Aguirre-Joya et al. - 2020 - Nanosystems of plant-based pigments and its relationship with oxidative stress

Food and Chemical Toxicology 143 (2020) 111433
Contents lists available at ScienceDirect
Food and Chemical Toxicology
journal homepage: www.elsevier.com/locate/foodchemtox
Nanosystems of plant-based pigments and its relationship with oxidative
stress
T
Jorge A. Aguirre-Joyaa, Luis E. Chacón-Garzaa, Guillermo Valdivia-Najárb,
Roberto Arredondo-Valdésc,d, Cecilia Castro-Lópeze, Janeth M. Ventura-Sobrevillaa,
Cristóbal N. Aguilar-Gonzálesf, Daniel Boone-Villag,∗
a
School of Health Science, Universidad Autonoma de Coahuila, Unidad Norte, Piedras Negras, Coahuila, Mexico
CONACYT - Department of Food Technology, Centro de Investigación y Asistencia en Tecnología y Diseño del Estado de Jalisco (CIATEJ), Zapopan, Jalisco, Mexico
c
Nanobioscience Group, Chemistry School, Universidad Autonoma de Coahuila, Blvd. V. Carranza e Ing. J. Cardenas V., Saltillo, Coahuila, Mexico
d
Research Group of Chemist Pharmacist Biologist, Chemistry School, Universidad Autonoma de Coahuila, Blvd. V. Carranza e Ing. J. Cardenas V., Saltillo, Coahuila,
Mexico
e
Laboratory of Chemistry and Biotechnology of Dairy Products, Research Centre in Food & Development, A.C (CIAD, A.C.), Gustavo Enrique Astiazarán Rosas Highway,
Hermosillo, Sonora, Mexico
f
Food Research Group, Chemistry School, Universidad Autonoma de Coahuila, Blvd. V. Carranza e Ing. J. Cardenas V., Saltillo, Coahuila, Mexico
g
School of Medicine North Unit, Universidad Autonoma de Coahuila, Unidad Norte, Piedras Negras, Coahuila, Mexico
b
A R T I C LE I N FO
A B S T R A C T
Keywords:
Food pigments
Nanotechnology
Oxidative stress
Non-communicable diseases
Plant-based pigments are widely present in nature, they are classified depending on their chemical structure as
tetrapyrroles, carotenoids, polyphenolic compounds, and alkaloids and are extensively used in medicine, food
industry, clothes, and others. Recently they have been investigated due to their role in the areas of food processing, food safety and quality, packaging, and nutrition. Many studies indicate a relationship between
bioactive pigments and Non-Communicable Diseases derived from oxidative stress. Their biological applications
can help in preventing oxidative injuries in the cell caused by oxygen and nitrogen reactive species. Those
pigments are easily degraded by light, oxygen, temperature, pH conditions, among others. Nanotechnology
offers the possibility to protect bioactive ingredients and increase its bioavailability after oral administration.
Safety to humans (mainly evaluated from toxicity data) is the first concern for these products. In the present
work, we present a comprehensive outlook of the most important plant-based pigments used as food colorants,
the principal nanotechnology systems prepared with them, and the relationship of these compounds with the
oxidative stress and related Non-Communicable Disease.
1. Introduction
1.1. Generalities
Natural pigments are produced by microorganisms, vegetables,
animals, and minerals. However, plant-based pigments are the most
widely distributed in nature. These compounds are located into the
plastids or in the vacuoles in the protoplasm of vegetable cells and are
responsible for the bright color of a large number of vegetables, fruits,
leaves, and flowers. The natural pigments are chemical and biological
molecules, also known as biochromes and widely used in medicines,
food, clothes, furniture, cosmetics, and other colored products (Shetty
et al., 2018). In fact, the color in these compounds is produced by the
chromosphere, a molecule-specific structure capable of capture and
∗
reflect/refract the energy attained from the visible solar radiation.
Moreover, natural pigments not only produce color, but they are also
responsible for essential functions in vegetable cells as protection and
metabolic reactions.
In past years, the consumers begin to question the use of synthetic
pigments in the food industry, and natural compounds have gained
considerable importance due to the increasing number of published
studies indicating that those substances may play an essential role in
human health. In this context, some plant-based pigments present antioxidant capacity, avoiding oxidative stress (OxS) and reducing the risk
of developing degenerative diseases.
Corresponding author.
E-mail address: [email protected] (D. Boone-Villa).
https://doi.org/10.1016/j.fct.2020.111433
Received 6 February 2020; Received in revised form 7 May 2020; Accepted 10 May 2020
Available online 20 June 2020
0278-6915/ © 2020 Elsevier Ltd. All rights reserved.
Food and Chemical Toxicology 143 (2020) 111433
J.A. Aguirre-Joya, et al.
Fig. 1. Basic structure of relevant plant-based pigments.
compounds are widely distributed in fruits, vegetables, flowers, and
seeds with colors ranging from yellow to intense red (Feng et al., 2018).
Carotenoids play an essential role in photosynthesis and light absorption, avoiding the photooxidation of basic compounds of the plants.
They can be found in nature as carotenes like lycopene and α, β, and γ,
which are linear hydrocarbons; and also, as xanthophylls, the oxygenated derivates of carotenes, such as lutein, violaxanthin, neoxanthin,
and zeaxanthin. The xanthophyll is the most abundant carotenoid in
nature; however, the carotenes are the most important carotenoids for
the food industry (Botella-Pavía and Rodríguez-Concepción, 2006). The
phenolic compounds are the most important secondary metabolites
present in plant tissues. Phenolic substances participate in defense responses against herbivores, bacterial, and fungal attack, but also to
other metabolic processes as pollination and plant camouflage
(Alasalvar et al., 2001).
Moreover, phenolic compounds are closely associated with flavor,
color, and astringency characteristics of fruits and vegetables. Phenolic
compounds are mainly divided into phenolic acids and polyphenols
(like lignans, stilbenes, tannins, coumarins, curcuminoids, and the most
plentiful group of phenolic compounds in nature, flavonoids) (Gan
et al., 2019). In general, phenolic compounds are created by two metabolic pathways, the simple-phenol compounds are created by the
acetic acid pathway, while most of the phenylpropanoids are formed by
the shikimic acid pathway (Hollman, 2001; Zhao, 2015). Finally, nitrogenated compounds are organic compounds synthesized as secondary metabolites in plant tissues and serve as a defense against insect
and herbivorous animals. These substances exhibit potent bioactivity as
regulators of the Central Nervous System (Allegra et al., 2019;
Lenkiewicz et al., 2016). The most representative nitrogenated compounds are alkaloids and betalains. Alkaloids are classified as proto
alkaloids when they are not heterocyclic but contain nitrogen, and as
1.2. Classification
Pigments can be classified by their origin as natural/synthetic or
organic/inorganic, but also by the chemical structure of the chromophore as chromophores with conjugated systems and metal-coordinated
porphyrins (Aggarwal et al., 2019). The classification of plant pigments
is based on their chemical structure and arranged into four categories:
tetrapyrroles (green), carotenoids (yellow, orange and red), polyphenolic compounds (red-blue and violet), and nitrogenated compounds like betalains (red-violet), and colored alkaloids (red-orange)
(Fabi and do Prado, 2019; Moser and Kräutler, 2019; Polturak and
Aharoni, 2018; Xiong et al., 2019). The categories of plant-based pigments and their representative compounds are presented in Fig. 1.
The tetrapyrroles are an abundant group of pigments in nature,
responsible for diverse biochemical functions and essential in most
known living organisms. Those compounds play essential roles in plants
such as photosynthesis, respiration, and assimilation of nitrogen/sulphur (Tanaka et al., 2011). In plants, four classes of tetrapyrroles are
produced: chlorophyll, heme, siroheme, and phytochromobilin. The
most abundant tetrapyrroles in nature are the chlorophylls, responsible
for the green color of plants. These compounds act as photosynthetic
pigments, capturing light energy and transferring it to the reaction
centre to trigger the synthesis of organic compounds necessary for the
plant. Chlorophylls a and b are the most reported isoforms in the photosynthetic tissues of plants where they can be found in a 3:1 relation,
respectively. Those are located at the vegetal chloroplasts, linked by
both, attraction and affinity to phytol groups of lipids and porphyrin
groups of proteins creating crystalline spherical conglomerates inside
the cells (Badui Dergal, 2015).
Carotenoids are one of the main groups of plant-based pigments
present in nature with almost six hundred identified members. These
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Food and Chemical Toxicology 143 (2020) 111433
J.A. Aguirre-Joya, et al.
Table 1
Carotenoids in aromatic herbs (μg/100 g).
Plant
Common name
Scientific name
Celery
Celery white
Celery green
Celery green cooked
Saffron
Coriander
Parsley
Apium graveolens L. var. Dulce
Apium graveolens L. var. Dulce
Apium graveolens L. var. Dulce
Apium graveolens L. var. Dulce
Crocus sativus L.
