for waterborne-disease outbreaks--United States, 1995-1996. MMWR CDC Surveill Summ 47, 1–34.

    PubMed  CAS  Google Scholar 

  • Ley, V., Higgins, J. and Fayer, R. (2002) Bovine enteroviruses as indicators of fecal contamination. Appl Environ Microbiol 68, 3455–3461.

    PubMed  CAS  Google Scholar 

  • Lipp, E.K., Futch, J.C. and Griffin, D.W. (2007) Analysis of multiple enteric viral targets as sewage markers in coral reefs. Mar Pollut Bull 54, 1897–1902.

    PubMed  CAS  Google Scholar 

  • Maluquer de Motes, C., Clemente-Casares, P., Hundesa, A., Martin, M. and Girones, R. (2004) Detection of bovine and porcine adenoviruses for tracing the source of fecal contamination. Appl Environ Microbiol 70, 1448–1454.

    PubMed  Google Scholar 

  • Markowitz, R.B., Thompson, H.C., Mueller, J.F., Cohen, J.A. and Dynan, W.S. (1993) Incidence of BK virus and JC virus viruria in human immunodeficiency virus-infected and -uninfected subjects. J Infect Dis 167, 13–20.

    PubMed  CAS  Google Scholar 

  • McQuaig, S.M. (2009) The development of a human polyomavirus quantitative PCR assay to assess viral persistence, water quality, and human health risks Dissertation, University of South Florida.

    Google Scholar 

  • McQuaig, S.M., Scott, T.M., Harwood, V.J., Farrah, S.R. and Lukasik, J.O. (2006) Detection of human derived fecal pollution in environmental waters using a PCR based human polyomavirus assay. Appl Environ Microbiol 72, 7567–7574.

    PubMed  CAS  Google Scholar 

  • McQuaig, S.M., Scott, T.M., Lukasik, J.O., Paul, J.H. and Harwood, V.J. (2009) 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 75, 3379–3388.

    PubMed  CAS  Google Scholar 

  • Moore, A.C., Herwaldt, B.L., Craun, G.F., Calderon, R.L., Highsmith, A.K. and Juranek, D.D. (1993) Surveillance for waterborne disease outbreaks--United States, 1991-1992. MMWR CDC Surveill Summ 42, 1–22.

    PubMed  CAS  Google Scholar 

  • Murray, P., Rosenthal, K., Kobayashi, G. and Pfaller, M. (2002) Medical Microbiology. St. Louis: Mosby-Year Book, Inc.

    Google Scholar 

  • Neefe, J.R., Baty, J.B., Reinhold, J.G. and Stokes, J. (1947) Inactivation of the Virus of Infectious Hepatitis in Drinking Water. Am J Public Health Nations Health 37, 365–372.

    CAS  Google Scholar 

  • Oberste, M.S., Maher, K., Kilpatrick, D.R. and Pallansch, M.A. (1999) Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J Virol 73, 1941–1948.

    PubMed  CAS  Google Scholar 

  • Olszewski, J., Winona, L. and Oshima, K.H. (2005) Comparison of 2 ultrafiltration systems for the concentration of seeded viruses from environmental waters. Can J Microbiol 51, 295–303.

    PubMed  CAS  Google Scholar 

  • Patel, M.M., Hall, A.J., Vinje, J. and Parashar, U.D. (2009) Noroviruses: a comprehensive review. J Clin Virol 44, 1–8.

    PubMed  CAS  Google Scholar 

  • Paul, J.H., Jiang, S.C. and Rose, J.B. (1991) Concentration of viruses and dissolved DNA from aquatic environments by vortex flow filtration. Appl Environ Microbiol 57, 2197–2204.

    PubMed  CAS  Google Scholar 

  • Payment, P., Berube, A., Perreault, D., Armon, R. and Trudel, M. (1989) Concentration of Giardia lamblia cysts, Legionella pneumophila, Clostridium perfringens, human enteric viruses, and coliphages from large volumes of drinking water, using a single filtration. Can J Microbiol 35, 932–935.

    PubMed  CAS  Google Scholar 

  • Payment, P., Larose, Y. and Trudel, M. (1979) Polioviruses and other enteroviruses in urban sewage from Laval (Canada): presence of non-vaccinal strains of poliovirus. Can J Microbiol 25, 1305–1309.

    PubMed  CAS  Google Scholar 

  • Phan, T.G., Khamrin, P., Quang, T.D., Dey, S.K., Takanashi, S., Okitsu, S., Maneekarn, N. and Ushijima, H. (2007) Detection and genetic characterization of group A rotavirus strains circulating among children with acute gastroenteritis in Japan. J Virol 81, 4645–4653.

