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Selenium enrichment of table eggs
Selenium enrichment of table eggs D. C. Bennett1 and K. M. Cheng Avian Research Centre, Faculty of Land and Food Systems, University of British Columbia, 2357 Main Mall, Vancouver, British Columbia, Canada, V6T 1Z4 Rock, Lohmann Brown, Lohmann White) a basal diet containing 0.3 μg of Se/g of diet as Na2SeO3. Into this diet, Se yeast (SelenoSource AF 600), an organic source of Se, was added at 1.0, 2.4, or 5.1 μg of Se/g of diet for 4 wk. Feed consumption, egg production, and egg mass were not affected by the dietary Se concentration in all 3 breeds. Within the range of Se levels employed in the laying hens’ diet, egg Se content increased linearly as dietary levels of Se increased. The results of this study indicate that feeding up to 5.1 μg/g of Se will not affect egg production and the welfare of the laying hen and is a practical way of producing Se-enriched eggs for the consumers.
Key words: selenium, laying hen, enriched egg 2010 Poultry Science 89:2166–2172 doi:10.3382/ps.2009-00571
INTRODUCTION Selenium is an essential trace element that is indispensable for normal functioning of the body and thus plays a critical role in the maintenance of optimal health. Currently, the US and Canadian recommended dietary allowance (RDA) for human adults is 55 μg/d (Institute of Medicine, 2000). This recommendation is based on the amount of dietary Se required to maximize the activity of plasma glutathione peroxidase. However, there is evidence that greater dietary Se intakes in the range of 100 to 300 μg/d may have possible health benefits (Finley, 2007; Fisinin et al., 2009; Schrauzer, 2009; Schrauzer and Surai, 2009). Schrauzer (2009) suggested that the optimal Se intake for adults is in the range of 250 to 300 μg/d, which would require increasing the Se intake by 100 to 200 μg/d for most North American diets. This increased Se intake could be achieved either through supplementation or through the consumption of Se-enriched foods. It should be noted that although Se is an essential nutrient, excess Se intake can have toxic effects. However, the optimal Se intake proposed ©2010 Poultry Science Association Inc. Received November 20, 2009. Accepted June 27, 2010. 1 Corresponding author: [email protected]
by Schrauzer (2009) is lower than the no adverse effect level of 800 μg/d proposed for Canada and the United States (Institute of Medicine, 2000). Several studies have examined the potential for enriching the Se content of various dietary items, including eggs. In fact, eggs have been shown to be an effective vehicle for supplementing Se in the diet (Surai et al., 2007). The Se content of eggs is easily manipulated when hens are fed with organic forms of Se (i.e., selenomethionine). Selenium-enriched eggs have been shown to be a good source of Se for humans (Surai et al., 2007). Furthermore, eggs are a traditional and affordable food in many countries and cultures; thus, Se-enriched eggs should be really acceptable. Most studies examining the Se enrichment of eggs have fed hens diets only containing 0.3 to 0.5 μg of Se/g of diet, the current legal limit in most jurisdictions. Hens fed organic sources of Se at these levels produce eggs containing 10 to 29 μg of Se, or 18 to 53% of the US and Canadian RDA (Moksnes, 1983; Paton et al., 2002; Payne et al., 2005; Chantiratikul et al., 2008). With regard to the suggestion of Schrauzer (2009) that adult humans should consume approximately 250 to 300 μg of Se/d, in order for a person to obtain an additional 100 to 200 μg of dietary Se/d, 2 eggs containing 50 to 100 μg of Se each would need to be consumed. This would necessitate feeding hens a diet containing
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ABSTRACT Selenium is an essential trace element with a recommended dietary allowance for human adults of 55 μg/d. However, there is evidence that greater dietary intakes may have possible health benefits, including a reduction in the risk of cancer. Several studies have shown the feasibility of enriching eggs using organic Se and that Se-enriched eggs are an effective way to supplement human diets. However, few studies have examined the response of egg Se concentration to high (>1 μg/g) dietary organic Se intake by the laying hens. The objective of the current study is to examine the effect of higher dietary organic Se levels on production, egg mass, and egg Se levels. These were assessed by feeding 3 breeds of laying hens (Barred Plymouth
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SELENIUM ENRICHMENT OF TABLE EGGS
MATERIALS AND METHODS Birds and Experimental Procedures Hens were maintained in accordance with the guidelines of the Canadian Council on Animal Care. All procedures were approved by the animal care committees of the Agassiz Research Centre (Agriculture and AgriFood Canada) and the University of British Columbia (A07-0039). One hundred fifty-two 60-wk-old laying hens of 3 breeds [48 Barred Plymouth Rocks (BR), 49 Lohmann Browns (LB), and 55 Lohmann Whites (Lohmann Selected Longhorn Lites; LW)] were used in this experiment. Barred Plymouth Rocks were chosen to represent a noncommercial heritage breed, whereas the LB and LW are commercial brown and white egg layers, respectively. Hens were housed either 2 or 3 birds per cage (mean = 2.5 ± 0.1 birds per cage, or 906 ± 50 cm2/ hen) for a total of 20 cages per breed. All hens were initially fed a commercial wheat-soybean meal-canola meal-based layer ration ad libitum [Unifeed (Viterra Inc.), Chilliwack, British Columbia, Canada]. This diet was formulated to meet NRC (1994) recommendations and contained 0.3 μg of Se/g of diet as inorganic Na2SeO3 (see Table 1 for nutrient analysis). Into this diet, Se yeast (SelenoSource AF 600, Diamond V Mills, Cedar Rapids, IA) was added at 1.0, 2.4, or 5.1 μg of Se/g of diet without substitution (see Table 2 for the Se content and source for these diets). These 3 experimental diets were fed to 6, 7, and 7 cages of hens from each breed, respectively, for 4 wk. Total feed intake for each cage was measured weekly. At the end of the experimental period (d 24 to 25), excreta output was measured for 4 cages of LB on each of the 3 experimental diets. All excreta produced from each cage in the 24-h period were individually collected, dried at 60°C, weighed, and stored until analyzed for Se content.
Table 1. Nutrient composition of base
(as-fed basis)
Item
Amount
Moisture (%) Protein (%) Fat (%) Carbohydrates (%) Ash (%) Se2 (μg/g) Energy Gross energy, analyzed (kcal/kg) AME, calculated (kcal/kg)
10.8 16.7 3.8 55.0 13.8 0.313 3,220 2,800
1Commercial layer ration supplied by Unifeed (Viterra Inc.), Chilliwack, British Columbia, Canada. Proximate analysis of diet determined according to AOAC official methods (AOAC, 2000). 2Selenium supplied as Na SeO . 2 3 3Analyzed value.