Coriandrum sativum cv. Mogiano
Petroselinum hortense
β-carotene
β-cryptoxanthin
lycopene
16,200
65 ± 2
570 ± 14
1109 ± 77
226
ND
ND
ND
ND
2100
7200 ± 900
1630
Lutein
26,400
163 ± 10
860 ± 17
1335 ± 91
3780
8700 ± 700
ND = No detected.
compounds linked via methine bridge in either a linear or a cyclic
array. The synthesis of tetrapyrroles is regulated by the biosynthetic
enzymes and regulators located in the cellular chloroplasts of plants
(Weatherby and Carter, 2013). The most representative tetrapyrroles in
nature are the chlorophylls, which are di-hydro-porphyrins integrated
by four pyrrole groups and a cyclopentanone ring by double conjugated
bones, linked to magnesium and some methyl, ethyl, vinyl, and propionic acid chains (Ferruzzi et al., 2001; Khyasudeen et al., 2019;
Schwartz et al., 1983). Because of their chemical structure, most of the
chlorophylls are highly stables in polar solvents like water. However,
low pH, non-polar solvents, high temperatures, and presence of organic
acids trigger the degradation of chlorophylls, replacing the magnesium
by hydrogen and forming pheophytin compounds with brown and olive
colors (MOSS, 1968). Moreover, light exposition and presence of enzymes as chlorophyllase and lipoxygenase enhance the phytol degradation and oxidation of chlorophylls (Carocho et al., 2018; Randy,
2010).
The carotenoids are hydrophobic polyols with a 40 carbon atoms
chain, conjugated double bonds, and some have hydrocarbon rings in
one or both ends of the molecule (Schwartz and Lorenzo, 1990).
Moreover, carotenoids are more stable at levels of water activity of the
medium in the average value or lower (Anguelova and Warthesen,
2000; Hassan et al., 1994). The stability of carotenoids is mainly influenced by their unsaturated structure, leading to the oxidation of
double conjugated bonds and the isomerization of the structure
(Ganguly and Sastry, 1985; Onyewu et al., 1982). Those mechanisms
are triggered by the presence of metals, oxygen, light, and high temperatures which prompt the creation of free radicals (García-de Blas
et al., 2013).
Phenolic compounds are formed by at least one aromatic ring and a
hydroxyl group. The phenolic acids (benzoic and cinnamic) are integrated with one ring, while polyphenols (flavonoids, anthocyanins,
and tannins) by two aromatic rings and a heterocyclic one. These
compounds are highly unstable due to their reactivity to organic acids,
sugars, or phenolic compounds. High temperature, oxygen, and light
are responsible for phenolic compound degradation (Ephrem et al.,
2018). An increasing pH triggers the deprotonation of the flavin group
of anthocyanins, turning the red color into blue (Nakayama et al.,
2012). Interaction of flavonoids, anthocyanins, tannins, and betaines
with other compounds such as metallic ions, acids, and enzymes leads
to the formation of uncolored compounds (Debicki-Pospišil et al., 1983;
Francis, 1999). On the other hand, most of the phenolic compounds are
water-soluble and highly degradable by lixiviation processes (Schwartz
et al., 2017).
The most important nitrogenated compounds are alkaloids and betalains. Alkaloids are characterized by some extremely different chemical structures that contain at least one nitrogen atom, they including
heterocyclic ring systems and even some compounds with neutral and
acidic properties (Dostál, 2000; Manske, 2010). Those compounds are
relatively stable at room temperature; however, the presence of oxygen
and carbon dioxide in the air leads to the formation of carbonated salts
true alkaloids, when they are heterocyclic and contain nitrogen (Rosa
et al., 2007). The synthesis of alkaloids occurs through the acetate,
shipmate, mevalonate, and deoxyxylulose pathways leading to their
diverse chemical structures (Wink, 2007) (see Table 1).
2. Structure and stability
The stability of natural pigments is highly conditioned by their
chemical structure (Table 2), which can be altered by different factors
like pH, light, oxygen, and the chemical substances present in the environment. In general, the absence of light, lack of oxygen, and low
temperature are well known as the principal factors contributing to the
stability of pigments (Khoo et al., 2017).
The molecules of tetrapyrroles consist of four pyrrole-derived
Table 2
Basic structures of plant-based pigments.
Compound name
Chemical structure
Curcumin
Catechol
Gallic acid
Pyrogallol
Alpha-tocopherol
Anthocyanins
Rosmarinic acid (from Rosemary)
Apigenin (from clove)
3
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J.A. Aguirre-Joya, et al.
CAR + ROO* → CAR* + ROOH (hydrogen abstraction)
and colored compounds, respectively. Alkaloids are soluble in acid
water and polar organic solvents but insoluble in neutral water. The
positive charge of the nitrogen atoms facilitates binding to the negative
charge of proteins (Aniszewski, 2015). In the other hand, betalains are
water-soluble, red-violet pigments with a structure made by an immonium conjugated of betalamic acid and cyclo-Dopa and aminated
compounds that may present coloration from yellow and orange to red
and violet, but the general structure of these compounds may be diversified by glycosylation and acylation processes (Rodriguez-Amaya,
2019). A system of conjugated double bonds constitutes the chromophore of betalains. Similarly to alkaloids, acidic (lower than 3) or alkaline (higher than 7) pH, light, high temperature, high water activity,
metal cations, as well as some enzymes (like peroxidases), and oxidant
agents (like O2) may be detrimental for betalains stability; the degree of
acylation or glycosylation also affects their molecular stability
(Herbach et al., 2007; Rodriguez-Amaya, 2019).
CAR + ROO* → (ROO-CAR)* (addition)
Where ROO* is a free radical and CAR is the carotenoid. The presence
of conjugated double bonds enables these compounds to accept electrons from reactive species, and then neutralize free radicals (Milani
et al., 2017). The rates and mechanisms of the reactions depend on the
properties of free radicals and the environment (aqueous or lipid phase)
(Mao et al., 2018).
Astaxanthin is a carotenoid found in high concentrations in the
microalga Haematococcus pluvialis as well as in fungi, complex plant,
salmonids, and crustaceans (Kang and Kim, 2017; Grimmig et al., 2017;
Visioli and Artaria, 2017). Astaxanthin is a carotenoid with high commercial potential in the pharmaceutical and food industries. Astaxanthin is a potent antioxidant (Visioli and Artaria, 2017) with a biological activity many times higher than that of α-tocopherol and βcarotene (Grimmig et al., 2017). The presence of the hydroxyl (OH) and
keto (C]O) moieties on each ionone ring explains some of its unique
features, namely, the ability to be esterified and a more polar nature
than other carotenoids (Jia and Ni, 2016). It has suggested that their
powerful antioxidant effect is due to this ketone-bearing ionone rings
by stabilizing radicals more effectively synergistically with polyene
backbone (Grimmig et al., 2017). The astaxanthin exerts its antioxidant
activity through various mechanisms including absorbing free radicals
into the polyene chain, by donating an electron, or by forming chemical
bonds with reactive species. This antioxidant versatility is a characteristic of astaxanthin and sets this molecule apart from other carotenoids (Grimmig et al., 2017). In toxicological aspects about human
health have been well-characterized the astaxanthin (unlike many other
plants or animal-derived food ingredients), resulting in astaxanthin as a
compound safe for human consumption (Visioli and Artaria, 2017).
The carotenoid lycopene can protect cells against oxidative damage
and is thought to be responsible for decreasing the risk of non-communicable diseases (NCD), including cardiovascular disease (CVD)
(Mao et al., 2018; Meroni and Raikos, 2018). The main sources of lycopene in the western diet are tomato products; at least 85% of our
dietary lycopene comes from both tomato fruits and tomato-based
products like ketchup, juice, and sauce. By using different in
vitro models (ECV304 endothelial cells, HUVECs, human macrophages),
lycopene has demonstrated to be a potential antiatherogenic agent, able
to prevent OxS and apoptosis. The hypothesized mechanism of action
for lycopene is mediated by preventing the oxidation of low-density
lipoprotein (Meroni and Raikos, 2018).
Flavonoids belong to a group of natural substances with variable
phenolic structures and are found in fruit, vegetables, grains, bark,
roots, stems, flowers, tea, and wine (Jia and Ni, 2016). More than 4000
varieties of flavonoids have been identified, many of which are responsible for the attractive colors of flowers, fruit, and leaves (Nijvelt
et al., 2018; Ibrahim et al., 2017) like flavonols, anthocyanidins, flavonones, Isoflavones, and flavones (Datta et al., 2004).
