Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-19T00:04:01.424Z Has data issue: false hasContentIssue false
  • English
  • Français

The accumulation of potentially-toxic metals by grazing ruminants

Published online by Cambridge University Press:  05 March 2007

J. M. Wilkinson ,
J. Hill  and
C. J. C. Phillips
J. M. Wilkinson*
Affiliation:
School of Biology, University of Leeds, Leeds, LS2 9JT, UK
J. Hill
Affiliation:
Faculty of Applied Science and Technology, Writtle College, Writtle, Chelmsford, Essex, CM1 3RR, UK
C. J. C. Phillips
Affiliation:
Department of Clinical Veterinary Medicine, University of Cambridge, Cambridge, CB3 0ES, UK
*
*Corresponding author: Dr J. M. Wilkinson Present address: Painshall, Church Lane, Welton, LincolnLN2 3LT, UK, fax +44 1673 863108, [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The main factors affecting the accumulation of potentially-toxic metals (PTM) by grazing animals are the presence of the metal, its concentration in herbage and at the soil surface, and the duration of exposure to the contaminated pasture and soil. In addition, the elapsed time between the contamination of the pasture and grazing, the quantity of soil ingested together with herbage, the mechanism of absorption of the metal into blood and the presence or absence of antagonistic metals can interact to influence the rate and extent of accumulation of heavy metals in edible body tissues. Models of the accumulation of metals by grazing animals may be used to determine the statutory limits of radionuclides and PTM in soils under grazed pastures. Meta-analysis of existing data, using a random-effects model, is a useful approach to understanding the factors affecting the accumulation of some metals, e.g. Cd. The target edible body tissues for the accumulation of most PTM are the liver and kidneys, with the exception of radiocaesium, which accumulates in muscle to a greater extent than in other tissues. The livers and kidneys of mature livestock that have been grazed on areas of pasture at the legal limit of contamination by Cd for more than one grazing season should be removed from the human food chain in order to reduce the risk of intake of Cd by the human population.

Keywords

Potentially-toxic metalsGrazing livestockContaminated pasture and soilAccumulation in edible body tissues
Type
Symposium on ‘Nutrition of farm animals outdoors’
Information
Proceedings of the Nutrition Society , Volume 62 , Issue 2 , May 2003 , pp. 267 - 277
Copyright
Copyright © The Nutrition Society 2003

References

Aitken, MN (1997) Short term leaf surface adhesion of heavy metals following application of sewage sludge to grassland. Grass and Forage Science 52. 73–85CrossRefGoogle Scholar
Aitken, MN (1998) Impact of applying agricultural and nonagricultural waste to farmland, Proceedings, Veterinary Public Health Association/British Veterinary Association Scientific Meeting 1998. pp. 1–15London: British Veterinary AssociationGoogle Scholar
Aldinger, H (2002) The current debate on regulating the risk associated with cadmium in phosphate fertilizer in the European Union. Proceedings of the 8th International Conference of the Arab Fertilizer Association. Cairo: Arab Fertilizer Association.Google Scholar
Alloway, BG (1995) Heavy Metals in Soils, 2nd ed Glasgow: Blackie Academic and ProfessionalCrossRefGoogle Scholar
Alloway, BG (1999) Land contamination and reclamation Understanding our Environment 199–236 Harrison RM Cambridge Royal Society of ChemistryCrossRefGoogle Scholar
Anon (1998) Lead Free. The Bulletin, Vol. 8 Szentendre, Hungary Regional Environmental Center of Central and Eastern EuropeGoogle Scholar
