Register      Login
Soil Research Soil Research Society
Soil, land care and environmental research
RESEARCH ARTICLE

Survival of pathogenic and indicator bacteria in biosolids applied to agricultural land

G. J. Eamens A D , A. M. Waldron A B and P. J. Nicholls A C
+ Author Affiliations
- Author Affiliations

A NSW Department of Primary Industries, Elizabeth Macarthur Agricultural Institute, PMB 8, Camden, NSW 2570, Australia.

B Present address: University of Sydney, PMB 3, Camden, NSW 2570, Australia.

C Present address: PO Box 20, Menangle, NSW 2568, Australia.

D Corresponding author. Email: graeme.eamens@dpi.nsw.gov.au

Australian Journal of Soil Research 44(7) 647-659 https://doi.org/10.1071/SR06015
Submitted: 2 February 2006  Accepted: 16 August 2006   Published: 20 October 2006

Abstract

Concentrations of surviving Escherichia coli, Clostridium perfringens, and Salmonella spp. were determined temporally in mechanically dewatered biosolids derived from anaerobic–mesophilic digestion and applied to agricultural land. Following applications in different seasons, repeated assessments of bacterial concentrations in biosolid clumps, using most-probable-number (MPN) techniques, found sustained high levels of these bacteria. Bacterial concentrations were often well above soil background levels at 6 months, and in some cases 11–12 months, after land application. Survival in surface-applied biosolids was similar to that for biosolids incorporated into the soil, and between application rates of 10 or 30 dry t/ha. Salmonella concentrations in applied biosolids were not predicted from, and could exceed those of, the indicator organism E. coli. Multiple plot analyses indicated regrowth of E. coli and Salmonella can occur within biosolids, up to several months after application. However, Salmonella serovars likely to pose a significant risk to animal health were not detected among isolates from the dewatered biosolids. Reduced accessibility for grazing livestock by soil incorporation, together with the time taken for normal pasture establishment practices, and the limited pathogenicity of the vast majority of salmonellae present in biosolids may significantly reduce the risk of spread of these organisms to the human food chain.

Additional keywords: sewage sludge, survival, splines.


Acknowledgments

This work was financially supported by the Sydney Water Corporation. The technical support of Kiley Seymour and Jocelyn Gonsalves during sample collection and bacteriological procedures is gratefully acknowledged. Dr Idris Barchia provided valuable assistance in the presentation of biometrical data.


References


Anon. (1998) ‘Human Annual Report 1997.’ p. 15. (National Enteric Pathogens Surveillance Scheme, Australia)

Anon. (1999 a) ‘Human Annual Report 1998.’ p. 15. (National Enteric Pathogens Surveillance Scheme, Australia)

Anon. (1999 b) ‘Non-human Annual Report 1998.’ p. 14. (National Enteric Pathogens Surveillance Scheme, Australia)

Anon. (2000 a) ‘Annual Report 2000, Australian Salmonella Reference Centre.’ p. 8. (Institute of Medical and Veterinary Science, Infectious Diseases Laboratories: Adelaide, S. Aust.)

Anon. (2000 b) ‘Human Annual Report 1999.’ p. 13. (National Enteric Pathogens Surveillance Scheme, Australia)

Anon. (2004) ‘Annual Report 2004.’ Australian Salmonella Reference Centre, p. 7. (Institute of Medical and Veterinary Science, Infectious Diseases Laboratories: Adelaide, S. Aust.)

Barker J, Brown MRW (1994) Trojan horses of the microbial world: protozoa and the survival of bacterial pathogens in the environment. Microbiology 140, 1253–1259.
PubMed |
open url image1

Barker J, Humphrey TJ, Brown MRW (1999) Survival of Escherichia coli 0157 in a soil protozoan: implications for disease. FEMS Microbiology Letters 173, 291–295.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Blaser MJ, Newman LS (1982) A review of human salmonellosis: I. Infective dose. Reviews of Infectious Diseases 4, 1096–1106.
PubMed |
open url image1

Burge WD, Enkiri NK, Hussong D (1987) Salmonella regrowth in compost as influenced by substrate. Microbial Ecology 14, 243–253.
Crossref | GoogleScholarGoogle Scholar | open url image1

Charman PEV (1991) Appendix II Identification of soil groups. In ‘Soils—their properties and management’. p. 329. (Sydney University Press/Oxford University Press: South Melbourne, Vic.)

