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Department of Animal Science and * Department of Nutrition, University of California–Davis, Davis, CA 95616
1To whom correspondence should be addressed. E-mail: kcklasing{at}ucdavis.edu
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • chicken • carotenoid • lutein • canthaxanthin • immune tissue
Carotenoids constitute a large (>600 identified carotenoids) group of lipid-soluble organic compounds that may have one or more oxygen substitutions. Carotenoids are of biological importance for their light-absorbing properties (providing the basis for many types of pigmentation), antioxidant functions and immunomodulatory functions [reviewed by Goodwin (1 )]. Carotenoid-based pigmentation of skin, feathers, egg yolks and other tissues is prevalent in invertebrates, crustaceans, fish, reptiles, birds and some mammals. Particularly in fish and birds, carotenoid-based pigmentation has been demonstrated to affect mate selection (2 ,3 ) and progeny development (4 ,5 ). Additionally, carotenoids (primarily lutein and canthaxanthin) are routinely fed in the commercial poultry and aquaculture industries at a wide range of dietary levels to provide pigmentation for animal products.
The role of carotenoids as immunomodulatory agents is of great interest to human and animal nutritionists that attempt to use dietary nutrients as health-promoting agents. Carotenoids modulate humoral immunity and reduce the incidence of many types of cancer in mammals [reviewed in Bendich (6 )]. Additionally, carotenoids can affect other types of immune responses under certain conditions (7 –9 ). The role of carotenoids in avian immunomodulation is less clear. However, before assessing functional effects of carotenoids, it is useful to examine the concentrations of specific carotenoids within immune tissues. This type of assessment ensures that carotenoids are available to immune tissues to provide functional effects, and has been used in a variety of mammalian species (10 –14 ).
Although the nutritional status of an animal is based primarily on its exposure to dietary nutrients, the role of maternal nutrition is also relevant. The developing embryo relies on maternally derived nutrients as substrates for cellular proliferation and differentiation [reviewed by McClellan and Novak (15 ) and Couch and Ferguson (16 )]. Additionally, maternal nutrient input may impact the physiology of the animal later in life, or may impact both embryogenesis and future function. In particular, the immune system is very susceptible to maternal nutrient deficiencies and toxicities. Deficiencies of vitamin A, vitamin D, vitamin E, magnesium, zinc and copper (17 –23 , respectively) negatively impact immune system development (e.g., organ weight, differentiation of leukocyte populations) as well as subsequent immune responses (presumably attributable to lack of the appropriate components of the immune system). However, the role of dietary compounds that are not considered essential nutrients, such as carotenoids, on the physiology of the developing and juvenile animal has not been examined.
Our objective was to examine the interactions between maternal dietary carotenoid concentration and chick dietary carotenoid concentration on the incorporation of carotenoids into the chick’s immune tissues. These data will provide a framework for analysis of the function of carotenoids in avian immune responses.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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0.17 pmol (0.1 ng) lutein, zeaxanthin or canthaxanthin/kg diet]. Subsequent to dietary treatment of hens, eggs were collected daily; egg yolks were isolated, weighed and stored at -80°C before analysis of carotenoid concentration by HPLC. Once a plateau of egg yolk carotenoid concentration was achieved (
30 d; see Fig. 2
), hens were artificially inseminated and chicks were hatched from C+ or C- eggs. Because of the magnitude of chick numbers required, four sequential hatches of chicks were used in these dose–response experiments. After hatch, chicks were randomly assigned to pens within brooder-batteries, at a stocking density of 
6 chicks/pen. Chicks were maintained under constant lighting and had ad libitum access to feed and water.
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Sampling
At 4 wk of age, chicks were bled by cardiac puncture into heparinized syringes for plasma collection. Birds were subsequently killed by CO2 overdose, then bursa (whole), thymus (3 to 4 lobes), liver (left lobe) and shank (left metatarsus) were excised. Tissues were immediately chilled to -80°C in light-tight containers, then frozen at -80°C until analysis. Before carotenoid extraction, epithelium samples were removed from shanks by scraping with a razor, removing only the top layer of epithelium. Because of differing numbers of C- and C+ eggs available for these experiments, we tested 10 dietary carotenoid levels in C+ chicks (0 to 58 mg/kg) but only 8 dietary carotenoid levels in C- chicks (0 to 38 mg/kg). Skin carotenoids were determined only in chicks fed 0 or 38 mg carotenoids/kg.
