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Bacteriophages as Fecal Indicator Organisms

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Viruses in Foods

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7.0. References

  • Ackermann, H.W., and Nguyen, T. M., 1983, Sewage coliphages studied by electron microscopy. Appl. Environ. Microbiol. 45:1049–1059.

    CAS  Google Scholar 

  • Allwood, P. B., Malik, Y. S., Hedberg, C.W., and Goyal, S. M., 2004, Effect of temperature and sanitizers on the survival of feline calicivirus, Escherichia coli, and Fspecific coliphage MS2 on leafy salad vegetables. J. Food Prot. 67:1451–1456.

    Google Scholar 

  • Ashbolt, N. J., Grabow, W. O. K., and Snozzi, M., 2001, Indicators of microbial water. Quality, in: Water Quality: Guidelines, Standards and Health (L. Fewtrell, and J. Bartram, eds.), IWA Publishing, London, pp. 289–315.

    Google Scholar 

  • Araujo, R. A., Puig, J., Lasobras, F., Lucena, F., and Jofre, J., 1997, Phages of enteric bacteria in fresh water with different levels of fecal pollution. J. Appl. Microbiol. 82:281–286.

    Article  CAS  Google Scholar 

  • Bell, R. G., 1976, The limitations of the ratio of fecal coliforms to total coliphage as a water pollution index. Water Res. 10:745–748.

    Article  Google Scholar 

  • Berg, G., Dahling, D. R., Brown, G. A., and Berman, D., 1978, Validity of fecal coliforms, total coliforms, and fecal streptococci as indicators of viruses in chlorinated primary sewage effluents. Appl. Environ. Microbiol. 36:880–884.

    CAS  Google Scholar 

  • Brion, G. M., Meschke, J. S., and Sobsey, M.D., 2002, F-specific RNA coliphages: occurrence, types, and survival in natural waters. Water Res. 36:2419–2425.

    Article  CAS  Google Scholar 

  • Carducci, A., Gemelli, C., Cantiani, L., Casini, B., and Rovini, E., 1999, Assessment of microbial parameters as indicators of viral contamination of aerosol from urban sewage treatment plants. Lett. Appl. Microbiol. 28:207–210.

    Article  CAS  Google Scholar 

  • Castillo, G. R., Thiers, R., Dutka, B. J., and El-Shaarawi, A. H., 1988, Coliphage association with coliform indicators: a case study in chile. Toxicity Assessment: An International Journal 3:535–550.

    Article  Google Scholar 

  • Ceballos, B. S., Soares, N. E., Moraes, M. R., Catao, R. M., and Konig, A., 2003, Microbiological aspects of an urban river used for unrestricted irrigation in the semiarid region of north-east Brazil. Water Sci. Technol. 47:51–57.

    CAS  Google Scholar 

  • Chung, H., and Sobsey, M. D., 1993, Comparative survival of indicator viruses and enteric viruses in seawater and sediment. Water Sci. Technol. 27:425–429.

    Google Scholar 

  • Cole, D., Long, S. C., and Sobsey, M. D., 2003, Evaluation of F+ RNA and DNA coliphages as source-specific indicators of fecal contamination in surface waters. Appl. Environ. Microbiol. 69:6507–6514.

    Article  CAS  Google Scholar 

  • Cornax, R., Moriñigo, M.A., Paez, I.G., Muñoz, M.A., and Borrego, J. J., 1990, Application of direct plaque assay for detection and enumeration of bacteriophages of Bacteroides fragilis from contaminated-water samples. Appl. Environ. Microbiol. 56:3170–3173.

    CAS  Google Scholar 

  • Croci, L., De Medici, D., Scalfaro, C., Fiore, A., Divizia, M., Donia, D., Cosentino, A. M., Moretti, P., and Costantini, G., 2000, Determination of enteroviruses, hepatitis A virus, bacteriophages and Escherichia coli in Adriatic Sea mussels. J. Appl. Microbiol. 88:293–298.

    Article  CAS  Google Scholar 

  • Davies, C. M., Yousefi, Z., and Bavor, H. J., 2003, Occurrence of coliphages in urban stormwater and their fate in stormwater management systems. Lett. Appl. Microbiol. 37:299–303.

    Article  CAS  Google Scholar 

  • Dhillon, T. S., Dhillon, E. K. S., Chau, H.C., Li, W. K., and Tsang, A. H.C., 1976, Studies on bacteriophage distribution—virulent and temperate bacteriophage content of mammalian feces. Appl. Environ. Microbiol. 32:68–74.

    CAS  Google Scholar 

  • Dore, W. J. and Lees, D. N., 1995, Behavior of Escherichia coli and male-specific bacteriophage in environmentally contaminated bivalve molluscs before and after depuration. Appl. Environ. Microbiol. 61:2830–2834.

