Selenium and 17 other largely essential and toxic metals in muscle and organ meats of Red Deer (Cervus elaphus) — Consequences to human health

Environment International 37 (2011) 882–888

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Environment International j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / e n v i n t

Selenium and 17 other largely essential and toxic metals in muscle and organ meats of Red Deer (Cervus elaphus) — Consequences to human health Grażyna Jarzyńska, Jerzy Falandysz ⁎ Research Group of Environmental Chemistry, Ecotoxicology & Food Toxicology, Institute of Environmental Sciences & Public Health, University of Gdańsk, 18 Sobieskiego Str., PL 80-952 Gdańsk, Poland

a r t i c l e

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Article history: Received 20 January 2011 Accepted 28 February 2011 Available online 22 March 2011 Keywords: Game animals Big game Food Food contaminants Heavy metals

a b s t r a c t Concentrations, composition and interrelationships of selenium and metallic elements (Ag, Ba, Cd, Co, Cr, Cs, Cu, Ga, Mn, Mo, Pb, Rb, Sb, Sr, Tl, V and Zn) have been examined in muscle and organ meats of Red Deer hunted in Poland. The analytical data obtained were also discussed in terms of Se supplementation and deficit to Deer as well as the benefits and risk to humans associated with the essential and toxic metals intake resulting from consumption of Deer meat and products. These elements were determined in 20 adult animals of both sexes that were obtained in the 2000/2001 hunting season from Warmia and Mazury in the north-eastern part of Poland. The whole kidneys contained Ba, Cd, Cr, Ga, Pb, Se, Sr and Tl at statistically greater concentrations than liver or muscle tissue from the same animal. Liver showed statistically greater concentrations of Ag, Co, Cu, Mn and Mo than kidneys or muscle tissue, and muscle tissue was richer in Zn, when compared to the kidneys or liver. Cs and Rb were similarly distributed between all three tissue types, while V was less abundant in liver than kidneys or muscle tissue. There were significant associations between some metallic elements retained in Red Deer demonstrated by Principal Component Analysis (PCA) of the data set. In organ and muscle meats (kidneys, liver and muscle tissue considered together) the first principal component (PC1) was strongly influenced by positively correlated variables describing Se, Ba and Cd and negatively correlated variables describing Ag, Co, Cs, Mn, Pb, Tl and V; PC2, respectively, by Cu, Mn and Mo (+) and Zn (−); PC3 by Ga (+) and PC4 by Sb (+). Selenium occurred in muscle tissue, liver and kidneys at median concentrations of 0.13, 0.19 and 4.0 mg/g dry weight, respectively. These values can be defined as marginally deficient (b 0.6 mg Se/ kg liver dw) or satisfactory (≤ 3.0 mg Se/kg kidneys dw) for the amount required to maintain the Deer's body condition and health, depending on the criterion for supplementation used. In terms of human nutritional needs, a relatively high selenium content of kidneys can be beneficial. The muscle meat, liver and kidneys of Red Deer can be considered as a very good source of essential Co, Cr, Cu, Mo, Mn, Se and Zn in the human diet. Lead is generally considered as toxic, and the concentrations found in Red Deer (via the food chain intake) were well below the European Union tolerance limit. Pb from the lead bullets can always create food hygienic problem, if not well recognized during sanitary inspection, and this was noted for one muscle meat sample in this study (5% surveyed). There is no tolerance limit of Cd in game animal meats. The median values of Cd noted in fresh muscle tissue, liver and whole kidneys were 0.07, 0.18, and 3.3 mg/kg wet weight, respectively. Cd exists as a chemical element present at trace levels in plants and mushrooms in Deer's food chain in background (uncontaminated) areas. When these are consumed by the Deer, the amount of Cd sequestered with metallothioneins and retained in the organ and muscle meat in this study is low enough to be considered safe for human consumption. © 2011 Elsevier Ltd. All rights reserved.

1. Introduction Muscle and organ meats of game animals are traditionally valued as natural food that is both tasty and nutritious. There is also a current preference for wild foods, which may be seen as ‘organic’, over conventionally reared farm produce using intensive conditions which

⁎ Corresponding author. Tel.: + 48 58 5235372; fax: + 48 58 5235472. E-mail address: [email protected] (J. Falandysz). 0160-4120/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.envint.2011.02.017

can be perceived as artificial. Environmental pollution with inorganic, organic and organometallic compounds is a deleterious factor impacting quality of foods. A comprehensive, simultaneous examination of all desired compounds but also the relevant environmental and toxic agents (e.g. heavy metal species, pesticides, metalloids, radionuclides, persistent organic pollutants, mycotoxins, pharmaceuticals, and biological vectors), which can contaminate any potential set of food can never be comprehensively achieved. One of the possible threats comes from trace mineral constituents that can be beneficial or highly toxic, depending on the concentration found.

