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Specific Viruses Present in Polluted Groundwater Are Indicative of the Source of Nitrates and Faecal Contamination in Agricultural Areas

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Experiences from Ground, Coastal and Transitional Water Quality Monitoring

Part of the book series: The Handbook of Environmental Chemistry ((HEC,volume 43))

Abstract

Microbial source tracking (MST) tools are used to identify sources of faecal pollution to accurately assess public health risks and implement best management practices. Many different viruses are excreted by humans and animals and are frequently detected in water contaminated with faeces or/and urine. Because of the large degree of host specificity of each virus and the substantial stability of many excreted viruses in the environment, some viral groups are considered to be accurate MST indicators. The Laboratory of Virus Contaminants of Water and Food at the University of Barcelona has proposed the use of viral indicators as well as cost-effective methods for the concentration of viruses from water. The developed procedures have been used to determine the levels of faecal pollution in environmental samples as well as for tracing the origin of faecal contamination. Such tools were recently used by the Catalan Water Agency to identify nitrate contamination sources in groundwater.

Human adenoviruses, human polyomavirus JC, porcine adenoviruses, bovine polyomaviruses, chicken/turkey parvoviruses, and ovine polyomaviruses can be quantified in samples using molecular methods (qPCR). The selected DNA viruses specifically infect their hosts and are persistently excreted in faeces and/or urine throughout the year in all geographical areas studied. The procedures that have been developed to quantify these viruses have been applied to bathing, coastal, surface and groundwater. In this study, the source of nitrate contamination in groundwater was identified by analysing viral markers, thereby demonstrating the usefulness of the selected viruses for the identification of sources of contamination in water. This methodology can be used to provide information to guide the proper application of measures in place to protect water from pollution caused by nitrates from several sources and thus to facilitate the accurate application of the 91/676/EEC Directive, which is mainly focused on agricultural sources of water contamination.

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Abbreviations

ACA:

Catalan Water Agency (in Catalan)

CRBD:

Catalan River Basin District

WFD:

Water Framework Directive

References

  1. Hunt RJ, Borchardt MA, Richards KD, Spencer SK (2010) Assessment of sewer source contamination of drinking water wells using tracers and human enteric viruses. Environ Sci Technol 44:7956–7963. doi:10.1021/es100698m

    Article  CAS  Google Scholar 

  2. Borchardt MA, Spencer SK, Kieke BA, Lambertini E, Loge FJ (2012) Viruses in nondisinfected drinking water from municipal wells and community incidence of acute gastrointestinal illness. Environ Health Perspect 120:1272–1279. doi:10.1289/ehp.1104499

    Article  Google Scholar 

  3. Abbaszadegan BYM, Lechevallier M, Gerba C (2003) Occurrence of viruses in ground waters. Am Water Works Assoc J 95:107–120

    CAS  Google Scholar 

  4. ACA (2012) Agència Catalana de l’Aigua, Generalitat de Catalunya. http://www.gencat.cat/aca/

  5. DEFRA (2006) Department for Environment, Food and Rural Affairs and the Forestry Commission, 2006 Report. http://archive.defra.gov.uk/corporate/about/reports/documents/2006deptreport.pdf. Accessed 17 Dec 2014

  6. IDESCAT (2012) Anuari estadístic de Ramaderia a Catalunya. http://www.idescat.cat/pub/?id=aec&n=48. Accessed 21 Mar 2014

  7. Decret 136/2009 (2009) Diari Oficial de la Generalitat de Catalunya, no5457, d’1 de setembre, d'aprovació del programa d’actuació aplicable a les zones vulnerables en relació amb la contaminació de nitrats que procedeixen de fonts agràries i de gestió de les dejeccions ra. 65858–65902

    Google Scholar 

  8. Decret 220/2001 (2001) Diari Oficial de la Generalitat de Catalunya, no3447, d’1 d'agost, de gestió de les dejeccions ramaderes. 2001:1–8

    Google Scholar 

  9. Rzezutka A, Cook N (2004) Survival of human enteric viruses in the environment and food. FEMS Microbiol Rev 28:441–453. doi:10.1016/j.femsre.2004.02.001

    Article  CAS  Google Scholar 

  10. John DE, Rose JB (2005) Review of factors affecting microbial survival in groundwater. Environ Sci Technol 39:7345–7356

    Article  CAS  Google Scholar 

  11. Meixell BW, Borchardt MA, Spencer SK (2013) Accumulation and inactivation of avian influenza virus by the filter-feeding invertebrate Daphnia magna. Appl Environ Microbiol 79:7249–7255. doi:10.1128/AEM.02439-13

    Article  CAS  Google Scholar 

  12. Gerba CP, Goyal SM, LaBelle RL, Cech I, Bodgan GF (1979) Failure of indicator bacteria to reflect the occurrence of enteroviruses in marine waters. Am J Public Health 69:1116–1119

    Article  CAS  Google Scholar 

  13. Solo-gabriele HM, Wolfert MA, Desmarais TR, Palmer CJ (2000) Sources of Escherichia coli in a Coastal Subtropical Environment. Appl Environ Microbiol 66:230–237

    Article  CAS  Google Scholar 

  14. Lipp EK, Farrah SA, Rose JB (2001) Assessment and impact of microbial fecal pollution and human enteric pathogens in a coastal community. Mar Pollut Bull 42:286–293

    Article  CAS  Google Scholar 

  15. Byappanahalli MN, Shively DA, Nevers MB, Sadowsky MJ, Whitman RL (2003) Growth and survival of Escherichia coli and enterococci populations in the macro-alga Cladophora (Chlorophyta). FEMS Microbiol Ecol 46:203–211. doi:10.1016/S0168-6496(03)00214-9

