Influence of Natural Pigments on Egg Quality and Yolk Colour Intensity - A Review
Keywords:
carotenoids, laying hens, marigold flowers, paprika powder extract, yolk colourAbstract
Eggs are a great source of animal protein that are rich in fatty acids, selenium, B vitamins, provitamin A, amino acids, and folic acid. Egg quality and yolk colour are important attributes for consumers. They associate a higher intensity colour of yolk with a healthy egg which its rich in nutrients. Because hens are unable to synthesise pigments, they must come from feed mixtures. Furthermore, the synthetic colourants are added to laying hens diets to improve the yolk colour intensity. However, human health received more attention in the last time, so, the consumers are attracted by natural-coloured eggs. Carotenoids are the most numerous and widespread group of pigments in nature. They are a class of widely distributed pigments that include red, yellow, and orange colour. Numerous studies have examined the use of carotenoids, particularly yellow carotenoids, in animal feed, which aid to make egg yolks more orange in colour. They are found in different plants, microalgae, bacteria, fungi and have various biological functions, including increasing production, antioxidant, anti-inflammatory, antibacterial and immunomodulator role. For practical purposes, the cost of carotenoids from natural sources needs to be considered. The objective of this review was to summarise the recent findings in available literature data on the supplementation with natural pigments based on marigold and calendula flowers and paprika extracts for egg quality and yolk colour pigmentation which are preferred over pigments of synthesis, due to their costs and biodisponibility.
References
Pal, M., and Molnár, J., The role of eggs as an important source of nutrition in human health. International Journal of Food Science and Agriculture, 2021, 5, 180-182.
Titcomb, T. J., Kaeppler, M. S., Cook, M. E., Simon, P. W., and Tanumihardjo, S. A., Carrot leaves improve color and xanthophyll content of egg yolk in laying hens but are not as effective as commercially available marigold fortificant, Poultry Science, 2019, 98(10), 5208-5213.
Applegate, E. Introduction: nutritional and functional roles of eggs in the diet. Journal of the American College of Nutrition, 2000, 19(sup5), 495S-498S.
Omri, B., Amraoui, M., Tarek, A., Lucarini, M., Durazzo, A., Cicero, N., Santini, A., and Kamoun, M. Arthrospira platensis (Spirulina) supplementation on laying hens’ performance: Eggs physical, chemical, and sensorial qualities. Foods, 2019, 8(9), 386.
Grashorn, M., Feed additives for influencing chicken meat and egg yolk color. In Handbook on natural pigments in food and beverages, 2016, (pp. 283-302). Woodhead Publishing.
Schweiggert, R.M., Carle, R., Carotenoid deposition in plant and animal foods and its impact on bioavailability, Crictical Reviews in Food Science and Nutrition, 2015, http://dx.doi.org/10.1080/10408398.2015.1012756.
Surai, P. F., Speake, B. K., and 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.
Landrum, J.T., Bone, R.A., Lutein, zeaxanthin, and the macular pigment. Archives of Biochemistry and Biophysics, 2001, 385, 28–40.
Grashorn, M.A., Steinberg, W., Blanch, A., Effects of canthaxanthin and saponified capsanthin/capsorubin in layer diets on yolk pigmentation in fresh and boiled eggs. XXI World’s Poultry Congress, Montreal, Canada, August, 2000, 20–24
Hernandes, J.-M., Beardswort, P.M., Weber, G., Egg quality – meeting consumer expectations, International Poultry Production, 2005, 13 (3): 20–23
Beardswort, P.M., Hernandes, J.-M., Yolk colour – an important egg quality attribute, International Poultry Production, 2004, 12 (5): 17–18
Hasin, B. M., Ferdaus, A. J. M., Islam, M. A., Uddin, M. J., and Islam, M. S., Marigold and orange skin as egg yolk color promoting agents, International Journal of Poultry Science, 2006, 5(10), 979-987
Karadas, F., Grammenidis, E., Surai, P.F., Acamovic, T., and Sparks, N.H.C., Effects of carotenoids from lucerne, marigold and tomato on egg yolk pigmentation and carotenoid composition, British Poultry Science, 2006, Vol. 47, N. 5, pp. 561—566
Parker, R.S., Absorption, metabolism, and transport of carotenoids, The FASEB Journal, 1996, 10(5), 542-551.