Beresford, NA, Barnett, CL & Mayes, RW (2000) Radiocaesium variability within sheep flocks: determination of 137Cs intake in free-ranging sheep. Radiation and Environmental Biophysics 39. 207–212CrossRefGoogle ScholarPubMed
Beresford, NA & Howard, BJ (1991) The importance of soil adhered to vegetation as a source of radionuclides ingested by grazing animals. The Science of the Total Environment 107. 237–254CrossRefGoogle ScholarPubMed
Berry, NR, Axford, RFE, ap, Dewi, I, Chiy, PC, Phillips CJC (1999) The effect of a low dose of cadmium on spermatogenesis in rams. Small Ruminant Research 32. 97–102CrossRefGoogle Scholar
Blake, L, Johnston, AE & Goulding, KWT (1994) Mobilisation of aluminium in soil by acid deposition and its uptake by grass cut for hay – a Chemical Time Bomb. Soil Use and Management 10. 51–55CrossRefGoogle Scholar
Blaxter, KL (1950) Lead as a nutritional hazard to farm livestock. II. The absorption and excretion of lead by sheep and rabbits. Journal of Comparative Pathology and Therapeutics 60. 140–159CrossRefGoogle ScholarPubMed
Bowen, HJM (1979) Environmental Chemistry of the Elements London Academic PressGoogle Scholar
Bramley, RGV (1991) Cadmium in New Zealand agriculture. New Zealand Journal of Agricultural Research 33. 505–519CrossRefGoogle Scholar
Branford, D, Mourne, RW & Fowler, D (1998) Spatial variations of wet deposition rates in an extended region of complex topography deduced from measurements of Pb-210 soil inventories. Journal of Environmental Radioactivity 41. 111–125CrossRefGoogle Scholar
Bremner, I (1978) Cadmium toxicity. World Review of Nutrition and Dietetics. Vol. 32 Human and Animal Nutrition 165–197 Bourne GH Basel S.KargerCrossRefGoogle Scholar
Buck, WB (1970) Lead and organic pesticide poisoning in cattle. Journal of American Veterinary Medicine Association 156. 1468–1472Google ScholarPubMed
Burkitt, A, Lester, P & Nickless, G (1972) Distribution of heavy metals in the of an industrial complex Nature, London 238. 327–328Google Scholar
Cain, K & Griffiths, B (1980) Transfer of liver cadmium to the kidney after aflatoxin induced liver damage. Biochemical Pharmacology 29. 1852–1855CrossRefGoogle Scholar
Chaney, RL & Lloyd, CA (1979) Adherence of spray-applied digested sewage sludge to tall fescue. Journal of Environmental Quality 8. 407–411CrossRefGoogle Scholar
Cherian, MG (1979) Metabolism of orally-administered Cdmetallothionein in mice. Environmental Health Perspectives 28. 127–130CrossRefGoogle Scholar
Chiy, PC, de, la, Fuente, M, Barrado, E, Vega, M & Phillips, CJC (1998) The determination of mineral balances in sheep offered feed with added cadmium and zinc. Fresenius Journal of Analytical Chemistry 361. 343–348CrossRefGoogle Scholar
Clegg, FG (1978) Lead pollution in Derbyshire due to mining and industry. State Veterinary Journal 33. 41–48Google Scholar
Commission, of, the, European Communities (1991) Directive (ECD) 1991 86/278/EEC. Protection of the environment and in particular the soil, when sewage sludge is used in water. Official Journal of the European Commission L181, 6–12Google Scholar
Commission, of, the, European Communities (2001) Directive EC 466/2001. Setting maximum levels for certain contaminants in foodstuffs. Official Journal of the European Commission L77, 1–13Google Scholar
Commission, of, the, European Communities (2002) Heavy Metals in Waste Brussels Commission of the European CommunitiesGoogle Scholar
Curtis, LF, Courtney, FM & Trudgill, ST (1976) Soils in the British Isles London LongmanGoogle Scholar