Their basic chemical structure consists of 15 carbon atoms with two
phenyl rings and one heterocyclic ring. Flavonoids such as genistein,
tangeritin, quercetin, and apigenin have antioxidant and anti-inflammatory effects that can be used as protective supplements against
3. Natural presence in food
The natural pigments like carotenoids, flavonoids, and others are
part of the human food chain. More than 650 different types of carotenoids exist in nature (Eggersdorfer and Wyss, 2018; Milani et al.,
2017). The carotenoids are mainly located in fruits and vegetables, as
well as in processed products. Dias et al. (2009) prepared a table reporting the content of carotenoids in Latin American food, some of
whose results are presented in Tables 2–4. It is also common to find
carotenoids in artificial pigments in commercial food products (Table 5)
(Shen et al., 2014).
However, only 30–40 carotenoids have been found in human blood
samples, with lycopene, lutein, zeaxanthin, β-cryptoxanthin, and βcarotene being the most abundant (Eggersdorfer and Wyss, 2018;
Milani et al., 2017). In 2004, the European Prospective Investigation
into Cancer and Nutrition measured the plasma levels of six carotenoids
in 3043 people and found the following levels: lycopene
0.43–1.32
μmol/L,
lutein
0.26–0.70
μmol/L,
β-carotene
0.21–0.68 μmol/L, β-cryptoxanthin 0.11–0.52 μmol/L, α-carotene
0.06–0.32 μmol/L, zeaxanthin 0.05–0.13 μmol/L (Eggersdorfer and
Wyss, 2018; Al-delaimy et al., 2004).
The primary benefits of carotenoids can be explained by their antioxidant potential. However, specific carotenoids may also act through
additional mechanisms (Eggersdorfer and Wyss, 2018). The antioxidant
properties of β-carotene are due to its exceptional capability to scavenge free-radicals and to quench singlet oxygen (1O2). β-Carotene
quenches 1O2 mostly through a physical mechanism, where excitation
energy of 1O2 is transferred to β-carotene, and the excited triplet state
β-carotene dissipates the energy through rotation and vibrational interactions with surrounding solvents and then returns to the ground
state (Mao et al., 2018). β-Carotene is also able to quench 1O2 chemically to initiate oxidation and produce several oxidized products (degradation). β-Carotene and other carotenoids scavenge free radicals
mainly through three mechanisms (Milani et al., 2017; Mao et al.,
2018):
CAR + ROO* → CAR*++ ROO− (electron transfer)
Table 3
Carotenoids in vegetables of the genus Brassica (μg/100 g).
Plant
Common name
Scientific name
Broccoli
Kale
Brussel sprouts
Cauliflower
Cabbage
Brassica
Brassica
Brassica
Brassica
Brassica
oleracea
oleracea
oleracea
oleracea
oleracea
var. Italica Plenck
var. Acephala DC.
subsp. Gemmifera (DC.) O.E. Schulz
subsp. Botrytis (L.) Metzg.
f. Viridis Duchesne
β-carotene
Lutein
1890 (1570–2220)
3070 (2280–4240)
77 ± 10
2 ± 0,2
3460 (3110–3960)
4440 (3290–5740)
185 ± 19
4 ± 0,4
250 ± 10
4
Zeaxantina
10 ± 10
Neoxantina
violaxantina
740 (670–830)
1200 (880–2590)
600 (310–680)
2050 (1610–4220)
Food and Chemical Toxicology 143 (2020) 111433
J.A. Aguirre-Joya, et al.
Table 4
Carotenoids in fruit vegetables (μg/100 g).
Plant
Common name
Scientific name
Pumpkin
Squash
Melon
Cucumber
Pepper
Pepper
Pepper
Pepper, Jalapeño,
green
Watermelon
Curcubita pepo L. var. Styriaca Greb.
Cucurbita maxima Duchesne
Cucumis melo var. Adana Pangalo Cucumis melo
Cucumis sativus subsp. Agrestis Gabaev Cucumis sativa L.
Capsicum annuum L., cvvar. Ancho. Capsicum indicum Lobel.
Capsicum annuum L., cvvar. Guajillo. Capsicum indicum Lobel.
Capsicum annuum L., cvvar. Mulato. Capsicum indicum Lobel.
Capsicum annuum L. var. Annuum L. cv. ‘Jalapeño'. Capsicum
indicum Lobel. Capsicum annuum L
Citrullus lanatus (Thunb.) Matsum. & Nakai Citrullus lamatus
cv. Crimson Sweet
Solanum lycopersicum Lam.Cultivar santa cruz
Tomato
β-carotene
β-criptoxantina
44 - 65,17
186–275
11 ± 1
1527 (1481–1572)
1153 (1095–1210)
938 (796–1079)
6374 (381–8576)
Lutein
Lycopene
β-Carotene
Vegetable beverage
Orange juice
Lemon bread
Herb tea
Corn chip
Canned corn
Canned pumpkin
Canned sweet potato
Orange jelly
Cocktail sauce
Tomato pasta
Ketchup
Salad dressing
14.79 ± 0.69
1.27 ± 0.01
6.37 ± 0.2
14.56 ± 0.44
1.76 ± 0.01
7.41 ± 0.11
1.91 ± 0.13
1.89 ± 0.06
158.37 ± 3.94
23.07 ± 0.91
2.59 ± 0.08
5.50 ± 0.04
0.21 ± 0.01
1.31 ± 0.11
2.38 ± 0.13
2.43 ± 0.17
14.12 ± 0.84
21.39 ± 0.97
7.75 ± 0.20
185.22 ± 5.43
8.68 ± 0.77
4.01 ± 0.02
7.76 ± 0.18
7.40 ± 0.41
1.66 ± 0.06
1.49 ± 0.01
1.84 ± 0.01
729
472 (299–644)
233 (23,9–442)
Lutein
Zeaxantina
49
8170 ± 1510
30 ± 10
16 ± 1
190 ± 30
10 ± 10
32,6 (1,45–63,7)
836
260 ± 170
3500 ± 200
510 ± 1,1
3110 ± 20,2
454 (258–649)
213 (127–298)
130 (2,17–258)
pheophytin b, pheophorbide a, and pheophorbide b) were also demonstrated (Ferreira and Sant, 2017).
Betalains are a class of water-soluble, nitrogen-containing compounds that comprise more than 55 derivatives of the betalamic acid
(Celli and Brooks, 2017). Common sources of betalains include red and
yellow beetroot (Beta vulgaris L. spp. Vulgaris) (< comment message=The citation "Mikolajczyk-Bator, 2017" has been changed to match
the author name in the reference list. Please check here and in subsequent
occurrences. > < /comment > Mikołajczyk-Bator
and
Czapski, 2017), colored Swiss chard (B. vulgaris L. spp. Cicla) (Yu et al.,
2015), leafy and grainy amaranth (Amaranthus sp.) (A and A, 2013),
prickly (or cactus) pear (Opuntia sp.) (Celli and Brooks, 2017), and
pitaya (Hylocereus sp.) (Celli and Brooks, 2017). Betalains can have
effects antioxidant, antiproliferative, cardioprotective, anti-inflammatory, and antimicrobial (Celli and Brooks, 2017).
Several studies strongly confirmed the high radical-scavenging activity of betalains. In the betalamic acid, the core structure of betalain
may reduce two molecules of Fe3+ to Fe2+ by donating 2 electrons to
an oxidizing agent. Consequently, the pH dependence of betalains antiradical activity was reported (Slimen et al., 2017).
Carotenoids, the primary sources of vitamin A, are widely used in
pharmaceutical, nutraceutical, and cosmeceutical industries. Vitamin
A, lutein, and zeaxanthin are essential factors for human vision (Ban
and Šircelj, 2011). Vitamin A also plays a crucial role in immunity, cell
differentiation, maintenance of cell membrane integrity, embryonic
development, and reproduction in humans (Priyadarshani, 2017). Different carotenoids (like astaxanthin, fucoxanthin, lutein, β-carotene,
and lycopene) may reduce the risk of developing cancer and CVD, reduce cancer progression, and help to avoid the onset of other pathologies like gastric and duodenal ulcers, allergies, viral and bacterial infections, and vascular fragility by reducing OxS (Ban and Šircelj, 2011;
Galasso et al., 2017; Priyadarshani, 2017). Retinoids and carotenoids
are potent antioxidants and anti-inflammatory agents that also have
neuroprotective properties (Honarvar et al., 2016).
Table 5
Concentrations of artificial and carotenoid pigments in commercial food products.
Sample
Lycopene
the development of cancer (Ibrahim et al., 2017). Flavonoids with
biological activity are often called bioflavonoids. They possess the
ability to capture superoxide, hydroxyl, and lipid radicals (Moro et al.,
2017; Brodowska, 2017).
Flavonoids can prevent injuries caused by free radicals in various
ways. One of those ways is the direct scavenging of free radicals.
Flavonoids are oxidized by radicals resulting in a more stable, less-reactive molecule. The radicals are inactivated according to the following
equation (Ibrahim et al., 2017)
Flavonoid (OH) + R* > flavonoid (O*) + RH
Where R* is a free radical and O* is an oxygen-free radical. Epicatechin
and Rutin are also powerful radical scavengers.
