Natural Sources of Food Colorants for Artificial Additives

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This entry is adapted from the peer-reviewed paper 10.3390/foods12224102

The demand of healthier food products and products made with natural ingredients has increased overwhelmingly, led by the awareness of human beings of the influence of food on their health, as well as by the evidence of side effects generated by different ingredients such as some additives. This is the case for several artificial colorants, especially azo colorants, which have been related to the development of allergic reactions, attention deficit and hyperactivity disorder. All the above has focused the attention of researchers on obtaining colorants from natural sources that do not present a risk for consumption and, on the contrary, show biological activity. The most representative compounds that present colorant capacity found in nature are anthocyanins, anthraquinones, betalains, carotenoids and chlorophylls.

natural colorants azo colorants anthocyanin betalain carotenoid chlorophyll natural sources

1. Introduction

Color is one of the most important organoleptic characteristics of food products since it is one of the parameters that gives the consumer an idea about the food’s acceptability, its composition, flavor and/or freshness ^[1]. According to the Food and Drug Administration (FDA), a food colorant is “any dye, pigment, or substance which when added or applied to a food, drug or cosmetic, or the human body, is capable (alone or through reactions with other substances) of imparting colour” ^[2].

Colorants are added to food products for different reasons such as restoring the original color lost due to the influence of exposure to light, temperature variations, moisture and/or storage conditions; enhancing the natural color or adding color to colorless products ^[2]^[3].

Color additives can be classified as subject to certification and exempt from certification. First are colorants that are obtained synthetically, while second comprise colorants that are obtained from vegetables, minerals, or animals; therefore, this classification is the same as artificial and natural colorants. Another way of categorizing them is as straight colors, lakes, and mixtures. Straight colors refer to colorants that have not been mixed or chemically reacted with any other substance (e.g., FD&C Blue No. 1). Lakes for food use refers to straight colors that have been chemically reacted with precipitants and substrates such as aluminum cation as the precipitant and aluminum hydroxide as the substratum (e.g., Blue 1 Lake). Finally, mixtures are colorants generated by mixing a color additive with one or more color additives or non-colored diluents without chemical reaction ^[2]^[4].

Currently, artificial food colorants are widely use by the food industry, among others, in children’s products, since they have high intensity, stability, uniformity of color, and are cheap. However, their use has been controversial since 1976 when Feingold ^[5] reported a quick improvement in the behavior of children with attention deficit and hyperactivity disorder (ADHD) due to the elimination of the intake of artificial food colorants (mostly azo colorants) and flavorings. Since then, several studies have been published, the most well-known being the one provided by McCann ^[6], who evidenced the increase in the incidence of ADHD including inattention, impulsivity, and overactivity not only in children with extreme hyperactivity, but also in the general child population due to the consumption of artificial food colors (AFCs) and other additives such as sodium benzoate preservative (E 211). It is important to mention that a few studies regarding the effect of artificial food colorants in adults have been completed, such as that of Murdoch et al. ^[7], who evidenced a significant increase in the histamine levels of adults after the consumption of 150 mg of tartrazine; Di Lorenzo et al. ^[8], who evidenced symptoms of allergy in patients with chronic urticaria to different additives including tartrazine and erythrosine, in response to mixture of additives; Pestana et al. ^[9], who did not find evidence of statistical differences between the reaction to tartrazine and the placebo in 26 adults with allergic pathologies such as rhinitis, asthma or urticaria; and Park et al. ^[10], who tested a mix of seven food additives that included amaranth, erythrosine, tartrazine and sunset yellow FCF in 54 adults with allergic diseases evidencing that there were no significant differences in the reactions to the mix of additives and the placebo. However, the vast majority of studies on the effect of artificial food colorants have been carried out on children as they are more affected than the rest of the population, mainly due to the lack of control in their diet and to the fact that they are highly attracted by colors and present a higher consumption of processed sweet products such as candies or ice creams ^[11].

Consequently, the responsible entities, EFSA (European Food Safety Agency) in the European Union and the FDA (Food and Drug Administration) in the United States of America, have carried out different reviews of the available studies in order to evaluate the safety of azo colorants, among other additives. On one hand, the most important communications have been the evaluation carried out in 2009 in the European Union by the EFSA where only a decrease in the acceptable daily intakes (ADI; the amount of the substances that a person can consume daily without risk) of three of these problematic colorants (quinoline yellow, E104; sunset yellow FCF, E110; and Ponceau 4R, E124) was established ^[12]^[13]^[14]; and the statement release in 2013 by EFSA, where it was assured that a revaluation from the ADI of any of the azo colorants was not necessary and it was recommended that new tests should be carried out related to genotoxicity ^[15]. On the other hand, in 2011, the Food Advisory Committee from the FDA from the United States concluded that a relationship between children’s consumption of AFCs and behavioral effects had not been established ^[16].

