Document Type : Research article
Authors
Food Inspection Lab. Alexandria, Animal Health Research Institute, Dokki, Giza.
Abstract
Keywords
Food Inspection Lab. Alexandria,
Animal Health Research Institute, Dokki, Giza.
Levels Of Some Heavy Metal Residues
In Meat Of Different Species In The West
Of Alexandria
(With 2 Tables)
By
M.A. Abd-Allah and Nabila F. Soliman
(Received at 22/12/2009)
مستويات بعض العناصر الثقيلة فى اللحوم المختلفة فى غرب الاسکندرية
محمد احمد محمد عبدالله ، نبيلة فؤاد سليمان
تم قياس مستوى ترکيز کل من العناصر الثقيلة التالية: الحديد والنحاس والمنجنيز والرصاص والنيکل فى لحوم الابقار والاغنام والماعز فى ثلاث مناطق غرب مدينة الاسکندرية هى العامرية وبرج العرب وکنج مريوط وذ لک خلال شهر اغسطس 2008 و قد اسفرت الدراسة عن وجود اختلاف معنوى فى ترکيزات کل من الحديد والنحاس والمنجنيز فى اللحوم المختلفة وذلک من منطقة الى اخرى بالاضافة الى الاختلاف الذى يعزى الى نوع الحيوان. اما عنصرى النيکل والرصاص فلم يوجد اى فروق معنوية فى ترکيزاتهم فى اللحوم فى المناطق الثلاث وان کانت توجد فروق معنوية ترجع لنوع الحيوان فى حالة عنصر الرصاص وذلک فى منطقة العامرية وبرج العرب. وبشکل عام جميع ترکيزات العناصر تم مناقشتها ومراجعتها لما هو مسموح به فى غذاء الانسان.
SUMMARY
Manganese, copper, iron, nickel and lead concentration levels have been determined in muscle meat of cattle, sheep and goat from three different sites in the western part of Alexandria city during August 2008 (El Amiriya, Burg Alarab and King Marriott). The mean values obtained related to wet weight for beef, mutton and chevon. The results showed that the concentration level of Fe > Cu > Mn > Pb > Ni in all samples. Substantial differences have been found in the mean copper, manganese and iron among the sites of collection. On the other hand, species difference was significantly clear in case of iron concentration in all sites and lead concentration in two sites (El Amiriya and Burg Alarab). The mean and maximum concentrations of lead found in meat of animals in the present study were low. The results obtained were compared with the literature data on the concentrations of the metals examined in meat.
Key words: Heavy metal,residues in meat, Alexandria,
environmental pollution
Introduction
The contamination of pastures with potentially-toxic metals (PTM) and their accumulation in grazing animals can occur on soils that are naturally rich in metals following accidental or anthropogenic events and also, following the prolonged use of sewage sludge as a fertilizer (Martin and Coughtrey, 1982; Howard and Beresford, 1994; Wilkinson et al., 2001).
Nieboer and Richardson (1980) classified ‘heavy metal’ chemically as elements with a density > 5 g/l and grouped them into three classes: A; B; and borderline. Class A elements (e.g. Cs, Mn, and Sr) have a preference for ligands containing oxygen. Class B elements (.e.g. Cd, Cu, Hg, Ag) show a preference to form ligands with nitrogen or sulpher. Borderline elements (e.g. Zn, Pb, Fe, Cr, Co, Ni, As, Sn, V) are of intermediate nature between classes A and B. This classification is important biologically. The characteristic of Class B elements to form ligands with N and/or S includes metallothioneins, phytochelatin and caeruloplasmin (Cousins, 1985; Lee et al., 1994; Marschner, 1995; Underwood and Suttle, 1999) and excretion in bile e.g. Cd; (Kiyozumi and Kojima, 1978). In grazing mammals the elements Cd and Pb tend to accumulate in the liver and kidneys, and in some cases (e.g. Pb) also in bone (Lee et al., 1999). Many elements interfere with essential enzyme reactions and/or organ function; hence their potential toxicity to the grazing animal and man.