Hen-day egg production was measured throughout the experiment. All eggs laid at the start of the experiment (presupplementation) and on d 3, 10, 17, and 25 of the experiment were collected and stored at 5°C until processed. Eggs were individually weighed and broken out. The shell and shell membrane were dried, weighed, and then discarded. The yolk and albumen were weighed together and eggs collected from the same cage were pooled, homogenized with a Polytron homogenizer (Brinkman Instruments, Westbury, NY), and stored at −20°C until analyzed for Se content. Samples of diets, excreta, and eggs were digested according to AOAC official method 986.15 (AOAC, 2000), as outlined in Lambert and Turoczy (2000). This method was chosen because facilities for using perchloric acid digestion were not available. Briefly, a 200- to 300-mg sample was weighed into a Teflon closed digestion vessel (Parr Instrument Company, Moline, IL), and 5 mL of concentrated HNO3 and 2 antibumping granules were added. The digestion vessel was sealed, and the sample was allowed to predigest for 18 h at room temperature. The digestion vessel was heated at 150°C for 2 h in a muffle furnace. After cooling, the digest was transferred to a 50-mL crucible and 1 mL of 75 mg/mL of magnesium nitrate solution was added. This mixture was dried slowly (2 to 3 h) on a hot plate and then ashed at 500°C for 30 min in a muffle furnace. After cooling, the residue was dissolved in 10 mL of concentrated HCl and heated on a steam bath for 15 min. After cooling, the solution was transferred to a Table 2. Selenium content of experimental diets (as-fed basis) Se content (μg of Se/g of diet) Diet
Na2SeO3
Se yeast1
Total2
Basal 1 2 3
0.31 0.31 0.31 0.31
0.00 1.03 2.38 5.12
0.31 1.34 2.69 5.43
1SelenoSource AF 600 (Diamond V Mills, Cedar Rapids, IA) containing 600 µg of Se/g of yeast. 2Total Se content of the diets was determined by analysis.
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over 1 μg of Se/g of diet (Moksnes, 1983; Payne et al., 2005; Vukasinovic et al., 2006; Chantiratikul et al., 2008). However, given the relatively few studies conducted employing these dietary levels and the apparent interstudy variability in egg Se, further work is needed to better describe the response of egg Se content to high dietary Se intake. The purpose of our current study is to describe the relationship between dietary Se and egg Se to determine the dietary Se requirement of hens needed to produce eggs containing high levels of Se. To achieve this, we conducted a feeding trial in which the egg Se content of 3 breeds of laying hens, each supplemented with 3 high levels of dietary Se, were measured. It should be noted that levels as high as 3 to 6 μg of organic Se/g diet are not toxic to the hen and have no effect on egg production (Moksnes, 1983; Payne et al., 2005; Chantiratikul et al., 2008). The secondary objective of the current study is to examine the effect of higher dietary organic Se levels on feed intake, egg mass, and egg production.
diet1
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Bennett and Cheng Table 3. Feed intake and egg production of the 3 breeds of laying hens used in this study Breed Parameter Feed intake (g/hen per d) Hen-day egg production (%) Weight (g/egg) Whole egg Eggshell Yolk + albumen
Barred Plymouth Rock 4.6B 4.0B
105.6 ± 63.9 ± 61.2 ± 0.9AB 5.1 ± 0.1C 56.1 ± 0.9A
Lohmann Brown 6.7A 2.7A
129.7 ± 86.2 ± 61.9 ± 0.9A 6.0 ± 0.1A 55.9 ± 0.9A
Lohmann White 112.8 ± 2.5B 87.7 ± 1.9A 58.4 ± 0.7B 5.5 ± 0.1B 52.9 ± 0.6B
A–CWithin-breed means within each row (parameter) with common superscripts are not significantly different (P < 0.05). None of these parameters were affected by dietary Se levels. Each within-breed mean is the average of 80 observations (20 cages, 4 wk).
Calculations and Statistical Analyses Egg production, feed consumption, and egg Se concentrations ([SE]egg) were analyzed by repeated measures 2-way ANOVA with breed and dietary Se as main effects. Excreta Se concentration and apparent Se absorption of the LB hens were analyzed by 1-way ANOVA with dietary Se as the main effect. When main effects were significant, differences were assessed by least significance difference test. The relationships between the dietary Se concentration ([SE]diet) and [SE]egg or total egg Se were determined by linear regression. Data are reported as means ± SEM. All statistical analyses were performed using JMP statistical software (version 7, SAS Institute Inc., Cary, NC) and significance was accepted when P < 0.05.
RESULTS Lohmann Browns had significantly higher feed intake than LW and BR (Table 3), but [SE]diet had no significant effect on feed intake. There was no significant diet × breed interaction. Egg production and egg weight were not significantly affected by the [SE]diet but did vary significantly among breeds (Table 3). Initial [SE]egg did not vary significantly among the dietary treatments in any of the breeds (diet × breed interaction, P < 0.56). When hens were fed the Sesupplemented diets, [SE]egg increased rapidly over the first 10 d (P < 0.001) but continued to increase over the last 2 wk (P < 0.001; Figure 1). By d 25, [Se]egg varied significantly both among dietary treatments and among breeds (diet × breed interaction, P < 0.002); there were no breed differences at each of the 2 lower [Se]diet, but at the highest [Se]diet, [Se]egg was significantly greater in the BR than in either of the 2 commercial breeds. Total egg Se followed the same response
pattern as [Se]egg (Figure 1). Overall, both [Se]egg and total egg Se were significantly related to [Se]diet and to daily Se intake (Figure 2). As [Se]diet increased, excreta Se concentration also increased and consequently so did the total amount of Se excreted (Table 4). However, the apparent Se absorption did not differ significantly between diets (mean = 70.2 ± 2.1%).
DISCUSSION There is evidence that a dietary Se intake greater than the RDA may have possible health benefits (Schrauzer, 2009). Although eggs have been shown to be an effective vehicle for supplementing Se in the diet (Surai et al., 2007), relatively few studies have fed hens diets containing enough Se to produce eggs at these levels. Furthermore, the response of egg Se levels to high dietary Se has been variable (Moksnes, 1983; Payne et al., 2005; Na et al., 2006; Vukasinovic et al., 2006; Chantiratikul et al., 2008).