  16. Pote J, Haller L, Kottelat R, Sastre V, Arpagaus P, Wildi W (2009) Persistence and growth of faecal culturable bacterial indicators in water column and sediments of Vidy Bay, Lake Geneva, Switzerland. J Environ Sci (China) 21:62–69

    Article  CAS  Google Scholar 

  17. Field KG, Samadpour M, Wuertz S, Field J (2007) Fecal source tracking, the indicator paradigm, and managing water quality. Water Res 41:3517–3538. doi:10.1016/j.watres.2007.06.056

    Article  CAS  Google Scholar 

  18. Stoeckel DM, Harwood VJ (2007) Microbial source tracking studies MINIREVIEW. Appl Environ Microbiol. doi:10.1128/AEM.02473-06

    Google Scholar 

  19. Scott TM, Rose JB, Jenkins TM, Samuel R, Lukasik J, Farrah SR (2002) Microbial source tracking : current methodology and future directions microbial source tracking : current methodology and future directions. Appl Environ Microbiol 68:5796–5803. doi:10.1128/AEM.68.12.5796

    Article  CAS  Google Scholar 

  20. Simpson J, Santo Domingo J, Reasoner D (2002) Microbial source tracking: state of the science. Environ Sci Technol 36:5279–5288

    Article  CAS  Google Scholar 

  21. EPA (2005) Microbial source tracking guide document. U.S. Environmental Protection Agency, Cincinnati

    Google Scholar 

  22. Savichtcheva O, Okabe S (2006) Alternative indicators of fecal pollution: relations with pathogens and conventional indicators, current methodologies for direct pathogen monitoring and future application perspectives. Water Res 40:2463–2476

    Article  CAS  Google Scholar 

  23. Roslev P, Bukh A (2011) State of the art molecular markers for fecal pollution source tracking in water. Appl Microbiol Biotechnol 89:3080. doi:10.1007/s00253-010-3080-7

    Google Scholar 

  24. Wu J, Long SC, Das D, Dorner SM (2011) Are microbial indicators and pathogens correlated? A statistical analysis of 40 years of research. J Water Health 9(2):265–278. doi:10.2166/wh.2011.117

    Article  CAS  Google Scholar 

  25. Boehm AB, Van De Werfhorst LC, Griffith JF, Holden PA, Jay JA, Shanks OC, Wang D, Weisberg SB (2013) Performance of forty-one microbial source tracking methods: a twenty-seven lab evaluation study. Water Res 47:6812–6828. doi:10.1016/j.watres.2012.12.046

    Article  CAS  Google Scholar 

  26. Harwood VJ, Staley C, Badgley BD, Borges K, Korajkic A (2013) Microbial source tracking markers for detection of fecal contamination in environmental waters: relationships between pathogens and human health outcomes. FEMS Microbiol Rev. doi:10.1111/1574-6976.12031

    Google Scholar 

  27. Girones R, Ferrús M, Alonso J, Rodriguez-Manzano J, Calgua B, Corrêa A, Hundesa A, Carratala A, Bofill-Mas S (2010) Molecular detection of pathogens in water–the pros and cons of molecular techniques. Water Res 44:4325–4339. doi:10.1016/j.watres.2010.06.030

    Article  CAS  Google Scholar 

  28. Albinana-Gimenez N, Miagostovich MP, Calgua B, Huguet JM, Matia L, Girones R (2009) Analysis of adenoviruses and polyomaviruses quantified by qPCR as indicators of water quality in source and drinking-water treatment plants. Water Res 43:2011–2019. doi:10.1016/j.watres.2009.01.025

    Article  CAS  Google Scholar 

  29. Bofill-Mas S, Albinana-Gimenez N, Clemente-Casares P, Hundesa A, Rodriguez-Manzano J, Allard A, Calvo M, Girones R (2006) Quantification and stability of human adenoviruses and polyomavirus JCPyV in wastewater matrices. Appl Environ Microbiol 72:7894–7896. doi:10.1128/AEM.00965-06

    Article  CAS  Google Scholar 

  30. Brady AMG, Gellner TM, Spencer SK, Williston AG, Borchardt MA, Bushon RN, Francy DS, Riddell KR, Stelzer EA (2012) Comparative effectiveness of membrane bioreactors, conventional secondary treatment, and chlorine and UV disinfection to remove microorganisms from municipal waste waters. Water Res 46:4164–4178. doi: 10.1016/j.watres.2012.04.044

    Google Scholar 

  31. Havelaar AH, Furuse K, Hogeboom WM (1986) Bacteriophages and indicator bacteria in human and animal faeces. J Appl Bacteriol 60:255–262

    Google Scholar 

  32. Hsu FC, Shieh YS, van Duin J, Beekwilder MJ, Sobsey MD (1995) Genotyping male-specific RNA coliphages by hybridization with oligonucleotide probes. Appl Environ Microbiol 61:3960–3966

    CAS  Google Scholar 

  33. Schaper M, Jofre J, Uys M, Grabow WOK (2002) Distribution of genotypes of F-specific RNA bacteriophages in human and non-human sources of faecal pollution in South Africa and Spain. J Appl Microbiol 92:657–667

    Article  CAS  Google Scholar 

  34. Kirs M, Smith DC (2007) Multiplex quantitative real-time reverse transcriptase PCR for F+-specific RNA coliphages: a method for use in microbial source tracking. Appl Environ Microbiol 73:808–814. doi:10.1128/AEM.00399-06

    Article  CAS  Google Scholar 

  35. Kim S-H, Cheon D-S, Kim J-H, Lee D-H, Jheong W-H, Heo Y-J, Chung H-M, Jee Y, Lee J-S (2005) Outbreaks of gastroenteritis that occurred during school excursions in Korea were associated with several waterborne strains of norovirus. J Clin Microbiol 43:4836–4839. doi:10.1128/JCM.43.9.4836

