1887

Chapter 6 : Potential Use of Bacteriophages as Indicators of Water Quality and Wastewater Treatment Processes

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Potential Use of Bacteriophages as Indicators of Water Quality and Wastewater Treatment Processes, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555816629/9781555815028_Chap06-1.gif /docserver/preview/fulltext/10.1128/9781555816629/9781555815028_Chap06-2.gif

Abstract:

Viruses and phages in water and the solid compartments undergo inactivation by both natural and human-introduced physical, chemical, and biological stressors. In primary sedimentation, flocculation-aided sedimentation, activated sludge digestion, activated sludge digestion plus precipitation, and upflow anaerobic sludge blanket processes, the die-off of the microorganisms seems to play a minor role in the reduction in counts. Viruses and bacteriophages persist longer than conventional bacterial indicators in water environments, and their persistence resembles that of viruses, as shown by model experiments and by the decreases in ratios between the numbers of conventional bacterial indicators and of viruses and phages in water environments with aged pollutants, either surface water. Bacteriophages infecting enteric bacteria have been reported in drinking water that fulfill the quality criteria based on bacterial indicators. Most likely, the application of advanced mathematical models such as artificial neural networks or support vector machines will reduce the uncertainty and give much better information about relationships between indicator bacteriophages and human viruses. In conclusion, it can be stated that, though not perfect, bacteriophages infecting enteric bacteria are useful additional indicators for water quality control because of their numbers in fecally contaminated water and their outcome in water environments and water treatment plants.

Citation: Lucena F, Jofre J. 2010. Potential Use of Bacteriophages as Indicators of Water Quality and Wastewater Treatment Processes, p 103-118. In Sabour P, Griffiths M (ed), Bacteriophages in the Control of Food-and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816629.ch6

Key Concept Ranking

Nucleic Acid Amplification Techniques
0.4010958
0.4010958
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

References

/content/book/10.1128/9781555816629.ch06
1. Abad, F. X.,, R. M. Pinto,, J. M. Diez, and, A. Bosch. 1994a. Disinfection of human enteric viruses in water by copper and silver in combination with low levels of chlorine. Appl. Environ. Microbiol. 60:23772383.
2. Abad, F. X.,, R. M. Pinto, and, A. Bosch. 1994b. Survival of enteric viruses on environmental fomites. Appl. Environ. Microbiol. 60:37043710.
3. Abbaszadegan, M.,, M. LeChevalier, and, C. P. Gerba. 2003. Occurrence of viruses in US groundwaters. J. Am. Water Works Assoc. 95:107120.
4. Abbaszadegan, M.,, P. Monteiro,, N. Nwachuku,, A. Alum, and, H. Ryu. 2008. Removal of adenovirus, calicivirus, and bacteriophages by conventional drinking water treatment. J. Environ. Sci. Health A Tox. Hazard Subst. Environ. Eng. 43:171177.
5. Alcalde, L.,, G. Oron, and, M. Salgot. 2004. Evaluation of an integrated waste stabilization pond system for microbial removal, p. 103110. In P. Lens and, R. Stuetz (ed.), Young Researchers 2004. IWA Publishing, London, United Kingdom.
6. Araujo, R.,, A. Puig,, J. Lasobras,, F. Lucena, and, J. Jofre. 1997. Phages of enteric bacteria in fresh water with different levels of faecal pollution. J. Appl. Microbiol. 82:281286.
7. Armon, R., and, Y. Kott. 1996. Bacteriophages as indicators of pollution. Crit. Rev. Environ. Sci. Technol. 26:299335.
8. Arraj, A.,, J. Bohatier,, H. Laveran, and, O. Traore. 2005. Comparison of bacteriophages and enteric virus removal in pilot scale activated sludge plants. J. Appl. Microbiol. 98:516524.
9. Benyahya, M.,, H. Laveran,, J. Bohatier,, J. Senaud, and, M. Ettayebi. 1998. Comparison of elimination of bacteriophages MS2 and ϕX174 during sewage treatment by natural lagooning or activated sludges. A study on laboratory scale pilot plants. Environ. Technol. 19:513519.
10. Berg, G., and, D. Berman. 1980. Destruction by anaerobic mesophilic and thermophilic digestion of viruses and indicator bacteria indigenous to domestic sludges. Appl. Environ. Microbiol. 39:361368.
