doi: 10.15389/agrobiology.2019.4.681eng

UDC: 636.084.524:637.4.04:615.322

Supported financially by Russian Science Foundation, grant No 16-16-04047



A.Sh. Kavtarashvili, I.L. Stefanova, V.S. Svitkin

Federal Scientific Center All-Russian Research and Technological Poultry Institute RAS, 10, ul. Ptitsegradskaya, Sergiev Posad, Moscow Province, 141311 Russia, e-mail (✉ corresponding author),,

Kavtarashvili A.Sh.
Svitkin V.S.
Stefanova I.L.

Received June 6, 2019


Recent growth of public awareness on the role of carotenoids (especially xanthophylls) in the prophylaxis and dietotherapy of certain oncologic, cardiovascular, and ocular diseases in human related to antioxidative and immunomodulating properties (E. Bakan et al., 2014) made these substances used earlier for the improvement of egg yolk color (and, as a consequence, attractibility of the eggs for consumers) valuable target substances in the production of dietetic, designer, and functional eggs (V.P. Singh et al., 2012). High bioavailability of carotenoids from table eggs due to the solubilization in yolk lipids makes the eggs a suitable source of carotenoids for the enrichment of human diet (H.-Y. Chung et al., 2004). In the study presented different aspects of practical production of functional eggs enriched with carotenoids are reviewed: the sources of carotenoids in the diets for laying hens and their comparative efficacy; metabolism of carotenoids in hens and its relation to the metabolism of lipids; the effects of different xanthophyll sources on health and productivity in hens, egg quality, the intensity of yolk coloration, concentrations of xanthophylls in yolk. The main advantage of synthetic preparations of carotenoids is their high availability for the layers (M. Marounek et al., 2016); however, due to their expensiveness these sources can be economically unprofitable in the production of enriched eggs. Natural sources of basic yolk carotenoids, lutein and zeaxanthin (S.M. Vostrikova et al., 2011), e.g. marigold (Tagetes spp.), frequently contain substantial part of these xanthophylls as ethers with fatty acids; the availability of these forms for layers is significantly lower in compare to the saponified forms (K. Lokaewmanee et al., 2011). These sources can be preliminary saponified to release the etherified xanthophylls: it will improve the availability of the latter for layers by 40-60 %, the transfer of these substances to egg yolks (H. Hencken, 1992), and prevent the resulting fatty acid profiles of eggs from the shift to higher percentage of saturated fatty acids (A. Altunta et al., 2014). The disadvantage of this approach is related to low stability of saponified preparations during the storage; researchers recommend these preparations to be stored frozen and to be used as soon as possible after the unpacking. Different effects of the sources of xanthophylls on the productive performance in layers (primarily the intensity of lay, egg weight and morphology) were reported: certain authors reported the significant improvements of these productivity parameters while other authors found these parameters to remain at the level of control treatments or be slightly lower. The majority of studied sources providing xanthophylls in the forms available for layers substantially and significantly improves the parameters of yolk coloration intensity (decreases index of lightness L* and increases indices of yellowness b* and redness a*) and concentrations of lutein and zeaxanthin in yolk. Reasonable choice of sources and doses can result in eggs enriched with xanthophylls to the extent where the eggs could be considered functional carotenoid sources for human (A. Sahoo et al., 2014), though no normal consumption rates for the xanthophylls irrespective to specific diseases were so far developed (E. Toti et al., 2018).

Keywords: functional eggs, carotenoids, lutein, zeaxanthin, layer diet, dietary carotenoid sources, egg yolk quality.



