Accepted Manuscript

Title: Arsenic, cadmium, cobalt, copper, lead, mercury,

molybdenum, selenium and zinc concentrations in liver,
kidney and muscle in Australian sheep

Author: D.J. MacLachlan K. Budd J. Connolly J. Derrick L.

Penrose T. Tobin

PII: S0889-1575(16)30072-2
DOI: http://dx.doi.org/doi:10.1016/j.jfca.2016.05.015
Reference: YJFCA 2724

To appear in:

Received date: 12-2-2016

Revised date: 25-5-2016
Accepted date: 30-5-2016

Please cite this article as: MacLachlan, DJ.,
J., Penrose, L., & Tobin, T., Arsenic,
mercury, molybdenum, selenium and zinc
and muscle in Australian sheep.Journal of
http://dx.doi.org/10.1016/j.jfca.2016.05.015
Budd, K., Connolly, J., Derrick,
cadmium, cobalt, copper, lead,
concentrations in liver, kidney
Food Composition and Analysis

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Page 1 of 33

Arsenic, cadmium, cobalt, copper, lead, mercury, molybdenum, selenium

and zinc concentrations in liver, kidney and muscle in Australian sheep

DJ MacLachlan, K Budd, J Connolly, J Derrick, L Penrose and T Tobin

Australian Government Department of Agriculture, 18 Marcus Clarke Street, Canberra City, ACT

2601, Australia

Corresponding author:

DJ MacLachlan, Australian Government Department of Agriculture and Water Resources, 18 Marcus

Clarke Street, Canberra City, ACT 2601, Australia. E-mail: dugald.maclachlan@agriculture.gov.au

Page 2 of 33

Highlights

 Study estimated the concentration of As, Cd, Co, Cu, Pb, Hg, Mo, Se and Zn in sheep liver,

kidney and muscle.

 Levels were within acceptable ranges

 For potentially toxic elements As, Cd, Pb and Hg the contribution of Australian sheep meat to

consumer exposure is low.

Abstract

Matched muscle, liver and kidney samples from 152 sheep in different states of Australia were

analysed for trace elements. Mean levels found in muscle, livers and kidneys were 0.010, 0.010 and

0.011 mg kg-1 (fresh weight) for arsenic; 0.0035, 0.280 and 0.853 mg kg-1 for cadmium; 0.006, 0.060

and 0.044 mg kg-1 for cobalt; 0.74, 66.0 and 2.72 mg kg-1 for copper; 0.007, 0.040 and 0.057 mg kg-1

for lead; 0.0025, 0.0034 and 0.0061 mg kg-1 for mercury; 0.014, 1.05 and 0.44 mg kg-1 for

molybdenum; 0.09, 0.31 and 0.95 mg kg-1 for selenium; and 40.4, 37.2 and 20.8 mg kg-1 for zinc. The

lead, mercury and arsenic concentrations in meat and organs may be regarded as low, but the

concentrations of cadmium in kidney and livers are sometimes relatively high. Apart from cadmium,

lead and selenium, tissue trace element concentrations were not related to the age of the investigated

animals. Differences in essential and non-essential trace element accumulation in sheep reared in

different regions (states and territories) of Australia were also evaluated. Cadmium, lead and selenium

were the only elements that appeared to show significant regional differences. Overall the results

show that concentrations of the elements considered are within current acceptable ranges.

Abbreviations: AUS Australia; DW dry weight basis; FSANZ Food Standards Australia New

Zealand; FW fresh weight basis; GEMS/Food Global Environment Monitoring System - Food

Contamination Monitoring and Assessment Programme; JECFA Joint FAO/WHO Expert Committee

on Food Additives; LOD limit of detection; LOQ limit of quantification; NIST National Institute of

Standards and Technology; NSW New South Wales; PTMI provisional tolerable monthly intake;
Page 3 of 33

PTWI provisional tolerable weekly intake; QLD Queensland; SA South Australia; TAS Tasmania;

VIC Victoria; WA Western Australia.

Keywords: arsenic, cadmium, cobalt, copper, lead, mercury, molybdenum,selenium, zinc, kidney,

liver, muscle, sheep

1. Introduction

The presence of various trace elements in farm animals is of interest from both animal and human

health perspectives. Trace elements are those that are required by animals in amounts measured in

either micrograms (µg) or milligrams (mg) per kilogram (kg) of dry matter ingested. They include

iron (Fe), manganese (Mn), zinc (Zn), copper (Cu), iodine (I), cobalt (Co), molybdenum (Mo) and

selenium (Se) (Suttle 2010). Levels of these elements in tissues can provide an indication of the

nutritional status of the animals. Exposure of livestock to either high levels of toxic metals, such as

cadmium (Cd) and lead (Pb), or less than optimal levels of the essential trace elements, such as Mo

and Se, can adversely affect animal productivity (Suttle 2010). Sheep meat can form an important part

of the human diet and contributes to the overall exposure of consumers to toxic elements through the

diet. A number of studies have reported concentrations of various elements in sheep tissues (Bilandžić

et al., 2010; Caggiano et al., 2005; Gerber et al., 2009; Ikem et al., 2015; Jorhem 1999; Reykdal &

Thorlacius 2001; Rudy 2009; Şenavci et al., 1997; Solly et al., 1981; Zantopoulos et al., 1999). As

production practices change with time it is important to periodically update our knowledge of trace

elements in sheep tissues.

In Australia, lambs are produced in a wide range of climates - from the arid and semi-arid parts of the

inland region to the high rainfall areas of New South Wales (NSW), Victoria (VIC), South Australia

(SA) and Tasmania (TAS) (Anon, 2012, Lehane et al., 1997). The southwest corner of Western

Australia (WA) is also an important sheep-producing region (Lehane et al., 1997). Mutton and wool

production however, is spread throughout the sheep-producing areas. Sheep breeds in Australia can
Page 4 of 33

generally be classified into three major groups: those bred for wool production, those bred for meat

production and dual-purpose sheep grown for both wool and meat (Thomas 1986). Differences in the

productions systems between states, including breeds of sheep, feeds used and soils, may lead to

differences in exposure of sheep to the elements studied and differences in concentrations in tissues.

In Australia, deficiency syndromes of grazing sheep are well recognised for Cu, I, Co and Se, whereas

poisoning is chiefly restricted to Cu, and less commonly to Se, although Mo excess can induce a

syndrome of Cu deficiency (Australian Agricultural Council 1990; Judson and McFarlane 1998).

The elements selected for study are either known to be physiologically important in livestock and to

be deficient or elevated in some soils of Australia (Co, Cu, Mo, Se and Zn) (Judson and McFarlane

1998, Masters 1996) or to be of interest to food safety regulators (As, Cd, Pb and Hg) (MacLachlan et

al., 2013). This paper explores concentrations of the elements in sheep kidney, liver and muscle

tissues, the major tissues for human consumption and in trade, and the influence on these

concentrations of age and the state of Australia where animals were raised. The levels found were

compared with those reported in sheep tissues from earlier studies in Australia and with those reported

in other countries. Estimates of consumer exposure from consumption of Australian sheep meat are

compared with relevant health-based guidance values.

