Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
REVIEW

Recycling biosolids to pasture-based animal production systems in Australia: a review of evidence on the control of potentially toxic metals and persistent organic compounds recycled to agricultural land

J. Hill
+ Author Affiliations
- Author Affiliations

Faculty of Land and Food Resources, University of Melbourne, Parkville, Vic. 3010, Australia. Email: julianh@unimelb.edu.au

Australian Journal of Agricultural Research 56(8) 753-773 https://doi.org/10.1071/AR04264
Submitted: 4 November 2004  Accepted: 6 May 2005   Published: 25 August 2005

Abstract

Biosolids from municipal waste water treatment are commonly used in agriculture as a source of nutrients, organic matter, and irrigation. There is, however, concern that the use of biosolids on pasture can lead to an accumulation of potentially toxic metals (PTM) and persistent organic compounds (POC) in the surface layers of soil and associated herbage that can be ingested by grazing livestock. This review examines the following two key questions. Is the use of these materials in an agricultural setting safe and practical? Is the use of biosolids safe in all climates, on all soils, and is it sustainable over the long term? To answer these important questions, the Australian regulatory framework is examined in light of similar legislation in Europe and the United States on the basis of scientific evidence that underpins the published limits, contaminant gradings, annual loadings, and prescribed restrictions on the use of biosolids in agriculture. The review concludes that the regulatory frameworks currently enacted at State level suffer from a lack of data to underpin the risk assessments conducted to prevent transfer of PTM and POC to the human food chain from livestock production and the basis of published thresholds is poorly defined. The important areas of future research are identified as studies on acquisition and transfer of PTM and POC to grazing animals and the subsequent effect of attenuation of the pollutant on the human food chain, the validation and acceptance of methods to quantify POC in biosolids, the effect of recycling of biosolids on the economic performance of pasture-based agriculture, and the market perception of animal products produced from land receiving biosolids.

Additional keywords: grazing livestock, legislation, contaminants, human food.


References


Agricultural and Veterinary Chemicals (Control of Use) Act (1992) Victorian Legislation and Parliamentary Document 46/1992. Victoria State Government, Melbourne, Australia.

Aitken MN (1997) Short-term leaf surface adhesion by heavy metals following application of sewage sludge to grassland. Grass and Forage Science 52, 73–83.
Crossref | GoogleScholarGoogle Scholar | open url image1

Alloway BJ (1999) Land contamination and reclamation. ‘Understanding our environment’. (Ed. RM Harrison) pp. 199–236. (Royal Society of Chemistry: Cambridge, UK)

Alloway BJ, Hird AB, Zhang P, Chambers B, Nicholson F, Smith S, Carlton-Smith CH (1999) Atmospheric deposition of metals in rural areas of England and Wales. Extension to Contract Ref.2736, Final Report to the Ministry of Agriculture, Fisheries and Food, UK Government, UK.

Alloway BJ, Zhang P, Mott CJB, Nicholson F, Chambers B, Smith S, Carlton-Smith C (1999) Atmospheric deposition of heavy metals onto agricultural land in England and Wales. ‘5th International Conference on Biogeochemistry of Trace Elements 1999’. (University of Agricultural Sciences: Vienna, Austria)


Anon. (1998) Lead free. The Bulletin Vol.8, Szentendre, Regional Environmental Center of Central and Eastern Europe, Budapest, Hungary.

ANZECC and ARMCANZ (2000). ‘National water quality management strategy: draft guidelines for sewerage systems sludge (biosolids) management.’ (Australian and New Zealand Environment and Conservation Council and Agriculture and Resources Management Council of Australia and New Zealand: Canberra, ACT)

ANZECC and ARMCANZ (2001). ‘National water quality management strategy.’ (Australian and New Zealand Environment and Conservation Council and Agriculture and Resources Management Council of Australia and New Zealand: Canberra, ACT)

ANZECC and NHMRC (1992). ‘Australian and New Zealand guidelines for assessment and management of contaminated sites.’ (Australian and New Zealand Environment and Conservation Council and National Health and Medical Research Council: Canberra, ACT)

ARMCANZ (1995). ‘Guidelines for sewerage systems — biosolids management.’ (Agriculture and Resources Management Council of Australia and New Zealand: Canberra, ACT)

Ashton D, Brittle S, Shaw I (2001) Dairy: outlook to 2005–2006. ‘ABARE (2001) Outlook 2001. Proceedings of the National Outlook Conference’. Canberra, Australia. (Australian Bureau of Agricultural and Resource Economics; Canberra, ACT)