Eamens GJ , Lavis AM , Ross AD (1996) Survival of pathogenic and indicator bacteria in biosolids applied to agricultural land. In ‘Biosolids Research in NSW, Proceedings of the Biosolids Summit’. (Eds GJ Osborne, RL Parkin, DL Michalk, AM Grieve) pp. 129–138. (NSW Agriculture, Organic Waste Recycling Unit: Rydalmere, NSW)

Edmonds RL (1976) Survival of coliform bacteria in sewage sludge applied to a forest clearcut and potential movement into groundwater. Applied and Environmental Microbiology 32, 537–546. open url image1

Gibbs RA , Hu CJ , Ho GE , Philips PA , Unkovich I (1995) Die-off of human pathogens in sludge amended soil. In ‘Proceedings of the Australian Water and Wastewater Association 16th Federal Convention’. pp. 667–674.

Gibbs RA, Hu CJ, Ho GE, Unkovich I (1997) Regrowth of faecal coliforms and salmonellae in stored biosolids and soil amended with biosolids. Water Science and Technology 35, 269–275.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gilmour AR , Cullis BR , Welham SJ , Thompson R (1999) ASReml Reference Manual. NSW Agriculture Biometric Bulletin No. 3, NSW Agriculture, Orange, NSW.

Glynn JR, Bradley DJ (1992) The relationship between infecting dose and severity of disease in reported outbreaks of Salmonella infections. Epidemiology and Infection 109, 371–388.
PubMed |
open url image1

Hagedorn C (1980) ‘Potential health hazard associated with the disposal of sewage sludge on agricultural soils in western Oregon.’ (Water Resource Research Institute, Oregon State University: Corvallis, OR)

Hess E, Breer C (1975) Epidemiology of salmonellae and fertilizing of grassland with sewage sludge, (author’s transl.) Zentralblatt fur Bakteriology [Orig B] 161, 54–60. open url image1

Hu CJ , Gibbs RA , Ho GE , Philips P , Unkovich I (1995) Pathogen densities in wastewater sludge treated by anaerobic digestion and dewatering. In ‘3rd International Conference on Appropriate Waste Management Technologies for Developing Countries’. pp. 23–31.

Ibiebele DD, Inyang AD, Lawrence CH, Coleman RL, Pees N (1985) Some characteristics of the behaviour of indicator bacteria in sewage-amended soil. Environmental Pollution Series A 39, 175–182.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jepsen SE, Krause M, Gruttner H (1997) Reduction of fecal Streptococcus and Salmonella by selected treatment methods for sludge and organic waste. Water Science and Technology 36, 203–210.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jones K, Betaieb M, Telford DR (1990) Seasonal variation of thermophilic campylobacters in sewage sludge. Journal of Applied Bacteriology 69, 185–189.
PubMed |
open url image1

Jones PW, Rennison LM, Lewin VH, Redhead DL (1980) The occurrence and significance to animal health of salmonellas in sewage and sewage sludges. Journal of Hygiene 84, 47–62.
PubMed |
open url image1

King CH, Shotts EBJ, Wooley RE, Porter KG (1988) Survival of coliforms and bacterial pathogens within protozoa during chlorination. Applied and Environmental Microbiology 54, 3023–3033.
PubMed |
open url image1

Linklater KA, Graham MM, Sharp JC (1985) Salmonellae in sewage sludge and abattoir effluent in south-east Scotland.  Journal of Hygiene 94, 301–307.
PubMed |
open url image1

Michalk DL , Curtis IH , Langford CM , Simpson PC , Seaman JT (1996) Effects of sewage sludge on pasture production and sheep performance. In ‘Proceedings 8th Australian Agronomy Conference’. pp. 439–432. (Australian Society of Agronomy)

Northcote KH (1974) Schema for Divisions and Subdivisions. In ‘A factual key for the recognition of Australian soils’. p. 34. (Rellim Technical Publications: Glenside, S. Aust.)