2. Materials and methods

2.1. Reagents

NIST traceable internal standard solutions containing a mixture of authentic elements (HPS-Q16544

Solution A and Solution B) were obtained from High-Purity Standards, Charleston, SC. The certified

reference material for bovine liver, AGAL-4, was obtained from the Australian government National

Measurement Institute. The nitric acid was prepared in-house by double sub-boiling distillation of

analytical reagent grade material (70%) obtained from Ajax Finechem.

2.2. Samples
Page 5 of 33

Kidney (two kidneys per animal, ca. 200 g), liver (500 g) and muscle (skeletal muscle 500 g, typically

flank) tissue of sheep were collected from randomly selected abattoirs around Australia by the

National Residue Survey (NRS) in 2009 and 2010. The samples were taken as part of a survey of

background metal concentrations in tissues of sheep in Australia. The number of samples collected

per state was determined by production in the previous 12 months (slaughter numbers) and further

subdivided into three age groups; lambs (<12 months), young (1‒3 years old) and mature (>3 years

old). Samples were collected from 16 of 23 export registered sheep abattoirs with a combined

throughput that accounted for 54% of the sheep slaughtered in Australia. The proportion of samples

collected per state was broadly in line with the proportion of the national flock in the respective state

(NSW 34.6%, VIC 21.3%, QLD 5.5%, SA 13.3%, WA 22.3%, TAS 2.8%). The tissues were sampled

by officials according to procedures outlined by the NRS (NRS 2009). Tissues were stored frozen

until analysis.

2.3. Analytical methods

At the time of analysis, the tissues were partially thawed and homogenised in a commercial

polycarbonate food processor. In the case of kidney the whole organ was homogenised. For each

tissue, 1-g sub-samples were mineralised by acid digestion (nitric acid). Trace element concentrations

in all digests were quantified by inductively coupled plasma-mass spectrometry (ICP-MS; Elan 9000

ICP-MS; PerkinElmer, Waltham, MA), in the case of As, Cd, Co, Hg, Mo, Pb and Se, and by

inductively coupled optical emission spectroscopy (ICP-OES; Varian MPX ICP-OES) for Cu and Zn.

Quality control measures included in each batch of 1-50 samples were: analysis of reagent blanks,

NIST traceable internal standards, duplicate samples and Certified Reference Materials (AGAL-4).

Additionally the laboratory also ran batch and monthly intra-laboratory check samples and

participated in regular proficiency tests. In case of deviations from a set of common criteria for

tolerable variations of blanks and values obtained for the reference materials, analyses in a batch were

repeated. Sub-samples were retained for repeat analysis where required. The analyses of As, Cd, Cu,

Hg, Pb, Se and Zn in meat and organs were performed under ISO/IEC 17025:2005 accreditation. The

limit of detection was determined as 1.64 times the standard deviation of the measured concentration
Page 6 of 33

of 21 low-level fortified reagent blanks taken through the analytical procedure (as per first reference),

multiplied by 2. The limit of quantification (LOQ) for the analysed trace elements was calculated

from 21 procedure blanks multiplied with the dilution factor. The LOQ values, expressed on a fresh

weight basis, were 0.005 mg Cd kg-1, 0.005 mg Hg kg-1, 0.01 mg Pb kg-1, 0.01 mg Co kg-1, 0.02 mg

As kg-1, 0.02 mg Se kg-1, 0.05 mg Cu kg-1, 0.05 mg Mo kg-1, and 0.05 mg Zn kg-1. Table 1 contains

information on the concentration range for linearity, limits of detection (LOD), LOQ, estimates of

measurement uncertainty and results for the certified reference material. The samples were collected

as part of a wider survey of chemical elements in different species and method validation was carried

out for the representative matrices pork muscle, calf liver and kidney. Information on recoveries for

spiked samples of the representative matrices as well as instrumental parameters is provided as Tables

S1 and S2 in the supplementary material.

[Table 1 near here]

2.4. Statistical tests

Statistical analyses were conducted using the R statistical package, version 2.15 (R Foundation for

Statistical Computing, Vienna, Austria). As the survey design was unbalanced, differences in metal

concentration between tissues, age classes and states were examined using mixed effect models, along

with interaction terms that were intrinsic to the design. The model fitted to data also accounted for the

time (date) of laboratory analysis, with the following model formula:-

concentration = β0 + β1×date of analysis + β2×state + β3×tissue + β4×age + β5×(tissue:age) + ε

(random terms are underlined)

Data were transformed (log or square root) prior to analysis, to yield normal and independent

residuals. Differences between states were tested using changes in likelihood, and differences

between age classes of animals were tested via simulated confidence intervals around treatment

medians (200 simulations for each analysis). Simulations were conducted in the scale of the data

transformations applied in original analyses, and resultant percentiles back-transformed to the scale of
Page 7 of 33

the original data for interpretation. To simplify the interpretation of confidence intervals (2.5 th and

97.5th percentiles), statistical models used to analyse the data included only additive fixed and random

terms (i.e. excluded interaction terms) with effects averaged across all other terms in the model

(unless otherwise stated). As tissue samples were not taken entirely at random, differences in element

concentrations between states are only indicative of state differences.

2.5 Estimation of contribution to human dietary exposure.

The results of the current survey were used to provide insights into the dietary contribution that meat

and meat products make to human exposure to toxic elements. At the concentrations found in the

survey, the elements will not be acutely toxic but may be of concern to consumers through long-term

exposure. Of the elements examined in this survey arsenic, cadmium, lead and mercury are of

particular interest with respect to the contribution of sheep meat and offal to overall human dietary

exposure. Mean tissue concentrations were placed in a spreadsheet used to calculate intakes for

contaminants and pesticides, with the world divided into one of thirteen clusters according to diet

(GEMS Food, Spreadsheet for the evaluation of chronic exposure

http://www.who.int/foodsafety/chem/IEDI_calculation14_FAO1.xlt). The calculated intakes are

compared against the tolerable intake in the form of the provisional tolerable weekly intake (PTWI) or

the provisional tolerable monthly intake (PTMI). These values provide an indication of the amount of

a chemical that can be consumed on a weekly or monthly basis without appreciable risk. The term

tolerable has been used by regulators to indicate the contaminants are not deliberately added to food.

Where a tolerable intake was not available, comparison was made with overall intakes estimated from

all food sources in the 23 rd Total Diet Study for the Australian population (FSANZ 2011).

3. Results

Results of kidney, liver and muscle are summarised in Tables 2‒6 and discussed below.

3.1. Arsenic

Arsenic concentrations in the tissues of sheep ranged from <0.005 to 0.05 mg kg -1 FW with most

samples for each tissue type containing arsenic at concentrations below the LOD of 0.005 mg kg-1
Page 8 of 33

(86–91% of all samples). In the small number of samples with detectable levels, kidneys contained

higher arsenic concentrations than liver, which were higher than muscle. The low prevalence of

concentrations above the LOD precluded meaningful investigation of age- and state-based differences.

Levels of arsenic in kidney showed a significant correlation with arsenic in liver (p < 0.01, r = 0.73, n

= 13), Table 6.

3.2. Cadmium

Concentrations of cadmium in sheep tissues ranged from <0.003 to 11.7 mg kg-1 FW. The highest

concentrations were observed in kidney (mean 0.853 mg kg-1 FW) followed by liver (mean 0.28 mg

kg-1 FW) with only low concentrations observed in muscle (mean 0.0035 mg kg -1). In 91% of muscle

samples the concentration of cadmium was below the detection limit. Age-related differences in tissue

concentrations were observed for cadmium (p < 0.01).