Egg Se Levels The [Se]egg due to the organic Se supplement in our study were in agreement with those previously reported in other studies (Moksnes, 1983; Payne et al., 2005; Na et al., 2006; Vukasinovic et al., 2006; Chantiratikul et al., 2008). We found that both [Se]egg and total egg Se were linearly related to [SE]diet and intake (Figure 2). This result is not surprising given that organic forms of Se, such as selenomethionine (the major form of Se in yeast Se products; Rayman, 2004), are absorbed by active transport and are nonspecifically incorporated into proteins in place of methionine (Schrauzer, 2003). In contrast, inorganic Se sources, such as Na2SeO3, are passively absorbed into the body and typically have lower rates of absorption. The current RDA of Se for human adults in the United States and Canada is 55 μg/d (Institute of Medicine, 2000). Based on the results of this study, hens would require a diet containing 1.4 μg of organic Se/g to produce an egg containing 55 μg of Se (Figure 2). Given that most North American adults have a Se in-
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volumetric flask and diluted to volume with distilled water. The Se concentrations of the digests were then determined using hydride generation atomic fluorescence spectroscopy (Millennium Excalibur PSA Model 10.055, PS Analytical Ltd., Kent, UK), as outlined in Pappas et al. (2006).
SELENIUM ENRICHMENT OF TABLE EGGS
table egg layers (Table 3). This implies that when hens with lower rates of egg production are fed high levels of dietary Se, they may be able to build greater body stores of Se (selenomethionine) that, when mobilized, would allow for the production of eggs with a higher Se content. This may have important implications for breed selection if Se-enriched eggs are to be produced commercially. For example, many niche market producers use heritage breeds, which have lower egg production rates.
Apparent Se Absorption Few studies have examined the apparent absorption of dietary organic Se by laying hens (Latshaw and Osman, 1975; Dobrzański and Jamroz, 2003; Richter et al., 2006). Therefore, as part of this study, we conducted a balance study using LB hens. Although the total amount of Se excreted increased as [Se]diet increased, apparent Se absorption did not differ significantly between diets and averaged 70%. This value is somewhat higher than the 60 to 65% apparent absorption previously reported (Latshaw and Osman, 1975; Dobrzański and Jamroz, 2003; Richter et al., 2006). Together, these results indicate that 30 to 40% of the ingested Se is excreted. Thus, future work should be undertaken to address potential environmental concerns associated with feeding high levels of dietary Se to laying hens over a full production cycle.
Figure 1. Time course of the effect of dietary Se on egg Se concentration ([Se]egg, upper panels) and total egg Se content (lower panels) in 3 breeds of laying hens. Base diet contained 0.3 μg of Se/g as inorganic Na2SeO3, which was supplemented with Se yeast at 1.0 (○), 2.4 (Δ), or 5.1 (□) mg of Se/kg of diet (see Table 2).
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take greater than this RDA (Combs, 2001), producing Se-enriched eggs to meet this level is unwarranted. However, in other regions of the world where there is inadequate Se intake (e.g., parts of China, Europe, and New Zealand), this target may be a desirable goal. There is evidence that a Se intake greater than the RDA may have possible health benefits (Finley, 2007; Fisinin et al., 2009; Schrauzer, 2009; Schrauzer and Surai, 2009). Based on this evidence, Schrauzer (2009) suggests that the optimal Se intake for human adults is in the range of 250 to 300 μg/d. Assuming that the average North American adult has a Se intake of 100 to 200 μg/d (Combs, 2001), this would require increasing the Se intake by 50 to 200 μg/d. To produce an egg containing 50, 100, or 200 μg of Se would necessitate feeding hens diets containing 1.3, 2.8, or 5.7 μg of Se/g, respectively (Figure 2). It should be noted that these dietary levels are all greater than the current legal limit for Se supplementation of livestock feeds in Canada and the United States (0.3 μg of Se/g of diet). As stated above, [Se]egg and total egg Se were significantly related to daily Se intake (Figure 2). However, this response was variable among hens fed the highest level of Se. Although BR hens had a lower feed intake (Table 3), and hence Se intake, they produced eggs that had a higher Se content than in either of the 2 commercial breeds (but only when hens were fed the highest level of Se yeast) (Figures 1 and 2). The BR hens have a lower rate of egg production than commercial
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Bennett and Cheng Table 4. Apparent Se absorption of Lohmann Brown laying hens used in this study Diet Parameter Feed Se content (µg/g) Feed intake (g/hen per d) Se intake (µg/hen per d) Excreta Output (g of DM/hen per d) Se content (µg/g) Se output (µg/g) Apparent Se absorption (%)
1
2
3
1.34 114.1 ± 11.7A 152.8 ± 15.7C 25.4 ± 1.4A 2.0 ± 0.1C 52.0 ± 3.2B 65.4 ± 2.8A
2.69 108.4 ± 3.6A 291.7 ± 9.6B 24.2 ± 1.7A 3.5 ± 0.1B 84.8 ± 4.5B 70.8 ± 2.1A
5.43 109.7 ± 3.8A 580.5 ± 6.1A 24.9 ± 3.6A 5.9 ± 0.4A 149.3 ± 27.7A 74.4 ± 4.6A
Figure 2. Relationships between egg Se content [egg Se concentration ([Se]egg) or total egg Se] and dietary Se concentration ([Se]diet) or total Se intake in 3 breeds of laying hens [Barred Plymouth Rock (Δ), Lohmann Brown (□), and Lohmann White (○)] after 4 wk of supplementation. Base diet contained 0.3 μg of Se/g as inorganic Na2SeO3, which was supplemented with Se yeast at 1.0, 2.4, or 5.1 mg of Se/kg of diet (see Table 2). Initial presupplement values are included.
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A–CMeans within each row (parameter) with common superscripts are not significantly different (P < 0.05). Each mean is the average of 4 observations.
SELENIUM ENRICHMENT OF TABLE EGGS
Effect of High Dietary Organic Se Levels on Production The high dietary Se levels used in this study did not affect feed intake, egg production, or egg weight, which is in agreement with previous studies (Moksnes, 1983; Paton et al., 2002; Payne et al., 2005; Na et al., 2006; Vukasinovic et al., 2006; Chantiratikul et al. 2008). This lack of an effect on production indicates that high dietary levels of organic Se do not negatively affect the welfare of the hen.
The maximum tolerable dietary level of Se for poultry is currently set at 3 µg/g (NRC, 2005). This level was determined based on the observations that the threshold level of dietary Se for decreased egg hatchability and chick growth occurs at 5 µg/g. However, no signs of toxicity were observed in the laying hens used in this study or in those used in previous studies that fed hens high levels (3 to 6 µg/g) of organic Se (Moksnes, 1983; Payne et al., 2005; Vukasinovic et al., 2006; Chantiratikul et al., 2008). Dietary Se levels of 5 to 6 µg/g have no effect on body mass, feed intake, or egg production of laying hens when either organic (Moksnes, 1983; Table 2) or inorganic (Ort and Latshaw, 1978; Moksnes and Norheim, 1982) sources of Se are used. The threshold for decreased egg production and egg weight is 8 to 9 µg of Se/g of diet (Arnold et al., 1973; Ort and Latshaw, 1978). The levels of organic Se proposed to be fed to hens in this study (1.3 to 5.7 µg/g) are below these levels. All Se studies except those of Moksnes and Norheim (1982) and Moksnes (1983) lasted 4 to 6 wk. The 2 studies fed hens Se for 18 wk. Future research should be directed at longer term feeding trials to establish the safe dietary limits for organic Se consumption in hens if Se-enriched eggs are to be produced commercially.