    Article  CAS  Google Scholar 

  36. Chung H, Sobsey MD (1993) Comparative survival of indicator viruses and enteric viruses in seawater and sediment. Water Sci Tech 27:425–428

    Google Scholar 

  37. Doré WJ, Henshilwood K, Lees DN (2000) Evaluation of F-specific RNA bacteriophage as a candidate human enteric virus indicator for bivalve molluscan shellfish. Appl Environ Microbiol 66:1280–1285

    Article  Google Scholar 

  38. Tartera C, Jofre J (1987) Bacteriophages active against Bacteroides fragilis in sewage-polluted waters. Appl Environ Microbiol 53:1632–1637

    CAS  Google Scholar 

  39. Gómez-Doñate M, Payán A, Cortés I, Blanch AR, Lucena F, Jofre J, Muniesa M (2011) Isolation of bacteriophage host strains of Bacteroides species suitable for tracking sources of animal faecal pollution in water. Environ Microbiol 13:1622–1631. doi:10.1111/j.1462-2920.2011.02474.x

    Article  Google Scholar 

  40. Tartera C, Lucena F, Jofre J (1989) Human origin of Bacteroides fragilis bacteriophages present in the environment. Appl Environ Microbiol 55:2696–2701

    CAS  Google Scholar 

  41. Puig M, Jofre J, Lucena F, Allard A, Wadell G, Girones R (1994) Detection of adenoviruses and enteroviruses in polluted waters by nested PCR amplification. Appl Environ Microbiol 60:2963–2970

    CAS  Google Scholar 

  42. Pina S, Lucena F, Girones R (1998) Viral pollution in the environment and in Shellfish : human adenovirus detection by PCR as an index of human viruses viral pollution in the environment and in Shellfish: human adenovirus detection by PCR as an index of human viruses. Appl Environ Microbiol 64:3376

    CAS  Google Scholar 

  43. Hernroth B, Conden-Hansson A, Rehnstam-Holm A, Girones R, Allard A (2002) Environmental factors influencing human viral pathogens and their potential indicator organisms in the blue mussel, Mytilus edulis: the first Scandinavian report. Appl Environ Microbiol 68:4523–4533. doi:10.1128/AEM.68.9.4523

    Article  CAS  Google Scholar 

  44. Bofill-Mas S, Pina S, 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

    Article  CAS  Google Scholar 

  45. Pal A, Sirota L, Maudru T, Peden K, Lewis AM (2006) Real-time, quantitative PCR assays for the detection of virus-specific DNA in samples with mixed populations of polyomaviruses. J Virol Methods 135:32–42. doi:10.1016/j.jviromet.2006.01.018

    Article  CAS  Google Scholar 

  46. Fong T-T, Griffin DW, Lipp EK (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. doi:10.1128/AEM.71.4.2070-2078.2005

    Article  CAS  Google Scholar 

  47. Wong K, Fong T-T, Bibby K, Molina M (2012) Application of enteric viruses for fecal pollution source tracking in environmental waters. Environ Int 45:151–164. doi:10.1016/j.envint.2012.02.009

    Article  CAS  Google Scholar 

  48. Rosario K, Symonds EM, Sinigalliano C, Stewart J, Breitbart M (2009) Pepper mild mottle virus as an indicator of fecal pollution. Appl Environ Microbiol 75:7261–7267. doi:10.1128/AEM.00410-09

    Article  CAS  Google Scholar 

  49. Maluquer de Motes C, Clemente-Casares P, Hundesa A, Martín M, Girones R (2004) Detection of bovine and porcine adenoviruses for tracing the source of fecal contamination. Appl Environ Microbiol 70:1448–1454. doi:10.1128/AEM.70.3.1448

    Article  CAS  Google Scholar 

  50. Wong K, Xagoraraki I (2011) A perspective on the prevalence of DNA enteric virus genomes in anaerobic-digested biological wastes. Environ Monit Assess. doi:10.1007/s10661-011-2316-z

    Google Scholar 

  51. Hundesa A, Maluquer de Motes C, Bofill-Mas S, Albinana-Gimenez N, 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. doi:10.1128/AEM.01090-06

    Article  CAS  Google Scholar 

  52. Hundesa A, Bofill-Mas S, Maluquer de Motes C, Rodriguez-Manzano J, Bach A, Casas M, Girones R (2010) Development of a quantitative PCR assay for the quantitation of bovine polyomavirus as a microbial source-tracking tool. J Virol Methods 163:385–389. doi:10.1016/j.jviromet.2009.10.029

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  54. Jiménez-Clavero MA, Escribano-Romero E, Mansilla C, Gómez N, Córdoba L, Roblas N, Ponz F, Ley V, Sáiz 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. doi:10.1128/AEM.71.7.3536-3543.2005

    Article  CAS  Google Scholar 

  55. Hundesa A, Maluquer de Motes C, Albinana-Gimenez N, Rodriguez-Manzano J, Bofill-Mas S, Suñen E, 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. doi:10.1016/j.jviromet.2009.02.006

    Article  CAS  Google Scholar 

  56. Viancelli A, Garcia LAT, Kunz A, Steinmetz R, Esteves PA, Barardi CRM (2012) Research in Veterinary Science Detection of circoviruses and porcine adenoviruses in water samples collected from swine manure treatment systems. Res Vet Sci 93:538–543. doi:10.1016/j.rvsc.2011.07.022

    Article  CAS  Google Scholar 

  57. Jiménez-Clavero MA, Fernández C, Ortiz JA, Pro J, Carbonell G, Tarazona JV, Roblas N, Ley V (2003) Teschoviruses as indicators of porcine fecal contamination of surface water. Appl Environ Microbiol 69:6311–6315. doi:10.1128/AEM.69.10.6311