There is much controversy regarding the purported toxic or even
mutagenic properties of flavonoids as quercetin. There are reports
about its possible involvement in the cell damage using in vitro model;
however, the results have shown an inverse relationship between the
intake of flavonoids (e.g., quercetin) and lung cancer in human studies
(Nijveldt et al., 2001). One possible explanation for these conflicting
data is that flavonoids are toxic to cancer immortalized cells but are not
toxic or are less toxic to normal cells (Nijveldt et al., 2001).
Chlorophyll a is the most abundant pigment in all photosynthetic
organisms; it plays a central role in photosynthesis by absorbing and
transferring light energy (Ferreira and Sant, 2017; Li and Chen, 2013;
Chen, 2014). Chlorophyll has numerous applications in the biotechnological field and human health. It may be used as a natural food
colorant, deodorant, and in the production of skincare cosmetics
(Ferreira and Sant, 2017). The molecule has been described as an antitumor agent (Vesenick et al., 2012). Furthermore, chlorophyll and its
derivative, pheophytin, have anti-inflammatory effects. The antioxidant
activities of chlorophyll a and b and its derivatives (pheophytin a,
4. Food-use nanosystems
4.1. Generalities
Nanotechnology represents a source of new responses and possibilities to the challenges that are faced by the food industry nowadays,
particularly for food sustainability and security (Enescu et al., 2019). As
already mentioned, plant-based pigments are unstable against endogenous factors (enzymes, water activity, temperature, oxygen content, light, and pH, among others) (Vila et al., 2015; Wijaya, 2011).
Some alternatives have been developed to improve their stability and
increase their application in the food industry. Nanoencapsulation
technologies, defined as the entrapment of a compound (core material)
5
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J.A. Aguirre-Joya, et al.
the lipophilic components in an aqueous phase (Arana et al., 2015;
Weiss et al., 2008). Furthermore, Nanostructured lipid carriers (Fig. 2d)
are partially crystallized lipid nanoparticles with a mean size lower
than 100 nm, dispersed in an aqueous phase with an emulsifier (Tamjidi
et al., 2014). On the other hand, nanosystems can be produced with
special equipment (Fig. 2e) by three typical techniques 1) electrospinning: a polymer solution is extruded to form a droplet, and an electric
field generates a fine fiber; 2) electrospraying: an electrical force atomizes a liquid that flows out from a capillary nozzle at a high electric
potential and is forced into fine and highly charged droplets; and 3)
nanospray drying: the spraying of a solution into droplets dried by hot
air (Arpagaus et al., 2018a; Bock et al., 2011; Wen et al., 2017).
Nanocarriers and nanocapsules increase the bioavailability of active
compounds by rising the surface/volume ratio, resulting in a higher
adherence in the small intestine and improving the interaction with
enzymes and metabolic factors; also they can easily emigrate trough
tissue walls to penetrate directly into the target cell to release their
cargos, like plant-derived polyphenols, antioxidants, and pigments
(Katouzian et al., 2017; Assadpour and Jafari, 2018). Nanocapsules are
a type of shell with a core composed of a solid shell surrounding a core
capable of entrapping bioactive compounds (Vert et al., 2012). Another
beneficial characteristic of nanocarriers is the capacity to improve the
hydrophobic nutraceuticals solubility with a minimum influence into
organoleptic qualities and appearance of the final product, such as
drinks and beverages (McClements and Jafari, 2018a).
4.2. Preparation
The selection of an appropriate method for the preparation of nanosystems depends on the physicochemical character of the polymer
(proteins, polysaccharides, lipids or synthetic polymers) and the compound to be loaded (Pal et al., 2011). Besides, to achieve the properties
of interest (i.e. final particle size, solubility and stability, desired release
profile, biocompatibility, among others), the mode of preparation also
plays a key role (Konwar and Ahmed, 2016; Tyagi and Pandey, 2016).
The techniques for the preparation of nanoparticles can be classified
in 1) Top-down process and 2) Bottom-up process. The bottom-up
processes are based on self-organization and self-assembly of the molecules by coacervation, inclusion complexation, layer by layer deposition, or encapsulation; some authors suggest that these techniques
are better to control the size of particles (Jia et al., 2016).
On the other hand, the leading examples of top-down techniques are
nanospray drying, extrusion, emulsification, and electrospinning
(Rehman et al., 2020). Since in the last years, the study of these encapsulation methods has been increasing, the mechanisms and equipment destined for nanosystem creation can be hugely diverse; thus,
brief characteristics are described below.
Fig. 2. Types of food nanosystems studied and developed in recent years.
into a shell (wall material) with the obtention of particles with a particle size lower than 1.0 μm, has been utilized to this purpose (Akhavan
and Jafari, 2017). Some authors mention that nanoparticles in the
range of 50–200 nm are useful for biological applications, like target
drug delivery (Fung et al., 2015); nevertheless, the European Commission defines nanomaterials as “a natural, incidental or manufactured
material containing particles, in an abundant state or as an aggregate,
or as agglomerate and where, for 50% or more of particles in the
number size distribution, one or more external dimensions is in a size
range of 1–100 nm” (Jeevanandam et al., 2018).
There has been previously reported that the main applications of
nanomaterials in the food and beverage industry are in packaging
materials and nutraceutical supplements for health applications
(Enescu et al., 2019). Depending on the method of preparation and
ingredients used, different structures can be prepared (De, 2017) like
nanocapsules, nanocarriers, nanocrystals, and nanoemulsion (Islan
et al., 2017). Nanoemulsions (Fig. 2a) corresponds to an emulsion with
disperse-phased droplets (with a diameter of 50–200 nm) into a continuous phase in the presence of a surfactant. It may be oil-in-water (O/
W) or water-in-oil (W/O) or bi-continuous, and either liquid in liquid,
or liquid in solid (Livney, 2015; McClements and Jafari, 2018a, 2018b;
Sanguansri and Augustin, 2006).
On the other hand, Liposomes or vesicles (Fig. 2b) are structures
constituted of phospholipid that present concentric lipid bilayers alternating with aqueous compartments. These structures vary in diameter with sizes in the nanometric to micrometric range; but liposomes
smaller than 200 nm are sometimes named nanoliposomes (Müller and
Landfester, 2015; Pereira dos Santos et al., 2018). Additionally, Solidlipid nanoparticle (SLN) (Fig. 2c) is the denomination for nanometricsize dispersion of lipids that should be solid at body temperatures
(37 °C). An SLN is composed of a solid lipid core with a compound
linked to the lipid matrix, a surfactant, and cosurfactant which stabilize
4.2.1. Top-down methods
Nano spray drying: As already mentioned, the spray drying technology is based on the transformation of a fluid (liquid state) into a
dried particulate (solid-state) form by spraying the fluid into a hot
drying medium (Arpagaus et al., 2017). A nanospray dryer is an ultrasonic atomizer capable to producing nano-sized droplets from an
initial liquid; it works with vibrating mesh technology and a flow of hot
air to evaporate the water in the feed liquid and form nanoparticles, it is
a simple, rapid and relative low-cost process with a limitation for volatile compounds (Arpagaus et al., 2018b). In this sense, the nanospray
dryer equipment is an ultrasonic atomizer capable of producing nanosized droplets from a feed liquid formulation (e.g. aqueous and organic
solutions, emulsions, and suspensions). It works with vibrating mesh
technology and a flow of hot air to evaporate the water in the feed
liquid and form nanoparticles (dry powders). The produced powders
are high in quality and have low moisture content, resulting in high
shelf stability, as well as a better redispersibility in aqueous solutions
(Ishwarya et al., 2015; Murugesan and Orsat, 2012). Finally, in order to
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Mahdi, 2016). Fundamentally, the electrospinning process is divided
into three basic steps: 1) the polymers have to be completely dissolved
in appropriate solvents, or they are melted; 2) during the main process,
a high voltage has to be used to create an electrically charged jet of a
polymer solution or melt out of the pipette; and 3) the polymer has to
be ejected from a needle with an inner diameter between 0.5 and
1.5 mm (Ghorani et al., 2017; Kurečič and Sfiligoj Smole, 2013). This
technology can produce fibers with thinner diameter; in general, the
average diameter of these fibers varies with process conditions and can
reach diameters between ≈5 nm and ≈10 μm (Kurečič and Sfiligoj
Smole, 2013). Electrospinning process, fiber morphology, fibrous
structure, and fiber production rate are influenced by several parameters (Niu et al., 2019). For example 1) the types of materials utilized
to generate nanofibers (e.g. organic polymers); 2) the solution properties (viscosity, polymer concentration, the molecular weight of the
polymer, electrical conductivity, elasticity, and surface tension); 3) the
processing conditions (applied voltage, distance from spinneret to the
collector, volume feed rate, and spinneret diameter); and 4) the ambient conditions (temperature, humidity, and atmospheric pressure)
(Ghorani et al., 2017; Shao et al., 2015; Tang et al., 2014; Xue et al.,
2019).
produce nanoscale particles whit this technology, some experimental
considerations are necessary. For example 1) the influences of process
parameters (e.g. the spray mesh size, the spray rate intensity, the drying
gas inlet temperature, and the drying gas flow rate); 2) the solid concentration (which influences the feed rate, particle size, and outlet
temperature); 3) the selection of the solvent and mixing ratio (which
must be based on the solubilization of the bioactive compound and the
encapsulating wall materials); and 4) the selection of suitable wall
material (based on mechanical strength, high encapsulation efficiency,
and final viscosity) (Arpagaus et al., 2017; Gharsallaoui et al., 2007;
Schoubben et al., 2013).
