Scientific Papers. Series D. Animal Science. Vol. LXI, Number 2, 2018 ISSN 2285-5750; ISSN CD-ROM 2285-5769; ISSN Online 2393-2260; ISSN-L 2285-5750 important role in molecular processes of cell molecules, joined in a head to tail pattern membranes whose structure, properties and (Mattea, 2009; Domonkos, 2013). Structurally, SOURCES OF CAROTENOIDS AND THEIR USES stability can be modified, leading to possible carotenoids take the form of a polyene chain AS ANIMAL FEED ADDITIVES – A REVIEW beneficial effects on human health (Zaheer, that functions as a chromophore, due to 9-11 2017). conjugated double bonds and possibly Diana PASARIN, Camelia ROVINARU Out of high production and marketability terminating in rings, what determines their reasons, carotenoids are present in the animal characteristic color in the yellow to red range National Institute for Research and Development in Chemistry and Petrochemistry kingdom, playing functions such as coloring (Vershinin, 1999). The presence of different 202 Spl. Independentei, Bucharest, Romania (pets/ornamental birds and fish, mimicking), number of conjugated double bounds leades to flavoring (scents and pollination in nature), various stereoisomers abbreviated as E- and Z- Corresponding author email: [email protected] reproduction (bird feathers and finding mates; isomers, depending on whether the double development of embryos), resistance to bonds are in the trans (E) or cis (Z) Abstract bacterial and fungal diseases, immune configuration (Vincente et al., 2017). responses (lutein connected to anti- Carotenoids are synthesized by all Carotenoids are natural pigments, widely distributed in nature, synthesized by plants, algae, fungi, and phototrophic bacteria. Carotenoids have coloring power and antioxidant properties, being used as colorants for foods, cosmetics and inflammatory natural substance in poultry), as photosynthetic organisms and some non- feeds. Nowadays, a small part of industrial carotenoids is obtained from algae and plants, and the most part is well as normal development of skin and photosynthetic bacteria and fungi (Ruiz-Sola, chemically synthesized, but with high production cost. Taking into account consumer’s demand for natural compounds, mucosa. 2012). Due to length of the polyene there is an increased trend for products containing natural ingredients including those used in animal feed. Products The aim of this review is to highlight the tail, carotenoid compounds are involved in quality and animal health are influenced by carotenoids added in feed as important component in daily diet. This paper various sources of carotenoids and their capturing energy from light, absorbing reviews aspects regarding the main sources of carotenoids used as feed additives for nutritional and coloring properties and their impact on animal and human health. application in animal feed additives. This topic wavelengths, ranging from 400-550 has rarely been described in a general matter, nanometers (violet to green light), thus Key words: carotenoids, feed additives, sources of carotenoids, pigmentation. and as such we endeavor to provide an assisting in photosynthesis and causes the overview of published works on the subject. compounds to be deeply colored yellow, INTRODUCTION properties and deposition of carotenoids crucial orange, or red (Vershinin, 1999; Zakynthinos, for consumers (egg yolks and other products). DEFINITION, CHEMICAL STRUCTURE 2016). Carotenoids gained great interest lately for food In fact, as studies show, there is a strong AND CLASSIFICATION OF There have been identified over 750 naturally and feeding, as their functions related to relationship between diets/foods rich in CAROTENOIDS occurring carotenoids, biosynthesized de novo nutrition, health and wellbeing are well carotenoids and the risk reduction of various by plants, algae, fungi and bacteria (Okada et appreciated. As consumers become more and diseases. Carotenoids increase the immune Carotenoids are natural pigments, widely al., 2008), among which only 50 have more aware of the importance of natural response, are excellent antioxidants, scavenging distributed in nature, responsible for the significant biological activity for animals and instead of synthetic and artificial ingredients, and inactivating free radicals. This is why both coloring of fruits, vegetables and flowers. humans (Mezzomo et al., 2016). they tend to change preferences and replace vitamin A precursor carotenoids and the non- Carotenoids take their name from carrot Animals cannot synthesize carotenoids (Rock, products in their diets according to norms precursors ones play an important role in the (Daucus carota), which accumulates high 2009), obtaining them through dietary intake, which no longer respond to good, tasty and protection and inhibition of serious diseases as levels of these pigments in the root, being an with a few exceptions, represented by aphids affordable consumptions, yet to higher, long- cancer, atherosclerosis, cataracts, macular exception among plants (Stange, 2015). They and spiders which acquired the ability and term perspective standards (García-Chavarría degeneration, multiple sclerosis, degenerative are used as food colorants, feed supplements, genes from fungi (Moran, 2010; Nováková, and Lara-Flores, 2013; Carotenoids Market by diseases, and cardiovascular diseases for cosmetic and pharmaceutical purposes. 2012) or are produced by endosymbiotic Type, 2016; Mohiseni., 2017). (Mezzomo et al., 2016). Most carotenoids are made up of eight bacteria in whiteflies (Sloan, 2012). In this line, arguments related to the On the other hand, there is no novelty feeding condensed 5-carbon-containing isoprene Carotenoids are classified in Table 1. replacement of synthetic carotenoids with animals with carotenoids, these have always natural ones in case of animal feed additives been part of their daily diet. Astaxanthin is the Table 1. Classification of carotenoids lay in multiple health impact through major carotenoid used for pigmentation of fish Classification Major classes Structure Examples Attribute References environment and animal to human health (Kaur muscle, mainly salmons (Bhosale, 2004). Beta- criteria and Shah, 2017). carotene, lycopene, and lutein increase growth Chemical Carotenes Hydrocarbons (constituted α-carotene -color range from pale Delgado-Vargas, 2000 As such, many researches have been directed to performance of animals and quality of structure by carbon and hydrogen) β- carotene yellow, bright orange to Tinoi, 2005 in-depth knowledge on carotenoid sources, pigmented products (Nelis and De Leenheer, that can be cyclized at one γ-carotene deep red Aizawa, 2007 or both ends of the molecule lycopene -maintains eye health Kaur and Shah, 2017 especially natural ones, for their use as animal 1991). Animals and humans are unable to torulene -does not color the fish feed additives, so as to benefit from their synthesize carotenoids, they have to meet their Oxycarotenoids Oxygenated hydrocarbon lutein, zeaxanthin, β- -generally yellow in color Delgado-Vargas, functions including skin and tissues daily nutritional needs from the products (xanthophylls) derivatives that contain at cryptoxanthin, -antiallergic and anti- 2000; pigmentation (especially when it comes to ingested (Priyadarshani and Rath, 2012). least one oxygen atom as astaxanthin, cancerous actions Bhosale and Berstein, hydroxyl groups, keto, canthaxanthin, -can color the fish 2005; animals/birds grown in captivity), as growth Carotenoids, as part of the nutrients in the feed, epoxy, methoxy, or violaxanthin,neoxanthin, -colors egg yolks Kushwaha et al, 2014. promoters (in terms of mass production), for support animal health and animal products carboxylic acid antheraxanthin reproduction and survival goals, sensory quality (Amaya et al., 2014). They have an 74 important role in molecular processes of cell molecules, joined in a head to tail pattern membranes whose structure, properties and (Mattea, 2009; Domonkos, 2013). Structurally, SOURCES OF CAROTENOIDS AND THEIR USES stability can be modified, leading to possible carotenoids take the form of a polyene chain AS ANIMAL FEED ADDITIVES – A REVIEW beneficial effects on human health (Zaheer, that functions as a chromophore, due to 9-11 2017). conjugated double bonds and possibly Diana PASARIN, Camelia ROVINARU Out of high production and marketability terminating in rings, what determines their reasons, carotenoids are present in the animal characteristic color in the yellow to red range National Institute for Research and Development in Chemistry and Petrochemistry kingdom, playing functions such as coloring (Vershinin, 1999). The presence of different 202 Spl. Independentei, Bucharest, Romania (pets/ornamental birds and fish, mimicking), number of conjugated double bounds leades to flavoring (scents and pollination in nature), various stereoisomers abbreviated as E- and Z- Corresponding author email: [email protected] reproduction (bird feathers and finding mates; isomers, depending on whether the double development of embryos), resistance to bonds are in the trans (E) or cis (Z) Abstract bacterial and fungal diseases, immune configuration (Vincente et al., 2017). responses (lutein connected to anti- Carotenoids are synthesized by all Carotenoids are natural pigments, widely distributed in nature, synthesized by plants, algae, fungi, and phototrophic bacteria. Carotenoids have coloring power and antioxidant properties, being used as colorants for foods, cosmetics and inflammatory natural substance in poultry), as photosynthetic organisms and some non- feeds. Nowadays, a small part of industrial carotenoids is obtained from algae and plants, and the most part is well as normal development of skin and photosynthetic bacteria and fungi (Ruiz-Sola, chemically synthesized, but with high production cost. Taking into account consumer’s demand for natural compounds, mucosa. 