11. Blanch, A. R.,, L. Belanche-Muñoz,, X. Bonjoch,, J. Ebdon,, C. Gantzer,, F. Lucena,, J. Ottoson,, C. Kourtis,, A. Iversen,, I. Kühn,, L. Mocé-Llivina,, M. Muniesa,, J. Schwartzbrod,, S. Skraber,, G. T. Papageorgiou,, H. Taylor,, J. Wallis, and, J. Jofre. 2006. Integrated analysis of established and novel microbial and chemical methods for microbial source tracking. Appl. Environ. Microbiol. 72:59155926.
12. Bofill-Mas, S.,, N. Albiñana-Gimenez,, P. Clemente-Casares,, A. Hundesa,, J. Rodríguez-Manzano,, A. Allard,, M. Calvo, and, R. Girones. 2006. Quantification and stability of human adenovirus and polyomavirus JCPyV in wastewater matrices. Appl. Environ. Microbiol. 72: 78947896.
13. Borchardt, M. A.,, P. D. Bertz,, S. K. Spencer, and, D. A. Battigelli. 2003. Incidence of enteric viruses in groundwater from household wells in Wisconsin. Appl. Environ. Microbiol. 69:11721180.
14. Borchardt, M. A.,, N. L. Haas, and, R. J. Hunt. 2004. Vulnerability of drinking-water wells in La Crosse, Wisconsin, to enteric-virus contamination from surface water contributions. Appl. Environ. Microbiol. 70:59375946.
15. Bosch, A.,, F. Lucena, and, J. Jofre. 1986. Fate of human enteric viruses (rotaviruses and enteroviruses) after primary sedimentation. Water Sci. Technol. 18:4752.
16. Brion, G.,, C. Viswanathan,, T. R. Neelakantan,, S. Lingireddy,, R. Girones,, D. Lees,, A. Allard, and, A. Vantarakis. 2005. Artificial neural network prediction of viruses in shellfish. Appl. Environ. Microbiol. 71:52445253.
17. Burkhardt, W., III,, W. D. Watkins, and, S. R. Rippey. 1992. Seasonal effects on accumulation of microbial indicator organisms by Mercenaria mercenaria. Appl. Environ. Microbiol. 58:826831.
18. Burkhardt, W., III, and, K. R. Calci. 2000. Selective accumulation may account for shellfish-associated viral illness. Appl. Environ. Microbiol. 66:13751378.
19. Calci, K. R.,, W. Burkhardt III,, W. D. Watkins, and, S. R. Rippey. 1998. Occurrence of male-specific bacteriophages in feral and domestic animal wastes, human feces and human associated wastewaters. Appl. Environ. Microbiol. 64:50275029.
20. Campos, C.,, A. Guerrero, and, M. Cárdenas. 2002. Removal of bacterial and viral fecal indicator organisms in a waste stabilization pond system in Choconta, Cundinamarca (Colombia). Water Sci. Technol. 45:6166.
21. Chung, H., and, M. D. Sobsey. 1993. Comparative survival of indicator viruses and enteric viruses in seawater and sediment. Water Sci. Technol. 27:425429.
22. Chung, H.,, L.-A. Jaykus,, G. Lovelance, and, M. D. Sobsey. 1998. Bacteriophages and bacteria as indicators of enteric viruses in oysters and their harvest waters. Water Sci. Technol. 38:3744.
23. Clesceri, L. S.,, A. E. Greenberg, and, A. D. Eaton (ed.). 1998. Standard Methods for the Examination of Water and Wastewater, 20th ed. American Public Health Association. Washington, DC.
24. Cole, D.,, S. Long, and, M. D. Sobsey. 2003. Evaluation of F+ RNA and DNA coliphages as source-specific indicators of faecal contamination in surface waters. Appl. Environ. Microbiol. 69:65076514.
25. Contreras-Coll, N.,, F. Lucena,, K. Mooijman,, A. Havelaar,, V. Pierzo,, M. Boqué,, A. Gawler,, C. Höller,, M. Lambiri,, G. Mirolo,, B. Moreno,, M. Niemi,, R. Sommer,, B. Valentin,, A. Wiedenmann,, V. Young, and, J. Jofre. 2002. Occurrence and levels of indicator bacteriophages in bathing waters through Europe. Water Res. 36:49634974.
26. Costán-Longares, A.,, L. Mocé-Llivina,, A. Avellón,, J. Jofre, and, F. Lucena. 2008a. Occurrence and distribution of culturable enteroviruses in wastewater and surface waters of north-eastern Spain. J. Appl. Microbiol. 105:19451955.
27. Costán-Longares, A.,, M. Montemayor,, A. Payan,, J. Mendez,, J. Jofre,, R. Mujeriego, and, F. Lucena. 2008b. Microbial indicators and pathogens: removal, relationships and predictive capabilities in water reclamation facilities. Water Res. 42:44394448.