  1. Kavtarashvili A.Sh., Stefanova I.L., Svitkin V.S., Novotorov E.N. Functional egg production. I. the role of ω-3 polyunsaturated fatty acids (review). Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2017, 52(2): 349-366 CrossRef
  2. Kavtarashvili A.Sh., Stefanova I.L., Svitkin V.S., Novotorov E.N. Finctional egg production. II. The roles of selenium, zinc, and iodine (review). Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2017, 52(4): 700-715 CrossRef
  3. Kavtarashvili A.Sh., Kodentsova V.M., Mazo V.K., Risnik D.V., Stefanova I.L. Biofortification of hen eggs: vitamins and carotenoids (review). Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2017, 52(6): 1094-1104 CrossRef
  4. Wagner K.H., Elmadfa I. Biological relevance of terpenoids. Overview focusing on mono-, di- and tetraterpenes. Ann. Nutr. Metab., 2003, 47: 95-106 CrossRef
  5. Oliver J., Palou A. Chromatographic determination of carotenoids in foods. Journal of Chromatography A, 2000, 881(1-2): 543-555 CrossRef
  6. Amorim-Carrilho K.T., Cepeda A., Fente C., Regal P. Review of methods for analysis of carotenoids. TrAC Trends in Analytical Chemistry, 2014, 56: 49-73 CrossRef
  7. Sajilata M.G., Singhal R.S., Kamat M.Y. The carotenoid pigment zeaxanthin — a review. Comprehensive Reviews in Food Science and Food Safety, 2008, 7(1): 29-49 CrossRef
  8. Olson J.A., Krinsky N.I. Introduction: the colorful fascinating world of the carotenoids: important physiologic modulators. FASEB J., 1995, 9(15): 1547-1550 CrossRef
  9. Hurst W.J. Methods of analysis for functional foods and nutraceuticals. 2nd Ed. CRC Press, Boca Raton, London-NY, 2008.
  10. Britton G. Structure and properties of carotenoids in relation to function. FASEB J., 1995, 9(15): 1551-1558 CrossRef
  11. Merhan O., Özcan A., Atakişi E., Öğün M., Kükürt A. The effect of β-carotene on acute phase response in diethylnitrosamine given rabbits. Kafkas Univ. Vet. Fak. Derg., 2016, 22(4): 533-537 CrossRef
  12. Gammone M.A., Riccioni G., D’Orazio N. Marine carotenoids against oxidative stress: effects on human health. Marines Drugs, 2015, 13(10): 6226-6246 CrossRef
  13. Krinsky N.I., Johnson E.J. Carotenoid actions and their relation to health and disease. Mol. Aspects Med., 2005,26(6): 459-516 CrossRef
  14. García E.F., Lérida I.C., Galán M.J., Fernández J.G., Gálvez A.P., Méndez D.H. Carotenoids bioavailability from foods: from plant pigments to efficient biological activities. Food Research International,2012, 46(2): 438-450 CrossRef
  15. Bakan E., Akbulut Z.T., Inanç A.L. Carotenoids in foods and their effects on human health. Acad. Food J., 2014, 12(2): 61-68.
  16. Tapiero H., Townsend D.M., Tew K.D. The role of carotenoids in the prevention of human pathologies. Biomedicine & Pharmacotherapy, 2004,58(2): 100-110 CrossRef
  17. Tavani A., Gallus S., Neqri E., Parpinel M., La Vecchia C. Dietary intake of carotenoids and retinol and the risk of myocardial infarction in Italy. Free Radical Research, 2006, 40(6): 659-664 CrossRef
  18. Ito Y., Kurata M., Suzuki K., Hamajima N., Hishida H., Aoki K. Cardiovascular disease mortality and serum carotenoid levels: a Japanese population-based follow-up study. J. Epidemiol., 2006,16(4): 154-160.
  19. Buijsse B., Feskens E.J., Schlettwein-Gsell D., Ferry M., Kok F.J., Kromhout D., de Groot L.C. Plasma carotene and alpha-tocopherol in relation to 10-y all-cause and cause-specific mortality in European elderly: the survey in Europe on nutrition and the elderly, a concerted action (SENECA). The American Journal of Clinical Nutrition, 2005,82(4): 879-886 CrossRef
  20. Kabagambe E.K., Furtado J., Baylin A., Campos H. Some dietary and adipose tissue carotenoids are associated with the risk of nonfatal acute myocardial infarction in Costa Rica. The Journal of Nutrition, 2005,135(7): 1763-1769 CrossRef
  21. Saksonova E.O. Rossiiskii meditsinskii zhurnal, 2005, 13(2): 124-129 (in Russ.).
