Bacteriophages as indicators of human and animal faecal contamination in raw and treated wastewaters from Tunisia

Journal of Applied Microbiology

Volumn 118, Issue 5, 2015, Pages 1217-1225

  Yahya, M ^a   Hmaied, F ^a   Jebri, S ^a   Jofre, J ^b   Hamdi, M ^c  

^a Centre National des Sciences et Technologies Nucleaires Tunis   (Tunisia)

^b UNIVERSITY OF BARCELONA   (Spain)

^c UNIVERSITY OF CARTHAGE   (Tunisia)

Author keywords

E. coli; Bacteroides bacteriophages; F specific RNA bacteriophages; Municipal wastewater treatment plant; Slaughterhouse wastewater treatment plant; Somatic coliphages; Source tracking; Wastewater

Indexed keywords

ANIMALS; BACTERIOPHAGES; CONTAMINATION; ESCHERICHIA COLI; HEALTH RISKS; PROTOZOA; SEWAGE PUMPING PLANTS; WASTEWATER RECLAMATION; WASTEWATER TREATMENT; WATER POLLUTION; WATER TREATMENT PLANTS;

BACTEROIDES BACTERIOPHAGE; E. COLI; F-SPECIFIC RNA BACTERIOPHAGE; FECAL CONTAMINATION; MUNICIPAL WASTEWATER TREATMENT PLANTS; SLAUGHTERHOUSE WASTEWATER TREATMENT; SLAUGHTERHOUSE WASTEWATER TREATMENT PLANT; SOMATIC COLIPHAGES; SOURCE TRACKING; WASTE WATER TREATMENT PLANTS;

RNA;

AGAR; BACTERIOPHAGE; BACTERIUM; BIOMARKER; CONCENTRATION (COMPOSITION); DETECTION METHOD; FECES; HEALTH RISK; RNA; SAMPLING; TRACKING; WASTEWATER; WATER MANAGEMENT; WATER TREATMENT;

ACTIVATED SLUDGE; ARTICLE; BACTERIOPHAGE; COLIPHAGE; EFFLUENT; ESCHERICHIA COLI; FOLLOW UP; GEOGRAPHIC DISTRIBUTION; NONHUMAN; RNA PHAGE; TUNISIA; WASTE WATER MANAGEMENT; WATER CONTAMINATION; WATER POLLUTION; WATER SUPPLY; ANIMAL; CLASSIFICATION; FECES; GENETICS; HUMAN; ISOLATION AND PURIFICATION; SEWAGE; VIROLOGY; WASTE WATER; WATER MANAGEMENT;

TUNISIA;

ANIMALIA; BACTERIA (MICROORGANISMS); BACTEROIDES; ESCHERICHIA COLI;

SEWAGE; WASTE WATER;

ANIMALS; BACTERIOPHAGES; COLIPHAGES; FECES; HUMANS; SEWAGE; TUNISIA; WASTE WATER; WATER PURIFICATION;

EID: 84926525779     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12774     Document Type: Article

References (38)