28. Coté, P.,, H. Buisson,, C. Pound, and, G. Arakaki. 1997. Immersed membrane activated sludge for the reuse of municipal wastewater. Desalination 113:189196.
29. Deborde, D. C.,, W. W. Woessner,, B. Lauerman, and, P. Ball. 1998. Coliphage prevalence in high school septic effluent and associated ground water. Water Res. 32:37813785.
30. Dee, S. W., and, J. C. Fogelman. 1992. Rates of inactivation of waterborne coliphages by monochloramine. Appl. Environ. Microbiol. 58:31363141.
31. Doré, W. J., and, D. N. Lees. 1995. Behavior of Escherichia coli and male specific bacteriophages in environmentally contaminated bivalve. Appl. Environ. Microbiol. 61:28302834.
32. Doré, W. J.,, K. Hensilwood, and, D. N. Lees. 1998. The development of management strategies for control of virological quality in oysters. Water Sci. Technol. 38:2935.
33. Duran, A. E.,, M. Muniesa,, X. Méndez,, F. Valero,, F. Lucena, and, J. Jofre. 2002. Removal and inactivation of indicator bacteriophages in fresh waters. J. Appl. Microbiol. 92:338347.
34. Duran. A. E.,, M. Muniesa,, L. Mocé-Llivina,, C. Campos,, J. Jofre, and, F. Lucena. 2003. Usefulness of different groups of bacteriophages as model micro-organisms for evaluating chlorination. J. Appl. Microbiol. 95:2937.
35. Dutka, B. J.,, G. A. Palmenteer,, S. M. Meissner,, E. M. Janzen, and, M. Sakellaris. 1990. Coliphages and bacteriophages in Canadian drinking waters. Water. Int. 15:157160.
36. Ebdon, J.,, M. Muniesa, and, H. Taylor. 2007. The application of a recently isolated strain of Bacteroides (GB-124) to identify human sources of faecal pollution in a temperate river catchment. Water Res. 41:36833690.
37. El-Abagy, M.,, B. J. Dutka, and, M. Kamel. 1988. Incidence of coliphage in potable water supplies. Appl. Environ. Microbiol. 56:16321633.
38. El-Senousy, W. M.,, S. Guix,, I. Abid,, R. M. Pintó, and, A. Bosch. 2007. Removal of astrovirus from water and sewage treatment plants, evaluated by a competitive reverse transcription PCR. Appl. Environ. Microbiol. 73:164167.
39. Engelbrecht, R. S.,, M. J. Weber,, B. L. Salter, and, C. A. Schmidt. 1980. Comparative inactivation by chlorine. Appl. Environ. Microbiol. 40:249256.
40. Enriquez, C. E.,, C. J. Hurst, and, C. P. Gerba. 1995. Survival of the enteric adenoviruses 40 and 41 in tap, sea, and waste water. Water Res. 29:25482553.
41. Farahbakhsh, K., and, D. W. Smith. 2004. Removal of coliphages in secondary effluent by microfiltration—mechanisms of removal and impact of operating parameters. Wat. Res. 38:585592.
42. Federal Register. 2006. National primary drinking water regulations: Ground Water Rule, final rule. 40 CFR parts 9, 141, and 142. Fed. Regist. 71:6557465660.
43. Feng, Y. Y.,, S. L. Ong,, J. Y. Hu,, X. L. Tan, and, W. J. Ng. 2003. Effects of pH and temperature on the survival of coliphages MS2 and Qβ. J. Ind. Microbiol. Biotechnol. 30:549552.
44. Fleisher, J.,, K. Schlafmann,, R. Otchwemah, and, K. Botzenhart. 2000. Elimination of enteroviruses, F-specific coliphages, somatic coliphages and E. coli in four sewage treatment plants of southern Germany. J. Water Suppl. Res. Technol. AQUA 49:127138.
45. Formiga-Cruz, M.,, A. K. Allard,, A.-C. Condin-Hansson,, K. Henshilwood,, B. E. Hernroth,, J. Jofre,, D. N. Lees,, F. Lucena,, M. Papapetropoulou,, R. E. Rangdale,, A. Tsibouxi,, A. Vantarakis, and, R. Girones. 2003. Evaluation of potential indicators of viral contamination in shellfish with applicability to diverse geographical areas. Appl. Environ. Microbiol. 69:15561563.
46. Gantzer, C.,, A. Maul,, J. M. Audic, and, L. Schwartzbrod. 1998. Detection of infectious enteroviruses, enterovirus genomes, somatic coliphages, and Bacteroides fragilis phages in treated wastewater. Appl. Environ. Microbiol. 64:43074312.