Copper (Cu) is an essential trace element for animals; it is required for normal biological activity of many enzymes, haemoglobin formation and hair keratin (Underwood, 1977; Prohaska and Gybina, 2004). High concentration of copper oxide may result from welding operations. The corrosion of copper containing alloys in pipe fitting may add measurable amount of copper into the water. Copper toxicity is manifested by nausea, vomiting, diarrhea and intestinal pain. While, copper deficiency results in anemia. On the other hands, the congenital inability to excrete copper and its accumulation in the body known as Wilson, S disease (Greenwood and Earnshaw, 1986).
Iron (Fe) has a number of fundamental roles in cellular biochemistry and metabolism. These include oxygen binding to heme proteins and the formation of active centers in enzymes involved in the mitochondrial electron transport chain. Iron canalso vary its redox state and can be rapidly oxidised from Fe2+ to Fe3+ (ferrous to ferric iron) in the presence of oxygen.This reaction generates the superoxide anion, which througha series of redox reactions leads to the generation of toxichydroxyl radicals. Thus iron can be both toxic and beneficialto organisms, and its status in the body must be carefullyregulated to provide sufficient iron for biological functions,whilst avoiding excess Fe2+ which can lead to oxidative stress(De Silva et al., 1996; Aisen et al., 2001).
Manganese (Mn) and its compounds exist naturally in the soil, rivers, lakes, underground water and in the air. In addition manganese can be introduced by human activity. Manganese can be released into the air by industry and by the burning of fossil fuels. Manganese from these human-made sources can enter surface water, groundwater, and sewage waters. Small manganese particles can also be picked up by water flowing through landfills and soil. The chemical state of manganese and the type of soil determine how fast it moves through the soil and how much is retained in the soil. Maneb and mancozeb, two pesticides that contain manganese, may also add to the amount of manganese in the environment when they are applied to crops or released to the environment from packaging factories. There is information on the amount of maneb and mancozeb released into the environment from facilities that make or use these pesticides. However, the amount of manganese in the environment because of the release and use of these pesticides is not known.
Nickel (Ni) is a natural element of the earth's crust; therefore, small amounts are found in food, water, soil, and air. Nickel is an essential nutrient for some mammalian species, and has been suggested to be essential for human nutrition. By extrapolation from animal data, it is estimated that a 70-kg person would have a daily requirement of 50 µg per kg diet of nickel (ATSDR, 1997). Food is the major source of nickel exposure, with an average intake for adults estimated to be approximately 100 to 300 micrograms per day (µg/d) (EPA, 1986 and ATSDR, 1997). There is some evidence that a few people may develop a skin sensitivity reaction to nickel. For these people, acid food cooked in stainless steel utensils and canned food may need to be avoided.
Lead (Pb) may enter the atmosphere during mining, smelting, refining, also automobile gasoline contains tetra-ethyl lead as knock inhibitor that is burned enters the atmosphere and manufacturing processes and by the use of lead containing products. Lead intake occurs from the consumption of fruit juices, food stored in lead lined containers, cosmetics, cigarettes (Benneth, 1981). Lead is able to cross the placenta as early as the 12th-14th week of gestation. Cord blood concentrations of lead are generally equivalent to that of the mother, or just a bit lower. Lead is not easily excreted, so it will continue to accumulate in fetal tissues throughout gestation, mostly accumulating in fetal brain (Schardein, 1998). Excess lead can cause serious damage to the brain, kidneys, nervous system and red blood cells. Young children, infants and fetuses are particularly vulnerable to lead poisoning. US environmental protection agency (EPA) says that lead may be implicated in causing leukemia (Anonymous, 2002).
The aim of the present study was determination of Fe, Cu, Pb, Mn and Ni concentrations in beef, mutton and goat meat from three different sites in west of Alexandria
Materials and Methods
Statistical Analysis: Comparisons of metal concentrations between sites for each species and between different species in each site were done with Analysis of Variance (ANOVA) and Fisher’s Least Significant Difference (LSD), using the Statistical Analysis System (SPSS 7.5, Michigan Avenue, Chicago).