1. Bertrand, I., Schiven, J.F., Sánchez, G., Wyn-Jones, P., Ottoson, J., Morin, T., Muscillo, M., Verani, M. et al. (2012) The impact of temperature on the inactivation of enteric viruses in food and water: a review. J Appl Microbiol 112, 1059-1074.
2. Blanch, A.R., Belanche-Muñoz, L., Bonjoch, X., Ebdon, J., Gantzer, C., Lucena, F., Ottoson, J., Kourtis, C. et al. (2006) Integrated analysis of established and novel microbial and chemical methods for microbial source tracking. Appl Environ Microbiol 72, 5915-5926.
3. Bouali, M., Zrafi, I., Mouna, F. and Bakhrouf, A. (2012) Pilot study of constructed wetlands for tertiary wastewater treatment using duckweed and immobilized microalgae. Afr J Microbiol Res 6, 6066-6074.
4. Chung, H., Jaykus, L.-A., Lovelance, G. and Sobsey, M.D. (1998) Bacteriophages and bacteria as indicators of enteric viruses in oysters and their harvest waters. Water Sci Technol 38, 37-44.
5. Contreras-Coll, N., Lucena, F., Mooijman, K., Havelaar, A., Pierz, V., Boque, M., Gawler, A., Höller, C. et al. (2002) Occurrence and levels of indicator bacteriophages in bathing waters throughout Europe. Water Res 36, 4963-4974.
6. Costán-Longares, A., Montemayor, M., Payán, A., Mendez, J., Jofre, J., Mujeriego, R. and Lucena, F. (2008) Microbial indicators and pathogens: removal, relationships and predictive capabilities in water reclamation facilities. Water Res 42, 4439-4448.
7. Fong, T.-T. and Lipp, E.K. (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.
8. Gantzer, C., Lucena, F., Schwartzbrod, L. and Jofre, J. (1998) Indicateurs de contamination virale du milieu hydrique: mythe ou réalité? Virologie 2, 117-125.
9. Gharbi-Khelifi, H., Ferre, V., Sdiri, K., Bertrhome, M., Fki, L., Harrath, R., Billaudell, S. and Aouni, M. (2006) Hepatitis A in Tunissia: phylogenetic analysis of hepatitis A virus from 2001 to 2004. J Virol Methods 138, 109-116.
10. Grabow, W. (2001) Bacteriophages: update on application as models for viruses in water. Water SA 27, 378-4738.
11. Grabow, W.O.K., Holtzhausen, C.S. and De Villiers, C.J. (1993) Research on Bacteriophages as Indicators of Water Quality 1990-1992. Water Research Commission Report no 321/1/93. Pretoria: Water Research Commission.
12. Hot, D., Legeay, O., Jacques, J., Gantzer, C., Caudrelier, Y., Guyard, K., Lange, M. and Andréoletti, 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.
13. IAWPRC Study Group on Health Related Water Microbiology (1991) Bacteriophages as model viruses in water quality control. Water Res 25, 529-545.
14. ISO. (1995) ISO 10705-1: Water Quality - Detection and Enumeration of Bacteriophages - part 1: Enumeration of F-Specific RNA Bacteriophages. Geneva, Switzerland: International Organisation for Standardisation.
15. ISO. (2000) ISO 10705-2: Water Quality - Detection and Enumeration of Bacteriophages - part 2: Enumeration of Somatic Coliphages. Geneva, Switzerland: International Organisation for Standardisation.
16. ISO. (2001) ISO 10705-4: Water Quality. Detection and Enumeration of Bacteriophages -Part 4: Enumeration of Bacteriophages Infecting Bacteroides fragilis. Geneva, Switzerland: International Organization for Standardization.
17. Jebri, S., Jofre, J., Barkallah, I., Saidi, M. and Hmaied, F. (2012) Presence and fate of coliphages and enteric viruses in three wastewater treatment plants effluents and activated sludge from Tunisia. Environ Sci Pollut Res Int 19, 2195-2201.
18. Jebri, S., Hmaied, F., Jofre, J., Yahya, M., Mendez, J., Barkallah, I. and Hamdi, M. (2013) Effect of gamma irradiation on bacteriophages used as viral indicators. Water Res 47, 3673-3678.
19. Jofre, J. (2007) Indicators of waterborne enteric viruses. In Human Viruses in Water (Series Perspectives in Medical Virology) ed. Bosch, A. pp. 227-249. London: Elsevier.