  22. Kijlstra A., Tian Y., Kelly E.R., Berendschot T.T. Lutein: more than just a filter for blue light. Progress in Retinal and Eye Research, 2012,31(4): 303-315 CrossRef
  23. Ham W.T., Mueller H.A., Ruffolo J.J., Millen J.E., Cleary S.F., Guerry R.K., Guerry D. Basic mechanisms underlying the production of photochemical lesions in the mammalian retina. Current Eye Research, 1984,3(1): 165-174 CrossRef
  24. Khachik F., Bernstein P.S., Garland D.L. Identification of lutein and zeaxanthin oxidation products in human and monkey retinas. Investigative Ophthalmology & Visual Science, 1997,38(9): 1802-1811.
  25. Chitchumroonchokchai C., Bomser J.A., Glamm J.E., Failla M.L. Xanthophylls and alpha-tocopherol decrease UVB-induced lipid peroxidation and stress signaling in human lens epithelial cells. The Journal of Nutrition, 2004, 134(12): 3225-3232 CrossRef
  26. Lessin W.J., Catigani G.I., Schwartz S.J. Quantification of cis-trans isomers of provitamin A carotenoids in fresh and processed fruits and vegetables. J. Agric. Food Chem., 1997, 45(10): 3728-3732 CrossRef
  27. Southon S., Faulks R. Carotenoids in food: bioavailability and functional benefits. In: Phytochemical functional foods. I. Johnson, G. Williamson (eds.). CRC Press, Boca Raton, Boston-NY-Washington, DC, 2003: 107-127.
  28. Olson J.A. Absorption, transport, and metabolism of carotenoids in humans. Pure and Applied Chemistry, 1994, 66(5): 1011-1016 CrossRef
  29. Hencken H. Chemical and physiological behavior of feed carotenoids and their effects on pigmentation. Poultry Science, 1992, 71(4): 711-717 CrossRef
  30. Schaeffer J.L., Tyczkowski J.K., Parkhurst C.R., Hamilton P.B. Carotenoid composition of serum and egg yolks of hens fed diets varying in carotenoid composition. Poultry Science, 1988, 67(4): 608-614 CrossRef
  31. Matsufuji H., Nakamura H., Chino M., Takeda M. Antioxidant activity of capsanthin and the fatty acid esters in paprika (Capsicum annuum). J. Agric. Food Chem., 1998, 46(9): 3468-3472 CrossRef
  32. van het Hof K.H., West C.E., Weststrate J.A., Hautvast J.G. Dietary factors that affect the bioavailability of carotenoids. The Journal of Nutrition, 2000, 130(3): 503-506 CrossRef
  33. de Pee S., West C.E., Permaesih D., Muhilal S.M., Hautvast J. Orange fruit is more effective than are dark-green, leafy vegetables in increasing serum concentrations of retinol and β-carotene in schoolchildren in Indonesia. The American Journal of Clinical Nutrition, 1998, 68(5): 1058-1067 CrossRef
  34. Rock C.L. Carotenoids: biology and treatment. Pharmacology & Therapeutics, 1997, 75: 185-197 CrossRef
  35. Paetau I., Chen H., Goh N., White W.S. Interactions in the postprandial appearance of β-carotene and canthaxanthin in plasma triacylglycerol-rich lipoproteins in humans. The American Journal of Clinical Nutrition, 1997, 66(5): 1133-1143 CrossRef
  36. Kostic D., White W.S., Olson J.A. Intestinal absorption, serum clearance, and interactions between lutein and β-carotene when administered to human adults in separate or combined oral doses. The American Journal of Clinical Nutrition, 1995, 62(3): 604-610 CrossRef
  37. Chung H.-Y., Rasmussen H.M., Johnson E.J. Lutein bioavailability is higher from lutein-enriched eggs than from supplements and spinach in men. The Journal of Nutrition, 2004, 134(8): 1887-1893 CrossRef
  38. Handelman G.J., Nightingale Z.D., Lichtenstein A.H., Schaefer E.J., Blumberg J.B. Lutein and zeaxanthin concentrations in plasma after dietary supplementation with egg yolk. The American Journal of Clinical Nutrition, 1999, 70(2): 247-251 CrossRef
  39. Sahoo A., Jena B. Designer egg and meat through nutrient manipulations. Journal of Poultry Science and Technology, 2014, 2(3): 38-47.
  40. Deineka L.A., Shaposhnikov A.A., Vostrikova S.M., Deineka V.I. Nauchnye vedomosti Belgorodskogo gosudarstvennogo universiteta. Seriya Estestvennye nauki, 2007, 5(36), vyp. 5: 133-138 (in Russ.).  