G. Jarzyńska, J. Falandysz / Environment International 37 (2011) 882–888

In case of the game muscle and organ meats the presence of Pb can create a specific hygienic problem. This is because the lead bullets, and especially those of shell burst type, always are the secondary source of Pb in these meats. This problem, and also a high Pb content of some game meat products purchased (e.g., pâ té), and the associated risk to human health, were first identified in Poland in the 1980s (Falandysz and Caboń, 1990). In a similar way, the White-tailed Sea Eagle (Haliaetus albicilla) was also a victim of Pb poisoning due to the Pb bullets or shot contained in carcasses of game animals (Falandysz et al., 1988, 2001a). Pb, Cd and Hg, and less frequently Cu, Fe, Mn and Zn, and exceptionally also highly toxic alpha nuclides (210Po), were identified in game meats in Poland (Falandysz, 1994; Falandysz et al., 2005; Skwarzec and Prucnal, 2007). Selenim (Se), which, depending on chemical species, has a relatively narrow margin of safety between an adequate, inadequate and excess intake, is highly potent and has great health impacts (Falandysz, 2008). In mammals, various Se species can be utilized for selenoproteins synthesis. Certain of them (containing selenocysteine), can be well tolerated if in excess to the standard nutritional needs. Se in non-Se-accumulating plants is contained largely as selenomethionine and less as selenocysteine — both in plant proteins. In Se-accumulating and Se-rich plants (Allium and Brassica spp.) Se is abundant also in detoxification products (metabolites) of these Seamino acids, such as Se-methyl-selenocysteine and γ-glutamyl-Semethylselenocysteine, while less as certain other Se-compounds (Dumont et al., 2006). Selenomethionine, incorporated instead of methionine into the plant proteins in the food chain, is incorporated (preferentially) and accumulated into the structural proteins of animal body. As such, it is less accessible when compared to selenocysteine of animal meats which is a better Se source for selenoenzymes expression. A good bio-available source of Se from foods is needed for full expression of selenoproteins with antioxidant function and particularly in diseases associated with oxidative stress. Se in selenocysteine is cofactor for a range of selenoenzymes contained in animal meats that can be considered as the most useful Se species for foods. Methyl selenol (CH3SeH), formed from the selenoproteins and in a biotransformation pathway of Se-methyl selenocysteine and γ-glutamyl-Se-methyl selenocysteine, is reported to be a potent anti-cancer agent (Rayman, 2008; Rayman et al., 2008). In Poland there is no data available on Se and many other trace metals in local populations of Red Deer (Cervus elaphus), which together with the Roe Deer (Capreolus capreolus) and especially the Wild Boar (Sus scrofa), highly dominate the big game species hunted. The aim of this study was to determine the content, composition and status of Se and 17 other metallic elements (Ag, Ba, Cd, Co, Cr, Cs, Cu, Ga, Mn, Mo, Pb, Rb, Sb, Sr, Tl, V, and Zn) in muscle and organ meats of Red Deer and to relate these analytical facts to meats and elements intake rates in the light of human requirements and associated health impacts.

2. Material and methods The muscle, kidney and liver samples were collected from 20 healthy Red Deer from Warmia and Mazury regions of Poland between October 2000 and January 2001 (Fig. 1). Aliquots of around 200–500 mg of the dried (at 105 °C) muscle tissue, liver and kidney samples were accurately weighted into closed vessels made of polytetrafluoroethylene (PTFE). The tissue was pre-digested with concentrated nitric acid solution (60%; 5 ml) at room temperature and further digested under pressure in an automatic microwave digestion system type MLS 1200. All reagents were of analytical grade. Nitric acid used was of super analytical grade (Kanto Chemicals Co. Inc., Chouku, Tokyo, Japan). Double distilled water was used to prepare the solutions and analyses were performed using clean practices (Falandysz et al., 2007a,b, 2008b).

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Fig. 1. Location of the Red Deer hunting ground in the north-eastern part of Poland.

2.1. Elements measured Se was determined by hydride generation-atomic absorption spectroscopy method (HVG-1 hydride system, Shimadzu, Kyoto, Japan). Other elements were determined using inductively coupled plasma-mass spectrometry (ICP-MS; Hewlett-Packard, HP-4700, Avondale, PA, USA) and external quantitative standards. Indium was an internal calibration standard added to each sample (Falandysz et al., 2007a,b, 2008b). 2.2. Analytical quality control/quality assurance The analytical methods used were validated by the analysis of several certified reference materials and through the participation in inter-laboratory trials. The standard reference materials used were such as Dogfish muscle (DORM2; National Institute of Standards, Ottawa, Canada) and SRM1577b (National Institute of Standards and Technology, Gaithersburg, MD, USA) (Falandysz et al., 2007c, 2008a). Discrepancies between the certified values and concentrations quantified were below 10%. For blank samples no major interferences were found for the trace chemical elements quantified. 2.3. Data analysis The computer software Statistica version 8.0 was used for data statistical analysis. Principal Component Analysis (PCA) was performed after log-transformation of elementary data. 3. Results and discussion Data on trace metals composition and interrelationships in Red Deer are shown in Table 1 and Figs. 2 and 3. The kidney contained Ba, Cd, Cr, Ga, Pb, Se, Sr and Tl at statistically greater concentrations than liver or muscle (b0.05 p b 0.001; Mann– Whitney U test). Liver showed greater concentrations of Ag, Co, Cu, Mn and Mo than kidney or muscle, and muscle was richer in Zn than kidneys or liver (b0.05 p b 0.001; Mann–Whitney U test). Cs and Rb were similarly distributed between these tissues, while V was less abundant in liver than kidney or muscle. 3.1. Se The variability of Se concentrations of kidney in this study was low, since it ranged from 2.8 to 5.1 mg/kg dry weight (maximum to minimum concentration quotient: 1.8). For the liver, the range of concentrations found was between 0.053 and 0.42 mg/kg dw (quotient: 7.9), and for muscle between 0.053 and 0.37 mg/kg dw (quotient: 7.0). The

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Table 1 Some mineral constituent's content of muscle, liver and kidneys of Red Deer; mg/kg dry weight (dried to constant weight at 105 °C). Parameter

Ag

Ba

Muscle meat Mean (A) S.D. Median Min. Max.