47. Gehr, R.,, M. Wagner,, P. Veerasubramanian, and, P. Payment. 2003. Disinfection efficiency of peracetic acid, UV and ozone after enhanced primary treatment of municipal wastewater. Water Res. 37:45734586.
48. Gerba, C. P. 1979. Failure of indicator bacteria to reflect the occurrence of enteroviruses in marine waters. Am. J. Public Health 69:11161119.
49. Gersberg, R. M.,, S. R. Lyon,, R. Brenner, and, B. V. Elkins. 1987. Fate of viruses in artificial wetlands. Appl. Environ. Microbiol. 54:731736.
50. Gironés, R.,, J. Jofre, and, A. Bosch. 1989. Natural inactivation of enteric viruses in seawater. J. Environ. Qual. 18:3439.
51. Gouvernement du Québec. 2001. Loi sur la qualité de l’environnement: règlement sur la qualité de l’eau potable, c. Q-2, r. 18.1.1. Gazette Officielle du Québec 24:3561.
52. Grabow, W. O. K.,, I. G. Middendorff, and, N. C. Basson. 1978. Role of lime treatment in the removal of bacteria, enteric viruses, and coliphages in a wastewater reclamation plant. Appl. Environ. Microbiol. 35:663669.
53. Grabow, W. O. K.,, P. Coubrough,, E. M. Nupen, and, B. W. Bateman. 1984. Evaluation of coliphages as indicators of the virological quality of sewage-polluted water. Water S. Afr. 10:714.
54. Grabow, W. O. K.,, C. S. Holtzhausen, and, C. J. De Villiers. 1993. Research on Bacteriophages as Indicators of Water Quality 1990–1992. Water Research Commission report no. 321/1/93. Water Research Commission. Pretoria, South Africa.
55. Grabow, W. O. K.,, T. E. Neubrech,, C. S. Holtzhausen, and, J. Jofre. 1995. Bacteroides fragilis and Escherichia coli bacteriophages. Excretion by humans and animals. Water Sci. Technol. 31:223230.
56. Grabow, W. O. K. 2001. Bacteriophages: update on application as models for viruses in water. Water S. Afr. 27:251268.
57. Green, D. H., and, G. D. Lewis. 1999. Comparative detection of enteric viruses in wastewaters, sediments and oysters by reverse transcription-PCR and cell culture. Water Res. 33:11951999.
58. Griffin, D. W.,, C. J. Gibson III,, E. K. Lipp,, K. Riley,, J. H. Paul III, and, J. B. Rose. 1999. Detection of viral pathogens by reverse transcriptase PCR and of microbial indicators by standard methods in the canals of the Florida Keys. Appl. Environ. Microbiol. 65:41184125.
59. Guelin, A. 1948. Etude quantitative de bacteriophages de la mer. Ann. Inst. Pasteur (Paris) 74:104112.
60. Guzmán, C.,, J. Jofre,, M. Montemayor, and, F. Lucena. 2007. Occurrence and levels of indicators and selected pathogens in different sludges and biosolids. J. Appl. Microbiol. 103:24202429.
61. Guzmán, C.,, L. Mocé-Llivina,, F. Lucena, and, J. Jofre. 2008. Evaluation of the Escherichia coli host strain (CB390) for simultaneous detection of somatic and F-specific coliphages. Appl. Environ. Microbiol. 74:531534.
62. Harakeh, S. 2006. The behaviour of viruses on disinfection by chlorine dioxide and other disinfectants in effluent. FEMS Microbiol. Lett. 44:335341.
63. Harwood, V. J.,, A. D. Levine,, T. M. Scott,, V. Chivukula,, J. Lukasik,, S. R. Farrah, and, J. B. Rose. 2005. Validity of the indicator organism paradigm for pathogen reduction in reclaimed water and public health protection. Appl. Environ. Microbiol. 71:31633170.
64. Havelaar, A. H.,, K. Furuse, and, W. M. Hogeboom. 1986. Bacteriophages and indicator bacteria in human and animal faeces. J. Appl. Bacteriol. 60:255262.
65. Havelaar, A. H. 1987. Bacteriophages as model organisms in water treatment. Microbiol. Sci. 4:362364.
66. Havelaar, A. H., and, W. M. Pot-Hogeboom. 1988. F-specific RNA bacteriophages as model viruses in water hygiene: ecological aspects. Water Sci. Technol. 20:399407.
67. Havelaar, A. H.,, M. van Olphen, and, Y. Drost. 1993. F-specific RNA bacteriophages are adequate model organisms for enteric viruses in fresh water. Appl. Environ. Microbiol. 59:29562962.
