Occurrence and levels of indicators and selected pathogens in different sludges and biosolids

Journal of Applied Microbiology

Volumn 103, Issue 6, 2007, Pages 2420-2429

  Guzman C ^a   Jofre, J ^a   Montemayor, M ^a   Lucena, F ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Bacteria; Bacteriophages; Biosolids; Indicators; Pathogens; Sludges; Treatment

Indexed keywords

BACTERIOPHAGES; BIOLOGICAL MATERIALS; BIOSOLIDS; DEVELOPING COUNTRIES; SALMONELLA;

CRYPTOSPORIDIUM SPP; DIFFERENT TREATMENTS; HELMINTH OVA; MESOPHILIC TREATMENT; RAW SLUDGES; SALMONELLA SPP; SLUDGE; SOMATIC COLIPHAGES; SULPHITES; TREATMENT;

PATHOGENS;

BIOSOLID; COMPARATIVE STUDY; FECAL COLIFORM; PATHOGEN; PROTOZOAN; SLUDGE;

ARTICLE; BACTERIAL SPORE; BACTERIUM; BIOSOLID; CLOSTRIDIA; COLIPHAGE; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); CRYPTOSPORIDIUM; ENTEROVIRUS; FECAL COLIFORM; HELMINTH; MICROORGANISM DETECTION; NONHUMAN; OOCYST; OOCYTE; PROTOZOON; SALMONELLA; SLUDGE; SLUDGE TREATMENT; VIRUS;

BACTERIA (MICROORGANISMS); CLOSTRIDIA; CRYPTOSPORIDIUM; ENTEROVIRUS; PROTOZOA; SALMONELLA; VERMES;

EID: 36549012275     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2007.03487.x     Document Type: Article

References (61)