Conclusions In this study, we assessed the response of egg Se levels to high dietary levels of organic Se to determine the dietary Se requirement of hens needed to produce Se-enriched table eggs. The results of this study indicate that within the range of Se levels that we fed to the hens, egg Se levels are linearly related to dietary organic Se levels. This and previous studies have not found any evidence of toxicity from organic Se to laying hens, even at levels as high as 3 to 6 μg of organic Se/g of diet. Future research should be directed at establishing the safe dietary limits for organic Se consumption in hens if Se-enriched eggs are to be produced commercially.
ACKNOWLEDGMENTS This research was supported by funds from the British Columbia Ministry of Agriculture and Lands, administered by the UBC Speciality Bird Research Committee. We thank Ilkyu Yoon, Diamond V Mills, for the Se yeast; Eduardo Jovel, Les Lavkulich and Gilles Galzi, Faculty of Land and Food Systems, University of British Columbia, for discussions on selenium analysis and use of equipment; Lisa Hedderson and Lee Struthers, AAFC Agassiz Poultry Research Centre, for technical assistance; and Fred Silversides, AAFC Agassiz Poultry Research Centre, Stewart Paulson, British Columbia Ministry of Agriculture and Lands, and Jennifer Arthur, Avian Research Centre, University of British Columbia, for valuable inputs.
REFERENCES AOAC. 2000. Official Methods of Analysis. AOAC Interational, Arlington, VA. Arnold, R. L., O. E. Olson, and C. W. Carlson. 1973. Dietary selenium and arsenic additions and their effects on tissue and egg selenium. Poult. Sci. 52:847–854. Chantiratikul, A., O. Chinrasri, and P. Chantiratikul. 2008. Effect of sodium selenite and zinc-l-selenomethionine on performance and selenium concentration in eggs of laying hens. Asian-australas. J. Anim. Sci. 21:1048–1052. Combs, G. F. Jr. 2001. Selenium in global food systems. Br. J. Nutr. 85:517–547. Dobrzański, Z., and D. Jamroz. 2003. Bioavailability of selenium and zinc supplied to the feed for laying hens in organic and inorganic form. http://www.ejpau.media.pl/volume6/issue2/animal/art03.html Accessed Jul. 9, 2010. Finley, J. W. 2007. Increased intakes of selenium-enriched foods may benefit human health. J. Sci. Food Agric. 87:1620–1627. Fisinin, V. I., T. T. Papazyan, and P. F. Surai. 2009. Producing selenium-enriched eggs and meat to improve the selenium status of the general population. Crit. Rev. Biotechnol. 29:18–28. Institute of Medicine. 2000. Dietary Reference Intakes for Vitamin C, Vitamin E, Selenium and Carotenoids. National Academy Press, Washington, DC. Lambert, D. F., and N. J. Turoczy. 2000. Comparison of digestion methods for the determination of selenium in fish tissue by cathodic stripping voltammetry. Anal. Chim. Acta 408:97–102. Latshaw, J. D., and M. Osman. 1975. Distribution of selenium in egg white and yolk after feeding natural and synthetic selenium compounds. Poult. Sci. 54:1244–1252. Moksnes, K. 1983. Selenium deposition in tissues and eggs of laying hens given surplus of selenium as selenomethionine. Acta Vet. Scand. 24:34–44. Moksnes, K., and G. Norheim. 1982. Selenium concentrations in tissues and eggs of growing and laying chickens fed sodium selenite at different levels. Acta Vet. Scand. 23:368–379. Na, J. C., S. H. Kim, D. B. Jang, J. H. Kim, D. J. Yu, G. H. Kang, H. K. Kim, D. S. Lee, S. J. Lee, J. C. Lee, and W. J. Lee. 2006. Effects of dietary organic selenium levels on performance and selenium retention in broiler chickens and laying hens. Korean J. Poult. Sci. 33:255–262. NRC. 1994. Nutrient Requirements of Poultry. 9th rev. ed. National Academy Press, Washington DC. NRC. 2005. Mineral Tolerance of Animals. 2nd rev. ed. National Academy Press, Washington, DC. Ort, J. F., and J. D. Latshaw. 1978. The toxic level of sodium selenite in the diet of laying chickens. J. Nutr. 108:1114–1120. Pappas, A. C., F. Karadas, P. F. Surai, N. A. R. Wood, P. Casey, G. R. Bortolotti, and B. K. Speake. 2006. Interspecies variation in
Downloaded from http://ps.oxfordjournals.org/ at EKU Libraries,SerialsEastern Kentucky University on May 25, 2015
Toxic Effect of High Dietary Organic Se Levels
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Bennett and Cheng Schrauzer, G. N. 2009. Selenium and selenium-antagonistic elements in nutritional cancer prevention. Crit. Rev. Biotechnol. 29:10– 17. Schrauzer, G. N., and P. F. Surai. 2009. Selenium in human and animal nutrition: Resolved and unresolved issues. A partly historical treatise in commemoration of the fiftieth anniversary of the discovery of the biological essentiality of selenium, dedicated to the memory of Klaus Schwarz (1914–1978) on the occasion of the thirtieth anniversary of his death. Crit. Rev. Biotechnol. 29:2–9. Surai, P. F., T. T. Papazyan, B. K. Speake, and N. H. C. Sparks. 2007. Enrichment in selenium and other trace elements. Pages 183–190 in Bioactive Egg Compounds. R. Huopalahti, R. LopezFandinño, and M. Anton, R. Schade, ed. Springer-Verlag Berlin, Germany. Vukasinovic, M., R. Mihailovic, M. Sekler, V. Kaljevic, and V. Kurcubic. 2006. The impact of the selenium content of laying hen feeds. Arch. Geflügelkd. 70:91–96.
Downloaded from http://ps.oxfordjournals.org/ at EKU Libraries,SerialsEastern Kentucky University on May 25, 2015
yolk selenium concentrations among eggs of free-living birds: The effect of phylogeny. J. Trace Elem. Med. Biol. 20:155–160. Paton, N. D., A. H. Cantor, A. J. Pescatore, and C. A. Smith. 2002. The effect of dietary selenium source and level on the uptake of selenium by developing chick embryos. Poult. Sci. 81:1548– 1554. Payne, R. L., T. K. Lavergne, and L. L. Southern. 2005. Effect of inorganic versus organic selenium on hen production and egg selenium concentration. Poult. Sci. 84:232–237. Rayman, M. P. 2004. The use of high-selenium yeast to raise selenium status: How does it measure up? Br. J. Nutr. 92:557–573. Richter, G., M. Leiterer, R. Kirmse, W. I. Ochrimenko, and W. Arnhold. 2006. Comparative investigation of dietary supplements of organic and inorganic bounded selenium in laying hens. Tierarztl. Umsch. 61:155–161. Schrauzer, G. N. 2003. The nutritional significance, metabolism and toxicology of selenomethionine. Adv. Food Nutr. Res. 47:73– 112.