0.005 0.004 0.004 0.002 0.017

0.16 0.15 0.093 0.035 0.57

Liver Mean S.D. Median Min. Max.

0.088 0.089 0.047 0.007 0.32

0.12 0.077 0.11 0.026 0.37

Kidneys Mean S.D. Median Min. Max.

0.006 0.008 0.003 0.001 0.010

0.44 0.18 0.45 0.056 0.83

Cd

Co

Cr

Cs

0.22 0.13 0.21 0.032 0.45

0.017 0.007 0.015 0.007 0.033

0.52 0.34 0.50 0.13 1.3

0.15 0.26 0.06 0.01 0.49

0.70 0.39 0.55 0.22 1.9

0.18 0.054 0.18 0.079 0.32

0.55 0.59 0.28 0.11 2.2

0.16 0.36 0.04 0.005 1.6

59 41 49 12 125

0.016 0.018 0.014 0.002 0.083

0.089 0.035 0.086 0.041 0.22

1.4 1.4 0.78 0.14 4.0

0.24 0.51 0.06 0.01 2.3

21 4 21 10 27

0.038 0.016 0.041 0.005 0.067

12 8 9.9 2.2 28

Cu 11 4 10 5.7 22

Ga 0.019 0.018 0.011 0.003 0.066

median values for Se in muscle, liver and kidney were 0.13, 0.19 and 4.0 mg/kg dw and these corresponded well with the mean values, respectively (Table 1). The liver and kidney Se concentrations in this study are roughly similar to what was found in Roe Deer in Poland, where it varied seasonally between 0.29 ± 0.13 and 1.3 ± 0.8, and 2.0 ± 0.8 and 5.1 ± 1.6 mg/kg dw, respectively (Pilarczyk et al., 2008). The medians of Se in Red Deer in this survey, when converted to fresh tissue concentrations (assuming 67% of moisture), were 0.043 (muscle), 0.063 (liver) and 1.3 mg/kg (kidney). In Red Deer in Croatia concentrations were 0.048, 0.11 and 1.6 mg Se/kg wet weight in muscle, liver and kidney, respectively (Lazarus et al., 2008). A value of 0.09 (0.04–1.0) mg Se/kg dw was median in Red Deers' liver in Norway (Vikøren et al., 2005). Se in liver in this study was, on the average, close to 0.6 mg/kg dw. This value, in the light of suggestion by Pollock (2005), can be considered as a marginally deficient (b 0.6 mg/kg dw) for Deer. A farmed young Red Deer with the symptoms of the white muscles disease (caused by Se deficiency) contained b 0.035 mg Se/kg ww in liver (b 0.12 mg/kg dw; 67% water) (Wilson and Grace, 2001). If this criterion is considered as the critical level, up to 20% of specimens in our study could be classed as Se deficient. According to McDowell et al. (1995), Se in kidney at 3.0 mg/kg dw is classed as a deficiency in Red Deer. In our study just 1 of 20 animals had Se in kidneys below this value (range 2.8–5.1 mg/kg dw). The Se enzyme glutathione peroxidase-3 (Gpx3) is secreted by the kidney into plasma. It binds to specific basement membranes of renal cortical tubule cells, intestinal mucosa cells, bile duct cells, gall bladder mucosal cells and efferent duct cells, and in mice both the Gpx3 and selenoprotein-P account for over 97% of plasma Se (Olson et al., 2010). A relative abundance of selenium in the Deer's kidney seems to be related mainly to the content of Gpx3 and its seleno-substrates. The currently recommended dietary daily intake of Se for humans is 57 μg (range 30–85 μg) but this sometimes can be insufficient for the expression of selenoprotein-P, which is considered to play a particular role in scavenging peroxynitrite and is required for the transport of Se and for certain brain functions (Rayman, 2008). There are many factors for which Se plays a role, and these need to be considered when deciding an optimal human supplementation with dietary Se (its species) and including a key cooccurrence of vitamin E and other antioxidants but also other mineral constituents such as hazardous As, Cd and Hg. Kidney of Red Deer in this study can be considered as good source of Se for human nutrition and the consumer can also benefit from the Co, Cr, Cu, Mn and Zn present (Table 1). Cooking can have a small effect on leaching of Se from meats but the Se will remain in the sauce or soup and so will often be consumed. Eating 50–100 g of Deer kidney in a meal results in an intake of 65–130 μg Se (largely as Gpx-3) and if other meal ingredients are taken into account that can also contain Se, the result is within a high-adequate intake rate (approximately, 100–200 μg Se/day) (Rayman, 2008). Liver of Red Deer is only ca. 1.5-fold better source of Se than muscle meat and eating a 50– 100 g portion of liver results in 3.1–6.3 μg Se but also 800–1600 μg of Cu and 1650– 3300 μg Zn intake, on the average, respectively. These values for Cu and Zn intake can be considered as highly adequate and safe, because the recommended intake of Cu for healthy men and women is between 900 and 1300 μg per day (Stern, 2010), and for Zn is between 3300 and 3800 μg per day (Boreiko, 2010). The kidney concentrations of Se were largely uniform between Red Deer (p N 0.05; Student's t-test), when compared to the more variable content of Cd. This suggests physiological saturation with respect to Se — as an essential element to Gpx3. Cu, Zn and Mn concentrations in kidneys were largely uniform too, and, if two extreme values were rejected as outliers, the maximum to minimum concentration quotients for these metals would be 1.4, 1.4 and 1.8, respectively, while for Cd the value was 7. These findings may suggest on saturation with the essential elements in Red Deer's surveyed.