  41. Tancharoenrat P., Ravindran V., Zaefarian F., Ravindran G. Influence of age on the apparent metabolisable energy and total tract apparent fat digestibility of different fat sources for broiler chickens. Animal Feed Science and Technology, 2013, 186(3-4): 186-192 CrossRef
  42. Hamilton P.B. The use of high-performance liquid chromatography for studying pigmentation. Poultry Science, 1992, 71(4): 718-724 CrossRef
  43. Kuz'minova E.V. Farmakologiya i primenenie karotinoidov v veterinarii i zhivotnovodstve. Avtoreferat doktorskoi dissertatsii [Pharmacology of carotenoids and their use in veterinary medicine and animal husbandry. DSc Thesis]. Krasnodar, 2007 (in Russ.).  
  44. Karadas F., Grammenidis E., Surai P.F., Acamovic T., Sparks N.H. Effects of carotenoids from lucerne, marigold and tomato on egg yolk pigmentation and carotenoid composition. British Poultry Science, 2006, 47(5): 561-566 CrossRef
  45. Fisinin V.I., Shtele A.L. Ptitsa i ptitseprodukty, 2008, 5: 58-60 (in Russ.).  
  46. Fisinin V.I., Shtele A.L. Ptitsa i ptitseprodukty, 2008, 6: 50-52 (in Russ.).  
  47. Breithaupt D.E. Modern application of xanthophylls in animal feeding — a review. Trends in Food Science & Technology, 2007, 18(10): 501-506 CrossRef
  48. Singh V.P., Pathak V., Akhilesh K.V. Modified or enriched eggs: a smart approach in egg industry: a review. American Journal of Food Technology, 2012, 7(5): 266-277 CrossRef
  49. Loetscher Y., Kreuzer M., Messikommer R.E. Utility of nettle (Urtica dioica) in layer diets as a natural yellow colorant for egg yolk. Animal Feed Science and Technology, 2013, 186(3-4): 158-168 CrossRef
  50. Surai P.F., Speake B.K., Sparks N.H.C. Carotenoids in avian nutrition and embryonic development. 1. Absorption, availability and levels in plasma and egg yolk. The Journal of Poultry Science, 2001, 38(1): 1-27 CrossRef
  51. Vladimirov V.L., Shaposhnikov A.A., Deineka D.V., Vostrikova S.M., Deineka V.I. Doklady RASKHN, 2005, 6: 46-48 (in Russ.).  
  52. Vostrikova S.M., Tret'yakov M.Yu., Deineka V.I., Deineka L.A., Shaposhnikov A.A. Nauchnye vedomosti Belgorodskogo gosudarstvennogo universiteta. Seriya Estestvennye nauki, 2011, 9(104), vyp. 15/2: 221-227 (in Russ.).  
  53. Nys Y. Dietary carotenoids and egg yolk coloration — a review. Archiv fur Geflugelkunde, 2000, 64(2): 45-54.
  54. Moreno J.A., Díaz-Gómez J., Nogareda C., Angulo E., Sandmann G., Portero-Otin M., Serrano J.C.E., Twyman R.M., Capell T., Zhu Ch., Christou P. The distribution of carotenoids in hens fed on biofortified maize is influenced by feed composition, absorption, resource allocation and storage. Sci. Rep., 2016, 6: 35346 CrossRef
  55. Abdel-Aal E.S.M., Akhtar H., Zaheer Kh., Ali R. Dietary sources of lutein and zeaxanthin carotenoids and their role in eye health. Nutrients, 2013, 5(4): 1169-1685 CrossRef
  56. Laudadio V., Ceci E., Lastella N.M.B., Introna M., Tufarelli V. Low-fiber alfalfa (Medicago sativa L.) meal in the laying hen diet: effects on productive traits and egg quality. Poultry Science, 2014, 93(7): 1868-1874 CrossRef
  57. Alagawany M., Farag M.R., Dhama K., Patra A. Nutritional significance and health benefits of designer eggs. World's Poultry Science Journal, 2018, 74(2): 317-330 CrossRef
  58. Egorov I.A., Lukashenko V.S., Borisova T.V., Dyadichkina L.F., Golovachev D.E., Kalashnikov A.I., Khamidullin T.N., Semenova E.A., Semenova E.A., Kuznetsov A.S. Ispol'zovanie promyshlennykh preparatov karotinoidov firmy BASF v kormlenii ptitsy: metodicheskie rekomendatsii /Pod redaktsiei V.I. Fisinina, Sh.A. Imangulova [The use of BASF carotenoids in poultry feeding: guidelines. V.I. Fisinin, Sh.A. Imangulov (eds.)]. Sergiev Posad, 2002 (in Russ.).   
  59. Marounek M., Skřivan M., Englmaierová M. Comparison of natural and synthetic carotenoids: Effection yolk colour and oxidative stability of yolk lipids. International Journal of Advances in Science Engineering and Technology, 2016, 5: 53-55.