    Article  CAS  Google Scholar 

  58. Rusiñol M, Carratalà A, Hundesa A, Bach A, Kern A, Vantarakis A, Girones R, Bofill-Mas S (2013) Description of a novel viral tool to identify and quantify ovine faecal pollution in the environment. Sci Total Environ 458–460:355–360. doi:10.1016/j.scitotenv.2013.04.028

    Article  CAS  Google Scholar 

  59. Carratalà A, Rusiñol M, Hundesa A, Biarnes M, Rodriguez-Manzano J, Vantarakis A, Kern A, Sunen E, Girones R, Bofill-Mas S (2012) A novel tool for specific detection and quantification of chicken/Turkey parvoviruses to trace poultry fecal contamination in the environment. Appl Environ Microbiol 78:7496–7499. doi:10.1128/AEM.01283-12

    Article  CAS  Google Scholar 

  60. Cantalupo PG, Calgua B, Zhao G, Hundesa A, Wier AD, Katz JP, Grabe M, Hendrix RW, Girones R, Wang D, Pipas JM (2011) Raw sewage harbors diverse viral populations. mBio 2:e00180–11–e00180–11. doi:10.1128/mBio.00180-11.Editor

  61. Bofill-Mas S, Formiga-cruz M, Clemente-casares P, Calafell F, Girones R (2001) Potential Transmission of human polyomaviruses through the gastrointestinal tract after exposure to virions or viral DNA. J Virol 75:10290–10299. doi:10.1128/JVI.75.21.10290

  62. Calgua B, Carratalà A, Guerrero-Latorre L, de Abreu CA, Kohn T, Sommer R, Girones R (2014) UVC inactivation of dsDNA and ssRNA viruses in water: UV fluences and a qPCR-based approach to evaluate decay on viral infectivity. Food Environ Virol. doi:10.1007/s12560-014-9157-1

    Google Scholar 

  63. Wyn-jones AP, Carducci A, Cook N, D’Agostino M, Divizia M, Fleischer J, Gantzer C, Gawler A, Girones R, Höller C, de Roda Husman AM, Kay D, Kozyra I, López-Pila J, Muscillo M, Nascimento MSJ, Papageorgiou G, Rutjes S, Sellwood J, Szewzyk R, Wyer M, Agostino MD, Ho C, Maria A, Husman DR, Sa M, Lo J (2011) Surveillance of adenoviruses and noroviruses in European recreational waters. Water Res 5:1025–1038. doi:10.1016/j.watres.2010.10.015

    Article  CAS  Google Scholar 

  64. Jones MS, Harrach B, Ganac RD, Gozum MMA, Dela Cruz WP, Riedel B, Pan C, Delwart EL, Schnurr DP (2007) New adenovirus species found in a patient presenting with gastroenteritis. J Virol 81:5978–5984. doi:10.1128/JVI.02650-06

    Article  CAS  Google Scholar 

  65. Robinson CM, Singh G, Henquell C, Walsh MP, Peigue-Lafeuille H, Seto D, Jones MS, Dyer DW, Chodosh J (2011) Computational analysis and identification of an emergent human adenovirus pathogen implicated in a respiratory fatality. Virology 409:141–147. doi:10.1016/j.virol.2010.10.020

    Article  CAS  Google Scholar 

  66. Walsh MP, Seto J, Liu EB, Dehghan S, Hudson NR, Lukashev AN, Ivanova O, Chodosh J, Dyer DW, Jones MS, Seto D (2011) Computational analysis of two species C human adenoviruses provides evidence of a novel virus. J Clin Microbiol 49:3482–3490. doi:10.1128/JCM.00156-11

    Article  CAS  Google Scholar 

  67. Buller CR, Moxley RA (1988) Natural infection of porcine ileal dome M cells with rotavirus and enteric adenovirus. Vet Pathol 25:516–517

    Article  CAS  Google Scholar 

  68. Adrian T, Schäfer G, Cooney MK, Fox JP, Wigand R (1988) Persistent enteral infections with adenovirus types 1 and 2 in infants: no evidence of reinfection. Epidemiol Infect 101:503–509

    Article  CAS  Google Scholar 

  69. Sharp IR, Wadell G (1995) Adenoviruses. In: Zuckerman AJ, Banatvala JE, Pattison JR (eds) Principles and practice of clinical virology, 3rd edn. Wiley, New York, pp 287–308

    Google Scholar 

  70. Formiga-Cruz M, Tofiño-Quesada G, Bofill-Mas S, Lees DN, Henshilwood K, Allard a K, Conden-Hansson A-C, Hernroth BE, Vantarakis A, Tsibouxi A, Papapetropoulou M, Furones MD, Girones R (2002) Distribution of human virus contamination in shellfish from different growing areas in Greece, Spain, Sweden, and the United Kingdom. Appl Environ Microbiol 68:5990–5998. doi:10.1128/AEM.68.12.5990

  71. Bofill-Mas S, Rodriguez-Manzano J, Calgua B, Carratala A, Girones R (2010) Newly described human polyomaviruses Merkel cell, KI and WU are present in urban sewage and may represent potential environmental contaminants. Virol J 7:141. doi:10.1186/1743-422X-7-141

    Article  CAS  Google Scholar 

  72. Rusiñol M, Fernandez-Cassi X, Hundesa A, Vieira C, Kern A, Eriksson I, Ziros P, Kay D, Miagostovich M, Vargha M, Allard A, Vantarakis A, Wyn-Jones P, Bofill-Mas S, Girones R (2014) Application of human and animal viral microbial source tracking tools in fresh and marine waters from five different geographical areas. Water Res 59:119–129. doi:10.1016/j.watres.2014.04.013