Mn

Mo

Pb

Rb

Sb

Se

Sr

Tl

V

Zn

0.17 0.06 0.16 0.082 0.32

0.18 0.34 0.076 0.014 1.4

19 18 13 2.9 75

0.020 0.048 0.005 0.005 0.03

0.14 0.08 0.13 0.053 0.37

0.13 0.08 0.10 0.040 0.36

0.026 0.035 0.009 0.002 0.14

0.026 0.028 0.016 0.005 0.095

150 55 140 87 290

12 3.9 11 5.2 21

3.1 0.8 3.2 1.4 4.2

0.17 0.11 0.15 0.048 0.44

23 22 13 4.6 85

0.009 0.010 0.005 0.005 0.034

0.20 0.10 0.19 0.053 0.42

0.11 0.045 0.091 0.048 0.19

0.047 0.048 0.037 0.004 0.18

0.013 0.019 0.007 0.001 0.086

100 21 100 66 150

6.6 1.5 6.3 4.7 11

1.4 0.5 1.5 0.18 2.1

0.30 0.26 0.24 0.089 1.3

21 20 12 4.5 80

0.007 0.004 0.005 0.005 0.01

4.0 0.6 4.0 2.8 5.1

0.18 0.07 0.16 0.040 0.36

0.28 0.29 0.17 0.015 1.3

0.019 0.017 0.014 0.003 0.040

130 19 130 100 170

2.3 0.9 2.1 0.89 4.0

A protective role of metallothioneins in a firm binding a food chain Cd, which is usually increasingly accumulated in kidney with age of mammals, is not followed by Se in Deer examined. Hence, a possible the protective role of Se against Cd toxicity (small doses of Cd absorbed via the food chain relationships of Deer) seems not to be a case in this study. This finding implies also that impact from Cd that is relatively high in Deer kidneys, is neutralized by metallothioneins without a special involvement of Se. Cd is higher in kidney of older (4–6 and N 6 years) when compared with younger (b 1.5 and 1.5–3.0 years) Deer but with Se, this is not the case (Lazarus et al., 2008). Principal component analysis (PCA) was applied to analyze the correlation matrix obtained from data for kidney, liver and muscle tissue alone and for these tissues together for Red Deer. This correlation matrix did indicate the existence of significant association between some metallic elements of Red Deer independently of the tissue. The correlation matrix was computed for 17 variables by the principal component method. The PCA of the data matrix projected models that accounted for 84% of the total variance for kidneys, 77% for liver, 87% for muscle tissue and 77% for kidneys, liver and muscle tissue together. These models explained, in detail, for kidneys 27, 42, 53, 62, 70, 78 and 84% of cumulative variability associated with the principal component (PC) 1, 2, 3, 4. 5. 6 and 7, respectively; for liver explained 26, 41, 52, 63, 70 and 77% of variability associated with PC1, 2, 3, 4, 5 and 6; for muscle meat explained 30, 49, 62, 72, 81 and 87% of variability associated with PC1, 2, 3, 4, 5 and 6; and for kidneys, liver and muscles together explained 48, 62, 71 and 77% of cumulative variability associated with PC1, 2, 3 and 4. Figs. 2 and 3 show graphically the interdependences among the metallic elements. The factor loadings (not visualized) shows that for kidneys the PC1 is strongly influenced by positively (+) correlated variables describing Ag and Co and negatively (−) correlated variables describing Ba, Cs, Cu, Ga and Sr; PC2 is influenced by Cr (+) and Rb (−); PC3 with Mo (−) (Fig. 2a) and PC4 by Se (−). In case of liver alone PC1 is strongly influenced by negatively correlated variables describing Ba, Cs, Ga, Rb and V; PC2 by Ag and Cu (−) and Mo (+) (Fig. 2b); PC4 by Se (+) and PC5 by Cd (−). In the case of muscle tissue PC1 is strongly influenced by negatively correlated variables describing Ba, Co, Ga, Mn, Se and Sr; PC2 by Ag, Cd, Cs and Rb (+); PC3 by Cr and V (−) (Fig. 2c); PC4 by Pb (+) and PC5 by Tl (+). In the case of kidneys, liver and muscle tissue considered together PC1 is strongly influenced by positively correlated variables describing Se, Ba and Cd and negatively correlated variables describing Ag, Co, Cs, Mn, Pb, Tl and V; PC2 by Cu, Mn and Mo (+) and Zn (−); PC3 by Ga (+) and PC4 by Sb (+) (Fig. 3). The configurations of cluster inter-correlations can be explained by considering that the trace metal content of Red Deer depends on: (i) essentiality concentrations of Co, Cr, Cu, Mn, Mo, Se and Zn; (ii) co-occurrence, availability and uptake from the Deer's diet of mineral nutrients not considered in this survey, e.g. Fe, Mg, Ca, K, Na; (iii) detoxification strategy — binding to metallothioneins and other proteins with sulphuryl (− SH) groups of toxic metals such as Ag, Ba, Cd, Pb, Sb, Sr, and Tl; and (iv) deficiency or excess and competitive absorption and retention or homeostatic regulation (Cu and Zn) of those usually found among the metallic elements ingested with food and water at background (uncontaminated) areas. Co-absorption of certain metals (toxic or non-essential), due to their chemical similarity to essential metals and their relative abundance in the Deer's diet, can be an explanation for the behavior of Se– Ba–Cd–Ag–Co–Cs–Mn–Pb–Tl–V and Cu–Mn–Mo–Zn in Red Deer, respectively. Both Cd and Se but also Ba and Tl occurred in greater concentration in kidney than liver or muscle (Table 1). Also Hg is compound usually accumulated in greater concentration in kidney than liver or muscles of Red Deer and also of cattle (Falandysz, 1991, 1993, 1994; Falandysz et al., 1994c). Hg is poor in plants but is efficiently bioconcentrated in mushrooms that are often eaten by Deer (Falandysz and Chwir,

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Fig. 3. Plot of loadings based on the concentration of metallic elements (n = 18) in muscle and organ meats (kidneys, liver and muscle tissue together) of Red Deer in three dimensional space of first, second and third principal components.