Results
Table 1: Metal concentration level (mg/kg wet weight ) in beef, mutton and chevon from different areas in western of Alexandria
|
|
Beef |
Mutton |
chevon |
||||||
|
|
El Amiriya |
Burg Alarab |
King Marriott |
El Amiriya |
Burg Alarab |
King Marriott |
El Amiriya |
Burg Alarab |
King Marriott |
Fe |
Min- Max |
21.5- 23.17 |
23-24.7 |
23-24.2 |
20.52-22 |
22.1-24 |
23-22 |
20-21.1 |
22-22.7 |
21-22.1 |
F (p) |
47.9 (0.0001) |
43.8 (0.0001) |
47.9 (0.0001) |
|||||||
X`± SE |
22.5±0.17 |
21.34±0.15 |
20.43±0.12 |
24.06±0.17 |
22.99±0.18 |
22.14±0.08 |
23.63±0.17 |
22.5±0.14 |
21.53±0.14 |
|
El Amiriya |
|
1.16 a |
2.07 a |
|
1.07 b |
1.92 b |
|
1.13 c |
2.1 c |
|
Burg Alarab |
|
|
0.9 a |
|
|
0.85 b |
|
|
0.97 c |
|
Cu |
Min- Max |
1.59-9 |
1.19-8.6 |
1.8-9.2 |
3.9-8.72 |
5.91-8.32 |
6.5-8.7 |
4.79-10.9 |
4.39-9.5 |
5-7.5 |
F (p) |
7.5 (0.0025) |
5.7 (0.009) |
11.0 (0.0003) |
|||||||
X`± SE |
5.47±0.77 |
7.27±0.47 |
8.87±0.58 |
4.96±0.81 |
7.43±0.33 |
7.82±0.87 |
5.05±0.78 |
7.79±0.29 |
8.78±0.57 |
|
El Amiriya |
|
1.8 d |
3.4 d |
|
2.74 e |
3.13 e |
|
2.74 f |
3.73 f |
|
BurgAlarab |
|
|
1.6 |
|
|
0.39 |
|
|
0.99 |
|
Mn |
Min- Max |
0.2-3 |
1-3.2 |
1.5-4.05 |
0.2-2.3 |
1.1-3 |
1.8-3 |
0.1-2.2 |
2.89-1.6 |
0.9-4.21 |
F (p) |
6.2 (0.006) |
7.8 (0.0021) |
6.3 (0.0055) |
|||||||
X`± SE |
1.38±0.3 |
2.11±0.18 |
2.6±0.25 |
1.33±0.22 |
2.1±0.17 |
2.28±0.14 |
1.36±0.19 |
2.25±0.14 |
2.37±0.3 |
|
El Amiriya |
|
0.73 g |
1.22 g |
|
0.77 h |
0.95 h |
|
0.89 i |
1.01 i |
|
Burg Alarab |
|
|
0.49 |
|
|
0.18 |
|
|
0.12 i |
|
Pb |
Min- Max |
0.01-0.5 |
0.01-0.6 |
0.02-0.7 |
0.01-0.2 |
0.01-0.2 |
0.01-0.2 |
0.01-0.09 |
0.01-0.3 |
0.01-0.5 |
F (p) |
0.7 (0.5) |
0.2 (0.85) |
1.0 (0.37) |
|||||||
X`± SE |
0.2±0.06 |
0.22±0.06 |
0.13±0.04 |
0.06±0.02 |
0.07±0.02 |
0.05±0.02 |
0.06±0.01 |
0.08±0.03 |
0.12±0.05 |
|
El Amiriya |
|
0.02 |
0.07 |
|
0.01 |
0.01 |
|
0.02 |
0.06 |
|
Burg Alarab |
|
|
0.09 |
|
|
0.02 |
|
|
0.04 |
|
Ni |
Min- Max |
0.01-0.53 |
0.02-0.5 |
0.01-0.08 |
0.02-0.2 |
0.01-0.09 |
0.02-0.5 |
0.01-0.7 |
0.01-0.1 |
0.01-0.08 |
F (p) |
1.4 (0.26) |
1.7 (0.19) |
0.8 (0.46) |
|||||||
X`± SE |
0.12±0.05 |
0.12±0.05 |
0.04±0.01 |
0.06±0.02 |
0.04±0.01 |
0.11±0.04 |
0.08±0.04 |
0.06±0.01 |
0.03±0.01 |
|
El Amiriya |
|
0.0 |
0.08 |
|
0.02 |
0.05 |
|
0.02 |
0.05 |
|
Burg Alarab |
|
|
0.08 |
|
|
0.07 |
|
|
0.03 |
Fisher’s LSD (0.05): a=0.4304, b=0.421, c=0.4401, d= 1.8013, e=2.072, f= 1.6921, g= 0.7167, h= 0.5191, and i=0.6291
Table 2: Metal concentration level (mg/kg wet weight) in beef, mutton and chevon from different areas in western of Alexandria
|
|
El Amiriya |
Burg Alarab |