    Article  CAS  Google Scholar 

  73. Rodriguez-Manzano J, Hundesa A, Calgua B, Carratala A, Maluquer de Motes C, Rusiñol M, Moresco V, Ramos AP, Martínez-Marca F, Calvo M, Monte Barardi CR, Girones R, Bofill-Mas S (2013) Adenovirus and norovirus contaminants in commercially distributed shellfish. Food Environ Virol. doi:10.1007/s12560-013-9133-1

    Google Scholar 

  74. Sauerbrei A, Wutzler P (2009) Testing thermal resistance of viruses. Arch Virol 154:115–119. doi:10.1007/s00705-008-0264-x

    Article  CAS  Google Scholar 

  75. Brodsky I, Rowe W, Hartley J, Lane W (1959) Studies of mouse polyoma virus infection II Virus stability. J Exp Med 109:439–447

    Article  CAS  Google Scholar 

  76. Page MA, Shisler JL, Mariñas BJ (2010) Mechanistic aspects of adenovirus serotype 2 inactivation with free chlorine. Appl Environ Microbiol 76:2946–2954. doi:10.1128/AEM.02267-09

    Article  CAS  Google Scholar 

  77. deAbreu CA, Carratalà A, Calvo M, Barardi CRM, Bofill-Mas S, Girones R, de Abreu CA (2012) Comparative inactivation of murine norovirus, human adenovirus, and human JC polyomavirus by chlorine in seawater. Appl Environ Microbiol 78:6450–6457. doi:10.1128/AEM.01059-12

    Article  CAS  Google Scholar 

  78. Girones R, Carratalà A, Calgua B, Calvo M, Rodriguez-Manzano J, Emerson S (2014) Chlorine inactivation of hepatitis E virus and human adenovirus 2 in water. J Water Health 12:436–442. doi:10.2166/wh.2014.027

    Article  Google Scholar 

  79. Gardner SD, Field AM, Coleman DV, Hulme B (1971) New human papovavirus (B.K.) isolated from urine after renal transplantation. Lancet 1:1253–1257

    Article  CAS  Google Scholar 

  80. Padgett BL, Walker DL, ZuRhein GM, Eckroade RJ, Dessel BH (1971) Cultivation of papova-like virus from human brain with progressive multifocal leucoencephalopathy. Lancet 1:1257–1260

    Article  CAS  Google Scholar 

  81. Berger JR, Houff SA, Major EO (2009) Monoclonal antibodies and progressive multifocal leukoencephalopathy. MAbs 1:583–589

    Article  Google Scholar 

  82. Yousry TA, Major EO, Ryschkewitsch C, Fahle G, Fischer S, Hou J, Curfman B, Miszkiel K, Mueller-Lenke N, Sanchez E, Barkhof F, Radue E-W, Jäger HR, Clifford DB (2006) Evaluation of patients treated with natalizumab for progressive multifocal leukoencephalopathy. N Engl J Med 354:924–933. doi:10.1056/NEJMoa054693

    Article  CAS  Google Scholar 

  83. Kitamura T, Aso Y, Kuniyoshi N, Hara K, Yogo Y (1990) High incidence of urinary JC virus excretion in nonimmunosuppressed older patients. J Infect Dis 161:1128–1133

    Article  CAS  Google Scholar 

  84. Koralnik IJ, Boden D, Mai VX, Lord CI, Letvin NL (1999) JC virus DNA load in patients with and without progressive multifocal leukoencephalopathy. Neurology 52:253–260

    Article  CAS  Google Scholar 

  85. Weber T (1997) Molecular epidemiology and emerging infectious diseases of the nervous system. J Neurovirol 3(Suppl 1):S46–S49

    Google Scholar 

  86. Albinana-Gimenez N, Clemente-casares P (2006) Distribution of human polyoma-viruses, adenoviruses, and hepatitis E virus in the environment and in a drinking-water treatment plant. Environ Sci Technol 40:7416–7422

    Article  CAS  Google Scholar 

  87. Norja P, Hedman L, Kantola K, Kemppainen K, Suvilehto J, Pitkäranta A, Aaltonen L-M, Seppänen M, Hedman K, Söderlund-Venermo M (2012) Occurrence of human bocaviruses and parvovirus 4 in solid tissues. J Med Virol 84:1267–1273. doi:10.1002/jmv.23335

    Article  Google Scholar 

  88. Väisänen E, Kuisma I, Phan TG, Delwart E, Lappalainen M, Tarkka E, Hedman K, Söderlund-Venermo M (2014) Bufavirus in feces of patients with gastroenteritis, Finland. Emerg Infect Dis 20:1077–1080. doi:10.3201/eid2006.131674

    Article  Google Scholar 

  89. Nath Srivastava R, Lund E (1980) The stability of bovine parvovirus and its possible use as an indicator for the persistence of enteric viruses. Water Res 14:1017–1021. doi:10.1016/0043-1354(80)90146-3

  90. Baylis SA, Tuke PW, Miyagawa E, Blümel J (2013) Studies on the inactivation of human parvovirus 4. Transfusion 53:2585–2592. doi:10.1111/trf.12372

    Article  CAS  Google Scholar 

  91. Zhang W, Li L, Deng X, Kapusinszky B, Delwart E (2014) What is for dinner? Viral metagenomics of US store bought beef, pork, and chicken. Virology 468–470:303–310. doi:10.1016/j.virol.2014.08.025

    Article  CAS  Google Scholar 

  92. Blinkova O, Rosario K, Li L, Kapoor A, Slikas B, Bernardin F, Breitbart M, Delwart E (2009) Frequent detection of highly diverse variants of cardiovirus, cosavirus, bocavirus, and circovirus in sewage samples collected in the United States. J Clin Microbiol 47:3507–3513. doi:10.1128/JCM.01062-09