1997). Since Cd in kidneys is mostly bound in metallothioneins, the Hg can have some associations with Se. Methylmercury can be an irreversible inhibitor of selenoenzymes (high binding affinity to selenocysteine of selenoproteins) (Ralston et al., 2010). Selenoneine is a major organoselenium compound identified in tuna fish muscle (Yamashita et al., 2010). 3.2. Cu, Zn, Cd, and Pb

Fig. 2. Plot of loadings based on the concentration of metallic elements (n = 18) in kidney (a), liver (b) and muscle meat (c) of Red Deer in three dimensional space of first, second and third principal components.

The median values of Cu and Zn, and toxic Cd and Pb for muscles, liver and kidneys (Table 1), when converted to fresh weight tissue data are: 3.3, 16 and 6.9 (Cu); 46, 33 and 43 (Zn); 0.07, 0.18, and 3.3 (Cd); 0.025, 0.05 and 0.079 mg/kg ww (Pb). These values are roughly within the ranges noted for Cu, Zn, Cd and Pb in the Red Deer earlier examined in Poland — as reviewed by Falandysz et al. (2005) or hunted in other countries (Kottferová and Koréneková, 1998; Pokorny and Ribarič-Lasnik, 2000; Gasparik et al., 2004; Bilandzic et al., 2009). Cu and Zn are the cofactors to many enzymes and a key role of Cu in human health is also due to its involvement in absorption, utilization and transport of Fe in body, and so, prevention from the Fe deficiency. A meal consisting of a 50–100 g portion of muscle meat, liver or kidney will provide Cu at 0.16–0.33, 0.80–1.6 and 0.34–0.69 mg, and Zn at 2.3–4.6, 1.6–3.3 and 2.2– 4.3 mg, respectively. An adequate intake of these trace elements by adults is 1.5–4 mg (Cu) and around 10 mg (Zn) per day (Kabata-Pendias and Pendias, 1999). Hence, Deer muscle and organ meat is a good source of Cu and Zn. Lead bullets and especially those of shell burst type are always the secondary source of Pb in all tissues of hunted big game. Close proximity to the wound site and is usually very high in Pb when lead shot is used. An important source of Hg, Cd and Pb but also of many other metals and metalloids to Red Deer are forest, pasture and meadow mushrooms which can be available as a diverse range of species, all of which are efficient bio-concentrators of trace elements (Brzostowski et al., 2009, 2011a,b; Chudzyński et al., 2009, 2011; Chudzyński and Falandysz, 2008; Falandysz, 2002, 2008; Falandysz et al., 2001b, 2002a,b,c,d, 2003a,b,c, 2007c, 2004, 2011; Falandysz and Bielawski 2001, 2007; Frankowska et al., 2010; Jarzyńska and Falandysz, 2011; Pokorny and Ribarič-Lasnik, 2000; Zhang et al., 2010). Cd and Pb in muscles and organ meats of big game animals are two toxic metals of primary concern. There are no tolerance limits of Cd and Pb in game animal meats. In the European Union the maximum levels of Cd allowed in meat, liver and kidneys of the slaughtered animals such as bovine animals, sheep, pig, poultry and horse are, respectively, 0.050, 0.50 and 1.0 mg/kg ww (EC, 2008). For Cd, the median values of this metal in fresh muscle tissue, liver and whole kidney were 0.07, 0.18, and 3.3 mg/kg ww, respectively. Cd is usually present in trace amount in plants, and can be measured in samples sourced from background (uncontaminated) areas, but it is bio-concentrated by many wild mushroom species, which can be consumed by Deer. Cd is accumulated in the kidney with concentrations increasing in relation to the age of the animal. The provisional tolerable weekly intake (PTWI) set by the Joint FAO/WHO Expert Committee on Food Additives (JECFA) for Cd is 7 μg/kg body weight (equivalent to 1 μg/ kg bw per day) (WHO, 1989), and a tolerable weekly intake (TWI) of 2.5 μg/kg bw (equivalent to 0.36 μg/kg bw per day) was established by EFSA (EFSA, 2009). The estimated Cd intake resulting from the consumption of a 50–100 g portion of muscle tissue, liver or kidney is: 0.0035–0.0070, 0.009–0.018 and 0.165–0.33 mg (equivalent to 0.05–0.1, 0.13–0.26 and 2.3–4.7 μg/kg bw), respectively, based on the median values of Cd concentrations noted in Deer muscle and organ meat from this survey. The assessed

