Eggs as a source of selenium in the human diet

Eggs as a source of selenium in the human diet

Journal of Food Composition and Analysis 78 (2019) 19–23 Contents lists available at ScienceDirect Journal of Food Composition and Analysis journal ...

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Journal of Food Composition and Analysis 78 (2019) 19–23

Contents lists available at ScienceDirect

Journal of Food Composition and Analysis journal homepage: www.elsevier.com/locate/jfca

Original Research Article

Eggs as a source of selenium in the human diet a,⁎

a

T b

a

Bogumiła Pilarczyk , Agnieszka Tomza-Marciniak , Renata Pilarczyk , Jarosław Kuba , Diana Hendzela, Jan Udałaa, Zofia Tarasewiczc a

Department of Animal Reproduction Biotechnology and Environmental Hygiene, West Pomeranian University of Technology, Szczecin, Janickiego 29, 71-270 Szczecin, Poland Department of Ruminant Science, West Pomeranian University of Technology, Szczecin, Janickiego 29, 71-270 Szczecin, Poland c Department of Poultry and Ornamental Bird Breeding, West Pomeranian University of Technology, Szczecin, Janickiego 29, 71-270 Szczecin, Poland b

A R T I C LE I N FO

A B S T R A C T

Keywords: Selenium RDA Avian eggs Turkey Duck Chicken Geese Food analysis Food composition

The aim of this study was to determine the selenium (Se) levels in the eggs of hens, turkeys, ducks and geese. In the investigated eggs, Se concentration was found to depend on bird species, with the highest concentration seen in geese and turkey eggs and the lowest in duck eggs. Se levels in hen eggs depended also on the husbandry system: the highest mean Se concentration being found in cage eggs and the lowest in barn-laid eggs. In all examined bird species, the highest Se concentration was found in the yolk being 3.0–6.7 times higher than in the albumen. One egg can supply 16–48% of Se RDA (Recommended Dietary Allowance), depending on the bird species. Eggs appear to be a valuable source of Se for humans and can play an important role as a functional food.

1. Introduction Selenium (Se) is needed to regulate growth and development in humans and animals. In addition to various other functions, selenium acts as a structural part of selenoproteins, which play a number of crucial structural and enzymatic roles and are of pivotal importance for many metabolic purposes (Gashu et al., 2018; Raygan et al., 2018; Rayman, 2000). The main selenoproteins are glutathione peroxidase, iodothyronine deiodinase, selenoproteins P and W and thioredoxin reductase (Labunskyy et al., 2014; Pappas et al., 2008). One of the many roles played by selenoproteins is the protection of macromolecules and cells against oxidative stress. Various redox-active selenoenzymes demonstrate antioxidant properties: five glutathione peroxidases, three thioredoxin reductases and methionine sulfoxide reductase 2 (Steinbrenner et al., 2016). Selenium is also involved in the metabolism of thyroid hormones (Gashu et al., 2018) and governs a range of processes, including the proper functioning of the immune system by stimulating T cell proliferation, NK cell and macrophage activity and innate immune cell functions (Avery and Hoffmann, 2018; Pilarczyk et al., 2008). Se deficiency in humans has been shown to correlate with an increased risk of some types of cancer and lead to impaired

mineralization of bones and teeth. In addition, cardiomyopathy (Keshan disease) has been observed in people living in areas with low Se levels (Liu et al., 2012; Rayman, 2000; Vinceti et al., 2018). Se intake varies between European countries. Stoffaneller and Morse (2015) report that Eastern European countries tend to have lower Se intake than their western counterparts. Generally, Se intake and status is suboptimal throughout the population of Europe, which can be explained by the low levels of Se in the environment, particularly in Eastern Europe (Brodowska et al., 2016; Stoffaneller and Morse, 2015; Pilarczyk et al., 2010) As Se is usually obtained by humans through the diet, Se intake is typically increased through greater consumption of Se-rich foods, most of which are rich in protein. Eggs are ideal in this regard: they are not only highly nutritious and potent accumulators of Se, but they are also widely available and relatively inexpensive in developed countries. In addition, their consumption is not typically limited by religious or ideological beliefs (Kralik and Kralik, 2017; Miranda et al., 2015; Surai and Sparks, 2001). In eggs, Se is present as both organic and inorganic compounds, with the organic forms predominating (Sun and Feng, 2011). Golubkina and Papazyan (2006) report that selenocysteine is deposited preferentially in the yolk, while selenomethionine is located mostly in the albumen. This was confirmed by Lipiec et al. (2010), who found