Pérez-Vendrell, A.M., Hernandez, J.M., Llaurado, L., Schierle, J. and Brufau, J., Influence of source and ratio of xanthophyll pigments on broiler chicken pigmentation and performance, Poultry Science, 2001, 80(3), 320-326
Faehnrich, B., Lukas, B., Humer, E. and Zebeli, Q., Phytogenic pigments in animal nutrition: Potentials and risks, Revisão, Journal Science Food Agriculture, 2016, 96, 420-1430
Vinus, R.D., Dalal, R., Sheoran, N., Maan, N.S., and Tewatia, B.S., Potential benefits of herbal supplements in poultry feed: A review, Journal Pharmacy Inn., 2018, 7, 651-656
Curvelo, E.R., Geraldo, A., Silva, L.M., Antos, T.A., Filho, J.A.V., Pinto, E.R.A., Oliveira, M.L.R., and Ferreira, C.B., Níveis de inclusão de extrato de urucum e açafrão em dietas para poedeiras semipesadas e seus efeitos sobre o desempenho e coloração da gema dos ovos, II Semana de Ciência e Tecnologia do IFMG campus Bambuí II Jornada Científica; Bambuí, 2009, Minas Gerais. Brasil
Kassis, N., Drake, S.R., Beamer, S.K., Matak, K.E., Jaczynski, J., Development of nutraceutical egg products with omega-3-rich oils, LWT-Food Science and Technology, 2010, 43(5), 777-783, [Google Scholar] [CrossRef]
Skrivan, M., Englamaierová, M., The deposition of carotenoids and α-tocopherol in hen eggs produced under a combination of sequential feeding and grazing, Animal Feed Science Technology, 2014, 190, 79–86, [Google Scholar] [CrossRef]
Rakonjac, S., Bogosavljevic-Boskovic, S., Pavlovski, Z., Skrbic, Z., Doskovic, V., Petrovic, M.D., Petricevic, V., Laying hen rearing Systems: A review of Chemicals composition and hygienic conditions of eggs, World Poultry Science Journal, 2014, 70, 151–163. [Google Scholar] [CrossRef]
Kelly, E.R., Plat, J., Haenen, G.R.M.M., Kijlstra, A., Berendschot, T.T.J.M., The effect of modified eggs and egg-yolk based bevegare on serum lutein and zeaxanthin concentrations and macular pigment optical density: Results from a randomized trial, PLoS One 2014, 9, e92659. [Google Scholar] [CrossRef] [PubMed]
Bovier, E.R., Renzi, L.M., Hammond, B.R., A doucle-blind, placebo-controlled study on the effects of lutein and zeaxathin on neural processing speed and efficiency, PLoS One, 2014, 9, e108178. [Google Scholar] [CrossRef] [PubMed]
Spasevski, N., Tasić, T., Vukmirović, Ð., Banjac, V., Rakita, S., Lević, J., and Ðuragić, O., Effect of different levels of marigold and paprika on egg production and yolk colour. Archiva Zootechnica, 2017, 20(2), 51-57
Berkhoff, J., Alvarado-Gilis, C., Keim, J. P., Alcalde, J. A., Vargas-Bello-Pérez, E., and Gandarillas, M., Consumer preferences and sensory characteristics of eggs from family farms, Poultry science, 2020, 99(11), 6239-6246.
Mahmoud, K.Z., Saad, M., Gharaibeh, Hana., Zakaria, A., Amer, M., Qatramiz. Garlic (Allium sativum) Supplementation: Influence on Egg Production, Quality, and Yolk Cholesterol Level in Layer Hens. Asian-Australasian Journal of Animal Sciences, 2010, 23(11), 1503-1509
Meliandasari, D., Dwiloka, B., and Suprijatna, E. Optimasi Daun Kayambang (Salvinia molesta) untuk Penurunan Kolesterol Daging dan Peningkatan Kualitas Asam Lemak Esensial. Jurnal Aplikasi Teknologi Pangan, 2015, 4, 1
Abeyrathne, E.D.N.S., Lee, H.Y., Ahn, D.U., Egg white proteins and their potential use in food processing or as nutraceutical and pharmaceutical agents—A review. Poultry Science, 2013, 92, 3292–3299. [Google Scholar] [CrossRef] [PubMed]
Leeson, S., and Caston, L., “Enrichment of Eggs with Lutein.”, Poultry Science, 2004, 83: 1709–1712. doi:10.1093/ps/83.10.1709
Zaheer, K., “Hen Egg Carotenoids (Lutein and Zeaxanthin) and Nutritional Impacts on Human Health: A Review.” Cyta - Journal of Food, 2017, 15 (3): 474–487. doi:10.1080/19476337.2016.1266033
Andersen, C. J., “Bioactive Egg Components and Inflammation.”Nutrients, 2015, 7: 7889–7913. doi:10.3390/nu7095372