2012). Due to length of the polyene there is an increased trend for products containing natural ingredients including those used in animal feed. Products The aim of this review is to highlight the tail, carotenoid compounds are involved in quality and animal health are influenced by carotenoids added in feed as important component in daily diet. This paper various sources of carotenoids and their capturing energy from light, absorbing reviews aspects regarding the main sources of carotenoids used as feed additives for nutritional and coloring properties and their impact on animal and human health. application in animal feed additives. This topic wavelengths, ranging from 400-550 has rarely been described in a general matter, nanometers (violet to green light), thus Key words: carotenoids, feed additives, sources of carotenoids, pigmentation. and as such we endeavor to provide an assisting in photosynthesis and causes the overview of published works on the subject. compounds to be deeply colored yellow, INTRODUCTION properties and deposition of carotenoids crucial orange, or red (Vershinin, 1999; Zakynthinos, for consumers (egg yolks and other products). DEFINITION, CHEMICAL STRUCTURE 2016). Carotenoids gained great interest lately for food In fact, as studies show, there is a strong AND CLASSIFICATION OF There have been identified over 750 naturally and feeding, as their functions related to relationship between diets/foods rich in CAROTENOIDS occurring carotenoids, biosynthesized de novo nutrition, health and wellbeing are well carotenoids and the risk reduction of various by plants, algae, fungi and bacteria (Okada et appreciated. As consumers become more and diseases. Carotenoids increase the immune Carotenoids are natural pigments, widely al., 2008), among which only 50 have more aware of the importance of natural response, are excellent antioxidants, scavenging distributed in nature, responsible for the significant biological activity for animals and instead of synthetic and artificial ingredients, and inactivating free radicals. This is why both coloring of fruits, vegetables and flowers. humans (Mezzomo et al., 2016). they tend to change preferences and replace vitamin A precursor carotenoids and the non- Carotenoids take their name from carrot Animals cannot synthesize carotenoids (Rock, products in their diets according to norms precursors ones play an important role in the (Daucus carota), which accumulates high 2009), obtaining them through dietary intake, which no longer respond to good, tasty and protection and inhibition of serious diseases as levels of these pigments in the root, being an with a few exceptions, represented by aphids affordable consumptions, yet to higher, long- cancer, atherosclerosis, cataracts, macular exception among plants (Stange, 2015). They and spiders which acquired the ability and term perspective standards (García-Chavarría degeneration, multiple sclerosis, degenerative are used as food colorants, feed supplements, genes from fungi (Moran, 2010; Nováková, and Lara-Flores, 2013; Carotenoids Market by diseases, and cardiovascular diseases for cosmetic and pharmaceutical purposes. 2012) or are produced by endosymbiotic Type, 2016; Mohiseni., 2017). (Mezzomo et al., 2016). Most carotenoids are made up of eight bacteria in whiteflies (Sloan, 2012). In this line, arguments related to the On the other hand, there is no novelty feeding condensed 5-carbon-containing isoprene Carotenoids are classified in Table 1. replacement of synthetic carotenoids with animals with carotenoids, these have always natural ones in case of animal feed additives been part of their daily diet. Astaxanthin is the Table 1. Classification of carotenoids lay in multiple health impact through major carotenoid used for pigmentation of fish Classification Major classes Structure Examples Attribute References environment and animal to human health (Kaur muscle, mainly salmons (Bhosale, 2004). Beta- criteria and Shah, 2017). carotene, lycopene, and lutein increase growth Chemical Carotenes Hydrocarbons (constituted α-carotene -color range from pale Delgado-Vargas, 2000 As such, many researches have been directed to performance of animals and quality of structure by carbon and hydrogen) β- carotene yellow, bright orange to Tinoi, 2005 in-depth knowledge on carotenoid sources, pigmented products (Nelis and De Leenheer, that can be cyclized at one γ-carotene deep red Aizawa, 2007 or both ends of the molecule lycopene -maintains eye health Kaur and Shah, 2017 especially natural ones, for their use as animal 1991). Animals and humans are unable to torulene -does not color the fish feed additives, so as to benefit from their synthesize carotenoids, they have to meet their Oxycarotenoids Oxygenated hydrocarbon lutein, zeaxanthin, β- -generally yellow in color Delgado-Vargas, functions including skin and tissues daily nutritional needs from the products (xanthophylls) derivatives that contain at cryptoxanthin, -antiallergic and anti- 2000; pigmentation (especially when it comes to ingested (Priyadarshani and Rath, 2012). least one oxygen atom as astaxanthin, cancerous actions Bhosale and Berstein, hydroxyl groups, keto, canthaxanthin, -can color the fish 2005; animals/birds grown in captivity), as growth Carotenoids, as part of the nutrients in the feed, epoxy, methoxy, or violaxanthin,neoxanthin, -colors egg yolks Kushwaha et al, 2014. promoters (in terms of mass production), for support animal health and animal products carboxylic acid antheraxanthin reproduction and survival goals, sensory quality (Amaya et al., 2014). They have an 75 Classification Major classes Structure Examples Attribute References eye strain and fatigue, and seeing in fine global carotenoids market is estimated to be criteria detail), immune-boosting effects (improves the valued at USD 1.53 Billion by 2021 and this is Functionality Primary Xanthophylls β-carotene -structural and functional Delgado-Vargas, 2000 ability of protective white blood cells to mainly due to the increasing number of health- violaxanthin neoxanthin components of the cellular photosynthetic apparatus surround and destroy infecting organisms, conscious consumers and the rising demand for

Secondary α-carotene -localized in fruits and Delgado-Vargas, 2000 especially fungi), prevention of different types natural coloration. The quality of food is β-cryptoxanthin flowers of cancer (colon and breast cancer) (Amaya et associated with color, flavor, texture, and odor, zeaxanthin -encompasses carotenoids al., 2014). humans considering color as the most relevant antheraxanthin capsanthin produced at large levels capsorubin Canthaxanthin is an orange-red oxycarotenoid aspect due to its appealing nature (Amaya et

Nutritionally Precursors of Have at least one ring of β- α-carotene -helps maintain eye Ambrosio et al., 2006; found in crustaceans, fungi and algae, al., 2014). vitamin A ionone not replaced and side β-carotene health, healthy mucus Premkumar, 2014 particularly used in color feeding. If, today, carotenoids produced commercially polyenic chain with at least β-cryptoxanthin membranes and immunity 11 carbons Canthaxanthin has an antioxidant activity and are mostly by total synthesis to meet the enhances junctional communication between demands, intention is to growingly substitute Non lutein Premkumar, 2014 provitamin A zeaxanthin cells directly or through the formation of 4- these with natural ones, if possible obtained by lycopene oxo-retinoic acid, which is also able to as mild as possible methods and processes stimulate the retinoic acid receptor (Amaya et (Mezzomo and Ferreira, 2016). β-carotene is used as food colorant and food ruberrimus. Its structural characteristics make al., 2014). Synthetic carotenoids supplement having antioxidant capacity and possible antitumoral and immune enhancing For carotenoid synthesis, one need to construct provitamin A activity, in a concentration ranges activities and could be used as food, feed and SOURCES OF CAROTENOIDS FOR the polyene chain, meaning the hydrocarbon from 2 to 50 ppm. Once converted to vitamin cosmetic additives (Zoz et al, 2015). FEED ADDITIVES skeleton conjugated by alternating double and A, health benefits include maintenance of Lutein is a dihydroxy-carotene with an alcohol single bonds. For the specific location of the normal eye health, epithelial function, group containing hydroaromatic α structure As have been pointed out above, there has been double and single bonds, different reactions embryonic development, and immune system (Kim, 2006) being in covalent interactions a change lately in the perspective towards the have been developed along time, the first to be function. Currently, the application of within fatty acids (Mezzomo, 2016). Lutein is ingredients of foods, what is considered healthy obtained being the β-carotene (Amaya et al., carotenoids in food formulations is limited found in leaves of green vegetables (spinach, for humans and for the environment and what 2014). because of it poor water solubility, high kale, pumpkin, turnip greens) and is yellow- should constitute the food of animals and birds. Out of economic and technological reasons, melting point and chemical instability (Qian, colored. Lutein gives color to chicken fat, egg Yet, researches are still conducted to efficiently although various carotenoids have been 2012a; Piorkowski, 2014), promoted by heat, yolk, and chicken feathers and also increase the obtain natural carotenoids and optimal feed synthesized at laboratory level, few of them light, singlet oxygen, acid, iron and iodine, and efficacy of vaccination against infectious formulas for animals/birds. (Kaur and Shah, went to commercial scale, among which are the free radical, because of conjugated polyene bronchitis virus in laying hens (McGraw, 2017). following: astaxanthin, astaxanthin-dimethyl- chain which is characteristic of carotenoids 2003). According to the new study by di-succinate, as well as β-carotene, β-apo-8’- (Dutta, 2005; Boon, 2010). Good sources of Lutein and zeaxanthin are associated with eye reportsnreports.com (2016), the carotenoid carotenal, also canthaxanthin, citranaxanthin, beta-carotene are cantaloupe, mangoes, papaya, health, because they are the only carotenoids market is led by the feed segment. The demand and the ethyl ester of β-apo-8’-carotenoic acid. carrots, sweet potatoes, spinach, kale and found in the retina in macula lutea, being likely for incorporation of carotenoids in animal feed For commercial use in animal nutrition, they pumpkin (Premkumar, 2014). effective in age-related macular degeneration is growing due to consumers preference for are usually formulated as 10% concentrated Lycopene is an aliphatic carotenoid which (Premkumar, 2014). good quality and meat, meat products, and fish products as a powder or beadlet (Amaya et al., dissolves in the oil, and that is why the Astaxanthin is a dark-red organic pigment aspect. Carotenoids also increase the palata- 2014). presence of oils greatly increases its absorption being the most valuable microalgal compounds. bility of feed, aquaculture being currently the Currently, carotenoids synthetic production is by the digestive system (Story, 2010). Haematococcus pluvialis strain is the richest fastest growing sector. It is known that the the most common manufacturing method. Over Lycopene is abundant in tomatoes, source of astaxanthin (Mezzomo and Ferreira, farming of salmon and shrimp grew 95% of the feed market uses synthetic watermelons, pink grapefruit, papaya and are 2016; Zaheer, 2017). This substance gives the exponentially in the last years and the trend is astaxanthin, mainly from major producers the most effective singlet oxygen scavenger in pinkish-red hue to the salmonids (salmons and ascendant, so the market of feed carotenoids, BASF (Germany) (Lucantin pink) and vitro (Sies and Sthal, 1995). Epidemiological trout), shrimps, lobsters and crabs and has an especially of astaxanthin, expands rapidly Hoffman-La Roche (Switzerland) (Carrophyll studies concluded that diets rich in