Corresponding author. E-mail addresses: Bogumił[email protected] (B. Pilarczyk), [email protected] (A. Tomza-Marciniak), [email protected] (R. Pilarczyk), [email protected] (J. Udała). https://doi.org/10.1016/j.jfca.2019.01.014 Received 2 March 2018; Received in revised form 8 October 2018; Accepted 18 January 2019 Available online 25 January 2019 0889-1575/ © 2019 Elsevier Inc. All rights reserved.

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calcium, 4.0 g of digestible phosphorus, and 0.25 mg of selenium (source: sodium selenate IV). The feed provided 2708 kcal/kg of ME. The ducks were kept in an extensive herding system. Their diet consisted of feed produced onsite and added fodder. Daily feed intake was not balanced and included various grains and steamed potatoes. No light regime was applied for the ducks owing to the extensive character of their aviculture.

selenocysteine to represent, on average, 16% of the total Se content in the albumen and 76% in the yolk, and conversely, selenomethionine to constitute 17% of the total Se in the yolk, and 68%. in the albumen. They also note that both yolk and albumen contained small amounts of selenite (ca. 10% of the total Se concentration per egg). Selenite-selenium is bound by globulin and ovalbumin in the albumen (Magat and Sell, 1979) and by phosvitin in the yolk (Davis and Fear, 1996). Se is laid down in eggs because it is crucial for embryonic growth. Studies indicate that the amount of Se accumulating in eggs varies according to bird species and living conditions. For example, the eggs of free-living birds contain a few times more selenium than the eggs of domestic hens (Nisianakis et al., 2009; Pappas et al., 2006). The aim of the present study was to compare the concentration and distribution of selenium in eggs laid by different species of domestic birds, and to determine the degree to which the eggs satisfy the dietary requirements for Se in humans.

All chemicals used in food analysis were of analytical grade. Most of the chemicals were obtained from Chempur®(Piekary Śląskie, Poland), except 2,3-diaminonaphtalene (DAN), which was obtained from Sigma Aldrich (Saint Luis, Missouri, USA). Certified reference material NIST SRM 8415 (whole egg powder) was obtained from LGC Standards GmbH (Wesel, Germany).

2. Materials and methods

2.3. Chemical analyses

2.1. Materials

The Se concentrations of the eggs were determined using spectrofluorometric methods (Pilarczyk et al., 2010). The yolk, albumen, membrane and shell of all eggs were subjected to chemical analysis. The samples were digested in HNO3 at 230 °C for 180 min and in HClO4 at 310 °C for 20 min. Then, selenate (Se6+) was reduced to selenite (Se4+) using 3 mL of 9% HCl. Selenium content was determined with 2,3 – diaminonaphthalene (DAN) at pH 1–2 by the formation of the selenodiazole complex. This complex was extracted into cyclohexane. EDTA and hydroxylamine hydrochlorine were used as masking agents. The Se concentration was finally determined fluorometrically using a Shimadzu RF–5001 PC spectrofluorophotometer (Shimadzu Corporation, Tokyo, Japan). The excitation wavelength was 376 nm, and the fluorescence emission wavelength was 518 nm. The limit of detection was 0.003 μg/g. The accuracy of the analyses was verified using certified reference material NIST SRM 8415 (whole egg powder). Se concentrations ranged between 87% and 93% of reference values. The precision (RSD%) of the analysis was 2.7%.