Carotenoid analysis
Tissues and diets were analyzed for carotenoids by HPLC after extraction procedures. All procedures were completed under amber light and/or in amber tubes. Briefly, tissues and diet were homogenized in phosphate-buffered saline (PBS) at a ratio of two parts tissue to one part PBS (w/v). Carotenoids were extracted from 1 g tissue/diet homogenate or 500 µl plasma. For each sample, butanol:acetonitrile (1:1 v/v) was added at twice the sample volume. Samples were shaken vigorously for 5 min, then hexane:chloroform (2:1 v/v) was added at 1x sample volume. Samples were again shaken for 5 min, then a saturated solution of K2HPO4 was added at 0.1x sample volume. Samples were shaken vigorously for 5 min, then centrifuged (5000 x g, 15 min). The top organic phase was removed and dried under N2, then samples were frozen until analysis. Before HPLC analysis, samples were reconstituted into methanol:methylene chloride (47:53% v/v).
HPLC analysis was performed using a C18 reverse-phase column (5 µm, 300 Å, 4.6 mm ID x 250 mm L; Vydac 201TP54, Hesperia CA) and high performance guard column (5 µm; Vydac 201GD54T). The column was chilled to 15°C using a water jacket (35 cm; Alltech, Deerfield, IL) and a circulating water chiller (RF-10; New Brunswick Scientific, Edison, NJ). The isocratic mobile phase (100% methanol, HPLC grade, Fisher Scientific #A452-4, Springfield, NJ) was maintained at a flow rate of 1.0 mL/min (Waters 510 pump, Milford MA), and automated injections (Waters WISP 712) of 75 µl were made. Absorbance at 445 was monitored and peaks were integrated using UV/visible detector (Waters 484) monitored at 445 nm, and Millenium software (Waters) was used to process and integrate peaks.
Peak identification and quantitation of sample concentration was made by comparison to purified standards of lutein, zeaxanthin and canthaxanthin (provided by Roche Vitamins). Respective retention time was 7.5, 8.5 and 14.5 min, and the limit of detection for each carotenoid in our standards was 
0.17 pmol. Three injections of each standard at different volumes were made before each sample set, and standard curves were generated using linear regression (JMP software; SAS Institute, Cary, NC).
Statistical analysis
ANOVA (JMP software) was used to examine the main effect of the time of hen dietary treatment (i.e., date of chick hatch) on tissue carotenoid incorporation. Time of hen treatment was not statistically significant for any parameter measured (P > 0.10); therefore, this effect was removed from statistical analyses.
ANOVA was used to examine the main effect of hen dietary treatment, chick dietary treatment and their interaction on tissue carotenoids and production parameters (feed intake, body weight gain). When main effects were significant (P < 0.05), orthogonal contrasts were used to identify differences between means. Additionally, tissue carotenoid concentrations (except skin) were analyzed using regression models (JMP software), with diet and tissue carotenoid concentration as continuous variables. Differences were considered significant at P < 0.05.
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Egg yolk carotenoids
Deposition of egg yolk is completed 24 h before its ovulation, and it takes 24 h from the time of ovulation until the egg is laid in commercial layer hens (25
). Therefore, the effect of hen dietary treatment on egg yolk composition should be detectable 48 h after onset of dietary treatment, and so egg yolks were analyzed for carotenoids starting 2 d after switching hens from a carotenoid-containing diet to a carotenoid-free diet. Egg yolk carotenoid concentration decreased over time, and yolks contained no detectable carotenoids (0.17 pmol/egg) after 30 d of dietary treatment (Fig. 2)
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Tissue carotenoids
Effect of hen dietary carotenoid treatment on their chicks’ tissue carotenoids. Hen dietary treatment affected the concentration of plasma total carotenoids (lutein + zeaxanthin + canthaxanthin, Fig. 3A , P < 0.01), lutein (P < 0.01) and canthaxanthin (P = 0.02), but not zeaxanthin (P = 0.13) of 4-wk-old chicks. In the liver, hen dietary treatment affected the concentration of total carotenoids (Fig. 3 B, P = 0.04) and canthaxanthin (P = 0.02), but not lutein (P = 0.07) or zeaxanthin (P = 0.25). Similarly, thymic total carotenoids (Fig. 3 C) and thymic canthaxanthin deposition were dependent on hen dietary treatment (P < 0.01 and P = 0.03, respectively), whereas thymic lutein and zeaxanthin were not (P = 0.17 and P = 0.25, respectively).