    Article  CAS  Google Scholar 

  93. Bofill-Mas S, Rusiñol M, Fernandez-Cassi X, Carratalà A, Hundesa A, Girones R (2013) Quantification of human and animal viruses to differentiate the origin of the fecal contamination present in environmental samples. BioMed Res Int 2013:192089. doi:10.1155/2013/192089

    Article  CAS  Google Scholar 

  94. Choi S, Jiang SC (2005) Real-time PCR quantification of human adenoviruses in urban rivers indicates genome prevalence but low infectivity. Appl Environ Microbiol 71:7426–7433. doi:10.1128/AEM.71.11.7426

    Article  CAS  Google Scholar 

  95. He J-W, Jiang S (2005) Quantification of enterococci and human adenoviruses in environmental samples by real-time PCR. Appl Environ Microbiol 71:2250–2255. doi:10.1128/AEM.71.5.2250

    Article  CAS  Google Scholar 

  96. Haramoto E, Katayama H, Oguma K, Ohgaki S (2005) 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 71:2403–2411. doi:10.1128/AEM.71.5.2403

    Article  CAS  Google Scholar 

  97. Dong Y, Kim J, Lewis GD (2010) Evaluation of methodology for detection of human adenoviruses in wastewater, drinking water, stream water and recreational waters. J Appl Microbiol 108:800–809. doi:10.1111/j.1365-2672.2009.04477.x

    Article  CAS  Google Scholar 

  98. Heim A, Ebnet C, Harste G, Pring-Akerblom P (2003) Rapid and quantitative detection of human adenovirus DNA by real-time PCR. J Med Virol 70:228–239. doi:10.1002/jmv.10382

    Article  CAS  Google Scholar 

  99. Hamza IA, Jurzik L, Stang A, Sure K, Uberla K, 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. doi:10.1016/j.watres.2009.03.020

    Article  CAS  Google Scholar 

  100. Ogorzaly L, Tissier A, Bertrand I, Maul A, Gantzer C (2009) Relationship between F-specific RNA phage genogroups, faecal pollution indicators and human adenoviruses in river water. Water Res 43:1257–1264. doi:10.1016/j.watres.2008.12.011

    Article  CAS  Google Scholar 

  101. Bofill-Mas S, Hundesa A, Calgua B, Rusiñol M, Maluquer de Motes C, Girones R (2011) Cost-effective method for microbial source tracking using specific human and animal viruses. J Vis Exp 58:2820. doi:10.3791/2820

    Google Scholar 

  102. Haramoto E, Kitajima M, Katayama H, Ohgaki S (2010) Real-time PCR detection of adenoviruses, polyomaviruses, and torque teno viruses in river water in Japan. Water Res 44:1747–1752. doi:10.1016/j.watres.2009.11.043

    Article  CAS  Google Scholar 

  103. Jurzik L, Hamza IA, Puchert W, Uberla K, Wilhelm M (2010) Chemical and microbiological parameters as possible indicators for human enteric viruses in surface water. Int J Hyg Environ Health 213:210–216. doi:10.1016/j.ijheh.2010.05.005

    Article  CAS  Google Scholar 

  104. Rigotto C, Victoria M, Moresco V, Kolesnikovas CK, Corre AA, Miagostovich MP (2010) Assessment of adenovirus, hepatitis A virus and rotavirus presence in environmental samples in Florianopolis, South. J Appl Microbiol. doi:10.1111/j.1365-2672.2010.04827.x

    Google Scholar 

  105. Schlindwein A, Rigotto C, Cm S, Cr B (2010) Detection of enteric viruses in sewage sludge and treated wastewater effluent. Water Sci Technol 61:2166. doi:10.2166/wst.2010.845.Detection

  106. Calgua B, Barardi C, Bofill-Mas S, Rodriguez-Manzano J, Girones R (2011) Detection and quantitation of infectious human adenoviruses and JC polyomaviruses in water by immunofluorescence assay. J Virol Methods 171:1–7. doi:10.1016/j.jviromet.2010.09.013

    Article  CAS  Google Scholar 

  107. Gibson KE, Opryszko MC, Schissler JT, Guo Y, Schwab KJ (2011) Evaluation of human enteric viruses in surface water and drinking water resources in southern Ghana. Am J Trop Med Hyg 84:20–29. doi:10.4269/ajtmh.2011.10-0389

    Article  CAS  Google Scholar 

  108. Guerrero-Latorre L, Carratala A, Rodriguez-Manzano J, Calgua B, Hundesa A, Girones R (2011) Occurrence of water-borne enteric viruses in two settlements based in Eastern Chad: analysis of hepatitis E virus, hepatitis A virus and human adenovirus in water sources. J Water Health 9:515. doi:10.2166/wh.2011.126.Occurrence

    Article  Google Scholar 

  109. Hamza IA, Jurzik L, Überla K, Wilhelm M (2011) Methods to detect infectious human enteric viruses in environmental water samples. Int J Hyg Environ Health 214:424–436. doi:10.1016/j.ijheh.2011.07.014

    Article  Google Scholar 

  110. Kokkinos PA, Ziros PG, Mpalasopoulou A, Galanis A, Vantarakis A (2011) Molecular detection of multiple viral targets in untreated urban sewage from Greece. Virol J 8:195. doi:10.1186/1743-422X-8-195

  111. Barardi CRM, Viancelli A, Rigotto C, Pilotto MR, Garcia LA. T, Kunz A, Esteves PA (2012) Surveillance of human and swine adenovirus, human norovirus and swine circovirus in water samples in Santa Catarina, Brazil. J Water Health 10:445–52. doi:10.2166/wh.2012.190