    PubMed  CAS  Google Scholar 

  • Pianetti, A., Baffone, W., Citterio, B., Casaroli, A., Bruscolini, F. and Salvaggio, L. (2000) Presence of enteroviruses and reoviruses in the waters of the Italian coast of the Adriatic Sea. Epidemiol Infect 125, 455–462.

    PubMed  CAS  Google Scholar 

  • Pina, S., Puig, M., Lucena, F., Jofre, J. and Girones, R. (1998) Viral pollution in the environment and in shellfish: human adenovirus detection by PCR as an index of human viruses. Appl Environ Microbiol 64, 3376–3382.

    PubMed  CAS  Google Scholar 

  • Polo, C., Perez, J.L., Mielnichuck, A., Fedele, C.G., Niubo, J. and Tenorio, A. (2004) Prevalence and patterns of polyomavirus urinary excretion in immunocompetent adults and children. Clin Microbiol Infect 10, 640–644.

    PubMed  CAS  Google Scholar 

  • Pusch, D., Oh, D.Y., Wolf, S., Dumke, R., Schroter-Bobsin, U., Hohne, M., Roske, I. and Schreier, E. (2005) Detection of enteric viruses and bacterial indicators in German environmental waters. Arch Virol 150, 929–947.

    PubMed  CAS  Google Scholar 

  • Rafique, A. and Jiang, S.C. (2008) Genetic diversity of human polyomavirus JCPyV in Southern California wastewater. J Water Health 6, 533–538.

    PubMed  Google Scholar 

  • Rajal, V.B., McSwain, B.S., Thompson, D.E., Leutenegger, C.M. and Wuertz, S. (2007) Molecular quantitative analysis of human viruses in California stormwater. Water Res 41, 4287–4298.

    PubMed  CAS  Google Scholar 

  • Rigotto, C., Kolesnikovas, C.K., Moresco, V., Simoes, C.M. and Barardi, C.R. (2009) Evaluation of HA negatively charged membranes in the recovery of human adenoviruses and hepatitis A virus in different water matrices. Mem Inst Oswaldo Cruz 104, 970–974.

    PubMed  CAS  Google Scholar 

  • Rose, M.A., Dhar, A.K., Brooks, H.A., Zecchini, F. and Gersberg, R.M. (2006) Quantitation of hepatitis A virus and enterovirus levels in the lagoon canals and Lido beach of Venice, Italy, using real-time RT-PCR. Water Res 40, 2387–2396.

    PubMed  CAS  Google Scholar 

  • Schwartzbrod, L., Pommepuy, M., Albert, M., Dupray, E., Boher, S., Beril, C. and Guichaoua, C. (1991) Influence of sewage discharge on the pollution of an estuary (Morlaix, France). Zentralbl Hyg Umweltmed 192, 238–247.

    PubMed  CAS  Google Scholar 

  • Shah, K.V. (1996) Polyomaviruses. Philadelphia: Lippincott–Raven.

    Google Scholar 

  • Shah, K.V., Daniel, R.W. and Warszawski, R.M. (1973) High prevalence of antibodies to BK virus, an SV40-related papovavirus, in residents of Maryland. J Infect Dis 128, 784–787.

    PubMed  CAS  Google Scholar 

  • Shields, P.A. and Farrah, S.R. (1986) Concentration of viruses in beef extract by flocculation with ammonium sulfate. Appl Environ Microbiol 51, 211–213.

    PubMed  CAS  Google Scholar 

  • Sobsey, M.D. and Glass, J.S. (1984) Influence of water quality on enteric virus concentration by microporous filter methods. Appl Environ Microbiol 47, 956–960.

    PubMed  CAS  Google Scholar 

  • Thurston-Enriquez, J.A., Haas, C.N., Jacangelo, J. and Gerba, C.P. (2003a) Chlorine inactivation of adenovirus type 40 and feline calicivirus. Appl Environ Microbiol 69, 3979–3985.

    PubMed  CAS  Google Scholar 

  • Thurston-Enriquez, J.A., Haas, C.N., Jacangelo, J., Riley, K. and Gerba, C.P. (2003b) Inactivation of feline calicivirus and adenovirus type 40 by UV radiation. Appl Environ Microbiol 69, 577–582.

    PubMed  CAS  Google Scholar 

  • Tsai, Y.L., Sobsey, M.D., Sangermano, L.R. and Palmer, C.J. (1993) Simple method of concentrating enteroviruses and hepatitis A virus from sewage and ocean water for rapid detection by reverse transcriptase-polymerase chain reaction. Appl Environ Microbiol 59, 3488–3491.