However, the scientific community has continued working to establish the possible harmful effects of AFCs, having evidenced so far the potential of azo colorant to alter the normal functioning of the kidneys and liver, generation of reactive oxygen species, induction of hypersensitivity ^[11], proinflammatory responses ^[17] and, principally, an effect on ADHD ^[18]. In addition, in recent years, the use of AFCs in the food industry has exponentially increased, to the point that in some categories, mainly in children’s products such as cakes, chips, chocolates, ice creams, drinks, etc., all products contain at least one AFC, and it should be noted that there have even been cases where the product exceeded the allowed level ^[18]^[19]^[20]. On the whole, the different results have evidenced that is highly possible that many children may be consuming higher amounts of AFCs than previously thought ^[21].

As a result of all the evidence regarding the problems that AFCs can generate, as well as the growing interest of the general population in healthier and more natural food, it has been necessary to provide a revaluation of the AFCs ADI, or the approval of their use, and at the same time, to acknowledge the development of natural colorants that can be used instead of AFCs obtaining the same or even better results in the final product.

2. Principal Colorant Compounds Found in Natural Matrices

Among the compounds present in plants that show coloring properties, there are four main groups, anthocyanins, which have the widest range of colors presenting hues from blue to red; betalains, for which the color could be red-violet, yellow-orange color, and mainly pink; carotenoids, which can range from red to yellow; and chlorophylls, which are mostly green but also can present blue tones. All these compounds, in addition to their colorant capacity, exhibit different bioactive properties evidencing health benefits with their consumption ^[22].

2.1. Anthocyanins

Anthocyanins are pigments, for which the color can vary from blue to red. They derive from flavonoids and their base structure is an anthocyanidin which is constituted by two hexanes linked by three carbon atoms that form an oxygenated heterocycle; this structure presents a positive charge and is also known as a flavylium ion. When this anthocyanidin is in its glycosylated form, linked to a sugar, it is known as an anthocyanin (Figure 1) and this sugar can be bonded in different positions, mainly position C3 or C5 of the first ring. In addition, anthocyanin can be hydroxylated and/or methoxylated in different positions. This chemical structure of conjugated double bonds provides them with strong colors as well as high antioxidant properties through the scavenging of free radicals ^[23]^[24]^[25].

Figure 1. Principal colorant compounds found in natural sources.

More than 700 different anthocyanins have been reported ^[26]^[27], which are differentiated from each other via the number and position of the hydroxy and methoxy substitutions, and the type and position of the sugar linked to the anthocyanidin ^[24]^[28]. These variations provide them with different colors, stability, bioavailability, and health effects ^[24]^[29].

Twenty-seven anthocyanidins have been observed in nature; however, cyanidin, delphinidin, pelargonidin, peonidin, malvidin, and petunidin represent 90% (50%, 12%, 12%, 12%, 7%, and 7%, respectively) of the anthocyanidins found in plants, being cyanidine-3-glucoside which is the predominant anthocyanin. The main edible sources of anthocyanins are berry fruits, including blueberry (Vaccinium corymbosum L.), bilberry (Vaccinium myrtillus L.), and strawberry (Fragaria vesca L.), among others. In addition, they can also be found in other foods, such as red sweet potato (Ipomoea batatas L.) and purple corn (Zea mays L.) ^[28]. Furthermore, different possible health benefits have been related to anthocyanins, such as possessing anti-inflammatory, anticancerogenic, antimutagenic and cardioprotective effects, being regulators of total cholesterol, LDL, HDL, and triglyceride levels, anticoagulants, and providing help in the prevention of neurological and cognitive alterations ^[24].

Anthocyanins are one of the biggest types of natural pigment; hence, they have been highly studied for the generation of natural colorants, as an alternative to artificial one. Nevertheless, one of the biggest problems to overcome is the low stability that anthocyanins present, since they can be affected by light, temperature, pH, metal ions, enzymes, oxygen, and co-pigments ^[30].

