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Environmental and Adaptive Changes Necessitate a Paradigm Shift for Indicators of Fecal Contamination

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  • Authors: Pedro Teixeira1,2,3, Daniel Salvador4,5, João Brandão6,7, Warish Ahmed8, Michael J. Sadowsky9, Elisabete Valério10
  • Editor: Michael Sadowsky11
    Affiliations: 1: Câmara Municipal de Lisboa, Direcção Municipal do Ambiente, Estrutura Verde, Clima e Energia, Laboratório de Bromatologia e Águas, Lisbon, Portugal; 2: Centro de Estudos do Ambiente e do Mar (CESAM), Faculdade de Ciências da Universidade de Lisboa, Lisbon, Portugal; 3: Departamento de Saúde Ambiental, Instituto Nacional de Saúde Doutor Ricardo Jorge, Lisbon, Portugal; 4: Centro de Estudos do Ambiente e do Mar (CESAM), Faculdade de Ciências da Universidade de Lisboa, Lisbon, Portugal; 5: Instituto de Saúde Ambiental (ISAMB), Faculdade de Medicina da Universidade de Lisboa, Lisbon, Portugal; 6: Centro de Estudos do Ambiente e do Mar (CESAM), Faculdade de Ciências da Universidade de Lisboa, Lisbon, Portugal; 7: Departamento de Saúde Ambiental, Instituto Nacional de Saúde Doutor Ricardo Jorge, Lisbon, Portugal; 8: CSIRO Land and Water, Ecosciences Precinct, Dutton Park, Australia; 9: BioTechnology Institute and Departments of Soil, Water, & Climate and Plant and Microbial Biology, University of Minnesota, St. Paul, Minnesota, USA; 10: Departamento de Saúde Ambiental, Instituto Nacional de Saúde Doutor Ricardo Jorge, Lisbon, Portugal; 11: BioTechnology Institute, University of Minnesota, St. Paul, MN
  • Source: microbiolspec March 2020 vol. 8 no. 2 doi:10.1128/microbiolspec.ERV-0001-2019
  • Received 12 June 2019 Accepted 12 December 2019 Published 27 March 2020
  • Elisabete Valério, [email protected]
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  • Abstract:

    Changes in the occurrence, distribution, and seasonal variation of waterborne pathogens due to global climate change may increase the risk of human exposure to these microorganisms, thus heightening the need for more reliable surveillance systems. Routine monitoring of drinking water supplies and recreational waters is performed using fecal indicator microorganisms, such as , spp., and coliphages. However, the presence and numbers of these indicators, especially and spp., do not correlate well with those of other pathogens, especially enteric viruses, which are a major cause of waterborne outbreaks associated with contaminated water and food, and recreational use of lakes, ponds, rivers, and estuarine waters. For that reason, there is a growing need for a surveillance system that can detect and quantify viral pathogens directly in water sources to reduce transmission of pathogens associated with fecal transmission. In this review, we present an updated overview of relevant waterborne enteric viruses that we believe should be more commonly screened to better evaluate water quality and to determine the safety of water use and reuse and of epidemiological data on viral outbreaks. We also discuss current methodologies that are available to detect and quantify these viruses in water resources. Finally, we highlight challenges associated with virus monitoring. The information presented in this review is intended to aid in the assessment of human health risks due to contact with water sources, especially since current environmental and adaptive changes may be creating the need for a paradigm shift for indicators of fecal contamination.

  • Citation: Teixeira P, Salvador D, Brandão J, Ahmed W, Sadowsky M, Valério E. 2020. Environmental and Adaptive Changes Necessitate a Paradigm Shift for Indicators of Fecal Contamination. Microbiol Spectrum 8(2):ERV-0001-2019. doi:10.1128/microbiolspec.ERV-0001-2019.


1. Coumou D, Rahmstorf S. 2012. A decade of weather extremes. Nat Clim Change 2:491–496.
2. Wikipedia contributors. Accessed 7 February 2020. 2010 Madeira floods and mudslides. https://en.wikipedia.org/wiki/2010_Madeira_floods_and_mudslides.
3. Romão D, Abreu R, Calado G, Freitas F, Rodrigues P, Ferreira C, Campos A, Temtem Rita, Freitas C, Andrade C, Prada S, Figueira C, Brandão J. 2017. Madeira 2010: aftermath of flashfloods and mudslides on bathing water quality indicators and on sand microbial levels. Pan-European Symposium Water and Sanitation Safety Planning and Extreme Weather Events, Bilthoven, Nederlands.
4. Kauppinen A, Pitkänen T, Al-Hello H, Maunula L, Rimhanen-Finne R, Miettinen I. 2018. Two drinking water outbreaks caused by sapovirus in Finland. 6th Food and Environmental Virology Conference, Tempe, AZ.
5. Roca MA, Brown, RS, Solo-Gabriele HM. 2019. Fecal indicator bacteria levels at beaches in the Florida Keys after Hurricane Irma. Marine Pollut Bull 138:266–273.
6. Tang Y, Wu S, Miao X, Pollard SJT, Hrudey SE. 2013. Resilience to evolving drinking water contamination risks: a human error prevention perspective. J Cleaner Prod 57:228–237.
7. Fujioka RS, Solo-Gabriele HM, Byappanahalli MN, Kirs M. 2015. US recreational water quality criteria: a vision for the future. Int J Environ Res Public Health 12:7752–7776. [PubMed]
8. USEPA. 2007. Report of the Experts Scientific Workshop on Critical Research Needs for the Development of New or Revised Recreational Water Quality Criteria. EPA 823-R-07–006, United States Environmental Protection Agency, Washington, DC.
9. Byappanahalli MN, Nevers MB, Korajkic A, Staley ZR, Harwood VJ. 2012. Enterococci in the environment. Microbiol Mol Biol Rev 76:685–706. [PubMed]
10. Ishii S, Sadowsky M. 2008. Escherichia coli in the environment: implications for water quality and human health. Microbes Environ 23:101–108. [PubMed]
11. Wright ME, Solo-Gabriele HM, Elmir S, Fleming LE. 2009. Microbial load from animal feces at a recreational beach. Marine Pollut Bull 58:1649–1656. [PubMed]
12. Wade TJ, Calderon RL, Sams E, Beach M, Brenner KP, Williams AH, Dufour AP. 2006. Rapidly measured indicators of recreational water quality are predictive of swimming-associated gastrointestinal illness. Environ Health Perspect 114:24–28. [PubMed]
13. 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. [PubMed]
14. Hughes B, Beale DJ, Dennis PG, Cook S, Ahmed W. 2017. Cross-comparison of human wastewater-associated molecular markers in relation to fecal indicator bacteria and enteric viruses in recreational beach waters. Appl Environ Microbiol. 83:e00028-17. [PubMed]
15. Rusiñol M, Fernandez-Cassi X, Hundesa A, Vieira C, Kern A, Eriksson, 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. [PubMed]
16. Symonds E, Sinigalliano C, Gidley M, Ahmed W, McQuaig SM, Breitbart M. 2016. Fecal pollution along the southeastern coast of Florida and insight into the use of pepper mild mottle virus as an indicator. J Appl Microbiol 121:1469–1481. [PubMed]
17. Stachler E, Kelty C, Sivaganesan M, Li X, Bibby K, Shanks OC. 2017 Quantitative CrAssphage PCR assays for human fecal pollution measurement. Environ Sci Technol 51:9146–9154. [PubMed]
18. Ahmed W, Goonetilleke A, Gardner T. 2010. Human and bovine adenoviruses for the detection of source-specific fecal pollution in coastal waters in Australia. Water Res 44:4662–4673. [PubMed]
19. Wolf S, Hewitt J, Greening GE. 2010. Viral multiplex quantitative PCR assays for tracking sources of fecal contamination. Appl Environ Microbiol 76:1388–1394. [PubMed]
20. 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. [PubMed]
21. Cai L, Zhang T. 2013. Detecting human bacterial pathogens in wastewater treatment plants by a high-throughput shotgun sequencing technique. Environ Sci Technol 47:5433–5441. [PubMed]
22. Ahmed W, O’Dea C, Masters N, Kuballa A, Marinoni O, Katouli M. 2019. Marker genes of fecal indicator bacteria and potential pathogens in animal feces in subtropical catchments. Sci Total Environ 656:1427–1435. [PubMed]
23. Jebri S, Muniesa M, Jofre J. 2017. General and host-associated bacteriophage indicators of fecal pollution. In Rose JB, Jiménez-Cisneros B (eds), Global Water Pathogen Project. http://www.waterpathogens.org. Part 2 Indicators and Microbial Source Tracking Markers. http://www.waterpathogens.org/book/coliphage. Michigan State University, E. Lansing, MI, UNESCO. https://doi.org/10.14321/waterpathogens.7.