Key words: selenium, laying hen, enriched egg 2010 Poultry Science 89:2166–2172 doi:10.3382/ps.2009-00571
INTRODUCTION Selenium is an essential trace element that is indispensable for normal functioning of the body and thus plays a critical role in the maintenance of optimal health. Currently, the US and Canadian recommended dietary allowance (RDA) for human adults is 55 μg/d (Institute of Medicine, 2000). This recommendation is based on the amount of dietary Se required to maximize the activity of plasma glutathione peroxidase. However, there is evidence that greater dietary Se intakes in the range of 100 to 300 μg/d may have possible health benefits (Finley, 2007; Fisinin et al., 2009; Schrauzer, 2009; Schrauzer and Surai, 2009). Schrauzer (2009) suggested that the optimal Se intake for adults is in the range of 250 to 300 μg/d, which would require increasing the Se intake by 100 to 200 μg/d for most North American diets. This increased Se intake could be achieved either through supplementation or through the consumption of Se-enriched foods. It should be noted that although Se is an essential nutrient, excess Se intake can have toxic effects. However, the optimal Se intake proposed ©2010 Poultry Science Association Inc. Received November 20, 2009. Accepted June 27, 2010. 1 Corresponding author: [email protected]
by Schrauzer (2009) is lower than the no adverse effect level of 800 μg/d proposed for Canada and the United States (Institute of Medicine, 2000). Several studies have examined the potential for enriching the Se content of various dietary items, including eggs. In fact, eggs have been shown to be an effective vehicle for supplementing Se in the diet (Surai et al., 2007). The Se content of eggs is easily manipulated when hens are fed with organic forms of Se (i.e., selenomethionine). Selenium-enriched eggs have been shown to be a good source of Se for humans (Surai et al., 2007). Furthermore, eggs are a traditional and affordable food in many countries and cultures; thus, Se-enriched eggs should be really acceptable. Most studies examining the Se enrichment of eggs have fed hens diets only containing 0.3 to 0.5 μg of Se/g of diet, the current legal limit in most jurisdictions. Hens fed organic sources of Se at these levels produce eggs containing 10 to 29 μg of Se, or 18 to 53% of the US and Canadian RDA (Moksnes, 1983; Paton et al., 2002; Payne et al., 2005; Chantiratikul et al., 2008). With regard to the suggestion of Schrauzer (2009) that adult humans should consume approximately 250 to 300 μg of Se/d, in order for a person to obtain an additional 100 to 200 μg of dietary Se/d, 2 eggs containing 50 to 100 μg of Se each would need to be consumed. This would necessitate feeding hens a diet containing
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ABSTRACT Selenium is an essential trace element with a recommended dietary allowance for human adults of 55 μg/d. However, there is evidence that greater dietary intakes may have possible health benefits, including a reduction in the risk of cancer. Several studies have shown the feasibility of enriching eggs using organic Se and that Se-enriched eggs are an effective way to supplement human diets. However, few studies have examined the response of egg Se concentration to high (>1 μg/g) dietary organic Se intake by the laying hens. The objective of the current study is to examine the effect of higher dietary organic Se levels on production, egg mass, and egg Se levels. These were assessed by feeding 3 breeds of laying hens (Barred Plymouth
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SELENIUM ENRICHMENT OF TABLE EGGS
MATERIALS AND METHODS Birds and Experimental Procedures Hens were maintained in accordance with the guidelines of the Canadian Council on Animal Care. All procedures were approved by the animal care committees of the Agassiz Research Centre (Agriculture and AgriFood Canada) and the University of British Columbia (A07-0039). One hundred fifty-two 60-wk-old laying hens of 3 breeds [48 Barred Plymouth Rocks (BR), 49 Lohmann Browns (LB), and 55 Lohmann Whites (Lohmann Selected Longhorn Lites; LW)] were used in this experiment. Barred Plymouth Rocks were chosen to represent a noncommercial heritage breed, whereas the LB and LW are commercial brown and white egg layers, respectively. Hens were housed either 2 or 3 birds per cage (mean = 2.5 ± 0.1 birds per cage, or 906 ± 50 cm2/ hen) for a total of 20 cages per breed. All hens were initially fed a commercial wheat-soybean meal-canola meal-based layer ration ad libitum [Unifeed (Viterra Inc.), Chilliwack, British Columbia, Canada]. This diet was formulated to meet NRC (1994) recommendations and contained 0.3 μg of Se/g of diet as inorganic Na2SeO3 (see Table 1 for nutrient analysis). Into this diet, Se yeast (SelenoSource AF 600, Diamond V Mills, Cedar Rapids, IA) was added at 1.0, 2.4, or 5.1 μg of Se/g of diet without substitution (see Table 2 for the Se content and source for these diets). These 3 experimental diets were fed to 6, 7, and 7 cages of hens from each breed, respectively, for 4 wk. Total feed intake for each cage was measured weekly. At the end of the experimental period (d 24 to 25), excreta output was measured for 4 cages of LB on each of the 3 experimental diets. All excreta produced from each cage in the 24-h period were individually collected, dried at 60°C, weighed, and stored until analyzed for Se content.
Table 1. Nutrient composition of base
(as-fed basis)
Item
Amount
Moisture (%) Protein (%) Fat (%) Carbohydrates (%) Ash (%) Se2 (μg/g) Energy Gross energy, analyzed (kcal/kg) AME, calculated (kcal/kg)
10.8 16.7 3.8 55.0 13.8 0.313 3,220 2,800
1Commercial layer ration supplied by Unifeed (Viterra Inc.), Chilliwack, British Columbia, Canada. Proximate analysis of diet determined according to AOAC official methods (AOAC, 2000). 2Selenium supplied as Na SeO . 2 3 3Analyzed value.