Gammone, M. A., Riccioni, G., and D’orazio, N., “Carotenoids: Potential Allies of Cardiovascular Health?” Food and Nutrition Research, 2015, 59: 26762. doi:10.3402/fnr.v59.26762
Fiedor, J., and Burda., K., “Potential Role of Carotenoids as Antioxidants in Human Health and Disease.” Nutrients, 2014, 6: 466–488. doi:10.3390/nu6020466
Calabrese, V., Cornelius, C., Mancuso, C., Lentile, R., Stella, A. G., and Butterfield, D. A., “Redox Homeostasis and Cellular Stress Response in Aging and Neurodegeneration.” Methods in Molecular Biology, 2010, 610: 285–308. doi:10.1007/978-1-60327-029-8_17
Nolan, J., Loskutova, M. E., Howard, A., Mulcahy, R., Moran, R., Stack, J., and Beatty, S., “The Impact of Supplemental Macular Carotenoids in Alzheimer’s Disease: A Randomized Clinical Trial.” Journal of Alzheimer’s Disease, 2015, 44: 1157–1169. doi:10.3233/JAD-142265
Mares-Perlman, J. A., Millen, A. E., Ficek, T. L., and Hankinson, S. E., “The Body of Evidence to Support a Protective Role for Lutein and Zeaxanthin in Delaying Chronic Disease, Overview”The Journal of Nutrition, 2002, 132: 518S–524S. doi:10.1093/jn/132.9.2514
Salajegheh, M. H., Ghazi, S., Mahdavi, R., and Mozafari, O., Effects of different levels of dried tomato pomace on performance, egg quality and serum metabolites of laying hens. African journal of biotechnology, 2012, 11(87), 15373-15379
Seidavi, A.R., Azizi, M., Ragni, M., Laudadio, V., Tufarelli, V., Practical applications of agricultural wastes in poultry feeding in Mediterranean and Middle East regions. Part 2: tomato, olive, date, sunflower wastes. World’s Poultry Science Journal, 2018, 74(3):443–452
Jafari, M., Pirmohammadi, R.R., Bampidis, V., The use of dried tomato pulp in diets of laying hens. International Journal Poultry Science, 2006, 5:618-622
Dotas, D., Zamanidis, S., Balios, J., Effect of dried tomato pulp on the performance and egg traits of laying hens. British Poultry Science, 1999, 40, 695-697
Xue, F., Li, C., and Pan, S., In vivo antioxidant activity of carotenoid powder from tomato byproduct and its use as a source of carotenoids for egg-laying hens.
Story, E.N., Kopec, R.E., Schwartz, S. J., and Harris, G. K., An update on the health effects of tomato lycopene, Annual review of food science and technology, 2010, 1, 189-210
Nuraini, Mirzah and Djulardi, A., Extract carotenoid from yellow of flower and tuber to produced egg low of cholesterol. Research Report, Competention Grand DIKTI, LPPM Andalas University, Indonesia, 2016
Vahed, R., Kermanshahi, H., Nasiri Moghaddam, H., Hassanabadi, A., and Behesthti Moghaddam, S., Effect of different levels of marigold (Calendula officinalis) oil extract on performance, blood parameters and immune response of broiler chickens challenged with CCl4. Iranian Journal of Animal Science Research, 2016, 7, 447-455
Frum, A., HPLC determination of polyphenols from Calendula officinalis L. flowers. Acta Universitatis Cibiniensis Series E: Food Technology, 2017, 21(2), 97-101
Demasi, S., Caser, M., Donno, D., Enri, S.R., Lonati, M. and Scariot, V., Exploring wild edible flowers as a source of bioactive compounds: New perspectives in horticulture. Folia Horticulturae, 2021, 33(1), 1-22
Kljak, K., Carovič- Stanko, K., Kos, J., Janečic, Zl., Kiš, G., Duvnjak, M., Safner, T. and Bedekoviċ, D., Plants carotenoids as pigment sources in laying hens diets: Effect on egg yolk color, carotenoid content, oxidative stability and sensory properties of eggs. Foods, 2021, 10(4), 721. https://doi.org/10.3390/foods10040721
Göcer, M., Yanar, M., Kumlu, M., Yanar, Y., The effects of red pepper, marigold flower, and syntheticastaxanthin on pigmentation, growth, and proximate composition of Penaeus semisulcatus. Turkish Journal of Veterinary and Animal Science, 2006, v.30, n.4, p.359365
Jung, E.K., Clark, R.M., Park, J., Lee, J., and Fernandez M.L., Lutein decreases oxidative stress and inflammation in liver and eyes of guinea pigs fed a hypercholesterolemic diet. Nutrition Research and Practice, 2012, 6, 113-119.
