Chapter 3.1.5 : Waterborne Enteric Viruses: Diversity, Distribution, and Detection

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Enteric viruses are a leading cause of gastroenteritis and they constitute a diverse group. The viruses commonly implicated in gastroenteritis (cases or outbreaks) are classified into the families Picornaviridae (polioviruses, enteroviruses, coxsakieviruses, and echoviruses), Adenoviridae (adenovirus 40 and 41), Caliciviridae (noroviruses, Sapporoviruses,), and Reoviridae (reoviruses). Although enteric virus infections are mainly associated with diarrhea and self-limiting gastroenteritis in healthy humans, they have also been linked to aseptic meningitis, encephalitis, myocarditis and insulin-dependent diabetes.

Currently, about 140 waterborne viruses are known to infect humans. The waterborne viruses not only show wide diversity in the illness (including diarrhea, fever, hepatitis, paralysis, meningitis, respiratory and heart diseases, they also show broad diversity in their size, shape, infection process and replication mechanisms. Most of waterborne enteric viruses have icosahedral capsid; however, the structural feature on the surface of capsids varies among different virus groups. The rotavirus capsid is composed of three concentric protein layers and the outermost layer comprises the proteins VP4 and VP7. The PV4 forms spike like structures which are responsible for virus attachment to host cell. Adenovirus has an icosahedral capsid composed of hexon the major capsid protein. In addition, capsid has penton with elongated fibers projecting out of each penton. The distal ends of these fibers have a globular "knob" which functions as the major attachment site for host cell receptors. In general, the members of enteroviruses and caliciviruses / norovirus have capsid with less pronounced surface features; but members of these groups have significantly different annotation of their capsid.

Citation: Abbaszadegan M, Alum A. 2016. Waterborne Enteric Viruses: Diversity, Distribution, and Detection, p 3.1.5-1-3.1.5-13. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch3.1.5
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Chronology of milestones in waterborne viruses. doi:10.1128/9781555818821.ch3.1.5.f1

Citation: Abbaszadegan M, Alum A. 2016. Waterborne Enteric Viruses: Diversity, Distribution, and Detection, p 3.1.5-1-3.1.5-13. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch3.1.5
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Image of FIGURE 2

Shapes and structures of virions of major groups of enteric viruses. Source: ( ) Images used with permission from Philippe Le Mercier, SIB Swiss Institute of Bioinformatics, http://viralzone.expay.org. doi:10.1128/9781555818821.ch3.1.5.f2