There were sufficient liver and kidney samples with concentrations detected above the LOQ to

examine possible correlations between elements and tissues (Table 6). Levels in kidney, liver and

muscle showed positive correlations (kidney–liver r = 0.84, p < 0.001; kidney–muscle r = 0.71, p <

0.001; liver–muscle r = 0.73, p < 0.001). Cadmium concentrations also were positively correlated

with lead concentrations for a range of tissue combinations (kidney–kidney r = 0.36, p < 0.001; liver–

liver r = 0.56, p < 0.001; kidney–liver r = 0.49, p < 0.001; liver–kidney r = 0.44, p < 0.001; muscle–

liver r = 0.34, p < 0.001). Levels in liver exhibited correlations with mercury levels in liver (liver–

liver r = 0.33, p < 0.01). Correlations were also observed with molybdenum (liver–kidney r = 0.17, p

< 0.01; kidney–kidney r = 0.16, p < 0.05).

3.3 Cobalt

Mean cobalt concentrations are highest in liver (0.06 mg kg-1) followed by kidney (0.044 mg kg-1) and

muscle (0.006 mg kg-1). As with the earlier study, age- and state-related differences in cobalt

concentrations were not significant (p > 0.05) for any of the tissues. Concentrations of cobalt were

correlated in kidney, liver and muscle (kidney–liver r = 0.55, p < 0.001; kidney–muscle r = 0.28, p <
Page 9 of 33

0.01). Concentrations of cobalt were negatively correlated with copper concentrations for a range of

tissue combinations (liver–kidney r = ‒0.20, p < 0.05; kidney–muscle r = ‒0.17, p < 0.05; muscle–

kidney r = ‒0.30, p < 0.05; liver–muscle r = ‒0.25, p < 0.01).

3.4. Copper

Sheep exhibit a high capacity for storing excess copper in the liver (Suttle 2010). This is reflected in

the differences in mean concentrations for liver, kidney and muscle which were 66.0, 2.72 and 0.74

mg kg-1 FW respectively. For copper, concentrations in liver, kidney and muscle did not show a trend

with age for the three broad age-classes studied. Copper concentrations in tissues of sheep from

different states showed a dependence with concentrations from QLD>VIC>SA, WA, NSW>TAS;

however, the differences were not statistically significant (p > 0.05).

Copper and zinc concentrations showed a strong positive correlation in a range of tissue combinations

(kidney–kidney r = 0.77, p < 0.001; kidney–liver r = 0.30, p < 0.01; kidney–muscle r = 0.28, p < 0.05;

muscle–kidney r = 0.41, p < 0.001) and may reflect a link in dietary levels of exposure (Table 6).

Copper in muscle and kidney also exhibited positive correlations with selenium levels in kidney

(muscle–kidney r = 0.28, p < 0.01; kidney–kidney r = 0.26, p < 0.01). Negative correlations were

observed between copper and molybdenum in liver (liver–liver r = ‒0.32, p < 0.01). There were also

correlations in levels of copper with cobalt in various tissues.

3.5. Lead

Mean lead concentrations in sheep tissues were significantly higher in kidneys (0.057 mg kg -1 FW)

compared to liver (0.040 mg kg-1 FW), while the mean concentration in muscle was much lower

(0.007 mg kg-1). Mean and median lead concentrations in kidney generally followed the order WA >

VIC >SA> NSW, TAS > QLD. The differences in concentrations between states were significant (p <

0.0001).

Age-related differences in kidney and liver concentrations were observed for lead (p < 0.0001).
Page 10 of 33

Concentrations of lead were correlated in kidney and liver (kidney–liver r = 0.23, p < 0.05). Levels of

lead were also positively correlated with levels of arsenic, cadmium, mercury and molybdenum for

various tissue combinations (Table 6).

3.6. Mercury

Concentrations in kidney (mean 0.0061 mg kg-1 FW), liver (0.0034 mg kg-1 FW) and muscle (0.0025

mg kg-1 FW) were low, with a large number of samples having concentrations below the LOD (kidney

18%, liver 51% and muscle 96%). Based on mean and median concentrations in kidney, mercury

concentrations were generally higher in South Australia compared to the other states, although the

differences were not statistically significant (p > 0.05). However, as stated above, in all cases mercury

concentrations were low.

In addition to correlations between mercury and cadmium reported above there were significant

correlations between mercury and lead (liver–liver r = 0.56, p < 0.001; liver–kidney r = 0.29, p < 0.05)

and mercury and selenium (kidney–muscle r = 0.19, p < 0.05), Table 6.

3.7. Molybdenum

Liver contained the highest molybdenum concentration (mean 1.05 mg kg -1 FW), followed by kidney

(0.44 mg kg-1 FW) and muscle (0.014 mg kg-1 FW). There were no state- or age-related trends in

tissue concentrations. In addition to correlations between cadmium and molybdenum and copper and

molybdenum, lead (kidney–kidney r = 0.25, p < 0.01; kidney–liver r = 0.24, p < 0.01), selenium

(liver–liver r = 0.16, p < 0.05; liver–muscle r = 0.23, p < 0.01), and zinc (liver–liver r = 0.22, p < 0.01)

also exhibited significant correlations with molybdenum (Table 6).

3.8. Selenium

Mean concentrations were highest in kidney (0.95 mg kg-1 FW) followed by liver (0.31 mg kg-1 FW)

and muscle (0.09 mg kg-1 FW). Age-related differences in liver concentrations were observed for

selenium (p < 0.001) but not kidney and muscle. Concentrations in tissues by state generally followed

the order QLD > NSW, SA> VIC, WA> TAS. Concentrations of selenium were correlated in kidney
Page 11 of 33

and liver (kidney–liver r = 0.38, p < 0.001). Correlations between selenium and other elements were

observed for copper, mercury and molybdenum as reported above and also for zinc (kidney–kidney r

= 0.37, p < 0.001; muscle–kidney r = 0.16, p < 0.05).

3.9. Zinc

Mean concentrations of zinc are highest in muscle (40.4 mg kg-1 FW), followed by liver (37.2 mg kg-1

FW) and lowest in kidney (20.8 mg kg-1 FW). There were no state- or age-related trends in

concentration of zinc in the various tissues studied. Concentrations of zinc were correlated in kidney

and liver (kidney–liver r = 0.19, p < 0.05). Levels of zinc were also correlated with levels of copper,

mercury, molybdenum and selenium for various tissue combinations (Table 6).

4. Discussion

Arsenic

The arsenic contents of tissues in the current study were considerably lower than reported for samples

collected in 1992 (NRS 1997) from Queensland, Victoria and Western Australia, where the median

concentrations were 0.04 mg kg-1 FW for kidney, 0.01 mg kg-1 FW for liver and <0.01 mg kg-1 FW for

muscle. The reason for the difference is unclear but may be due to the removal of arsenic-containing

agricultural and veterinary products from the marketplace. Age-related differences were not observed

which is consistent with the reported short half-life in the body, such that concentrations in tissues

reflect recent exposure (NRC 2005).