Cousins, RJ (1985) Absorption, transport and hepatic metabolism of Cu and Zn: Special reference to metallothionein and ceruloplasmin. Physiological Reviews 65. 238–309CrossRefGoogle Scholar
Davis, RD, Carlton-Smith, CH, Stark, JH & Campbell, JA (1988) Distribution of metals in grassland soils following surface applications of sewage sludge. Environmental Pollution 49. 99–115CrossRefGoogle ScholarPubMed
Department, of & the, Environment (1974) Lead in the Environment and its Significance to Man London H. M. Stationery OfficeGoogle Scholar
Dewes, HF (1986) The rate of soil ingestion by dairy cows and the effect on availabilities of Cu, Ca, Na and Mg. New Zealand Veterinary Journal 44. 199–200CrossRefGoogle Scholar
Dorn, CR, Pierce, JO, Chase, GR & Phillips, PE (1975) Environmental contamination by lead, cadmium, zinc and copper in a new lead producing area. Environmental Research 9. 159–172CrossRefGoogle Scholar
Doyle, JJ & Pfander, WH (1975) Interactions of cadmium with copper, iron, zinc and manganese in ovine tissues. Journal of Nutrition 105. 599–606CrossRefGoogle ScholarPubMed
Doyle, JJ, Pfander, WH, Grebing, SE & Pierce, JOD (1974) Effect of dietary cadmium on growth, cadmium absorption and cadmium tissue levels in growing lambs. Journal of Nutrition 104. 160–166CrossRefGoogle ScholarPubMed
Elsenhans, BG, Hunder, G, Strugala, G & Schumann, K (1999) Longitudinal pattern of enzymatic and absorptive functions in the small intestine of rats after short-term exposure to dietary cadmium chloride. Archives of Environmental Contamination and Toxicology 36. 341–346CrossRefGoogle ScholarPubMed
Environmental, Resources Management (1999) Study on Data Requirements and Programme for Data Production and Gathering to Support a Future Evaluation of the Risks to Health and the Environment from Cd in Fertilisers. Final Report to the European Commission – DGIII, March 1999 London ERMGoogle Scholar
Environmental, Resources Management (2001) Analysis and Conclusions from Member States' Assessment of the Risk to Health and the Environment from Cd in Fertilisers. Final Report to the European Commission – DGIII, October 2001 London ERMGoogle Scholar
Foulkes, EC (1984) Intestinal absorption of heavy metals Pharmacology of Intestinal Permeation. Vol. 1, 543–565 Csáky TZ Berlin Springer VerlagCrossRefGoogle Scholar
Foulkes, EC & Voner, C (1981) Effects of zinc status, bile and other endogenous factors on jejunal cadmium absorption. Toxicology 22. 115–122CrossRefGoogle Scholar
Fowler, BA (1996) The nephropathology of metals Toxicology of Metals 721–729 Chang LW Boca Raton, FL CRC PublishersCrossRefGoogle Scholar
Fowler, D, Mourne, R & Branford, D (1995) The application of Pb-210 inventories in soil to measure long-term average wet deposition of pollutants in complex terrain. Water, Air and Soil Pollution 85. 2113–2118CrossRefGoogle Scholar
Fox, MR (1987) Assessment of cadmium, lead and vanadium status of large animals as related to the human food chain. Journal of Animal Science 65. 1744–1752Google Scholar
Galey, FD, Slenning, BD, Anderson, ML, Breneman, PC, Littlefield, ES, Melton, L & Tracey, ML (1990) Lead concentration in blood and milk from periparturient dairy heifers seven months after an episode of acute lead toxicosis. Journal of Veterinary Diagnostic Investigation 2. 222–226CrossRefGoogle ScholarPubMed
Gawthorne, JM (1987) Copper interactions Copper in Man and Animals Vol. 1, 79–99 Howell JM Gawthorne JM Boca Raton, FL CRC Press IncGoogle Scholar
Goyer, RA & Wilson, MH (1975) Lead-induced inclusion bodies. Results of ethylenediaminetetra-acetic acid treatment. Laboratory Investigation 32. 149Google Scholar