Citation: Abbaszadegan M, Alum A. 2016. Waterborne Enteric Viruses: Diversity, Distribution, and Detection, p 3.1.5-1-3.1.5-13. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch3.1.5
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1. Wolf AT. 2007. Shared waters: conflict and cooperation. Ann Rev Environ Resour 32 : 241 269.[CrossRef]
2. Wittfogel KA. 1956. The Hydraulic Civilizations. University of Chicago Press, Chicago, IL.
3. Delli Priscoli J. 2000. Water and civilization: using history to reframe water policy debates and to build a new ecological realism. Water Pol 1 : 623 636.[CrossRef]
4. Robbins F, Daniel T., 1997. A history of poliomyelitis, p 5–22. In Daniel TM, and Robbins EC (eds.), Polio, University of Rochester Press.
5. Trevelyan B, Smallman-Raynor M, Cliff AD. 2005. The spatial dynamics of poliomyelitis in the United States: from epidemic emergence to vaccine-induced retreat, 1910–1971. Ann Assoc Am Geographers 95 : 269 293.[CrossRef]
6. Viswanathan R. 1957. Epidemiology: infectious hepatitis in New Delhi 1955–56. Indian J Med Res 45 : 1 29.[PubMed]
7. Enquist L. 2009. Virology in the 21st century. J Virol 83 : 5296 5308.[PubMed][CrossRef]
8. Abbaszadegan M, Alum A. 2004. Microbiological contaminants and threats of concern, pp 2.1 2.12. In Water Supply Systems Security, McGraw-Hill, New York, NY.
9. Shan T, Wang C, Cui L, Yu Y, Delwart E, Zhao W, Zhu C, Lan D, Dai X, Hua X. 2010. Picornavirus salivirus/klassevirus in children with diarrhea, China. Emerg Infect Dis 16 : 1303 1305, 10.3201/eid1608.100087.[PubMed] http://dx.doi.org/10.3201/eid1608.100087
10. Hall AJ, Wikswo ME, Manikonda K, Roberts VA, Yoder JS, Gould LH. 2013. Acute gastroenteritis surveillance through the National Outbreak Reporting System, United States. Emerg Infect Dis 19 : 1305 1309, 10.3201/eid1908.130482.[CrossRef] http://dx.doi.org/10.3201/eid1908.130482
11. Griffin DW, Donaldson KA, Paul JH, Rose JB. 2003. Pathogenic human viruses in coastal waters. Clin Microbiol Rev 16 : 129 143.[PubMed][CrossRef]
12. Kocwa-Haluch R. 2001. Waterborne enteroviruses as a hazard for human health. Pol J Environ Stud 10 : 485 488.
13. Melnick JL,. 1984. Etiologic agents and their potential for causing waterborne virus diseases, pp 1–16. In Melnick JL (ed.), Enteric Viruses in Water, vol. 15. Karger, Basel, Switzerland.
14. Knipe D, Howley PM (eds.). 2013. Fields Virology, 6th ed., Lippincott Williams & Wilkins, Philadelphia, PA.
15. Hulo C, De Castro E, Masson P, Bougueleret L, Bairoch A, Xenarios I, Le Mercier P. 2011. ViralZone: a knowledge resource to understand virus diversity. Nucleic Acids Res 39 : D576 D582.[PubMed][CrossRef]
16. Piao J, Jiang J, Xu B, Wang X, Guan Y, Wu W, Liu L, Zhang Y, Huang X, Wang P. 2012. Simultaneous detection and identification of enteric viruses by PCR-mass assay. PLoS One 7 : e42251.[PubMed][CrossRef]
17. 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.[PubMed][CrossRef]
18. Finkbeiner SR, Kirkwood CD, Wang D. 2008. Complete genome sequence of a highly divergent astrovirus isolated from a child with acute diarrhea. Virol J 5 : 117.[PubMed][CrossRef]
19. Victoria JG, Kapoor A, Li L, Blinkova O, Slikas B, Wang C, Naeem A, Zaidi S, Delwart E. 2009. Metagenomic analyses of viruses in stool samples from children with acute flaccid paralysis. J Virol 83 : 4642 4651.[PubMed][CrossRef]
20. Chiu CY, Greninger AL, Kanada K, Kwok T, Fischer KF, Runckel C, Louie JK, Glaser CA, Yagi S, Schnurr DP. 2008. Identification of cardioviruses related to Theiler's murine encephalomyelitis virus in human infections. Proc Natl Acad Sci 105 : 14124 14129.[PubMed]
21. Greninger AL, Runckel C, Chiu CY, Haggerty T, Parsonnet J, Ganem D, DeRisi JL. 2009. The complete genome of klassevirus—a novel picornavirus in pediatric stool. Virol J 6 : 82.[PubMed][CrossRef]
22. Holtz LR, Finkbeiner SR, Zhao G, Kirkwood CD, Girones R, Pipas JM, Wang D. 2009. Klassevirus 1, a previously undescribed member of the family Picornaviridae, is globally widespread. Virol J 6 : 422 426.[CrossRef]
23. Jones MS, Lukashov VV, Ganac RD, Schnurr DP. 2007. Discovery of a novel human picornavirus in a stool sample from a pediatric patient presenting with fever of unknown origin. J Clin Microbiol 45 : 2144 2150.[PubMed][CrossRef]
24. Kapoor A, Victoria J, Simmonds P, Slikas E, Chieochansin T, Naeem A, Shaukat S, Sharif S, Alam MM, Angez M. 2008. A highly prevalent and genetically diversified Picornaviridae genus in South Asian children. Proc Natl Acad Sci 105 : 20482 20487.[PubMed]
25. Li L, Victoria J, Kapoor A, Blinkova O, Wang C, Babrzadeh F, Mason CJ, Pandey P, Triki H, Bahri O. 2009. A novel picornavirus associated with gastroenteritis. J Virol 83 : 12002 12006.[PubMed][CrossRef]
26. Kapoor A, Li L, Victoria J, Oderinde B, Mason C, Pandey P, Zaidi S, Delwart E. 2009. Multiple novel astrovirus species in human stool. J Gen Virol 90 : 2965 2972.[PubMed][CrossRef]
27. Kapoor A, Mehta N, Esper F, Poljsak-Prijatelj M, Quan P-L, Qaisar N, Delwart E, Lipkin WI. 2010. Identification and characterization of a new bocavirus species in gorillas. PLoS One 5 : e11948.[PubMed][CrossRef]
