Survival of Escherichia coli and Salmonella spp. after application of sewage sludge to a Pinus radiata forest

Journal of Applied Microbiology

Volumn 103, Issue 4, 2007, Pages 1321-1331

  Horswell, J ^a   Ambrose, V ^a   Clucas, L ^b   Leckie, A ^c   Clinton, P ^c   Speir, T W ^a  

^a INSTITUTE OF ENVIRONMENTAL SCIENCE AND RESEARCH   (New Zealand)

^b LINCOLN UNIVERSITY   (New Zealand)

^c Ensis   (Australia)

Author keywords

Escherichia coli; Pathogens; Pinus radiata; Salmonella spp.; Sewage sludge

Indexed keywords

FORESTRY; HEALTH RISKS; SALMONELLA; SEWAGE SLUDGE;

BEST MANAGEMENT PRACTISE; DIE-OFF; DRY CONDITION; E. COLI; ENVIRONMENTAL AND HEALTH RISKS; PINUS RADIATA; PUBLIC ACCESS; SALMONELLA SPP; SALMONELLA SPP.; YOUNG STANDS;

ESCHERICHIA COLI;

BACTERIUM; CONIFEROUS FOREST; CONIFEROUS TREE; ENVIRONMENTAL RISK; HEALTH RISK; PATHOGEN; REGROWTH; SEASONAL VARIATION; SEWAGE; SLUDGE; SURVIVAL;

ARTICLE; AUTUMN; BACTERIAL SURVIVAL; CONTROLLED STUDY; CORRELATION ANALYSIS; DESICCATION; ESCHERICHIA COLI; FOREST; NONHUMAN; SALMONELLA; SLUDGE; SOLID WASTE; SPRING; WINTER;

ESCHERICHIA COLI; PINUS RADIATA; SALMONELLA;

EID: 34848838562     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2007.03373.x     Document Type: Article

References (45)