Hen-day egg production was measured throughout the experiment. All eggs laid at the start of the experiment (presupplementation) and on d 3, 10, 17, and 25 of the experiment were collected and stored at 5°C until processed. Eggs were individually weighed and broken out. The shell and shell membrane were dried, weighed, and then discarded. The yolk and albumen were weighed together and eggs collected from the same cage were pooled, homogenized with a Polytron homogenizer (Brinkman Instruments, Westbury, NY), and stored at −20°C until analyzed for Se content. Samples of diets, excreta, and eggs were digested according to AOAC official method 986.15 (AOAC, 2000), as outlined in Lambert and Turoczy (2000). This method was chosen because facilities for using perchloric acid digestion were not available. Briefly, a 200- to 300-mg sample was weighed into a Teflon closed digestion vessel (Parr Instrument Company, Moline, IL), and 5 mL of concentrated HNO3 and 2 antibumping granules were added. The digestion vessel was sealed, and the sample was allowed to predigest for 18 h at room temperature. The digestion vessel was heated at 150°C for 2 h in a muffle furnace. After cooling, the digest was transferred to a 50-mL crucible and 1 mL of 75 mg/mL of magnesium nitrate solution was added. This mixture was dried slowly (2 to 3 h) on a hot plate and then ashed at 500°C for 30 min in a muffle furnace. After cooling, the residue was dissolved in 10 mL of concentrated HCl and heated on a steam bath for 15 min. After cooling, the solution was transferred to a Table 2. Selenium content of experimental diets (as-fed basis) Se content (μg of Se/g of diet) Diet
Na2SeO3
Se yeast1
Total2
Basal 1 2 3
0.31 0.31 0.31 0.31
0.00 1.03 2.38 5.12
0.31 1.34 2.69 5.43
1SelenoSource AF 600 (Diamond V Mills, Cedar Rapids, IA) containing 600 µg of Se/g of yeast. 2Total Se content of the diets was determined by analysis.
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over 1 μg of Se/g of diet (Moksnes, 1983; Payne et al., 2005; Vukasinovic et al., 2006; Chantiratikul et al., 2008). However, given the relatively few studies conducted employing these dietary levels and the apparent interstudy variability in egg Se, further work is needed to better describe the response of egg Se content to high dietary Se intake. The purpose of our current study is to describe the relationship between dietary Se and egg Se to determine the dietary Se requirement of hens needed to produce eggs containing high levels of Se. To achieve this, we conducted a feeding trial in which the egg Se content of 3 breeds of laying hens, each supplemented with 3 high levels of dietary Se, were measured. It should be noted that levels as high as 3 to 6 μg of organic Se/g diet are not toxic to the hen and have no effect on egg production (Moksnes, 1983; Payne et al., 2005; Chantiratikul et al., 2008). The secondary objective of the current study is to examine the effect of higher dietary organic Se levels on feed intake, egg mass, and egg production.
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Bennett and Cheng Table 3. Feed intake and egg production of the 3 breeds of laying hens used in this study Breed Parameter Feed intake (g/hen per d) Hen-day egg production (%) Weight (g/egg) Whole egg Eggshell Yolk + albumen
Barred Plymouth Rock 4.6B 4.0B
105.6 ± 63.9 ± 61.2 ± 0.9AB 5.1 ± 0.1C 56.1 ± 0.9A
Lohmann Brown 6.7A 2.7A
129.7 ± 86.2 ± 61.9 ± 0.9A 6.0 ± 0.1A 55.9 ± 0.9A
Lohmann White 112.8 ± 2.5B 87.7 ± 1.9A 58.4 ± 0.7B 5.5 ± 0.1B 52.9 ± 0.6B
A–CWithin-breed means within each row (parameter) with common superscripts are not significantly different (P < 0.05). None of these parameters were affected by dietary Se levels. Each within-breed mean is the average of 80 observations (20 cages, 4 wk).
Calculations and Statistical Analyses Egg production, feed consumption, and egg Se concentrations ([SE]egg) were analyzed by repeated measures 2-way ANOVA with breed and dietary Se as main effects. Excreta Se concentration and apparent Se absorption of the LB hens were analyzed by 1-way ANOVA with dietary Se as the main effect. When main effects were significant, differences were assessed by least significance difference test. The relationships between the dietary Se concentration ([SE]diet) and [SE]egg or total egg Se were determined by linear regression. Data are reported as means ± SEM. All statistical analyses were performed using JMP statistical software (version 7, SAS Institute Inc., Cary, NC) and significance was accepted when P < 0.05.
RESULTS Lohmann Browns had significantly higher feed intake than LW and BR (Table 3), but [SE]diet had no significant effect on feed intake. There was no significant diet × breed interaction. Egg production and egg weight were not significantly affected by the [SE]diet but did vary significantly among breeds (Table 3). Initial [SE]egg did not vary significantly among the dietary treatments in any of the breeds (diet × breed interaction, P < 0.56). When hens were fed the Sesupplemented diets, [SE]egg increased rapidly over the first 10 d (P < 0.001) but continued to increase over the last 2 wk (P < 0.001; Figure 1). By d 25, [Se]egg varied significantly both among dietary treatments and among breeds (diet × breed interaction, P < 0.002); there were no breed differences at each of the 2 lower [Se]diet, but at the highest [Se]diet, [Se]egg was significantly greater in the BR than in either of the 2 commercial breeds. Total egg Se followed the same response
pattern as [Se]egg (Figure 1). Overall, both [Se]egg and total egg Se were significantly related to [Se]diet and to daily Se intake (Figure 2). As [Se]diet increased, excreta Se concentration also increased and consequently so did the total amount of Se excreted (Table 4). However, the apparent Se absorption did not differ significantly between diets (mean = 70.2 ± 2.1%).
DISCUSSION There is evidence that a dietary Se intake greater than the RDA may have possible health benefits (Schrauzer, 2009). Although eggs have been shown to be an effective vehicle for supplementing Se in the diet (Surai et al., 2007), relatively few studies have fed hens diets containing enough Se to produce eggs at these levels. Furthermore, the response of egg Se levels to high dietary Se has been variable (Moksnes, 1983; Payne et al., 2005; Na et al., 2006; Vukasinovic et al., 2006; Chantiratikul et al., 2008).
Egg Se Levels The [Se]egg due to the organic Se supplement in our study were in agreement with those previously reported in other studies (Moksnes, 1983; Payne et al., 2005; Na et al., 2006; Vukasinovic et al., 2006; Chantiratikul et al., 2008). We found that both [Se]egg and total egg Se were linearly related to [SE]diet and intake (Figure 2). This result is not surprising given that organic forms of Se, such as selenomethionine (the major form of Se in yeast Se products; Rayman, 2004), are absorbed by active transport and are nonspecifically incorporated into proteins in place of methionine (Schrauzer, 2003). In contrast, inorganic Se sources, such as Na2SeO3, are passively absorbed into the body and typically have lower rates of absorption. The current RDA of Se for human adults in the United States and Canada is 55 μg/d (Institute of Medicine, 2000). Based on the results of this study, hens would require a diet containing 1.4 μg of organic Se/g to produce an egg containing 55 μg of Se (Figure 2). Given that most North American adults have a Se in-
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volumetric flask and diluted to volume with distilled water. The Se concentrations of the digests were then determined using hydride generation atomic fluorescence spectroscopy (Millennium Excalibur PSA Model 10.055, PS Analytical Ltd., Kent, UK), as outlined in Pappas et al. (2006).