2.2. Betalains

Betalains are water soluble nitrogen-containing pigments with a core protonated structure commonly known as betalamic acid [4-(2-oxoethylidene)-1,2,3,4-tetrahydropyridine-2,6-dicarboxylic acid that can be found as betacyanins or betaxanthins, which have a pink–violet and yellow–orange color, respectively. Up to now, 75 different betalains have been identified, wherein, 51 of them are betacyanins. Therefore, betacyanins are the most commonly found. These pigments belong to 17 families of the order Caryophyllales. They are present in fruits, flowers, leaves, and roots, with betanin being the most common structure. On the other hand, betaxanthins can also be found in tubers, but not as much in leaves, with proline-betaxanthin being the most common ^[31]^[32]. The main edible sources of betalains are red beet roots (Beta vulgaris L.), amaranth (Amaranthus sp.) cacti (Opuntia sp.) fruits, and dragon fruit (Hylocereus sp.), among others. Different bioactivities have been related to betalains such as antioxidant, antibacterial, antifungal, antiprotozoal, and anticancer properties. Some of these effects, particularly the antioxidant properties, are related to the chemical structure of betalains, as they have a phenolic group and a cyclic amine, which are excellent electron donors and exhibit antiradical activities ^[32].

Betalains are also characterized by their reduced stability, as these pigments are thermolabile and affected by light, high water activity, pH under 3 or above 7 and oxygen. For these reasons, recent research has focused on the preservation of the chemical structure and the functionality of betalains, by using different techniques such as complex formation, copigmentation and encapsulation ^[33].

2.3. Carotenoids

Carotenoids are lipophilic pigments that go from yellow to red. They are composed of a C₄₀ skeleton which contains polyene groups with end groups at both ends of the chain (Figure 1). Carotenoids can be classified in two categories according to their composition, namely carotenes and xanthophylls. Carotenes are hydrocarbons and include α-carotene, ß-carotene or lycopene. Xanthophylls contain functional groups with oxygen and include lutein, zeaxanthin or astaxanthin. These pigments can be found in different natural sources such as fruits, seed, roots and flowers, fulfilling functions as antioxidants, color attractants or hormone plant precursors. About 50 different carotenoids have been described in common human foods, including tomatoes (Solanum lycopersicum L.), persimmon (Diospyros kaki L.) and Gac fruit (Momordica cochinchinensis Spreng.), these being some of the most representative sources. Regarding their beneficial effect on human health, some beneficial properties have been related in relation to ocular, cardiovascular and fatty liver diseases, liver fibrosis and cancer. The majority of these potential health benefits have been attributed to the anti-inflammatory and immunomodulatory activity, and the regulation of cell cycle/apoptosis exhibited by these molecules ^[34]^[35].

Regarding the stability of these pigments, carotenoids are susceptible to various degradation and isomerization reactions, as was mentioned, above which cause their discoloration and can lead to a decrease and thus reduction in their biological activity. In particular, the stability of carotenoids is mainly affected by thermal processes, as well as by the presence of oxygen or light ^[36].

2.4. Chlorophylls

Chlorophylls are green natural colorants present in a wide number of green fruits and vegetables. Spinach, alfalfa, grass and nettles are natural sources of chlorophylls. These pigments are constituted of a porphyrin ring with a magnesium atom as the central metal (chlorophyll a and b) or without a central metal (e.g., phaeophytin a and b, pheophorbide a and pyropheophytin a), with an isocyclic five-membered ring and a chain of propionic acid esterified with phytol (Figure 1). To date, there are more than 100 chlorophylls or chlorophyll derivatives reported, with chlorophylls a and b being the most common in plants, which are found in a 3:1 proportion, respectively ^[37]^[38]^[39]. Chlorophylls present a significant antioxidant activity through chelation of reactive ions and scavenging of free radicals preventing DNA damage and lipid peroxidation, as well as antimutagenic and antigenotoxic activity through the prevention of mutagen migration and its coupling to DNA by the formation of a chlorophyll–mutagen complex which facilitates the degradation of the mutagen ^[37]^[40].

Chlorophylls are highly sensitive pigments that could be degraded by several factors, such as oxygen, light, heat, acids, and enzymes, causing a color change from green to brown, mostly due to the substitution of the central magnesium ion by two hydrogens, losing the green color characteristic of the presence of the magnesium ion ^[37]^[41].

3. Source of Natural Colorants as a Potential Replacers of Artificial Food Colorants

Currently, the European Food Safety Authority (EFSA) and the Food and Drugs Administration (FDA) have approved the use of different extracts from plants as colorants, as can be seen in Table 1, with the principal colorant compounds, anthocyanins, carotenoids, and chlorophylls being present, so there is a wide variety of colors. However, some of them are limited in their use to exact types of products, e.g., butter pea flower extract, which in the United States can only be used in beverages, juices, ice cream and candies, or copper complex of chlorophylls, which can only be used in citrus-based dry beverage mixes. Moreover, there is a bigger problem with these natural colorants than the restrictions of use to specific products, their low stability and therefore the small range of use, as these natural colorants can be affected by pH, temperature and light, among others, that make their use difficult in variety of products.