Extrusion: The nanoextrusion technique is based on the immobilization of the active core material into in a polysaccharide gel,
which is then put in contact with a multivalent ion (Teixeira da Silva
et al., 2014). During the production of the nanoparticles, the active core
material is incorporated in a sodium alginate solution. The mixture is
subjected to a drop-wise extrusion via a syringe into a hardening solution (e.g. calcium chloride), which results in the formation of the
particles with typical sizes between 200 and 1000 nm (Khinast et al.,
2013). Although the main advantage of nanoextrusion is to produce
capsules of a variety of compound with a long shelf life (Shishir et al.,
2018), it is not suitable for industrial operations because it presents
many restrictions such as difficulty to scale up, production of relatively
large particle size with a porous structure and is suitable for limited
matrix materials (Jia et al., 2016). Thus, in order to improve the application of nanoextrusion technique, it has been reported several
strategies/considerations. When applying nanoextrusion it is necessary
to take into account 1) the use of multi nozzle-system or rotating disk;
2) the influences of process parameters (e.g. the nozzle diameter, the
rotation frequency of cutting wire, the number and diameter of the
wire, among others); 3) the possibility of applying extrusion vibration
or an electric field; and 4) the viscosity of wall material (Rodríguez
et al., 2016; Shishir et al., 2018).
Emulsification: Emulsification technique is a process which consists
of mixing two or more immiscible liquids into a stable one, through
homogenization by the application of stirring, one of the dispersed liquids has the bioactive compounds. It includes single emulsion (O/W
and W/O) and double emulsion (W/O/water and O/W/oil), and this
technique is recommended for both hydrophilic and hydrophobic ingredients (Rehman et al., 2019). Nevertheless, since emulsions are
usually thermodynamically unstable, it is necessary to add surfactants
and stabilizers in order to stabilize emulsion droplets (Jenjob et al.,
2019). Once the emulsion process ends, it has been described that this
technique provides submicron polymer particles, typically with an
average size between 20 and 200 nm (Marzuki et al., 2019). From a
more specific point of view, it has been reported that there are two
main approaches to prepare nanoemulsions. The first is known as Low
energy method, which is distinguished by the preparation of nanoemulsions via spontaneous emulsification without the use of any device
or energy (Solans and Solé, 2012). The second one is known as High
energy method, in which case has required the use of specific devices to
supply enough energy to increase the water/oil interfacial area for
generating the nanodroplets (Marzuki et al., 2019). Although each of
these approaches has its advantages; in general, for the preparation of
nanoemulsions, it is proposed to take into account several preparation
conditions such as 1) the operating conditions (energy intensity to
produce disruptive forces and duration of the process); 2) the sample
composition (oil type, emulsifier type and concentrations); 3) the
physicochemical properties of the phases (interfacial tension and viscosity); 4) the polymer/surfactant ratio (high or low surfactant concentration relative to monomer); and 5) it is required a gradual dilution
of the oil phase with the water phase, or vice versa (A. Salem and M.
Ezzat, 2019; McClements et al., 2015; Wooster et al., 2008).
Electrospinning: Electrospinning technology is an approach that uses
electrostatic forces applied to a biopolymer (with the bioactive compound) and the consequent formation of electrospun fibers (Faridi and
5. Food applications
The use of nanotechnology in the food industry is not only promising but is also acknowledged by the European Commission as part of
its Key Enabling Technologies. It means nanotechnology can help the
food industry to grow competitiveness sustainably (Parisi et al., 2015)
and concordance with diverse United Nation Sustainable Development
Goals, particular goal 3, good health and wellbeing; goal 6, clean water
and sanitization; goal 12, responsible production and consumption, and
goal 13, climate action (Henchion et al., 2019).
As tangible examples of the advantages of nanotechnology in the
food industry are the current inversions of some food companies’ leaders in the area, such as Nestlé, Hershey, Kraft, H.J. Heinz and Unilever
(Momin and Joshi, 2015). As a particular example, we can mention the
low-fat ice-cream from Nestlé that uses nano-emulsion to obtain a lowfat concentration, getting a nano-enabled food (Sampathkumar et al.,
2020).
Due to their size (10−9 m), nanosystems display particular properties that can be different for those exhibits of the same material or
system in macro-scale; nanosystems can improve sensorial characteristics (color, flavor), bioavailability, and solubility, prevent undesirable
physical and chemical reactions, protect sensitive biological compounds from oxidation or degradation (de Souza Simões et al., 2017).
Some practical examples of the use of nanosystems in foods are those
used in drinks and beverages to improve the solubility of hydrophobic
nutraceuticals with a minimum impact on the organoleptic properties
of the final product.
The unique properties of nanosystems can be related to the area-tovolume ratio and the interactions among the nanosystem components
(physical and chemical interactivity) (Silva et al., 2013).
The nanomaterials can be extensively used in practically every area
of the food industry, from the field, food agriculture, processing, storage, and distribution to the final consumer (He et al., 2019). Nevertheless, there is one important aspect to be considered before using
nanosystems efficiently on the food industry: the public acceptance,
often ignored by researchers, public authorities, and manufacturers
(Arnaldi and Muratorio, 2013).
5.1. General examples
The need to preserve food for prolonged periods gave rise to food
processing, the intention of which was to keep the nutritional and organoleptic characteristics of food intact as far as possible, despite food
preservation has existed since prehistoric times, in recent days
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(yellow-orange phenolic component) to get fortified milk with antioxidant capacity.
2) Food safety and quality: The food safety and quality refer to maintain
control along the production and distribution chain, from farm to
plate, to minimize or avoid risks for consumers, maintaining the
nutritional and organoleptic qualities of the food (Eleftheriadou
et al., 2017). For food safety, nanotechnology offers the possibility
to detect in hours or even minutes the food spoilage using nanosensors; they work with thousands of nanoparticles in an array
created to fluorescence in different colors at the contact with food
pathogens (Ravichandran, 2010). Both characteristics are intimately
related to food contact materials (all materials and objects intended
to be in direct contact with food) and packaging including those that
protect and preserve the food during transportation and storage
(Peters et al., 2019).
3) Packaging: Traditional food packages are intended only to protect
the food during storage and transportation, but with the use of nanotechnology in food packaging, there are new functions for food
packaging, such as intelligent and active packaging. Intelligent
packaging refers to the capacity to share information about safety
and quality of the product, like smart labelling with nanosensors to
detect food spoilage in real-time, with time-temperature indicator,
etc. Meanwhile, active packaging uses nanoparticles to improve interactions with polymeric matrix (in the packaging) to favor better
gas, water and/or aroma barrier properties; they also offer other
functions such as antimicrobial, antioxidant, biosensing, and shelflife preservation (Enescu et al., 2019). In the case of food packaging,
shelf-life improvement is a crucial topic where active packaging is
explicitly made to achieve this goal, for active packaging, ingredients can be engineered with active nanoparticles to keep microorganism away from food (Zhong et al., 2017). In this context, a
large variety of natural plant-based pigments has been employed as
antimicrobial and antioxidant ingredients such as catechol, green
tea leaf (Camellia sinensis L.) polyphenols, gallic acid, pyrogallol, αtocopherol, and phenolic extracts from rosemary (Salvia rosmarinus
L.), clove (Syzygium aromaticum L.), and oregano (Origanum vulgare
L.) (Panrong et al., 2019; Topuz and Uyar, 2020; Vilela et al., 2018;
Wrona et al., 2017).