28. Phan TG, Kapusinszky B, Wang C, Rose RK, Lipton HL, Delwart EL. 2011. The fecal viral flora of wild rodents. PLoS Pathog 7 : e1002218.[PubMed][CrossRef]
29. Fong T-T, 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][CrossRef]
30. Li L, Kapoor A, Slikas B, Bamidele OS, Wang C, Shaukat S, Masroor MA, Wilson ML, Ndjango J-BN, Peeters M. 2010. Multiple diverse circoviruses infect farm animals and are commonly found in human and chimpanzee feces. J Virol 84 : 1674 1682.[PubMed][CrossRef]
31. Borucki MK, Allen JE, Chen-Harris H, Zemla A, Vanier G, Mabery S, Torres C, Hullinger P, Slezak T. 2013. The role of viral population diversity in adaptation of bovine coronavirus to new host environments. PLoS One 8 : e52752.[PubMed][CrossRef]
32. Wentworth DE, Holmes KV. 2001. Molecular determinants of species specificity in the coronavirus receptor aminopeptidase N (CD13): influence of N-linked glycosylation. J Virol 75 : 9741 9752.[PubMed][CrossRef]
33. Schwegmann-Wessels C, Herrler G. 2008. Identification of sugar residues involved in the binding of TGEV to porcine brush border membranes, pp 319 329. SARS and Other Coronaviruses, Springer, New York, NY.
34. Mathapati BS, Mishra N, Rajukumar K, Nema RK, Behera SP, Dubey SC. 2010. Entry of bovine viral diarrhea virus into ovine cells occurs through clathrin-dependent endocytosis and low pH-dependent fusion. In Vitro Cell Dev Biol-Anim 46 : 403 407.[PubMed]
35. Shakeel S, Seitsonen JJ, Kajander T, Laurinmäki P, Hyypiä T, Susi P, Butcher SJ. 2013. Structural and Functional analysis of coxsackievirus A9 integrin αvβ6 binding and uncoating. J Virol 87 : 3943 3951.[PubMed][CrossRef]
36. Elena SF, Carrasco P, Daròs JA, Sanjuán R. 2006. Mechanisms of genetic robustness in RNA viruses. EMBO Rep 7 : 168 173.[PubMed][CrossRef]
37. Oberste MS, Maher K, Pallansch MA. 2004. Evidence for frequent recombination within species human enterovirus B based on complete genomic sequences of all thirty-seven serotypes. J Virol 78 : 855 867.[PubMed][CrossRef]
38. Estes MK,. 2001. Rotaviruses and their replication, pp 1747 1786. In Knipe D, Howley PM (eds.), Fields Virology, 4th ed., vol. 2. Lippincott Williams & Wilkins, Philadelphia, PA.
39. 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][CrossRef]
40. Xerry J, Gallimore CI, Iturriza-Gómara M, Gray JJ. 2009. Tracking the transmission routes of genogroup II noroviruses in suspected food-borne or environmental outbreaks of gastroenteritis through sequence analysis of the P2 domain. J Med Virol 81 : 1298 1304.[PubMed][CrossRef]
41. Sukhrie FH, Beersma MF, Wong A, van der Veer B, Vennema H, Bogerman J, Koopmans M. 2011. Using molecular epidemiology to trace transmission of nosocomial norovirus infection. J Clin Microbiol 49 : 602 606.[PubMed][CrossRef]
42. Vega E, Barclay L, Gregoricus N, Williams K, Lee D, Vinjé J. 2011. Novel surveillance network for norovirus gastroenteritis outbreaks, United States. Emerg Infect Dis 17 : 1389 1395, 10.3201/eid1708.101837.[PubMed] http://dx.doi.org/10.3201/eid1708.101837
43. 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][CrossRef]
44. Sattar SA, Jason T, Bidawid S, Farber J. 2000. Foodborne spread of hepatitis A: recent studies on virus survival, transfer and inactivation. Can J Infect Dis 11 : 159.[PubMed]
45. Reynolds KA, Mena KD, Gerba CP. 2008. Risk of waterborne illness via drinking water in the United States, Revi Environ Contam Toxicol 192 : 117 158.[CrossRef]
46. Choffnes ER, Mack A. 2009. Global issues in water, sanitation, and health: workshop summary. National Academies Press, Washington D.C.
47. Rackoff LA, Bok K, Green KY, Kapikian AZ. 2013. Epidemiology and evolution of rotaviruses and noroviruses from an archival WHO Global Study in Children (1976–79) with implications for vaccine design. PloS One 8 : e59394.[PubMed][CrossRef]
48. Jalilian S, Samarbaf-Zadeh AR, Mozhgani R, Hamid S, Makvandi M, Parsa-nahad M, Pirmoradi R, Shamsi-Zadeh A. 2012. Relative frequency of norovirus infection in children suffering from gastroenteritis and Referred to Aboozar Hospital, Ahvaz, Iran. Jund J Microbiol 5 : 355 358.
49. Ferreira MSR, Xavier MdPTP, Tinga ACDC, Rose TL, Fumian TM, Fialho AM, De Assis RM, Costa FAC, De Oliveira SA, Leite JPG. 2012. Assessment of gastroenteric viruses frequency in a children's day care center in Rio De Janeiro, Brazil: a fifteen year study (1994–2008). PLoS One 7 : e33754.[PubMed][CrossRef]
50. Pham NTK, Khamrin P, Nguyen TA, Kanti DS, Phan TG, Okitsu S, Ushijima H. 2007. Isolation and molecular characterization of Aichi viruses from fecal specimens collected in Japan, Bangladesh, Thailand, and Vietnam. J Clin Microbiol 45 : 2287 2288.[PubMed][CrossRef]
51. 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][CrossRef]
52. Yamashita T, Sakae K, Tsuzuki H, Suzuki Y, Ishikawa N, Takeda N, Miyamura T, Yamazaki S. 1998. Complete nucleotide sequence and genetic organization of Aichi virus, a distinct member of the Picornaviridae associated with acute gastroenteritis in humans. J Virol 72 : 8408 8412.[PubMed]