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 9:265–278. [PubMed]
25. Hoff JC, Akin EW. 1986. Microbial resistance to disinfectants: mechanisms and significance. Environ Health Pers 69:7–13. [PubMed]
26. Bonadonna L, La Rosa G. 2019. A review and update on waterborne viral diseases associated with swimming pools. Int J Environ Res Public Health 16:166. [PubMed]
27. McDonnell G, Russell AD. 1999. Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev 12:147–179. [PubMed]
28. Cromeans TL, Kahler AM, Hill VR. 2010. Inactivation of adenoviruses, enteroviruses, and murine norovirus in water by free chlorine and monochloramine. Appl Environ Microbiol 76:1028–1033. [PubMed]
29. Tree JA, Adams MR, Lees DN. 2003. Chlorination of indicator bacteria and viruses in primary sewage effluent. Appl Environ Microbiol 69:2038–2043. [PubMed]
30. Funari E, Kistemann T, Herbst S, Rechenburg A. 2011. Technical Guidance on Water-Related Disease Surveillance. World Health Organization Europe, Copenhagen, Denmark.
31. Stanwell-Smith R. 2003. Classification of water-related disease, p 1–24. In Water and Health. Encyclopedia of Life Support Systems (EOLSS). UNESCO – Encyclopedia Life Support Systems (UNESCO-EOLSS), Paris, France.
32. Hutton G. 2012. Global Costs and Benefits of Drinking-Water Supply and Sanitation Interventions to Reach the MDG Target and Universal Coverage. World Health Organization, Geneva, Switzerland.
33. UNICEF, WHO. 2017. Progress on Drinking Water, Sanitation and Hygiene: 2017 Update and SDG Baselines. World Health Organization (WHO)/United Nations Children’s Fund (UNICEF), Geneva, Switzerland.
34. Dorfman M, Stoner N, Merkel M. 2004. Swimming in sewage. Natural Resources Defense Council and the Environmental Integrity. http://environmentalintegrity.org/pdf/publications/Swimming_in_Sewage_REPORT.pdf.
35. Ramírez-Castillo FY, Loera-Muro A, Jacques M, Garneau P, Avelar-González FJ, Harel J, Guerrero-Barrera AL. 2015. Waterborne pathogens: detection methods and challenges. Pathogens 4:307–334. [PubMed]
36. Campos CJ, Avant J, Lowther J, Till D, Lees DN. 2016. Human norovirus in untreated sewage and effluents from primary, secondary and tertiary treatment processes. Water Res 103:224–232. [PubMed]
37. Guerrero-Latorre L, Gonzales-Gustavson E, Hundesa A, Sommer R, Rosina G. 2016. UV disinfection and flocculation-chlorination sachets to reduce hepatitis E virus in drinking water. Int J Hygiene Environ Health 219:405–411. [PubMed]
38. Kokkinos P, Mandilara G, Nikolaidou A, Velegraki A, Theodoratos P, Kampa D, Blougoura A, Christopoulou A, Smeti E, Kamizoulis G, Vantarakis A, Mavridou A. 2015. Performance of three small-scale wastewater treatment plants. A challenge for possible reuse. Environ Sci Pollut Res Int 22:17744–17752. [PubMed]
39. Chigor VN, Okoh AI. 2012. Quantitative RT-PCR detection of hepatitis A virus, rotaviruses and enteroviruses in the Buffalo River and source water dams in the Eastern Cape Province of South Africa. Int J Environ Res Public Health 9:4017–4032. [PubMed]
40. WHO. 2017. Guidelines for Drinking-Water Quality, 4th ed, incorporating the 1st addendum, p 1–541. Geneva, Switzerland.
41. Macy JT, Quick RE. 2009. Transmission and prevention of water-related diseases, p 104–107. In Grabow W (ed), Water and Health, vol I. EOLSS Publications. UNESCO – Encyclopedia Life Support Systems (UNESCO-EOLSS), Paris, France.
42. Buckwalter SP, Teo R, Espy MJ, Sloan LM, Smith TF, Pritt BS. 2012. Real-time qualitative PCR for 57 human adenovirus types from multiple specimen sources. J Clin Microbiol 50:766–771. [PubMed]
43. Mangel WF, San Martín C. 2014. Structure, function and dynamics in adenovirus maturation. Viruses 6:4536–4570. [PubMed]
44. Russell WC. 2009. Adenoviruses: update on structure and function. J Gen Virol 90:1–20. [PubMed]
45. Elhag WI, Saeed HA, Omer el FE, Ali AS. 2013. Prevalence of rotavirus and adenovirus associated with diarrhea among displaced communities in Khartoum, Sudan. BMC Infect Dis 13:209. [PubMed]
46. Gray GC, McCarthy T, Lebeck MG, Schnurr DP, Russell KL, Kajon AE, Landry ML, Leland DS, Storch GA, Ginocchio CC, Robinson CC, Demmler GJ, Saubolle MA, Kehl SC, Selvarangan R, Miller MB, Chappell JD, Zerr DM, Kiska DL, Halstead DC, Capuano AW, Setterquist SF, Chorazy ML, Dawson JD, Erdman DD. 2007. Genotype prevalence and risk factors for severe clinical adenovirus infection, United States 2004-2006. Clin Infect Dis 45:1120–1131. [PubMed]
47. Zlateva KT, Maes P, Rahman M, Van Ranst M. 2005. Chromatography paper strip sampling of enteric adenoviruses type 40 and 41 positive stool specimens. Virol J 2:6. [PubMed]
48. Crabtree KD, Gerba CP, Rose JB, Haas CN. 1997. Waterborne adenovirus: a risk assessment. Water Sci Technol 35:1–6.
49. Cruz JR, Cáceres P, Cano F, Flores J, Bartlett A, Torún B. 1990. Adenovirus types 40 and 41 and rotaviruses associated with diarrhea in children from Guatemala. J Clin Microbiol 28:1780–1784. [PubMed]
50. Hendrix RM, Lindner JL, Benton FR, Monteith SC, Tuchscherer MA, Gray GC, Gaydos JC. 1999. Large, persistent epidemic of adenovirus type 4-associated acute respiratory disease in U.S. army trainees. Emerg Infect Dis 5:798–801. [PubMed]
51. Kapikian AZ, Wyatt RG. 1992. Viral gastrointestinal infections, p 667–676. In Feigin RD, Cherry JF (ed), Textbook of Pediatric Infectious Diseases, vol. 1, 3rd ed. Elsevier, Ontario, Canada.