The concentrations detected in the current study can be put into their public health context. A recent

evaluation of arsenic by JECFA determined that a tolerable limit for exposure to inorganic arsenic

could not be established (WHO 2010a), and as such levels should be kept as low as reasonably

achievable. Generally, most foods contain low levels of arsenic, due to its wide distribution in the

environment and, to some extent, to its use in agriculture. While dietary arsenic represents the major

source of arsenic exposure for most of the population, sheep meat and offal are very minor

contributors to exposure, accounting for less than 0.5% of the estimated upper limit of mean exposure

for adults in Australia reported in the 23 rd total diet survey (FSANZ 2011).
Page 12 of 33

Cadmium

Cadmium is a toxic heavy metal that is also ubiquitous in the environment. Age-related differences in

tissue concentrations were observed for cadmium (p < 0.01). This is consistent with previous surveys

in Australia (Langlands et al., 1988; Morcombe et al., 1994a; NRS 1997) and elsewhere for sheep

exposed to low-level environmental concentrations (Prankel et al., 2005; Rudy 2009) and also with

the long half-life for elimination from exposed animals. Once absorbed by sheep, cadmium is poorly

excreted, with half-lives for elimination from tissues that are typically greater than 1000 days

(Beresford et al., 1999; Neathery et al., 1974; Houpert et al., 1995).

In agreement with other studies, there are regional differences in tissue cadmium levels. An extensive

study by Langlands et al. (1988) reported on cadmium in samples of sheep kidney, liver and muscle

samples that were collected from various states in Australia in the period 1975‒1983. Median

concentrations of cadmium in sheep kidney reported by Langlands et al. (1988) were 0.040 (NSW),

0.370 (VIC), 0.640 (SA), 0.063 (QLD), 2.200 (WA) and 0.150 (TAS) mg kg-1. In the current study

median concentrations in kidney are: 0.086 (NSW), 0.501 (VIC), 0.226 (SA), 0.129 (QLD), 1.57 (WA)

and 0.109 (TAS) mg kg-1, which are similar to those from Langlands et al. (1988). It is well known

that there are regional differences in the relative importance of various cadmium sources that may be

present in the environment. Important industrial sources of cadmium pollution are reported to include

the combustion of coal, metal smelting, mining waste and alloy processing. Agricultural practices,

such as the application of sewage sludge and contaminated fertilisers, also contribute to

environmental levels. Of these sources it is the contamination of pastures with cadmium present in

phosphate fertilisers and its subsequent uptake by grazing sheep that is most important in Australia

(Bramley 1990; Morcombe et al., 1994ab; Loganathan et al., 2008).

Historically, the greatest use of phosphate fertilisers in Australia occurred in cropping and improved-

pasture regions of the south of WA, SA and VIC. Mean and median cadmium concentrations in

kidney and liver showed a trend: WA >VIC, SA, TAS>NSW>QLD, which parallels the major known

risk factor in the Australian sheep growing regions, the use of phosphate fertilisers (Morcombe et al.,

1994b). The data also suggest that there has been little change in the exposure of sheep to cadmium in

the last 27 years. A review of cadmium levels in liver from a larger database available from NRS
Page 13 of 33

random monitoring program for the years 1990 to 2014 revealed essentially no change in mean

cadmium levels in the last ten years (personal communication). Overall the results suggest cadmium

inputs into Australian farming systems are being effectively managed to stabilise soil levels.

There were sufficient liver and kidney samples with cadmium concentrations above the LOQ to

examine possible correlations with other elements and tissues. Cadmium concentrations were

positively correlated with lead for a range of tissue combinations. Lead binds to divalent metal

transporter 1, which is induced by cadmium exposure, giving rise to increased absorption and tissue

concentrations. Phillips et al. (2003) reported lead concentrations in pig tissues are increased when

animals are simultaneously exposed to lead and cadmium. Other significant correlations were with

arsenic, mercury and molybdenum. Although cadmium is known to interact with the metabolism of

the essential elements copper, selenium and zinc, significant correlations were not observed with these

elements in the current study.

None of the samples in the current survey were indicative of exposure of sheep to toxic levels of

cadmium. Puls (1994) suggests that for sheep normal cadmium kidney concentrations are 0.03‒0.1

mg kg-1 FW, high levels are 1.0‒5.0 mg kg-1 FW and toxic levels are 100‒250 mg kg-1 FW. The

highest concentration in kidney observed in the current study was 11.7 mg kg -1.

The contribution of sheep tissues to overall consumer cadmium exposure can also be assessed. The

PTMI set by JECFA for cadmium is 25 µg/kg bw (WHO 2010b). Australia is a major exporter of

sheep meat and meat products and it was decided to utilise the consumption figures reported by

GEMS/Food and used internationally for the evaluation of long-term dietary exposure to

contaminants and pesticides. GEMS/Food analysed international consumption patterns for a wide-

range of foods and derived 13 “cluster” diets that are representative of the world. Potential exposure

to cadmium through consumption of Australian sheep meat and meat products amounts to 0‒0.1% of

the PTMI, with the highest exposure estimated for those countries belonging to GEMS/Food cluster

diet B (Africa/Europe/Middle East). These estimates do not take into account the cadmium
Page 14 of 33

management activities in Australia, which restrict the age of animals from which liver and kidney can

be harvested (DAWR 2015), and ensure substantially reduced dietary exposures to cadmium from

consumption of sheep meat and meat products.

Cobalt

Cobalt is an essential trace element for the nutrition of sheep and as such a regular dietary supply is

essential for health and efficient production. The order of levels in the various tissues agrees with a

survey conducted in 1992 of cobalt in kidney, liver and muscle in sheep from QLD, VIC and WA

(NRS 1997) with liver>kidney>muscle. As with the earlier study, age- and state-related differences in

cobalt concentrations were not significant (p>0.05) for any of the tissues. The lack of age-related

differences is consistent with the known rate of cobalt turnover in the body (Suttle 2010), which

suggests cobalt concentrations reflect more recent exposures. Concentrations of cobalt were

negatively correlated with copper concentrations for a range of tissue combinations (Table 6).

In South Australia cobalt deficiency of sheep is associated with ‘coast disease’ (Lines 1935, Marston

1935). Suttle (2010) notes that cobalt deficiency in sheep is primarily a vitamin B12 deficiency,

resulting from the inability of the rumen microorganisms to synthesise sufficient vitamin B12 from

their cobalt supply. In addition to feed, soil can be a significant source of bioavailable cobalt (Brebner

et al., 1987; Grace 2006; Macpherson 1983; Clark et al., 1989). The current data can be used to assess

the cobalt status of the Australian sheep flock. Liver cobalt concentrations in this study ranged from

0.006 to 0.24 mg kg-1 FW. It has been suggested that a liver cobalt concentration <0.04–0.06 mg kg-1

DW indicates cobalt inadequacy and that concentrations >0.08–0.12 mg kg-1 DW in sheep indicate

sufficiency (Suttle 2010). Equivalent fresh weight values are <0.01‒0.015 mg kg-1 FW for an

insufficiency and >0.02‒0.03 mg kg-1 FW for sufficiency. In one lamb the concentration of cobalt in

liver was indicative of an insufficiency. The cobalt tissue concentrations were all below levels that

might be indicative of toxicity (Dickson and Bond, 1974).