53. Yamashita T, Kobayashi S, Sakac K, Nakata S, Chiba S, Ishihara Y, Isomura S. 1991. Isolation of cytopathic small round viruses with BS-Cl cells from patients with gastroenteritis. J Infect Dis 164 : 954 957.[PubMed][CrossRef]
54. Oh D-Y, Silva P, Hauroeder B, Diedrich S, Cardoso D, Schreier E. 2006. Molecular characterization of the first Aichi viruses isolated in Europe and in South America. Arch Virol 151 : 1199 1206.[PubMed][CrossRef]
55. Sdiri-Loulizi K, Hassine M, Gharbi-Khelifi H, Sakly N, Chouchane S, Guediche MN, Pothier P, Aouni M, Ambert-Balay K. 2009. Detection and genomic characterization of Aichi viruses in stool samples from children in Monastir, Tunisia. J Clin Microbiol 47 : 2275 2278.[PubMed][CrossRef]
56. Velazquez O, Stetler HC, Avila C, Ornelas G, Alvarez C, Hadler SC, Bradley DW, Sepúlveda J. 1990. Epidemic transmission of enterically transmitted non-A, non-B hepatitis in Mexico, 1986–1987. J Am Med Assoc 263 : 3281 3285.[CrossRef]
57. Maila HT, Bowyer SM, Swanepoel R. 2004. Identification of a new strain of hepatitis E virus from an outbreak in Namibia in 1995. J Gen Virol 85 : 89 95.[PubMed][CrossRef]
58. Wang Y, Ling R, Erker JC, Zhang H, Li H, Desai S, Mushahwar IK, Harrison TJ. 1999. A divergent genotype of hepatitis E virus in Chinese patients with acute hepatitis. J Gen Virol 80 : 169 177.[PubMed][CrossRef]
59. Yu J, Kim M, Kim D, Kim S, Lee J, Park S, Song C, Shin H, Seo K, Choi I. 2008. Prevalence of hepatitis E virus and sapovirus in post-weaning pigs and identification of their genetic diversity. Arch Virol 153 : 739 742.[PubMed][CrossRef]
60. Svraka S, Vennema H, van der Veer B, Hedlund K-O, Thorhagen M, Siebenga J, Duizer E, Koopmans M. 2010. Epidemiology and genotype analysis of emerging sapovirus-associated infections across Europe. J Clin Microbiol 48 : 2191 2198.[PubMed][CrossRef]
61. Abbaszadegan M, Lechevallier M, Gerba C. 2003. Occurrence of viruses in US groundwaters. J Am Water Works Assoc 95: 107 120.
62. Franco MA, Greenberg HB,. 2012. Epidemiologic and clinical features of rotaviruses, noroviruses, and other gastrointestinal viruses. pp. 2244 2247. In Goldman L, Schafer AI (eds.), Goldman-Cecil Medicine 25th Edition, Elsevier, Philadelphia, PA.
63. 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][CrossRef]
64. 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][CrossRef]
65. Pina S, Puig M, Lucena F, Jofre J, Girones R. 1998. Viral pollution in the environment and in shellfish: human adenovirus detection by PCR as an index of human viruses. Appl Environ Microbiol 64 : 3376 3382.[PubMed]
66. Craun GF, Brunkard JM, Yoder JS, Roberts VA, Carpenter J, Wade T, Calderon RL, Roberts JM, Beach MJ, Roy SL. 2010. Causes of outbreaks associated with drinking water in the United States from 1971 to 2006. Clin Microbiol Rev 23 : 507 528.[PubMed][CrossRef]
67. Bosch A. 2010. Human enteric viruses in the water environment: a minireview. Int Microbiol 1 : 191 196.
68. Moore M. 1982. Enteroviral disease in the United States, 1970–1979. J Infect Dis 146 : 103 108.[PubMed][CrossRef]
69. Moe C. 2002. Prospective studies of endemic waterborne disease in developing countries, pp 197 206. In Hunter PR, Waite M, Rochi E (eds.), Drinking Water and Infectious Disease: Establishing the Links. CRC Press, Boca Raton, FL.[CrossRef]
70. Boyd DR. 2001. Canada vs. the OECD: an environmental comparison University of Victoria: Eco-Research Chair of Environmental Law and Policy, University of Victoria, B.C. http://bibvir2.uqac.ca/archivage/12536745.pdf.
71. U.S. EPA. 2003. Strategically Addressing Raw Sewage Discharges Across Nation to Protect Public. EPA 300-N-03-001. Office of Enforcement and Compliance Assurance.
72. Ferguson CM, Coote BG, Ashbolt NJ, Stevenson IM. 1996. Relationships between indicators, pathogens and water quality in an estuarine system. Water Res 30 : 2045 2054.[CrossRef]
73. 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.[CrossRef]
74. Borchardt MA, Bertz PD, Spencer SK, Battigelli DA. 2003. Incidence of enteric viruses in groundwater from household wells in Wisconsin. Appl Environ Microbiol 69 : 1172 1180.[PubMed][CrossRef]
75. Berg G. 1967. Transmission of Viruses by the Water Route, Interscience Publishers, New York, 484p.
76. Hill VR, Polaczyk AL, Hahn D, Narayanan J, Cromeans TL, Roberts JM, Amburgey JE. 2005. Development of a rapid method for simultaneous recovery of diverse microbes in drinking water by ultrafiltration with sodium polyphosphate and surfactants. Appl Environ Microbiol 71 : 6878 6884.[PubMed][CrossRef]
77. Polaczyk AL, Narayanan J, Cromeans TL, Hahn D, Roberts JM, Amburgey JE, Hill VR. 2008. Ultrafiltration-based techniques for rapid and simultaneous concentration of multiple microbe classes from 100-L tap water samples. J Microbiol Methods 73 : 92 99.[PubMed][CrossRef]