68. He, J.-W., and, S. Jiang. 2005. Quantification of enterococci and human adenoviruses in environmental samples by real-time PCR. Appl. Environ. Microbiol. 71:22502255.
69. Herath, G.,, K. Yamamoto, and, T. Urase. 1998. Mechanism of bacterial and viral transport through microfiltration membranes. Water Sci. Technol. 38:489496.
70. Hill, V. R., and, M. D. Sobsey. 1998. Microbial indicator reductions in alternative treatment systems for swine wastewater. Water Sci. Technol. 38:119122.
71. IAWPRC Study Group on Health Related Water Microbiology. 1991. Bacteriophages as model viruses in water quality control. Water Res. 25:529545.
72. International Organization for Standardization. 1995. ISO 10705-1: Water Quality. Detection and Enumeration of Bacteriophages, Part 1. Enumeration of F-specific RNA Bacteriophages. International Organization for Standardization, Geneva, Switzerland.
73. International Organization for Standardization. 2000. ISO 10705-2: Water Quality. Detection and Enumeration of Bacteriophages, Part 2. Enumeration of Somatic Coliphages. International Organization for Standardization. Geneva, Switzerland.
74. International Organization for Standardization. 2001. ISO 10705-4: Water Quality. Detection and Enumeration of Bacteriophages, Part 4. Enumeration of Bacteriophages Infecting Bacteroides fragilis. International Organization for Standardization, Geneva, Switzerland.
75. Irving, L. G., and, F. A. Smith. 1981. One-year survey of enteroviruses, adenoviruses, and reoviruses isolated from effluent at an activated-sludge purification plant. Appl. Environ. Microbiol. 41:5159.
76. Jancangelo, J. G.,, P. Loughram,, B. Petric,, D. Simpson, and, C. Mcllroy. 2003. Removal of enteric viruses and selected microbial indicators by UV irradiation of secondary effluent. Water Sci. Technol. 47:193198.
77. Jiang, S.,, R. Noble, and, W. Chu. 2001. Human adenoviruses and coliphages in urban runoff-impacted coastal waters of Southern California. Appl. Environ. Microbiol. 67:179184.
78. Jofre, J.,, M. Blasi,, A. Bosch, and, F. Lucena. 1989. Occurrence of bacteriophages infecting Bacteroides fragilis and other viruses in polluted marine sediments. Water Sci. Technol. 21:1519.
79. Jofre, J.,, E. Ollé,, F. Ribas,, A. Vidal, and, F. Lucena. 1995. Potential usefulness of bacteriophages that infect Bacteroides fragilis as model organisms for monitoring virus removal in drinking water treatment plants. Appl. Environ. Microbiol. 61:32273231.
80. Jofre, J. 2002. Bacteriophages as indicators, p. 354363. In G. Bitton (ed.), Encyclopedia of Environmental Microbiology, vol. 1. John Wiley & Sons, Inc., New York, NY.
81. Jofre, J. 2009. Is the replication of somatic coliphages in water environments significant? J. Appl. Microbiol. 106:10591069.
82. Karim, M. R.,, F. D. Manshadi,, M. M. Karpisck, and, C. P. Gerba. 2004. The persistence and removal of enteric pathogens in constructed wetlands. Water Res. 38:18311837.
83. Koch, K., and, D. Strauch. 1981. Removal of polio and parvovirus in sewage sludge by lime-treatment. Zentralbl. Bakteriol. Mikrobiol. Hyg. B 174:335347.
84. Kott, Y.,, N. Roze,, S. Sperber, and, N. Betzer. 1974. Bacteriophages as viral pollution indicators. Water Res. 8:165171.
85. Leclerc, H.,, S. Edberg,, V. Pierzo, and, J. M. Delattre. 2000. Bacteriophages as indicators of enteric viruses and public health risk in groundwaters. J. Appl. Microbiol. 88:521.
86. Levine, A. D.,, V. J. Harwood,, S. R. Farrah,, T. M. Scott, and, J. B. Rose. 2008. Pathogen and indicator organism reduction through secondary effluent filtration: implications for reclaimed water production. Water Environ. Res. 80:596608.
87. Lodder, W. J., and, A. M. de Roda Husman. 2005. Presence of noroviruses and other enteric viruses in sewage and surface water in The Netherlands. Appl. Environ. Microbiol. 71:14531461.
88. Lucena, F.,, J. Lasobras,, D. McIntosh,, M. Forcadell, and, J. Jofre. 1994. Effect of distance from the polluting focus on relative concentrations of Bacteroides fragilis phages and coliphages in mussels. Appl. Environ. Microbiol. 60:22722277.