4) Nutrition: The role of nanotechnology in human nutrition is to create
food with better nutritional value for consumers at a lower price as
possible (Handford et al., 2014). There are several examples of nanotechnology applications to achieve food with higher nutritional
value, for instance, nanoencapsulation of bioactive molecules, nutrients and supplements, the nanosizing of food ingredients and
additives and nanotechnology for nutraceutical release (Villena de
Francisco and García-Estepa, 2018). With this applications, nanotechnology makes possible increasing the biological function of
nutrients, improving the sensory characteristics of supplements, the
development of nutraceuticals, increasing the nutrient delivery and
the fortification with vitamins and minerals, as long as other
bioactive compounds (Henchion et al., 2019). Currently, there is
under high demand the commercialization of special food with
particular nutritional quality as the called “superfoods”, “healthy
foods” and “functional foods”, that are in most cases result of plantbased pigment incorporation to improve their nutritional characteristics, as well as preservation and coloration. Despite the high
instability of plant-based pigments, it is a common practice to protect them by micro and nanoencapsulation (Chuacharoen and
Sabliov, 2019; Carvalho Gomes Corrêa et al., 2019). As an example
of functional food with higher pigment concentration is the elaboration of bread from purple pericarp durum wheat rich in anthocyanins to obtain a functional bread (Bianca et al., 2018).
nanotechnology has offered new tools to food processing (Hamad et al.,
2018). Some nanotechnologies used in food processing are: incorporation of nutraceuticals, vitamin and mineral fortification, nutrient delivery and nanoencapsulation of flavors (Huang et al., 2010).
In the food industry, one of the most used components for nanosystems is the polyphenols, since they can be used in food formulations
as anti-microbial, anti-thrombotic, anti-inflammatory, anti-allergic, and
anti-oxidant (Assadpour and Jafari, 2018).
Polyphenols are naturally present in virtually all the plants and
vegetable-derived food, like fruits, vegetables, legumes, cereals, herbs,
and spices, constituting an integral part of a balanced human diet.
Phenolic compounds are secondary metabolites of the plants and are
traditionally classified into two main categories: a) flavonoids and b)
phenolic acids (see section 1.2).
Nanotechnology has diverse applications in the agri-food industry in
1) food processing, 2) food safety and quality, 3) packaging and 4)
nutrition (Henchion et al., 2019). 1) Food processing includes all the
processes that help improve aromas, texture, flavors and colors in the
food, in this last context food color is important in terms of marketability and consumers acceptability, however there has been studies
that correlate the use of synthetic colorants with the possibility of increasing development of cancer, allergies and hyperactivity in children;
for this reason food added with natural colorants (e.g. extracts of plants,
plant-based pigments) are preferred by the consumers (Munawar and
Jamil, 2014); 2) food safety and quality involves diagnostic sensors and
disinfection agents, in the case of diagnostic sensors nano-sensors are
helpful to detect color changes in the food and any gas produced by
microorganisms in the case of spoilage, nano sensors are characterized
by high sensibility compared to traditional sensos (Hamad et al., 2018);
in the case of 3) packaging, nanocomponents are used as food contact
materials, oxygen-scavengers, antimicrobials, and barrier properties
compounds, food packaging provides physical protection for external
interference, such as temperature changes, microbial infection or
spoilage, by oxygen modification but also by antimicrobial nanoparticle
addition (Hamad et al., 2018); there has been demonstrated the efficiency of plant extracts and plant deriver by-products as antimicrobials
and antioxidants, particularly when are added into food packaging
(Jafarzadeh et al., 2020); for 4) nutrition, nanomaterials are used as
supplements and nutraceuticals, like the use of nanotechnology to treat
obesity (J. Li et al., 2019). Anther application of nanotechnology in
nutrition is the development of nano-delivery systems such as nanocapsules, nanospheres, and nanoemulsions were diverse nature-derived
polymers have been used to encapsulate bioactive molecules for instance antimicrobials, antioxidants, nutraceuticals and flavors with the
intention that this natural nano-particles act as preservatives, supplements and flavor enhancements (Jafarizadeh-Malmiri et al., 2019; Luo
and Hu, 2017).
5.2. Specific examples
1) Food processing: Food processing is a necessary process that determines the physicochemical characteristics such as flavor, texture,
and stability of the food. The changes at a nano-scale in the structure
of food systems have a direct repercussion on food quality at a
macro scale, on this aspect nanomaterials are frequently created as
flavor additives, supplements, and preservatives (He et al., 2019),
also are used to produce desirable effects in food processing like
coagulation, emulsifier or homogenizer (Bajpai et al., 2018). One of
the specific examples of nanotechnology in food processing is the
elaboration of nanoemulsions to increase stability. A nanoemulsion
can be defined as an emulsion where the disperse droplets have a
maximum diameter of 500 nm (Ravichandran, 2010). As has been
previously described by Chuacharoen and Sabliov (2019), nanoemulsions can be used in functionalized dairy products with plantderived phenolic colorants to enhance some biological activities of
the final product; they incorporate a nanoemulsion with curcumin
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6. Food nanosystems and oxidative stress
Anthocyanins are derived from phenylpropanoid pathways in the
cytosol and then are transported in vacuoles for storage by anthocyanin
transporters MATE (AM1 and AM3) and ABC (Gu et al., 2019; M'mbone
et al., 2018; Taki et al., 2019). Biosynthesis and accumulation are
regulated two types of genes structural and transcription factors (Ye
et al., 2017), such as MYB-bHLH-WD40 complex for accumulation and
ANS, UFGT, DFR, F3H, and MYB10 for synthesis (Gu et al., 2019; M. Wu
et al., 2019). Plant hormones such as jasmonic acid, abscisic acid (Islam
et al., 2019; Malovini et al., 2019; Moro et al., 2017), and plant growth
regulators such as auxins and cytokinins are internal factors for biosynthesis and accumulation of anthocyanins (Gu et al., 2019; Jia et al.,
2017; Li et al., 2008; Müller et al., 2019).
Betalains are another type of plant-based pigment with important
functions due to their antioxidant properties to eliminate an excess of
ROS in plants and humans. A recent review, the authors indicated that
betalains and anthocyanins have similar aspects like.
6.1. Generalities
Reactive oxygen species (ROS) and reactive nitrogen species (RNS)
are molecules with the ability to oxide and therefore modify human and
plant redox status. The chemical structure of these oxidants species
appears as free radical or non-radicals.
The most common free radical ROS and RNS are singlet oxygen
(O.−2), hydroxyl radical (OH.), hydroperoxyl radical (HOO.), alkoxide
radicals (RCOO.), and thiyl peroxyl radicals (RSOO.), while those nonradicals are hydrogen peroxide (H2O2), anion superoxide (O2.-), nitric
oxide (NO), and peroxynitrite (ONOO−) (Kandola et al., 2015; Singh
et al., 2019). The ROS are generated mainly in mitochondria during
respiration, β-oxidation of lipids, and purine metabolism. The complexes II and III in the electron transport chain convert near of 1–4% of
molecular oxygen into O2.-. Further O2.- is transformed into other ROS,
such as H2O2 and OH., by superoxide dismutase, xanthine oxidase,
Fenton reaction, and other mechanisms. Hydroxyl radical has a short
half-life of 10–9 s but is the most active ROS (Huang, 2019).
The OxS is generated when an imbalance between pro-oxidant and
antioxidant systems occurs in the organism, favoring the first
(Hernández-Ruiz and Villanona-García, B, Guerra-Hernandez, E.
Amiano, P, Ruiz-Canela, M, Molina-Montes, 2019). Oxidative compounds alter the structure of macromolecules such as lipid, DNA, proteins, and carbohydrates, leading to cell injury and diseases (Anavi and
Tirosh, 2020; Sottero et al., 2019; Souliotis et al., 2020; Zhong et al.,
2019; Zorrilla et al., 2019).
In human cells under physiological conditions, mitochondria releases free radicals, that are considered as critical signaling molecules
in essential cellular signaling, so the organism regulates an elaborate
defense mechanism to avoid dyshomeostasis by pro-oxidant effects
(Huang and Li, 2020; Magnani and Mattevi, 2019). Besides the intrinsic
factors, external conditions (like smoking or diet), and physical activity
produce pro-oxidants (Hernández-Ruiz and Villanona-García, B,
Guerra-Hernandez, E. Amiano, P, Ruiz-Canela, M, Molina-Montes,
2019).
1. Both are storage as glycoside in vacuoles,
2. Both are located in dermal and vascular tissues of vegetal organs,
3. Prephenate is a precursor for betalains and phenylalanine for anthocyanins,
4. Both use MYB as cofactor transcription for production.
It is suggested that both pigments cannot exist in the same plant.
However, the molecular mechanism of inhibition has not been demonstrated (G. Li et al., 2019).
Metabolism of plant tetrapyrroles occurs in the stroma of the
chloroplast. The 5-aminolevulinic acid is regulated by light stage and
converted into protochlorophyllide; the photoconversion process produces chlorophyllide and various forms of chlorophylls (Sineshchekov
and Belyaeva, 2019; Y. Wu et al., 2019).