Australia Government (1991). ‘Australia New Zealand Food Authority Act 1991.’ (AGP: Canberra, ACT)

Australian Bureau of Statistics (2001). ‘Year book Australia: agriculture.’ (ABS: Canberra, ACT)

Bååth E (1989) Effects of heavy metals in soil on microbial processes and populations (a review). Water, Air, and Soil Pollution 47, 335–379.
Crossref | GoogleScholarGoogle Scholar | open url image1

Baize, D (1997). ‘Teneurs totales en éléments traces métalliques dans les sols (France).’ (INRA: París, France)

Barry GA, Gardner EA, Bloesch P (1998) Studies on reuse of biosolids on Queensland agricultural lands. ‘WaterTECH, Proceedings of the Australian Water and Wastewater Association Conference’. Brisbane, Queensland. (Australian Water and Wastewater Association: Artarmon, NSW)


Bethel M (1999) Best practice management of effluent and biosolids. ‘62nd Victorian Water Industry Engineers and Operators’ Conference, 1999’. Wodonga, Vic.. (Victorian Water Industry Engineers and Operators: Wodonga, Vic.)


Boswell FC (1975) Municipal sewage sludge and selected element additions to soil: Effect on soil and fescue. Journal of Environmental Quality 4, 267–273. open url image1

Carrington EG, Davis RD, Hall JE, Pike EB, Smith SR, Unwin RJ (1998) Review of scientific evidence relating to the controls on the agricultural use of sewage sludge. Part 2. Evidence since 1989 relevant to controls on the agricultural use of sewage sludge. Final report to DETR, DoH, MAFF and UKWIR, Water Research Centre, Medmenham, UK.

CEC (1986) Council Directive 86/278/EEC on the protection of the environment, and in particular of the soil, when sewage sludge is used in agriculture. Official Journal of the European Communities 181, 6–12. open url image1

CEC (1991) Council Directive 91/271/EEC of 21 May 1991 concerning urban waste water treatment. Official Journal of the European Communities L135, 40–52. open url image1

CEC (2001) Council Directive EC 466/2001. Setting maximum levels for certain contaminants in foodstuff. Official Journal of the European Communities L77, 1–13. open url image1

CEC (2002b) Directive EC 221/2002. Amending Regulation (EC) No. 446/2001 setting maximum levels for certain contaminants in foodstuff. Official Journal of the European Communities L37, 4–6. open url image1

CEC (2002a). ‘Heavy metals in waste.’ a. (COWI A/S Copenhagen: Denmark)

CEC (2004) Regulation (EC) No. 882/2004 of the European Parliament and of the Council of 29 April 2004 on official controls performed to ensure the verification of compliance with feeds and food law, animal health and animal welfare rules. Official Journal of the European Communities L165, 1–141. open url image1

Chambers, BJ , Hickman, G ,  and  Aitken, MN (2001). ‘The safe sludge matrix.’ (ADAS Gleadthorpe: Nottingham, UK)

Chaney RL (1985) Potential effects of sludge-borne heavy metals and toxic organics on soils, plants and animals, and related regulatory guidelines. Final Report of the Workshop on the International Transportation, Utilisation or Disposal of Sewage Sludge including recommendations, PNSP/85-01, Pan American Health Organisation, Washington, DC.

Chaney RL (1993) Risks associated with the use of sewage sludge in agriculture. ‘Proceedings of 15th Federal Convention Australian Water and Wastewater Association’. Gold Coast, Queensland, Vol 1.. (Australian Water and Wastewater Association (Queensland Branch: West End, Qld)


Chaney RL, Lloyd CA (1979) Adherence of spray-applied liquid digested sewage sludge to tall fescue. Journal of Environmental Quality 8, 407–411. open url image1

Chaney RL, Ryan JA (1992) Regulating residual management practices. Journal of Environmental Technology 4, 36–41. open url image1

Chang, AC , Page, AL ,  and  Asano, T (1993). ‘Developing human health-related chemical guidelines for reclaimed wastewater and sewage sludge applications.’ (Community Water Supply and Sanitation Unit, Division of Environmental Health, WHO: Geneva, Switzerland)

Codex Alimentarius Commission (1999) Joint FAO/WHO Food Standard Programme: Report of the 13th Session of the Codex Committee on Food Additives and Contaminants. The Hague, 9–13 March 1998, FAO, Rome, Italy.