2.2. Reagents

The present study examined the Se concentration in the eggs of four species of domestic birds: hens, turkeys, ducks and geese. A total of 298 eggs were examined, comprising 106 hen eggs (64 cage eggs, 40 barn laid eggs and 40 free-range eggs), 60 turkey eggs, 48 goose eggs and 56 duck eggs (24 Peking duck eggs and 32 Muscovy duck eggs). The hens, turkeys and geese were housed in a barn with bedding, while the chickens were kept in cages. The animals were kept in the optimum microclimate conditions needed to provide welfare. Special attention was paid to two environmental factors: lighting and feeding. The birds were kept in three imposed light regimes of 17, 16 and 14 h of diurnal light. In accordance with Polish legislation, permission from the local Ethics Committee is not required if the study is performed based on standard production processes which themselves are in accordance with the provisions concerning the keeping and breeding of livestock (Resolution Number 22/2006 of the National Commission for the Ethics of Experiments on Animals, 7th November 2006Resolution Number 22/ of the National Commission for the Ethics of Experiments on Animals, 2019Resolution Number 22/2006 of the National Commission for the Ethics of Experiments on Animals, 7th November 2006). With regard to nutrition, the hens were fed a basal diet containing triticale grain, maize grain, wheat grain, extracted soybean meal, rapeseed meal, wheat bran, soybean oil, fodder chalk, 1-Ca phosphate, vitamin and mineral supplementation, and phytase. One kilogram of the feed mixture contained 155 g of crude protein, 35.2 g of roughage, 33.9 g of calcium, 4.89 g of digestible phosphorus, 2.02 g of sodium, 6.93 g of lysine, 3.18 g of methionine + cysteine, and 0.2 mg of selenium (source: sodium selenate IV). The feed provided 2842 kcal/kg of ME. During the reproductive period, turkeys were fed a basal diet containing wheat grain, maize grain, extracted soybean meal, fish meal, wheat bran, soybean oil, calcium carbonate, monocalcium phosphate, sodium chloride, sodium carbonate, vitamin and mineral supplementation with micro-elements includingSe, synthetic amino acids (lysine, methionine), enzymes (phytase, beta-xylanase) and natural antioxidants. One kilogram of the feed mixture contained 169.5 g of crude protein, 18.8 g of roughage, 36.1 g of crude fat, 105.6 g of crude ash, 7.8 g of lysine, 3.8 g of methionine, 30.2 g of calcium, 1.7 g of sodium and 0.2 mg of selenium (source: sodium selenate IV). The feed provided 2850 kcal/kg of ME. Goose eggs were obtained from fouryear-old geese. Their basal diet was based on fodder produced in the farm containing wheat grain, barley grain, maize grain, oat grain, extracted soybean meal, rapeseed meal, fodder chalk, rapeseed oil and vitamin/mineral mix. One kilogram of the feed mixture contained 163.2 g of total protein, 50 g of roughage, 97.4 g of crude ash, 7.7 g of lysine, 3.4 g of methionine, 6.7 g of methionine + cysteine, 27.9 g of

2.4. Statistical analysis The results were subjected to statistical analysis using Statistica software (StatSoft Inc., Tulsa, OK, United States, ver. 9.0). All data was expressed throughout as arithmetic mean, standard deviation and geometric mean. The Se concentrations were log-transformed to attain or approach a normal distribution of data. The results were processed statistically by analysis of variance (ANOVA). The significance of the differences between means was determined by Duncan’s test at P < 0.05, P < 0.01 and P < 0.001. Relationships between Se concentrations in the yolk, albumen, shell membranes and shell were evaluated by calculating the Pearson’s correlation coefficient (rx,y). The statistical significance of the correlation coefficients was tested at P < 0.05, P < 0.01 and P < 0.001. 3. Results 3.1. Interspecific differences in Se concentration and distribution in eggs The mean Se concentration varied from 0.124 to 0.416 μg/g in the yolk, from 0.039 to 0.106 μg/g in the albumen, from 0.047 to 0.191 μg/ g in the shell membranes, and from 0.024 to 0.058 μg/g in the shell (Table 1). The total Se concentration in eggs followed the following order: goose eggs (67 μg/100 g) > turkey eggs (63 μg/100 g) > Peking duck eggs (52 μg/100 g) > hen eggs (51 μg/100 g) > Muscovy duck eggs (23 μg/100 g) (Fig. 1). The following order was observed for the Se concentration in the yolk and albumen only: turkey eggs (48 μg/ 100 g) > caged hen eggs (43 μg/100 g) > geese eggs (42 μg/100 g) > free-range hen eggs (38 μg/100 g) > barn laid hen (36 μg/100 g) > 20

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Table 1 Mean concentrations of selenium (μg/g w.w.) in the yolk, albumen, shell membranes and shell of eggs of various poultry species. Type of eggs

n

yolk

albumen

Mean Turkey eggs Goose eggs Free-range chicken eggs Barn laid chicken eggs Caged chicken eggs Peking duck eggs Muscovy duck eggs