SELENIUM ENRICHMENT OF TABLE EGGS
table egg layers (Table 3). This implies that when hens with lower rates of egg production are fed high levels of dietary Se, they may be able to build greater body stores of Se (selenomethionine) that, when mobilized, would allow for the production of eggs with a higher Se content. This may have important implications for breed selection if Se-enriched eggs are to be produced commercially. For example, many niche market producers use heritage breeds, which have lower egg production rates.
Apparent Se Absorption Few studies have examined the apparent absorption of dietary organic Se by laying hens (Latshaw and Osman, 1975; Dobrzański and Jamroz, 2003; Richter et al., 2006). Therefore, as part of this study, we conducted a balance study using LB hens. Although the total amount of Se excreted increased as [Se]diet increased, apparent Se absorption did not differ significantly between diets and averaged 70%. This value is somewhat higher than the 60 to 65% apparent absorption previously reported (Latshaw and Osman, 1975; Dobrzański and Jamroz, 2003; Richter et al., 2006). Together, these results indicate that 30 to 40% of the ingested Se is excreted. Thus, future work should be undertaken to address potential environmental concerns associated with feeding high levels of dietary Se to laying hens over a full production cycle.
Figure 1. Time course of the effect of dietary Se on egg Se concentration ([Se]egg, upper panels) and total egg Se content (lower panels) in 3 breeds of laying hens. Base diet contained 0.3 μg of Se/g as inorganic Na2SeO3, which was supplemented with Se yeast at 1.0 (○), 2.4 (Δ), or 5.1 (□) mg of Se/kg of diet (see Table 2).
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take greater than this RDA (Combs, 2001), producing Se-enriched eggs to meet this level is unwarranted. However, in other regions of the world where there is inadequate Se intake (e.g., parts of China, Europe, and New Zealand), this target may be a desirable goal. There is evidence that a Se intake greater than the RDA may have possible health benefits (Finley, 2007; Fisinin et al., 2009; Schrauzer, 2009; Schrauzer and Surai, 2009). Based on this evidence, Schrauzer (2009) suggests that the optimal Se intake for human adults is in the range of 250 to 300 μg/d. Assuming that the average North American adult has a Se intake of 100 to 200 μg/d (Combs, 2001), this would require increasing the Se intake by 50 to 200 μg/d. To produce an egg containing 50, 100, or 200 μg of Se would necessitate feeding hens diets containing 1.3, 2.8, or 5.7 μg of Se/g, respectively (Figure 2). It should be noted that these dietary levels are all greater than the current legal limit for Se supplementation of livestock feeds in Canada and the United States (0.3 μg of Se/g of diet). As stated above, [Se]egg and total egg Se were significantly related to daily Se intake (Figure 2). However, this response was variable among hens fed the highest level of Se. Although BR hens had a lower feed intake (Table 3), and hence Se intake, they produced eggs that had a higher Se content than in either of the 2 commercial breeds (but only when hens were fed the highest level of Se yeast) (Figures 1 and 2). The BR hens have a lower rate of egg production than commercial
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Bennett and Cheng Table 4. Apparent Se absorption of Lohmann Brown laying hens used in this study Diet Parameter Feed Se content (µg/g) Feed intake (g/hen per d) Se intake (µg/hen per d) Excreta Output (g of DM/hen per d) Se content (µg/g) Se output (µg/g) Apparent Se absorption (%)
1
2
3
1.34 114.1 ± 11.7A 152.8 ± 15.7C 25.4 ± 1.4A 2.0 ± 0.1C 52.0 ± 3.2B 65.4 ± 2.8A
2.69 108.4 ± 3.6A 291.7 ± 9.6B 24.2 ± 1.7A 3.5 ± 0.1B 84.8 ± 4.5B 70.8 ± 2.1A
5.43 109.7 ± 3.8A 580.5 ± 6.1A 24.9 ± 3.6A 5.9 ± 0.4A 149.3 ± 27.7A 74.4 ± 4.6A
Figure 2. Relationships between egg Se content [egg Se concentration ([Se]egg) or total egg Se] and dietary Se concentration ([Se]diet) or total Se intake in 3 breeds of laying hens [Barred Plymouth Rock (Δ), Lohmann Brown (□), and Lohmann White (○)] after 4 wk of supplementation. Base diet contained 0.3 μg of Se/g as inorganic Na2SeO3, which was supplemented with Se yeast at 1.0, 2.4, or 5.1 mg of Se/kg of diet (see Table 2). Initial presupplement values are included.
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A–CMeans within each row (parameter) with common superscripts are not significantly different (P < 0.05). Each mean is the average of 4 observations.
SELENIUM ENRICHMENT OF TABLE EGGS
Effect of High Dietary Organic Se Levels on Production The high dietary Se levels used in this study did not affect feed intake, egg production, or egg weight, which is in agreement with previous studies (Moksnes, 1983; Paton et al., 2002; Payne et al., 2005; Na et al., 2006; Vukasinovic et al., 2006; Chantiratikul et al. 2008). This lack of an effect on production indicates that high dietary levels of organic Se do not negatively affect the welfare of the hen.
The maximum tolerable dietary level of Se for poultry is currently set at 3 µg/g (NRC, 2005). This level was determined based on the observations that the threshold level of dietary Se for decreased egg hatchability and chick growth occurs at 5 µg/g. However, no signs of toxicity were observed in the laying hens used in this study or in those used in previous studies that fed hens high levels (3 to 6 µg/g) of organic Se (Moksnes, 1983; Payne et al., 2005; Vukasinovic et al., 2006; Chantiratikul et al., 2008). Dietary Se levels of 5 to 6 µg/g have no effect on body mass, feed intake, or egg production of laying hens when either organic (Moksnes, 1983; Table 2) or inorganic (Ort and Latshaw, 1978; Moksnes and Norheim, 1982) sources of Se are used. The threshold for decreased egg production and egg weight is 8 to 9 µg of Se/g of diet (Arnold et al., 1973; Ort and Latshaw, 1978). The levels of organic Se proposed to be fed to hens in this study (1.3 to 5.7 µg/g) are below these levels. All Se studies except those of Moksnes and Norheim (1982) and Moksnes (1983) lasted 4 to 6 wk. The 2 studies fed hens Se for 18 wk. Future research should be directed at longer term feeding trials to establish the safe dietary limits for organic Se consumption in hens if Se-enriched eggs are to be produced commercially.