King Marriott |
||||||
|
|
Beef |
Mutton |
Chevon |
Beef |
Mutton |
Chevon |
Beef |
Mutton |
Chevon |
Fe |
Min- Max |
21.5-23.17 |
23-24.7 |
23-24.2 |
20.52-22 |
22.1-24 |
22-23 |
20-21.1 |
22-22.7 |
21-22.1 |
F (p) |
23.1 (0.0001) |
29.4 (0.0001) |
54.2 (0.0001) |
|||||||
X`± SE |
22.5±0.17 |
24.06±0.17 |
23.63±0.17 |
21.34±0.15 |
22.99±0.18 |
22.5±0.14 |
20.43±0.12 |
22.14±0.08 |
21.53±0.14 |
|
Beef |
|
1.56 a |
1.13 a |
|
1.65 b |
1.16 b |
|
1.71 c |
1.1 c |
|
Mutton |
|
|
0.43 |
|
|
0.49 |
|
|
0.61 c |
|
Cu |
Min- Max |
1.59-9 |
1.19-8.6 |
1.8-9.2 |
3.9-8.72 |
5.92-8.8 |
6.5-9 |
4.79-10.9 |
5.91-8.8 |
5-11 |
F (p) |
0.2 (0.78) |
0.5 (0.6) |
0.7 (0.49) |
|||||||
X`± SE |
5.47±0.77 |
4.69±0.81 |
5.05±0.78 |
7.27±0.47 |
7.43±0.33 |
7.79±0.29 |
8.87±0.58 |
7.82±0.87 |
8.78±0.57 |
|
Beef |
|
0.78 |
0.42 |
|
0.16 |
0.52 |
|
1.05 |
0.09 |
|
Mutton |
|
|
0.36 |
|
|
0.36 |
|
|
0.96 |
|
Mn |
Min- Max |
0.2-3 |
0.2-2.3 |
0.1-2.2 |
1-3.2 |
1.1-3 |
1.6-2.89 |
1.5-4.05 |
1.8-3 |
0.9-4.21 |
F (p) |
0.1 (0.99) |
0.3 (0.78) |
0.5 (0.61) |
|||||||
X`± SE |
1.38±0.3 |
1.33±0.22 |
1.36±0.19 |
2.11±0.18 |
2.1±0.17 |
2.25±0.14 |
2.60±0.25 |
2.28±0.87 |
2.37±0.3 |
|
Beef |
|
0.05 |
0.02 |
|
0.15 |
0.14 |
|
0.32 |
0.23 |
|
Mutton |
|
|
0.03 |
|
|
0.15 |
|
|
0.09 |
|
Pb |
Min- Max |
0.01-0.5 |
0.01-0.2 |
0.01-0.09 |
0.01-0.6 |
0.01-0.2 |
0.01-0.3 |
0.02-0.4 |
0.01-0.2 |
0.01-0.5 |
F (p) |
4.7 (0.018) |
4.0 (0.031) |
1.4 (0.27) |
|||||||
X`± SE |
0.2±0.06 |
0.06±0.02 |
0.06±0.01 |
0.22±0.06 |
0.07±0.02 |
0.08±0.03 |
0.13±0.04 |
0.05±0.02 |
0.12±0.05 |
|
Beef |
|
0.14 d |
0.14 d |
|
0.15 e |
0.14 e |
|
0.08 |
0.01 |
|
Mutton |
|
|
0.0 |
|
|
0.01 |
|
|
0.07 |
|
Ni |
Min- Max |
0.01-0.54 |
0.02-0.2 |
0.01-0.4 |
0.02-0.5 |
0.01-0.09 |
0.01-0.1 |
0.01-0.08 |
0.02-0.5 |
0.01-0.08 |
F (p) |
0.7 (0.49) |
1.7 (0.21) |
2.8 (0.079) |
|||||||
X`± SE |
0.12±0.05 |
0.06±0.02 |
0.08±0.04 |
0.12±0.05 |
0.04±0.01 |
0.06±0.01 |
0.04±0.01 |
0.11±0.04 |
0.03±0.01 |
|
Beef |
|
0.06 |
0.04 |
|
0.08 |
0.06 |
|
0.07 |
0.01 |
|
Mutton |
|
|
0.02 |
|
|
0.02 |
|
|
0.08 |
Fisher’s LSD (0.05): a=0.4856, b=0.4588, c=0.3434, d=0.0918, e=0.1298
Discussion
Environmental pollution is one of the most serious problems in our planet which require our urgent practical attention due to adverse effects on the behavior and life of mankind and considerably damaging the animal and plant life. Garbage's, trash, raw sewage, chemical effluents of the industries and emission of irritant and harmful gases from various sources are considered as the primary sources of pollutants. These pollutants emerge from rapid population growth, massive urbanization and extensive industrialization through the world. West of Alexandria city shows a big load of newly settled population in the last few decades due to forming several industrial cities, however, facing the load of transportation especially the cars and vehicles.