Čolović, D., Rakita, S., Spasevski, N., Tasić, T., Popović, S., Duragić, O., and Čolović, R., Enhancement of egg yolk colour with paprika and marigold flower as source of natural pigments. In: “Feed Technology”, Proceedings of XVII International Symposium, 25-27 October 2016, Novi Sad, Serbia, 2016, 1-46.
Doreau, M., BAUCHART, D., CHILLIARD, Y., Enhancing fatty acid composition of milk and meat through animal feeding. Animal Production Science, 2010, 51, 19-29
Guroy, B., Sahin, I., Mantoglu, S., Kayali, S., Spirulina as a natural carotenoid source on growth, pigmentation and reproductive performance of yellow tail cichlid Pseudotropheus acei. Aquaculture International, 2012, 20, 869878.
Coelho, D.F.M., Alfaia, C.M.R.P.M., Assunção, J.M.P., Costa, M., Pinto, R.M.A., de Andrade Fontes, C.M.G., Lordelo, M.M., Prates, J.A.M., Impact of dietary Chlorella vulgaris and carbohydrate-active enzymes incorporation on plasma metabolites and liver lipid composition of broilers. BMC Veterinary-Research, 2021, 17, 229. [Google Scholar] [CrossRef]
Hyrslova, I., Krausova, G., Smolova, J., Stankova, B., Branyik, T., Malinska, H., Huttl, M., Kana, A., Doskocil, I., Curda, L., Prebiotic and Immunomodulatory Properties of the Microalga Chlorella vulgaris and Its Synergistic Triglyceride-Lowering Effect with Bifidobacteria. Fermentation 2021, 7, 125. [Google Scholar] [CrossRef]
Zheng, L., Oh, S.T., Jeon, J.Y., Moon, B.H., Kwon, H.S., Lim, S.U., Kang, C.W., The dietary effects of fermented Chlorella vulgaris (CBT®) on production performance, liver lipids and intestinal microflora in laying hens. Asian-Australasian Journal of Animal Sciences,2012, 25, 261. [Google Scholar] [CrossRef] [PubMed]
Marín, A., Ferreres, F., Tomás-Barberán, F.A., Gil, M.I., Characterization and quantitation of antioxidant constituents of sweet pepper (Capsicum annuum L.). Journal Agriculture Food Chemistry, 2004, 52, 3861-3869
Hamilton, P.B., Tirado, J.F., Garcia-Hernandez, F., Deposition in egg yolks of the carotenoids from saponified and unsaponified oleoresin of red pepper (Capsicum annuum). Poultry Science, 1990, 69, 462-470
Barbero, G.F., Liazid, A., Palma, M., Barroso, C.G., Ultrasound-assisted extraction of capsaicinoids from peppers. Talanta, 2008, 75, 1332-1337
Al-Kassie, G.A.M., Mamdooh, A.M.A., Saba, J.A., The effects of using hot red pepper as a diet supplement on some performance traits in broiler. Pakistan Journal Nutrition, 2011, 9, 842-845
Hernandez, J.M., Blanch, A., Consumers often associate colour with product quality. World Poultry 2000, 16, 25-26
Li, H., Jin, L., Wu, F., Thacker, P., Li, X., You, J., Wang, X., Liu, S., Li, S., Xu. Y., Effect of red pepper (Capsicum frutescens) powder or red pepper pigment on the performance and egg yolk color of laying hens. Asian-Australasian Journal of Animal Sciences 2012, 25, 1605-1610
Sözcü, A., Effects of supplementing layer hen diet with red pepper (Capsicum annuum L.) powder as natural yolk colourant on laying performance, pigmentation of yolk, egg quality and serum immunoglobulin levels. Journal of Poultry Research, 2019, 16(2), 80-85
Karadas, F., Grammenidis, E., Surai, P.F., Acamovic, T., and Sparks, N.H.C., Effects of carotenoids from lucerne, marigold and tomato on egg yolk pigmentation and carotenoid composition. British Poultry Science, 2006, Vol. 47, N. 5, pp. 561—566
European Food Safety Authority, Opinion of the scientific panel on food additives and nutrient sources added to food (ANS) on request of the European commission related to the reevaluation of lutein (E 161b) as a food additive, 2010, EFSA Journal 1678.