high important role in their immune-system and (Anonimous, 2010). pink), which contains only 25% of the biologi- lycopene foods may reduce risk of fertility. Nutritionally, astaxanthin is the most With the growth of world population and cally active stereoisomer found naturally. For cardiovascular diseases and different cancer powerful antioxidant in the nature, with role to increased awareness and demand for better replacing, only in aquaculture feed additive, the types (Boon C., 2010). scavenge efficiently free radicals from the animal nutrition (in terms of quality and synthetic pigment with natural astaxanthin Torulene has one β-ionone ring and a longer human body (Koller et al., 2014). quantity), carotenoid additives seem to be the produced by Haematococcus, the biomass of polyene chain than that of β-carotene; it has 13 Similarly to lutein, it was proved to have a solution (García-Chavarría and Lara-Flores, this microalga should be increased to 10 000 double bonds and red color, in contrast to other positive role in many human health problems, 2013; Mohiseni, 2017). ton per year, the price of astaxanthin being too carotenoids produced by the microorganisms. such as: UV-light protection, anti-inflammatory According to global trends and forecasts high (Lorenz, 2000; Minyuk, 2008). Torulene is found in red yeasts such as properties, support for eye health (helps (https://www.marketsandmarkets.com/Market- The addition of synthetic carotenoids to the diet Rhodotorula glutinis, Sporobolomyces diabetic retinopathy, macular degeneration, Reports/carotenoid-market-158421566.html), of laying hens and broilers is a common 76 Classification Major classes Structure Examples Attribute References eye strain and fatigue, and seeing in fine global carotenoids market is estimated to be criteria detail), immune-boosting effects (improves the valued at USD 1.53 Billion by 2021 and this is Functionality Primary Xanthophylls β-carotene -structural and functional Delgado-Vargas, 2000 ability of protective white blood cells to mainly due to the increasing number of health- violaxanthin neoxanthin components of the cellular photosynthetic apparatus surround and destroy infecting organisms, conscious consumers and the rising demand for

Secondary α-carotene -localized in fruits and Delgado-Vargas, 2000 especially fungi), prevention of different types natural coloration. The quality of food is β-cryptoxanthin flowers of cancer (colon and breast cancer) (Amaya et associated with color, flavor, texture, and odor, zeaxanthin -encompasses carotenoids al., 2014). humans considering color as the most relevant antheraxanthin capsanthin produced at large levels capsorubin Canthaxanthin is an orange-red oxycarotenoid aspect due to its appealing nature (Amaya et

Nutritionally Precursors of Have at least one ring of β- α-carotene -helps maintain eye Ambrosio et al., 2006; found in crustaceans, fungi and algae, al., 2014). vitamin A ionone not replaced and side β-carotene health, healthy mucus Premkumar, 2014 particularly used in color feeding. If, today, carotenoids produced commercially polyenic chain with at least β-cryptoxanthin membranes and immunity 11 carbons Canthaxanthin has an antioxidant activity and are mostly by total synthesis to meet the enhances junctional communication between demands, intention is to growingly substitute Non lutein Premkumar, 2014 provitamin A zeaxanthin cells directly or through the formation of 4- these with natural ones, if possible obtained by lycopene oxo-retinoic acid, which is also able to as mild as possible methods and processes stimulate the retinoic acid receptor (Amaya et (Mezzomo and Ferreira, 2016). β-carotene is used as food colorant and food ruberrimus. Its structural characteristics make al., 2014). Synthetic carotenoids supplement having antioxidant capacity and possible antitumoral and immune enhancing For carotenoid synthesis, one need to construct provitamin A activity, in a concentration ranges activities and could be used as food, feed and SOURCES OF CAROTENOIDS FOR the polyene chain, meaning the hydrocarbon from 2 to 50 ppm. Once converted to vitamin cosmetic additives (Zoz et al, 2015). FEED ADDITIVES skeleton conjugated by alternating double and A, health benefits include maintenance of Lutein is a dihydroxy-carotene with an alcohol single bonds. For the specific location of the normal eye health, epithelial function, group containing hydroaromatic α structure As have been pointed out above, there has been double and single bonds, different reactions embryonic development, and immune system (Kim, 2006) being in covalent interactions a change lately in the perspective towards the have been developed along time, the first to be function. Currently, the application of within fatty acids (Mezzomo, 2016). Lutein is ingredients of foods, what is considered healthy obtained being the β-carotene (Amaya et al., carotenoids in food formulations is limited found in leaves of green vegetables (spinach, for humans and for the environment and what 2014). because of it poor water solubility, high kale, pumpkin, turnip greens) and is yellow- should constitute the food of animals and birds. Out of economic and technological reasons, melting point and chemical instability (Qian, colored. Lutein gives color to chicken fat, egg Yet, researches are still conducted to efficiently although various carotenoids have been 2012a; Piorkowski, 2014), promoted by heat, yolk, and chicken feathers and also increase the obtain natural carotenoids and optimal feed synthesized at laboratory level, few of them light, singlet oxygen, acid, iron and iodine, and efficacy of vaccination against infectious formulas for animals/birds. (Kaur and Shah, went to commercial scale, among which are the free radical, because of conjugated polyene bronchitis virus in laying hens (McGraw, 2017). following: astaxanthin, astaxanthin-dimethyl- chain which is characteristic of carotenoids 2003). According to the new study by di-succinate, as well as β-carotene, β-apo-8’- (Dutta, 2005; Boon, 2010). Good sources of Lutein and zeaxanthin are associated with eye reportsnreports.com (2016), the carotenoid carotenal, also canthaxanthin, citranaxanthin, beta-carotene are cantaloupe, mangoes, papaya, health, because they are the only carotenoids market is led by the feed segment. The demand and the ethyl ester of β-apo-8’-carotenoic acid. carrots, sweet potatoes, spinach, kale and found in the retina in macula lutea, being likely for incorporation of carotenoids in animal feed For commercial use in animal nutrition, they pumpkin (Premkumar, 2014). effective in age-related macular degeneration is growing due to consumers preference for are usually formulated as 10% concentrated Lycopene is an aliphatic carotenoid which (Premkumar, 2014). good quality and meat, meat products, and fish products as a powder or beadlet (Amaya et al., dissolves in the oil, and that is why the Astaxanthin is a dark-red organic pigment aspect. Carotenoids also increase the palata- 2014). presence of oils greatly increases its absorption being the most valuable microalgal compounds. bility of feed, aquaculture being currently the Currently, carotenoids synthetic production is by the digestive system (Story, 2010). Haematococcus pluvialis strain is the richest fastest growing sector. It is known that the the most common manufacturing method. Over Lycopene is abundant in tomatoes, source of astaxanthin (Mezzomo and Ferreira, farming of salmon and shrimp grew 95% of the feed market uses synthetic watermelons, pink grapefruit, papaya and are 2016; Zaheer, 2017). This substance gives the exponentially in the last years and the trend is astaxanthin, mainly from major producers the most effective singlet oxygen scavenger in pinkish-red hue to the salmonids (salmons and ascendant, so the market of feed carotenoids, BASF (Germany) (Lucantin pink) and vitro (Sies and Sthal, 1995). Epidemiological trout), shrimps, lobsters and crabs and has an especially of astaxanthin, expands rapidly Hoffman-La Roche (Switzerland) (Carrophyll studies concluded that diets rich in high important role in their immune-system and (Anonimous, 2010). pink), which contains only 25% of the biologi- lycopene foods may reduce risk of fertility. Nutritionally, astaxanthin is the most With the growth of world population and cally active stereoisomer found naturally. For cardiovascular diseases and different cancer powerful antioxidant in the nature, with role to increased awareness and demand for better replacing, only in aquaculture feed additive, the types (Boon C., 2010). scavenge efficiently free radicals from the animal nutrition (in terms of quality and synthetic pigment with natural astaxanthin Torulene has one β-ionone ring and a longer human body (Koller et al., 2014). quantity), carotenoid additives seem to be the produced by Haematococcus, the biomass of polyene chain than that of β-carotene; it has 13 Similarly to lutein, it was proved to have a solution (García-Chavarría and Lara-Flores, this microalga should be increased to 10 000 double bonds and red color, in contrast to other positive role in many human health problems, 2013; Mohiseni, 2017). ton per year, the price of astaxanthin being too carotenoids produced by the microorganisms. such as: UV-light protection, anti-inflammatory According to global trends and forecasts high (Lorenz, 2000; Minyuk, 2008). Torulene is found in red yeasts such as properties, support for eye health (helps (https://www.marketsandmarkets.com/Market- The addition of synthetic carotenoids to the diet Rhodotorula glutinis, Sporobolomyces diabetic retinopathy, macular degeneration, Reports/carotenoid-market-158421566.html), of laying hens and broilers is a common 77 practice, for improving yolk color (Santos- The majority of naturally occurring carotenoids Table 2. Natural animal feed supplements Bocanegra, 2004). Canthaxanthin is the are found in vegetables and fruits, dark green Natural sources Main carotenoids Role as feed additive References preferred synthetic red xanthophyll in poultry leaves of plants and seeds, flowers and roots Carrots β-Carotene Increases yolk color parameters and carotenoid Isler, 1967 farming available as Carophyll® Red (DSM (Amaya et al., 2014). Carotenoids found in α-Carotene contents Hammershoj et al, 2010 Nutritional Products, Switzerland) or plants differ in concentration depending on Coloration of skin and flesh of food fish Weerakkody et al., 2016 Lucantin® Red (BASF, Germany). The plant varieties, degree of ripeness, time of Alfalfa (Medicago Lutein Pigmentation of broilers Amaya et al., 2014 sativa) Zeaxanthin Improve egg quality Varzaru et al., 2015 preferred yellow xanthophyll is β-apo-8´- harvest, growing and storage conditions, etc. β-apo-8’-carotenal carotenoic acid ethyl ester available as (Zakynthinos et al., 2016). β-apo-8’-carotenoic acid Lycopene Carophyll® Yellow and Lucantin® Yellow Feed ingredients such as corn, maize, tomato, Marigold flower Lutein Poultry