1. Anon. (1986) European Commission. Council directive on the protection of the environment, and in particular of the soil, when sewage sludge is used in agriculture. Directive 86/278/EEC. Off J Eur Communities L181, 6 12.
2. Anon. (1992) USEPA 625/R-92/013. Environmental Regulations and Technology Control of Pathogens and Vector Attraction in Sewage Sludge. Cincinnati, OH : United States Environmental Protection Agency.
3. Anon. (1995a) ISO 6340. Water Quality. Detection and Enumeration of Salmonella. Geneva, Switzerland : International Organization for Standardization.
4. Anon. (1995b) ISO 10705-1: Water Quality. Detection and Enumeration of Bacteriophages - Part 1: Enumeration of F-specific RNA Bacteriophages. Geneva, Switzerland : International Organization for Standardization.
5. Anon. (2000) ISO 10705-2: Water Quality. Detection and Enumeration of Bacteriophages - Part 2: Enumeration of Somatic Coliphages. Geneva, Switzerland : International Organization for Standardization.
6. Anon. (2001a) European Community. Working Document - Biological Treatment of Biowaste, 2nd draft. In the Commission web site Europa : http://europa.eu.int/comm/environment/waste/facts_en.htm (access date: 07.03.07).
7. Anon. (2001b) ISO 10705-4: Water Quality. Detection and Enumeration of Bacteriophages - Part 4: Enumeration of Bacteriophages Infecting Bacteroides Fragilis. Geneva, Switzerland : International Organization for Standardization.
8. Anon. (2003) USEPA 625/R-92/013. Control of Pathogens and Vector Attraction in Sewage Sludge. Cincinnati, OH : United States Environmental Protection Agency.
9. Berg, G. Berman, D. (1980) Destruction of anaerobic mesophilic and thermophilic digestion of viruses and indicator bacteria indigenous to domestic sludges. Appl Environ Microbiol 39, 361 368.
10. Berman, D., Berg, G. Safferman, S. (1981) A method for recovering viruses from sludge. J Virol Methods 3, 283 291.
11. Blanch, A.R., Belanche-Muñoz, L., Bonjoch, X., Ebdon, J., Gantzer, C., Lucena, F., Ottoson, J., Kourtis, C. et al. (2004) Tracking the origin of fecal pollution in surface water. An ongoing project within the European Union Research Programme. J Water Health 2, 249 260.
12. Bufton, A.W. (1959) A note on the enumeration of thermophilic sulphite-reducing bacteria. J Appl Bacteriol 22, 278 280.
13. Campbell, A.T., Robertson, L.J. Smith, H.V. (1992) Viability of Cryptosporidium parvum oocysts: correlation of in vitro excystation with inclusion or exclusion of fluorogenic vital dyes. Appl Environ Microbiol 58, 3488 3493.
14. Carrington, E.G., Pike, E.B., Auty, D. Morris, R. (1991) Destruction of faecal bacteria, enteroviruses and ova of parasites in wastewater sludge by aerobic thermophilic and anaerobic mesophilic digestion. Water Sci Technol 24, 377 380.
15. Casas, I., Palacios, G.F., Trallero, G., Cisterna, D., Freire, M.C Tenorio, A. (2001) Molecular characterization of human enteroviruses in clinical samples: comparison between VP2,VP1, and RNA polymerase regions using RT nested PCR assays and direct sequencing of products. J Med Virol 65, 138 148.
16. Chauret, C., Springthorpe, S. Sattar, S. (1999) Fate of Cryptosporidium oocysts, Giardia cysts, and microbial indicators during wastewater treatment and anaerobic sludge digestion. Can J Microbiol 45, 257 262.
17. Chesnot, T. Schwartzbrod, J. (2004) Quantitative and qualitative comparison of density-based purification methods for detection of Cryptosporidium oocyst in turbid environmental matrices. J Microbiol Methods 58, 375 386.
18. Déportes, I., Benoit-Guyod, J.L., Zmirou, D. Bouvier, M.C. (1998) Microbial disinfection capacity of municipal solid waste (MSW) composting. J Appl Microbiol 85, 238 246.
19. Entrala, E., Molina, J., Rosales, M., Sánchez, M. Mascaró, C. (2000) Cryptosporidium parvum: oocysts purification using potassium bromide discontinuous gradient. Vet Parasitol 92, 223 226.
20. Gale, P. (2005) Land application of treated sewage sludge: quantifying pathogen risks from consumption of crops. J Appl Microbiol 98, 380 396.