NSW Environment Protection Authority (1997) Section 3.4 - 3.6. In ‘Environmental guidelines: Use and disposal of biosolids products’. pp. 11–18. (NSW EPA: Chatswood, NSW)

Patterson HD, Thompson R (1971) Recovery of interblock information when block sizes are unequal. Biometrika 58, 545–554.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pepper I, Josephson K, Bailey R, Burr M, Gerba C (1993) Survival of indicator organisms in Sonoran Desert soil amended with sewage sludge. Journal of Environmental Science and Health, Part A: Environmental Science and Engineering 28, 1287–1302. open url image1

Pillai SD, Widmer KW, Dowd SE, Ricke SC (1996) Occurrence of airborne bacteria and pathogen indicators during land application of sewage sludge. Applied and Environmental Microbiology 62, 296–299.
PubMed |
open url image1

Robinson MB, Polglase PJ, Weston CJ (2002) Loss of mass and nitrogen from biosolids applied to a pine plantation. Australian Journal of Soil Research 40, 1027–1039.
Crossref | GoogleScholarGoogle Scholar | open url image1

Russ CF, Yanko WA (1981) Factors affecting salmonellae repopulation in composted sludges. Applied and Environmental Microbiology 41, 597–602.
PubMed |
open url image1

Sidhu J, Gibbs R, Ho G, Unkovich I (2001) The role of indigenous microorganisms in suppression of Salmonella regrowth in composted biosolids. Water Research 35, 913–920.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Skanavis C, Yanko WA (1994) Evaluation of composted sewage sludge based soil amendments for potential risks of salmonellosis. Journal of Environmental Health 56, 19–23. open url image1

Soares H, Cardenas B, Weir D, Switzenbaum M (1995) Evaluating pathogen regrowth in biosolids compost. BioCycle 36, 70–76. open url image1

St. John WD, Matches JR, Wekell MM (1982) Use of iron milk medium for enumeration of Clostridium perfringens. Journal – Association of Official Analytical Chemists 65, 1129–1133. open url image1

Standards Association of Australia (1987) Methods for the microbiological examination of food. Part 2—Examination for Specific Organisms. In ‘Australian Standard 1766.2.3 Coliforms and Escherichia coli’. pp. 1–3.

Standards Australia (1991 a) Method 2.5. Examination for specific organisms—Salmonellae. In ‘Australian Standard 1766.2.5. Food microbiology’. pp. 1–8.

Standards Australia (1991 b) Method 2.8. Examination for specific organisms—Clostridium perfringens. In ‘Australian Standard 1766.2.8 Food microbiology’. pp. 1–6.

Steinert M, Birkness K, White E, Fields B, Quinn F (1998) Mycobacterium avium bacilli grow saprozoically in coculture with Acanthamoeba polyphaga and survive within cyst walls. Applied and Environmental Microbiology 64, 2256–2261.
PubMed |
open url image1

Stelzer W, Jacob J (1991) A study of Campylobacter in sewage, sewage sludge and in river water. Water Science and Technology 24, 117–120. open url image1

Surampalli RY, Banerji SK, Chen JC (1994) Microbiological stability of wastewater sludges from activated sludge systems. Bioresource Technology 49, 203–207.
Crossref | GoogleScholarGoogle Scholar | open url image1

Verbyla AP, Cullis BR, Kenward MG, Welham SJ (1999) The analysis of designed experiments and longitudinal data by using smoothing splines (with discussion). Applied Statistics 48, 269–311. open url image1

Ward RL, Yeager JG, Ashley CS (1981) Response of bacteria in wasterwater sludge to moisture loss by evaporation and effect of moisture content on bacterial inactivation by ionizing radiation. Applied and Environmental Microbiology 41, 1123–1127.
PubMed |
open url image1

Waterman SR, Small PL (1998) Acid-sensitive enteric pathogens are protected from killing under extremely acidic conditions of pH 2.5 when they are inoculated onto certain solid food sources. Applied and Environmental Microbiology 64, 3882–3886.
PubMed |
open url image1

Yanko WA , Glass JS , Van Sluis RJ , Dahlgren JA , Easly RC (1978) Survival of pathogenic and indicator microorganisms in sewage sludge amended agricultural soils – winter and summer growing seasons, 1977. County Sanitation Districts of Los Angeles County, San Jose Creek Water Quality Lab, Whittier, CA.

Yeager JG, Ward RL (1981) Effects of moisture content on long-term survival and regrowth of bacteria in wastewater sludge. Applied and Environmental Microbiology 41, 1117–1122.
PubMed |
open url image1