52. Jiang S, Noble R, Chu W. 2001. Human adenoviruses and coliphages in urban runoff-impacted coastal waters of southern California. Appl Environ Microbiol 67:179–184. [PubMed]
53. Couch RB, Cate TR, Douglas RG, Jr, Gerone PJ, Knight V. 1966. Effect of route of inoculation on experimental respiratory viral disease in volunteers and evidence for airborne transmission. Bacteriol Rev 30:517–529. [PubMed]
54. Aw TG, Gin KY. 2010. Environmental surveillance and molecular characterization of human enteric viruses in tropical urban wastewaters. J Appl Microbiol 109:716–730. [PubMed]
55. Iaconelli M, Muscillo M, Della Libera S, Fratini M, Meucci L, De Ceglia M, Giacosa D, La Rosa G. 2017. One-year surveillance of human enteric viruses in raw and treated wastewaters, downstream river waters, and drinking waters. Food Environ Virol 9:79–88. [PubMed]
56. Adefisoye MA, Nwodo UU, Green E, Okoh AI. 2016. Quantitative PCR detection and characterisation of human adenovirus, rotavirus and hepatitis A virus in discharged effluents of two wastewater treatment facilities in the Eastern Cape, South Africa. Food Environ Virol 8:262–274. [PubMed]
57. Carducci A, Verani M. 2013. Effects of bacterial, chemical, physical and meteorological variables on virus removal by a wastewater treatment plant. Food Environ Virol 5:69–76. [PubMed]
58. Katayama H, Haramoto E, Oguma K, Yamashita H, Tajima A, Nakajima H, 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]
59. Thurston-Enriquez JA, Haas CN, Jacangelo J, Gerba CP. 2003. Chlorine inactivation of adenovirus type 40 and feline calicivirus. Appl Environ Microbiol 69:3979–3985. [PubMed]
60. Fong TT, Lipp EK. 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]
61. Lu QB, Tong YG, Wo Y, Wang HY, Liu EM, Gray GC, Liu W, Cao WC. 2014. Epidemiology of human adenovirus and molecular characterization of human adenovirus 55 in China, 2009-2012. Influenza Other Respir Viruses 8:302–308. [PubMed]
62. Sinclair RG, Jones EL, Gerba CP. 2009. Viruses in recreational water-borne disease outbreaks: a review. J Appl Microbiol 107:1769–1780. [PubMed]
63. 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. [PubMed]
64. McBride GB, Stott R, Miller W, Bambic D, Wuertz S. 2013. Discharge-based QMRA for estimation of public health risks from exposure to stormwater-borne pathogens in recreational waters in the United States. Water Res 47:5282–5297. [PubMed]
65. Vergara GG, Rose JB, Gin KY. 2016. Risk assessment of noroviruses and human adenoviruses in recreational surface waters. Water Res 103:276–82. [PubMed]
66. Bae S, Wuertz S. 2012. Survival of host-associated Bacteroidales cells and their relationship with Enterococcus spp., Campylobacter jejuni, Salmonella enterica serovar Typhimurium, and adenovirus in freshwater microcosms as measured by propidium monoazide-quantitative PCR. Appl Environ Microbiol 78:922–932. [PubMed]
67. Eifan SA. 2013. Enteric viruses and aquatic environment. Internet J Microbiol 12:1–7.
68. Bruu AL. 2002. Enteroviruses: polioviruses, coxsackieviruses, echoviruses and newer enteroviruses, p 44–45. In Haaheim LR, Pattison JR, Whitley RJ (ed), A Practical Guide to Clinical Virology, 2nd ed. John Wiley & Sons, Ltd., Chichester, United Kingdom.
69. Holm-Hansen CC, Midgley SE, Fischer TK. 2016. Global emergence of enterovirus D68: a systematic review. Lancet Infect Dis 16:64–75.
70. Solomon T, Lewthwaite P, Perera D, Cardosa MJ, McMinn P, Ooi MH. 2010. Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect Dis 10:778–790.
71. Muehlenbachs A, Bhatnagar J, Zaki SR. 2015. Tissue tropism, pathology and pathogenesis of enterovirus infection. J Pathol 235:217–228. [PubMed]
72. Palminha P, Ribeiro C, Roque C, Vinagre E. 2015. Vigilância laboratorial da infeção a Enterovirus entre 2010 e 2013. Bol Epidemiol Observações 5:19–21.
73. Chang PC, Chen SC, Chen KT. 2016. The current status of the disease caused by enterovirus 71 infections: epidemiology, pathogenesis, molecular epidemiology, and vaccine development. Int J Environ Res Public Health 13:29–34. [PubMed]
74. Symonds EM, Verbyla ME, Lukasik JO, Kafle RC, Breitbart M, Mihelcic JR. 2014. A case study of enteric virus removal and insights into the associated risk of water reuse for two wastewater treatment pond systems in Bolivia. Water Res 65:257–270. [PubMed]
75. Clarke IN, Estes MK, Green KY, Hansman GS, Knowles NJ, Koopmans M, Matson DO, Meyers G, Neill J, Radford A, Smith AW, Studdert M, Thiel H-J., Vinjé J. 2012. Caliciviridae, p 977–985. In King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds), Virus Taxonomy: Classification and Nomenclature of Viruses. 9th report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, San Diego, CA.
76. Green K. 2013. Caliciviridae: the noroviruses, p 583–609, In Knipe DM, Howley PM(ed), Fields Virology, vol 1, 6th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
77. Kroneman A, Vega E, Vennema H, Vinjé J, White PA, Hansman G, Green K, Martella V, Katayama K, Koopmans M. 2013. Proposal for a unified norovirus nomenclature and genotyping. Arch Virol 158:2059–2068. [PubMed]
78. Vinjé J. 2015. Advances in laboratory methods for detection and typing of norovirus. J Clin Microbiol 53:373–381. [PubMed]
79. Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe SS. 2006. Norovirus classification and proposed strain nomenclature. Virology 346:312–323. [PubMed]
80. Bartsch SM, Lopman BA, Ozawa S, Hall AJ, Lee BY. 2016. Global economic burden of norovirus gastroenteritis. PLoS One 11:e0151219. [PubMed]
81. Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinjé J, Parashar UD. 2008. Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg Infect Dis 14:1224–1231. [PubMed]
82. Graham DY, Jiang X, Tanaka T, Opekun AR, Madore HP, Estes MK. 1994. Norwalk virus infection of volunteers: new insights based on improved assays. J Infect Dis 170:34–43. [PubMed]
83. Phillips G, Tam CC, Rodrigues LC, Lopman B. 2010. Prevalence and characteristics of asymptomatic norovirus infection in the community in England. Epidemiol Infect 138:1454–1458. [PubMed]
84. Harris JP, Edmunds WJ, Pebody R, Brown DW, Lopman BA. 2008. Deaths from norovirus among the elderly, England and Wales. Emerg Infect Dis 14:1546–1552. [PubMed]
85. Hutson AM, Atmar RL, Estes MK. 2004. Norovirus disease: changing epidemiology and host susceptibility factors. Trends Microbiol 12:279–287. [PubMed]
86. Payne DC, Vinjé J, Szilagyi PG, Edwards KM, Staat MA, Weinberg GA, Hall CB, Chappell J, Bernstein DI, Curns AT, Wikswo M, Shirley SH, Hall AJ, Lopman B, Parashar UD. 2013. Norovirus and medically attended gastroenteritis in U.S. children. N Engl J Med 368:1121–1130. [PubMed]
87. Siebenga JJ, Vennema H, Zheng DP, Vinjé J, Lee BE, Pang XL, Ho EC, Lim W, Choudekar A, Broor S, Halperin T, Rasool NB, Hewitt J, Greening GE, Jin M, Duan ZJ, Lucero Y, O’Ryan M, Hoehne M, Schreier E, Ratcliff RM, White PA, Iritani N, Reuter G, Koopmans M. 2009. Norovirus illness is a global problem: emergence and spread of norovirus GII.4 variants, 2001-2007. J Infect Dis 200:802–812. [PubMed]
88. Tian G, Jin M, Li H, Li Q, Wang J, Duan ZJ. 2014. Clinical characteristics and genetic diversity of noroviruses in adults with acute gastroenteritis in Beijing, China in 2008-2009. J Med Virol 86:1235–1242. [PubMed]
89. Ahmed SM, Hall AJ, Robinson AE, Verhoef L, Premkumar P, Parashar UD, Koopmans M, Lopman BA. 2014. Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis 14:725–730.
90. Pires SM, Fischer-Walker CL, Lanata CF, Devleesschauwer B, Hall AJ, Kirk MD, Duarte AS, Black RE, Angulo FJ. 2015. Aetiology-specific estimates of the global and regional incidence and mortality of diarrhoeal diseases commonly transmitted through food. PLoS One 10:e0142927. [PubMed]
91. Ahmed SM, Lopman BA, Levy K. 2013. A systematic review and meta-analysis of the global seasonality of norovirus. PLoS One 8:e75922. [PubMed]
92. Lanata CF, Fischer-Walker CL, Olascoaga AC, Torres CX, Aryee MJ, Black RE. 2013. Global causes of diarrheal disease mortality in children <5 years of age: a systematic review. PLoS One 8:e72788. [PubMed]
93. Lopman BA, Steele D, Kirkwood CD, Parashar UD. 2016. The vast and varied global burden of norovirus: prospects for prevention and control. PLoS Med 13:e1001999. [PubMed]
94. Teunis PF, Moe CL, Liu P, Miller SE, Lindesmith L, Baric RS, Le Pendu J, Calderon RL. 2008. Norwalk virus: how infectious is it? J Med Virol 80:1468–1476. [PubMed]
95. Atmar RL, Opekun AR, Gilger MA, Estes MK, Crawford SE, Neill FH, Ramani S, Hill H, Ferreira J, Graham DY. 2014. Determination of the 50% human infectious dose for Norwalk virus. J Infect Dis 209:1016–1022. [PubMed]
96. Kirby AE, Teunis PF, Moe CL. 2014. Two human challenge studies confirm high infectivity of Norwalk virus. J Infect Dis. https://doi.org/10.1093/infdis/jiu585.