In the present study, metals measured in beef, mutton and chevon samples can be arranged in descending order according to their concentrations as Fe > Cu > Mn > Pb >Ni. Iron concentrations levels in beef, mutton and chevon were significantly different from an area to another. Hence, the areas can be arranged according to Fe concentrations in the meat samples collected from it as El Amiriya>Burg Alarab>King Marriott (Table1). Fe concentrations of mutton and chevon were significantly higher than beef in all areas. While, no significant differences between mutton and chevon except within King Marriott, mutton samples were significantly higher than chevon in Fe concentration. Generally, El Amiriya had the highest Fe concentration in all meat samples particularly in mutton. Previous study (Hoppe et al. 1955)pointed tothat acute toxicity of Fe ingested from normal dietary source has not been reported in human. However, acute toxicity may result from ingestion of large doses of medicinal Fe, especially in children. So, in present study Fe concentration level of meat may not contribute a hazard effect on human health.
Cu is an essential element present normally in sufficient amounts in forage and feed stuffs. Ruminants have a high capacity for hepatic copper storage and are also most susceptible to copper toxicosis. This is particularly in sheep. Concentrations of Cu in tissue are dependent on concurrent dietary levels of iron, zinc, cadmium, molybdenum, selenium and inorganic sulphur (Davis and Mertz, 1986).
In the present study, statistical significant differences were found among Cu concentration levels in beef samples collected from El Amiriya, Burg Alarab and King Marriott. Similar results were obtained with mutton and chevon samples (Table 1). On other hand, no significant differences found among meat samples can be related to species differences (Table 2). In general copper concentration levels in beef, mutton and chevon meat samples not exceeded the permissible limits (15mg Cu/kg wet weight) proposed by ES (1993). El Amiriya and Burg Alarab showed lower concentration levels of Cu in mutton and chevon than beef on contrast to Burg Alarab. This result may explained in the light of Walter study in 1986as that the distribution of the total body Cu among the tissues of animals varies with the species, age and Cu status.