Table 1. Natural food colorants with approved use in Europe and United States, by EFSA and FDA, respectively ^[42]^[43].

Color	Origin	Scientific Name	Chemical Compound	Isolation	E Number	CFR Section
Blue	Butterfly pea flower extract	Clitoria ternatea L.	Anthocyanins	Aqueous extraction	NA	73.69
Blue-green	Spirulina extract	Arthrospira platensis	Phycocyanins		NA	73.530
Green	Edible plant material, grass, lucerne and nettle extract	Gramineae, Medicago sativa L., Urtica dioica L.	Chlorophylls	Solvent extraction	E140i Cl natural green 3; magnesium chlorophyll; magnesium phaeophytin
Green-blue	Edible plant material, grass, lucerne and nettle extract	Gramineae, Medicago sativa L., Urtica dioica L.	Chlorophyllins	Solvent extract and saponification	E140ii Cl natural green 5; sodium chlorophyllin; potassium chlorophyllin
Green-blue	Edible plant material, grass, lucerne and nettle extract	Gramineae, Medicago sativa L., Urtica dioica L.	Copper complex of chlorophylls	Solvent extraction and addition of a salt of copper	E141i Cl natural green 3; copper chlorophyll; copper phaeophytin
Green-blue	EU: Edible plant material, grass, lucerne and nettle. US: alfalfa extract	US: Medicago sativa L.	Copper complex of chlorophylls	Solvent extract, saponification, and addition of a salt of copper	E141 (ii) CI Natural Green 5; Sodium Copper Chlorophyllin; Potassium Copper Chlorophyllin	73.125
Yellow	Turmeric extract	Curcuma longa L.	Curcumin	Solvent extraction	E100 Cl natural yellow 3, turmeric yellow, diferoyl methane	73.600
	Turmeric oleoresin	Curcuma longa L.	Curcumin	Extraction with exact solvents	NA	73.615
Yellow-orange	Edible plants, carrots, vegetable oils, grass, alfalfa, and nettle extract	Daucus carota L.	Carotenoid—Beta-carotene	Solvent extraction	E160a (ii) Cl food orange 5	73.95
Yellow-orange	Algae extract	Dunaliella salina Teod.	Carotenoid—Beta-carotene	Essential oil extraction	E160a (iv) Cl Food orange 5
Yellow-brown	Edible fruits and plants, grass, lucerne and African marigold extract	African marigold: Tagetes erecta L.	Carotenoids–Lutein	Solvent extraction	E161b Lutein; mixed carotenoids; xanthophylls
Red-brown	Annatto tree seeds outer coating extract	Bixa orellana L.	Carotenoid–bixin	Solvent extraction	E160b (i) Annatto; bixin; norbixin; Cl natural orange 4	73.30
	Annatto tree seeds outer coating extract	Bixa orellana L.	Carotenoid–bixin	Alkali extraction	E160b (ii) Cl natural orange 4
	Annatto tree seeds outer coating extract	Bixa orellana L.	Carotenoid–bixin	Vegetal oil extraction	E160b (ii) Cl natural orange 4
Yellow-orange	Carrot oil	Daucus carota L.	Carotenoid	Solvent extraction	NA	73.300
Yellow-orange	Dried stigma powder	Crocus sativus L.	Carotenoid–crocin	Dry grinding	NA	73.500
Red	Ground dried paprika	Capsicum annuum L.	Carotenoid–capsanthin and capsorubin	Dry grinding	NA	73.340
Red	Paprika oleoresin	Capsicum annuum L.	Carotenoid–capsanthin and capsorubin	Solvent extraction	E160c	73.345
Red	Red tomatoes extract	Lycopersicon esculentum L.	Lycopene	Solvent extraction	E160d (ii) Natural yellow 27	73.585
	Red beets roots extract	Beta vulgaris L. var. Rubra	Betalaine	Pressing, aqueous extraction or dehydrating	E162 Beet red	73.40
Red-purple	Grape or black carrot extract	Vitis vinifera L., Daucus carota L.	Anthocyanin	Aqueous extraction	163	73.169
	Grape skin extract	Vitis vinifera L.	Anthocyanin–enocianina	Aqueous extraction	163	73.170

E number: European number; CFR: Code of Federal Regulations; NA: not approved.

4. Incorporation of Natural Food Colorants in Food Matrix

Different studies report the novel use of natural food colorants in food product formulations in order to replace the use of synthetic ones. In this sense, Table 2 shows the most recent studies in this field.

Table 2. Recent studies of natural food colorants incorporated in different food matrices.