Grace, ND, Rounce, JR & Lee, J (1993) Intake and excretion of cadmium in sheep fed fresh herbage. Proceedings of the New Zealand Society of Animal Production 53. 251–253Google Scholar
Groten, JP, Luten, JB, Bruggeman, IM, Temmink, JHM & Vanbladeren, PJ (1992) Comparative toxicity and accumulation of cadmium chloride and cadmium metallothionein in primary cells and cell lines of rat intestine, liver and kidney. Toxicology Vitro 6. 509–517CrossRefGoogle ScholarPubMed
Hammond, PB & Aronson, AL (1964) Lead poisoning in cattle and horses in the vicinity of a smelter. Annals of the New York Academy of Sciences 111. 595–611CrossRefGoogle ScholarPubMed
Hapke, H-J & Abel, J (1977) Die Ansammlung von Cadmim in verzehrbaren Geweben in abhangigkeit von der Cd-Menge im Futter (The accumulation of cadmium in the food chain from cadmium in fodder). Archiv fur Lebensmittelhygiene 28. 174–177Google Scholar
Harrison, PD & Dyer, MI (1984) Lead in mule deer forage in Rocky Mountain National Park, Colorado. Journal of Wildlife Management 48. 510–517CrossRefGoogle Scholar
Healy, WB (1967) Ingestion of soil by sheep. Proceedings of the New Zealand Society of Animal Production 27. 109–120Google Scholar
Henry, RB, Liu, J, Choudhuri, S & Klassen, CD (1994) Species variation in hepatic metallothionein. Toxicology Letters 74. 23–33CrossRefGoogle ScholarPubMed
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. Effects of type of soil and level of sewage sludge in the diet. Animal Science 67. 73–86CrossRefGoogle Scholar
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 ingestion of soils treated historically with sewage sludge. Animal Science 67. 87–96CrossRefGoogle Scholar
Hodge, VF & Stallard, MO (1986) Platinum and palladium in roadside dust. Environmental Science and Technology 20. 1058–1060CrossRefGoogle ScholarPubMed
Howard, BJ & Beresford, NA (1994) Radiocaesium contamination of sheep in the United Kingdom after the Chernobyl accident Pollution in Livestock Production Systems 97–118 Ap Dewi I Axford RFE Fayez I Aarai M Omed HM Wallingford, Oxon CAB InternationalGoogle Scholar
International, Atomic & Energy, Authority (1990) The Radiological Consequences in the USSR from the Chernobyl Accident: Assessment of Health and Environmental Effects and Evaluation of Protective Measures Vienna IAEAGoogle Scholar
Johnson, MS & Eaton, JW (1980) Environmental contamination through residual trace metal dispersal from a derelict lead-zinc mine. Journal of Environmental Quality 9. 175–179CrossRefGoogle Scholar
Jones, KC, Symon, C, Taylor, PJL, Walsh, J & Johnston, AE (1991) Evidence for a decline in rural herbage lead levels in the UK. Atmospheric Environment 25. 361–369CrossRefGoogle Scholar
Jones, SG, Brow, KW, Deuel, LE & Donnelly, KC (1979) Influence of simulated rainfall on the retention of sludge heavy metals by the leaves of forage crops. Journal of Environmental Quality 8. 69–72CrossRefGoogle Scholar
Kello, D & Kostial, K (1977) Influence of age on whole-body retention and distribution of 115 m cadmium in the rat. Environmental Research 14. 92–98CrossRefGoogle Scholar
Kiyozumi, M & Kojima, S (1978) Studies on poisonous metals V. Excretion of cadmium through bile and gastro-intestinal mucosa and effect of chelating agents on its excretion in cadmiumpretreated rats Chemical Pharmacology Bulletin, Tokyo 26. 3410–3415Google Scholar
Kjellstrom, T & Nordberg, GF (1978) A kinetic model of cadmium metabolism in the human being. Environmental Research 16. 248–269CrossRefGoogle ScholarPubMed
Klessa, DA, Desira-Buttegieg, A (1992) The adhesion to leaf surfaces of heavy metals from sewage sludge applied to grassland. Soil Use and Management 8. 115–121CrossRefGoogle Scholar