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20 mg dietary carotenoid/kg.
In the thymus (Fig. 3
C), increasing chick dietary carotenoids significantly increased total carotenoids (P < 0.01) and canthaxanthin (P = 0.05), but not lutein or zeaxanthin (P = 0.85 and P = 0.95, respectively). Chick dietary treatment predicted >50% of the variation in thymic carotenoids for chicks hatched from C+ eggs, but <25% of the variation in thymic carotenoids in chicks hatched from C- eggs. Carotenoid saturation of C+ chick thymus occurred at 40 mg/kg diet. In the bursa, the main effect of chick dietary treatment was not significant for any carotenoid tested (P > 0.05 for each, Fig. 3
D), and chick dietary treatment predicted <23% of the variation in chicks hatched from C+ and C- eggs. Finally, there was a hen dietary treatment x chick dietary treatment interaction for skin lutein (P < 0.05). In C- chicks, skin lutein was not different for chicks fed 0 or 38 mg carotenoids (0.04 mmol lutein/kg vs. 0.15 mmol lutein/kg, respectively, P = 0.29), but skin lutein of C+ chicks was significantly increased by 38 mg dietary carotenoids compared to 0 mg dietary carotenoids (0.77 µmol lutein/kg vs. 0.24 µmol lutein/kg, respectively, P < 0.01). Skin zeaxanthin, canthaxanthin and total carotenoids were significantly increased by feeding chicks 38 mg dietary carotenoids compared to chicks fed 0 mg/kg diet (Fig. 4
, P < 0.05).
Effect of dietary carotenoid treatment on enrichment of specific carotenoids in tissues. In plasma and liver, chicks hatched from C+ eggs and fed 38 mg total carotenoid/kg diet contained equivalent amounts of lutein and canthaxanthin, even though the diet lutein level was almost quadruple that of the canthaxanthin diet (Table 2 ). In contrast, the ratio of lutein:canthaxanthin in the plasma and liver of chicks hatched from C- eggs approximated the dietary ratio. In the thymus, relative canthaxanthin concentrations were greater in chicks hatched from C+ or C- eggs and fed 38 mg total carotenoid/kg diet, compared to that in liver and plasma. In the bursa of chicks hatched from C+ eggs, relative lutein deposition was approximately twice that of canthaxanthin, whereas canthaxanthin was not detected in the bursa of any chicks hatched from C- eggs. Finally, the skin of chicks hatched from C+ eggs and fed 38 mg carotenoid/kg diet contained similar amounts of lutein and canthaxanthin, whereas the skin of chicks hatched from C- eggs contained greater amounts of canthaxanthin than of lutein.
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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30 d. This time course is slightly longer than previously demonstrated (3 wk), although previous experiments did not aim to deplete yolk carotenoids to undetectable levels (26
,27
). In a similar manner, the time required to maximize egg yolk carotenoids in response to dietary treatment can be variable, ranging from 14 to 35 d of feeding carotenoid-containing diets (27
–29
). It is likely that the length of time required to achieve stable yolk carotenoid concentrations is a function of the bioavailability of various dietary carotenoid sources in addition to previous hen nutritional status.