Mn is an essential trace element and is necessary for good health. The human body typically contains small quantities of Mn and under normal circumstances; the body controls these amounts so that neither too little nor too much is present (ATSDR 2000).Significant differences in Mn concentration levels were found among beef samples collected from El Amiriya, Burg Alarab or King Marriott. Similar results obtained with mutton and chevon samples collected from the same areas (Table 1). But no significant differences in Mn concentration levels could be attributed to the species differences although; Mn concentration levels in mutton and chevon were higher than beef in all areas (Table 2). With regard to the effect of dietary Mn on human health, the NRC (1989) has recommended safe and adequate daily intake levels for Mn that ranged from 0.3 to 1mg/day for children up to 1year, 1-2mg/day for children up to age 10, and 2-5 mg/day children 10 and older. Additionally, the upper tolerable intake level of Mn for children (1-3years old) and male/females (19-20 years old) is 2 and 11mg/day, respectively.
The potential effects of Ni on human health is discussed previously (ATSDR, 1997), very small amounts of Ni in people’s diets may promote good health. However, some people exposed to small amounts of Ni for a long time develop an allergic reaction to it. The most common reaction is itching when Ni contacts their skin. In less common, severe cases, people experience vomiting and diarrhea when they swallow Ni or asthma attacks when they breathe it. In present study, the mean concentration levels of Ni in beef, mutton and chevon were not significantly different from area to anther and from species to anther species of animal (Table1 and 2). The mean daily intake of Ni assumed for an adult from food sources is therefore approximately 152 µg Ni per day (ATSDR, 1997). So, toxicity is considered unlikely to be a problem in humans with the current levels in meat samples.
The effects of Pb are similar across inhalation and oral routes of exposure. Pb has been shown to affect virtually every organ and system in the body in both humans and animals. The most sensitive effects of Pb appear to be neurological (particularly in children), hematological, and cardiovascular (ATSDR 1999). Pb concentration level in beef, mutton and chevon samples were not significantly differing from area to another within the same species (Table 1). However, the percentage of beef samples exceeded the permissible limits (0.1mg Pb/kg) proposed by ES (1993) which was 50% for El Amiriya, 60% for Burg Alarab and 30% for King Marriott. Also, for mutton samples were 20% for El Amiriya, 10% for Burg Alarab and 10% for King Marriott. As for Chevon samples it were 10% for El Amiriya, 20% for Burg Alarab, and 20% for King Marriott. Pb concentration levels of mutton and chevon samples were significantly lower than that of beef in El Amiriya as well as Burg Alarab. While, King Marriott did not show any differences among samples of different species (Table 2).
In conclusion the results of the present study indicated that beef, mutton and chevon may differ in metal concentrations from area to another in the western part of Alexandria. The environment may be contributed with an important part in this problem. So, This require more intensification of hygienic control that’s being applied upon such feeding stuffs, in addition, effective ecological measures should be taken that would have a beneficial effect on reducing metals in the animal feeds, water and air. Awareness of public about toxic metals, which may accumulate in beef, mutton and chevon meat and causing health problems.
References
Aisen, P.C. Enns and Wessling-Resnick, M. (2001): Chemistry and biology of eukaryotic iron metabolism. Int. J. Biochem. Cell Biol. 33,940 -959.
Anonymous (2002):Neb guide, published by cooperative extension institute of Agriculture and natural resources, University of Nebraska Lincoln.
ATSDR (1997): Agency for Toxic Substances and Disease Registry. Toxicological Profile for Nickel (Update). Public Health Service, U.S. Department of Health and Human Services, Altanta, GA.
ATSDR (1999): Agency for Toxic Substances and Disease Registry. Toxicological Profile for Lead (Update). Public Health Service, U.S. Department of Health and Human Services, Atlanta, GA.
ATSDR (2000): Agency for Toxic Substances and Disease Registry. Toxicological Profile for Manganese (Update). Public Health Service, U.S. Department of Health and Human Services, Atlanta, GA.
Benneth, B.G. (1981): Exposure commitment assessment of environmental pollution. Monitoring and assessment ResearchCenter. London, Vol.1.
Carvalho, S.M.M. and Ziemer, P.L. (1982): Distribution and clearance of 63NiCl2 in the rat: Intra tracheal study. Arch. Environ. Contam. Toxicol. 11: 245-248.
Cousins, R.J. (1985): Absorption, transport and hepatic metabolism of Cu and Zn: Special reference to metallothionein and caeruloplasmin Physiological Reviews65, 238–309.