Page 15 of 33

Copper

Copper is an essential trace element for the activity of numerous enzymes, cofactors and reactive

proteins. For copper, concentrations in liver, kidney and muscle did not show a trend with age for the

three broad age-classes studied. Copper concentrations in tissues of sheep from different states

showed a dependence with concentrations from QLD>VIC>SA, WA, NSW>TAS; however, the

differences were not statistically significant (p > 0.05).

Langlands et al. (1987) reported mean copper concentrations in liver, kidney and muscle of 65.2, 4.59

and 1.36 mg kg-1 FW respectively for samples collected from all states of Australia in the years 1975

through 1983. While the liver results are similar to those in the present study, the mean levels in

kidney and muscle reported by Langlands et al. (1987) are 70 to 80% greater. The levels of copper in

the tissues are not too dissimilar to those reported by others. For example, Sivertsen and Plassen

(2004) reported a mean liver copper level of 69 mg kg-1 FW (range 4‒600) for lambs from Norway.

Mean copper levels in different muscle tissue of young sheep (2 yrs old) from Poland ranged from

0.071 to 2.13 mg kg-1 FW (Massáanyi et al., 2001) while mean levels in retail samples of lamb muscle

from the USA and New Zealand were 1.2 mg kg-1 FW (Ikem et al., 2015).

Levels of copper in liver can be used to estimate the prevalence of deficiencies and toxicity in the

Australian sheep population. Animals most susceptible to trace element deficiencies are young,

rapidly growing animals and animals during their first pregnancy and lactation. Copper deficiency

occurs in all states of Australia (Hosking et al., 1986). Copper deficiency may occur following use of

high concentrations of zinc supplements (200–400 mg kg-1) for treatment of facial eczema (Morris et

al., 2006). Hosking et al. (1986) have described forms of chronic Cu toxicity affecting sheep in

Victoria. The main form occurs in sheep ingesting plant-based hepatotoxins. Pyrrolizidine alkaloid

damage to the liver from the heliotrope is associated with excessive accumulation of Cu in the liver. A

similar situation exists in Western Australia for sheep grazing lupin stubble infected with the

hepatotoxin phomopsin (Allen et al., 1979). Chronic Cu toxicity may also occur in sheep on pasture of

high subterranean clover content (Hosking et al., 1986). Additionally in Australia molybdenum

responsive chronic poisoning of sheep in eastern Australia has been reported and found to be
Page 16 of 33

associated with abnormally low molybdenum concentrations in forage (Dick and Bull 1945). In

contrast over-supplementation with copper may also give rise to chronic poisoning. None of the

animals in the current study had liver copper concentrations below 2 mg kg-1 FW, a level considered

to indicate a copper responsive disorder (Suttle 2010). One animal had a liver level that exceeded 337

mg kg-1 FW, a level indicative of toxicity. Based on liver Cu concentrations, our results suggest sheep

in Australia are generally well managed with respect to copper supplementation.

Lead

Lead is a toxic heavy metal present as a natural contaminant in the environment with additional

anthropogenic sources of exposure. In agreement with other studies (Fick et al., 1976), the present

study supports the observation that lead does not accumulate in muscle following commonly

encountered levels of exposure. Age-related differences in kidney and liver concentrations were

observed for lead (p < 0.0001). Rudy (2009) also reported lead concentrations in meat and liver

increased with age of sheep. However Pareja-Carrera et al. (2014) found lead levels decreased with

age. Tissue lead concentrations are thought to reflect recent exposure (Suttle 2010) and it is possible

that the differences observed may have been due to differences in dietary lead intake for the different

age-classes in the last few weeks before slaughter. Mean and median lead concentrations in kidney

generally followed the order WA > VIC >SA> NSW, TAS > QLD. The differences in concentrations

between states were significant (p < 0.0001).

Normal lead kidney levels are reported to be 0.1‒0.5 mg kg-1 FW, high levels 0.7‒4.0 mg kg-1 FW and

toxic levels >20 mg kg-1 FW (Suttle 2010). None of the samples in the current survey were indicative

of exposure of sheep to toxic levels of lead.

Levels of lead were correlated with levels of arsenic, cadmium, mercury and molybdenum for various

tissue combinations.

The diet is a significant source of human exposure to lead. Currently there is no international health-

based guidance value for lead, as the 73rd JECFA was unable to derive a tolerable level for lead in the
Page 17 of 33

diet, concluding that levels should be as low as reasonably achievable (WHO 2010b). Exposure to

lead through consumption of Australian sheep meat and meat products is low and for Australian

consumer’s amounts to less than 1% of the mean intake for adults of 0.0092 mg/day reported in the

23rd total diet survey (FSANZ 2011).

Mercury

Mercury is a toxic heavy metal that is subject to regulation of concentrations permitted in food. Only

low levels are found in the grazing environment, though sheep may be exposed through feeding of

fish meal, an uncommon practice in Australia, or through the use of contaminated feed additives. The

results for mercury are similar to those obtained in the 1992 survey (NRS 1997).

Although diet is the major source of human exposure to mercury, seafood contains much higher levels

of mercury than most other foods, such that other sources are usually insignificant. JECFA established

a PTWI for inorganic mercury of 4 μg/kg bw (WHO 2011). Exposure to mercury through

consumption of Australian sheep meat is low and for Australian consumers of sheep meat products

amounts to less than 0.05% of the PTWI.

Molybdenum

Molybdenum is an essential trace element that can also be an antagonist to copper absorption as

mentioned earlier. All samples were within the normal range for molybdenum concentrations listed

by Puls (1994). In addition to correlations between cadmium and molybdenum and copper and

molybdenum, lead, selenium, and zinc also exhibited significant correlations with molybdenum.

Selenium

Selenium is an essential trace element. The variation in selenium levels with state is reflective of

known environmental concentrations. Tissue selenium concentrations were highest in samples from

Queensland and may reflect the presence of known areas of elevated selenium environmental levels in

some parts of Queensland combined with the presence of some hypo-accumulating plants in pasture.

For sheep in southern Australia, Se responsive disorders are a serious problem in all states particularly
Page 18 of 33

in regions of high rainfall (>500 mm annually). Langlands et al. (1991) reported a negative

relationship between rainfall and selenium status in sheep.

Mean levels of selenium in muscle in the current study (0.09 mg kg-1 FW) are consistent with those

reported for Australian lamb by Williamson et al., (2005) at 0.1 mg kg-1 FW but lower than the report

of Tinggi et al., (1992), who found levels of 0.22 mg kg-1 FW in lamb muscle. Levels in the current

study are also lower than those reported for retail samples of lamb muscle from the USA and New

Zealand which had mean levels of 0.55 mg kg-1 FW (Ikem et al., 2015).

Levels of selenium in liver can be used to estimate the prevalence of deficiencies in the Australian

sheep populations. Mean selenium concentrations in Australian sheep liver are 0.31 mg kg -1 FW.

According to the criteria developed by Suttle (2010), animals receiving diets adequate in vitamin E

are considered deficient in selenium if liver levels are below 0.02 mg kg -1 FW and at risk of chronic

selenosis if liver levels exceed 25 mg kg-1 FW. No animals had selenium liver levels below 0.02 or

above 25 mg kg-1 FW.