Yolk-derived carotenoids were conserved in the tissues of posthatch chicks, given that chicks fed a carotenoid-free diet for 4 wk still had detectable levels of tissue carotenoids. Similar observations have been made in very young (<1 wk of age) chickens and in other avian species (28
,30
–32
), suggesting that there is tight conservation of carotenoids in avian tissues. In fact, 25% of liver carotenoids in a 4-wk-old chick hatched from a C+ egg are predicted to be yolk-derived, based on previous research that examined yolk-derived carotenoid deposition in tissues of 5-d-old chicks (28
,31
). Similar calculations for the other tissues cannot be made because the carotenoid concentration of bursa, thymus and skin in very young chicks has not been previously reported.
In addition to tissue deposition of yolk-derived carotenoids, the presence of yolk carotenoids was critical for subsequent deposition of dietary carotenoids into tissues. When chicks were hatched from C- eggs, they never achieved the same degree of carotenoid deposition as did chicks hatched from C+ eggs. Additionally, yolk carotenoid exposure had carotenoid-specific effects. For example, although they were fed canthaxanthin, this carotenoid was not detected in the bursa, thymus or skin of chicks hatched from C- eggs. These data suggest that in ovo carotenoid exposure is important for subsequent absorption, metabolism and/or tissue deposition of diet-derived carotenoids.
Although tissue carotenoid deposition was altered by yolk carotenoid exposure, the dietary carotenoid level of chicks also affected the relative concentration of tissue carotenoids. In particular, when fed 0 mg carotenoids, the relative bursal carotenoid concentration in chicks hatched from C- or C+ eggs was second only to liver in C- chicks, and liver and skin in C+ chicks. In contrast, when fed 38 mg carotenoids, bursal carotenoid concentration was the lowest of all tissues tested, suggesting that when carotenoids are limiting, either in diets or egg yolks, the bursa may have priority to deposit those carotenoids. A substantial portion of avian B-cell development occurs in the bursa during embryogenesis (33 ), and the developmental events that lead to the diversification of the B-cell repertoire require considerable cell proliferation and cell–cell communication. These developmental events can be modulated by carotenoids (34 ,35 ), which may explain the apparent priority of the bursa for carotenoids.
The effects of egg yolk carotenoids and subsequent dietary carotenoid levels on chick tissue carotenoid deposition have several important implications, in terms of the biology of carotenoid metabolism, and in terms of feeding birds. First, exposure to carotenoids during embryonic development enables chicks to better deposit dietary carotenoids later in life. This observation may simply be an additive effect of egg yolk plus dietary carotenoids; if yolk carotenoids (125 nmol/egg in the present experiment) were retained by a chick for 4 wk, tissue carotenoid differences between chicks hatched from C+ and C- eggs, and fed 38 mg total carotenoids/kg diet, could be accounted for (183.6 nmol/C+ chick vs. 76.2 nmol/C- chick). However, it is doubtful that 100% of egg yolk–derived carotenoids are still present in a 4-wk-old chicks, given that tissue carotenoids decline after hatching (31
). Additionally, if the effects of yolk and diet carotenoids were additive, then increasing dietary carotenoid levels in C- chicks would produce tissue carotenoid deposition similar to that seen in C+ chicks. However, our results demonstrate that thymic and bursal carotenoid depositions were not correlated to diet, and thus it would be difficult to enhance the carotenoid concentrations of these tissues by increasing chick dietary carotenoid levels. In contrast, markedly increasing the level of carotenoids fed to C- chicks would be predicted to enhance the carotenoid concentration of plasma (by feeding 335 mg total carotenoid/kg diet), liver (by feeding 75 mg total carotenoid/kg diet) and skin (by feeding 105 mg total carotenoid/kg diet), to levels similar to those seen in chicks hatched from C+ eggs and fed 38 mg total carotenoid/kg diet. In addition to the effects of yolk carotenoids, carotenoids fed to the early posthatch chick can have a marked impact on tissue carotenoid deposition later in life. For example, chicks fed low carotenoid starter diets (6.7 mg/kg diet) and high carotenoid finisher diets (25.5 mg/kg diet) were not able to achieve the same degree of shank pigmentation as were birds fed medium or high (16.9 and 25.5 mg/kg diet, respectively) carotenoid starter and finisher diets (37
). These data demonstrate that early carotenoid exposure may be important for future efficiency of carotenoid deposition.