Koo, SI, Fullmer, CS & Wasserman, RH (1978) Intestinal absorption and retention of 109 Cd; Effects of cholecalciferol, calcium status and other variables. Journal of Nutrition 108. 1812–1822CrossRefGoogle Scholar
Lamy, I, Bourgeois, S & Bermond, A (1993) Soil cadmium mobility as a consequence of sewage sludge disposal. Journal of Environmental Quality 22. 731–737CrossRefGoogle Scholar
Lee, J, Grace, ND, Mackay, AD, Hedley, MJ & Rounce, JR (1993) Cadmium in soil, pasture and grazing ruminants Proceedings of the XVII International Grassland Congress 817–818 Palmerston North, New Zealand Massey UniversityGoogle Scholar
Lee, J, Masters, DG, White, CL, Grace, ND & Judson, GJ (1999) Current issues in trace element nutrition of grazing livestock in Australia and New Zealand. Australian Journal of Agricultural Research 50. 1341–1364Google Scholar
Lee, J, Teloar, BP & Harris, PM (1994) Metallotheonein and trace element metabolism in sheep tissues in response to high and sustained Zn dosages. I. Characterisation and turnover of metallothionein isoforms. Australian Journal of Agricultural Research 45. 303–320CrossRefGoogle Scholar
Livens, FR, Horrill, AD & Singleton, DL (1991) Distribution of radionuclides in the soil-plant systems of upland areas. Health Physics 60. 539–545CrossRefGoogle ScholarPubMed
Livesey, CT (1994) Contamination of animal feeds: A review of principal causes, detection, investigation and control of toxic contaminants Pollution in Livestock Production Systems 19–41 Ap Dewi I Axford RFE Fayez I Aarai M Omed HM Wallingford, Oxon CAB InternationalGoogle Scholar
McGrath, SP & Loveland, PJ (1992) The Soil Geochemical Atlas of England and Wales Glasgow Blackie Academic and ProfessionalGoogle Scholar
Marschner, H (1995) Mineral Nutrition of Plants London Academic PressGoogle Scholar
Martin, MH & Coughtrey, PJ (1982) Biological Monitoring of Heavy Metal Pollution London Applied Science PublishersCrossRefGoogle Scholar
Marumo, F & Li, JP (1996) Renal disease and trace elements. Nippon Rinsho 54. 93–98Google ScholarPubMed
Mench, M & Martin, E (1991) Mobilisation of cadmium and other metals from two soils by plant root exudates of Zea mays L., Nicotiana tabacum L., and Nicotiana rustica L. Plant and Soil 132. 187–196CrossRefGoogle Scholar
Mench, M, Morel, JL, Guckert, A & Guillet, B (1988) Metal binding with root exudates of low molecular weight. Journal of Soil Science 39. 521–527CrossRefGoogle Scholar
Merian, E (1991) Speciation of metal compounds (interrelation between chemistry and biology). Trac-Trends in Analytical Chemistry 10. 172–175CrossRefGoogle Scholar
Mills, CF & Dalgarno, AC (1972) Copper and zinc status of ewes and lambs receiving increased dietary concentrations of cadmium. Nature 239. 171–173CrossRefGoogle ScholarPubMed
Ministry of Agriculture, Fisheries and Food (1993) Code of Good Practice for the Protection of Soil London MAFFGoogle Scholar
Mohamed, MO (2002) Effect of supplementary nutritive and toxic elements on the mineral balances and preferences of ruminants. PhD Thesis, University of Cambridge.Google Scholar
Motto, HL, Daines, RH, Chilko, DM & Motto, CK (1970) Lead in soils and plants: Its relationship to traffic volume and proximity to highways. Environmental Science and Technology 4. 231CrossRefGoogle Scholar
National, Research Council (1980) Lead in the Human Environment Washington, DC National Academy of SciencesGoogle Scholar
Nieboer, E & Richardson, DHS (1980) The replacement of the nondescript term ‘heavy metals’ by a biologically and chemically significant classification of metal ions. Environmental Pollution 1. 3–26Google Scholar