skin and egg coloration Rajput et al, 2012 (Marounek, 2015). green beans and cabbage, pumpkins, prunes or (Tagetes erecta) Zeaxanthin García-Chavarría and Lara-Flores, Synthetic carotenoids are technologically red pepper all are sources of carotenoids with 2013 feasible and cost-effective. These are benefits for animals (Amaya et al., 2014; Yellow maize Lutein Boosts carotenoids in eggs and improve egg yolk Breithaupt, 2007 standardized and more stable, i.e. apo-carotene- Zakynthinos et al., 2016; Mezzomo and Cryptoxanthin, Zeaxanthin color ester concentration in feed samples showed Ferreira, 2016,). Natural sources Main carotenoids Role as feed additive References very little variation from expected values, Red pepper or paprika (Capsicum annuum) is Saffron (Crocus Crocetin Oxidative stability of shell eggs and liquid yolks Botsoglou et al, 2005 sativus) β-Carotene whereas it was 30% below expectations for reported to be a rich, abundant and inexpensive Zeaxanthin marigold extracts. source of keto-carotenoids (capsanthin). It has Seeds of Bixa orellana Bixin and decomposition products Animal nutrition Amaya et al., 2014 It has been determined that 1 ppm of apo- been studied as a fish feed additive but with a Paprika (red pepper) Capsanthin Pigmentation and weight gain of rainbow trout Yanar, 2016 carotene-ester is equivalent to about 2 ppm of lower efficacy in comparison to commercially (Capsicum annuum) Capsorubin Pigmentation of salmonids lutein-zeaxanthin from marigold. available astaxanthin and a less desirable Pigmentation of Pacific white shrimps Talebi et al., 2013 Yolk pigmentation in laying hens Arredondo- Canthaxanthin is the red carotenoid which coloration in comparison to canthaxanthin in Weight gain in broilers Figueroa et al., 2003 dominates pigmentation of broilers, whereas rainbow trout (Akhtar et al., 1999). In addition Vicente et al., 2007 Galib et al., 2011 paprika xanthophylls which require two to to pigmentation, paprika increased growth rate three times the amount compared to and improved the reproductive performance in canthaxanthin, receives little attention. yellow tail. Good results have also been There are some problems regarding carotenoids 70% of the raw weights of the catch are The stability of various red carotenoids reported for laying hens’ yolk pigmentation production from plant origin, due to seasonal processing discards” reducing at the same time products in premixes was checked after three (Yanar et al., 2016). and geographic variability that cannot be an environmental problem (Shahidi et al., months of storage and recovery varied Marigold flower (Tagetes erecta) is rich in controlled. A better option, regarding yields 1998). Lobsters, crabs and shrimps, together considerably: 66% to 92% for canthaxanthin, lutein and zeaxanthin and it is efficient for and costs, is the microbial production of with their processing waste are sources of 76% for citranaxanthin, and 39% for poultry skin and egg coloration. Lutein from carotenoids on agro-industrial wastes which are astaxanthin (Mezzomo et al., 2016). capsanthin from paprika, which shows that marigold is also used as a yellow coloration for cheap substrates (Mata-Gómez, 2014). Supply of marine animal based natural carotenoids are very unstable on their isomeric cultured marine fish yellow tail and red sea Crustacea and marine animals carotenoids are limited because of declining forms. Another property is the transfer bream (Maoka T, 2011). As consumers Marine animals accumulate various carotenoids trend in catches of crustaceans from marine efficiency from feed to egg, which is better for associate color to nutritive value, healthiness, from foods (bacteria, algae, other animals) and resources. These sources of carotenoids are the synthesized ones. Apo-carotene-ester has a freshness and taste, this may count as an modify them through metabolic reactions very expensive and thus aquaculture feed 55% transfer efficiency to egg yolk, as interesting dietary alternative (García- (oxidation, reduction, translation of double production involves high production costs compared to only 17% for marigold Chavarría and Lara-Flores, 2013). bonds, oxidative cleavage of double bonds, (García-Chavarría and Lara-Flores, 2013). carotenoids and canthaxanthin an average Medicinal plants are known to be sources of cleavage of epoxy bonds). Many of these Microbial sources of carotenoids deposition rate of about 40% natural antioxidants used in treatments for carotenoids are metabolites of β-carotene, Interest in microbial sources of carotenoids was (www.poultryworld.net/Broilers/Nutrition/2012 human and animal diseases. Because of their fucoxanthin, peridinin, diatoxanthin, renewed due to consumers opinions against /8/The-effect-of-carotenoids-on-yolk-and-skin- fair price and strong effects, medicinal plants alloxanthin, and astaxanthin (Maoka, 2011). synthetic additives. Types of carotenogenic pigmentation-WP010752W/). are rapidly becoming a safe alternative for Astaxanthin is distributed in both marine and microorganisms, like bacteria and fungi, can be The consumer’s demand for “non-synthetic” antibiotics and chemical drugs in aquaculture. fresh water fish. Cyprinidae fishes synthesize stimulated to produce cost-effective colorants has driven the industry to identify and Furthermore, these can help increase growth as (3S,3′S)-astaxanthin from zeaxanthin by carotenoids in response to environmental stress develop natural sources of carotenoids to they maintain healthy intestinal microflora oxidative metabolic conversion. Perciformes (light, temperature), chemical compounds or replace chemical synthesis (Olesen, 2010). (Mohiseni, 2017). and Salmonidae fish cannot synthesize modification of metabolic pathway using Natural sources of carotenoids Some valuable natural supplements for astaxanthin from other carotenoids (Matsuno, recombinant DNA technology (Bhosale, Plants pigmentation of chicken eggs, broilers and fish 2001). Astaxanthin present in these fishes 2004). Advances have been made through are presented in the following Table 2. originates from crustacean sources (Atlantic genetic manipulation of some non- krill, crayfish meal, crab meal) used in carotenogenic microbes such as Escherichia aquaculture feed formulation as additive. coli, Saccharomyces cerevisiae, Candida utilis

Crustacean by-products represent an “attractive in terms of carotenoids production (Das et al., ingredient for industrialization, since around 2007). 78 practice, for improving yolk color (Santos- The majority of naturally occurring carotenoids Table 2. Natural animal feed supplements Bocanegra, 2004). Canthaxanthin is the are found in vegetables and fruits, dark green Natural sources Main carotenoids Role as feed additive References preferred synthetic red xanthophyll in poultry leaves of plants and seeds, flowers and roots Carrots β-Carotene Increases yolk color parameters and carotenoid Isler, 1967 farming available as Carophyll® Red (DSM (Amaya et al., 2014). Carotenoids found in α-Carotene contents Hammershoj et al, 2010 Nutritional Products, Switzerland) or plants differ in concentration depending on Coloration of skin and flesh of food fish Weerakkody et al., 2016 Lucantin® Red (BASF, Germany). The plant varieties, degree of ripeness, time of Alfalfa (Medicago Lutein Pigmentation of broilers Amaya et al., 2014 sativa) Zeaxanthin Improve egg quality Varzaru et al., 2015 preferred yellow xanthophyll is β-apo-8´- harvest, growing and storage conditions, etc. β-apo-8’-carotenal carotenoic acid ethyl ester available as (Zakynthinos et al., 2016). β-apo-8’-carotenoic acid Lycopene Carophyll® Yellow and Lucantin® Yellow Feed ingredients such as corn, maize, tomato, Marigold flower Lutein Poultry skin and egg coloration Rajput et al, 2012 (Marounek, 2015). green beans and cabbage, pumpkins, prunes or (Tagetes erecta) Zeaxanthin García-Chavarría and Lara-Flores, Synthetic carotenoids are technologically red pepper all are sources of carotenoids with 2013 feasible and cost-effective. These are benefits for animals (Amaya et al., 2014; Yellow maize Lutein Boosts carotenoids in eggs and improve egg yolk Breithaupt, 2007 standardized and more stable, i.e. apo-carotene- Zakynthinos et al., 2016; Mezzomo and Cryptoxanthin, Zeaxanthin color ester concentration in feed samples showed Ferreira, 2016,). Natural sources Main carotenoids Role as feed additive References very little variation from expected values, Red pepper or paprika (Capsicum annuum) is Saffron (Crocus Crocetin Oxidative stability of shell eggs and liquid yolks Botsoglou et al, 2005 sativus) β-Carotene whereas it was 30% below expectations for reported to be a rich, abundant and inexpensive Zeaxanthin marigold extracts. source of keto-carotenoids (capsanthin). It has Seeds of Bixa orellana Bixin and decomposition products Animal nutrition Amaya et al., 2014 It has been determined that 1 ppm of apo- been studied as a fish feed additive but with a Paprika (red pepper) Capsanthin Pigmentation and weight gain of rainbow trout Yanar, 2016 carotene-ester is equivalent to about 2 ppm of lower efficacy in comparison to commercially (Capsicum annuum) Capsorubin Pigmentation of salmonids lutein-zeaxanthin from marigold. available astaxanthin and a less desirable Pigmentation of Pacific white shrimps Talebi et al., 2013 Yolk pigmentation in laying hens Arredondo- Canthaxanthin is the red carotenoid which coloration in comparison to canthaxanthin in Weight gain in broilers Figueroa et al., 2003 dominates pigmentation of broilers, whereas rainbow trout (Akhtar et al., 1999). In addition Vicente et al., 2007 Galib et al., 2011 paprika xanthophylls which require two to to pigmentation, paprika increased growth rate three times the amount compared to and improved the reproductive performance in canthaxanthin, receives little attention. yellow tail. Good results have also been There are some problems regarding carotenoids 70% of the raw weights of the catch are The stability of various red carotenoids reported for laying hens’ yolk pigmentation production from plant origin, due to seasonal processing discards” reducing at the same time products in premixes was checked after three (Yanar et al., 2016). and geographic variability that cannot be an environmental problem (Shahidi et al., months of storage and recovery varied Marigold flower (Tagetes erecta) is rich in controlled. A better option, regarding yields 1998). Lobsters, crabs and shrimps, together considerably: 66% to 92% for canthaxanthin, lutein and zeaxanthin and it is efficient for and costs, is the microbial production of with their processing waste are sources of 76% for citranaxanthin, and 39% for poultry skin and egg coloration. Lutein from carotenoids on agro-industrial wastes which are astaxanthin (Mezzomo et al., 2016). capsanthin from paprika, which shows that marigold is also used as a yellow coloration for cheap substrates (Mata-Gómez, 2014). Supply of marine animal based natural carotenoids are very