89. Lucena, F.,, X. Mendez,, A. Morón,, E. Calderón,, C. Campos,, A. Guerrero,, M. Cárdenas,, C. Gantzer,, L. Schwartzbrod,, S. Skraber, and, J. Jofre. 2003. Occurrence and densities of bacteriophages proposed as indicators and bacterial indicators in river waters from Europe and South America. J. Appl. Microbiol. 94:808815.
90. Lucena, F.,, A. E. Duran,, A. Morón,, E. Calderón,, C. Campos,, C. Gantzer,, S. Skraber, and, J. Jofre. 2004. Reduction of bacterial indicators and bacteriophages infecting faecal bacteria in primary and secondary wastewater treatments. J. Appl. Microbiol. 97:10691076.
91. Lucena, F.,, F. Ribas,, A. E. Duran,, S. Skraber,, C. Gantzer,, C. Campos,, A. Morón,, E. Calderón, and, J. Jofre. 2006. Occurrence of bacterial indicators and bacteriophages infecting enteric bacteria in groundwater in different geographical areas. J. Appl. Microbiol. 101:96102.
92. Luther, K., and, R. Fujioka. 2004. Usefulness of monitoring tropical streams for male-specific RNA coliphages. J. Water Health 2:171181.
93. Meleg, E.,, K. Bányai,, V. Martella,, B. Jiang,, B. Kocsis,, P. Kisfali,, B. Melegh, and, G. Szücs. 2008. Detection and quantification of group C rotaviruses in communal sewage. Appl. Environ. Microbiol. 74:33943399.
94. Mendez, J.,, A. Audicana,, M. Cancer,, A. Isern,, J. Llaneza,, J. Moreno,, M. Navarro,, M. L. Tarancon,, F. Valero,, F. Ribas,, J. Jofre, and, F. Lucena. 2004. Assessment of drinking water quality using indicator bacteria and bacteriophages. J. Water Health 2:201214.
95. Meng, Q. S., and, C. P. Gerba. 1996. Comparative inactivation of enteric adenoviruses, polioviruses and coliphages by ultraviolet irradiation. Water Res. 30:26652668.
96. Mignotte-Cadiergues, B.,, A. Maul, and, L. Schwartzbrod. 1999. Comparative study of techniques used to recover viruses from residual urban sludge. J. Virol. Methods 78:7180.
97. Mignotte-Cadiergues, B.,, C. Gantzer, and, L. Schwartzbrod. 2002. Evaluation of bacteriophages during the treatment of sludge. Water Sci. Technol. 46:189194.
98. Mocé-Llivina, L.,, M. Muniesa,, H. Pimenta-Vale,, F. Lucena, and, J. Jofre. 2003. Survival of bacterial indicator species and bacteriophages after thermal treatment of sludge and sewage. Appl. Environ. Microbiol. 69:14521456.
99. Mocé-Llivina, L.,, F. Lucena, and, J. Jofre. 2005. Enteroviruses and bacteriophages in bathing waters. Appl. Environ. Microbiol. 71:68386844.
100. Montemayor, M.,, A. Costán,, F. Lucena,, J. Jofre,, J. Muñoz,, E. Dalmau,, R. Mujeriego, and, L. Sala. 2008. The combined performance of UV light and chlorine during reclaimed water disinfection. Water Sci. Technol. 57:935940.
101. Mooijman, K. A.,, Z. Ghameshlou,, M. Bahar,, J. Jofre, and, A. Havelaar. 2005. Enumeration of bacteriophages in water by different laboratories of the European Union in two interlaboratory comparison studies. J. Virol. Methods 127:6068.
102. Mossel, D. A. A. 1982. Marker (index and indicator organisms) in food and drinking water. Semantics, ecology, taxonomy and enumeration. Antoine van Leeuwenhoek 48:609611.
103. Muniain-Mujika, I.,, R. Gironés,, G. Tofiño-Quesada,, M. Calvo, and, F. Lucena. 2002. Depuration dynamics of viruses in shellfish. Int. J. Food Microbiol. 77:125133.
104. Nieuwstad, T. J.,, E. P. Mulder,, A. H. Havelaar, and, M. van Olphen. 1988. Elimination of microorganisms from wastewater by tertiary precipitation followed by filtration. Water Res. 22:13891397.
105. Nwachuku, N.,, C. P. Gerba,, A. Oswald, and, F. D. Mashadi. 2005. Comparative inactivation of adenovirus serotypes by UV light disinfection. Appl. Environ. Microbiol. 71:56335636.