Second, the effect of hen dietary carotenoid levels on their chicks’ subsequent carotenoid deposition may be important for both domestic poultry and wild birds. Supplementing dietary carotenoids to breeder hens to enhance egg yolk carotenoids may allow for more effective pigmentation of progeny, and decrease production costs by reducing the amount of dietary carotenoids needed to achieve optimal pigmentation. Wild birds may also benefit from high yolk carotenoid levels. Based on the Hamiton–Zuk hypothesis that more highly pigmented males have greater success in mate choice and subsequent reproductive efforts (36 ), increased yolk carotenoids may enhance the ability of male offspring to accumulate carotenoid-based pigmentation and thus increase breeding success. Additionally, because the degree of carotenoid pigmentation of chicks may determine the rate of parental feeding (4 ,5 ), enhanced yolk carotenoids and subsequently higher pigmentation levels may enhance progeny success.
Finally, tissue carotenoid deposition is specific, as evidenced by differences in relative concentrations of individual carotenoids between tissues, even though diets contained a consistent ratio of lutein:canthaxanthin. Tissue-specific differences in carotenoid concentration have been previously demonstrated in the posthatch tissues of the chicken (28 ), common moorhen (Gallinula chloropus), American coot (Fulica Americana), lesser black-backed gull (Larus fuscus) (30 ) and Japanese quail (Coturnix coturnix japonica) (38 ), and similar trends are observed in a variety of mammals [see review by Mares-Perlman et al. (39 )]. These differences may reflect saturation of particular tissues when yolk carotenoids are present and high dietary carotenoids were fed (e.g., liver and plasma in the present experiment). Alternatively, differences may reflect specific uptake of carotenoids (e.g., in thymus and bursa in the present experiment); the presence of a binding protein for specific carotenoids has been demonstrated in ferret liver (40 ). Specific uptake may also be related to differences in transport of various carotenoids in blood and subsequent differences in tissue uptakes of these components (e.g., HDL vs. LDL vs. lipoprotein remnants vs. freely transported carotenoids) (41 ).
These data demonstrate the importance of maternal carotenoid nutrition on the subsequent deposition of carotenoids into tissues of growing chicks. Skin, liver, thymus, bursa and plasma carotenoid concentration were dependent on yolk carotenoid exposure. Additionally, for all tissues except bursa, dietary carotenoids were incorporated in a dose-dependent manner, although the relative proportions of lutein and canthaxanthin were variable, depending on the tissue tested and the level of carotenoids in the hen’s diet. When chicks were hatched from carotenoid-replete egg yolks, thymic carotenoids were maximal when chicks were fed 40 mg carotenoid/kg diet, and liver carotenoids were maximal when chicks were fed 20 mg carotenoid/kg diet. Future research concerning carotenoids in birds should control for hen dietary carotenoid levels.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Manuscript received 3 October 2002. Initial review completed 15 November 2002. Revision accepted 9 January 2003.
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LITERATURE CITED |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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1. Goodwin, T. W. (1986) Metabolism, nutrition, and function of carotenoids. Annu. Rev. Nutr. 6:273-297.[Medline]
2. Gray, D. A. (1996) Carotenoids and sexual dichromatism in North American passerine birds. Am. Nat. 148:453-480.
3. Stradi, R. (1995) The Colour of Flight: Carotenoids in Bird Plumage 1995 Solei Gruppo Editoriale Informatico Milan, Italy.
4. Saino, N., Ninni, P., Calza, S., Martinelli, R., De Bernardi, F. & Moller, A. P. (2000) Better red than dead: carotenoid-based mouth coloration reveals infection in barn swallow nestlings. Proc. R. Soc. Lond. B 267:57-61.[Medline]
5. Lyon, B. E., Eadie, J. M. & Hamilton, L. D. (1994) Parental choice selects for ornamental plumage in American coot chicks. Nature 371:240-243.