60 48 40 40 64 24 32

GM AFbc

0.416 0.314Bb 0.329C 0.305Dc 0.370EG 0.243FGa 0.142ABCDEa

0.399 0.300 0.322 0.300 0.366 0.237 0.141

Sd

shell membranes

Mean

0.126 0.086 0.071 0.060 0.065 0.051 0.017

GM Aa

0.063 0.106ABCDEF 0.045B 0.049C 0.055D 0.061Eb 0.039Fab

0.061 0.101 0.044 0.048 0.053 0.060 0.037

Sd 0.08 0.031 0.010 0.012 0.020 0.010 0.013

Mean

GM a

0.155 0.191A 0.107 0.123 0.117 0.113 0.047Aa

0.147 0.155 0.105 0.116 0.115 0.111 0.045

shell Sd 0.051 0.150 0.025 0.047 0.026 0.018 0.015

Mean Aa

0.033 0.058ABCDE 0.033Bb 0.036Cc 0.049FGabc 0.029DF 0.024EG

GM

Sd

0.031 0.054 0.032 0.035 0.045 0.029 0.024

0.010 0.019 0.009 0.009 0.025 0.006 0.007

GM – geometric mean, Sd- standard deviation. A,B – upper case letters denote statistically significant differences at P < 0.01. a,b – lower case letters denote statistically significant differences at P < 0.05.

(P < 0.01) or turkey eggs (P < 0.05). In the shell, the mean Se concentration was significantly higher in goose eggs (P < 0.01) and caged hen eggs (P < 0.05) than in other analysed species. In all the investigated species, the mean Se concentration was significantly higher in the yolk than either the albumen, shell membranes or shell (P < 0.01). Likewise, the mean Se concentration in the albumen was significantly higher than in either the egg membranes (P < 0.01) (except in Muscovy duck eggs) or the shell (P < 0.05). In the Muscovy duck eggs, the mean Se concentration was significantly (P < 0.01) higher in the shell membranes than in the shell, whereas in other species, no significant difference was found between shell and shell membrane (Table 2).

Fig. 1. Concentration of Se (average ± Sd) in eggs of different bird species, calculated per 100 g and per single egg (based on average egg weight for individual bird species).

3.2. Correlation between Se concentrations in the yolk, albumen, shell membrane and shell

Peking duck eggs (30 μg/100 g) > Muscovy duck eggs (18 μg/100 g). It was found that Se concentration in hen eggs depended on the husbandry system. The highest mean Se concentration was found in cage eggs (- 54 μg/100 g), while the lowest was found in barn-laid eggs (48 μg/100 g). The highest Se concentration was found in the egg yolk for all bird species. The highest mean Se concentration was found in the yolk of turkey eggs, while the lowest was found in Muscovy duck eggs, which was significantly lower than in other species (P < 0.01 and P < 0.05). Regarding husbandry model, the highest Se levels were found in various parts of eggs laid by hens housed in cages; however, the Se levels in shell membranes did not significantly vary between husbandry models (Tables 1 and 2). The mean Se concentration in albumen was significantly (P < 0.01) higher in goose eggs than other analysed species, while Muscovy duck albumen contained significantly lower Se concentrations than goose (P < 0.01), turkey or Peking duck egg albumen (P < 0.05). Interestingly, the Se concentration of the shell membranes was also significantly lower in the Muscovy duck eggs than in the goose

Correlation analysis revealed very high significant positive correlations between Se levels in different egg parts. For turkey eggs, significant positive correlations in Se concentration were found between yolk and albumen (r = 0.79, P < 0.001), yolk and membrane (r = 0.82, P < 0.001), yolk and shell (r = 0.91, P < 0.001), albumen and membrane (r = 0.67, P < 0.01), albumen and shell (r = 0.79, P < 0.001) and finally between membrane and shell (r = 0.69, P ≤ 0.01). Significant positive correlations in Se levels were found between yolk and albumen for goose eggs (r = 0.82, P < 0.001), between albumen and shell membranes in barn-laid hen eggs (r = 0.74, P < 0.05), and between albumen and shell in cage-laid hen eggs (r = 0.96, P < 0.05). In Peking duck eggs, significant positive correlations in Se levels were found between yolk and membrane (r = 0.82, P < 0.05), and between membrane and shell (r = 0.86, P < 0.05); in Muscovy duck eggs, such correlations were found between yolk and shell (r = 0.92, P < 0.001), and between albumen and membrane (r = 0.92, P < 0.001)(Table 3).