unstable on their isomeric cultured marine fish yellow tail and red sea Crustacea and marine animals carotenoids are limited because of declining forms. Another property is the transfer bream (Maoka T, 2011). As consumers Marine animals accumulate various carotenoids trend in catches of crustaceans from marine efficiency from feed to egg, which is better for associate color to nutritive value, healthiness, from foods (bacteria, algae, other animals) and resources. These sources of carotenoids are the synthesized ones. Apo-carotene-ester has a freshness and taste, this may count as an modify them through metabolic reactions very expensive and thus aquaculture feed 55% transfer efficiency to egg yolk, as interesting dietary alternative (García- (oxidation, reduction, translation of double production involves high production costs compared to only 17% for marigold Chavarría and Lara-Flores, 2013). bonds, oxidative cleavage of double bonds, (García-Chavarría and Lara-Flores, 2013). carotenoids and canthaxanthin an average Medicinal plants are known to be sources of cleavage of epoxy bonds). Many of these Microbial sources of carotenoids deposition rate of about 40% natural antioxidants used in treatments for carotenoids are metabolites of β-carotene, Interest in microbial sources of carotenoids was (www.poultryworld.net/Broilers/Nutrition/2012 human and animal diseases. Because of their fucoxanthin, peridinin, diatoxanthin, renewed due to consumers opinions against /8/The-effect-of-carotenoids-on-yolk-and-skin- fair price and strong effects, medicinal plants alloxanthin, and astaxanthin (Maoka, 2011). synthetic additives. Types of carotenogenic pigmentation-WP010752W/). are rapidly becoming a safe alternative for Astaxanthin is distributed in both marine and microorganisms, like bacteria and fungi, can be The consumer’s demand for “non-synthetic” antibiotics and chemical drugs in aquaculture. fresh water fish. Cyprinidae fishes synthesize stimulated to produce cost-effective colorants has driven the industry to identify and Furthermore, these can help increase growth as (3S,3′S)-astaxanthin from zeaxanthin by carotenoids in response to environmental stress develop natural sources of carotenoids to they maintain healthy intestinal microflora oxidative metabolic conversion. Perciformes (light, temperature), chemical compounds or replace chemical synthesis (Olesen, 2010). (Mohiseni, 2017). and Salmonidae fish cannot synthesize modification of metabolic pathway using Natural sources of carotenoids Some valuable natural supplements for astaxanthin from other carotenoids (Matsuno, recombinant DNA technology (Bhosale, Plants pigmentation of chicken eggs, broilers and fish 2001). Astaxanthin present in these fishes 2004). Advances have been made through are presented in the following Table 2. originates from crustacean sources (Atlantic genetic manipulation of some non- krill, crayfish meal, crab meal) used in carotenogenic microbes such as Escherichia aquaculture feed formulation as additive. coli, Saccharomyces cerevisiae, Candida utilis

Crustacean by-products represent an “attractive in terms of carotenoids production (Das et al., ingredient for industrialization, since around 2007). 79 Several bacteria have biotechnological Mycobacterium brevicaie, Mycobacterium their biomass, are Chlorella, Chlamydomonas, sources of natural pigments (β-carotene, α- potential for the production of carotenoids. lacticola, Rhodobacter sphaeroides, Dunaliella, Muriellopsis and Haematococcus carotene, β-cryptoxanthin and zeaxanthin, Some thermophilic halophilic bacteria such as Rhodococcus maris, Streptomyces spp, offering economical alternatives to respectively) for the culture of black tiger Halococcus morrhuae and Halobacterium chrestomyceticus (Dannert, 2000). chemical synthesis (Bhosale and Berstein, prawns (Penaeus monodon), salmonid fish and salinarum develop red and orange colonies, Some examples of carotenoid-producing 2005). ornamental fish (Priyadarshani and Rath, bacterioruberin synthetized by H. salinarum microorganisms are presented in Table 3. Carotenoids, even at levels of parts per million, 2012). Zeaxanthin from Spirulina is used as a being the most found carotenoid (Asker and Practical obstacles still need to be overcome for are strong dyes, especially canthaxanthin, red coloration for goldfish and ornamental Ohta, 1999). Haloferax alexandrines has good their commercial exploitation, though astaxanthin and lutein from Chlorella, which carp. Astaxanthin became the most important industrial perspective for the production of developments in recent years have proven that, have been used as pigments and included as carotenoid in salmons and rainbow trout with canthaxanthin (Asker and Ohta, 2002) and the in both farmed fish and poultry, carotenoids ingredients in feed for salmonid fish, trout, and the development of salmonid farming. marine bacterium Flavobacterium sp. produces like astaxanthin, canthaxanthin, β-carotene, poultry to enhance the reddish color of fish and Astaxanthin can be incorporated in feeds up to zeaxanthin, being considered one of the best zeaxanthin and lycopene from bacterial sources egg yolk yellowish color (Plaza et al., 2009). 100 mg/ kg and canthaxanthin up to 25 mg/kg microbial sources of zeaxanthin (Masetto et al., impart color to skin, flesh and eggs (Bhosale, Broiler chickens fed with algae have yellow (high accumulation in humans can be toxic). 2001). Other bacteria with ability to synthesize 2004). skin and shanks, and the egg yolk is darker Animal feed is the largest field of commercial carotenoids are Agrobacterium aurantiacum, indicating higher carotenoids content (Becker, application of microalgae carotenoids due to 2004). Microalgae like Chlorella vulgaris and the importance of astaxanthin and Table 3. Microorganisms sources of carotenoids and their application as feed additives Haematococcus pluvialis synthetize large canthaxanthin in aquaculture (Britton, 2004). Bacteria and Yeasts Carotenoids/Activity Application as animal feed additives References amount of astaxanthin (Yin, 2013; Kim, 2016) Bellow given is Table 4, including the sources Mycobacterium lacticola Astaxanthin/ antioxidant, Fish feeds Kushwaha et al., 2014 and Dunaliella salina, Spirulina maxima and S. of carotenoids from microalgae with photo- protectant platensis are biotechnologically relevant, as application as feed additives. Paracoccus carotinifaciens Astaxanthin/ Coloration of farm raised salmon and Bories, 2007 (commercially sold as Panaferd) pigmentation trout Table 4. Microalgae sources of carotenoids Spongiococcum excentricum Lutein/antioxidant Poultry feeds Kushwaha et al., 2014 Algae and cyanobacteria Carotenoid Application as feed additives References Flavobacterium sp. Zeaxanthin/ Additive in poultry feed to increase Alcantara and Sanchez, 1999 Haematococcus pluvialis Astaxanthin Animal feed additives Priyadarshani and Rath, 2012 pigmentation yellow color of animal’s skin and egg Masetto et al., 2001 (commercially sold as Aquaculture Mezzomo and Ferreira, 2016 yolk Bhosale, 2004 NaturRose) Used for culture of prawns, salmonid García-Chavarría, Lara-Flores, 2013 Fish feed fish and for ornamental and tropical Bhosale, 2004 Haloferax alexandrines Canthaxanthin/ Feed in salmon farming to guarantee Asker and Ohta, 2002 fish Amaya et al., 2014 pigmentation the flesh color of fish Dunaliella sp. β-carotene Animal feed additives Priyadarshani and Rath, 2012 Dietzia natronolimnaea HS-1 Canthaxanthin/ Egg yolk pigmentation Esfahani-Mashhour et al., 2009 Used as natural food coloring agent in Mezzomo and Ferreira, 2016 pigmentation, antioxidant Gharibzahedi et al., 2012 aquaculture feed industry García-Chavarría, Lara-Flores, 2013 Bhosale, 2004 Phaffia rhodozyma Astaxanthin/ Pigmentation of salmon, trout, and red Maoka, 2011 Amaya et al., 2014 pigmentation sea bream (Pagrus sp.) Kushwaha et al., 2014 Pigment source for egg yolk of laying Chlorella vulgaris Lutein Used in diets of rainbow trout yielding Priyadarshani and Rath, 2012 hens Astaxanthin both muscle and skin pigmentation Mezzomo and Ferreira, 2016 Fucoxanthin effects García-Chavarría M., Lara-Flores M, 2013 Blakeslea trispora β-carotene/growth Chickens for fattening Sales et al., 2008 Animal feed additives performance Shrimp feed Feed for dairy cows Chlorella protothecoides Lutein The reddish color of salmonid fish and Guedes et al., 2011 yellowish color of egg yolk Mezzomo and Ferreira, 2016 Rhodotorula spp. β-carotene Nutrition of laying hens Bhosale P., 2004 Torulene Kushwaha et al., 2014 Algae and cyanobacteria Carotenoid Application as feed additives References Torularhodin/ Chlorella zofingiensis Lutein Enhances the reddish color of salmonid Guedes et al., 2011 antioxidant, precursor of

vitamin A Muriellopsis sp. Lutein Poultry farming and/or aquaculture Blanco et al., 2006 Xanthophyllomyces dendrorhous Astaxanthin Feed supplement for salmons, crabs, Bhosale P, 2004 shrimps, chickens and egg production Kushwaha et al., 2014 Scenedesmus obliquus Lutein Fish feed Mezzomo and Ferreira, 2016 Mushrooms Tetraselmis sp Lutein Aquaculture and larval feeds Priyadarshani and Rath, 2012 Cantharellus cinnabarinus Canthaxanthin Poultry feeds and fish feeds Kushwaha et al., 2014 Nannochloropsis oculata Astaxanthin Aquaculture & larval feeds Priyadarshani and Rath, 2012 Hen supplements - increases egg Zaheer, 2017 nutritional value Gładkowski et al, 2011 Microbial sources are an environmental-friendly researched and commercialized both for Spirulina sp β-carotene Animal feed additives Indira Priyadarshani and Biswajit Rath, 2012 method for the production of carotenoids, which nutritional supplements for humans and as meet the increasing demand of these natural animal feed additives to replace synthetic The market demand for pigments natural The European legislation specifies that before products (Das, 2007). components (Priyadarshani and Rath, 2012). sources has promoted large-scale cultivation of their use in EU, carotenoids have to be Microalgae, rich source of carbohydrates, Microalgae play an important role in the high- microalgae for biosynthesis of such compounds subjected to an authorization process. protein, enzymes and fiber, have been a major level nutrition for both aquaculture and farm (well-established are β-carotene and A general overview of the current legal source of food for humans in Asian countries. animals. The most famous sources of astaxanthin), so significant decreases in situation of the different carotenoids used as They have been naturally taken over, microalgae, which accumulate carotenoids in production costs are expected in coming years. feed additives in compound feed in European 80 Several bacteria have biotechnological Mycobacterium brevicaie, Mycobacterium their biomass, are Chlorella, Chlamydomonas, sources of natural pigments (β-carotene, α- potential for the production of carotenoids. lacticola, Rhodobacter sphaeroides, Dunaliella, Muriellopsis and Haematococcus