COM (2003) Proposal for a Regulation of the European Parliament and of the Council laying down requirements for feed hygiene. COM/2003/0180 final – COD 2003/0071 */., Commission of the European Communities, Brussels, Belgium.

Davis RD, Carlton-Smith CH, Stark JH, Hunter JA (1988) Distribution of metals in grassland soils following surface applications of sewage sludge. Environmental Pollution 49, 99–115.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dewes HF (1996) The rate of soil ingestion by dairy cows and the effect on availabilities of Cu, Ca, Na and Mg. New Zealand Veterinary Journal 44, 199–200.
PubMed |
open url image1

DFSV (2001). ‘The use of biosolids (sewage sludge) as a fertiliser/soil conditioner on dairy pastures: a review from a dairy food safety perspective.’ (Dairy Food Safety: Melbourne, Vic.)

DNRE (2002). ‘Victorian Biosolids Market Survey.’ (Pollution Solutions and Designs Pty Ltd.: Melbourne, Vic.)

DSE (2003). ‘Biosolids in Victoria: Report on options for beneficial use of biosolids.’ (Department of Sustainability and Environment, State of Victoria: Melbourne, Vic.)

Duarte-Davidson R, Courage C, Rushton B, Levy L (2001) Benzene in the environment: an assessment of the potential risks to the health of the population. Occupational and Environmental Medicine 58, 2–13.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Duarte-Davidson R, Jones KC (1996) Screening of the environmental fate of organic contaminants in sewage sludge applied to agricultural soils. II. The potential for transfers to plants and grazing animals. The Science of the Total Environment 185, 59–70.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

EC/DG Environment (2001) Disposal and recycling routes for sewage sludge. Part 3. Scientific and Technical Report 14 KH-17-01-003-EN-N, Office for Official Publications of the European Communities, L-2985, Luxembourg

EC/DG Environment (2001) Disposal and recycling routes for sewage sludge. Part 2. Regulatory Report, 14 KH-17-01-002-EN-N, Office for Official Publications of the European Communities, L-2985, Luxembourg.

EC/DG Environment (2001) Disposal and recycling routes for sewage sludge. Part 1. Sludge use acceptance Report. 14 KH-17-01-001-EN-N, Office for Official Publications of the European Communities, L-2985, Luxembourg.

EC/DG Environment (2001) Disposal and recycling routes for sewage sludge. Part 4. Economic Report, 14 KH-17-01-004-EN-N, Office for Official Publications of the European communities, L-2985, Luxembourg.

Eisler R (1987) Polycyclic aromatic hydrocarbons hazards to fish, wildlife and invertebrates: a synoptic review. US Fisheries and Wildlife Services Biology Report 85 (1.11). USDA, Washington, DC.

Eisler R (1993) Zinc hazards to fish, wildlife and invertebrates: a synoptic review. US Fisheries and Wildlife Services Biology Report 10, USDA, Washington, DC.

Eisler R (1998) Copper hazards to fish, wildlife and invertebrates: a synoptic review. US Geological Survey, Biological Resources Division, Biological Services Report USGS/BRD/BSR 1998–0002, UGS, Washington, DC.

Eisler R, Beliske AA (1996) Planar PCB hazards to fish, wildlife and invertebrates: a synoptic review. US Fisheries and Wildlife Services Biology Report 31, USDA, Washington DC.

Environmental Protection Act (1970). ‘Victorian Legislation and Parliamentary Document 8056/1970.’ (Victoria State Government: Melbourne, Vic.)

EPAV (2004). ‘Guidelines for environmental management: biosolids land application’. (Environmental Protection Authority Victoria: Southbank, Vic.)

EU (2000) Working document on sludge — 3rf draft: reappraisal of EC directives 86/298/EC and 91/271/EC. ENV.E. 3/LM 27 April 2000, European Union, Brussels.

Feil VJ, Ellis RL (1998) The USDA perspective on dioxin concentrations in dairy and beef. Journal of Animal Science 76, 152–159.
PubMed |
open url image1

Food Act (1984). ‘Victorian Legislation and Parliamentary Document 10082/1984.’ (Victoria State Government: Melbourne, Vic.)