20. Jofre, J., Stewart, J.R. and Grabow, W. (2011) Phage methods. In Microbial Source Tracking: Methods, Applications, and Case Studies. Chapter 6. eds Hagedorn, C., Blanch, A.R. and Harwood, V.J. pp. 137-156. New York: Springer.
21. Jofre, J., Blanch, A.R., Lucena, F. and Muniesa, M. (2014) Bacteriophages infecting Bacteroides as markers for microbial source tracking. Water Res 55, 1-11.
22. Lucena, F., Duran, A.E., Moron, A., Calderon, E., Campos, C., Gantzer, C., Skraber, S. and Jofre, J. (2004) Reduction of bacterial indicators and bacteriophages infecting faecal bacteria in primary and secondary wasterwater treatments. J Appl Microbiol 97, 1069-1076.
23. Mandilara, G.D., Smeti, E.M., Mavridou, A.T., Lambiri, M.P., Vatopoulos, A.C. and Rigas, F.O. (2006) Correlation between bacterial indicators and bacteriophages in sewage and sludge. FEMS Microbiol Lett 263, 119-126.
24. Mauffret, A., Caprais, M.-P. and Gourmelon, M. (2012) Relevance of Bacteroidales and F-specific RNA bacteriophages for efficient fecal contamination tracking at the level of a catchment in France. Appl Environ Microbiol 78, 5143-5152.
25. Mc Laughlin, M.R. and Rose, J.B. (2006) Application of Bacteroides fragilis phages as an alternative indicator of sewage pollution in Tampa Bay, Florida. Estuaries Coasts 29, 246-256.
26. Mellado, V., Yáñez, M.A. and Catalán, V. (2006) Evaluation of the MicroFoss system for the analysis of Escherichia coli in water. Microbiol Res 161, 20-24.
27. Mendez, J., Audicana, A., Isern, A.J., Llanez, J., Moreno, B., Tarancón, M.L., Jofre, J. and Lucena, F. (2004) Standardised evaluation of the performance of a simple membrane filtration-elution method to concentrate bacteriophages from drinking water. J Virol Methods 117, 19-25.
28. Muniesa, M., Lucena, F., Blanch, A.R., Payán, A. and Jofre, J. (2012) Use of abundance ratios of somatic coliphages and bacteriophages of Bacteroides thetaiotaomicron GA17 for microbial source identification Original Research Article. Water Res 46, 6410-6418.
29. Nieuwstad, T.J., Mulder, E.P., Havelaar, A.H. and Van Olphen, M. (1988) Elimination of micro-organisms from wastewater by tertiary precipitation followed by filtration. Water Res 22, 1389-1397.
30. Payan, A., Ebdon, J., Taylor, H., Gantzer, C., Ottoson, J., Papageorgiou, G.T., Blanch, A.R., Lucena, F. et al. (2005) Method for isolation of bacteroides bacteriophage host strains suitable for tracking sources of fecal pollution in water. Appl Environ Microbiol 71, 5659-5662.
31. Rodríguez-Lazaro, D., Cook, N., Ruggeri, F.M., Sellwood, J., Nasser, A., Nascimento, M.S.J., D'Agostino, M., Santos, R. et al. (2012) Virus hazards from food, water and other contaminated environments. FEMS Microbiol Rev 36, 786-814.
32. Scott, T.M., Rose, J.B., Jenkins, T.M., Farrah, S.R. and Lukasik, J. (2002) Microbial source tracking: current methodology and future directions. Appl Environ Microbiol 68, 5796-5803.
33. Sdiri-Louizi, K., Gharbi-Khélifi, H., De Rougemont, A., Chouchane, S., Sakly, N., Ambert-Balay, K., Hassine, M., Guédiche, M.N. et al. (2008) Acute infantile gastroenteritis associated with human enteric viruses in Tunisia. J Clin Microbiol 46, 1349-1355.
34. Tartera, C., Bosch, A. and Jofre, J. (1988) The inactivation of bacteriophages infecting Bacteroides fragilis by chlorine treatment and UV-irradiation. FEMS Microbiol Lett 56, 313-316.
35. Trad Rais, M. and Xanthoulis, D. (1999) Amélioration de la qualité microbiologique des effluents secondaires par stockage en bassins. Biotechnol Agron Soc Environ 3, 149-157.
36. USEPA. (2004) Report to Congress. Impacts of COSs and SSOs. EPA 833-R-04-001. Washington, DC, USA: USEPA.
37. Venegas, C., Diez, H., Blanch, A.R., Juan Jofre, J. and Campos, C. (2015) Microbial source markers assessment in the Bogotá River basin (Colombia). J Wat Health 48, 1.
38. WHO. (2008) The Global Burden of Disease, 2004 Update. Geneva, Switzerland: World Health Organization. [WWW document]. URL. http://www.who.int/healthinfo/global_burden_disease/en/.