carotene, β-cryptoxanthin and zeaxanthin, Some thermophilic halophilic bacteria such as Rhodococcus maris, Streptomyces spp, offering economical alternatives to respectively) for the culture of black tiger Halococcus morrhuae and Halobacterium chrestomyceticus (Dannert, 2000). chemical synthesis (Bhosale and Berstein, prawns (Penaeus monodon), salmonid fish and salinarum develop red and orange colonies, Some examples of carotenoid-producing 2005). ornamental fish (Priyadarshani and Rath, bacterioruberin synthetized by H. salinarum microorganisms are presented in Table 3. Carotenoids, even at levels of parts per million, 2012). Zeaxanthin from Spirulina is used as a being the most found carotenoid (Asker and Practical obstacles still need to be overcome for are strong dyes, especially canthaxanthin, red coloration for goldfish and ornamental Ohta, 1999). Haloferax alexandrines has good their commercial exploitation, though astaxanthin and lutein from Chlorella, which carp. Astaxanthin became the most important industrial perspective for the production of developments in recent years have proven that, have been used as pigments and included as carotenoid in salmons and rainbow trout with canthaxanthin (Asker and Ohta, 2002) and the in both farmed fish and poultry, carotenoids ingredients in feed for salmonid fish, trout, and the development of salmonid farming. marine bacterium Flavobacterium sp. produces like astaxanthin, canthaxanthin, β-carotene, poultry to enhance the reddish color of fish and Astaxanthin can be incorporated in feeds up to zeaxanthin, being considered one of the best zeaxanthin and lycopene from bacterial sources egg yolk yellowish color (Plaza et al., 2009). 100 mg/ kg and canthaxanthin up to 25 mg/kg microbial sources of zeaxanthin (Masetto et al., impart color to skin, flesh and eggs (Bhosale, Broiler chickens fed with algae have yellow (high accumulation in humans can be toxic). 2001). Other bacteria with ability to synthesize 2004). skin and shanks, and the egg yolk is darker Animal feed is the largest field of commercial carotenoids are Agrobacterium aurantiacum, indicating higher carotenoids content (Becker, application of microalgae carotenoids due to 2004). Microalgae like Chlorella vulgaris and the importance of astaxanthin and Table 3. Microorganisms sources of carotenoids and their application as feed additives Haematococcus pluvialis synthetize large canthaxanthin in aquaculture (Britton, 2004). Bacteria and Yeasts Carotenoids/Activity Application as animal feed additives References amount of astaxanthin (Yin, 2013; Kim, 2016) Bellow given is Table 4, including the sources Mycobacterium lacticola Astaxanthin/ antioxidant, Fish feeds Kushwaha et al., 2014 and Dunaliella salina, Spirulina maxima and S. of carotenoids from microalgae with photo- protectant platensis are biotechnologically relevant, as application as feed additives. Paracoccus carotinifaciens Astaxanthin/ Coloration of farm raised salmon and Bories, 2007 (commercially sold as Panaferd) pigmentation trout Table 4. Microalgae sources of carotenoids Spongiococcum excentricum Lutein/antioxidant Poultry feeds Kushwaha et al., 2014 Algae and cyanobacteria Carotenoid Application as feed additives References Flavobacterium sp. Zeaxanthin/ Additive in poultry feed to increase Alcantara and Sanchez, 1999 Haematococcus pluvialis Astaxanthin Animal feed additives Priyadarshani and Rath, 2012 pigmentation yellow color of animal’s skin and egg Masetto et al., 2001 (commercially sold as Aquaculture Mezzomo and Ferreira, 2016 yolk Bhosale, 2004 NaturRose) Used for culture of prawns, salmonid García-Chavarría, Lara-Flores, 2013 Fish feed fish and for ornamental and tropical Bhosale, 2004 Haloferax alexandrines Canthaxanthin/ Feed in salmon farming to guarantee Asker and Ohta, 2002 fish Amaya et al., 2014 pigmentation the flesh color of fish Dunaliella sp. β-carotene Animal feed additives Priyadarshani and Rath, 2012 Dietzia natronolimnaea HS-1 Canthaxanthin/ Egg yolk pigmentation Esfahani-Mashhour et al., 2009 Used as natural food coloring agent in Mezzomo and Ferreira, 2016 pigmentation, antioxidant Gharibzahedi et al., 2012 aquaculture feed industry García-Chavarría, Lara-Flores, 2013 Bhosale, 2004 Phaffia rhodozyma Astaxanthin/ Pigmentation of salmon, trout, and red Maoka, 2011 Amaya et al., 2014 pigmentation sea bream (Pagrus sp.) Kushwaha et al., 2014 Pigment source for egg yolk of laying Chlorella vulgaris Lutein Used in diets of rainbow trout yielding Priyadarshani and Rath, 2012 hens Astaxanthin both muscle and skin pigmentation Mezzomo and Ferreira, 2016 Fucoxanthin effects García-Chavarría M., Lara-Flores M, 2013 Blakeslea trispora β-carotene/growth Chickens for fattening Sales et al., 2008 Animal feed additives performance Shrimp feed Feed for dairy cows Chlorella protothecoides Lutein The reddish color of salmonid fish and Guedes et al., 2011 yellowish color of egg yolk Mezzomo and Ferreira, 2016 Rhodotorula spp. β-carotene Nutrition of laying hens Bhosale P., 2004 Torulene Kushwaha et al., 2014 Algae and cyanobacteria Carotenoid Application as feed additives References Torularhodin/ Chlorella zofingiensis Lutein Enhances the reddish color of salmonid Guedes et al., 2011 antioxidant, precursor of vitamin A Muriellopsis sp. Lutein Poultry farming and/or aquaculture Blanco et al., 2006 Xanthophyllomyces dendrorhous Astaxanthin Feed supplement for salmons, crabs, Bhosale P, 2004 shrimps, chickens and egg production Kushwaha et al., 2014 Scenedesmus obliquus Lutein Fish feed Mezzomo and Ferreira, 2016 Mushrooms Tetraselmis sp Lutein Aquaculture and larval feeds Priyadarshani and Rath, 2012 Cantharellus cinnabarinus Canthaxanthin Poultry feeds and fish feeds Kushwaha et al., 2014 Nannochloropsis oculata Astaxanthin Aquaculture & larval feeds Priyadarshani and Rath, 2012 Hen supplements - increases egg Zaheer, 2017 nutritional value Gładkowski et al, 2011 Microbial sources are an environmental-friendly researched and commercialized both for Spirulina sp β-carotene Animal feed additives Indira Priyadarshani and Biswajit Rath, 2012 method for the production of carotenoids, which nutritional supplements for humans and as meet the increasing demand of these natural animal feed additives to replace synthetic The market demand for pigments natural The European legislation specifies that before products (Das, 2007). components (Priyadarshani and Rath, 2012). sources has promoted large-scale cultivation of their use in EU, carotenoids have to be Microalgae, rich source of carbohydrates, Microalgae play an important role in the high- microalgae for biosynthesis of such compounds subjected to an authorization process. protein, enzymes and fiber, have been a major level nutrition for both aquaculture and farm (well-established are β-carotene and A general overview of the current legal source of food for humans in Asian countries. animals. The most famous sources of astaxanthin), so significant decreases in situation of the different carotenoids used as They have been naturally taken over, microalgae, which accumulate carotenoids in production costs are expected in coming years. feed additives in compound feed in European 81 Union is shown in Table 5 (Vincent et al., (Pérez-Gálvez, 2003; Baldo, 2011; Amaya et CONCLUSIONS REFERENCES 2017), with added data regarding what al., 2014; Rodriguez-Amaya, 2015; Mezzomo carotenoids are totally synthesized and which and Ferreira, 2016). Beyond the properties related to health, various Aguila M Ruiz-Sola, Rodriguez-Concepcion M, 2012. are extracted or biosynthesized come from natural sources of carotenoids have been and Carotenoid biosynthesis in Arabidopsis: a colorful pathway, Arabidopsis book. American Society of still are investigated as they represent Plant Biologists. Table 5. 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Journal of Food Science, 64, 234- paulensis) has long been met by synthetic technology, 239. processing waste because of by-products with undesirable effects Alcantara S., Sanchez S., 1999. Influence of carbon and on consumption, production of carotenoids nitrogen sources on Flavobacterium growth and Astaxanthin Fish X EURL-FA Feed zeaxanthin biosynthesis. Journal of Industrial Ornamental fish Additives (2010a) from natural sources, improvement of Crustaceans Microbiology and Biotechnology, 23(1), 697–700. bioproduction techniques and development of Amaya E., Becquet P., Carné S., Peris S, Miralles P., Astaxanthin Salmon and trout X EURL-FA Feed dimethyldisuccinate1 Additives (2007a) extraction methods, became the focus of 2014. Carotenoids in Animal Nutrition; FEFANA extensive research. (European Union Association of Specialty Feed β-apo-8’-carotenoic Poultry X EURL-FA Feed Ingredients and their Mixtures). acid ethyl ester Additives (2011c) In order to reach industrial production, more (apoester)2 Ambrósio C.L.B., Campos F., De Faro Z.P., 2006. optimization studies and also validation Carotenóides como alternativa contra a Astaxanthin, Salmon and trout Red carotenoid-rich EURL-FA Feed methods are required to scale up the processes. adonirubin, Paracoccus Additives (2007b) hipovitaminose A. Revista de Nutrição, 19(2), 233– canthaxanthin carotinifaciens A most important part in animal nutrition is 243. Asker D., Ohta Y., 1999. Production of canthaxanthin by Canthaxanthin2 Chickens for fattening and minor X Chlorella vulgaris EURL-FA Feed represented by feed additives, including poultry species for fattening; Additives (2011a) especially carotenoids, which are mainly extremely halophilic bacteria. J. Biosci. Bioeng., 88, Laying poultry and poultry reared 617-621. for laying; sensory additives used in the coloring of fish, Asker D., Ohta Y., 2002. Haloferax alexandrinus sp. Ornamental fish and ornamental birds and food of animal origin. nov., an extremely halophilic canthaxanthin- birds; Ornamental breeder hens Many natural sources with high potential for producing archaeon from a solar saltern in Alexandria (Egypt). Int. J. Syst. Evol. Microbiol., 52, 3 animal feed additives have already been Capsanthin Poultry Red peppers EURL-FA Feed 729-738. Additives (2012b) identified and studied, some of these being Baldo F.C., Obraztsova I., Couso I., Leon R., Vargas Citranaxanthin2 Poultry X EURL-FA Feed highlighted in this article. M.A., Rodriguez H., 2011. Enhancement of lutein Additives (2016) According to market reports, demand for production in Chlorella sorokiniana (Chlorophyta) Lutein3 Poultry Marigold EURL-FA Feed carotenoids in animal feed is increasing due to by improvement of culture conditions and random (Tagetes erecta Additives (2012a) mutagenesis. Mar.Drugs, 9, 1607-1624. and Tagetes the increasing preference for good quality and patula) appearance of meat, meat products, and fish. Bhosale P., 2004. Environmental and cultural stimulants Rose fruit in the production of carotenoids from (Rosa canina) Global carotenoids market is expected to reach microorganisms. Appl. Microbiol. Biotechnol., 63, Carrot USD 1.53 Billion by 2021 and, due to the 351–361. β-carotene (solid All animal species X Chlorella vulgaris EURL-FA Feed increasing number of health-conscious Blanco A.M., Moreno J., Del Campo J., Rivas J., form) Dunaliella salina Additives (2010b) consumers and the rising demand for natural Guerrero M., 2006. Outdoor cultivation of lutein-rich Arthrospira maxima coloration, the use of natural carotenoids will cells of Muriellopsis sp in open ponds. Applied Zeaxanthin3 Poultry Marigold EURL-FA Feed Microbiology and Biotechnology, 3(6), 1259-1266. (Tagetes erecta Additives (2012a) contribute to the enhancement of the market Boon C.S., McClements D.J., Weiss J., Decker E.A., and Tagetes growth. 