78. Lambertini E, Spencer SK, Bertz PD, Loge FJ, Kieke BA, Borchardt MA. 2008. Concentration of enteroviruses, adenoviruses, and noroviruses from drinking water by use of glass wool filters. Appl Environ Microbiol 74 : 2990 2996.[PubMed][CrossRef]
79. Gerba CP, Farrah SR, Goyal SM, Wallis C, Melnick JL. 1978. Concentration of enteroviruses from large volumes of tap water, treated sewage, and seawater. Appl Environ Microbiol 35 : 540 548.[PubMed]
80. Sobsey MD, Moore RS, Glass JS. 1981. Evaluating adsorbent filter performance for enteric virus concentrations in tap water. J Am Water Works Assoc 73 : 542 548.
81. Wallis C, Henderson M, Melnick JL. 1972. Enterovirus concentration on cellulose membranes. Appl Microbiol 23 : 476 480.[PubMed]
82. Ma J-F, Naranjo J, Gerba CP. 1994. Evaluation of MK filters for recovery of enteroviruses from tap water. Appl Environ Microbiol 60 : 1974 1977.[PubMed]
83. Wen Li J, Wei Wang X, Yi Rui Q, Song N, Guang Zhang F, Chuan Ou Y, Huan Chao F. 1998. A new and simple method for concentration of enteric viruses from water. J Virol Meth 74 : 99 108.[CrossRef]
84. Haramoto E, Katayama H, Ohgaki S. 2004. Detection of noroviruses in tap water in Japan by means of a new method for concentrating enteric viruses in large volumes of freshwater. Appl Environ Microbiol 70 : 2154 2160.[PubMed][CrossRef]
85. Sobsey MD, Glass JS. 1980. Poliovirus concentration from tap water with electropositive adsorbent filters. Appl Environ Microbiol 40 : 201 210.[PubMed]
86. 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][CrossRef]
87. Wommack K, Hill R, Colwell R. 1995. A simple method for the concentration of viruses from natural water samples. J Microbiol Meth 22 : 57 67.[CrossRef]
88. Olszewski J, Winona L, Oshima KH. 2005. Comparison of 2 ultrafiltration systems for the concentration of seeded viruses from environmental waters. Can JMicrobiol 51 : 295 303.[CrossRef]
89. Winona L, Ommani A, Olszewski J, Nuzzo J, Oshima K. 2001. Efficient and predictable recovery of viruses from water by small scale ultrafiltration systems. Can J Microbiol 47 : 1033 1041.[PubMed][CrossRef]
90. Abbaszadegan M, Alum A, Abbaszadegan H, Stout V. 2011. Cell surface display of poliovirus receptor on Escherichia coli, a novel method for concentrating viral particles in water. Appl Environ Microbiol 77 : 5141 5148.[PubMed][CrossRef]
91. Abbaszadegan M, Huber M, Gerba CP, Pepper I. 1993. Detection of enteroviruses in groundwater with the polymerase chain reaction. Appl Environ Microbiol 59 : 1318 1324.[PubMed]
92. Abbaszadegan M, Stewart P, LeChevallier M. 1999. A strategy for detection of viruses in groundwater by PCR. Appl Environ Microbiol 65 : 444 449.[PubMed]
93. Green DH, Lewis GD. 1999. Comparative detection of enteric viruses in wastewaters, sediments and oysters by reverse transcription-PCR and cell culture. Water Res 33 : 1195 1200.[CrossRef]
94. U.S. EPA. 1992. Technical support document for Part 503 pathogen and vector attraction reduction requirements in sewage sludge. NTIS No. PB89-136618. National Technical Information Service, Springfield, VA.
95. Abbaszadegan M. 2001. Advanced detection of viruses and protozoan parasites in water. Rev Biol Biotech 1 : 21 26.
96. Schneider-Schaulies J. 2000. Cellular receptors for viruses: links to tropism and pathogenesis. J Gen Virol 81 : 1413 1429.[PubMed][CrossRef]
97. Berg G, Saffermann R, Dahling D, Berman D, Hurst C. 1984. USEPA Manual of Methods for Virology. U.S. Environmental Protection Agency. Cincinnati, OH.
98. Dahling DR, Wright BA. 1984. Processing and transport of environmental virus samples. Appl Environ Microbiol 47 : 1272 1276.[PubMed]
99. Dahling DR, Wright BA. 1986. Recovery of viruses from water by a modified flocculation procedure for second-step concentration. Appl Environ Microbiol 51 : 1326 1331.[PubMed]
100. Benton WH, Hurst CJ. 1986. Evaluation of mixed cell types and 5-iodo-2′-deoxyuridine treatment upon plaque assay titers of human enteric viruses. Appl Environmen Microbiol 51 : 1036 1040.
101. Smith EM, Gerba CP. 1982. Development of a method for detection of human rotavirus in water and sewage. Appl Environ Microbiol 43 : 1440 1450.[PubMed]
102. Whitaker A, Hayward C. 1984. The characterization of three monkey kidney cell lines. Dev Biol Stand 60 : 125 131.
103. Chonmaitree T, Ford C, Sanders C, Lucia H. 1988. Comparison of cell cultures for rapid isolation of enteroviruses. J Clin Microbiol 26 : 2576 2580.[PubMed]
104. Brashear DA, Ward RL. 1982. Comparison of methods for recovering indigenous viruses from raw wastewater sludge. Appl Environ Microbiol 43 : 1413 1418.[PubMed]
105. U.S. EPA. 1995. Part 503 implementation guidance. U.S. EPA, Washington, DC.
106. Chapron CD, Ballester NA, Fontaine JH, Frades CN, Margolin AB. 2000. Detection of astroviruses, enteroviruses, and adenovirus types 40 and 41 in surface waters collected and evaluated by the information collection rule and an integrated cell culture-nested PCR procedure. Appl Environ Microbiol 66 : 2520 2525.[PubMed][CrossRef]