Nordberg, M & Nordberg, GF (1975) Distribution of metallothionein-bound cadmium and cadmium chloride in mice: preliminary studies. Environmental Health Perspectives 12. 103–108CrossRefGoogle ScholarPubMed
Oberleas, D, Muhrer, ME, O'Dell, BL (1966) Dietary metalcomplexing agents and zinc availability in the rat. Journal of Nutrition 90. 56–62CrossRefGoogle ScholarPubMed
Oskarsson, A, Jorhim, L, Sundberg, J, Nilsson, NG & Albanus, L (1992) Lead poisoning in cattle, transfer of lead to milk. Science of the Total Environment 111. 83–94CrossRefGoogle ScholarPubMed
Pigman, EA, Blanchard, J & Laird, HE (1997) A study of cadmium transport pathways using the Caco–2 cell model. Toxicology and Applied Pharmacology 142. 243–247CrossRefGoogle ScholarPubMed
Pinkerton, C, Hammer, DI, Birdbord, K, Creason, JP, Kent, JL & Murthy, GK (1973) Human milk as a dietary source of cadmium and lead Trace Substances in Environmental Health – VI. A symposium 000–000 Hemphill DD Columbia, MO University of MissouriGoogle Scholar
Piscator, M (1985) Dietary exposure to cadmium and health effects: impact of environmental changes. Environonmental Health Perspectives 63. 127–132CrossRefGoogle ScholarPubMed
Pittia, P (1992) Indagine sul contenuto in piombo in latte della Provincia di Udine (The content of lead in milk from the Province of Udine). Scienza e Tecnica Lattiero Casearia 43. 201–208Google Scholar
Prankel, S (2002) Models of cadmium accumulation in sheep and cattle as a part of the human food chain. PhD thesis, University of Cambridge.Google Scholar
Prankel, SH, Nixon, RM & Phillips, CJC (2001) A meta-analysis of cadmium accumulation in sheep liver and kidney. Toxicology 164. Suppl. 73Google Scholar
Rambeck, WA (1994) Influences on the carry-over of cadmium in the food chain. Proceedings of the Society of Nutrition Physiology 2. 23–29Google Scholar
Renberg, I, Brannvall, ML, Bindler, R & Emteryd, O (2000) Atmospheric lead pollution history during four millennia (2000 BC to 2000 AD) in Sweden. Ambio 29. 150–156CrossRefGoogle Scholar
Richards, MP & Cousins, RJ (1975) Mammalian zinc homeostasis; Requirement for RNA and metallothionein synthesis. Biochemical and Biophysical Research Communications 64. 1215–1223CrossRefGoogle ScholarPubMed
Sansom, BF (1989) An assessment of the risks to the health of grazing animals from the radioactive contamination of pastures. British Veterinary Journal 145. 206–211CrossRefGoogle Scholar
Savchenko, VK (1995) The Ecology of the Chernobyl Catastrophe Paris UNESCOGoogle Scholar
Smith, GM & White, CL (1997) A molybdenum-sulfur-cadmium interaction in sheep. Australian Journal of Agricultural Research 48. 147–154CrossRefGoogle Scholar
Snitsarev, V, Budde, T, Stricker, TP, Cox, JM, Krupa, DJ, Geng, L & Kay, AR (2001) Fluorescent detection of Zn(2+)-rich vesicles with Zinquin: mechanism of action in lipid environments. Biophysical Journal 80. 1538–1546CrossRefGoogle ScholarPubMed
Spears, JW (1966) Organic trace elements in ruminant nutrition. Animal Feed Science and Technology 58. 151–163CrossRefGoogle Scholar
Stark, BA, Livesey, CT, Smith, SR, Wilkinson, JM & Cripps, PJ (1998) Implications of Research on the Uptake of PTEs from Sewage Sludge by Grazing Animals. Report to the Department of the Environment, Transport and the Regions (DETR) and the Ministry of Agriculture, Fisheries and Food (MAFF) London H. M. Stationery OfficeGoogle Scholar
Starnes, SR, Spears, JW, Froetschel, MA & Croom, WJ (1984) Influence of monensin and lasalocid on mineral metabolism and ruminal urease activity in steers. Journal of Nutrition 114. 518–525CrossRefGoogle ScholarPubMed