6. Bendich, A. (1989) Carotenoids and the immune response. J. Nutr. 119:112-115.
7. Hughes, D. A. (1999) Effects of carotenoids on human immune function. Proc. Nutr. Soc. 58:713-718.[Medline]
8. Jyonouchi, H., Sun, S., Mizokami, M. & Gross, M. D. (1996) Effects of various carotenoids on cloned effector-stage T-helper cell activity. Nutr. Cancer 26:313-324.[Medline]
9. Park, J. S., Chew, B. P., Wong, T. S., Zhang, J. & Magnuson, N. S. (1999) Dietary lutein but not astaxanthin or ß-carotene increases pim-1 gene expression in murine lymphocytes. Nutr. Cancer 33:206-212.[Medline]
10. Chew, B. P., Wong, T. S., Michal, J. J., Standaert, F. E. & Heirman, L. R. (1991) Subcellular distribution of ß-carotene, retinol, and 
-tocopherol in porcine lymphocytes after a single injection of ß-carotene. J. Anim. Sci. 69:4892-4897.[Abstract]
11. Chew, B. P., Wong, T. S. & Michal, J. J. (1993) Uptake of orally administered ß-carotene by blood plasma, leukocytes, and lipoproteins in calves. J. Anim. Sci. 71:730-739.[Abstract]
12. Chew, B. P., Park, J. S., Weng, B. C., Wong, T. S., Hayek, M. G. & Reinhart, G. A. (2000) Dietary ß-carotene absorption by blood plasma and leukocytes in domestic cats. J. Nutr. 130:2322-2325.
13. Chew, B. P., Park, J. S., Wong, T. S., Kim, H. W., Weng, B.B.C., Byrne, K. M., Hayek, M. G. & Reinhart, G. A. (2000) Dietary ß-carotene stimulates cell-mediated and humoral immune response in dogs. J. Nutr. 130:1910-1913.
14. Chew, B. P., Park, J. S., Weng, B. C., Wong, T. S., Hayek, M. G. & Reinhart, G. A. (2000) Dietary ß-carotene is taken up by blood plasma and leukocytes in dogs. J. Nutr. 130:1788-1791.
15. McClellan, R. & Novak, D. (2001) Fetal nutrition: how we become what we are. J. Pediatr. Gastroenterol. Nutr. 33:233-244.[Medline]
16. Couch, J. R. & Ferguson, T. M. (1975) Nutrition and embryonic development in the domestic fowl. Proc. Nutr. Soc. 34:1-3.[Medline]
17. Nauss, K. M., Chew-Chin, P., Ambrogi, L. & Newberne, P. M. (1985) Immunological changes during progressive stages of vitamin A deficiency in the rat. J. Nutr. 115:909-918.
18. Semba, R. D. (1998) The role of vitamin A and related retinoids in immune function. Nutr. Rev. 56:S38-S48.[Medline]
19. Alsam, S. M., Garlich, J. D. & Qureshi, M. A. (1998) Vitamin D deficiency alters the immune response of broiler chicks. Poult. Sci. 77:842-849.
20. Erf, G. F., Bottje, W. G., Bersi, T. K., Headrick, M. D. & Fritts, C. A. (1998) Effects of dietary vitamin E on the immune system in broilers: altered proportions of CD4 T cells in the thymus and spleen. Poult. Sci. 77:529-537.
21. Malpuech-Brugere, C., Nowacki, W., Gueux, E., Kuryszko, J., Rock, E., Rayssiguier, Y. & Mazur, A. (1999) Accelerated thymus involution in magnesium-deficient rats is related to enhanced apoptosis and sensitivity to oxidative stress. Br. J. Nutr. 81:405-411.[Medline]
22. Prohaska, J. R. & Lukasewycz, O. A. (1989) Copper deficiency during perinatal development: effects on the immune response of mice. J. Nutr. 119:922-931.
23. Beach, R. S., Gershwin, M. E., Makishima, R. K. & Hurley, L. S. (1980) Impaired immunologic ontogeny in postnatal zinc deprivation. J. Nutr. 110:805-815.
24. National Research Council (NRC) (1994) Nutrient Requirements of Poultry 9th ed. 1994 National Academy Press Washington, DC.