Davis, G.K. and Mertz, W. (1986): in Trace Elements in Human and Animal Nutrition, Vol. 1, 5th Ed., W. Mertz (Ed.), Academic press, New York, Ch. 10.
De Silva, D.M.; Askwith, C.C. and Kaplan, J. (1996): Molecular mechanisms of iron uptake in eukaryotes. Physiol. Rev. 76, 31 -47.
EPA (1986):U.S. Environmental Protection Agency. Health Assessment. Document for Nickel. EPA/600/8-83/012F. NationalCenter for Environmental Assessment, Office of Research and Development, Washington, DC.
ES (1993): Egyptian Organization for Standardization and Quality Control. Maximum Level for Heavy Metal Contamination in Food. No. 2360.
Greenwood, N.N. and Earnshaw, A. (1986): Chemistry of the Elements. Pergamon press, Oxford, 12:5-14.
Holak, W. (1980): Analysis of foods for lead, cadmium, copper, zinc, arsenic, and selenium using closed system sample digestion: collaborative study. J. Assoc. Off. Anal. Chem.63 (3): 485-495.
Hoppe, J.O.; Marcelli, M.G. and Tainter, M.L. (1955): A review of the toxicity of iron compounds, Am. J. Med. Sci., 230(5), 558-571
Howard, B.J. and Beresford, N.A. (1994): Radiocaesium contamination of sheep in the United Kingdom after the Chernobyl accident. In Pollution in Livestock Production Systems, pp. 97–118 [I Ap Dewi, RFE Axford, I Fayez, M Aarai and HM Omed, editors]. Wallingford, Oxon. CAB International.
Kiyozumi, M. and 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 cadmium pretreated rats. Chemical Pharmacology Bulletin, Tokyo26, 3410–3415.
Lee, J.; Masters, D.G.; White, C.L.; Grace, N.D. and Judson, G.J. (1999): Current issues in trace element nutrition of grazing livestock in Australia and New Zealand. Australian Journal of Agricultural Research50, 1341–1364.
Lee. J.; Teloar, B.P. and Harris, P.M. (1994): Metallotheonein and trace element metabolism in sheep tissues in response to high and sustained Zn dosages. I. Characterization and turnover of metallothioneins isoforms. Australian Journal of Agricultural Research 45, 303–320
Marschner, H. (1995): Mineral Nutrition of Plants. London: Academic Press.
Martin, M.H. and Coughtrey, P.J. (1982): Biological Monitoring of Heavy Metal Pollution. London: Applied Science Publishers.
Nieboer, E. and Richardson, D.H.S. (1980): The replacement of the nondescript term ‘heavy metals’ by a biologically and chemically significant classification of metal ions. Environmental Pollution1B, 3–26.
NRC (1989): National Research Council Recommended. Dietary Allowances, North Revised Edition. National Academy of Sciences, Washington, D.C., United States of America
Prohaska, J.R. and Gybina, A.A. (2004): Intracellular copper transport in mammals. The Journal of Nutrition, 134, 1003-1006.
Schardein, J. (1993): Chemically Induced Birth Defects. 2nd ed., New York. Marcel Dekker, Inc.
Sunderman, F. and Oskarsson, W.A. (1991): Metals and their compounds in the environment. VCH Verlagsgesellschaft mbH, Weinheim 25, 1101-1126.
Underwood, E.J. (1977): Trace Elements in Human and Animal Nutrition, 4th Ed, Academic Press, Inc., New York.
Underwood, E.J. and Suttle, N.F. (1999): The Mineral Nutrition of Livestock, 3rd ed., pp. 514–517. Wallingford, Oxon. CABI International.
Walter, M. (1986): Trace Elements in Human and Animal Nutrition, 5th Ed, Vol. 2. Academic Press Inc., Harcourt Brace Jovanovich Publisher.
Wilkinson, J.M.; Hill, J. and Livesey, C.T. (2001): Accumulation of potentially toxic elements by sheep grazed on grassland given repeated applications of sewage sludge. Animal Science 72, 179–190.