107. Sedmak G, Bina D, MacDonald J. 2003. Assessment of an enterovirus sewage surveillance system by comparison of clinical isolates with sewage isolates from Milwaukee, Wisconsin, collected August 1994 to December 2002. Appl Environ Microbiol 69 : 7181 7187.[PubMed][CrossRef]
108. Sedmak G, Bina D, MacDonald J, Couillard L. 2005. Nine-year study of the occurrence of culturable viruses in source water for two drinking water treatment plants and the influent and effluent of a wastewater treatment plant in Milwaukee, Wisconsin (August 1994 through July 2003). Appl Environ Microbiol 71 : 1042 1050.[PubMed][CrossRef]
109. Vivier J, Ehlers M, Grabow W. 2004. Detection of enteroviruses in treated drinking water. Water Res 38 : 2699 2705.[PubMed][CrossRef]
110. Duizer E, Schwab KJ, Neill FH, Atmar RL, Koopmans MP, Estes MK. 2004. Laboratory efforts to cultivate noroviruses. J Gen Virol 85 : 79 87.[PubMed][CrossRef]
111. Wobus CE, Karst SM, Thackray LB, Chang K-O, Sosnovtsev SV, Belliot G, Krug A, Mackenzie JM, Green KY, Virgin IV HW. 2004. Replication of norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol 2 : e432.[PubMed][CrossRef]
112. Papafragkou E, Hewitt J, Park GW, Greening G, Vinjé J. 2013. Challenges of culturing human norovirus in three-dimensional organoid intestinal cell culture models. PLoS One 8 : e63485.[PubMed][CrossRef]
113. Alum A, Shieh, YC Sun, Y, Stewart, DS, Reineke, KF, Tortorello ML. 2012. Method development for rapid concentration of noroviruses in water and tomato eluate. Institute for Food Safety and Health, Annual Review, Bedford Park, IL.
114. Straub TM, Bartholomew RA, Valdez CO, Valentine NB, Dohnalkova A, Ozanich RM, Bruckner-Lea CJ, Call DR. 2011. Human norovirus infection of Caco-2 cells grown as a 3-dimensional tissue structure. J Water and Health 9 : 225.[CrossRef]
115. Straub TM,, zu Bentrup KH, Orosz Coghlan P, Dohnalkova A, Mayer BK, Bartholomew RA, Valdez CO, Bruckner-Lea CJ, Gerba CP, Abbaszadegan M, Nickerson CA. 2007. In vitro cell culture infectivity assay for human noroviruses. Emerg Infect Dis 13 : 396 403.[PubMed]
116. Straub TM, Hutchison JR, Bartholomew RA, Valdez CO, Valentine NB, Dohnalkova A, Ozanich RM, Bruckner-Lea CJ. 2013. Defining cell culture conditions to improve human norovirus infectivity assays. Water Sci Technol 67 : 863 868.[PubMed][CrossRef]
117. 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][CrossRef]
118. Parker J, Chang TY, Meschke J. 2011. Amplification of viral RNA from drinking water using TransPlex™ whole-transcriptome amplification. J Appl Microbiol 111 : 216 223.[PubMed][CrossRef]
119. Wong K, Onan BM, Xagoraraki I. 2010. Quantification of enteric viruses, pathogen indicators, and salmonella bacteria in class B anaerobically digested biosolids by culture and molecular methods. Appl Environ Microbiol 76 : 6441 6448.[PubMed][CrossRef]
120. Brown B, Oberste MS, Maher K, Pallansch MA. 2003. Complete genomic sequencing shows that polioviruses and members of human enterovirus species C are closely related in the noncapsid coding region. J Virol 77 : 8973 8984.[PubMed][CrossRef]
121. Oberste MS, Peñaranda S, Maher K, Pallansch MA. 2004. Complete genome sequences of all members of the species Human enterovirus A. J Gen Virol 85 : 1597 1607.[PubMed][CrossRef]
122. DeLeon R, Shieh C, Baric RS, Sobsey MD. 1990. Detection of enteroviruses and hepatitis A virus in environmental samples by gene probes and polymerase chain reaction, pp 833 853. In Advances in Water Analysis and Treatment. Proceedings, 1989 Water Quality Technology Conference. American Water Works Association, Denver, CO.
123. Xu W, McDonough MC, Erdman DD. 2000. Species-specific identification of human adenoviruses by a multiplex PCR assay. J Clin Microbiol 38 : 4114 4120.[PubMed]
124. Dierssen U, Rehren F, Henke-Gendo C, Harste G, Heim A. 2008. Rapid routine detection of enterovirus RNA in cerebrospinal fluid by a one-step real-time RT-PCR assay. J Clin Virol 42 : 58 64.[PubMed][CrossRef]
125. Schwab KJ, De Leon R, Baric RS, Sobsey MD. 1991 Detection of rotaviruses, enteroviruses, and hepatitis A virus by reverse transcriptase-polymerase chain reaction, p 475–491. In Advances in water analysis and treatment. Proceedings of the AWWA Water Quality Technology Conference, Orlando, FL, 10 to 14 November 1991 American Water Works Association, Denver, CO.
126. Ouyang X, Zhang H, Bayston TA, Archard LC. 1995. Detection of coxsackievirus B3 RNA in mouse myocarditis by nested polymerase chain reaction. Clin Diagn Virol 3 : 233 245.[PubMed][CrossRef]
127. Kageyama T, Kojima S, Shinohara M, Uchida K, Fukushi S, Hoshino FB, Takeda N, Katayama K. 2003. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J Clin Microbiol 41 : 1548 1557.[PubMed][CrossRef]
128. Laverick M, Wyn-Jones A, Carter M. 2004. Quantitative RT-PCR for the enumeration of noroviruses (Norwalk-like viruses) in water and sewage. Lett Appl Microbiol 39 : 127 136.[PubMed][CrossRef]