97. Kambhampati A, Payne DC, Costantini V, Lopman BA. 2016. Host genetic susceptibility to enteric viruses: a systematic review and meta-analysis. Clin Infect Dis 62:11–18. [PubMed]
98. Pang XL, Preiksaitis JK, Lee BE. 2014. Enhanced enteric virus detection in sporadic gastroenteritis using a multi-target real-time PCR panel: a one-year study. J Med Virol 86:1594–601. [PubMed]
99. Parrino TA, Schreiber DS, Trier JS, Kapikian AZ, Blacklow NR. 1977. Clinical immunity in acute gastroenteritis caused by Norwalk agent. N Engl J Med 297:86–89. [PubMed]
100. Fankhauser RL, Monroe SS, Noel JS, Humphrey CD, Bresee JS, Parashar UD, Ando T, Glass RI. 2002. Epidemiologic and molecular trends of “Norwalk-like viruses” associated with outbreaks of gastroenteritis in the United States. J Infect Dis 186:1–7. [PubMed]
101. Rockx B, De Wit M, Vennema H, Vinjé J, De Bruin E, Van Duynhoven Y, Koopmans M. 2002. Natural history of human calicivirus infection: a prospective cohort study. Clin Infect Dis 35:246–253. [PubMed]
102. Matsui SM, Greenberg HB. 2000. Immunity to calicivirus infection. J Infect Dis 181:S331–335. [PubMed]
103. Johnson PC, Mathewson JJ, DuPont HL, Greenberg HB. 1990. Multiple-challenge study of host susceptibility to Norwalk gastroenteritis in US adults. J Infect Dis 161:18–21. [PubMed]
104. Wyatt RG, Greenberg HB, Dalgard DW, Allen WP, Sly DL, Thornhill TS, Chanock RM, Kapikian AZ. 1978. Experimental infection of chimpanzees with the Norwalk agent of epidemic viral gastroenteritis. J Med Virol 2:89–96. [PubMed]
105. Bernstein DI, Atmar RL, Lyon GM, Treanor JJ, Chen WH, Jiang X, Vinjé J, Gregoricus N, Frenck RW, Jr, Moe CL, Al-Ibrahim MS, Barrett J, Ferreira J, Estes MK, Graham DY, Goodwin R, Borkowski A, Clemens R, Mendelman PM. 2015. Norovirus vaccine against experimental human GII.4 virus illness: a challenge study in healthy adults. J Infect Dis 211:870–878. [PubMed]
106. Debbink K, Lindesmith LC, Baric RS. 2014. The state of norovirus vaccines. Clin Infect Dis 58:1746–1752. [PubMed]
107. Treanor JJ, Atmar RL, Frey SE, Gormley R, Chen WH, Ferreira J, Goodwin R, Borkowski A, Clemens R, Mendelman PM. 2014. A novel intramuscular bivalent norovirus virus-like particle vaccine candidate: reactogenicity, safety, and immunogenicity in a phase 1 trial in healthy adults. J Infect Dis 210:1763–1771. [PubMed]
108. Podewils LJ, Zanardi Blevins L, Hagenbuch M, Itani D, Burns A, Otto C, Blanton L, Adams S, Monroe SS, Beach MJ, Widdowson M. 2007. Outbreak of norovirus illness associated with a swimming pool. Epidemiol Infect 135:827–833. [PubMed]
109. Widdowson MA, Cramer EH, Hadley L, Bresee JS, Beard RS, Bulens SN, Charles M, Chege W, Isakbaeva E, Wright JG, Mintz E, Forney D, Massey J, Glass RI, Monroe SS. 2004. Outbreaks of acute gastroenteritis on cruise ships and on land: identification of a predominant circulating strain of norovirus: United States, 2002. J Infect Dis 190:27–36. [PubMed]
110. White PA. 2014. Evolution of norovirus. Clin Microbiol Infect 20:741–745. [PubMed]
111. Xerry J, Gallimore CI, Iturriza-Gómara M, Allen DJ, Gray JJ. 2008. Transmission events within outbreaks of gastroenteritis determined through analysis of nucleotide sequences of the P2 domain of genogroup II noroviruses. J Clin Microbiol 46:947–953. [PubMed]
112. Bitler EJ, Matthews JE, Dickey BW, Eisenberg JN, Leon JS. 2013. Norovirus outbreaks: a systematic review of commonly implicated transmission routes and vehicles. Epidemiol Infect 141:1563–1571. [PubMed]
113. Glass R, Umesh D, Parashar U, Estes M. 2009. Norovirus gastroenteritis. N Engl J Med 361:1776–1785. [PubMed]
114. Kotwal G, Cannon JL. 2014. Environmental persistence and transfer of enteric viruses. Curr Opin Virol 4:37–43. [PubMed]
115. Widdowson MA, Sulka A, Bulens SN, Beard RS, Chaves SS, Hammond R, Salehi ED, Swanson E, Totaro J, Woron R, Mead PS, Bresee JS, Monroe SS, Glass RI. 2005. Norovirus and foodborne disease, United States, 1991-2000. Emerg Infect Dis 11:95–102. [PubMed]
116. Kukkula M, Maunula L, Silvennoinen E, von Bonsdorff CH. 1999. Outbreak of viral gastroenteritis due to drinking water contaminated by Norwalk-like viruses. J Infect Dis 180:1771–1776. [PubMed]
117. Doyle MP, Erickson MC. 2008. Summer meeting 2007—the problems with fresh produce: an overview. J Appl Microbiol 105:317–330. [PubMed]
118. Maunula L, Miettinen IT, von Bonsdorff CH. 2005. Norovirus outbreaks from drinking water. Emerg Infect Dis 11:1716–1721. [PubMed]
119. Matthews JE, Dickey BW, Miller RD, Felzer JR, Dawson BP, Lee AS, Rocks JJ, Kiel J, Montes JS, Moe CL, Eisenberg JN, Leon JS. 2012. The epidemiology of published norovirus outbreaks: a review of risk factors associated with attack rate and genogroup. Epidemiol Infect 140:1161–1172. [PubMed]
120. Riera-Montes M, Brus Sjölander K, Allestam G, Hallin E, Hedlund KO, Löfdahl M. 2011. Waterborne norovirus outbreak in a municipal drinking-water supply in Sweden. Epidemiol Infect 139:1928–1935. [PubMed]
121. Berg DE, Kohn MA, Farley TA, McFarland LM. 2000. Multi-state outbreaks of acute gastroenteritis traced to fecal-contaminated oysters harvested in Louisiana. J Infect Dis 181:S381–S386. [PubMed]
122. EFSA Panel on Biological Hazards (BIOHAZ). 2012. Norovirus (NoV) in oysters: methods, limits and control options. EFSA J 10:2500–2539.
123. Le Guyader FS, Krol J, Ambert-Balay K, Ruvoen-Clouet N, Desaubliaux B, Parnaudeau S, Le Saux JC, Ponge A, Pothier P, Atmar RL, Le Pendu J. 2010. Comprehensive analysis of a norovirus-associated gastroenteritis outbreak, from the environment to the consumer. J Clin Microbiol 48:915–920. [PubMed]
124. Lees D. 2000. Viruses and bivalve shellfish. Int J Food Microbiol 59:81–116.
125. Lopman BA, Reacher MH, Van Duijnhoven Y, Hanon FX, Brown D, Koopmans M. 2003. Viral gastroenteritis outbreaks in Europe, 1995-2000. Emerg Infect Dis 9:90–96. [PubMed]
126. Thebault A, Teunis PF, Le Pendu J, Le Guyader FS, Denis JB. 2013. Infectivity of GI and GII noroviruses established from oyster related outbreaks. Epidemics 5:98–110. [PubMed]
127. Fitzgerald TL, Merritt TD, Zammit A, McLeod C, Landinez LM, White PA, Munnoch SA, Durrheim DN. 2014. An outbreak of norovirus genogroup II associated with New South Wales oysters. Commun Dis Intell Q Rep 38:E9–E15.
