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Soil, land care and environmental research
RESEARCH ARTICLE

Salmonella uptake in sheep exposed to pastures after biosolids application to agricultural land

G. J. Eamens A C and A. M. Waldron A B
+ 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 Corresponding author. Email: graeme.eamens@dpi.nsw.gov.au

Australian Journal of Soil Research 46(4) 302-308 https://doi.org/10.1071/SR07152
Submitted: 4 October 2007  Accepted: 19 March 2008   Published: 23 June 2008

Abstract

Young adult sheep grazing pasture on land treated with dewatered biosolids 1–3 weeks before pasture sowing were used to assess the risk of transfer of Salmonella spp. from biosolids to the food chain. Monthly determinations of Salmonella spp. concentrations in the biosolids after land application showed survival for at least 7 months, with concentrations fluctuating between 104/g and below detection limits at various time points. Low concentrations were measured 4–5 months after application, followed by a return to 102–103/g on subsequent samplings. Sheep introduced at 3 or 6 months after biosolids applications of 0, 10, or 15 dry t/ha were assessed monthly for faecal shedding of salmonellae, and at slaughter, 8 months after biosolids application, for intestinal carriage of Salmonella spp. None of 80 sheep grazing the biosolids-treated land were found to excrete salmonellae. A single sheep among those grazing treated land showed Salmonella carriage in slaughter tissues, but the serovar isolated from this animal was different from the 6 serovars of Salmonella detected in the applied biosolids. Use of dewatered biosolids on land later sown for pasture and grazed by sheep thus posed no risk to animal uptake or faecal shedding of Salmonella spp. This in part relates to a low risk of direct pathogen ingestion by grazing sheep and the period of several months necessary for pasture establishment before grazing stock can be introduced.


Acknowledgments

This work was supported by funds from the Sydney Water Corporation. We thank Jocelyn Gonsalves who provided excellent backup technical support, Stephen Pitt for assistance in the regular mustering of experimental sheep for monthly samplings, and Dr Trevor Gibson for valuable comments on the manuscript. The assistance of Dorothy Thompkins, Kim Koeford and Joe Kormos in initial sheep handling procedures and fencing required for the experiment was also invaluable.


References


Acha PN , Szyfres B (2001) Salmonellosis. In ‘Zoonoses and communicable diseases common to man and animals.’ pp. 233–246. (Pan American Health Organisation: Washington, DC)

Anon. (1999) National Enteric Pathogens Surveillance Scheme—Non-human Annual Report 1998. (Ed. J Powling) p. 14.

Anon. (2000) National Enteric Pathogens Surveillance Scheme—Non-human Annual Report 1999. (Ed. J Powling) p. 19.

Anon. (2003) National Enteric Pathogens Surveillance Scheme—Non-Human Annual Report 2002. (Ed. J Powling) p. 24.

Anon. (2004a) National Enteric Pathogens Surveillance Scheme—Non-Human Annual Report 2003. (Ed. J Powling) p. 25.

Anon. (2004b) Australian Salmonella Reference Centre—Annual Report 2004. Institute of Medical and Veterinary Science, Infectious Diseases Laboratories, Adelaide, S. Aust. pp. 23–32.

Anon. (2004c) National Enteric Pathogens Surveillance Scheme—Human Annual Report 2003. (Ed. J Powling) p. 18.

Anon. (2005) National Enteric Pathogens Surveillance Scheme—Non-Human Annual Report 2004. (Ed. J Powling) p. 24.

Anon. (2006a) Australian Salmonella Reference Centre—Annual Report 2006. Institute of Medical and Veterinary Science, Infectious Diseases Laboratories: Adelaide, S. Aust. pp. 25–37.

Anon. (2006b) National Enteric Pathogens Surveillance Scheme—Human Annual Report 2005. (Ed. J Powling) p. 41.

Bridson EY (1990) Rappaport Vassiliadis Enrichment Broth. In ‘The Oxoid manual’. pp. 2.181–2.182. (Unipath Ltd: Basingstoke, Hants, UK)

Brown DD, Ross JG, Smith AFG (1977) Experimental infection of sheep with Salmonella infantis. The British Veterinary Journal 133, 435–441.
PubMed |
open url image1

Clegg FG, Wray C, Dancan AL, Appleyard WT (1986) Salmonellosis in two dairy herds associated with a sewage farm and water reclamation. Journal of Hygiene 97, 237–246. open url image1

Daniel RG, Barrow P, Szmolleny G, Wood M (1997) Salmonella hindmarsh infection in sheep and ponies. The Veterinary Record 141, 203.
PubMed |
open url image1

Dickson PH , Tribe HT (1986) ‘The fate of salmonellae, presumptive coliform bacteria and faecal streptococci in raw sewage sludge buried in soils.’ (WRC Environment Medmenham: Bucks, UK)

DuPont HL (2007) The growing threat of foodborne bacterial enteropathogens of animal origin. Clinical Infectious Diseases 45, 1353–1361.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Eamens G , Waldron A (1999) Survival and growth of pathogenic and indicator bacteria in dewatered sewage sludges after agricultural application. In ‘IX International Congress of Bacteriology and Applied Microbiology’. p. 20. (International Union of Microbiological Societies: Utrecht, The Netherlands)