Zinc

Zinc is required for the function of a large number of enzymes and is essential for growth and

reproduction in both plants and animals (Suttle 2010). The zinc concentrations in kidney, liver and

muscle found in the current study are within the range found in other studies on Australian sheep

(Langlands et al., 1987; Flanjak and Lee 1979; Kramer et al., 1983). The results from a recent large-

scale study Australian lamb reported mean zinc muscle levels of 24.3 mg kg -1 FW (Pannier et al.,

2014) are at odds with those reported here and the earlier studies. The mean levels of zinc in

Australian lamb muscle reported in the current study at 40.4 mg kg-1 FW are higher than those

reported for retail samples of lamb muscle from the USA and New Zealand which were 26.3 mg kg-1

FW (Ikem et al., 2015).

4.10. Comparison of levels of non-essential elements to those other countries

Page 19 of 33

The levels found in tissues can be compared to those reported for other countries for the elements of

concern to regulators (As, Cd, Hg and Pb). Noting that the tissue levels for these elements are highest

in kidney, only data for this tissue are reported in Table 7. Levels of arsenic in Australia sheep are

lower than those observed in the countries for which data were obtained. Similarly, levels of mercury

and lead are also lower than the mean values reported by other countries. The interpretation of results

for cadmium levels in sheep kidney are complicated by the strong age dependence of the levels and

the differences in the age profile of the animals sampled in the various studies. The cadmium levels

observed in Australian sheep kidney are similar to or lower than those reported in other countries.

Mean levels in kidney from the age groups studied here were 0.126 mg kg -1 for lambs, 0.677 mg kg-1

for young sheep and 1.75 mg kg-1 for mature sheep. Cadmium levels in lambs’ kidney were 0.058 mg

kg-1 for Iceland, <0.0035 and 1.035 mg kg-1 from two studies for Italy and 0.18 mg kg-1 for the USA.

Only a limited number of data from other countries are available for mature sheep kidney with

reported mean levels in the range 0.24‒1.73 mg kg-1.

[insert Table 7 near here]

Internationally, a number of regulators have established maximum limits for arsenic, cadmium, lead

and mercury relevant to sheep meat (China 2005, Codex 2010, EC 2006, FSANZ 2015, Mexico 2011,

Russia 2010), Table 8. Limits for arsenic, lead and mercury are rarely exceeded in sheep meat. In the

case of cadmium, as cadmium accumulates with age in kidney and liver a number of regulators have

introduced age-based restrictions for harvesting kidney and also in some instances liver to reduce

consumer exposure. Such an approach has been utilised in Australia where, noting the differences in

cadmium levels between states, restrictions in Australia are based on the combination of age of sheep

and their state of origin (DAWR 2011).

[insert Table 8 near here]

Page 20 of 33

4. Conclusion

The concentration of the elements studied here are generally consistent with surveys conducted in

Australia over the last 20 to 50 years. Cadmium concentrations in tissues have stabilised over the last

25 years or so, suggesting strategies to manage agricultural inputs and reduce any increase in

environmental loads are having an effect. The concentrations of the essential trace elements in tissues

suggest sheep are well managed with few cases of deficiency or toxicity detected.

There was good compliance with maximum levels established by food regulators. Estimates of the

contribution of arsenic, cadmium, lead and mercury in sheep meat to human dietary exposure show

sheep products are only minor contributors.

Conflict of interest

The authors declare no conflicts of interest.

Acknowledgements

The authors would like to thank Titus Vimalasiri and Carmel Boatwright from ALS Environmental,

Canberra for the analytical work they provided for this study. The authors would also like to thank the

Sheepmeat Council of Australia for supporting the funding the survey.

Page 21 of 33

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Table 1 Method limits of detection and quantification, linear range and measurement uncertainty
Element LODa LOQb Linear range Measurement Certified valued Measured valuee
(mg kg-1) (mg kg-1) (mg kg-1) uncertainty (%)c (mg kg-1) (mg kg-1)
Arsenic 0.0047 0.02 0.005-30 24 0.46±0.11 0.44±0.04
Cadmium 0.0029 0.005 0.003-30 18 0.87±0.07 0.92±0.08
Cobalt 0.004 0.01 0.004-30 16 0.63±0.10 0.58±0.07
Copper 0.0109 0.05 0.01-300 15 149±10 152±6.4
Lead 0.0079 0.01 0.008-30 20 0.74±0.12 0.71±0.07
Mercury 0.0011 0.005 0.001-30 20 0.35±0.06 0.35±0.03
Molybdenum 0.0057 0.05 0.006-30 20 3.70±0.35 3.76±0.28
Selenium 0.017 0.02 0.02-30 15 1.55±0.23 1.47±0.13
Zinc 0.0357 0.05 0.04-300 12 157±11 161±6.4
a
LOD limit of detection
b
LOQ limit of quantification
c
Measurement uncertainty at 95% confidence interval
d
Certified reference material consisted of bovine liver (AGAL-4) from the National Measurement Institute
e
the number of analyses was 75 for copper and zinc and 103 for the other elements.
Page 27 of 33

Table 2 Concentrations of various elements in sheep kidney by state

State As Cd Co Cu Pb Mo Hg Se Zn
(mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1)
NSW Meana 0.011 0.326 0.044 2.84 0.0317 0.42 0.0061 0.98 21.0
median nd 0.086 0.040 2.72 0.02 0.41 0.0022 0.97 20.3
Range nd-0.0503 0.013-2.83 0.021-0.11 1.85-6.07 0.004-0.33 0.028-0.86 nd-0.0838 0.27-1.53 11.8-34.9
QLD Meana 0.01 0.299 0.059 2.48 0.014 0.35 0.0059 1.07 18.6
Median nd 0.129 0.058 2.48 0.014 0.32 0.0034 1.11 18.6
Range 0.036-
nd-0.0099 0.116-1.16 0.085 1.98-3.09 nd-0.019 0.27-0.47 nd-0.0184 0.66-1.38 13.4-23.5
SA Meana 0.014 0.384 0.045 2.51 0.042 0.44 0.0085 1.00 19.5
Median nd 0.226 0.037 2.36 0.024 0.39 0.0038 0.93 17.5
Range 0.015-
nd-0.046 0.041-1.32 0.139 1.94-3.91 nd-0.278 0.17-0.87 nd-0.069 0.74-1.78 12.9-36.6
TAS Meana 0.01 0.175 0.061 2.45 0.037 0.47 0.0067 0.65 18.5
Median nd 0.109 0.048 2.27 0.010 0.43 0.0017 0.66 18.4
Range nd-0.0082 nd-0.525 0.027- 2.18-2.92 nd-0.172 0.36-0.66 0.0011- 0.53-0.81 15.6-21.9
0.142 0.027
VIC Meana 0.01 1.13 0.043 3.17 0.085 0.40 0.0060 0.99 24.5
Median nd 0.501 0.041 3.07 0.039 0.35 0.0024 0.97 23.4
Range 0.026-
nd-0.008 0.026-4.65 0.073 2.30-4.42 nd-0.714 0.21-0.68 nd-0.063 0.59-1.46 15.4-44.5
WA Meana 0.012 2.17 0.036 2.39 0.103 0.53 0.0046 0.84 19.5
Median nd 1.57 0.030 2.36 0.055 0.40 0.0025 0.82 19.6
Range 0.010- 0.009-
nd-0.040 0.086-11.7 0.129 1.74-3.44 0.885 0.25-2.28 nd-0.0161 0.50-1.33 13.2-28.3
Aus n<LOD 130 1 0 0 13 0 27 0 0
Meana 0.011 0.853 0.044 2.72 0.057 0.44 0.0061 0.95 20.8
Range nd-0.050 nd-11.7 0.010- 1.74-6.07 nd-0.88 0.028-2.28 nd-0.084 0.27-1.78 11.7-44.5
0.142
nd = below the limit of detection
a means were calculated assuming levels below the LOQ were present at ½LOQ.
Page 28 of 33