6.3. Oxidative stress and non-communicable diseases
The presence of OxS may produce molecular damage in several
cellular components like proteins, carbohydrates, nucleic acids, and
lipids (Holmström and Finkel, 2014; Kaushal et al., 2019; Reczek and
Chandel, 2015). It is necessary to remark that OxS includes perturbation in Redox signaling rather than only the unbalance between the
concentration of oxidative/antioxidative molecules (Kolbert et al.,
2020; Sturza et al., 2019). Like virtually any other process in metabolism, OxS is not isolated from other cellular conditions. There is literature reporting that a low-grade chronic inflammatory state commonly accompanies OxS (Alissa and Ferns, 2011; Bertrand and Tardif,
2017; Festa Gomes and de Melo Accardo, 2019; Lee and Kader, 2000;
Siti et al., 2015; Song et al., 2020; Sturza et al., 2019; Zeng et al., 2019).
These conditions are related to the development of NCD like CVD
(Boovarahan and Kurian, 2018), Chronic Respiratory Diseases (CRD)
(Sears, 2019), cancer (Zhang et al., 2020), and Diabetes mellitus (DM)
(Festa Gomes and de Melo Accardo, 2019). There is not well established
if OxS is a risk factor for the development or a consequence of the
pathologies. Some reports support the precedence of the oxidative imbalance, but others reinforce the perception as a sequel (GonzalezChávez et al., 2018; Stefanovic et al., 2019; Zamani-Ahari et al., 2017).
Despite this lack of consensus, there are some factors, metabolic and
environmental, that can trigger OxS. In the metabolic group we can
found molecular factors (like ROS, NOS, advanced glycation end-products -AGE-, lipopolysaccharides, or NO), proinflammatory cytokines
(like Interleukin -IL- 1, nuclear factor-k B -NFkB-, tumor necrosis factorα -TNFα-, interferon g, among others) (Baek et al., 2012; Festa Gomes
and de Melo Accardo, 2019; Fullerton et al., 2013). On the other side,
the environmental factors that can trigger OxS involve air pollution
(principally particulate matter), silica dust, nighttime work, smoking,
alcohol consumption, bad nutrition, physical inactivity, and chronic
stress (Barnes et al., 2019; Boovarahan and Kurian, 2018; Gowda et al.,
2019). All of these contributes to establishing, developing, maintaining,
6.2. Significance of antioxidant pigments in plants
Plant-based pigments are synthesized in plants for internal survival
functions as growth, development, protection, and adaptation to external conditions including environmental conditions, pathogen attacks, and physical conditions (UV radiation, high and low temperatures, salinity, drought) (Thakur et al., 2019; Woodson, 2019; Zahedi
et al., 2019), so pigments are necessary to response on biotic and
abiotic stress.
In plants, the peroxisomes are organelles responsible for detoxification of ROS and RNS. In low concentrations, ROS lead to plant
survival, because they have essential functions in biotic and abiotic
response under environmental conditions, growth, respiration, development, seed germination, accumulation, oxidation, mobilization of
lipids and biosynthesis of hormones, and signal molecules (Borek et al.,
2019; Das and Roychoudhury, 2014). Other organelles that produce
ROS are chloroplast, mitochondrial, and cytosol. ROS are produced in
several fundamental pathways, for example, in photosynthesis for
chloroplast, respiration in mitochondria, fatty acid oxidation in peroxisomes, and activity of quinone oxidase in the cytosol (Ansar et al.,
2019).
Carotenoids are produced in plastids and are useful native naturals
antioxidants that regulate the redox state and prevent the oxidative
stress in the chloroplast from plant cells. The response to the redox
status of some enzymes, particularly the plastid terminal oxidase and
plastoquinones are linked in phytoene desaturation; phytoene is a βcarotene, α-carotene, zeinoxanthin, zeaxanthin, and lutein precursor
(Sandmann, 2019; Shen et al., 2018; Sun and Li, 2020).
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Table 6
Some natural pigments and its antioxidant capacity against oxidative stress.
Pigment
Description
Antioxidant activity
References
Anthocyanins
Group of phenolic pigments found in red wine, some cereals,
root vegetables, and red fruits. The red, blue, and purple colors,
fruits, flowers, and leaves are due to anthocyanins. They are
glycosides (water-soluble molecules) of aglycons called
anthocyanidins and active donors of hydrogen. Six common
anthocyanin aglycons (cyanidin, delphinidin, pelargonidin,
malvidin, peonidin, and petunidin)
Astaxanthin found in algae, yeast, and aquatic animals such as
salmon, trout, shrimp, and lobster.
Astaxanthin, which is a red-colored pigment that belongs to the
xanthophyll subclass of carotenoids, have a strong antioxidant
capacity and can scavenge singlet oxygen and free radicals, and
thus prevent lipid peroxidation
Anthocyanins behave as antioxidants in a variety of ways,
including direct trapping of reactive oxygen species (ROS),
inhibition of enzymes accountable for superoxide anion
production, chelation of transition metals involve in processes
creating radicals and anticipation of the peroxidation process by
reducing alkoxy and peroxyl radicals.
Martín et al. (2017)
Astaxanthin significantly reduces physiologically occurring
oxidative stress and maintains the mitochondria in a more
reduced state, even after stimulation with H2O2. Astaxanthin
might prevent mitochondrial dysfunction by permeating and colocalizing within mitochondria. Astaxanthin was shown to inhibit
cytochrome c release resulting from mitochondria
permeabilization, and thereby, prevent mitochondria-mediated
apoptotic death of cells.
Carotenoids, being exceptionally efficient physical and chemical
quenchers of 1O2 and other ROS, have garnered particular
attention as potential protective agents against ROS-mediated
disorders. Up to date, in several epidemiological, interventional
and clinical investigations, several results on experiments with βcarotene, lycopene, lutein, and zeaxanthin, have been collected,
generally supporting the observation that the adequate intake of
Carotenoid-rich fruits and vegetables or carotenoid supplements
may significantly reduce the risk of some chronic diseases.
Kim and Kim (2018)
Several studies have demonstrated that melanin act as
antioxidants and suggest its use as a raw cosmetic material to
minimize light- and toxin-induced tissue destruction. In this
context, as an antioxidative agent in cosmetic formulations
economically. Advantageous. Appeared to confer cellular redox
properties similar to those conferred by melanin. Melanin protects
melanocytes and keratinocytes from the induction of DNA strand
breaks by hydrogen peroxide, indicating that this pigment has an
essential antioxidant role in the skin.
The oxidation of some organic compounds, as naphthoquinones,
allows them to act in different ways, as scavengers of free radicals,
chelators of metal ions such iron and copper, and also inhibitors of
the enzymes accountable for the manufacture of free radicals. This
imbalance between the creation and removal of ROS causes
damage to the cells at nucleic acids, proteins, and membrane
lipids, thus leading to many health problems associated with
ageing (carcinogenesis, cardiovascular and coronary diseases)
De Goncalves and
Pombeiro-Sponchiado
(2005)
Astaxanthin
Carotenoids
Melanin
Naphthoquinone
Riboflavin
Natural pigments of the polyene type. Happen ubiquitously in
all organisms capable of conducting photosynthesis, a process
in which sunlight converts into chemical energy. Carotenoids
are essential constituents of photosynthetic organelles of all
higher plants, mosses, ferns, and algae. They found in
photosynthetic membranes of phototropic bacteria and
cyanobacteria. While not synthesized by humans and animals,
they are also current in blood and tissues. They are important
precursors of retinol (vitamin A); however, their primary
function in all non-photosynthetic organisms seem to be
(photo)protection.
Melanin are black or brown pigments of high molecular weight
shaped by oxidative polymerization of phenolic or indolic
compounds. They found in organisms of all phylogenetic
kingdoms, showing a broad spectrum of biological roles,
including thermoregulation, chemoprotection, camouflage,
and sexual display.
The naphthoquinone is a functional component of biochemical
systems that can act as in the human defense system. Several
naphthoquinones have pharmacological properties like
antibacterial, antifungal, antitumoral, or antiprotozoal agents.
The quinones are known to be electron transporters (e.g.,
ubiquinone, vitamin K), and are essential for many enzymatic
processes. They can act as anti- or pro-oxidants dependent on
the conditions of the media, and this chemical versatility gives
them an essential role in different biochemical processes that
are essential to living organisms
Riboflavin, Vitamin B2, as a natural constituent in living
organisms, supports the organism energy metabolism through
coenzyme forms, flavin adenine dinucleotide and flavin
mononucleotide and has an essential role in biochemical
processes.
Properties of riboflavin, in Dextran 70 and Human Serum
Albumin based system, has been studied by absorption,
fluorescence, circular dichroism and electrochemistry.
Recently, antioxidant and cytotoxic properties of Ribofllavin in
polyethylene glycol/BSA systems reported. It found that 0.12%
PEGs increase the antioxidant activity of riboflavin as a function
of PEG molecular structure, Tween20 > Myrj52.
Also, RF has a pro-oxidant effect in the presence of Bovine Serum
Albumin (BSA), while in the PEG/BSA systems, its antioxidant
activity increases up to ~20%. Fluorescence spectroscopy showed
that RF entrapped in the Tween20/BSA system increases Tyrosine
fluorescence and PEG cross-linking to Riboflavin in the presence
of BSA leads to the thermal stability of BSA.