Table 2 Significance of differences in mean Se concentrations in the yolk, albumen, shell membranes and shell, and the ratio of Se concentrations between the parts in tested bird species. Type of eggs

Turkey eggs Goose eggs Free-range chicken eggs Barn laid chicken eggs Caged chicken eggs Peking duck eggs Muscovy duck eggs

n

yolk vs albumen

yolk vs shell membranes

yolk vs shell

albumen vs shell membranes

albumen vs shell

shell membranes vs shell

P values

ratio

P values

ratio

P values

ratio

P values

ratio

P values

ratio

P values

ratio

60 48 40

< 0.001 < 0.001 < 0.001

6.6 3.0 7.3

< 0.001 < 0.001 < 0.001

2.7 1.6 3.1

< 0.001 < 0.001 < 0.001

12.6 5.4 10.0

< 0.001 < 0.05 < 0.001

2.5 1.8 2.4

< 0.001 < 0.001 < 0.001

1.9 1.8 1.4

ns ns ns

4.7 3.3 3.2

40 64 24 32

< 0.001 < 0.001 < 0.001 < 0.001

6.2 6.7 4.0 3.6

< 0.001 < 0.001 < 0.001 < 0.001

2.5 3.2 2.2 3.0

< 0.001 < 0.001 < 0.001 < 0.001

8.5 7.6 8.4 5.9

< 0.001 < 0.05 < 0.001 ns

2.5 2.1 1.9 1.2

< 0.001 < 0.001 < 0.001 < 0.05

1.4 1.1 2.1 1.6

ns ns ns < 0.01

3.4 2.4 3.9 2.0

21

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Table 3 Correlation coefficient values between Se concentrations in different parts of the egg in the investigated bird species. Type of eggs Turkey eggs Goose eggs Free-range chicken eggs Barn-laid chicken eggs Caged chicken eggs Peking duck eggs Muscovy duck eggs

n 60 48 40 40 64 24 32

yolk vs albumen ***

0.79 0.82*** ns ns ns ns ns

yolk vs membranes ***

0.82 ns ns ns ns 0.82* ns

yolk vs shell ***

0.91 ns ns ns ns 0.82* 0.92***

albumen vs membranes **

0.67 ns ns 0.74* ns ns 0.92***

albumen vs shell ***

0.79 ns ns ns 0.96* ns ns

membranes vs shell 0.69** ns ns ns ns 0.86* ns

ns - non-significant correlation coefficient. *** Significant correlation coefficient at P ≤ 0.001. ** Significant correlation coefficient at P ≤ 0.01. * Significant correlation coefficient at P ≤ 0.05.

mean content of Se in a single egg is 18 μg, one egg constitutes about 30% of the daily selenium demand for a human. The lowest concentration of selenium was found in duck eggs, which can be accounted for by the extensive herding system and the fact that the daily feed intake was not balanced. In addition, interesting differences in selenium level were found between the two examined duck species: The selenium concentration in Muscovy duck eggs was half that that of Peking duck eggs, even though both duck species were maintained under the same conditions. This situation may be explained with some anatomical differences between the two species: The Muscovy duck has a shorter digestive tract in comparison to the Peking duck; as some organic selenium forms need to be digested before absorption (Delezie et al., 2014), a shorter digestive tract may result in reduced absorbance of Se and thus, a lower transfer of selenium from food to eggs. Like those of other authors (e.g. Golubkina and Papazyan, 2006), our present findings suggest that the two compartments of the egg display significant differences in Se distribution. The efficiency of Se deposition in yolk, albumen or other parts depends on the concentration of Se in the diet, its form, and the methionine content (Surai and Fisinin, 2014). Selenocysteine, similarly to inorganic Se, tends to accumulate in the yolk, while selenomethionine is incorporated mainly in the albumen. Irrespective of the preferred site of accumulation of Se, a positive correlation was found between the Se concentrations in individual egg parts, although this relationship was not significant in all cases (Table 3). This suggests that as the incorporation of Se into the egg increases, the concentration of Se increases in all parts of the egg, even though this growth may be uneven. In all examined bird species, the yolk was found to have higher Se concentrations, and to be a more potent selenium source, than the albumen. Similar findings have been reported by other authors (Golubkina and Papazyan, 2006; Pappas et al., 2005; Paton et al., 2002). Likewise, greater Se accumulation has also been found in the egg yolk in free living species of birds (Pappas et al., 2006). Surai et al. (2004) report Se levels to be low in the shell and high in the shell membrane. Previous studies indicate that the shells of avian eggs contain from 1 to 5% to 12% of the total Se present in the egg (Burger, 1994; Surai et al., 2004). The ratio of Se levels in different egg parts was found to vary depending on the bird species. The mean concentration of Se in the yolk was three to 6.7 times higher than the albumen, from 1.6 to 3.1 times higher than in the egg membranes and from 5.4 to 12.6 times higher than in the shell. The mean Se concentration in the albumen was 1.2 to 2.5 times higher than the egg membranes, and from 1.1 to 1.9 times higher than in the shell. The mean Se concentration in egg membranes was between two and 4.7 times higher than in the shell. The mean Se concentration in the yolk of turkey eggs was almost seven times higher than in the albumen, almost three times higher than in the egg membranes and over 12 times higher than in the shell. In goose eggs, the ratio was smaller, with the concentration in the yolk being three times