106. Omura, T.,, M. Onuma,, J. Aizawa,, T. Umita, and, T. Yagi. 1989. Removal efficiency of indicator micro-organisms in sewage treatment plants. Water Sci. Technol. 21:119124.
107. Ottoson, A.,, B. Hansen,, B. Björlenius,, H. Norder, and, T. A. Stentröm. 2006. Removal of viruses, parasitic protozoa and microbial indicators in conventional and membrane processes in a wastewater pilot plant. Water Res. 40:14491457.
108. Paul, J. H.,, J. B. Rose,, S. C. Jiang,, C. A. Kellogg, and, L. Dickson. 1993. Distribution of viral abundance in the reef environment of Key Largo, Florida. Appl. Environ. Microbiol. 59:718724.
109. Payán, A.,, J. Ebdon,, H. Taylor,, C. Gantzer,, J. Ottoson,, G. T. Papageorgiou,, A. R. Blanch,, F. Lucena,, J. Jofre, and, M. Muniesa. 2005. Method for isolation of Bacteroides bacteriophage host strains suitable for tracking sources of fecal pollution in water. Appl. Environ. Microbiol. 71:56595662.
110. Payment, P.,, M. Trudel, and, R. Plante. 1985a. Elimination of viruses and indicator bacteria at each step of treatment during preparation of drinking water at seven water treatment plants. Appl. Environ. Microbiol. 49:14181482.
111. Payment, P.,, M. Tremblay, and, M. Trudel. 1985b. Relative resistance to chlorine of poliovirus and coxsackievirus isolates from environmental sources and drinking water. Appl. Environ. Microbiol. 49:981983.
112. Payment, P.,, E. Morin, and, M. Trudel. 1988. Coliphages and enteric viruses in the particulate phase of river water. Can. J. Microbiol. 34:907910.
113. Payment, P., and, E. Franco. 1993. Clostridium perfringens and somatic coliphages as indicators of the efficiency of drinking water treatment for viruses and protozoan cysts. Appl. Environ. Microbiol. 59:24182424.
114. Pillai, S. D. 2007. Bacteriophages as fecal indicators, p. 205222. In S. M. Goyal (ed.), Viruses in Foods. Springer, New York, NY.
115. Puig, A.,, N. Queralt,, J. Jofre, and, R. Araujo. 1999. Diversity of Bacteroides fragilis strains in their capacity to recover phages from human and animal wastes and from fecally polluted wastewater. Appl. Environ. Microbiol. 65:17721776.
116. Schaper, M.,, J. Jofre,, M. Uys, and, W. Grabow. 2002. Distribution of genotypes of F-specific RNA bacteriophages in human and non-human sources of faecal pollution in South Africa and Spain. J. Appl. Microbiol. 92:657667.
117. Scheuerman, P. R.,, S. R. Farrah, and, G. Bitton. 1987. Reduction of microbial indicators and viruses in a cypress strand. Water Sci. Technol. 19:539546.
118. Schijven, J. F.,, G. Medema,, A. J. Vogelaar, and, S. M. Hassanizadeh. 2000. Removal of microorganisms by deep well injection. J. Contam. Hydrol. 44:301327.
119. Schvoerer, E.,, M. Ventura,, O. Dubos,, G. Cazaux,, R. Serceau,, N. Gournier,, V. Dubois,, P. Caminade,, H. J. Fleury, and, M. E. Lafon. 2001. Qualitative and quantitative molecular detection of enteroviruses in water from bathing areas and from sewage treatment plant. Res. Microbiol. 152:179186.
120. Sedmak, G.,, D. Bina,, J. MacDonald, and, L. Couillard. 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. 71:10411050.
121. Shaffer, P. T.,, T. G. Metcalf, and, O. Sproul. 1980. Chlorine resistance of poliovirus isolates recovered from drinking water. Appl. Environ. Microbiol. 40:11151121.
122. Shang, C.,, H. M. Wong, and, G. Chen. 2005. Bacteriophage MS2 removal by submerged membrane bioreactor. Water Res. 39:42114219.
123. Shin, G. A., and, M. D. Sobsey. 2003. Reduction of Norwalk virus, poliovirus 1, and bacteriophage MS2 by ozone disinfection of water. Appl. Environ. Microbiol. 69:39753978.
124. Sinton, L. W.,, R. K. Finley, and, P. A. Lynch. 1999. Sunlight inactivation of fecal bacteriophages and bacteria in sewage-polluted seawater. Appl. Environ. Microbiol. 65:36053613.
125. Skraber, S.,, B. Gassilloud, and, C. Gantzer. 2004. Comparison of coliforms and coliphages as tools for assessment of viral contamination in river water. Appl. Environ. Microbiol. 70:36443649.