1. Alexander, M. (1982) Most probable number method for microbial populations. Methods of Soil Analysis, Part 2. Chemical and Microbiological Properties - Agronomy Monograph no. 9. 2nd edn. Madison, USA : ASA-SSSA.
2. Allison, L.J., Carter, P.E. Thomson-Carter, F.M. (2000) Characterization of a recurrent clonal type of Escherichia coli O157:H7 causing major outbreaks of infection in Scotland. J Clin Microbiol 38, 1632 1635.
3. American Public Health Association (APHA) (2005) 9221 Multiple-tube fermentation technique for members of the coliform group. In Standard Methods for the Examination of Water and Wastewater, 20th edn ed. Clesceri, L.S., Greenberg, A.E. Eaton, A.D. Washington, USA : American Public Health Association, the American Water Works Association and the Water Environment Federation.
4. Bruce, A.M., Pike, E.B. Fisher, W.J. (1990) A review of treatment process options to meet the EC sludge directive. J IWEM 4, 1 13.
5. Cochran, W.G. (1950) Estimation of bacterial densities by means of the "most probable number". Biometrics 6, 105 116.
6. Cools, D., Merckx, R., Vlassak, K. Verhaegen, J. (2001) Survival of E. coli and Enterococcus spp. derived from pig slurry in soils of different texture. Appl Soil Ecol 17, 53 62.
7. Cooper, R.C. Riggs, J.L. (1994) Status of pathogen analytical techniques applicable to biosolids. In Management of Water and Wastewater Solids for the 21st Century: a Global Perspective, Proceedings of WEF Specialty Conference p. 13. Alexandria VA : Water and Environmental Federation.
8. Cox, J.E. (1978) Soils and Agriculture of Part Paparua County, Canterbury, New Zealand. Soil Bureau Bulletin 34. Wellington : DSIR Soil Bureau, pp. 27 28.
9. Davies, R.D., Carrington, E.G., Gendebien, A., Aitken, M.N., Fenlon, D. Svoboda, I. (1999) A Users Guide to Research on Application of Organic Wastes to Land. Report SR 4624/3 Medmenham : WRc.
10. Department of National Health and Welfare (1977) Microbiological Quality of Drinking Water. 77-EHD-2. Ottawa, Ontario : Environmental Health Directorate, Department of National Health and Welfare.
11. Doyle, M.P. Erickson, M.C. (2006) Closing the door on the fecal coliform assay: The faecal coliform assay, the results of which have led to numerous misinterpretations over the years, may have outlived its usefulness. Microbe, April, Forum, 1, 162 163.
12. ESR (2005) New Zealand Public Health Surveillance Report Volume 3, Issue 2, June 2005. http://www.surv.esr.cri.nz/surveillance.
13. European Commission (EC) (2001) Evaluation of Sludge Treatments for Pathogen Reduction. Luxembourg : European Commission Directorate-General Environment, Study contract No. B4-3040/2001/322179/MAR/A2.
14. Gantzer, C., Gillerman, L., Kuznesov, M. Oron, G. (2001) Adsorption and survival of faecal coliforms, somatic coliphages and F-specific RNA phages in soil irrigated with wastewater. Water Sci Technol 43, 117 124.
15. Garrec, N., Picard-Bonnaud, F. Pourcher, A.M. (2003) Occurrence of Listeria sp. and L. monocytogenes in sewage sludge used for land application: effect of dewatering, liming and storage in tank on survival of Listeria species. FEMS Immunol Med Microbiol 35, 275 283.
16. Gerba, C.P. Smith, J.E. (2005) Sources of pathogenic microorganisms and their fate during land application of wastes. J Environ Qual 34, 42 48.
17. Guan, T.Y. Holley, R.A. (2003) Pathogen survival in swine manure environments and transmission of human enteric illness - a review. J Environ Qual 32, 383 392.
18. 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 Microbiolol 71, 3163 3170.
19. Hillborn, E.D., Mermin, J.H., Mshar, P.H., Hadler, J.L., Voetsch, A., Wojtkunski, C., Swartz, M., Mshar, R. et al. (1999) A multistate outbreak of Escherichia coli O157:H7 on dairy farms in Wisconsin. Appl Environ Microbiol 159, 1758 1764.
20. Hon, A. (2003) National Study of Risk Substances in Sewage-Sludge - Phase 1: Literature Review of Existing Knowledge and Identification of Expected Risk Contaminants. Prepared by CH2 M Beca Ltd for the New Zealand Ministry for the Environment.
21. Jenkins, M.B., Bowman, D.D., Fogarty, E.A. Ghiorse, W.C. (2002) Cryptosporidium parvum oocyst inactivation in three soil types at various temperatures and water potentials. Soil Biol Biochem 34, 1101 1109.
22. LeClerc, H., Mossel, D.A., Edberg, A.S.C. Struijk, C.B. (2001) Advances in the bacteriology of the coliform group: Their suitability as markers of microbial water safety. Ann Rev Microbiol 55, 201 234.
23. Lewis, D.L. Gattie, D.K. (2002) Pathogen risks from applying sewages sludge to land. Environ Sci Technol 36, 286A 293A.
24. Lewis, V.H., Jones, P.W. Redhead, D.L. (1981) The fate of bacterial pathogens in sewage treatment process. Wat Pollut Control 80, 42 53.
25. Maldonado, Y., Fiser, J.C., Nakatsu, C.H. Bhunia, A.K. (2005) Cytotoxicity potential and genotypic characterization of Escherichia coli isolates from environmental and food sources. Appl Environ Microbiol 71, 1890 1898.
26. Mills, J. Barea, H. (2003) Effect of pre-enrichment incubation time on recovery of Salmonella spp. - A Review. AgResearch Client Report CR 907.
27. Moce-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.
28. New South Wales Environmental Protection Agency (NSW EPA) (1998) Environmental Guidelines: Use and Disposal of Biosolid Products. Sydney : NSW EPA.
29. New Zealand Waste Water Association (NZ WWA) (2003) Guidelines for the Safe Application of Biosolids to Land in New Zealand. Wellington : NZWWA.
30. Palacios, M.P., Lupiola, P., Tejedor, M.T., Del-Nero, E., Pardo, A. Pita, L. (2001) Climatic effects on Salmonella survival in plant and soil irrigated with artificially inoculated wastewater: preliminary results. Water Sci Technol 43, 103 108.
31. Ponugoti, P.R., Dahab, M.F. Surampalli, R. (1997) Effects of different biosolids treatment systems on pathogen and pathogen indicator reduction. Water Environ Res 69, 1195 1206.
32. Shaban, A.M. (1999) Bacteriological evaluation of composting systems in sludge treatment. Water Sci Technol 40, 167 170.
33. Smith, S.R. (1996) Agricultural Recycling of Sewage Sludge and the Environment. Oxford, UK : CAB International.
34. Sonnenwirth, A.C. (1980) The enteric bacilli and bacteroides. In Microbiology 3rd edn. ed. Davis, B.D., Dulbecco, R., Eisen, H.N. Ginsberg, H.S. Philadelphia, Pennsylvania : Harper and Row Publishers Inc.
35. Sorber, C.A. Moore, B.E. (1987) Survival and Transport of Pathogens in Sludge-Amended Soil. A Critical Literature Review. US EPA Report No. EPA/600/2-97/028. Springfield, VA : National Technical Information Service.
36. Statistics New Zealand 2005) Demographic Trends 2004. Catalogue Number 30.001, ISSN 0113-3667.
37. United Kingdom Department of the Environment (UK DoE) (1989) (Revised 1996) Code of Practice for Agricultural Use of Sewage Sludge. London : HMSO.
38. United States Environment Protection Agency (US EPA) (1993) Part 503 - standards for use and disposal of sewage sludge. Fed Regis 58, 9387 9404.
39. Vasseur, L., Cloutier, C., Labelle, A., Duff, J-N., Beaulieu, C. Ansseau, C. (1996) Responses of indicator bacteria to forest soil amended with municipal sewage sludge from aerated and non-aerated ponds. Environ Poll 92, 67 72.
40. Whitmore, T. Robertson, L.J. (1995) The effect of sewage sludge treatment processes on oocysts of Cryptosporidium parvum. J Appl Bac 78, 34 38.
41. Wilson, I.G. (1997) Inhibition and facilitation of nucleic acid amplification. Appl Environ Microbiol 63, 3741 3751.
42. Wolstenholme, R., Dutch, J., Moffat, A.J., Bayes, C.D. Taylor, C.M.A. (1992) A Manual of Good Practice for the Use of Sewage Sludge in Forestry. London : Forestry Commission Bulletin 107, HMSO.
43. Woomer, P.L. (1994) Most probable number counts. In Methods of Soil Analysis, Part 2. Microbiological and Biochemical Properties ed. Weaver, R.W., Angle, S., Bottomly, P., Bezdicek, D., Smith, S., Tabatabai, A. Wollum, A. Madison, USA : ASA-SSSA.
44. Yeager, J.G. Ward, R.L. (1981) Effects of moisture contents on long-term survival and regrowth of bacteria in wastewater sludge. Appl Environ Microbiol 41, 1117 1122.
45. Zaleski, K.J., Josephson, K.L., Gerba, C.P. Pepper, I.L. (2005) Potential regrowth and recolonization of Salmonellae and indicators in biosolids and biosolids-amended soil. Appl Environ Microbiol 71, 3701 3708.