Fries GF (1995) A review of the significance of animal food products as potential pathways of human exposure to dioxins. Journal of Animal Science 73, 1639–1650.
PubMed |
open url image1

Fries GF, Marrow GS, Snow PA (1981) Soil ingestion by dairy cattle. Journal of Dairy Science 65, 611–618. open url image1

FSANZ (2003). ‘The 20th Australian total diet survey.’ (Food Standards Australia New Zealand: Canberra, ACT)

Gaskin JW, Brobst RB, Miller WP, Tollner EW (2003) Long-term biosolids application effects on metal concentrations in soil and Bermuda grass forage. Journal of Environmental Quality 32, 146–152.
PubMed |
open url image1

Gleeson T, Brittle S (2001) Meat: outlook to 2005–2006. ‘ABARE (2001) Outlook 2001. Proceedings of the National Outlook Conference’. Canberra, Australia.. (Australian Bureau of Agricultural and Resource Economics; Canberra, ACT)


Government of Denmark (2000) Statutory Order (Sludge Order — Slambekendygørelsen) No. 49 of 20.1.2000 on the Application of Waste Products for Agricultural Purposes (Bekendygørelse om anvendelse af affaldsproduckter til jordbrugsformål) , Copenhagen, Denmark.

Government of Denmark (2000) Statutory Order No. 56 of 24.1.2000 describing the control of sewage sludge for agricultural use (Bekendygørelse om tilsym med spildevandsslam m.m til jordbrugsformål). , Copenhagen, Denmark.

Great Britain Parliament (1989). ‘The Sludge (use in agriculture) Regulations.’ Statutory Instrument 1989 No. 1263 amended 1990 The sludge (use on agriculture) (Amendment) Regulations. Statutory Instrument 1990 No. 880. (Majesty’s Stationary Office: London, UK)

Hall JE, Dalimier F (1994) Waste management — sewage sludge. Part 1. Survey of sludge production, treatment, quality and disposal in the European Union. Water Research Centre Report European Community 3646 to Directorate General XI of the Commission of the Euorpean communities under contract 3040/01456/92, CEC DG XI, Brussels, Belgium.

Hall, JE , L’Hermite, L ,  and  Newman, PJ (1992). ‘Treatment and use of sewage sludge and liquid agricultural wastes. Review of COST 68/861 programme, 1972–1990’. (Office of Official Publications of the European Communities: Luxembourg)

Hamon RE, McLaughlin MJ, Warne M, Davies H, Wong E, Chapman J, Kookana R, Saison C (2004) A possible framework for developing ecological guidelines for assessment of contaminated soils. ‘Workshop on Contaminants and Ecological Risk Assessment’. 5–7 April 2004. (CSIRO: Adelaide, S. Aust.)

Health Act (1958). ‘Victorian Legislation and Parliamentary Document 6270/1958.’ (Victoria State Government: Melbourne, Vic.)

Healy WD (1968) Ingestion of soil by dairy cows. New Zealand Journal of Agricultural Research 11, 487–499. open url image1

Hill J, Morgan JE, Wilkinson JM (2003) Impact of lead from municipal sewage sludge on ruminant livestock production. Bulletinul USAMV-CN, A-H, 58/2003; ISSN 1454-2382.

Hill J, Stark BA, Wilkinson JM, Curran MK, Lean IJ, Hall JE, Livesey CT (1998a) Accumulation of potentially toxic elements by sheep given diets containing soil and sewage sludge. 1. Effect of type of soil and level of sewage sludge in the diet. Animal Science 67, 73–86. open url image1

Hill J, Stark BA, Wilkinson JM, Curran MK, Lean IJ, Hall JE, Livesey CT (1998b) Accumulation of potentially toxic elements by sheep given diets containing soil and sewage sludge. 2. Effect of the ingestion of soils treated historically with sewage sludge. Animal Science 67, 87–96. open url image1

Hill J, Wilkinson JM (1997) Effect of season and methods of application of sewage sludge to grassland on the voluntary intake, digestibility of herbage and growth of weaned lambs. Proceedings of the British Society of Animal Science [British Society of Animal Science: Edinburgh]. 1997, 151. open url image1

Hillman JP, Hill J, Morgan JE, Wilkinson JM (2003) Recycling of sewage sludge to grassland: a review of the legislation to control the localisation and accumulation of potentially toxic metals in grazing systems. Grass and Forage Science 58, 101–111.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hillman JP, Hill J, Wilkinson JM (2004) Effect of season of application on the adhesion, retention and recontamination of herbage by potentially toxic metals and sewage sludge. The Science of the Total Environment 333, 283–293.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Holmes, CW ,  and  Wilson, GF (1984). ‘Milk production from pasture.’ (Butterworths Agricultural Books: Auckland, New Zealand)

Holmgren G, Myer M, Cheneu R, Daniels K (1993) Cadmium, lead, zinc, copper and nickel in agricultural soils of the United States. Journal of Environmental Quality 22, 335–348. open url image1

Imray, PLA ,  and  Langley, A (1996). ‘Health-based soil investigation levels. National Environmental Health Forum monographs No. 1.’ (South Australian Health Commission: Adelaide, S. Aust.)