    Google Scholar 

  112. Fongaro G, Nascimento MA, Viancelli A, Tonetta D, Petrucio MM, Barardi CRM (2012) Surveillance of human viral contamination and physicochemical profiles in a surface water lagoon. Water Sci Technol 66:2682–2687. doi:10.2166/wst.2012.504

    Article  CAS  Google Scholar 

  113. Rodriguez-Manzano J, Alonso JL, Ferrús MA, Moreno Y, Amorós I, Calgua B, Hundesa A, Guerrero-Latorre L, Carratala A, Rusiñol M, Girones R (2012) Standard and new faecal indicators and pathogens in sewage treatment plants, microbiological parameters for improving the control of reclaimed water. Water Sci Technol 66:2517–2523. doi:10.2166/wst.2012.233

    Article  CAS  Google Scholar 

  114. Fumian TM, Vieira CB, Leite JPG, Miagostovich MP (2013) Assessment of burden of virus agents in an urban sewage treatment plant in Rio de Janeiro, Brazil. J Water Health 11:110–119. doi:10.2166/wh.2012.123

    Article  CAS  Google Scholar 

  115. Hewitt J, Greening GE, Leonard M, Lewis GD (2013) Evaluation of human adenovirus and human polyomavirus as indicators of human sewage contamination in the aquatic environment. Water Res 47:6750–6761. doi:10.1016/j.watres.2013.09.001

    Article  CAS  Google Scholar 

  116. Katukiza AY, Temanu H, Chung JW, Foppen JWA, Lens PNL (2013) Genomic copy concentrations of selected waterborne viruses in a slum environment in Kampala, Uganda. J Water Health 11:358–370. doi:10.2166/wh.2013.184

    Article  CAS  Google Scholar 

  117. Sidhu JPS, Ahmed W, Gernjak W, Aryal R, McCarthy D, Palmer A, Kolotelo P, Toze S (2013) Sewage pollution in urban stormwater runoff as evident from the widespread presence of multiple microbial and chemical source tracking markers. Sci Total Environ 463–464:488–496. doi:10.1016/j.scitotenv.2013.06.020

    Article  CAS  Google Scholar 

  118. Sidhu JPS, Ahmed W, Toze S (2013) Sensitive detection of human adenovirus from small volume of primary wastewater samples by quantitative PCR. J Virol Methods 187:395–400. doi:10.1016/j.jviromet.2012.11.002

    Article  CAS  Google Scholar 

  119. Ye XXY, Ming X, Zhang YLY, Xiao WQW, Huang XN, Cao YG, Gu KD (2012) Real-time PCR detection of enteric viruses in source water and treated drinking water in Wuhan, China. Curr Microbiol 65:244–253. doi:10.1007/s00284-012-0152-1

    Article  CAS  Google Scholar 

  120. Lee CS, Lee C, Marion J, Wang Q, Saif L, Lee J (2014) Occurrence of human enteric viruses at freshwater beaches during swimming season and its link to water inflow. Sci Total Environ 472:757–766. doi:10.1016/j.scitotenv.2013.11.088

    Article  CAS  Google Scholar 

  121. McQuaig SM, Scott TM, Lukasik JO, Paul JH, Harwood VJ (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. doi:10.1128/AEM.02302-08

    Article  CAS  Google Scholar 

  122. Biel SS, Held TK, Landt O, Niedrig M, Gelderblom HR, Siegert W, Nitsche A, Koch-institut R (2000) Rapid quantification and differentiation of human polyomavirus DNA in undiluted urine from patients after bone marrow transplantation. J Clin Microbiol 38:3689–3695

    CAS  Google Scholar 

  123. Abdelzaher AM, Wright ME, Ortega C, Solo-Gabriele HM, Miller G, Elmir S, Newman X, Shih P, Bonilla JA, Bonilla TD, Palmer CJ, Scott T, Lukasik J, Harwood VJ, McQuaig S, Sinigalliano C, Gidley M, Plano LRW, Zhu X, Wang JD, Fleming LE (2010) Presence of pathogens and indicator microbes at a non-point source subtropical recreational marine beach. Appl Environ Microbiol 76:724–732. doi:10.1128/AEM.02127-09

    Article  CAS  Google Scholar 

  124. Ahmed W, Wan C, Goonetilleke A, Gardner T (2010) Evaluating sewage-associated JCV and BKV polyomaviruses for sourcing human fecal pollution in a Coastal River in Southeast Queensland, Australia. J Environ Qual 39:1743. doi:10.2134/jeq2010.0062

    Article  CAS  Google Scholar 

  125. Fumian TM, Guimarães FR, Pereira Vaz BJ, da Silva MTT, Muylaert FF, Bofill-Mas S, Gironés R, Leite JPG, Miagostovich MP (2010) Molecular detection, quantification and characterization of human polyomavirus JC from waste water in Rio De Janeiro, Brazil. J Water Health 8:438–445. doi:10.2166/wh.2010.090

    Article  CAS  Google Scholar 

  126. Hellein K, Battie C (2011) Culture-based indicators of fecal contamination and molecular microbial indicators rarely correlate with Campylobacter spp. in recreational waters. J Water Health 9:1–14. doi:10.2166/wh.2011.154

    Article  CAS  Google Scholar 

  127. Chase E, Hunting J, Staley C, Harwood VJ (2012) Microbial source tracking to identify human and ruminant sources of faecal pollution in an ephemeral Florida river. J Appl Microbiol 113:1396–1406. doi:10.1111/jam.12007

    Article  CAS  Google Scholar 

  128. Gordon KV, Mott J, Wang S, Brownell M, Lepo JE, Nathaniel R, Hellein KN, Harwood VJ, Kilgen M, Kennedy E (2012) Relationship of human-associated microbial source tracking markers with enterococci in Gulf of Mexico waters. Water Res 47:996–1004. doi:10.1016/j.watres.2012.10.032