21. Gantzer, C., Gaspard, P., Galvez, L., Huyard, A., Dumouthier, N. Schwartzbrod, J. (2001) Monitoring of bacterial and parasitological contamination during various treatment of sludge. Water Res 35, 3763 3770.
22. Gerba, C.P., Goyal, S.M., LaBelle, R.L., Cech, I. Bodgan, G.F. (1979) Failure of indicator bacteria to reflect the occurrence of enteroviruses in marine waters. Am J Public Health 69, 1116 1119.
23. Gow, J.W., Behan, W.M.H., Clements, G.B., Woodall, C., Riding, M. Behan, P.O. (1991) Enteroviral RNA sequences detected by polymerase chain reaction in muscle of patients with postviral fatigue syndrome. Br Med J 302, 692 696.
24. Harwood, V.J., Levine, A.D., Scott, T.M., Chivukula, V., Lukasik, J., Farrah, S.R. Rose, J.B. (2005) Validity of the indicator organism paradigm for pathogen reduction in reclaimed water and public health protection. Appl Environ Microbiol 71, 3163 3170.
25. Havelaar, A.H. Pot Hogeboom, W.M. (1988) F-specific RNA bacteriophages as model viruses in water hygiene: ecological aspects. Water Sci Technol 20, 399 407.
26. Hurst, C.J. (1989) Fate of viruses during wastewater sludge treatment processes. Crit Rev Environ Control 18, 317 343.
27. IAWPRC (1991) Study group on health related water microbiology. Bacteriophages as model viruses in water quality control. Water Res 25, 529 545.
28. Jiménez, B., Maya, C., Sánchez, E., Romero, A., Lira, L. Barrios, J.A. (2002) Comparison of the quantity and quality of the microbiological content of sludge in countries with low and high content of pathogens. Water Sci Technol 46, 17 24.
29. Jofre, J., Bosch, A., Lucena, F., Gironés, R. Tartera, C (1986) Evaluation of bacteriophages active against Bacteroides fragilis as indicators of the virological quality of water. Water Sci Technol 18, 167 173.
30. Kato, S., Fogarty, E. Bowman, D. (2003) Effect of aerobic and anaerobic digestion on the viability of Cryptosporidium parvum oocysts and Ascaris suum eggs. Int J Environ Health Res 13, 169 179.
31. Katzenelson, E., Fattal, B. Hostoversky, T. (1976) Organic flocculation: an efficient second-step concentration method for the detection of viruses in tap water. Appl Environ Microbiol 32, 638 639.
32. Kott, Y., Roze, N., Sperber, S Betzer, N. (1974) Bacteriophages as viral pollution indicators. Water Res 8, 165 171.
33. Lasobras, J., Dellundé, J., Jofre, J. Lucena, F. (1999) Occurrence and levels of phages proposed as surrogate indicators of enteric viruses in different types of sludges. J Appl Microbiol 86, 723 729.
34. Lucena, F., Bosch, A., Ripoll, J. Jofre, J. (1988) Faecal pollution in Llobregat river: interrelationship of viral, bacterial and physico-chemical parameters. Water Air Soil Pollut 39, 15 25.
35. Lucena, F., Duran, A.E., Morón, A., Calderón, E., Campos, C., Gantzer, C. Skraber, S. (2004) Reduction of bacterial indicators and bacteriophages infecting faecal bacteria in primary and secondary wastewater treatments. J Appl Microbiol 97, 1069 1076.
36. McLaughlin, M.R. Rose, J.B. (2006) Application of Bacteroides fragilis phage as an alternative indicator of sewage pollution in Tampa Bay, Florida. Estuaries Coasts 29, 246 256.
37. Mignotte, B., Maul, A. Schwartzbrod, L. (1999) Comparative study of techniques used to recover viruses from residual urban sludge. J Virol Methods 78, 71 80.
38. Mignotte-Cadiergues, B., Gantzer, C. Schwartzbrod, L. (2002) Evaluation of bacteriophages during the treatment of sludge. Water Sci Technol 46, 189 194.
39. Mocé-Llivina, L., Muniesa, M., Pimenta-Vale, H., Lucena, F. Jofre, J. (2003) Survival of bacterial indicator species and bacteriophages after thermal treatment of sludge and sewage. Appl Environ Microbiol 69, 1452 1456.
40. Mocé-Llivina, L., Lucena, F. Jofre, J. (2004) A double layer plaque assay for the quantification of enteroviruses. Appl Environ Microbiol 70, 2801 2805.
41. Mocé-Llivina, L., Lucena, F. Jofre, J. (2005) Enteroviruses and bacteriophages in bathing waters. Appl Environ Microbiol 71, 6838 6844.