128. Huppatz C, Munnoch SA, Worgan T, Merritt TD, Dalton C, Kelly PM, Durrheim DN. 2008. A norovirus outbreak associated with consumption of NSW oysters: implications for quality assurance systems. Commun Dis Intell Q Rep 32:88–91.
129. Bernard H, Faber, M, Wilking H, Haller S, Höhle M, Schielke A, Ducomble T, Siffczyk C, Merbecks SS, Fricke G, Hamouda O, Stark K, Werber D. 2014. Large multistate outbreak of norovirus gastroenteritis associated with frozen strawberries, Germany, 2012. Euro Surveill 19:20719. https://www.eurosurveillance.org/content/10.2807/1560-7917.ES2014.19.8.20719.
130. Ethelberg S, Lisby M, Bottiger B, Schultz AC, Villif A, Jensen T, Olsen KE, Scheutz F, Kjelso C, Muller L. 2010. Outbreaks of gastroenteritis linked to lettuce, Denmark, January 2010. Euro Surveill 15:19484. https://www.eurosurveillance.org/content/10.2807/ese.15.06.19484-en.
131. Hennechart-Collette C, Martin-Latil S, Guillier L, Perelle S. 2015. Determination of which virus to use as a process control when testing for the presence of hepatitis A virus and norovirus in food and water. Int J Food Microbiol 202:57–65. [PubMed]
132. Mathijs E, Stals A, Baert L, Botteldoorn N, Denayer S, Mauroy A, Scipioni A, Daube G, Dierick K, Herman L, Van Coillie E, Uyttendaele M, Thiry E. 2012. A review of known and hypothetical transmission routes for noroviruses. Food Environ Virol 4:131–152. [PubMed]
133. Rodríguez-Lázaro D, Cook N, Ruggeri FM, Sellwood J, Nasser A, Nascimento MS, D’Agostino M, Santos R, Saiz JC, Rzeżutka A, Bosch A, Gironés R, Carducci A, Muscillo M, Kovač K, Diez-Valcarce M, Vantarakis A, von Bonsdorff CH, de Roda Husman AM, Hernández M, van der Poel WH. 2012. Virus hazards from food, water and other contaminated environments. FEMS Microbiol Rev 36:786–814. [PubMed]
134. Robilotti E, Deresinski S, Pinsky BA. 2015. Norovirus. Clin Microbiol Rev 28:134–164. [PubMed]
135. La Rosa G, Fontana S, Di Grazia A, Iaconelli M, Pourshaban M, Muscillo M. 2007. Molecular identification and genetic analysis of norovirus genogroups I and II in water environments: comparative analysis of different reverse transcription-PCR assays. Appl Environ Microbiol 73:4152–4161. [PubMed]
136. van den Berg H, Lodder W, van der Poel W, Vennema H, de Roda Husman AM. 2005. Genetic diversity of noroviruses in raw and treated sewage water. Res Microbiol 156:532–540. [PubMed]
137. Bae J, Schwab KJ. 2008. Evaluation of murine norovirus, feline calicivirus, poliovirus, and MS2 as surrogates for human norovirus in a model of viral persistence in surface water and groundwater. Appl Environ Microbiol 74:477–484. [PubMed]
138. Ngazoa ES, Fliss I, Jean J. 2008. Quantitative study of persistence of human norovirus genome in water using TaqMan real-time RT-PCR. J Appl Microbiol 104:707–715. [PubMed]
139. Seitz SR, Leon JS, Schwab KJ, Lyon GM, Dowd M, McDaniels M, Abdulhafid G, Fernandez ML, Lindesmith LC, Baric RS, Moe CL. 2011. Norovirus infectivity in humans and persistence in water. Appl Environ Microbiol 77:6884–6888. [PubMed]
140. Hörman A, Rimhanen-Finne R, Maunula L, von Bonsdorff CH, Torvela N, Heikinheimo A, Hänninen ML. 2004. Campylobacter spp., Giardia spp., Cryptosporidium spp., noroviruses, and indicator organisms in surface water in southwestern Finland, 2000-2001. Appl Environ Microbiol 70:87–95. [PubMed]
141. Lee SG, Jheong WH, Suh CI, Kim SH, Lee JB, Jeong YS, Ko G, Jang KL, Lee GC, Paik SY. 2011. Nationwide groundwater surveillance of noroviruses in South Korea, 2008. Appl Environ Microbiol 77:1466–1474. [PubMed]
142. Charles KJ, Shore J, Sellwood J, Laverick M, Hart A, Pedley S. 2009. Assessment of the stability of human viruses and coliphage in groundwater by PCR and infectivity methods. J Appl Microbiol 106:1827–1837. [PubMed]
143. Dienus O, Sokolova E, Nyström F, Matussek A, Löfgren S, Blom L, Pettersson TJ, Lindgren PE. 2016. Norovirus dynamics in wastewater discharges and in the recipient drinking water source: long-term monitoring and hydrodynamic modeling. Environ Sci Technol 50:10851–10858. [PubMed]
144. Pusch D, Oh DY, Wolf S, Dumke R, Schröter-Bobsin U, Höhne M, Röske I, Schreier E. 2005. Detection of enteric viruses and bacterial indicators in German environmental waters. Arch Virol 150:929–947. [PubMed]
145. Westrell T, Teunis P, van den Berg H, Lodder W, Ketelaars H, Stenström TA, de Roda Husman AM. 2006. Short- and long-term variations of norovirus concentrations in the Meuse river during a 2-year study period. Water Res 40:2613–2620. [PubMed]
146. Pérez-Sautu U, Sano D, Guix S, Kasimir G, Pintó RM, Bosch A. 2012. Human norovirus occurrence and diversity in the Llobregat River catchment, Spain. Environ Microbiol 14:494–502. [PubMed]
147. Mounts AW, Ando T, Koopmans M, Bresee JS, Noel J, Glass RI. 2000. Cold weather seasonality of gastroenteritis associated with Norwalk-like viruses. J Infect Dis 181:S284–S287. [PubMed]
148. Atmar RL, Opekun AR, Gilger MA, Estes MK, Crawford SE, Neill FH, Graham DY. 2008. Norwalk virus shedding after experimental human infection. Emerg Infect Dis 14:1553–1557. [PubMed]
149. Chan M, Sung J, Lam R. Chan P, Lee N, Lai R, Leung WK. 2006. Fecal viral load and norovirus-associated gastroenteritis. Emerg Infec Dis 12:1278–1280. [PubMed]
150. Flannery J, Keaveney S, Rajko-Nenow P, O’Flaherty V, Doré W. 2012. Concentration of norovirus during wastewater treatment and its impact on oyster contamination. Appl Environ Microbiol 78:3400–3406. [PubMed]
151. Ciocca M. 2000. Clinical course and consequences of hepatitis A infection. Vaccine 18:71–74.
152. Bosan A, Qureshi H, Bile KM, Ahmad I, Hafiz R. 2010. A review of hepatitis viral infections in Pakistan. J Pak Med Assoc 60:1045–1058.
153. Shuval H. 2003. Estimating the global burden of thalassogenic diseases: human infectious diseases caused by wastewater pollution of the marine environment. J Water Health 1:53–64. [PubMed]
154. Koff RS. 1998. Hepatitis A. Lancet 351:1643–1649.
155. Franco E, Meleleo C, Serino L, Sorbara D, Zaratti L. 2012. Hepatitis A: epidemiology and prevention in developing countries. World J Hepatol 4:68–73. [PubMed]
156. European Centre for Disease Prevention and Control. 26 June 2017. https://www.ecdc.europa.eu/en/hepatitis-A/facts. Accessed 10 June 2019.