Jones KC, Johnston AE, McGrath SP (1995) The importance of long- and short-term air-soil exchanges of organic contaminants. International Journal of Environmental Analytical Chemistry 59, 167–178. open url image1

Jones KC, Sewart AP (1997) Dioxins and furans in sewage sludges: a review of their occurrence and sources in sludge and of their environmental fate, behaviour and significance in sludge-amended agricultural systems. Critical Reviews in Environmental Science and Technology 27, 1–85. open url image1

Klessa DA, Desira-Buttegieg A (1992) The adhesion on leaf surfaces of heavy metals from sewage sludge applied to grassland. Soil Use and Management 8, 115–121. open url image1

Lamand MC, Lab J, Tressal C, Mason J (1980) Biochemical parameters useful for the diagnosis of mild molybdenosis in sheep. Annales de Recherche Veterinnaire 11, 141–145. open url image1

Lee J, Rounce JR, Mackay AD, Grace ND (1996) Accumulation of cadmium with time in Romney sheep grazing ryegrass–white clover pasture: effect of cadmium from pasture and soil intake. Australian Journal of Agricultural Science 47, 877–894.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lee J, Treloar BP, Grace ND (1994) Metallothionein and trace element metabolism in sheep tissues in response to high and sustained zinc dosages. II. Expression of metallothionein mRNA. Australian Journal of Agricultural Science 45, 321–332.
Crossref | GoogleScholarGoogle Scholar | open url image1

Livesey CT (1993) Contamination of animal feed: a review of principal causes, detection, investigation and control of toxic contaminants. ‘Pollution in livestock production systems’. (Ed. I Ap Dewi) pp. 19–43. (CAB International: Wallingford, UK)

Livestock Disease Control Act (1994). ‘Victorian Legislation and Parliamentary Document 115/1994.’ (Victoria State Government: Melbourne, Vic.)

Loganathan P, Hedley MJ, Grace ND, Lee J, Cronin SJ, Bolan NS, Zanders JM (2003) Fertiliser contaminants in New Zealand grazed pasture with special reference to cadmium and fluorine: a review. Australian Journal of Soil Research 41, 501–532.
Crossref | GoogleScholarGoogle Scholar | open url image1

MacDonald, DD , Berger, T , Wood, K , Brown, J , Johnsen, T , Haines, ML , Brydges, K , MacDonald, MJ , Smith, SI ,  and  Shaw, DP (1999). ‘A compendium of environmental benchmarks.’ (Environment Canada: Vancouver BC, Canada)

Martin, MH ,  and  Coughtrey, PJ (1982). ‘Biological monitoring of heavy metal pollution.’ (Applied Science Publishers: London)

McBride MB (1995) Toxic metal accumulation from agricultural use of sludge: Are USEPA regulations protective? Journal of Environmental Quality 24, 5–18. open url image1

McGrath SP (1994) Effects of heavy metals from sewage sludge on soil microbes in agricultural ecosystems. ‘Toxic metals in soil-plant systems’. (Ed. SM Ross) pp. 247–274. (John Wiley and Sons: Chichester, UK)

McGrath SP, Chang AC, Page AL, Witter E (1994) Land applications of sewage sludge: scientific perspectives of heavy metal loading limits in Europe and the United States. Environmental Reviews 2, 108–118. open url image1

McGrath, SP ,  and  Loveland, PJ (1992). ‘The soil geochemical atlas of England and Wales.’ (Blackie Academic and Professional: Glasgow, UK)

McLachlan MS, Thoma H, Reissinger M, Hutzinger O (1990) PCDD/F in an agricultural food chain. Part 1. PCDD/F mass balance of a lactating dairy cow. Chemosphere 20, 1013–1020.
Crossref | GoogleScholarGoogle Scholar | open url image1