Tufarelli, V., Baghban-Kanani, P., Azimi-Youvalari, S., Hosseintabar-Ghasemabad, B., Slozhenkina, M., Gorlov, I., Viktoronova, F.M., and Laudadio, V., Effect of dietary flaxseed meal supplemented with dried tomato and grape pomace on performance traits and antioxidant status of laying hens. Animal Biotechnology, 2022, 33(7), 1525-1532
Xue, F., Li, C., PAN, S., In vivo antioxidant activity of carotenoid powder from tomato by-product and its use as a source of carotenoids for egg-laying hens. Food Functional 2013, 4, 610-617
Akdemir, F., Orhan, C., Sahin, N., Hayirli, A., Tomato powder inlaying hen diets: effects on concentrations of yolk carotenoids and lipid peroxidation. British Poultry Science, 2012, 53: 675–680
Salajegheh, M.H., Ghazi, S., Mahdavi, R., and Mozafari, O., Effects of different levels of dried tomato pomace on performance, egg quality and serum metabolites of laying hens. African journal of biotechnology, 2012, 11(87), 15373-15379
Maia, K. M., Grieser, D. O., Ton, A. P. S., Aquino, D. R., Paulino, M. T. F., Toledo, J. B., and Marcato, S. M., Performance and egg quality of light laying hens fed with canthaxanthin and marigold flower extract. South African Journal of Animal Science, 2022, 52(4), 433-443
Grčević, M., Kralik, Z., Kralik, G., and Galović, O., Effects of dietary marigold extract on lutein content, yolk color and fatty acid profile of omega‐3 eggs. Journal of the Science of Food and Agriculture, 2019, 99(5), 2292-2299
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. Journal of Animal and Feed Sciences, 2016, 25: 58–64
Altuntaş, A., and Aydin, R., Fatty acid composition of egg yolk from chickens fed a diet including marigold (Tagetes erecta L.). Journal of lipids, 2014
Lokaewmanee, K., Yamauchi, K., Komori, T., Saito, K., Enhancement of yolk color in raw and boiled egg yolk with lutein from marigold flower meal and marigold flower extract. Japanese Journal of Poultry Science, 2011, 48: 25–32
Panaite, T. D., Cornescu, G. M., Predescu, N. C., Cismileanu, A., Turcu, R. P., Saracila, M., and Soica, C. Microalgae (Chlorella vulgaris and Spirulina platensis) as a Protein Alternative and Their Effects on Productive Performances, Blood Parameters, Protein Digestibility, and Nutritional Value of Laying Hens’ Egg. Applied Sciences, 2023, 13(18), 10451
Tufarelli, V., Baghban-Kanani, P., Azimi-Youvalari, S., Hosseintabar-Ghasemabad, B., Slozhenkina, M., Gorlov, I., Viktoronova, F.M., and Laudadio, V. Effects of horsetail (Equisetum arvense) and spirulina (Spirulina platensis) dietary supplementation on laying hens productivity and oxidative status. Animals, 2021, 11(2), 335
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: 584–588
Kim, Y.B., Park, J., Heo, Y.J., Lee, H.G., Kwon, B.Y., Joo, S.S., Kim, M., Kim, Z.-H., & Lee, K.W., Effect of Dietary Chlorella vulgaris or Tetradesmus obliquus on Laying Performance and Intestinal Immune Cell Parameters. Animals, 2023, 13(10), 1589
Moradi kor, N., Akbari, M., and Olfati, A., The effects of different levels of Chlorella microalgae on blood biochemical parameters and trace mineral concentrations of laying hens reared under heat stress condition. International Journal of Biometeorology, 2016, 60, 757-762
Englmaierova, M., Skrivan, M., Bubancova, I. A comparison of lutein and spray-dried Chlorella, and synthetic carotenoids effects on yolk colour, oxidative stability, and reproductive performance of laying hens. Czech Journal of Animal Science, 2013, 58, 412–419
Aktaran Bala, D., Matur, E., Ergul Ekiz, E., Akyazi, I., Ergen, E., Erek, M., Atmaca, G., Eseceli, H., and Keten, M., Can dried tomato and red pepper powder be used as a dietary supplement to strengthen defence systems and production performance in laying hens. European Poultry Science/Archiv für Geflügelkunde, 2020, (323)
Lokaewmanee, K., Yamauchi, K., Okuda, N., Effects of dietary red pepper on egg yolk colour and histological intestinal morphology in laying hens. Journal of Animal Physiology and Animal Nutrition, 2013, 97: 986–995