42. Monpoeho, S., Maul, A., Mignotte-Cadiergues, B., Schwartzbrod, L., Billaudel, S. Ferré, V. (2001) Best viral elution method available for quantification of enteroviruses in sludge by both cell culture and reverse transcription-PCR. Appl Environ Microbiol 67, 2484 2488.
43. Monpoeho, S., Maul, A., Bonnin, C., Patria, L., Ranarijaona, S., Billaudel, S. Ferré, V. (2004) Clearance of human-pathogenic viruses from sludge: study of four stabilization processes by real-time reverse transcription-PCR and cell culture. Appl Environ Microbiol 70, 5434 5440.
44. Monteleone, M.C., Furness, D., Jefferson, B. Cartmell, E. (2004) Fate of E. coli across mechanical dewatering processes. Environ Technol 25, 825 831.
45. Montemayor, M., Valero, F., Jofre, J. Lucena, F. (2005) Occurrence of Cryptosporidium spp oocysts in raw and treated sewage and river water in north-eastern Spain. J Appl Microbiol 99, 1455 1462.
46. Muniesa, M., Blanch, A.R., Lucena, F. Jofre, J. (2005) Bacteriophages may bias the outcome of bacterial enrichment cultures. Appl Environ Microbiol 71, 4269 4275.
47. Payment, P. Franco, E. (1993) Clostridium perfringens and somatic coliphages as indicators of the efficiency of drinking water treatment for viruses and protozoan cysts. Appl Environ Microbiol 59, 2418 2424.
48. Pourcher, A.M., Morand, P., Picard-Bonnaud, F., Billaudel, S., Monpoeho, S., Federighi, M., Ferré, V. Moguedet, G. (2005) Decrease of enteric micro-organisms from rural sewage sludge during their composting in straw mixture. J Appl Microbiol 99, 528 539.
49. Rimhanen-Finne, R., Vuorinen, A., Marmo, S., Malmberg, S. Hänninen, M.L. (2004) Comparative analysis of Cryptosporidium, Giardia and indicator bacteria during sewage sludge hygienization in various composting processes. 2004. Lett Appl Microbiol 38, 301 305.
50. Safferman, R.S., Rohr, M.E. Goyke, T. (1988) Assessment of recovery efficiency of beef extract reagents for concentrating viruses from municipal wastewater sludge solids by the organaic flocculation procedure. Appl Environ Microbiol 54, 309 316.
51. Schwartzbrod, J. Banas, S. (2003) Parasite contamination of liquid sludge from urban wastewater treatment plants. Water Sci Technol 47, 163 166.
52. Shaban, A.M. (1999) Bacteriological evaluation of composting systems in sludge treatment. Water Sci Technol 40, 165 170.
53. Shin, G-A., Linden, K.G., Arrowood, M.J. Sobsey, M.D. (2001) Low-pressure UV inactivation and DNA repair potential of Cryptosporidium parvum oocysts. Appl Environ Microbiol 67, 3029 3032.
54. Soares, A.C., Straub, T.M., Pepper, I.L. Gerba, C.P. (1994) Effect of anaerobic digestion on the occurrence of enteroviruses and Giardia cysts in sewage sludge. J Environ Sci Health Part A 29, 1887 1898.
55. Statistical Program (1990) S.A.S. Useŕs Guide: Statistics, edn 6.04. Gary, NC : S.A.S. Institute.
56. Straub, T.M., Pepper, I.L. Gerba, C.P. (1992) Persistence of viruses in desert soils amended with anaerobically digested sewage sludge. Appl Environ Microbiol 58, 636 641.
57. Straub, T.M., Pepper, I.L. Gerba, C.P. (1993) Hazards from pathogenic microorganisms in land-disposed sewage sludge. Rev Environ Contam Toxicol 132, 55 91.
58. Whitmore, T.N. Robertson, L.J. (1995) The effect of sewage sludge treatment processes on oocysts of Cryptosporidium parvum. J Appl Bacteriol 78, 34 38.
59. Williams, F.P. Jr. Hurst, C.J. (1988) Detection of environmental viruses in sludge: enhancement of enterovirus plaque assay titers with 5-iodo-2′-deoxiuridine and comparison to adenovirus and coliphage titers. Water Res 22, 847 851.
60. Wyer, M.D., Fleisher, J.M., Gough, J., Kay, D. Merrett, H. (1995) An investigation into parametric relationships between enterovirus and faecal indicator organisms in the coastal waters of England and Wales. Water Res 29, 1863 1868.
61. Yaziz, M.I. Lloyd, B.J. (1979) The removal of salmonellas in conventional sewage treatment processes. J Appl Bacteriol 46, 131 142.