Fiedor and Burda
(2014)
Oliveira et al. (2017)
Voicescu et al. (2018)
points of link for the oxidative unbalance and the statement or developments of NCD or its complications.
and worsening of OxS, producing undesirables secondary effects like
respiratory tract infections, cataracts, sarcopenia, cell and tissue damage, lung cancer, DNA damage, worsening of RCD, diabetic nephropathy, and many other health issues (Boovarahan and Kurian, 2018;
Kim et al., 2019; Zeng et al., 2019). All these aggressions use different
molecular effects/mechanism in its operation. Of course, an excessive
generation or an incomplete neutralization of ROS and RNS are the
most known triggering factor for OxS. Also, the accumulation of AGEs,
the constant presence of chronic inflammation, changes in the cycles of
melatonin secretion, the activation of the mammalian target of rapamycin, activation of monoamine oxidase, inactivation of adenosine
monophosphate-activated protein kinase, and the infiltration of macrophages into hepatic, renal, or adipose tissue (Barnes et al., 2019;
Fullerton et al., 2013; Gowda et al., 2019; Kaushal et al., 2019; Ren
et al., 2020; Song et al., 2020; Sturza et al., 2019; Zeng et al., 2019) are
6.4. The potential use of food nanopigments for oxidative stress control
Researches of nanotechnology in food science are progressively
developing applications in several fields on the nutrition industry. As
we established before (section 2.1), nanotechnology can be applied to
food industry production, processing, storage, and quality control of
foods (Singh et al., 2017). Nanomaterials, unlike conventional microscale resources, having novel characteristics that can improve sensory
quality of foods by imparting new texture, color or pigments, and appearance. Nanoencapsulation is the most significant knowledge in food
discipline, especially for bioactive compounds and flavors. Directed
delivery systems designed with nanoencapsulation can increase the
10
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J.A. Aguirre-Joya, et al.
encapsulated in modified starch as the wall material using freezedrying. These encapsulated colors have been applying in food and
beverage systems like yogurt, soft drinks, cake, and others, and these
have shown to be stable and effective (Sen et al., 2019).
Recently, polysaccharide-protein nanocarriers have reported as
being promising for polyphenols encapsulation. Active components
bind to the protein part of the nanocarrier via hydrogen bonding and
hydrophobic interactions, while polysaccharides contribute to the prevention of enzymatic protein degradation in gastric conditions.
Polysaccharide–bioactive peptide nanoparticles can also be valuable
nanocarriers for the encapsulation of small molecular polyphenols,
providing better bioavailability of these useful components (Hu et al.,
2012). Between polyphenols, the most commonly encapsulated are
catechins, quercetin, eugenol, epigallocatechin, epigallocatechin-gallate, curcumin, and polyphenols derived from teas or essential oils
(Milinčić et al., 2019).
Natural foods are an essential and growing food category that requires natural ingredients and additives. Subsequently, there is a high
demand to replace synthetic pigments with natural pigments in food
and beverages. Development and integration of advancements like
strain development in fermentations, systems biology, metabolic, and
protein engineering, can make a substantial difference in both the
quality and quantity of natural food colors. Since nowadays our main
focus is to implement nanotechnology and develop novel products in
the food industry, the number of marketing products has been increasing in folders every year. Regulation and legislation are vital.
Safety to a human being (mainly evaluated from toxicity data) is the
first concern for all these new products. Whether or not these novel
products can have a standpoint in the food market also depends on
public attitude and consumers’ acceptance.
bioavailability of bioactive complexes after oral administration. Besides, nanoencapsulation permits to regulator the release of flavors at
the desired time and to protect their degradation during treating and
storage (Yu et al., 2018).
Emergent new colors for the food industry are challenging, as colorants need to be compatible with food flavors, safety, and food value,
and need to have a minimal impact on the price of the product. Besides,
food colorants should preferably be natural rather than synthetic
compounds (Sen et al., 2019). As required by law, food color additives
are subjected to approval by the Office of Cosmetics and Colors in the
Centre for Food Safety and Applied Nutrition, on U.S. Food and Drug
Administration (FDA), and must be used only in agreement with the
approved uses, specifications, and restrictions. With the advent of nanotechnology, a wide range of nanoscale color additives is studied and
manufactured. Several nanomaterial products have been currently approved for use as food color additives, which have an essential role in
the psychological appeal of consumer products (He and Hwang, 2016).
The FDA approved TiO2 as a food color additive with the stipulation
that the additive should not exceed 1% w/w and now are exempt from
certification. Color additive combinations for food use made with TiO2
may also contain SiO2 and Al2O3, as dispersing aids not more than 2%
total. Nevertheless, the use of carbon black as a food color additive is no
longer authorized (FDA, 2016a, 2016b). It does not yet exist any product that has been approved as a food additive or pigment, directly
consumed by human beings, except titanium dioxide and iron oxide
that have been used as food pigment and colorant already (He and
Hwang, 2016).
Color has an essential role in the food manufacture and processing
sector, contributing to the sensory attribute of food. It means freshness,
nutritional value, safety, and aesthetic value of food, directly affecting
the market value of the colored food product. Natural colors assume if
they are non-allergic, non-toxic, non-carcinogenic, and biodegradable,
thereby rendering no risk to the environment (Wrolstad et al., 1990).
Due to the lower risk improvement of natural colors and moving perceptions of consumers to consume natural crops, there is an accumulative interest in the discovery of new natural colors. The user demand
for natural colors and their growth as a category predicted to increase
by 7% annually (Scotter, 2015). Pigments are categorized as organic/
inorganic or natural/synthetic. Biological pigments can classify based
on structural affinities and natural occurrence (Malik et al., 2012),
some of the dominant pigments found in microorganisms employed as
food colorants (like canthaxanthin, astaxanthin, prodigiosin, phycocyanin, violacein, riboflavin, β-carotene, melanin, and lycopene. Pigments like violacein, carotenoids, anthocyanins, astaxanthin, granadaene, canthaxanthin, lycopene, riboflavin, β-carotene, torularhodin,
and naphthoquinone) are potent antioxidants agents (Sen et al., 2019).
Table 6 presents the potential of pigments against oxidative stress.
The latest nanotechnology tenders in food science contain the progress of functional foods and nanosized food compounds, the development of delivery systems for bioactive compounds, and innovations in
food packaging. Micro-encapsulation and nano-encapsulation improve
the functional properties of active transporting of the bioactive compounds to achieve the goal purposes (Milinčić et al., 2019). Microencapsulation and nanoformulations it applies to stabilize, improve
solubility, and deliver natural pigments to food matrices (Singh et al.,
2017).
Natural colors like anthocyanins and carotenoids (Table 2), have
stability topics in various eco-friendly conditions and also present solubility problems in some matrices. Encapsulated colors are easier to
handle, have better solubility, and show improved stability to ambient
conditions, leading to increased shelf life (Sen et al., 2019). The wall
material protects the active core material from light, temperature,
oxygen, humidity, and matrix interactions (Ibrahim Silva et al., 2013).
Several reports on encapsulated microbial pigments, such as anthocyanin, in which maltodextrin has been micro-encapsulated as the wall
material, using spray-drying. β-Carotene has the report to be
7. Conclusions
Nanotechnology represents a promising tool to improve the properties of plant-based pigments by the elaboration of different nanosystems (nanoemulsions, nanocapsules, nanolayers, nanocarriers, etc.).
The desired bioactivity of plant-based pigments, such as tetrapyrroles,
carotenoids, polyphenolic compounds, and alkaloids, is closely related
to preventing priority NCD. The oxidative stress into the cell may derive
in the development of NCD. Bioactive plant-based pigments can constrain oxidative stress acting as antioxidants. These pigments not only
present antioxidant activity but also the antimicrobial effect is ubiquitously reported for those compounds. Nanosystems are hopeful used
with plant-based pigments in the food industry for food processing,
food safety, food quality, food packaging, and nutrition. Each day, more
researches suggest the effectiveness of nanotechnology to prevent NCD
with bioactive plant-based pigments.
CRediT authorship contribution statement
Jorge A. Aguirre-Joya: Visualization, Writing - original draft. Luis
E. Chacón-Garza: Writing - original draft. Guillermo Valdivia-Najár:
Writing - original draft. Roberto Arredondo-Valdés: Writing - original
draft. Cecilia Castro-López: Writing - original draft. Janeth M.
Ventura-Sobrevilla: Visualization, Writing - original draft. Cristóbal
N. Aguilar-Gonzáles: Writing - original draft. Daniel Boone-Villa:
Visualization, Writing - review & editing.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence the work reported in this paper.
11
Food and Chemical Toxicology 143 (2020) 111433
J.A. Aguirre-Joya, et al.
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