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

Eamens GJ, Lavis AM, Nicholls PJ (2006) Survival of pathogenic and indicator bacteria in biosolids in agricultural applications. Australian Journal of Soil Research 44, 647–659.
Crossref | GoogleScholarGoogle Scholar | open url image1

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

Fricker CR (1987) The isolation of salmonellas and campylobacters. Journal of Applied Bacteriology 63, 99–116. open url image1

Gerba CP, Smith JEJ (2005) Sources of pathogenic microorganisms and their fate during land application of wastes. Journal of Environmental Quality 34, 42–48.
PubMed |
open url image1

Gibbs RA , Hu CJ , Ho GE , Philips PA , Unkovitch 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. (Australian Water and Wastewater Association: Artarmon, NSW)

Grau FH, Smith MG (1972) A comparison of methods for the enrichment of salmonellae from sheep faeces. Journal of Applied Bacteriology 35, 531–536.
PubMed |
open url image1

Grau FH (1974) Salmonella contamination of sheep and mutton carcasses related to pre-slaughter holding conditions. Journal of Applied Bacteriology 37, 111–116. open url image1

Hall GA, Jones PW (1978) A study of the susceptibility of cattle to oral infection by salmonellas contained in raw sewage sludges. Journal of Hygiene 80, 409–414.
PubMed |
open url image1

Hu C, Gibbs R, Mort N, Hofstede H, Ho G, Unkovitch I (1996) Organisms a threat in stored sludge. Waste Management and Environment 7, 21–23. open url image1

Isbell RF (1996) ‘The Australian Soil Classification. Vol 4.’ (CSIRO: Collingwood, Vic.)

Jay S , Grau FH , Smith K , Lightfoot D , Murray C , Davey GR (1997) Salmonella. In ‘Foodborne microorganisms of public health significance’. (Eds AD Hocking, G Arnold, I Jenson, K Newton, P Sutherland) pp. 169–192. (CSIRO Food Science and Technology: North Ryde, NSW)

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

Jones PW (1984) The survival and infectivity for cattle of salmonellas on grassland. In ‘Processing and use of sewage sludge’. (Eds P L’Hermite, H Ott) pp. 178–190. (D. Reidel Publishing Co.: Dortrecht, The Netherlands)

June GA, Sherrod PS, Hammack TS, Amaguana RM, Andrews RH (1995) Relative effectiveness of selenite cystine broth, tetrathionate broth, and Rappaport-Vasiliadis medium for the recovery of Salmonella from raw flesh and other highly contaminated foods. Journal of AOAC International 78, 375–380.
PubMed |
open url image1

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

McAuliffe PR, Hardefeldt KW, Hucker DA (1978) Health problems associated with export of live sheep. Australian Veterinary Journal 54, 594–595.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

McCaughey WJ, McClelland TG, Hanna J (1971) Some observations on Salmonella dublin infection in clinically healthy beef cattle. The British Veterinary Journal 127, 549–556. open url image1

Moo D, O’Boyle D, Mathers W, Frost AJ (1980) The isolation of salmonella from jejunal and caecal lymph nodes of slaughtered animals. Australian Veterinary Journal 56, 181–183.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Peterz M, Wilberg C, Norberg P (1989) The effect of incubation temperature and magnesium chloride concentration on growth of salmonella in home-made and in commercially available dehydrated Rappaport-Vassiliadis broths. Journal of Applied Bacteriology 66, 523–528. open url image1

Purvis GM, Hullah K, Pascoe SJS, Evans SJ, Davies RH (2005) Persistence of Salmonella Typhimurium DT120 in abattoir paddocks holding sheep. The Veterinary Record 157, 165–167.
PubMed |
open url image1

Reilly WJ, Forbes GI, Paterson GM, Sharp JCM (1981) Human and animal salmonellosis in Scotland associated with environmental contamination 1973–1979. The Veterinary Record 108, 553–555.
PubMed |
open url image1

Richards RB, Norris RT, Higgs ARB (1993) Distribution of lesions in ovine salmonellosis. Australian Veterinary Journal 70, 326–330.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Samuel JL, Eccles JA, Francis J (1981) Salmonella in the intestinal tract and associated lymph nodes of sheep and cattle. Journal of Hygiene 87, 225–232. 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

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

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

Strauch D (1991) Survival of pathogenic micro-organisms and parasites in excreta, manure and sewage sludge. Revue Scientifique et Technique Office International des Epizooties 10, 813–846. open url image1

Taylor J , McCoy JH (1969) Salmonella and Arizona infections. In ‘Food borne infections and intoxications’. (Ed. H Riemann) pp. 4–5. (Academic Press: New York)

Thorns CJ (2000) Bacterial food-borne zoonoses. Revue Scientifique et Technique Office International des Epizooties 19, 226–239. open url image1

Wray C, Callow RJ (1985) A note on potential hazards to animals grazing on pasture improperly treated with sewage sludge. Journal of Applied Bacteriology 58, 257–258. open url image1