McLaren RG, Smith CJ (1996) Issues in the disposal of industrial and urban wastes. ‘Contaminants and the soil environment in the Australasia–Pacific region’. (Ed. R Naidu) pp. 183–212. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

McLaughlin MJ, Hamon RE, McClaren RG, Speir TW, Rogers SL (2000) Review: A bioavailability-based rationale for controlling metal and metalloid contamination of agricultural land in Australia and New Zealand. Australian Journal of Soil Research 38, 1037–1086.
Crossref | GoogleScholarGoogle Scholar | open url image1

McLaughlin MJ, Parker DR, Clarke JM (1999) Metals and micronutrients – food safety issues. Field Crops Research 60, 143–163.
Crossref | GoogleScholarGoogle Scholar | open url image1

Moen JET (1988) Soil protection in the Netherlands. ‘Contaminated soil’. (Ed. K Wolf) pp. 1495–1503. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Moolenaar SW, van der Zee SEATM, Lexmond TM (1997) Indicators of the sustainability of heavy metal management in agro-ecosystems. The Science of the Total Environment 201, 155–169.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

NEPC (1994). ‘National Environmental Protection Council Act.’ (National Environment Protection Council: Canberra, ACT)

NEPC (2004). ‘National Environmental Protection Measures: National Pollutant Inventory.’ (National Environment Protection Council: Adelaide, S. Aust.)

Nie ZN, Ward GN, Michael AT (2001) Impact of pugging by dairy cows on pastures and indicators of pugging damage to pasture soil in south-western Victoria. Australian Journal of Agricultural Research 52, 37–43.
Crossref | GoogleScholarGoogle Scholar | open url image1

NRC (1983). ‘Risk assessment and management: framework for decision making.’ (National Research Council: Washington, DC)

NRC (1984). ‘Nutrient requirements of domestic animals.’ 7th edn . (National Research Council: Washington, DC)

NRC (1996). ‘Use of reclaimed water and sludge in food crop production.’ (National Academy Press: Washington, DC)

NSW EPA (1997). ‘Environmental management guidelines for the use and disposal of biosolids products.’ (New South Wales Environmental Protection Authority: Sydney)

O’Riordan EG, Dodd VA, Gleming GA, Tunney H (1994) Repeated applications of a metal-rich sewage sludge to grassland. Irish Journal of Agricultural and Food Research 33, 41–51. open url image1

Reid H (2002) Key guideline requirements for biosolids land application: The basis and practical implications. Paper 15. ‘65th Victorian Water Industry Engineers and Operators’ Conference, 2002’. (Victorian Water Industry Engineers and Operators: Wodonga, Vic.)


Richardson SJ (1980) Composition of soils and crops following treatment with sewage sludge. ‘Inorganic pollution and agriculture’. MAFF-ADAS Reference Book 326.,(Ed. AFF-ADAS) pp. 252–278. (Majesty’s Stationary Office: London, UK)

Richter W, McLachlan MS (2001) Uptake and transfer of PCDD/F by cattle fed naturally contaminated feedstuffs and feed contaminated as a result of sewage sludge application. 2. Non lactating cows. Journal of Agricultural and Food Chemistry 49, 5857–5865.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rideout K, Teschke K (2004) Potential for increased human foodborne exposure to PCDD/F when recycling sewage sludge on agricultural land. Environmental Health Perspectives 112, 959–969.
PubMed |
open url image1

Roeder RA, Garber MJ, Schelling GT (1998) Assessment of dioxins in foods from animal origins. Journal of Animal Science 76, 142–151.
PubMed |
open url image1

SA EPA (1997). ‘South Australian biosolids guidelines for safe handling, reuse or disposal of biosolids.’ (South Australia Environmental Protection Authority: Adelaide, S. Aust.)

Schmidt JP (1997) Understanding phytotoxicity thresholds for trace elements in land applied sewage sludge. Journal of Environmental Quality 26, 4–10. open url image1

Smith, SR (1996). ‘Agricultural recycling of sewage sludge and the environment.’ (CAB International: Wallingford, UK)

SPWQM (1997). ‘Environmental guidelines for the use of recycled water in Tasmania.’ (Environment Division: Hobart, Tas.)

Stark BA (1988) Effects on grazing animals of ingestion of inorganic and organic materials contained in sewage sludge. Report PRU 1691-M, Water Research Centre, Medmenham, UK.