Food Color	Natural Colorant	Food Matrix	Natural Sources	Main Food Characteristics: Color and Stability	Reference
Red-purple	Anthocyanins	Yogurt	Black rice bran extract	Pink color with 0.2% (L: 80.20, C: 9.67, h: 18.34) and purplish pink with 0.6%, the highest percentage added (L: 68.42, C: 15.23, h: 8.73)	^[44]
		Yogurt	Red onion by-products	Time zero: 0.05 mg cya-3-gluE/g (L: 75.27, a: 11.20, b: 9.55) After 4 weeks of storage 0.039 mg cya-3-gluE/g (L: 75.19, a: 11.35, b: 9.75)	^[45]
		Yogurt	Eggplant	Color parameters of the yogurt with 1% of encapsulated extract: L: 83.74, a: 3.96 b*: 8.18.	^[46]
		Bakery products	Onion skin	Color parameters of the extracts: L: 22.56, a: 20.84, b*: −0.78.	^[47]
		Marmalade	Black carrot	Thermal processing caused a loss of anthocyanins (79.2–89.5%)	^[48]
		Red beer	Eggplant peel extract	Color parameters: L: 74.67, a: 9.86, b*: 21.76	^[49]
	Carotenoids (lycopene)	Butter	Tomato skin	Extract concentration: 20 mg/kg Color parameters, at initial time: L: 48.78, a: 2.36, b: 14.17 Color parameters at 4 months of storage at 4–6 °C: L: 48.37, a: 2.25, b: 14.18	^[50]
		Mayonnaise	Tomato skin	Extract concentration: 50 mg/kg Color parameters, at initial time: L: 55.82, a: 10.32, b: 19.95 Color parameters at 4 months of storage at 4–6 °C: L: 53.66, a: 9.64, b: 19.10	^[50]
		Ice cream	Tomato skin	Extract concentration: 70 mg/kg Color parameters, at initial time: L: 84.41, a: 11.56, b: 28.59 Color parameters at 4 months of storage at −25 °C: 83.97, a: 11.16, b*: 21.29	^[50]
		Ice cream	Tomato peel	The ice cream prepared with 3% of extract obtained the highest score in all the parameters of the sensorial analysis	^[51]
Pink	Betalains	Gummy candies	Cactus (Opuntia ficus-indica L. Mill.) fruit pulp	High stability of the color in the gummy candies were observed after 30 days of storage al 4 °C	^[52]
		Yogurt	Pitaya	The yogurts with 0.5% and 2% of the colorant were statistically similar to the commercial yogurts with beetroot and carmine colorants, respectively	^[53]
		Cookies	Gomphrena globose L.	Color parameters of samples with the lyophilized extract: L: 56.3, a: 22.1, b: 8.0 Color parameters of samples with the spray dried extract: L: 56.0, a: 25.5, b: 4.3	^[54]
		Ice cream	Gomphrena globose L.	Color parameters: L: 86, a: 8, b*: 2.4	^[55]
		Tagliatelle pasta	Flowers of Amaranthus caudatus	Color parameters: L: 62, a: 17, b*: 8	^[55]
		Meringue cookies	Red-fleshed pitaya peels	Color parameters: L: 79.6, a: 14.5, b*: 1.24	^[55]
Yellow-Orange	Carotenoids	Dough biscuits	Mango peel	Color parameters of product with 20% of mango peel: L: 52.90, a: 7.71, b*: 22.02	^[56]
Yellow-Orange	Carotenoids	Macaroni	Mango peel	-	^[56]
Green	Chlorophylls	Syrup	Centella asiatica L.	The syrups with the extracts treated with zinc and copper were stable and presented minimum change in color, mostly an increase in the h* value.	^[57]
		Bread	Centella asiatica L.	The bread with the extract treated with zinc presented a yellow–green color, while the one with the extract treated with copper presented a green color. All of them changed significantly after 7 days	^[57]
		White chocolate	Nannochloropsis oculata D.J. Hibberd	Samples with the encapsulated extract presented a higher quantity of chlorophylls. However, the samples with free extract presented a better stability of the color along the 28 days	^[58]
		Chewing gum	Isochrysis galbana Pascher	Samples showed a decrease in hardness as well as in the cohesiveness, which is advantageous for a chewing gum	^[59]
		Yogurt	Spirulina	The preparation with 0.25% showed the best acceptability in the sensory analysis	^[60]
Blue	Anthocyanins	Cooked rice	Butterfly pea flowers	The incorporation of 0.6% of extract resulted in better acceptance by consumers	^[61]

L*: lightness; a*: red/green coordinate; b*: yellow/blue coordinate; h: hue; C*: chroma.

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