2010. Factors influencing the chemical stability of patula) Paprika The potential health benefits of microalgae carotenoids in foods. Critical Reviews in Food (Capsicum represents the main drive behind the new Science and Nutrition, 50, 515–532. annuum) developments in their usage in feed and foods. Bories G., 2007. Safety and efficacy of Panaferd-AX 1formulated in an organic matrix (red carotenoid rich bacterium Paracoccus 2 formulation containing the active substance and other ingredients Even so, carotenoid production from algae is not carotinifaciens) as feed additive for salmon and trout. 3formulation containing a natural source of the active substance and other ingredients as cost effective as the synthetic counterpart. EURL-FA - EU Reference Laboratory for Feed Additives Scientific opinion of the panel on additives and products or substances used in animal feed, EFSA J., ACKNOWLEDGEMENT 546, 1-30. In the EU, carotenoids used as feed additives Union is currently limited to 80 ppm (mg/kg), Britton G., Liaaen-Jensen F., Pfander H., 2009. are mainly authorised under the category excepted canthaxanthin, whose limit is 8 ppm, The authors would like to thanks the Carotenoids vol.5: (Eds.) Birkhauser Verlag Basel, „sensory additives”, as colorants (Vincente et because excessive exposure in humans can lead ISBN 978-3-7643-7500-3. UEFISCDI that have supported 57PTE/2016 Chow E.P.Y., Liong K.H., Schoeters E., 2016. The al., 2017). The addition of natural and synthetic to the development of precipitated crystals in research project. Effect of dietary carotenoids of different forms: carotenoids in layer feeds in the European the retina (Baker, 2001). 82 Union is shown in Table 5 (Vincent et al., (Pérez-Gálvez, 2003; Baldo, 2011; Amaya et CONCLUSIONS REFERENCES 2017), with added data regarding what al., 2014; Rodriguez-Amaya, 2015; Mezzomo carotenoids are totally synthesized and which and Ferreira, 2016). Beyond the properties related to health, various Aguila M Ruiz-Sola, Rodriguez-Concepcion M, 2012. are extracted or biosynthesized come from natural sources of carotenoids have been and Carotenoid biosynthesis in Arabidopsis: a colorful pathway, Arabidopsis book. American Society of still are investigated as they represent Plant Biologists. Table 5. Carotenoids used in the feed industry as feed additives in the European Union renewable raw materials, are profitable in terms Aizawa K, Inakuma T., 2007. Quantitation of of culture/cultivation costs, as well as for their carotenoids in commonly consumed vegetables in Carotenoids feed Target animal Total Extracted Biosynthesized EURL-FA evaluation additive synthesized report replicability in terms of processes, and they act Japan. Food Sci. Technol. Res., 13(3), 247-252. synergistically – complementing one-another in Akhtar, P., Gray J.I., Cooper T.H., Graling D.L., Booren A.M., 1999. Dietary pigmentation and deposition of Astaxanthin Fish (salmon, trout) Crustaceans Phaffia rhodozyma EURL-FA Feed diets. Pink shrimp Haematococcus pluvialis Additives (2014) α-tocopherol and carotenoids in rainbow trout muscle (Penaeus Chlorella vulgaris Even though the high demand of carotenoids and liver tissue. Journal of Food Science, 64, 234- paulensis) has long been met by synthetic technology, 239. processing waste because of by-products with undesirable effects Alcantara S., Sanchez S., 1999. Influence of carbon and on consumption, production of carotenoids nitrogen sources on Flavobacterium growth and Astaxanthin Fish X EURL-FA Feed zeaxanthin biosynthesis. Journal of Industrial Ornamental fish Additives (2010a) from natural sources, improvement of Crustaceans Microbiology and Biotechnology, 23(1), 697–700. bioproduction techniques and development of Amaya E., Becquet P., Carné S., Peris S, Miralles P., Astaxanthin Salmon and trout X EURL-FA Feed dimethyldisuccinate1 Additives (2007a) extraction methods, became the focus of 2014. Carotenoids in Animal Nutrition; FEFANA extensive research. (European Union Association of Specialty Feed β-apo-8’-carotenoic Poultry X EURL-FA Feed Ingredients and their Mixtures). acid ethyl ester Additives (2011c) In order to reach industrial production, more (apoester)2 Ambrósio C.L.B., Campos F., De Faro Z.P., 2006. optimization studies and also validation Carotenóides como alternativa contra a Astaxanthin, Salmon and trout Red carotenoid-rich EURL-FA Feed methods are required to scale up the processes. adonirubin, Paracoccus Additives (2007b) hipovitaminose A. Revista de Nutrição, 19(2), 233– canthaxanthin carotinifaciens A most important part in animal nutrition is 243. Asker D., Ohta Y., 1999. Production of canthaxanthin by Canthaxanthin2 Chickens for fattening and minor X Chlorella vulgaris EURL-FA Feed represented by feed additives, including poultry species for fattening; Additives (2011a) especially carotenoids, which are mainly extremely halophilic bacteria. J. Biosci. Bioeng., 88, Laying poultry and poultry reared 617-621. for laying; sensory additives used in the coloring of fish, Asker D., Ohta Y., 2002. Haloferax alexandrinus sp. Ornamental fish and ornamental birds and food of animal origin. nov., an extremely halophilic canthaxanthin- birds; Ornamental breeder hens Many natural sources with high potential for producing archaeon from a solar saltern in Alexandria (Egypt). Int. J. Syst. Evol. Microbiol., 52, 3 animal feed additives have already been Capsanthin Poultry Red peppers EURL-FA Feed 729-738. Additives (2012b) identified and studied, some of these being Baldo F.C., Obraztsova I., Couso I., Leon R., Vargas Citranaxanthin2 Poultry X EURL-FA Feed highlighted in this article. M.A., Rodriguez H., 2011. Enhancement of lutein Additives (2016) According to market reports, demand for production in Chlorella sorokiniana (Chlorophyta) Lutein3 Poultry Marigold EURL-FA Feed carotenoids in animal feed is increasing due to by improvement of culture conditions and random (Tagetes erecta Additives (2012a) mutagenesis. Mar.Drugs, 9, 1607-1624. and Tagetes the increasing preference for good quality and patula) appearance of meat, meat products, and fish. Bhosale P., 2004. Environmental and cultural stimulants Rose fruit in the production of carotenoids from (Rosa canina) Global carotenoids market is expected to reach microorganisms. Appl. Microbiol. Biotechnol., 63, Carrot USD 1.53 Billion by 2021 and, due to the 351–361. β-carotene (solid All animal species X Chlorella vulgaris EURL-FA Feed increasing number of health-conscious Blanco A.M., Moreno J., Del Campo J., Rivas J., form) Dunaliella salina Additives (2010b) consumers and the rising demand for natural Guerrero M., 2006. Outdoor cultivation of lutein-rich Arthrospira maxima coloration, the use of natural carotenoids will cells of Muriellopsis sp in open ponds. Applied Zeaxanthin3 Poultry Marigold EURL-FA Feed Microbiology and Biotechnology, 3(6), 1259-1266. (Tagetes erecta Additives (2012a) contribute to the enhancement of the market Boon C.S., McClements D.J., Weiss J., Decker E.A., and Tagetes growth. 2010. Factors influencing the chemical stability of patula) Paprika The potential health benefits of microalgae carotenoids in foods. Critical Reviews in Food (Capsicum represents the main drive behind the new Science and Nutrition, 50, 515–532. annuum) developments in their usage in feed and foods. Bories G., 2007. Safety and efficacy of Panaferd-AX 1formulated in an organic matrix (red carotenoid rich bacterium Paracoccus 2 formulation containing the active substance and other ingredients Even so, carotenoid production from algae is not carotinifaciens) as feed additive for salmon and trout. 3formulation containing a natural source of the active substance and other ingredients as cost effective as the synthetic counterpart. EURL-FA - EU Reference Laboratory for Feed Additives Scientific opinion of the panel on additives and products or substances used in animal feed, EFSA J., ACKNOWLEDGEMENT 546, 1-30. In the EU, carotenoids used as feed additives Union is currently limited to 80 ppm (mg/kg), Britton G., Liaaen-Jensen F., Pfander H., 2009. Carotenoids vol.5: (Eds.) Birkhauser Verlag Basel, are mainly authorised under the category excepted canthaxanthin, whose limit is 8 ppm, The authors would like to thanks the „sensory additives”, as colorants (Vincente et because excessive exposure in humans can lead ISBN 978-3-7643-7500-3. UEFISCDI that have supported 57PTE/2016 Chow E.P.Y., Liong K.H., Schoeters E., 2016. The al., 2017). The addition of natural and synthetic to the development of precipitated crystals in research project. Effect of dietary carotenoids of different forms: carotenoids in layer feeds in the European the retina (Baker, 2001). 83 microemulsified and non-microemulsified on the Kushwaha K., Saini A., Saraswat P., Agarwal M. K., Premkumar L., 2014. Fascinating facts about Stange Klein C., Rodriguez-Concepcion M., 2015. growth performance, pigmentation and hematological Saxena J., 2014. Colorful World of Microbes: phytonutrients in spices and healthy food: Carotenoids in carrot. Pigments in Fruits and parameters in hybrid catfish (Clarias macrocephalus Carotenoids and Their Applications, Article ID scientifically proven facts, Xlibris Publisher. Vegetables, 217-228. & Clarias gariepinus). Journal of Aquaculture – 837891 Hindawi Publishing Corporation; Advances Priyadarshani I., Biswajit R., 2012. Commercial and Story E.N., Kopec R.E., Schwartz S.J., Harris GK., 2010. Research & Development, 7, 437. in Biology, 1-13. industrial applications of micro algae – A review. J. An update on the health effects of tomato lycopene. Dannert C.S., 2000. Engineering novel carotenoids in Maoka T., 2011. Carotenoids in marine animals. Algal Biomass Utln., 3 (4), 89–100. Annual Review of Food Science and Technology, 1, microorganisms. Curr. Opin. Biotechnol., 11, 255- Mar.Drugs, 9(2), 278-293. Qian C., Decker E.D., Xiao H., McClements D.J., 2012. 1-16. 261. Marounek M., Skrivan M., Englmaierova M., 2015. Physical and chemical stability of beta carotene- Tinoi J., Rakariyatham N., Deming R.L., 2005. Simplex Das A., Yoon S.-H., Lee S.-H., Kim J.-Y., Kim S.