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doses show that a single meal composed of 50–100 g kidney meat will result in exceeding the PTWI and revised TWI rates for Cd. This is because of elevated absolute Cd concentration in kidneys. Nevertheless, in the kidney of game animals from unpolluted areas, Cd is almost likely retained in the form bound to metallothioneins. These endogenous proteins are characterized by their high affinity to divalent “heavy metals” such as cadmium (Cd II). Apart from Cd, the metallothioneins can be also rich in bound Cu, Zn, Hg and Ag, which can all induce synthesis of these endogenous ligands. Cd in metallothioneins is relatively firmly bound (Merian, 1991), but its toxicological significance when found in foods is disputable matter of some debate. Because of mentioned facts and due to the uncertainty in allowable intake rates assessment (margin of safety in toxicology), and the relatively infrequent consumption of game for most of the population, meaning the risk is not necessarily great. Hence, Cd in the amounts found in both organ and muscle meat in this study might be considered as safe for human consumption. In the case of Pb, the maximum levels permitted by EU regulations in meat and offal of bovine animals, sheep, pig, poultry and horse are, respectively, 0.10 and 0.50 mg/kg ww (EC, 2006). A few of the muscle meat samples (5%) contained Pb at concentrations well above 0.10 mg/kg. In these cases the high Pb may be attributed to lead bullets used. A level of 0.50 mg Pb/kg was not exceeded in the case of the Deer's liver or kidneys. The acceptable daily intake of Pb for adults is between 0.21 and 0.25 mg per day and 1.5 and 1.75 mg per week (WHO, 1993). Estimated Pb intake from consumption of a 50–100 g portion of muscle, liver or kidney, was 0.0012–0.0025, 0.0025–0.0050 and 0.0039– 0.0079 mg, respectively. These values are based on the median amounts of Pb found in Deer muscle and organ meats from this survey. They show no cause for concern associated with Pb resulting from the consumption of between 50 and 100 g daily of Deer muscle, liver or kidney, on an occasional or regular basis. Since the muscle meat and kidneys of Red Deer are also a good dietary source of Se, Cu and Zn, benefits may outweigh any risks associated with Cd from metallothioneins in the kidney. Pb associated with the use of certain types of bullet, as discussed above, can be highly risky in game animal meats and especially to vulnerable individuals. Good practice and a proper veterinary inspection should result in the removal of the wound area and thus the tissues with elevated Pb concentrations. The most vulnerable individuals to consuming this tissue would be those who particularly enjoy consuming game meat and those with easy access to this kind of foods — the hunters and their relatives, those engaged in processing industry and the employees in the game meet serving restaurants (the hunters' restaurants). Certainly, exposure could be minimized or avoided by the use of a different type of bullet that does not contain Pb.

compared to an estimated safe and adequate daily dietary intake of Mn for adolescents and adults. Mn is micronutrient abundant in vegetables and cereals (Kabata-Pendias and Pendias, 1999), which are the major Mn source for human. Mo in animals and man is an essential component of the enzymes xanthine oxidase, aldehyde oxidase and sulphite oxidase (Anke et al., 2010). As estimated by World Health Organization (WHO) a daily requirement for Mo to adults is of 0.1–0.3 mg (Rose et al., 2010). Liver is considered richest in the Mo enzymes but kidneys are also abundant in Mo. This element was found in Deer liver in greater concentration (median: 3.2 mg/kg dw), when compared to muscle with 0.16 or kidney with 1.5 mg/ kg dw (0.001 b p b 0.01; Table 1). A meal consisting of a 50–100 g portion of muscle meat, liver or kidney will provide Mo at 2.5–5.3, 50–100 and 25–50 μg, which is a small or adequate portion of a daily requirement to adults, respectively. 3.4. Ga, Rb, and V Ga has physical and chemical properties similar to Fe and they both share a similar metabolic pathway, while no a definite biological function is known. Kidney was richer in Ga (p b 0.001) than muscle or liver and the median concentrations found were 0.041, 0.011 and 0.014 mg/kg dw, respectively. Rb is antagonistic to Li (lithium) and abundant in meats (Kabata-Pendias and Pendias, 1999). The median values of Rb were 13 mg/kg dw for muscle and liver and 12 mg/kg dw for the kidney. Hence, the muscle and organ meat of Red Deer can be considered also as a good source of Rb, while this element has no a given physiological significance (Kabata-Pendias and Pendias, 1999). The median concentrations of V were 0.016, 0.014, and 0.007 mg/kg dw in the muscle, kidney and liver respectively. This metal is usually found in various types of fresh food below 0.1 mg/kg but data are limited (Merian, 1991). As reviewed by Falandysz et al. (2007c), in the European forests, the Fly Agaric (Amanita muscaria) mushroom is a type of vegetation exceptionally rich in V. Fly Agaric, depending on the site harvested in Poland, contained V in caps in concentrations varying between 22 ± 11 and 130 ± 45 mg/kg dw, while in whole fruiting bodies collected from the Czech Republic, concentrations were between 190 ± 6 and 260 ± 8 mg/kg dw (Falandysz et al., 2007c). V is thought to be a possible essential element that reacts with hydrogen peroxide to form a pervanadate that is required to catalyze the oxidation of halide ions and/or stimulate the phosphorylation of receptor proteins (Anke et al., 2002). 3.5. Ag, Ba, Sb, Sr, and Tl