129. Jothikumar N, Lowther JA, Henshilwood K, Lees DN, Hill VR, Vinjé J. 2005. Rapid and sensitive detection of noroviruses by using TaqMan-based one-step reverse transcription-PCR assays and application to naturally contaminated shellfish samples. Appl Environ Microbiol 71 : 1870 1875.[PubMed][CrossRef]
130. Jääskeläinen AJ, Maunula L. 2006. Applicability of microarray technique for the detection of noro-and astroviruses. J Virol Meth 136 : 210 216.[CrossRef]
131. Connelly JT, Kondapalli S, Skoupi M, Parker JS, Kirby BJ, Baeumner AJ. 2012. Micro-total analysis system for virus detection: microfluidic pre-concentration coupled to liposome-based detection. Anal Bioanal Chem 402 : 315 323.[PubMed][CrossRef]
132. Liu Y, Xu Z-q, Zhang Q, Jin M, Yu J-m, Li J-s, Liu N, Cui S-x, Kong X-y, Wang H. 2012. Simultaneous detection of seven enteric viruses associated with acute gastroenteritis by a multiplexed Luminex-based assay. J Clin Microbiol 50 : 2384 2389.[PubMed][CrossRef]
133. Rohayem J, Berger S, Juretzek T, Herchenröder O, Mogel M, Poppe M, Henker J, Rethwilm A. 2004. A simple and rapid single-step multiplex RT-PCR to detect norovirus, astrovirus and adenovirus in clinical stool samples. J Virol Meth 118 : 49 59.[CrossRef]
134. Formiga-Cruz M, Hundesa A, Clemente-Casares P, Albiñana-Gimenez N, Allard A, Girones R. 2005. Nested multiplex PCR assay for detection of human enteric viruses in shellfish and sewage. J Virolo Meth 125 : 111 118.[CrossRef]
135. Blinkova O, Victoria J, Li Y, Keele BF, Sanz C, Ndjango J-BN, Peeters M, Travis D, Lonsdorf EV, Wilson ML. 2010. Novel circular DNA viruses in stool samples of wild-living chimpanzees. J Gen Virol 91 : 74 86.[PubMed][CrossRef]
136. Canuti M, Eis-Huebinger AM, Deijs M, de Vries M, Drexler JF, Oppong SK, Mueller MA, Klose SM, Wellinghausen N, Cottontail VM. 2011. Two novel parvoviruses in frugivorous new and old world bats. PLoS One 6 : e29140.[PubMed][CrossRef]
137. Donaldson EF, Haskew AN, Gates JE, Huynh J, Moore CJ, Frieman MB. 2010. Metagenomic analysis of the viromes of three North American bat species: viral diversity among different bat species that share a common habitat. J Virol 84 : 13004 13018.[PubMed][CrossRef]
138. Ge X, Li J, Peng C, Wu L, Yang X, Wu Y, Zhang Y, Shi Z. 2011. Genetic diversity of novel circular ssDNA viruses in bats in China. J Gen Virol 92 : 2646 2653.[PubMed][CrossRef]
139. Kapoor A, Simmonds P, Dubovi EJ, Qaisar N, Henriquez JA, Medina J, Shields S, Lipkin WI. 2011. Characterization of a canine homolog of human aichivirus. J Virol 85 : 11520 11525.[PubMed][CrossRef]
140. Li L, Pesavento PA, Shan T, Leutenegger CM, Wang C, Delwart E. 2011. Viruses in diarrhoeic dogs include novel kobuviruses and sapoviruses. J Gen Virol 92 : 2534 2541.[PubMed][CrossRef]
141. Li L, Shan T, Wang C, Côté C, Kolman J, Onions D, Gulland FM, Delwart E. 2011. The fecal viral flora of California sea lions. J Virol 85 : 9909 9917.[PubMed][CrossRef]
142. Li L, Victoria JG, Wang C, Jones M, Fellers GM, Kunz TH, Delwart E. 2010. Bat guano virome: predominance of dietary viruses from insects and plants plus novel mammalian viruses. J Virol 84 : 6955 6965.[PubMed][CrossRef]
143. Reuter G, Nemes C, Boros Á, Kapusinszky B, Delwart E, Pankovics P. 2012. Astrovirus in wild boars ( Sus scrofa) in Hungary. Arch Virol 157 : 1143 1147.[PubMed][CrossRef]
144. Reuter G, Pankovics P, Delwart E, Boros Á. 2012. Identification of a novel astrovirus in domestic sheep in Hungary. Arch Virol 157 : 323 327.[PubMed][CrossRef]
145. Kapoor A, Slikas E, Simmonds P, Chieochansin T, Naeem A, Shaukat S, Alam MM, Sharif S, Angez M, Zaidi S. 2009. A newly identified bocavirus species in human stool. J Infect Dis 199 : 196 200.[PubMed][CrossRef]
146. Rock C, Alum A, Abbaszadegan M. 2010. PCR inhibitor levels in concentrates of biosolid samples predicted by a new method based on excitation-emission matrix spectroscopy. Appl Environ Microbiol 76 : 8102 8109.[PubMed][CrossRef]
147. Sano D, Fukushi K, Yoshida Y, Omura T. 2003. Detection of enteric viruses in municipal sewage sludge by a combination of the enzymatic virus elution method and RT-PCR. Water Res 37 : 3490 3498.[PubMed][CrossRef]
148. Enterovirus R, Real-Time ST. 2000. RT-PCR. Biotechniques 29 : 88 93.[PubMed]
149. Kopecka H, Dubrou S, Prevot J, Marechal J, Lopez-Pila J. 1993. Detection of naturally occurring enteroviruses in waters by reverse transcription, polymerase chain reaction, and hybridization. Appl Environ Microbiol 59 : 1213 1219.[PubMed]
150. 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.[PubMed]
151. Tsai Y-L, Sobsey M, Sangermano L, Palmer C. 1993. Simple method of concentrating enteroviruses and hepatitis A virus from sewage and ocean water for rapid detection by reverse transcriptase-polymerase chain reaction. Appl Environ Microbiol 59 : 3488 3491.[PubMed]
152. U.S. EPA. 2004. Quality Assurance/Quality Control Guidance for Laboratories Performing PCR Analyses on Environmental Samples. EPA 815-B-04-001. U.S. EPA.
153. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL. 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55 : 611 622.[PubMed][CrossRef]