Taylor JK (1983) The Australian environment. ‘Soils: an Australian viewpoint’. pp. 1–2. (CSIRO publishing: Melbourne, Vic.)

Tiffany ME, McDowell LR, O’Connor GA, Martin FG, Wilkinson NS, Cardoso EC, Percival SS, Rabiansky PA (2000) Effects of pasture applied biosolids on performance and mineral status of grazing beef heifers. Journal of Animal Science 78, 1331–1337.
PubMed |
open url image1

US EPA (1982). ‘Fate of priority pollutants in publicly owned treatment works.’ Vol. 1, EPA 440/1-82-3.3. (US Environmental Protection Agency, Industrial Technology Division: Washington, DC)

US EPA (1990) National sewage sludge survey: Availability of information and data, and anticipated impacts on proposed regulations; Proposal Rule 40CFR Part 503. , 47210–47283, 9 November 1990, Washington, DC.

US EPA (1992) Statistical support documentation for the 40 CFR Part 503 Final Standards for the Use and Disposal of Sewage Sludge. Final report 11 November 1992, Vols 1 and 2, US Environmental Protection Agency, Office of Science and Technology Engineering and Analysis, Washington, DC.

US EPA (1993) Standards for the use or disposal of sewage sludge; Final rules, 40CFR Parts 257, 403 and 503. , 9248–9415, 19 February 1993, Washington, DC.

US EPA (1993). ‘Wildlife exposure factors handbook. EPA/60/P-92–003C.’ (United States Environmental Protection Agency: Washington, DC)

US EPA (1995). ‘A guide to the biosolids risk assessment for the EPA Part 503 Rule. EPA/832-B-93–005.’ (United States Environmental Protection Agency: Washington, DC)

US EPA (2002). ‘Exposure analysis for dioxins, dibenzofurans and coplanar polychlorinated biphenyls in sewage sludge.’ (The Office of Water, US Environmental Protection Agency: Washington, DC)

Van der Berg, R ,  and  Roels, JM (1991). ‘Risk assessment to man and the environment in case of exposure to soil contamination. Integration of different aspects.’ (RIVM Report No. 75201013. (Rijksinstituut voor Volksgezondheid en Milieu (RIVM): Bilthoven, The Netherlands)

Vigerust E, Selmer-Olsen AR (1986) Basis for metal limits relevant to sludge utilisation. ‘Factors influencing sludge utilisation in Europe’. (Ed. RD Davies) pp. 127–142. (Elsevier Applied Science Publishers Ltd: Amsterdam, The Netherlands)

Water and Rivers Commission (1999). ‘Biosolids – application to land.’ Water Quality Protection Note. (Water and Rivers Commission: Perth, W. Aust.)

Webber MD, Kloke A, Tjell J (1984) A review of current sludge use guidelines for the control of heavy metal contamination of soils. ‘Processing and use of sewage sludge’. (Eds P L’Hermite, H Ott) pp. 371–386. (D. Reidel: Dordecht, The Netherlands)

Whatmuff MS (2002) Applying biosolids to acid soils in New South Wales: are guideline soil metal limits from other countries appropriate? Australian Journal of Soil Research 40, 1041–1056. open url image1

Whatmuff, MS ,  and  Osbourne, GJ (1992). ‘The behaviour of heavy metals in soils. A review of published literature on the land application of sewage sludge.’ (NSW Agriculture, Organic Waste Recycling Unit: Richmond, NSW)

Wilkinson JM, Hill J, Hillman JP (2003b) The accumulation of potentially toxic metals in edible body tissues of lambs grazing after a single application of sewage sludge. Water Research 37, 128–138.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wilkinson JM, Hill J, Livesey CT (2001) Effect of repeated applications of sewage sludge to grassland on the growth of lambs at pasture and the composition of body tissues. Animal Science 72, 179–190. open url image1

Wilkinson JM, Hill J, Phillips CJC (2003a) The accumulation of potentially toxic metals by grazing ruminants. The Proceedings of the Nutrition Society 62, 267–277.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yingming L, Corey RB (1993) Redistribution of sludge-borne cadmium, copper and zinc in a cultivated plot. Journal of Environmental Quality 22, 1–8. open url image1

Young, ARM ,  and  Young, R (2001). ‘Soils in the Australian landscape.’ (Oxford University Press: South Melbourne, Vic.)

Zach R, Mayoh KR (1984) Soil ingestion by cattle: a neglected pathway. Health Physics 46, 426–431.
PubMed |
open url image1