157. CDC. 2020. Widespread person-to-person outbreaks of hepatitis A across the United States. https://www.cdc.gov/hepatitis/outbreaks/2017March-HepatitisA.htm. Accessed 10 June 2019.
158. Savage RD, Rosella LC, Brown KA, Khan K, Crowcroft NS. 2016. Underreporting of hepatitis A in non-endemic countries: a systematic review and meta-analysis. BMC Infect Dis 16:1–12. [PubMed]
159. Pond K. 2005. Water Recreation and Disease—Plausibility of Associated Infections: Acute Effects, Sequelae and Mortality. World Health Organization, Geneva, Switzerland.
160. Yezli S, Otter JA. 2011. Minimum infective dose of the major human respiratory and enteric viruses transmitted through food and the environment. Food Environ Virol 3:1–30.
161. Jacobsen K. 2009. The Global Prevalence of Hepatitis A Virus Infection and Susceptibility: a Systematic Review. World Health Organization, Geneva, Switzerland.
162. Yong HT, Son R. 2009. Hepatitis A virus: a general overview. Int Food Res J 467:455–467.
163. Gupta E, Ballani N. 2014. State of the globe: hepatitis a virus—return of a water devil. J Global Infect Dis 6:57–58. [PubMed]
164. Osuolale O, Okoh A. 2015. Incidence of human adenoviruses and hepatitis A virus in the final effluent of selected wastewater treatment plants in Eastern Cape Province, South Africa. Virol J 12:98. [PubMed]
165. Jacobsen KH, Wiersma ST. 2010. Hepatitis A virus seroprevalence by age and world region, 1990 and 2005. Vaccine 28:6653–6657. [PubMed]
166. Yeh HY, Hwang YC, Yates MV, Mulchandani A, Chen W. 2008. Detection of hepatitis A virus by using a combined cell culture-molecular beacon assay. Appl Environ Microbiol 74:2239–2243. [PubMed]
167. Polo D, Varela MF, Romalde JL. 2015. Detection and quantification of hepatitis A virus and norovirus in Spanish authorized shellfish harvesting areas. Int J Food Microbiol 193:43–50. [PubMed]
168. Aggarwal R. 2011. Hepatitis E: historical, contemporary and future perspectives. J Gastroenterol Hepatol 26:72–82. [PubMed]
169. Tam AW, Smith MM, Guerra ME, Huang CC, Bradley DW, Fry KE, Reyes GR. 1991. Hepatitis E virus (HEV): molecular cloning and sequencing of the full-length viral genome. Virology 185:120–131.
170. Hakim MS, Wang W, Bramer WM, Geng J, Huang F, de Man RA, Peppelenbosch MP, Pan Q. 2017. The global burden of hepatitis E outbreaks: a systematic review. Liver Int 37:19–31. [PubMed]
171. Rein DB, Stevens GA, Theaker J, Wittenborn JS, Wiersma ST. 2012. The global burden of hepatitis E virus genotypes 1 and 2 in 2005. Hepatology 55:988–997. [PubMed]
172. Goel A, Aggarwal R. 2016. Advances in hepatitis E. II. Epidemiology, clinical manifestations, treatment and prevention. Expert Rev Gastroenterol Hepatol 10:1065–1074. [PubMed]
173. Kumar S, Subhadra S, Singh B, Panda BK. 2013. Hepatitis E virus: the current scenario. Int J Infect Dis 17:228–233. [PubMed]
174. Łapiński TW, Jaroszewicz J. 2016. Hepatitis E virus infection: a new threat for Europe. Przeglad Epidemiol 70:11–14.
175. Song YJ, Park WJ, Park BJ, Lee JB, Park SY, Song CS, Lee NH, Seo KH, Kang YS, Choi IS. 2014. Hepatitis E virus infections in humans and animals. Clin Exp Vaccine Res 3:29–36. [PubMed]
176. Fierro NA, Realpe M, Meraz-Medina T, Roman S, Panduro A. 2016. Hepatitis E virus: an ancient hidden enemy in Latin America. World J Gastroenterol 22:2271–2283. [PubMed]
177. Park W, Park B, Ahn H, Lee J, Park S, Song C, Lee S, Yoo H, Choi I. 2016. Hepatitis E virus as an emerging zoonotic pathogen. J Vet Sci 17:1–11. [PubMed]
178. Doceul V, Bagdassarian E, Demange A, Pavio N. 2016. Zoonotic hepatitis E virus: classification, animal reservoirs and transmission routes. Viruses 8:1–25. [PubMed]
179. Dalton HR, Seghatchian J. 2016. Hepatitis E virus: emerging from the shadows in developed countries. Transf Apher Sci 55:271–274. [PubMed]
180. Dalton HR, Bendall R, Ijaz S, Banks M. 2008. Hepatitis E: an emerging infection in developed countries. Lancet Infect Dis 8:698–709.
181. Ferreira CM, Santos JA, Lourenço T, Benoliel C, Matos R, Martins HC. 2013. Diagnóstico da infeção por vírus da hepatite E no INSA 2000-2012. Bol Epidemiol Observações 10:27–28.
182. Meng XJ. 2010. Hepatitis E virus: animal reservoirs and zoonotic risk. Vet Microbiol 140:256–265. [PubMed]
183. Ruggeri FM, Di Bartolo I, Ponterio E, Angeloni G, Trevisani M, Ostanello F. 2013. Zoonotic transmission of hepatitis E virus in industrialized countries. New Microbiol 36:331–344.
184. Dalton H, Izopet J. 2018. Transmission and epidemiology of hepatitis E virus genotype 3 and 4 infections. Cold Spring Harb Perspect Med 8:a032144. [PubMed]
185. EFSA. 2017. Hepatitis E: raw pork is main cause of infection in EU. https://www.efsa.europa.eu/en/press/news/170711. Accessed 10 June 2019.
186. Cashdollar JL, Brinkman NE, Griffin SM, Mcminn BR, Rhodes ER, Varughese EA, Grimm AC, Parshionikar SU, Wymer L, Shay Fout G. 2012. Development and evaluation of EPA method 1615 for detection of enterovirus and norovirus in water. Appl Environ Microbiol 79:215–223. [PubMed]
187. Griffin DW, Donaldson KA, Paul JH, Rose JB. 2003. Pathogenic human viruses in coastal waters. Clin Microbiol Rev 16:129–143. [PubMed]
188. Ettayebi K, Crawford SE, Murakami K, Broughman JR, Karandikar U, Tenge VR, Neill FH, Blutt SE, Zeng XL, Qu L, Kou B, Opekun AR, Burrin D, Graham DY, Ramani S, Atmar RL, Estes MK. 2016. Replication of human noroviruses in stem cell-derived human enteroids. Science 353:1387–1393. [PubMed]
189. Iaconelli M, Purpari G, Libera S, Petricca S, Guercio A, Ciccaglione AR, Bruni R, Taffon S, Equestre M, Fratini M, Muscillo M, La Rosa G. 2015. Hepatitis A and E viruses in wastewaters, in river waters, and in bivalve molluscs in Italy. Food Environ Virol 7:316–324. [PubMed]
190. Montazeri N, Goettert D, Achberger EC, Johnson CN, Prinyawiwatkul W, Janes ME. 2015. Pathogenic enteric viruses and microbial indicators during secondary treatment of municipal wastewater. Appl Environ Microbiol 81:6436–6445. [PubMed]
191. Leifels M, Hamza IA, Krieger M, Wilhelm M, Mackowiak M, Jurzik L. 2016. From lab to lake: evaluation of current molecular methods for the detection of infectious enteric viruses in complex water matrices in an urban area. PLoS One 11:1–16. [PubMed]
192. Hamza IA, Jurzik L, Uberla K, Wilhelm M. 2011. Evaluation of pepper mild mottle virus, human picobirnavirus and torque teno virus as indicators of fecal contamination in river water. Water Res 45:1358–68. [PubMed]
193. Rodríguez RA, Pepper IL, Gerba CP. 2009. Application of PCR-based methods to assess the infectivity of enteric viruses in environmental samples. Appl Environ Microbiol 75:297–307. [PubMed]
194. Donia D, Bonanni E, Diaco L, Divizia M. 2010. Statistical correlation between enterovirus genome copy numbers and infectious viral particles in wastewater samples. Lett Appl Microbiol 50:237–240. [PubMed]
195. Hamza IA, Bibby K. 2019. Critical issues in application of molecular methods to environmental virology. J Virol Methods 266:11–24. [PubMed]
196. Harrison CG, Williams PR. 2016. A systems approach to natural disaster resilience. Simul Model Pract Theory 65:11–31.