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Genomic and morphological characteristics of major enteric viruses

Citation: Abbaszadegan M, Alum A. 2016. Waterborne Enteric Viruses: Diversity, Distribution, and Detection, p 3.1.5-1-3.1.5-13. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch3.1.5
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The relative frequencies (%) of rotaviruses and noroviruses detected in different countries

Citation: Abbaszadegan M, Alum A. 2016. Waterborne Enteric Viruses: Diversity, Distribution, and Detection, p 3.1.5-1-3.1.5-13. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch3.1.5
Generic image for table

Pathobiology and prevalence of major waterborne enteric viruses

Citation: Abbaszadegan M, Alum A. 2016. Waterborne Enteric Viruses: Diversity, Distribution, and Detection, p 3.1.5-1-3.1.5-13. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch3.1.5
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Comparison of different types of filters used to concentrate waterborne viruses

Citation: Abbaszadegan M, Alum A. 2016. Waterborne Enteric Viruses: Diversity, Distribution, and Detection, p 3.1.5-1-3.1.5-13. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch3.1.5
Generic image for table

Recovery efficiency of enteric viruses from water

Citation: Abbaszadegan M, Alum A. 2016. Waterborne Enteric Viruses: Diversity, Distribution, and Detection, p 3.1.5-1-3.1.5-13. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch3.1.5
Generic image for table

Comparison of common methods for the detection of enteric viruses from environmental sources

Citation: Abbaszadegan M, Alum A. 2016. Waterborne Enteric Viruses: Diversity, Distribution, and Detection, p 3.1.5-1-3.1.5-13. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch3.1.5
Generic image for table

Major groups of enteric viruses and their receptors

Citation: Abbaszadegan M, Alum A. 2016. Waterborne Enteric Viruses: Diversity, Distribution, and Detection, p 3.1.5-1-3.1.5-13. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch3.1.5

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