3.3. Co, Cr, Cs, Mn, and Mo Co in liver (and less so in kidney) of Red Deer is a relatively abundant metal — in the light of it being essential to animals and humans and its occurrence in meat in the form of a component of vitamin B12. The median values of Co are 0.18 for liver, 0.086 for kidneys and 0.015 mg/kg dw for muscle (Table 1). A meal consisting of a 50–100 g portion of muscle meat, liver or kidney will provide Co at 0.25–0.5, 2.9–5.8 and 1.4– 2.8 μg. Estimated dietary intake of Co by adult humans is 40–50 μg daily, while its absorption rate from gastrointestinal tract is 50% (Kabata-Pendias and Pendias, 1999). Cr, as reviewed by Krejpcio (2001), is an essential element for the human and is associated with biologically active Cr (naturally occurring tri-valent Cr, while hexavalent Cr doesn't occurs naturally) as a cofactor of insulin which is involved in glucose metabolism as well as in lipid and protein metabolism. Cr in Red Deer from unpolluted regions seems to be naturally occurring and present in the tri-valent form. Kidney is richer with respect to Cr with a median of 0.78 mg/kg dw (p b 0.001; Mann–Whitney U test), when compared to the liver with 0.28 or muscle with 0.50 mg/kg dw (Table 1). An adequate Cr intake is believed to be about 25 μg per day for adults and between 0.1 and 1.0 μg for children and adolescents — as quoted by Rose et al. (2010). According to some other sources the adequate daily dose for children (N6 years), adolescents and adults is 50–200 μg (Krejpcio, 2001). Based on the median values of Cr in muscle and organ meats of Red Deer, re-calculated to fresh weight, eating a 50–100 g portion of muscle meat, liver or kidneys will result in intake of 4.6 – 9.2, 8–16 and 13–26 μg Cr, respectively. The reported the adequate daily dose of Cr for adults vary between 25 and 200 μg, i.e. nearly 10-fold, and Deer's muscle meat, liver or kidneys can be more or less a good source of this micronutrient. Cs has antagonistic properties in relation to K. At toxic doses this metal accumulates in soft tissues (Kabata-Pendias and Pendias, 1999). Cs was similarly distributed between tissues examined with the median values of 0.06 in muscles, 0.06 in kidneys and 0.04 mg/kg dw in the liver. Mn, which in animal cells is associated as an enzymatic cofactor in mitochondria, takes a role in the regulation of cell metabolism, receptor binding and signal transduction pathways, and an estimated safe and adequate daily dietary intake of Mn for adolescents and adults ranges from 2 to 5 mg (Santamaria and Sulsky, 2010). The UK Expert Group on Vitamins and Minerals assumed, for guidance purposes, that daily total Mn intakes up to 200 μg per kg bw (14 mg for 70 kg bw man) in the general population is unlikely to result in adverse effects (Rose et al., 2010). Mn in Red Deer occurred at median concentration of 11 mg/kg dw in rich in mitochondria liver, while was less abundant (p b 0.001) in kidneys with 2.1 and muscles with 6.3 mg/kg dw (Table 1). A meal consisting of a 50–100 g portion of muscle meat, liver or kidney will provide Mn at 34–69, 180–360 and 105–210 μg, which is a small or adequate portion of a daily requirement to adults, respectively. These doses are relatively small when

Ag on the average was twelve to sixteen-fold higher (median values) in liver (range 0.007–0.32) than muscle (range 0.002–0.017) or kidney (0.001–0.10 mg/kg dw) (Table 1). Ag has a high affinity to sulfhydryl, amino and phosphate groups, and it readily complexes with many endogenous ligands of the mammalian body. Ag is easy taken-up by and can be abundant in wild mushrooms that are foods for Deer (Borovička et al., 2009; Falandysz et al., 1994a,b; Falandysz and Danisiewicz, 1995), while in trace amount is always found in animal and plant origin foods (Merian, 1991). Soluble Ag in the diet is antagonistic to Se. Ba in the human body accumulates mainly in bone tissue. The daily intake of Ba for humans is assessed on around 500 μg (Kabata-Pendias and Pendias, 1999). The possibility that Ba is an essential element has not yet been well documented. Deer kidney with a median value of 0.45 mg/kg dw are richer in Ba, compared to the liver with 0.11 mg/kg dw or muscle with 0.093 mg/kg dw (Table 1). Sb is a toxic element and is known to share some of the toxic features of As. This trace but widespread element in the earth's crust is a common micro mineral toxic constituent in plants and animals from background (unpolluted) areas. In Red Deer Sb was present in ultra-trace concentrations and median values for the muscle and organ meats examined were 0.005 mg/kg dw (Table 1). A Tolerable Daily Intake of Sb is set by WHO at 6 μg per kg bw (Rose et al., 2010). In the United Kingdom, Sb in the meat products group contributes the greatest percentage (24%) to the total population dietary exposure (Rose et al., 2010). In our study, due to the small Sb content of Deer muscle and organ meats, these products can be considered as a minor source of this element (0.08–0.16 μg Sb per 50–100 g meat eaten). Sr is considered as an essential element involved in Ca and P management for animals. Nevertheless, the possibility that Sr is essential has not been confirmed. Its median concentration in meats examined were 0.10 mg/kg dw for muscle, 0.091 mg/kg dw for liver and 0.16 mg/kg dw for kidney. Tl is known due to its high acute toxicity to animals and human if absorbed at elevated doses. Plants and wildlife can contain Tl in tissues due to a widespread occurrence of this rare element in the earth's crust. Tl was found in muscles, liver and kidney of all Deer but in small concentrations (Table 1). Kidney with median value of 0.17 mg/kg dw are significantly (p b 0.001) more abundant in Tl, when compared to the liver with 0.037 mg/kg dw or muscles with 0.009 mg/kg dw.