197. U.S. Environmental Protection Agency. 2016. Climate Change Indicators: Sea Level. https://www.epa.gov/climate-indicators/climate-change-indicators-sea-level.
199. Gall AM, Mariñas BJ, Lu Y, Shisler JL. 2015. Waterborne viruses: a barrier to safe drinking water. PLoS Pathog 11:1–7. [PubMed]
200. Voulvoulis N. 2018. Water reuse from a circular economy perspective and potential risks from an unregulated approach. Curr Opin Environ Sci Health 2:32–45.
201. Lodder WJ, de Roda Husman AM. 2005. Presence of noroviruses and other enteric viruses in sewage and surface waters in The Netherlands. Appl Environ Microbiol 71:1453–1461. [PubMed]
202. Amenu D. 2014. Wastewater treatment plants as a source of microbial pathogens in receiving watersheds. Res J Chem Environ Sci 2:11–19.
203. Ahmad T, Arshad N, Adnan F, Sadaf Zaidi NU, Shahid MT, Zahoor U, Afzal MS, Anjum S. 2016. Prevalence of rotavirus, adenovirus, hepatitis A virus and enterovirus in water samples collected from different region of Peshawar, Pakistan. Ann Agric Environ Med 23:576–580. [PubMed]
204. Bergamaschi B, Rodrigues MT, Silva JV, Kluge M, Luz RB, Fleck JD, Bianchi E, Silva LB, Spilki FR. 2015. Moving beyond classical markers of water quality: detection of enteric viruses and genotoxicity in water of the Sinos River. Braz J Biol 75:63–67. [PubMed]
205. Sauerbrei A, Wutzler P. 2009. Testing thermal resistance of viruses. Arch Virol 154:115–119. [PubMed]
206. Connell C, Tong HI, Wang Z, Allmann E, Lu Y. 2012. New approaches for enhanced detection of enteroviruses from Hawaiian environmental waters. PLoS ONE 7:1–9. [PubMed]
207. Fuhrman JA, Liang X, Noble RT. 2005. Rapid detection of enteroviruses in small volumes of natural waters by real-time quantitative reverse transcriptase PCR. Appl Environ Microbiol 71:4523–4530. [PubMed]
208. Jiang SC, Chu W. 2004. PCR detection of pathogenic viruses in southern California urban rivers. J Appl Microbiol 97:17–28. [PubMed]
209. O’Brien E, Nakyazze J, Wu H, Kiwanuka N, Cunningham W, Kaneene JB, Xagoraraki I. 2017. Viral diversity and abundance in polluted waters in Kampala, Uganda. Water Res 127:41–49. [PubMed]
210. Pennino F, Nardone A, Montuori P, Aurino S, Torre I, Battistone A, Delogu R, Buttinelli G, Fiore S, Amato C, Triassi M. 2018. Large-scale survey of human enteroviruses in wastewater treatment plants of a metropolitan area of southern Italy. Food Environ Virol 10:187–192. [PubMed]
211. Prevost B, Lucas FS, Gonçalves A, Richard F, Moulin L, Wurtzer S. 2015. Large scale survey of enteric viruses in river and wastewater underlines the health status of the local population. Environ Int 79:42–50. [PubMed]
212. Updyke EA, Wang Z, Sun S, Connell C, Kirs M, Wong M, Lu Y. 2015. Human enteric viruses: potential indicators for enhanced monitoring of recreational water quality. Virol Sin 30:344–353. [PubMed]
213. Blanco A, Guix S, Fuster N, Fuentes C, Bartolomé R, Cornejo T, Pintó R, Bosch A. 2017. Norovirus in bottled water associated with outbreak, Spain, 2016. Emerg Infect Dis 23:1531–1534. [PubMed]
214. Grøndahl-Rosado RC, Yarovitsyna E, Trettenes E, Myrmel M, Robertson LJ. 2014. A one year study on the concentrations of norovirus and enteric adenoviruses in wastewater and a surface drinking water source in Norway. Food Environ Virol 6:232–245. [PubMed]
215. Hall AJ. 2012. Noroviruses: the perfect human pathogens? J Infect Dis 205:1622–1624. [PubMed]
216. Lee BR, Lee SG, Park JH, Kim KY, Ryu SR, Rhee OJ, Park JW, Lee JS, Paik SY. 2013. Norovirus contamination levels in ground water treatment systems used for food-catering facilities in South Korea. Viruses 5:1646–1654. [PubMed]
217. Ahmad T, Anjum S, Zaidi N, Ali A, Waqas M, Afzal MS, Arshad N. 2015. Frequency of hepatitis E and hepatitis A virus in water sample collected from Faisalabad, Pakistan. Ann Agric Environ Med 22:661–664. [PubMed]
218. Béji-Hamza A, Khélifi-Gharbi H, Hassine-Zaafrane M, Della Libera S, Iaconelli M, Muscillo M, Petricca S, Ciccaglione AR, Bruni R, Taffon S, La Rosa G. 2014. Qualitative and quantitative assessment of hepatitis A virus in wastewaters in Tunisia. Food Environ Virol 6:246–252. [PubMed]
219. Dias J, Pinto R, Vieira C, Abreu Corrêa A. 2018. Detection and quantification of human adenovirus (HAdV), JC polyomavirus (JCPyV) and hepatitis A virus (HAV) in recreational waters of Niterói, Rio de Janeiro, Brazil. Mar Pollut Bull 133:240–245. [PubMed]
220. Elmahdy MEI, Fongaro G, Magri ME, Petruccio MM, Barardi CRM. 2016. Spatial distribution of enteric viruses and somatic coliphages in a lagoon used as drinking water source and recreation in Southern Brazil. Int J Hyg Environ Health 219:617–625. [PubMed]
221. Hamza H, Abd-Elshafy DN, Fayed SA, Bahgat MM, El-Esnawy NA, Abdel-Mobdy E. 2017. Detection and characterization of hepatitis A virus circulating in Egypt. Arch Virol 162:1921–1931. [PubMed]
222. Peláez-Carvajal D, Guzmán BL, Rodríguez J, Acero F, Nava G. 2016. Presence of enteric viruses in water samples for consumption in Colombia: challenges for supply systems. Biomedica 36:169–172. [PubMed]
223. Shin E, Kim JS, Oh KH, Oh SS, Kwon MJ, Kim S, Parka J, Kwaka H, Chunga G, Kimc C, Kim J. 2017. A waterborne outbreak involving hepatitis A virus genotype IA at a residential facility in the Republic of Korea in 2015. J Clin Virol 94:63–66. [PubMed]
224. Silva AM, Vieira H, Martins N, Granja ATS, Vale MJ, Vale FF. 2009. Viral and bacterial contamination in recreational waters: a case study in the Lisbon bay area. J Appl Microbiol 108:1023–1031. [PubMed]
225. Baez PA, Lopez MC, Duque-Jaramillo A, Pelaez D, Molina F, Navas MC. 2017. First evidence of the hepatitis E virus in environmental waters in Colombia. PLoS One 12:e0177525. [PubMed]
226. Hellmér M, Paxéus N, Magnius L, Enache L, Arnholm B, Johansson A, Bergström T, Norder H. 2014. Detection of pathogenic viruses in sewage provided early warnings of hepatitis A virus and norovirus outbreaks. Appl Environ Microbiol 80:6771–6781. [PubMed]
227. La Rosa G, Pourshaban M, Iaconelli M, Vennarucci VS, Muscillo M. 2010. Molecular detection of hepatitis E virus in sewage samples. Appl Environ Microbiol 76:5870–5873. [PubMed]
228. La Rosa G, Proroga Y, De Medici D, Capuano F, Iaconelli M, Della Libera S, Suffredini E. 2018. First detection of hepatitis E virus in shellfish and in seawater from production areas in southern Italy. Food Environ Virol 10:127–131. [PubMed]
229. Dongdem JT, Adjimani J, Armah G. 2010. Detection and characterization of human rotavirus in tap water by multiplex RT-PCR. Int J Med Med Sci 1:223–230.