Fig. 2. Percentage share of total Recommended Daily Allowance of selenium supplied by the yolk and albumen per egg in the tested eggs obtained from different bird species.

3.3. Assessment of supply of Se demand by eggs from different species of domestic birds Assuming that the recommended daily allowance (RDA) of Se for an adult person is 55 μg, the eggs examined in the present study can supply 16–48% of that RDA per egg, depending on the species (Fig. 2); goose and turkey eggs provide respectively 48 and 43%. Regarding the share of yolk and albumen, the yolk of a goose, Peking duck or hen egg provides more than 80% of the total Se dose, taken with one egg. 4. Discussion Eggs are regarded as one of the most valuable food products. They have been treated as a source of bioactive compounds for many years, and thanks to their multifunctional properties, eggs are now considered to be a very important component of the diet (Sparks, 2006). Our findings indicate that domestic bird eggs contain large amounts of Se and hence, their consumption can be regarded as a valuable source of Se in the human diet, even more so because the selenium present in eggs is in the form of well-absorbed chemical compounds (Golubkina and Papazyan, 2006; Sun and Feng, 2011). The highest levels of Se were present in goose and turkey eggs, at more than 0.6 μg/ g, but in many countries, consumption of these eggs is much lower than hen eggs. The mean Se concentration in hen eggs was found to be 0.51 μg/g; this figure is higher than those reported previously in Scotland (0.066 to 0.210 μg/g; Zagrodzki, 2000), Croatia (0.177 μg/g; Klapec et al., 2004), France (0.15 μg/g; Paton et al., 2002) and Greece (0.087 μg/g; Baratakos et al., 1987). Higher concentrations have only been found in Germany, where the Se concentration was 0.863 μg/g (Zagrodzki, 2000). However, Kralik et al. (2009) report a higher selenium concentration (i.e. more than 0.7 μg/g) in the eggs of hens fed a similar diet to those in the present study, with a basal diet containing 0.2 mg Se. As the recommended dietary allowance (RDA) for Se is 55 μg (IMFNB, Institute of Medicine, Food and Nutrition Board, 2000) and the 22

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greater than in the albumen, almost two times higher than in membranes and over five times higher than in the shell. In a study of hen eggs, Golubkina and Papazyan (2006) found the albumen to contain roughly one quarter of the total Se content, and that the Se occurred in the following descending order: yolk > chalazae > internal viscous albumen > external liquid egg white. Our findings identify differences in Se concentration are present between eggs laid by different species of domestic birds. In general it is said that the content of Se in eggs depends on the Se content in the diet; However, our results suggest that probably that the type of husbandry, and probably some anatomical and metabolic differences, can also influence the amount of Se absorbed from the food and transferred later to eggs. Eggs appear to be a valuable source of Se for humans. They not only have high nutritional value and high selenium content, but the Se is typically incorporated into well-absorbed chemical compounds. They can therefore play an important role as a functional food.

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