4. Conclusions The muscle and organ meats of Red Deer can be considered as a good source of essential Co, Cr, Cu, Mo, Mn, Se and Zn in the human diet. Along with the toxic trace elements such as Hg, Pb, Cd, Ag, Sb or Tl (the trace mineral constituents found in the food chain of game at

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background concentrations), all are also micro-constituents of Deer muscle and organ meats. Cd in kidneys, due to the food web accumulation, exceeds tolerance limits imposed for slaughtered animal organ meats. Cd in kidneys is the most problematic heavy metal to the potential Deer organ meat consumers, while toxicological significance of this phenomenon is disputable matter of some debate. Because of mentioned facts and due to the uncertainty in allowable intake rates assessment (margin of safety in toxicology), and the relatively infrequent consumption of game for most of the population, meaning the risk of Cd in Deer kidneys is not necessarily great. Acknowledgements The authors are grateful to Dr. Marin Rose (UK), Dr. Takashi Kunito, Dr. Reiji Kubota and Dr. Shinsuke Tanabe (Japan) and Dr. Kazimierz Zalewski (Poland) for suggestions and support. A partial financial support by the Ministry of Science and Higher Education under grant DS/8250-4-0092-11 is acknowledged. References Anke M, Illing-Günther K, Günther H, Holzinger S, Jaritz S, Anke S, et al. Vanadium — an essential element for animals and humans? Trace Elem Man Anim 2002;10:221–5. Anke M, Sejfert M, Arnhold W, Anke S, Schafer U. The biological and toxicological importance of molybdenum in the environment and in the nutrition of plants, animals and man Part V: essentiality and toxicity of molybdenum. Acta Aliment 2010;39:12–26. Bilandzic N, Sedak M, Vrataric D, Peric T, Simic B. Lead and cadmium in Red Deer and Wild Boar from different hunting grounds in Croatia. Sci Total Environ 2009;407: 4243–7. Boreiko CJ. Essentiality and toxicity in copper health risk assessment: overview of health risk assessments for zinc. J Toxicol Environ Health A 2010;73:166–74. Borovička J, Kotrba P, Gryndler M, Mihaljevič M, Řanda Z, Rohovec J, et al. Bioaccumulation of silver in ectomycorrhizal and saprobic macrofungi from pristine and polluted areas. Sci Total Environ 2009;408:2733–44. Brzostowski A, Bielawski L, Orlikowska A, Plichta S, Falandysz J. Instrumental analysis of metals profile in Poison Pax (Paxillus involutus) collected at two sites in Bory Tucholskie. Chem Anal (Warsaw) 2009;54:907–19. Brzostowski A., Jarzyńska G., Falandysz J., Zhang D. Bioconcentration potential of metallic elements by Poison Pax (Paxillus involutus) mushroom. J Environ Sci Health Pt A 2011a;46:378–93. Brzostowski A, Jarzyńska G, Kojta AK, Wydmańska D, Falandysz J. Variations in metal levels accumulated in Poison Pax (Paxillus involutus) mushroom collected at one site over four years. J Environ Sci Health Pt A 2011b;46. doi:10.1080/10934529.2011.562827. Chudzyński K, Falandysz J. Multivariate analysis of elements content of Larch Bolete (Suillus grevillei) mushroom. Chemosphere 2008;73:1230–9. Chudzyński K, Bielawski L, Falandysz J. Mercury bio-concentration potential of Larch Bolete, Suillus grevillei, mushroom. Bull Environ Contam Toxicol 2009;83:275–9. Chudzyński K, Jarzyńska G, Stefańska A, Falandysz J. Mercury content and bioconcentration potential of Slippery Jack, Suillus luteus, mushroom. Food Chem 2011;125:986–90. Dumont E, Vanhaecke F, Cornelis R. Selenium speciation from food source to metabolites, a critical review. Anal Bioanal Chem 2006;385:1304–23. EC. Commission Regulation (EC) No 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Off J Eur Un L 2006;364/5 20.12.2006. EC. Commission Regulation (EC) No 629/2008 of 2 July 2008 setting maximum levels for certain contaminants in foodstuffs. Off J Eur Un L 2008;173/6 3.7.2008. EFSA. European Food Safety Authority (EFSA). Cadmium in food. EFSA J. 2009;980:1-139 [cited 2009 Dec 12]. Available from:http://www.efsa.europa.eu/cs/BlobServer/ Scientific_Opinion/contam_op_ej980_cadmium_en_rev.1.pdf?ssbinary=true/. Falandysz J. Manganese, copper, zinc, iron, cadmium, mercury and lead in muscle meat, liver and kidneys of poultry, rabbit and sheep slaughtered in the northern part of Poland, 1987. Food Addit Contam 1991;8:70–83. Falandysz J. Some toxic and essential trace metals in cattle from the northern part of Poland. Sci Total Environ 1993;135:177–91. Falandysz J. Some toxic and trace metals in big game hunted in the northern part of Poland in 1987–1991. Sci Total Environ 1994;141:59–73. Falandysz J. Mercury in mushrooms and soil of the Tarnobrzeska Plain, south-eastern Poland. J Environ Sci Health C 2002;37:343–52. Falandysz J. Selenium in edible mushrooms. J Environ Sci Health C 2008;26:256–99. Falandysz J, Bielawski L. Mercury content of wild edible mushrooms collected near the town of Augustow. Pol J Environ Stud 2001;10:67–71. Falandysz J, Bielawski L. Mercury and its bioconcentration factors in Brown Birch Scaber Stalk (Leccinum scabrum) from various sites in Poland. Food Chem 2007;105: 635–40. Falandysz J, Caboń J. Lead in processed big game meat. Med Weter 1990;46:427–8 (in Polish).

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