-W., Comparison of natural and synthetic carotenoids: enriched nanoemulsions: Influence of pH, ionic optimization of carotenoid production by 2007. An update on microbial carotenoid production: effect on yolk colour and oxidative stability of yolk strength, temperature and emulsifier type. Food Rhodotorula glutinis using hydrolyzed mung bean Application of recent metabolic engineering tools. lipids. International Journal of Advances in Science Chemistry, 132, 1221– 1229. waste flour as substrate. Proc Biochem., 40: 2551- Applied Microbiology and Biotechnology, 77, 505– Engineering and Technology, ISSN: 2321-9009 Rock C.L., 2009. Carotenoids and cancer. Carotenoids 2557. 512. Special Issue-5. vol.5: Nutrition and helath. Birkhauser Verlag basel. Vershinin, A., 1999. Biological functions of carotenoids DeQuiros A.R.B., Costa H.S., 2006. Analysis of Masetto A., Flores-Cotera L.B., Diaz C., Langley E., 269-286. - diversity and evolution. BioFactors., 10(2-3), 99– carotenoids in vegetable and plasma samples: A Sanchez S., 2001. Application of a complete factorial Rodriguez-Amaya D.B., 2015. Carotenes and 104. review. J. Food Composit. Anal., 19, 97-111. design for the production of zeaxanthin by xanthophylls as antioxidants. In: Handbook of Vincent U., Serano F., Von Holst C., 2017. Development Diler I., Dilek K., 2002. Significance of pigmentation Flavobacterium sp. J. Biosci. Bioeng., 92(1), 55-58. antioxidants for food preservation,Woodhead and validation of a multi-analyte method for the and use in aquaculture. Turkish Journal of Fisheries Mata-Gómez L.C, Montañez J.C, Méndez-Zavala A., Publishing Series in Food Science, Technology and regulatory control of carotenoids used as feed and Aquatic Science, 2, 97-99. Aguilar C.N., 2014. Biotechnological production of Nutrition, 17–50. additives in fish and poultry feed, Food Dutta D., Chaudhuri U.R., Chakraborty R., 2005. carotenoids by yeasts: an overview. Micro Cell Fact., Sales J.N., Dias L.M., Viveiros A.T., Pereira M.N., Addit.Contam. Part A Chem.Anal.Control Expo.Risk Structure, health benefits, antioxidant property and 13(1), 1. Souza J.C., 2008. Embryo production and quality of Assess., 34(8), 1285-1297. processing and storage of carotenoids. African Matsuno T., 2001. Aquatic animal carotenoids. Fish. Holstein heifers and cows supplemented with beta- Yanar M., Büyükçapar H.M., Yanar Y., 2016. Effects of Journal of Biotechnology, 4(13), 1510–1520. Sci., 67, 771–789. carotene and tocopherol. Animal Reproduction hot and sweet red peppers (Capsicum annuum) as Esfahani-Mashhour M., Moravej H., Mehrabani- Mattea F., Martin A., Cocero M.J., 2009. Carotenoid Science, 106, 77–89. feed supplements on pigmentation, sensory properties Yeganeh H., Razavi S.H., 2009. Evaluation of processing with supercritical fluids. J. Food Eng., 93, Santos-Bocanegra E..; Ospina-Osorio X., Oviedo- and weight gain of rainbow trout. Ann. Anim. Sci., coloring potential of Dietzia natronolimnaea biomass 255-265. Rondon E.O., 2004. Evaluation of xanthophylls 16(3), 825–834. as source of canthaxanthin for egg yolk pigmentation. McGraw K.J., Beebee M.D., Hill G.E., Parker R.S., extracted from Tagetes rectus (Marigold Flower) and Zaheer K., 2017. Hen egg carotenoids (lutein and Asian-Aust. J. Anim. Sci., 22(2), 254 – 259. 2003. Lutein-based plumage coloration in songbirds Capsicum sp. (Red Pepper Paprika) as a pigment for zeaxanthin) and nutritional impacts on human health: García-Chavarría M., Lara-Flores M, 2013. The use of is a consequence of selective pigment incorporation egg-yolks campare with synthetic pigments. A review. Cyta – Journal of Food, (15(3), 474–487. carotenoid in aquaculture. Research Journal of into feathers. Comparative Biochemistry and International Journal of Poultry Science, 11, 685-689. Zakynthinos Z., Varzakas T., 2016. Carotenoids: from Fisheries and Hydrobiology, 8(2), 38-49. Physiology. Part B., 135, 689–696. Shahidi, F., Metusalach A., Brown J.A, 1998. Carotenoid plants to food industry. Current Research in Nutrition Gharibzahedi S.M.T., Razavi S.H., Mousavi S.M., Mezzomo N., Ferreira S., 2016. Carotenoids pigments in seafood and aquaculture. Critical and Food Science, 4(Special Issue 1), 38-51. Moayedi V., 2012. High efficiency canthaxanthin functionality, sources, and processing by supercritical Reviews of Food Science and Nutrition, 38, 1-67. Zoz L., Carvalho J.C., Socco V.T., Casagrande T.C., and production by a novel mutant isolated from Dietzia technology: a review. Hindawi Publishing Sies H., Stahl W., 1995. Vitamins E and C, beta- Cardoso L., 2015. Torularhodin and torulene: natronolimnaea HS-1 using central composite design Corporation, Journal of Chemistry, Article ID carotene, and other carotenoids as antioxidants. Am J bioproduction, properties and prospective analysis. Ind. Crop Prod. 40, 345-354. 3164312, 1-16. Clin Nutr., 62(6 Suppl), 1315S-1321S. applications in food and cosmetics - a review. Gładkowski W., Kiełbowicz G., Chojnacka A., Gil M., Mohiseni.M., 2017. Medicinal herbs, strong source of Sloan D.B., Moran N.A., 2012. Endosymbiotic bacteria Brazilian Archives of Biology and Technology, Trziszka T., Dobrzański Z., Wawrzeńczyk C., 2011. antioxidant in aquaculture: a mini review. Mod Appl. as a source of carotenoids in whiteflies. Biol. Lett., 58(2), 278-288. Fatty acid composition of egg yolk phospholipid Pharm. Pharmacol. 1(1), 1-5. 8(6), 986–9. fractions following feed supplementation of Moran N.A, Jarvik T., 2010. 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84 microemulsified and non-microemulsified on the Kushwaha K., Saini A., Saraswat P., Agarwal M. K., Premkumar L., 2014. Fascinating facts about Stange Klein C., Rodriguez-Concepcion M., 2015. growth performance, pigmentation and hematological Saxena J., 2014. Colorful World of Microbes: phytonutrients in spices and healthy food: Carotenoids in carrot. Pigments in Fruits and parameters in hybrid catfish (Clarias macrocephalus Carotenoids and Their Applications, Article ID scientifically proven facts, Xlibris Publisher. Vegetables, 217-228. & Clarias gariepinus). Journal of Aquaculture – 837891 Hindawi Publishing Corporation; Advances Priyadarshani I., Biswajit R., 2012. Commercial and Story E.N., Kopec R.E., Schwartz S.J., Harris GK., 2010. Research & Development, 7, 437. in Biology, 1-13. industrial applications of micro algae – A review. J. An update on the health effects of tomato lycopene. Dannert C.S., 2000. Engineering novel carotenoids in Maoka T., 2011. Carotenoids in marine animals. Algal Biomass Utln., 3 (4), 89–100. Annual Review of Food Science and Technology, 1, microorganisms. Curr. Opin. Biotechnol., 11, 255- Mar.Drugs, 9(2), 278-293. Qian C., Decker E.D., Xiao H., McClements D.J., 2012. 1-16. 261. Marounek M., Skrivan M., Englmaierova M., 2015. Physical and chemical stability of beta carotene- Tinoi J., Rakariyatham N., Deming R.L., 2005. Simplex Das A., Yoon S.-H., Lee S.-H., Kim J.-Y., Kim S.-W., Comparison of natural and synthetic carotenoids: enriched nanoemulsions: Influence of pH, ionic optimization of carotenoid production by 2007. An update on microbial carotenoid production: effect on yolk colour and oxidative stability of yolk strength, temperature and emulsifier type. Food Rhodotorula glutinis using hydrolyzed mung bean Application of recent metabolic engineering tools. lipids. International Journal of Advances in Science Chemistry, 132, 1221– 1229. waste flour as substrate. Proc Biochem., 40: 2551- Applied Microbiology and Biotechnology, 77, 505– Engineering and Technology, ISSN: 2321-9009 Rock C.L., 2009. Carotenoids and cancer. Carotenoids 2557. 512. Special Issue-5. vol.5: Nutrition and helath. Birkhauser Verlag basel. Vershinin, A., 1999. Biological functions of carotenoids DeQuiros A.R.B., Costa H.S., 2006. Analysis of Masetto A., Flores-Cotera L.B., Diaz C., Langley E., 269-286. - diversity and evolution. BioFactors., 10(2-3), 99– carotenoids in vegetable and plasma samples: A Sanchez S., 2001. Application of a complete factorial Rodriguez-Amaya D.B., 2015. Carotenes and 104. review. J. Food Composit. Anal., 19, 97-111. design for the production of zeaxanthin by xanthophylls as antioxidants. In: Handbook of Vincent U., Serano F., Von Holst C., 2017. Development Diler I., Dilek K., 2002. Significance of pigmentation Flavobacterium sp. J. Biosci. Bioeng., 92(1), 55-58. antioxidants for food preservation,Woodhead and validation of a multi-analyte method for the and use in aquaculture. Turkish Journal of Fisheries Mata-Gómez L.C, Montañez J.C, Méndez-Zavala A., Publishing Series in Food Science, Technology and regulatory control of carotenoids used as feed and Aquatic Science, 2, 97-99. Aguilar C.N., 2014. Biotechnological production of Nutrition, 17–50. additives in fish and poultry feed, Food Dutta D., Chaudhuri U.R., Chakraborty R., 2005. carotenoids by yeasts: an overview. Micro Cell Fact., Sales J.N., Dias L.M., Viveiros A.T., Pereira M.N., Addit.Contam. Part A Chem.Anal.Control Expo.Risk Structure, health benefits, antioxidant property and 13(1), 1. Souza J.C., 2008. Embryo production and quality of Assess., 34(8), 1285-1297. processing and storage of carotenoids. African Matsuno T., 2001. Aquatic animal carotenoids. Fish. Holstein heifers and cows supplemented with beta- Yanar M., Büyükçapar H.M., Yanar Y., 2016. Effects of Journal of Biotechnology, 4(13), 1510–1520. Sci., 67, 771–789. carotene and tocopherol. Animal Reproduction hot and sweet red peppers (Capsicum annuum) as Esfahani-Mashhour M., Moravej H., Mehrabani- Mattea F., Martin A., Cocero M.J., 2009. Carotenoid Science, 106, 77–89. feed supplements on pigmentation, sensory properties Yeganeh H., Razavi S.H., 2009. Evaluation of processing with supercritical fluids. J. Food Eng., 93, Santos-Bocanegra E..; Ospina-Osorio X., Oviedo- and weight gain of rainbow trout. Ann. Anim. Sci., coloring potential of Dietzia natronolimnaea biomass 255-265. Rondon E.O., 2004. Evaluation of xanthophylls 16(3), 825–834. as source of canthaxanthin for egg yolk pigmentation. McGraw K.J., Beebee M.D., Hill G.E., Parker R.S., extracted from Tagetes rectus (Marigold Flower) and Zaheer K., 2017. Hen egg carotenoids (lutein and Asian-Aust. J. Anim. Sci., 22(2), 254 – 259. 2003. Lutein-based plumage coloration in songbirds Capsicum sp. (Red Pepper Paprika) as a pigment for zeaxanthin) and nutritional impacts on human health: García-Chavarría M., Lara-Flores M, 2013. The use of is a consequence of selective pigment incorporation egg-yolks campare with synthetic pigments. A review. Cyta – Journal of Food, (15(3), 474–487. carotenoid in aquaculture. Research Journal of into feathers. Comparative Biochemistry and International Journal of Poultry Science, 11, 685-689. Zakynthinos Z., Varzakas T., 2016. Carotenoids: from Fisheries and Hydrobiology, 8(2), 38-49. Physiology. Part B., 135, 689–696. Shahidi, F., Metusalach A., Brown J.A, 1998. Carotenoid plants to food industry. Current Research in Nutrition Gharibzahedi S.M.T., Razavi S.H., Mousavi S.M., Mezzomo N., Ferreira S., 2016. Carotenoids pigments in seafood and aquaculture. Critical and Food Science, 4(Special Issue 1), 38-51. Moayedi V., 2012. 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