25. Whittow, G. C. eds. Sturkie’s Avian Physiology 5th ed. 2000 Academic Press New York, NY. .
26. Schaeffer, J. L., Tyczkowski, J. K., Parkhurst, C. R. & Hamilton, P. B. (1988) Carotenoid composition of serum and egg yolks of hens fed diets varying in carotenoid composition. Poult. Sci. 67:608-614.[Medline]
27. Hinton, C. F., Fry, J. L. & Harms, R. H. (1974) Influence of a xanthophyll-free pullet grower diet on subsequent egg yolk pigmentation. Poult. Sci. 53:223-226.
28. Surai, P. F. & Speake, B. K. (1998) Distribution of carotenoids from the yolk to the tissues of the chick embryo. J. Nutr. Biochem. 9:645-651.
29. Belyavin, C. G. & Marangos, A. G. (1987) Natural products for egg yolk pigmentation. Recent Adv. Anim. Nutr. 7:239-260.
30. Surai, P. F., Speake, B. K., Wood, N. A., Blount, J. D., Bortolotti, G. R. & Sparks, N. H. (2001) Carotenoid discrimination by the avian embryo: a lesson from wild birds. Comp. Biochem. Physiol. B 128:743-750.[Medline]
31. Surai, P. F., Ionov, I. A., Kuchmistova, E. F., Noble, R. C. & Speake, B. K. (1998) The relationship between the levels of alpha-tocopherol and carotenoids in the maternal feed, yolk and neonatal tissues: comparison between the chicken, turkey, duck and goose. J. Sci. Food Agric. 76:593-598.
32. Surai, P. F., Noble, R. C. & Speake, B. K. (1996) Tissue-specific differences in antioxidant distribution and susceptibility to lipid peroxidation during development of the chick embryo. Biochim. Biophys. Acta 1304:1-10.[Medline]
33. Glick, G., Chang, T. S. & Jaap, R. G. (1956) The bursa of Fabricius and antibody production. Poult. Sci. 35:224-234.
34. Burri, B. J. (2000) Carotenoids and gene expression. Nutr 16:577-578.
35. DeFlora, S., Bagnasco, M. & Vainio, H. (1999) Modulation of genotoxic and related effects by carotenoids and vitamin A in experimental models: mechanistic issues. Mutagenesis 14:153-172.
36. Hamilton, W. D. & Zuk, M. (1982) Heritable true fitness and bright birds: a role for parasites?. Science 218:384-387.
37. Bartov, I. & Bornstein, S. (1969) Depletion and repletion of body xanthophylls’ reserves as related to broiler pigmentation. Poult. Sci. 48:495-504.[Medline]
38. Toyoda, Y., Thomson, L. R., Langner, A., Craft, N. E., Garnett, K. M., Nichols, C. R., Cheng, K. M. & Dorey, C. K. (2002) Effect of dietary zeaxanthin on tissue distribution of zeaxanthin and lutein in quail. Invest. Ophthalmol. Vis. Sci. 43:1210-1221.
39. Mares-Perlman, J. A., Millen, A. E., Ficek, T. L. & Hankinson, S. E. (2002) The body of evidence to support a protective role for lutein and zeaxanthin in delaying chronic disease. J. Nutr. 132:518S-524S.
40. Lakshman, M. R. & Rao, M. N. (1999) Purification and characterization of cellular carotenoid-binding protein from mammalian liver. Methods Enzymol 299:441-456.[Medline]
41. Parker, R. S. (1996) Absorption, metabolism, and transport of carotenoids. FASEB J. 10:542-551.[Abstract]
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C. Biard, P. F. Surai, and A. P. Moller Carotenoid availability in diet and phenotype of blue and great tit nestlings J. Exp. Biol., March 15, 2006; 209(6): 1004 - 1015. [Abstract] [Full Text] [PDF]
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 G. Y. Bedecarrats and S. Leeson Dietary Lutein Influences Immune Response in Laying Hens J. Appl. Poult. Res., January 1, 2006; 15(2): 183 - 189. [Abstract] [Full Text] [PDF]
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