Table 3 Concentrations of various elements in sheep liver by state

State As Cd Co Cu Pb Mo Hg Se Zn
(mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1)
NSW meana 0.011 0.082 0.061 61.2 0.0240 1.13 0.0027 0.32 37.4
Median nd 0.0394 0.057 52.1 0.0113 1.12 nd 0.32 36.8
Range 0.008- 0.025-
nd-0.0255 0.922 0.195 2.65-194 nd-0.259 0.12-2.06 nd-0.0052 0.05-1.65 22.2-56.0
QLD Meana 0.01 0.117 0.085 79.5 0.0119 1.16 0.0027 0.52 39.1
Median nd 0.066 0.090 87.3 0.0104 1.20 0.0021 0.62 36.6
Range 0.039- 0.064-
nd-0.0057 0.352 0.095 26.9-102 nd-0.0248 0.78-1.37 nd-0.0031 0.18-0.74 28.0-50.6
SA meana 0.010 0.189 0.062 67.2 0.0254 0.97 0.0034 0.35 31.7
Median <0.0047 0.086 0.050 58.4 0.0194 0.98 0.0014 0.32 32.8
Range 0.017- 14.5
nd-0.0154 0.018-1.13 0.241 192 nd-0.1004 0.41-1.38 nd-0.0133 0.16-0.72 20.8-45.0
TAS meana 0.01 0.142 0.072 43.7 0.0338 1.02 0.0029 0.12 36.5
Median nd 0.090 0.057 32.2 0.0076 1.03 0.001 0.11 37.1
Range 0.026- 0.049-
nd-nd 0.335 0.143 4.66-104 nd-0.1404 0.88-1.16 nd-0.0047 0.08-0.16 28.8-45.8
VIC meana 0.01 0.303 0.053 76.4 0.0314 0.98 0.0034 0.25 42.1
Median nd 0.120 0.053 70.1 0.0227 0.96 nd 0.26 38.3
Range 0.025-
nd-0.0074 0.026-1.27 0.081 2.95-182 nd-0.1703 0.42-1.58 nd-0.0134 0.07-0.49 19.0-111
WA meana 0.011 0.751 0.054 68.3 0.0898 0.98 0.0052 0.28 36.5
Median <0.0047 0.529 0.057 39.2 0.0527 0.95 0.0024 0.22 35.4
Range 0.006-
nd-0.0192 0.027-4.45 0.125 3.27-341 nd-0.3818 0.32-2.18 nd-0.0225 0.06-0.85 24.7-53.1
Aus n<LOD 130 0 0 0 31 0 78 0 0
Meana 0.01 0.280 0.060 66.0 0.0397 1.05 0.0034 0.31 37.2
Range nd-0.0255 0.008-4.45 0.006-0.24 2.65-341 nd-0.3818 0.12-2.18 nd-0.0225 0.05-1.65 19.0-111
nd = below the limit of detection
a
means were calculated assuming levels below the LOQ were present at ½LOQ
Page 29 of 33

Table 4 Concentrations of various elements in sheep muscle by state

State As Cd Co Cu Pb Mo Hg Se Zn
(mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1)
NSW Meana 0.01 0.0026 0.0055 0.76 0.005 0.010 0.0025 0.10 42.6
Median nd nd nd 0.71 nd 0.010 nd 0.09 43.0
Range nd -0.01 nd-0.006 nd-0.013 0.39-1.86 nd-nd nd-0.02 nd-0.0021 nd-0.35 15.1-60.3
QLD Meana 0.011 0.0025 0.0078 0.71 0.005 0.011 0.0025 0.12 33.9
Median nd nd 0.005 0.63 nd 0.011 nd 0.14 36.0
Range nd-nd 0.007- nd-nd
nd-0.0157 nd-nd nd-0.018 0.51-0.98 0.016 0.04-0.20 22.1-42.4
SA Meana 0.01 0.0027 0.0054 0.76 0.005 0.016 0.0025 0.11 41.3
Median nd nd nd 0.73 nd 0.009 nd 0.11 40.6
Range nd-0.0086 nd-0.005 nd-0.010 0.48-1.30 nd-0.014 nd-0.066 nd-0.0011 0.05-0.24 30.2-51.7
TAS Meana 0.01 0.003 0.006 0.73 0.005 0.011 0.0027 0.034 32.7
Median nd nd 0.006 0.81 nd 0.010 nd 0.03 33.3
Range nd-nd 0.007- nd-0.0039
nd-nd nd-0.005 nd-0.010 0.44-0.97 0.017 0.03-0.04 22.6-41.3
VIC Meana 0.01 0.0035 0.0052 0.67 0.005 0.007 0.0025 0.07 44.2
Median nd nd nd 0.69 nd 0.008 nd 0.07 42.2
Range nd-0.013 nd-0.014 nd-0.010 0.38-0.95 nd-nd nd-0.017 nd-nd 0.02-0.16 20.4-74.6
WA Meana 0.01 0.0061 0.0056 0.75 0.012 0.024 0.0025 0.07 35.6
Median nd nd nd 0.78 nd 0.016 nd 0.07 35.2
Range nd-0.034 0.006- nd-0.0033
nd-0.0078 nd-0.033 nd-0.015 0.37-0.97 0.197 0.02-0.15 12.9-56.6
Aus n<LOD 138 120 100 0 149 16 146 0 0
Meana 0.01 0.0035 0.0056 0.74 0.007 0.014 0.0025 0.09 40.4
Range nd-0.0157 nd-0.033 nd-0.018 0.37-1.86 nd-0.034 nd-0.200 nd-0.0039 0.01-0.35 12.9-74.6
nd = below the limit of detection
a
means were calculated assuming levels below the LOQ were present at ½LOQ
Page 30 of 33