    CAS  Google Scholar 

  • Dowd, S. E., Widmer, K.W., and Pillai, S.D., 1997, Thermotolerant clostridia as an airborne pathogen indicator during land application of biosolids. J. Environ. Qual. 26:194–199.

    Article  CAS  Google Scholar 

  • Duran, A. E., Muniesa, M., Moce-Llivina, L., Campos, C., Jofre, J., and Lucena, F., 2003, Usefulness of different groups of bacteriophages as model micro-organisms for evaluating chlorination. J. Appl. Microbiol. 95:29–37.

    Article  CAS  Google Scholar 

  • Endley, S. E., Vega, E., Lingeng, L., Hume, M., and Pillai, S. D., 2003a, Male-specific coliphages as an additional fecal contamination indicator for screening fresh carrots. J. Food Prot. 66:88–93.

    Google Scholar 

  • Endley, S., Johnson, E., and Pillai, S. D., 2003b, A simple method to screen cilantro and parsley for fecal indicator viruses. J. Food Prot. 66:1506–1509.

    Google Scholar 

  • Espinosa, I. Y. and Pillai, S. D., 2002, Impaction-based sampler for detecting malespecific bacteriophages in bioaerosols. J. Rapid Methods Autom. Microbiol. 10:117–127.

    Google Scholar 

  • Fiksdal, L., Maki, J. S., LaCroix, S. J., and Staley, J. T., 1985, Survival and detection of Bacteroides spp., prospective indicator bacteria. Appl. Environ. Microbiol. 49:148–150.

    CAS  Google Scholar 

  • Flint, L.W., Enquist, R. M., King, V. R., Racaniello and Skalka, A. M., 2000, Principles of virology, in: Molecular Biology, Pathogenesis and Control (S. J., ed.), American Society for Microbiology, Washington, DC, p. 804.

    Google Scholar 

  • Furuse, K., 1987, Distribution of phages in the environment: general considerations, in: Phage Ecology (S. M. Goyal, C. P. Gerba, and G. Bitton, eds.), Wiley Interscience, New York, pp. 87–123.

    Google Scholar 

  • Furuse, K., Ando, A., Osawa, S., and Wantanabe, I., 1981, Distribution of ribonucleic acid coliphages in raw sewage in South and East Asia. Appl. Environ. Microbiol. 41:995–1002.

    Google Scholar 

  • Gantzer, C., Henny, J., and Schwartzbrod, L., 2002, Bacteroides fragilis and Escherichia coli bacteriophages in human faeces. Int. J. Hyg. Environ. Health 205:325–328.

    Article  Google Scholar 

  • Gerba, C. P., 1987, Phage as indicators of fecal pollution, in: Phage Ecology (S. M. Goyal, C. P. Gerba, and G. Bitton, eds.), Wiley Interscience, New York, pp. 197–210.

    Google Scholar 

  • Gerba, C. P., Goyal, S. M., LaBelle, R. L., Cech, I., and Bodgan, G. F., 1979, Failure of indicator bacteria to reflect the occurrence of enteroviruses in marine waters. Am. J. Public Health 69:1116–1119.

    Article  CAS  Google Scholar 

  • Grabow, W. O. K., Neubrech, T. E., Holtzhausen, C. S., and Jofre, J., 1995, Bacteroides fragilis and Escherichia coli bacteriophages: excretion by humans and animals. Water Sci. Technol. 31:223–230.

    Article  Google Scholar 

  • Goyal, S. M., 1983, Indicators of viruses, in: Viral Pollution of the Environment (G. Berg, ed.), CRC Press, Boca Raton, FL, pp. 211–230.

    Google Scholar 

  • Havelaar, A. H., 1993, Bacteriophages as models of human enteric viruses in the environment. ASM News, 59:614–619.

    Google Scholar 

  • Havelaar, A. H., Furuse, K., and Hogeboom, W. M., 1986, Bacteriophages and indicator bacteria in human and animal feces. J. Appl. Bacteriol. 60:255–262.

    CAS  Google Scholar 

  • Havelaar, A. H., Olphen, M., Olphen, Y.C., and van Dorst, Y.C., 1993, F-specific RNA bacteriophages are adequate model organisms for enteric viruses in fresh water. Appl. Environ. Microbiol. 59:2956–2962.

    CAS  Google Scholar 

  • Hot, D., Legeay, O., Jacques, J., Gantzer, C., Caudrelier, Y., Guyard, K., Lange, M., and Andreoletti, L., 2003, Detection of somatic phages, infectious enteroviruses and enterovirus genomes as indicators of human enteric viral pollution in surface water. Water Res. 37:4703–4710.