Conclusions In this study, we assessed the response of egg Se levels to high dietary levels of organic Se to determine the dietary Se requirement of hens needed to produce Se-enriched table eggs. The results of this study indicate that within the range of Se levels that we fed to the hens, egg Se levels are linearly related to dietary organic Se levels. This and previous studies have not found any evidence of toxicity from organic Se to laying hens, even at levels as high as 3 to 6 μg of organic Se/g of diet. Future research should be directed at establishing the safe dietary limits for organic Se consumption in hens if Se-enriched eggs are to be produced commercially.
ACKNOWLEDGMENTS This research was supported by funds from the British Columbia Ministry of Agriculture and Lands, administered by the UBC Speciality Bird Research Committee. We thank Ilkyu Yoon, Diamond V Mills, for the Se yeast; Eduardo Jovel, Les Lavkulich and Gilles Galzi, Faculty of Land and Food Systems, University of British Columbia, for discussions on selenium analysis and use of equipment; Lisa Hedderson and Lee Struthers, AAFC Agassiz Poultry Research Centre, for technical assistance; and Fred Silversides, AAFC Agassiz Poultry Research Centre, Stewart Paulson, British Columbia Ministry of Agriculture and Lands, and Jennifer Arthur, Avian Research Centre, University of British Columbia, for valuable inputs.
REFERENCES AOAC. 2000. Official Methods of Analysis. AOAC Interational, Arlington, VA. Arnold, R. L., O. E. Olson, and C. W. Carlson. 1973. Dietary selenium and arsenic additions and their effects on tissue and egg selenium. Poult. Sci. 52:847–854. Chantiratikul, A., O. Chinrasri, and P. Chantiratikul. 2008. Effect of sodium selenite and zinc-l-selenomethionine on performance and selenium concentration in eggs of laying hens. Asian-australas. J. Anim. Sci. 21:1048–1052. Combs, G. F. Jr. 2001. Selenium in global food systems. Br. J. Nutr. 85:517–547. Dobrzański, Z., and D. Jamroz. 2003. Bioavailability of selenium and zinc supplied to the feed for laying hens in organic and inorganic form. http://www.ejpau.media.pl/volume6/issue2/animal/art03.html Accessed Jul. 9, 2010. Finley, J. W. 2007. Increased intakes of selenium-enriched foods may benefit human health. J. Sci. Food Agric. 87:1620–1627. Fisinin, V. I., T. T. Papazyan, and P. F. Surai. 2009. Producing selenium-enriched eggs and meat to improve the selenium status of the general population. Crit. Rev. Biotechnol. 29:18–28. Institute of Medicine. 2000. Dietary Reference Intakes for Vitamin C, Vitamin E, Selenium and Carotenoids. National Academy Press, Washington, DC. Lambert, D. F., and N. J. Turoczy. 2000. Comparison of digestion methods for the determination of selenium in fish tissue by cathodic stripping voltammetry. Anal. Chim. Acta 408:97–102. Latshaw, J. D., and M. Osman. 1975. Distribution of selenium in egg white and yolk after feeding natural and synthetic selenium compounds. Poult. Sci. 54:1244–1252. Moksnes, K. 1983. Selenium deposition in tissues and eggs of laying hens given surplus of selenium as selenomethionine. Acta Vet. Scand. 24:34–44. Moksnes, K., and G. Norheim. 1982. Selenium concentrations in tissues and eggs of growing and laying chickens fed sodium selenite at different levels. Acta Vet. Scand. 23:368–379. Na, J. C., S. H. Kim, D. B. Jang, J. H. Kim, D. J. Yu, G. H. Kang, H. K. Kim, D. S. Lee, S. J. Lee, J. C. Lee, and W. J. Lee. 2006. Effects of dietary organic selenium levels on performance and selenium retention in broiler chickens and laying hens. Korean J. Poult. Sci. 33:255–262. NRC. 1994. Nutrient Requirements of Poultry. 9th rev. ed. National Academy Press, Washington DC. NRC. 2005. Mineral Tolerance of Animals. 2nd rev. ed. National Academy Press, Washington, DC. Ort, J. F., and J. D. Latshaw. 1978. The toxic level of sodium selenite in the diet of laying chickens. J. Nutr. 108:1114–1120. Pappas, A. C., F. Karadas, P. F. Surai, N. A. R. Wood, P. Casey, G. R. Bortolotti, and B. K. Speake. 2006. Interspecies variation in
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Toxic Effect of High Dietary Organic Se Levels
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Bennett and Cheng Schrauzer, G. N. 2009. Selenium and selenium-antagonistic elements in nutritional cancer prevention. Crit. Rev. Biotechnol. 29:10– 17. Schrauzer, G. N., and P. F. Surai. 2009. Selenium in human and animal nutrition: Resolved and unresolved issues. A partly historical treatise in commemoration of the fiftieth anniversary of the discovery of the biological essentiality of selenium, dedicated to the memory of Klaus Schwarz (1914–1978) on the occasion of the thirtieth anniversary of his death. Crit. Rev. Biotechnol. 29:2–9. Surai, P. F., T. T. Papazyan, B. K. Speake, and N. H. C. Sparks. 2007. Enrichment in selenium and other trace elements. Pages 183–190 in Bioactive Egg Compounds. R. Huopalahti, R. LopezFandinño, and M. Anton, R. Schade, ed. Springer-Verlag Berlin, Germany. Vukasinovic, M., R. Mihailovic, M. Sekler, V. Kaljevic, and V. Kurcubic. 2006. The impact of the selenium content of laying hen feeds. Arch. Geflügelkd. 70:91–96.
Downloaded from http://ps.oxfordjournals.org/ at EKU Libraries,SerialsEastern Kentucky University on May 25, 2015
yolk selenium concentrations among eggs of free-living birds: The effect of phylogeny. J. Trace Elem. Med. Biol. 20:155–160. Paton, N. D., A. H. Cantor, A. J. Pescatore, and C. A. Smith. 2002. The effect of dietary selenium source and level on the uptake of selenium by developing chick embryos. Poult. Sci. 81:1548– 1554. Payne, R. L., T. K. Lavergne, and L. L. Southern. 2005. Effect of inorganic versus organic selenium on hen production and egg selenium concentration. Poult. Sci. 84:232–237. Rayman, M. P. 2004. The use of high-selenium yeast to raise selenium status: How does it measure up? Br. J. Nutr. 92:557–573. Richter, G., M. Leiterer, R. Kirmse, W. I. Ochrimenko, and W. Arnhold. 2006. Comparative investigation of dietary supplements of organic and inorganic bounded selenium in laying hens. Tierarztl. Umsch. 61:155–161. Schrauzer, G. N. 2003. The nutritional significance, metabolism and toxicology of selenomethionine. Adv. Food Nutr. Res. 47:73– 112.