Table 5 Concentrations of various elements in sheep kidney, liver and muscle by age class
As Cd Co Cu Pb Mo Hg Se Zn
(mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1) (mg kg-1)
Kidney
Lamb median nd 0.057 0.036 2.64 0.019 0.403 0.0022 0.90 18.6
P0.9 0.0052 0.268 0.061 3.31 0.066 0.630 0.0133 1.19 26.7
Young median nd 0.252 0.040 2.73 0.025 0.376 0.0027 0.97 20.6
P0.9 nd 2.042 0.064 3.38 0.108 0.620 0.0105 1.37 26.1
Mature median nd 0.826 0.041 2.44 0.031 0.397 0.0024 0.90 19.7
P0.9 0.0080 4.531 0.066 3.59 0.178 0.687 0.0090 1.30 28.6
Liver
Lamb median nd 0.049 0.051 56.5 0.011 1.01 nd 0.24 34.6
P0.9 nd 0.148 0.072 92.3 0.038 1.38 0.0048 0.47 47.0
Young median nd 0.085 0.058 65.9 0.019 1.03 0.0012 0.29 37.6
P0.9 0.0050 0.594 0.082 111 0.104 1.28 0.0034 0.62 48.4
Mature median nd 0.150 0.058 49.6 0.024 1.08 0.0006 0.31 36.2
P0.9 0.0061 1.316 0.090 174 0.187 1.44 0.0066 0.51 44.2
Muscle
Lamb median nd nd nd 0.72 nd 0.009 nd 0.070 38.9
P0.9 0.0055 nd 0.005 0.97 nd 0.016 nd 0.147 52.8
Young median nd nd nd 0.72 nd 0.010 nd 0.085 38.0
P0.9 nd 0.004 0.005 0.97 nd 0.016 nd 0.168 49.7
Mature median nd nd 0.004 0.76 nd 0.013 nd 0.080 40.2
P0.9 nd 0.008 0.009 0.89 nd 0.023 nd 0.150 56.6
nd = below the limit of detection
P0.9 = 90th percentile
 Page 31 of 33

Table 6 Significant correlations between elements and tissues based on Pearson’s correlation
coefficients. For n = 152, correlations are significant at 5% if >0.16, at 1% if >0.21 and 0.1% if >0.29.
Where sample sizes are less than 152, the sample size is reported in brackets.
Kidney1- Liver1- Kidney1- Muscle1- Liver1- Muscle1- Kidney1- Liver1-
1 2 Liver2 Kidney2 Muscle2 Kidney2 Muscle2 Liver2 Kidney2 Liver2
Cd Cd 0.84 0.71 (31) 0.73 (32)
Cd Hg 0.33 (74)
Cd Mo 0.17 0.16
Cd Pb 0.49 (120) 0.44 0.34 0.36 (138) 0.56
Co Co 0.55 0.28 (52)
Co Cu -0.20 -0.17 -0.30 (52) -0.25
Cu Mo -0.32
Cu Pb
Cu Se 0.28 0.26
Cu Zn 0.30 0.28 0.41 0.77
Hg Pb 0.29 (69) 0.56 (66)
Hg Se 0.19 (125)
Hg Zn
Pb Pb 0.23 (119)
Mo Pb 0.24 (121) 0.25 (139)
Mo Se 0.23 0.16
Mo Zn 0.22
Se Se 0.38
Se Zn 0.16 0.37
Zn Zn 0.19
Page 32 of 33

Table 7 Mean concentrations of arsenic, cadmium, mercury and lead (mg kg -1 FW) reported in sheep
kidney from various countries (values in parentheses are number of samples analysed)
As Cd Hg Pb Class Country (region) Reference
0.005 (182) 0.853 (182) 0.0055 (182) 0.056 (182) Sheep Australia This study
0.46 (10) 0.24 (10) Sheep 1-3yr China (Gansu) Liu 2003
0.014 a (25) 0.235 a (25) 0.007 a (25) 0.034 a (25) Sheep 1-3 yr Croatia Bilandžića et al., 2010
0.880 (12) 0.181 (12) Sheep Egypt (rural) Abou-Arab 2001
0.820 (12) 0.541 (12) Sheep Egypt (industrial) Abou-Arab 2001
0.547 (71) Sheep Germany Schulz-Schröder 1991
0.83 (70) 0.85 (70) Sheep Greece Zantopoulos et al., 1999
0.058 (96) 0.012 (96) Lambs <6m Iceland Reykdal & Thorlacius 2001
0.023 (60) Sheep 1-6 yr Iran Kazemeini et al., 2010
1.035 (30) 0.696 (30) Lambs Italy Amodio-Cocchieri & Fiore, 1987
<0.0035 0.172 Lambs Italy Forte & Bocca 2007
1.68 b (4) 0.0021 b (4) 0.5 b (4) Sheep Italy (SW) Caggiano et al., 2005
3.87 (40) Sheep Jordan Massadeh et al., 2006
0.301 (16) 0.145 (16) Sheep Kuwait Husain et al., 1996
0.310 (26) Sheep Kuwait Al-Sabbagh 2012
0.057 (20) Sheep < 1yr NZ (Otago) Birch et al., 1998
0.054 (20) Sheep 2yr NZ(Otago) Birch et al., 1998
0.229 (20) Sheep 4 yr NZ(Otago) Birch et al., 1998
0.586 (20) Sheep 6 yr NZ(Otago) Birch et al., 1998
0.25 Sheep NZ Solly et al., 1981
0.250 (5) Sheep Poland Falandysz 1991
0.27 (9) Sheep Slovakia Kramárová et al., 2005
0.751 (250) Sheep Spain (León) Sierra Carro et al., 2006
0.120 (98) 0.053 (98) Sheep Sweden Jorhem 1999
1.73 0.136 1.38 Sheep Turkey Şenavci et al., 1997
0.013 (52) Sheep UK Meharg 2009
0.18 (162) 0.64 Lambs USA Coleman et al., 1992
0.83 (34) Sheep mature USA Coleman et al., 1992
a geometric mean
b converted concentrations expressed on a dry weight basis to fresh weight equivalents by assuming kidney contains 75% moisture.
Page 33 of 33

Table 8 Maximum limits (mg kg-1 FW) for various trace elements in sheep tissues in various countries
or regions, figures in brackets are the number of samples above the standard compared to the total
number of samples analysed.
Element Liver Kidney Muscle Standard Reference
Arsenic (total) 0.5 (0) China China (2005)
0.1 fat (0) Codex Codex (2010)
1 (0) 1 (0) 0.1 (0) Russia Russia (2010)
Cadmium 1.25 (0/152a) 2.5 (1/152 a) 0.05 (0) Australia FSANZ (2015)
0.5 (0/152 a) 1 (2/152 a) 0.1 (0) China China (2005)
0.5 (0/152 a) 1 (2/152 a) 0.05 (0) European Union EC (2006)
0.5 (0/152 a) 1 (2/152 a) 0.05 (0) Mexico Mexico (2011)
0.3 (0/152 a) 1 (2/152 a) 0.05 (0) Russia Russia (2010)
Lead 0.5 (0) 0.5 (2/152) 0.1 (0/152) Australia FSANZ (2015)
0.5 (0) 0.5 (2/152) 0.2 (0/152) China China (2005)
0.1 (0/152) Codex Codex (2010)
0.5 (0) 0.5 (2/152) 0.1 (0/152) European Union EC (2006)
0.5 (0) 0.5 (2/152) 0.1 (0/152) Mexico Mexico (2011)
0.6 (0) 1 (0) 0.5 (0) Russia Russia (2010)
Mercury 0.05 (0) China China (2005)
0.1 (0) 0.2 (0) 0.03 (0) Russia Russia (2010)
a after implementation of age- and state-based sourcing requirements. If no risk management intervention were implemented the percentage

of kidney samples with cadmium concentrations above 1 and 2.5 mg kg -1 would be 24 and 13% respectively while the percentage of liver
samples with concentrations above 0.3, 0.5 and 1.25 mg kg-1 would be 24, 17 and 5.3%.