    Article  CAS  Google Scholar 

  • Hsu, F. C., Shieh, Y. S., van Duin, J., Beekwilder, M. J., and Sobsey, M. D., 1995, Genotyping male-specific RNA coliphages by hybridization with oligonucleotide probes. Appl. Environ. Microbiol. 61:3960–3966.

    CAS  Google Scholar 

  • Hsu, F. C., Shieh, Y. S., and Sobsey, M. D., 2002, Enteric bacteriophages as potential fecal indicators in ground beef and poultry meat. J. Food Prot. 65:93–99.

    CAS  Google Scholar 

  • Humphrey, T. J., and Martin, K., 1993, Bacteriophage as models for virus removal from Pacific oysters (Crassostrea gigas) during re-laying. Epidemiol. Infect. 111:325–335.

    Article  CAS  Google Scholar 

  • IAWPRC Study Group on Health Related Water Microbiology, 1991, Bacteriophages as model viruses in water quality control. Water Res. 25:529–545.

    Article  Google Scholar 

  • Ijzerman, M. M., Falkinham, J. O., and Hagedorn, C., 1994, A liquid, colorimetric presence-absence coliphage detection method. J. Virol. Methods 48:349.

    Article  Google Scholar 

  • ISO (International Standards Organization), 1999, Water Quality. Detection and Enumeration of Bacteriophages—Part 2. Enumeration of bacteriophages infecting Bacteroides fragilis. ISO/DIS10705-4, Geneva, Switzerland.

    Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jin, G., Englande, A. J., Bradford, H., and Jeng, H.W., 2004, Comparison of E. coli, enterococci, and fecal coliform as indicators for brackish water quality assessment. Water Environ. Res. 76:245–255.

    Article  CAS  Google Scholar 

  • Jofre, J., Olle, E., Ribas, F., Vidal, A., and Lucena, F., 1995, Potential usefulness of bacteriophages that infect Bacteroides fragilis as model organisms for monitoring virus removal in drinking water treatment plants. Appl. Environ. Microbiol. 61:3227–3231.

    CAS  Google Scholar 

  • Joklik, W. K., 1988, Virology, 3rd ed., Appleton and Lange, Norwalk, OH.

    Google Scholar 

  • Kibbey, H. J., Hagedorn, C., and McCoy, E. L., 1978, Use of fecal streptococci as indicators of pollution in soil. Appl. Environ. Microbiol. 35:711–717.

    CAS  Google Scholar 

  • Lucena, F., Lasobras, J., McIntosh, D., Forcadell, M., and Jofre, J., 1994, Effect of distance from the polluting focus on relative concentrations of Bacteroides fragilis phages and coliphages in mussels. Appl. Environ. Microbiol. 60:2272–2277.

    CAS  Google Scholar 

  • Meays, C. L., Broersma, K., Nordin, R., and Mazumdar, A., 2004, Source tracking fecal bacteria in water: a critical review of current methods. J. Environ. Mgt. 73:71–79.

    Article  Google Scholar 

  • Mena, K. D., and Pillai, S. D., 2003, Quantitative risk-based microbial standards for irrigation water quality. Abstract Annu. Mtg. Am. Soc. Microbiol. Washington, D.C.

    Google Scholar 

  • Mocé-Llivina, L., Maite Muniesa, H., Pimenta-Vale, F. L., and Jofre, J., 2003, Survival of bacterial indicator species and bacteriophages after thermal treatment of sludge and sewage. Appl. Environ. Microbiol. 69:1452–1456.

    Article  CAS  Google Scholar 

  • Muniain-Mujika, I., Calvo, M., Lucena. F., and Girones, R., 2003, Comparative analysis of viral pathogens and potential indicators in shellfish. Int. J. Food Microbiol. 25,83:75–85.

    Article  Google Scholar 

  • Muniesa, M., and Jofre, J., 2004a, Abundance in sewage of bacteriophages infecting Escherichia coli O157:H7. Methods Mol. Biol. 268:79–88.

    CAS  Google Scholar 

  • Muniesa, M., and Jofre, J., 2004b, Factors influencing the replication of somatic coliphages in the water environment. Antonie Van Leeuwenhoek J. Microbiol. 86:65–76.

    Article  Google Scholar 

  • Muniesa, M., Moce-Llivina, L., Katayama, H., and Jofre, J., 2003, Bacterial host strains that support replication of somatic coliphages. Antony Van Leeuwenhoek J. Microbiol. 83:305–315.

    Article  Google Scholar 

  • Nelson, K. L., Cisneros, B. J., Tchobanoglous, G., and Darby, J. L., 2004, Sludge accumulation, characteristics, and pathogen inactivation in four primary waste stabilization ponds in central Mexico. Water Res. 38:111–127.