    PubMed  CAS  Google Scholar 

  • Tsai, Y.L., Tran, B., Sangermano, L.R. and Palmer, C.J. (1994) Detection of poliovirus, hepatitis A virus, and rotavirus from sewage and ocean water by triplex reverse transcriptase PCR. Appl Environ Microbiol 60, 2400–2407.

    PubMed  CAS  Google Scholar 

  • U.S. Environmental Protection Agency (1995) USEPA Manual of Methods for Virology No. EPA 600/4-84/013 (N15). Washington, D.C.: U.S. Environmental Protection Agency.

    Google Scholar 

  • van Heerden, J., Ehlers, M.M., Heim, A. and Grabow, W.O. (2005) Prevalence, quantification and typing of adenoviruses detected in river and treated drinking water in South Africa. J Appl Microbiol 99, 234–242.

    PubMed  Google Scholar 

  • Vanchiere, J.A., White, Z.S. and Butel, J.S. (2005) Detection of BK virus and simian virus 40 in the urine of healthy children. J Med Virol 75, 447–454.

    PubMed  CAS  Google Scholar 

  • Vantarakis, A. and Papapetropoulou, M. (1999) Detection of enteroviruses, adenoviruses and hepatitis A viruses in raw sewage and treated eflluents by nested-PCR. Water, Air, and Soil Poll 114, 85–93.

    CAS  Google Scholar 

  • Villar, L.M., de Paula, V.S., Diniz-Mendes, L., Lampe, E. and Gaspar, A.M. (2006) Evaluation of methods used to concentrate and detect hepatitis A virus in water samples. J Virol Methods 137, 169–176.

    PubMed  CAS  Google Scholar 

  • Walter, J.E. and Mitchell, D.K. (2003) Astrovirus infection in children. Curr Opin Infect Dis 16, 247–253.

    PubMed  Google Scholar 

  • Wetz, J.J., Lipp, E.K., Griffin, D.W., Lukasik, J., Wait, D., Sobsey, M.D., Scott, T.M. and Rose, J.B. (2004) Presence, infectivity, and stability of enteric viruses in seawater: relationship to marine water quality in the Florida Keys. Mar Pollut Bull 48, 698–704.

    PubMed  CAS  Google Scholar 

  • White, M.K., Gordon, J., Reiss, K., Del Valle, L., Croul, S., Giordano, A., Darbinyan, A. and Khalili, K. (2005) Human polyomaviruses and brain tumors. Brain Res Brain Res Rev 50, 69–85.

    PubMed  CAS  Google Scholar 

  • Wolf, S., Hewitt, J. and Greening, G.E. A viral tool box of multiplex qPCR assays for tracking the sources of fecal contamination. Appl Environ Microbiol 2010; 76, 1388–1394.

    PubMed  CAS  Google Scholar 

  • Wong, M., Kumar, L., Jenkins, T.M., Xagoraraki, I., Phanikumar, M.S. and Rose, J.B. (2009) Evaluation of public health risks at recreational beaches in Lake Michigan via detection of enteric viruses and a human-specific bacteriological marker. Water Res 43, 1137–1149.

    PubMed  CAS  Google Scholar 

  • Yoder, J.S., Blackburn, B.G., Craun, G.F., Hill, V., Levy, D.A., Chen, N., Lee, S.H., Calderon, R.L. and Beach, M.J. (2004) Surveillance for waterborne-disease outbreaks associated with recreational water--United States, 2001-2002. MMWR Surveill Summ 53, 1–22.

    PubMed  Google Scholar 

  • Yoder, J.S., Hlavsa, M.C., Craun, G.F., Hill, V., Roberts, V., Yu, P.A., Hicks, L.A., Alexander, N.T., Calderon, R.L., Roy, S.L. and Beach, M.J. (2008) 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 57, 1–29.

    PubMed  Google Scholar 

  • Zaitlin, M. (1999) Tobacco mosaic virus and its contributions to virology. ASM News 65, 675–680.

    Google Scholar 

  • Zhong, S., Zheng, H.Y., Suzuki, M., Chen, Q., Ikegaya, H., Aoki, N., Usuku, S., Kobayashi,N., Nukuzuma, S., Yasuda, Y., Kuniyoshi, N., Yogo, Y. and Kitamura, T. (2007) Age-related urinary excretion of BK polyomavirus by nonimmunocompromised individuals. J Clin Microbiol 45, 193–198.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. M. McQuaig .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

McQuaig, S.M., Noble, R.T. (2011). Viruses as Tracers of Fecal Contamination. In: Hagedorn, C., Blanch, A., Harwood, V. (eds) Microbial Source Tracking: Methods, Applications, and Case Studies. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-9386-1_5

Download citation

Publish with us

Policies and ethics