    Article  CAS  Google Scholar 

  129. McQuaig S, Griffith J, Harwood VJ (2012) Association of fecal indicator bacteria with human viruses and microbial source tracking markers at coastal beaches impacted by nonpoint source pollution. Appl Environ Microbiol 78:6423–6432. doi:10.1128/AEM.00024-12

    Article  CAS  Google Scholar 

  130. Staley C, Gordon KV, Schoen ME, Harwood VJ (2012) Methods for microbial source tracking of performance of two quantitative PCR methods for microbial source tracking of human sewage and implications for microbial risk assessment in recreational waters. Appl Environ Microbiol 78:7317–7326. doi:10.1128/AEM.01430-12

    Article  CAS  Google Scholar 

  131. Calgua B, Fumian T, Rusiñol M, Rodriguez-Manzano J, Mbayed V, Bofill-Mas S, Miagostovich M, Girones R (2013) Detection and quantification of classic and emerging viruses by skimmed-milk flocculation and PCR in river water from two geographical areas. Water Res 47:2797–2810. doi:10.1016/j.watres.2013.02.043

    Article  CAS  Google Scholar 

  132. Bofill-Mas S, Hundesa A, Calgua B, Rusiñol M, Maluquer de Motes C, Girones R (2011) Cost-effective method for microbial source tracking using specific human and animal viruses. J Vis Exp 5:5–9. doi:10.3791/2820

    Google Scholar 

  133. Wolf S, Hewitt J, Greening G (2010) Viral multiplex quantitative PCR assays for tracking sources of fecal contamination. Appl Environ Microbiol 76:1388–1394. doi:10.1128/AEM.02249-09

    Article  CAS  Google Scholar 

  134. Wong K, Xagoraraki I (2011) Evaluating the prevalence and genetic diversity of adenovirus and polyomavirus in bovine waste for microbial source tracking. Appl Microbiol Biotechnol 90:1521–1526. doi:10.1007/s00253-011-3156-z

    Article  CAS  Google Scholar 

  135. Viancelli A, Kunz A, Steinmetz RLR, Kich JD, Souza CK, Canal CW, Coldebella A, Esteves PA, Barardi CRM (2013) Chemosphere performance of two swine manure treatment systems on chemical composition and on the reduction of pathogens. Chemosphere 90:1539–1544. doi:10.1016/j.chemosphere.2012.08.055

    Article  CAS  Google Scholar 

  136. Corsi SR, Borchardt MA, Spencer SK, Hughes PE, Baldwin AK (2014) Human and bovine viruses in the Milwaukee River watershed: hydrologically relevant representation and relations with environmental variables. Sci Total Environ 490:849–860. doi:10.1016/j.scitotenv.2014.05.072

    Article  CAS  Google Scholar 

  137. Directive 2000/60/EC of the European Parliament and of the Council establishing a framework for the Community action in the field of water policy. EU Water Framework Directive

    Google Scholar 

  138. European Commission DG XI (1997) The implementation of council directive 91/676/EEC concerning the protection of waters against pollution caused by nitrates from agricultural sources. Report COM (97)473

    Google Scholar 

  139. Skeffington R (2002) European nitrogen policies, nitrate in rivers and the use of the INCA model. Hydrol Earth Syst Sci 6:315–324

    Article  Google Scholar 

  140. Pinheiro LB, Coleman VA, Hindson CM, Herrmann J, Hindson BJ, Bhat S, Emslie KR (2012) Evaluation of a droplet digital polymerase chain reaction format for DNA copy number quantification. Anal Chem 84:1003–1011

    Google Scholar 

  141. Gilbride KA, Lee D-Y, Beaudette LA (2006) Molecular techniques in wastewater: understanding microbial communities, detecting pathogens, and real-time process control. J Microbiol Methods 66:1–20. doi:10.1016/j.mimet.2006.02.016

    Google Scholar 

  142. Ivnitski D, O’Neil DJ, Gattuso A, Schlicht R, Calidonna M, Fisher R (2003) Nucleic acid approaches for detection and identification of biological warfare and infectious disease agents. BioTechniques 35:862–869

    CAS  Google Scholar 

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Authors and Affiliations

  1. Laboratory of Virus Contaminants of Water and Food (Vircont), Department of Microbiology, Biology Faculty, Barcelona University, Barcelona, Spain

    Sílvia Bofill-Mas, Marta Rusiñol & Rosina Girones

  2. Catalan Water Agency, c/Provença, 204-208, 08036, Barcelona, Spain

    Josep Fraile, Teresa Garrido & Antoni Munné

Authors
  1. Sílvia Bofill-Mas
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  2. Marta Rusiñol
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  3. Josep Fraile
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  4. Teresa Garrido
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  5. Antoni Munné
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  6. Rosina Girones
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Correspondence to Sílvia Bofill-Mas .

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  1. Department of Water Quality and Monitori, Catalan Water Agency (ACA), Barcelona, Spain

    Antoni Munné

  2. Department of Environmental Chemistry, IDAEA-CSIC, Barcelona, Spain

    Antoni Ginebreda

  3. Department of Ecology, University of Barcelona (UB), Barcelona, Spain

    Narcís Prat

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Bofill-Mas, S., Rusiñol, M., Fraile, J., Garrido, T., Munné, A., Girones, R. (2015). Specific Viruses Present in Polluted Groundwater Are Indicative of the Source of Nitrates and Faecal Contamination in Agricultural Areas. In: Munné, A., Ginebreda, A., Prat, N. (eds) Experiences from Ground, Coastal and Transitional Water Quality Monitoring. The Handbook of Environmental Chemistry, vol 43. Springer, Cham. https://doi.org/10.1007/698_2015_426

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