126. Sobsey, M. D. 1989. Inactivation of health-related microorganisms in water by disinfection processes. Water Sci. Technol. 21:179195.
127. Sobsey, M. D.,, R. M. Hall, and, R. L. Hazard. 1995. Comparative reductions of hepatitis A virus, enteroviruses and coliphage MS2 in miniature soil columns. Water Sci. Technol. 31:203209.
128. Sobsey, M. D.,, M. V. Yates,, F.-C. Hsu,, G. Lovelace,, D. Battigelli,, A. Margolin,, S. D. Pillai, and, N. Nwachuku. 2004. Development and evaluation of methods to detect coliphages in large volumes of water. Water Sci. Technol. 50:211217.
129. Spillman, S. K.,, F. Traub,, M. Schwyzer, and, R. Wyler. 1987. Inactivation of animal viruses during sewage sludge treatment. Appl. Environ. Microbiol. 53:20772081.
130. Stetler, R. 1984. Coliphages as indicators of enteroviruses. Appl. Environ. Microbiol. 48:668670.
131. Tartera, C., and, J. Jofre. 1987. Bacteriophages active against Bacteroides fragilis in sewage-polluted waters. Appl. Environ. Microbiol. 53:16321637.
132. Tartera, C.,, F. Lucena, and, J. Jofre. 1989. Human origin of Bacteroides fragilis bacteriophages present in the environment. Appl. Environ. Microbiol. 55:26962701.
133. Tyrrell, S. A.,, S. R. Rippey, and, W. D. Watkins. 1995. Inactivation of bacterial and viral indicators in secondary sewage effluents, using chlorine and ozone. Water Res. 29:24832490.
134. Ueda, T., and, N. J. Horan. 2000. Fate of indigenous bacteriophage in a membrane bioreactor. Water Res. 34:21512159.
135. Uemura, S.,, K. Takahashi,, A. Takaishi,, I. Machdar,, A. Ohashi, and, H. Harada. 2002. Removal of indigenous coliphages and fecal coliforms by a novel sewage treatment system consisting of UASB and DHS units. Water Sci. Technol. 46:303309.
136. U.S. Environmental Protection Agency. 2000a. Method 1601. Male-Specific (F+) and Somatic Coliphage in Water by Two-Step Enrichment Procedure. EPA report no. 821-R-00-009. U.S. Environmental Protection Agency, Washington, DC.
137. U.S. Environmental Protection Agency. 2000b. Method 1602. Male-Specific (F+) and Somatic Coliphage in Water by Single Agar Layer Procedure. EPA report no. 821-R-00-010. U.S. Environmental Protection Agency, Washington, DC.
138. U.S. Environmental Protection Agency. 2004. Guidelines for Water Reuse. EPA report no. 625-R-04-108. U.S. Environmental Protection Agency, Washington, DC.
139. U.S. Environmental Protection Agency. 2006. Environmental Technology Verification Report, Removal of Microbial Contaminants From Drinking Water, Koch Membrane Systems, Inc., HF-82-35-PMPW Ultrafiltration Membrane (PDF). EPA report no. 600-R-06-100. U.S. Environmental Protection Agency, Washington, DC.
140. U.S. Environmental Protection Agency. 2006. Ultraviolet Disinfection Guidance Manual for the Final Long Term 2 Enhanced Surface Water Treatment Rule. EPA report no. 815-R-06-007. U.S. Environmental Protection Agency, Washington, DC.
141. Vega, E.,, B. Lesikar, and, S. D. Pillai. 2003. Transport and survival of bacterial and viral tracers through submerged-flow constructed wetland and sand-filter system. Bioresourc. Technol. 89:4956.
142. Vidales, J. A.,, C. P. Gerba, and, M. M. Karpiscak. 2003. Virus removal from wastewater in a multispecies subsurface-flow constructed wetland. Water Environ. Res. 75:238245.
143. Wentsel, R. S.,, P. E. O. Neill, and, J. F. Kitchens. 1982. Evaluation of coliphage detection as a rapid indicator of water quality. Appl. Environ. Microbiol. 43:430434.
144. Williams, F. P., and, C. J. Hurst. 1988. Detection of environmental viruses in sludge. Enhancement of enterovirus plaque assay titer with 5-iodo 2’-deoxiuridine and comparison to adenoviruses and coliphage titers. Water Res. 22:847851.
145. Yates, M. V.,, C. P. Gerba, and, L. M. Kelly. 1985. Virus persistence in groundwater. Appl. Environ. Microbiol. 49:778781.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error