    Article  CAS  Google Scholar 

  • Osawa, S., Furuse, K., and Watanabe, I., 1981, Distribution of ribonucleic acid coliphages in animals. Appl. Environ. Microbiol. 41:164–168.

    CAS  Google Scholar 

  • Ottoson, J., and Stenstrom, T. A., 2003, Faecal contamination of greywater and associated microbial risks. Water Res. 37:645–655.

    Article  CAS  Google Scholar 

  • Paul, J. H., Rose, J. B., Jiang, S. C., London, P., Xhou, X., and Kellogg, C., 1997, Coliphage and indigenous phage in Mamala Bay, Oahu, Hawaii. Appl. Environ. Microbiol. 63:133–138.

    CAS  Google Scholar 

  • Pillai, S. D., and Nwachuku, N., 2000, Field testing of coliphage methods for screening groundwater for fecal contamination. Proc. Am.Water Qual. Technol. Conf., Salt Lake City, UT.

    Google Scholar 

  • Pillai, S. D., and Nwachuku, N., 2002, Bacteriophage methodologies, in: Encyclopedia of Microbiology (G. Bitton, ed.), John Wiley & Sons, New York, pp. 374–384.

    Google Scholar 

  • Puig, A., Queralt, N., Jofre, J., and Araujo, R., 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. 65:1772–1776.

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Shah, P. C., and McCamish, J., 1972, Relative chlorine resistance of poliovirus I and coliphages f2 and T 2 in water. Appl. Microbiol. 24:658–659.

    CAS  Google Scholar 

  • Shin, G. A., and Sobsey, M. D., 2003, Reduction of Norwalk virus, poliovirus 1, and bacteriophage MS2 by ozone disinfection of water. Appl. Environ. Microbiol. 69:3975–3978.

    Article  CAS  Google Scholar 

  • Skraber, S., Gassilloud, B., and Gantzer, C., 2004, Comparison of coliforms and coliphages as tools for assessment of viral contamination in river water. Appl. Environ. Microbiol. 70:3644–3649.

    Article  CAS  Google Scholar 

  • Sobsey, M. D., Schwab, K. J., and Handzel, T. R., 1990, A simple membrane filter method to concentrate and enumerate male-specific RNA coliphages. J. Am. Water Works Assn. 82:52–59.

    Google Scholar 

  • Sobsey, M. D., Yates, M.V., Hsu, F. C., Lovelace, G., Battigelli, D., Margolin, A., Pillai, S.D., and Nwachuku, N., 2004, Development and evaluation of methods to detect coliphages in large volumes of water. Water Sci. Technol. 50:211–217.

    CAS  Google Scholar 

  • Suan, S.T., Chuen, H.Y., and Sivaborvorn, K., 1988, Southeast Asian experiences with the coliphage test. Toxicity Assessment: An International Journal 3:551–564.

    Article  Google Scholar 

  • Toranzos, G. A., Gerba, C. P., and Hanssen, H., 1988, Enteric viruses and coliphages in Latin America. Toxicity Assessment: An International Journal 3:391–394.

    Google Scholar 

  • Torrella, F., Lopez, J. P., and Banks, C. J., 2003, Survival of indicators of bacterial and viral contamination in wastewater subjected to low temperatures and freezing: application to cold climate waste stabilisation ponds, Water Sci. Technol. 48: 105–112.

    CAS  Google Scholar 

  • USEPA, 1996, ICR (Information Collection Rule). Microbial Laboratory Manual, Office of Research and Development, Washington, DC.

    Google Scholar 

  • USEPA, 2000a, Method 1601, Male-specific (F+) and somatic coliphage in water by a two-step enrichment procedure. EPA 821-R-00-009, Washington, DC.

    Google Scholar 

  • USEPA, 2000b, Method 1602, Male-specific (F+) and somatic coliphage in water by single agar layer (SAL) procedure. EPA 821-R-00-009, Washington, DC.

    Google Scholar 

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Authors and Affiliations

  1. Poultry Science Department, Institute of Food Science and Engineering, Texas A&M University, College Station, Texas, 77843

    Suresh D. Pillai

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  1. Suresh D. Pillai
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  1. Department of Veterinary Population Medicine, University of Minnesota, 1333 Gortner Avenue, St Paul, MN, 55108

    Sagar M. Goyal

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Pillai, S.D. (2006). Bacteriophages as Fecal Indicator Organisms. In: Goyal, S.M. (eds) Viruses in Foods. Food Microbiology and Food Safety. Springer, Boston, MA. https://doi.org/10.1007/0-387-29251-9_8

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