Statutory, Instrument (1989) The Sludge (Use in Agriculture) Regulations Statutory Instrument no. 1263 London H. M. Stationery OfficeGoogle Scholar
Statutory, Instrument (1995) The Feeding Stuffs Regulations 1995. Statutory Instrument no. 1412 London H. M. Stationery OfficeGoogle Scholar
Strojan, ST & Phillips, CJC (2002) The detection and avoidance of lead contaminated pasture by cattle. Journal of Dairy Science 85. 3045–3053CrossRefGoogle Scholar
Sumner, ME & McLaughlan, MJ (1996) Contaminants and Soil Environment in the Australasia-Pacific Region Dordrecht, The Netherlands Kluwer Academic PublishersGoogle Scholar
Suttle, NF (1994) Meeting the copper requirements of ruminants Recent Advances in Animal Nutrition 173–178 Garnsworthy PC Cole DJA Nottingham Nottingham University PressGoogle Scholar
Swarup, D (1993) Lead in feed and blood of bovines in varied environmental localities. Indian Journal of Veterinary Research 2. 34–37Google Scholar
Taguchi, T & Suzuki, S (1978) Cadmium binding components in the supernatant fraction of the small intestinal mucosa of rats administered cadmium. Japanese Journal of Hygiene 33. 467–473Google ScholarPubMed
Turecki, T, Cibulka, J, Slamova, A & Barcalikova, R (1998) Effect of organic and inorganic forms of dietary cadmium on cadmium, zinc, copper, iron and manganese availability to rats. Tierphysiologie Tierartz Futtermittung 78. 119–128Google Scholar
Underwood, EJ & Suttle, NF (1999) The Mineral Nutrition of Livestock 3rd ed. 514–517 Wallingford, Oxon CABI InternationalCrossRefGoogle Scholar
Valberg, LS, Haist, J & Cherian, MG (1977) Cadmium-induced enteropathy: comparative toxicity of cadmium chloride and cadmium-thionein. Journal of Toxicology and Environmental Health 2. 963–975CrossRefGoogle ScholarPubMed
Walker, CH, Hopkin, SP, Sibly, RM & Peakall, DB (1996) Principles of Ecotoxicology 67–103 London Taylor and Francis LtdGoogle Scholar
Ward, NI, Brooks, RR & Roberts, E (1978) Blood lead levels in sheep exposed to automotive emissions. Bulletin of Environmental Contamination and Toxicology 20. 44–51CrossRefGoogle ScholarPubMed
Ward, NI & Savage, MJ (1994) Elemental status of grazing animals located adjacent to the London Orbital (M25) motorway. Science of the Total Environment 147. 185–189CrossRefGoogle Scholar
Wilkinson, JM, Hill, J & Livesey, CT (2001) Accumulation of potentially toxic elements by sheep grazed on grassland given repeated applications of sewage sludge. Animal Science 72. 179–190CrossRefGoogle Scholar
Wilkinson, JM, Hill, J & Hillman, JP (2003) The accumulation of potentially toxic elements in edible body tissues of lambs after a single application of sewage sludge. Water Research 37. 128–138CrossRefGoogle ScholarPubMed
Williams, CH & David, DJ (1973) The effects of superphosphate on the cadmium content of soils and plants. Australian Journal of Soil Science Research 11. 43–56CrossRefGoogle Scholar
Wilson, DO & Cline, JF (1966) Removal of plutonium 239, tungsten 185 and lead 210 from soils. Nature 209. 941–942CrossRefGoogle Scholar
Winteringham, FPW (1989) Radioactive Fallout in Soils, Crops and Food. FAO Soils Bulletin no. 61 Rome FAOGoogle Scholar
Wiren, N, von, Rumheld, V, Morel, JL, Guckert, A, Marschner H (1993) Influence of microorganisms on iron acquisition in maize. Soil Biology and Biochemistry 25. 371–376Google Scholar
Zachou, E, Phillips, CJC & Chiy, PC (1997) Relative effects of organic and inorganic sources of cadmium on nutrient bioavailability Bioavailability 97, Conference Proceedings 135 Wageningen, The Netherlands The VLAG Graduate SchoolGoogle Scholar