230. Gratacap-Cavallier B, Genoulaz O, Soule H, Bost M, Gofti L, Zmirou D, Seigneurin JM. 2000. Detection of human and animal rotavirus sequences in drinking water. Appl Environ Microbiol 66:2690–2692. [PubMed]
231. Lodder WJ, Berg HHJL, Rutjes SA, Husman AMDR. 2010. Presence of enteric viruses in source waters for drinking water production in the Netherlands. Appl Environ Microbiol 76:5965–5971. [PubMed]
232. Rutjes SA, Lodder WJ, Leeuwen A, Husman A. 2009. Detection of infectious rotavirus in naturally contaminated source waters for drinking water production. J Appl Microbiol 107:97–105. [PubMed]
233. Haramoto E, Fujino S, Otagari M. 2015. Distinct behaviors of infectious F-specific RNA coliphage genogroups at a wastewater treatment plant. Sci Total Environ 520:32–38. [PubMed]
234. Schmitz BW, Kitajima M, Campillo ME, Gerba CP, Pepper IL. 2016. Virus reduction during advanced Bardenpho and conventional wastewater treatment processes. Environ Sci Technol 50:9524−9532. [PubMed]
235. 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. [PubMed]
236. Lin J, Singh A. 2015. Detection of human enteric viruses in Umgeni River, Durban, South Africa. J Water Health 13:1098–1112. [PubMed]
237. Maurer CP, Simonetti AB, Staggemeier R, Rigotto C, Heinzelmann LS, Spilki FR. 2015. Adenovirus, enterovirus and thermotolerant coliforms in recreational waters from Lake Guaíba beaches, Porto Alegre, Brazil. J Water Health 13:1123–1129. [PubMed]
238. 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. [PubMed]
239. 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. [PubMed]
240. El-Senousy W, Abdel-Moneim A, Abdel-Latif M, El-hefnawy M, Khalil G. 2018. Coxsackievirus B4 as a causative agent of diabetes mellitus type 1: is there a role of inefficiently treated drinking water and sewage in virus spreading? Food Environ Virol 10:89–98. [PubMed]
241. Aslan A, Xagoraraki I, Simmons FJ, Rose JB, Dorevitch S. 2011. Occurrence of adenovirus and other enteric viruses in limited-contact freshwater recreational areas and bathing waters. J Appl Microbiol 1:1250–1261. [PubMed]
242. Rose MA, Dhar AK, Brooks HA, Zecchini F, Gersberg RM. 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]
243. Staggemeier R, Heck TMS, Demoliner M, Ritzel RGF, Röhnelt NMS, Girardi V, Venker C, Spilki FR. 2017. Enteric viruses and adenovirus diversity in waters from 2016 Olympic venues. Sci Total Environ 586:304–312. [PubMed]
244. Kazama S, Masago Y, Tohma K, Souma N, Imagawa T, Suzuki A, Liu X, Saito M, Oshitani H, Omura T. 2016. Temporal dynamics of norovirus determined through monitoring of municipal wastewater by pyrosequencing and virological surveillance of gastroenteritis cases. Water Res 92:244–253. [PubMed]
245. Pouillot R, Van Doren JM, Woods J, Plante D, Smith M, Goblick G, Roberts C, Locas A, Hajen W, Stobo J, White J, Holtzman J, Buenaventura E, Burkhardt W III, Catford A, Edwards R, DePaola A, Calci KR. 2015. Meta-analysis of the reduction of norovirus and male-specific coliphage concentrations in wastewater treatment plants. Appl Environ Microbiol 81:4669–4681. [PubMed]
246. Iwai M, Hasegawa S, Obara M, Nakamura K, Horimoto E, Takizawa T, Kurata T, Sogen S, Shiraki K. 2009. Continuous presence of noroviruses and sapoviruses in raw sewage reflects infections among inhabitants of Toyama, Japan (2006 to 2008). Appl Environ Microbiol 75:1264–1270. [PubMed]
247. Eftim SE, Hong T, Soller J, Boehm A, Warren I, Ichida A, Nappier SP. 2017. Occurrence of norovirus in raw sewage: a systematic literature review and meta-analysis. Water Res 111:366–374. [PubMed]
248. Nordgren J, Matussek A, Mattsson A, Svensson L, Lindgren PE. 2009. Prevalence of norovirus and factors influencing virus concentrations during one year in a full-scale wastewater treatment plant. Water Res 43:1117–25. [PubMed]
249. da Silva AK, Le Saux JC, Parnaudeau S, Pommepuy M, Elimelech M, Le Guyader FS. 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]
250. López-Gálvez F, Truchado P, Sánchez G, Aznar R, Gil MI, Allende A. 2016. Occurrence of enteric viruses in reclaimed and surface irrigation water: relationship with microbiological and physicochemical indicators. J Appl Microbiol 121:1180–1188. [PubMed]
251. 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. [PubMed]
252. Ouardani I, Manso CF, Aouni M, Romalde JL. 2015. Efficiency of hepatitis A virus removal in six sewage treatment plants from central Tunisia. Appl Microbiol Biotechnol 99:10759–10769. [PubMed]
253. Chigor VN, Sibanda T, Okoh AI. 2014. Assessment of the risks for human health of adenoviruses, hepatitis A virus, rotaviruses and enteroviruses in the Buffalo River and three source water dams in the Eastern Cape. Food Environ Virol 6:87–98. [PubMed]
254. Sibanda T, Okoh AI. 2013. Real-time PCR quantitative assessment of hepatitis A virus, rotaviruses and enteroviruses in the Tyume River located in the Eastern Cape Province, South Africa. Water SA 39:295–304.
255. Wang H, Sikora P, Rutgersson C, Lindh M, Brodin T, Björlenius B, Larsson DGJ, Norder H. 2018. Differential removal of human pathogenic viruses from sewage by conventional and ozone treatments. Int J Hyg Environ Health 221:479–488. [PubMed]
256. Masclaux FG, Hotz P, Friedli D, Savova-Bianchi D, Oppliger A. 2013. High occurrence of hepatitis E virus in samples from wastewater treatment plants in Switzerland and comparison with other enteric viruses. Water Res 47:5101–5109. [PubMed]

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Changes in the occurrence, distribution, and seasonal variation of waterborne pathogens due to global climate change may increase the risk of human exposure to these microorganisms, thus heightening the need for more reliable surveillance systems. Routine monitoring of drinking water supplies and recreational waters is performed using fecal indicator microorganisms, such as , spp., and coliphages. However, the presence and numbers of these indicators, especially and spp., do not correlate well with those of other pathogens, especially enteric viruses, which are a major cause of waterborne outbreaks associated with contaminated water and food, and recreational use of lakes, ponds, rivers, and estuarine waters. For that reason, there is a growing need for a surveillance system that can detect and quantify viral pathogens directly in water sources to reduce transmission of pathogens associated with fecal transmission. In this review, we present an updated overview of relevant waterborne enteric viruses that we believe should be more commonly screened to better evaluate water quality and to determine the safety of water use and reuse and of epidemiological data on viral outbreaks. We also discuss current methodologies that are available to detect and quantify these viruses in water resources. Finally, we highlight challenges associated with virus monitoring. The information presented in this review is intended to aid in the assessment of human health risks due to contact with water sources, especially since current environmental and adaptive changes may be creating the need for a paradigm shift for indicators of fecal contamination.

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Transmission routes of enteric viruses.

Source: microbiolspec March 2020 vol. 8 no. 2 doi:10.1128/microbiolspec.ERV-0001-2019
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Symptoms, transmission pathways, and infectious doses of the most common waterborne enteric viruses in water sources

Source: microbiolspec March 2020 vol. 8 no. 2 doi:10.1128/microbiolspec.ERV-0001-2019
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Virus concentrations in wastewater, treated wastewater, surface water, groundwater, and seawater samples

Source: microbiolspec March 2020 vol. 8 no. 2 doi:10.1128/microbiolspec.ERV-0001-2019
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Advantages and disadvantages of currently used virus detection methods

Source: microbiolspec March 2020 vol. 8 no. 2 doi:10.1128/microbiolspec.ERV-0001-2019

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