  60. EFSA (European Food Safety Authority). Scientific opinion on the re-evaluation of paprika extract (E 160c) as a food additive. EFSA J., 2015, 13(12): 4320 CrossRef
  61. Leeson S., Caston L. Enrichment of eggs with lutein. Poultry Science, 2004, 83(10): 1709-1712 CrossRef
  62. Lokaewmanee K., Yamauchi K., Komori Ts., Saito K. Enhancement of yolk color in raw and boiled egg yolk with lutein from marigold flower meal and marigold flower extract. The Journal of Poultry Science, 2011, 48(1): 25-32 CrossRef
  63. Grashorn M., Steinberg W. Deposition rates of canthaxanthin in egg yolks. Archiv fur Geflugelkunde, 2002, 66(6): 258-262.
  64. Damaziak K., Marzec A., Riedel J., Szeliga J., Koczywąs E., Cisneros F., Michalczuk M., Lukasiewicz M., Gozdowski D., Siennicka A., Kowalska H., Niemiec J., Lenart A. Effect of dietary canthaxanthin and iodine on the production performance and egg quality of laying hens. Poultry Science, 2018, 97(11): 4008-4019 CrossRef
  65. Englmaierová M., Skřivan M., Bubancová I. A comparison of lutein, spray-dried Chlorella, and synthetic carotenoids effects on yolk colour, oxidative stability, and reproductive performance of laying hens. Czech J. Anim. Sci., 2013, 58(9): 412-419 CrossRef
  66. Skřivan M., Englmaierová M., Skřivanová E., Bubancová I. Increase in lutein and zeaxanthin content in the eggs of hens fed marigold flower extract. Czech J. Anim. Sci., 2015, 60(3): 89-96 CrossRef
  67. Skřivan M., Marounek M., Englmaierová M., Skřivanová E. Effect of increasing doses of marigold (Tagetes erecta) flower extract on eggs carotenoids content, colour and oxidative stability. J. Anim. Feed Sci., 2015, 25(1): 58-64 CrossRef
  68. Spada F.P., Selani M.M., Coelho A.A.D., Savino V.J.M., Rodella A.A., Souza M.C., Fischer F.S., Lemes D.E.A., Canniatti-Brazaca S.G. Influence of natural and synthetic carotenoids on the color of egg yolk. Scientia Agricola, 2016, 73(3): 234-242 CrossRef
  69. Altuntaş A., Aydin R. Fatty acid composition of egg yolk from chickens fed a diet including marigold (Tagetes erecta L.). Journal of Lipids, 2014, Article ID 564851 CrossRef
  70. Guseva T.S. Biokhimicheskii status kur-nesushek i kachestvo yaits pri ispol'zovanii v ikh ratsione karotinoidov rastitel'nogo i mikrobiologicheskogo sinteza. Kandidatskaya dissertatsiya [Biochemical status and egg quality of laying hens in using dietary carotenoids of plant and microbial origin. PhD Thesis]. Belgorod, 2008 (in Russ.).    
  71. Gao Y.-Y., Xie Q.-M., Ma J.Y., Zhang X.-B., Zhu J.-M., Shu D.-M., Sun B.-L., Jin L., Bi Y.-Z. Supplementation of xanthophylls increased antioxidant capacity and decreased lipid peroxidation in hens and chicks. British Journal of Nutrition, 2013, 109: 977-983 CrossRef
  72. Zahroojian N., Moravej H., Shivazad M. Comparison of marine algae (Spirulina platensis) and synthetic pigment in enhancing egg yolk colour of laying hens. British Poultry Science, 2011, 52(5): 584-588 CrossRef
  73. Akshaya H.R., Banyal N., Singh K.P., Saha S., Panwar S., Bharadwaj C. Standardization of storage conditions of marigold (Tagetes sp.) petal extract for retention of carotenoid pigments and their antioxidant activities. Indian Journal of Agricultural Sciences, 2017,87(6): 765-775.
  74. Boon C.S., McClements D.J., Weiss J., Decker E.A. Factors influencing the chemical stability of carotenoids in foods. Critical Reviews in Food Science and Nutrition, 2010, 50(6): 515-532 CrossRef
  75. Toti E., Chen C.-Y. O., Maura Palmery M., Valencia D.V., Peluso I. Non-provitamin A and provitamin A carotenoids as immunomodulators: recommended dietary allowance, therapeutic index, or personalized nutrition? Oxid. Med. Cell Longev., 2018; Article ID 4637861 CrossRef







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