Food Research International 100 (2017) 501–509

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Food Research International

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Impact of extraction and processing conditions on betalains and

comparison of properties with anthocyanins — A current review
Giovana Bonat Celli, Marianne Su-Ling Brooks ⁎
Department of Process Engineering and Applied Science, Dalhousie University, PO Box 15000, Halifax, NS B3H 4R2, Canada

a r t i c l e i n f o a b s t r a c t

Article history: The search for natural pigments has been driven by growing evidence indicating that synthetic colorants can
Received 13 May 2016 cause deleterious health effects. Betalains, in addition to anthocyanins, have been proposed as an alternative to
Received in revised form 23 August 2016 address this need. However, the incorporation of natural pigments poses some challenges to the food industry,
Accepted 25 August 2016
such as reduced stability in comparison to their synthetic counterparts. Moreover, betalains are not well studied
Available online 28 August 2016
in comparison to anthocyanins and information about the effects of processing on their physicochemical proper-
Keywords:
ties and stability is scattered. Thus, this review will provide an overview of the recent research on the extraction
Colorant and processing of betalains from natural sources, and comparison of their colorant and physicochemical proper-
Betalain ties with anthocyanins.
Betacyanin © 2016 Elsevier Ltd. All rights reserved.
Betaxanthin
Stability

Products containing natural ingredients are generally perceived by 2013; Slatnar, Stampar, Veberic, & Jakopic, 2015), colored Swiss chard
the consumer to be of better quality, safer, and healthier than those (B. vulgaris L. spp. cicla) (Yu, Han, & Xiao, 2015), leafy and grainy ama-
with synthetic compounds (Martins, Roriz, Morales, Barros, & Ferreira, ranth (Amaranthus sp.) (Li et al., 2015), prickly (or cactus) pear (Opuntia
2016). Concerns have also been raised about the deleterious sp.) (Robert, Torres, García, Vergara, & Sáenz, 2015), and dragon fruit (or
effects associated with artificial food dyes (Amchova, Kotolova, & pitaya) (Hylocereus sp.) (Mello et al., 2015). It is worth noting that an-
Ruda-Kucerova, 2015; El-Wahab & Moram, 2013; Stevens et al., 2013), thocyanins and betalains are mutually exclusive pigments, i.e. they are
which has contributed to increased regulatory pressure and demand not naturally found in the same plant species (Brockington, Walker,
for natural colorants (Shahid, Islam, & Mohammad, 2013). Anthocya- Glover, Soltis, & Soltis, 2011; Harris et al., 2012). Alternatively, betalains
nins are commonly used as natural colorants (Chung, Rojanasasithara, have also been found in some higher fungi (e.g. Amanita muscaria)
Mutilangi, & McClements, 2016; Díaz-García et al., 2015; Žilić, (Girod & Zryd, 1991).
Kocadağlı, Vančetović, & Gökmen, 2016). However, betalains are an in- Betalain derivatives can be classified as betacyanins (red-violet
teresting alternative as they are more hydrophilic and have a higher color, λmax at 540 nm) and betaxanthins (yellow-orange color, λmax at
tinctorial strength (Stintzing & Carle, 2007), which is dependent on 480 nm), depending on the residues attached to the main structure
the solvent system in which they are found (Kumar, Manoj, Shetty, (Strack, Vogt, & Schliemann, 2003). The former exhibits a closed struc-
Prakash, & Giridhar, 2015). In addition, betalains are suitable for appli- ture of cyclo-DOPA (cyclo-3,4-dihydroxy-phenylalanina) and can be
cation in low acid and neutral foods due to their stability at pH 3 to 7 substituted with sugar and acyl groups, whereas the latter is conjugated
(Montes-Lora, Hurtado, Mosquera, Heredia, & Cejudo-Bastante, 2016). with amines and amino acids (Delgado-Vargas, Jiménez, & Paredes-
Betalains are a class of water-soluble nitrogen-containing com- López, 2000). In addition to their tinctorial properties, betalains have
pounds that comprise more than 55 immonium derivatives (Stintzing attracted the interest due to the health-related properties associated
& Carle, 2007) of the chromophore betalamic acid (Piatelli, 1981) with their consumption. Some effects attributed to these compounds
(Fig. 1). They are found in most families of the order Caryophylalles, include antioxidant (Albano et al., 2015; Ravichandran et al., 2013),
appearing in the flowers and fruit, and also to a minor extent in their antiproliferative (Kumar, Manoj, Giridhar, Shrivastava, & Bharadwaj,
vegetative tissues (Kumar, Manoj, Shetty, et al., 2015; Swarna, 2015; Naselli et al., 2014), cardioprotective (Hobbs et al., 2013),
Lokeswari, Smita, & Ravindhran, 2013). Common sources of betalains antiinflamatory (Vidal, López-Nicolás, Gandía-Herrero, & García-
include: red and yellow beetroot (Beta vulgaris L. spp. vulgaris) Carmona, 2014), and antimicrobial effects (Faridah, Holinesti, &
(Sanchez-Gonzalez, Jaime-Fonseca, San Martin-Martinez, & Zepeda, Syukri, 2015; Vulić et al., 2013).
Similarly to anthocyanins, the activity of betalains is dependent on
⁎ Corresponding author. the environmental conditions in which they are found and as well as
E-mail address: [email protected] (M.S.-L. Brooks). their intrinsic chemical properties. For instance, the free radical

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502 G.B. Celli, M.S.-L. Brooks / Food Research International 100 (2017) 501–509

Allegra, Butera, and Livrea (2004) identified a high concentration of

betalains in plasma after the consumption of cactus pear. This could in-
dicate that the food matrix plays a role in the bioaccessibility and bio-
availability of these compounds (Tesoriere et al., 2013), which is
similar to what is exhibited by anthocyanins (Charron et al., 2009),
and that these properties could be modified by processing.
Recent studies have investigated the addition of betalains to differ-
ent food matrices, such as milk (Gengatharan, Dykes, & Choo, 2016),
ice cream (Kumar, Manoj, Shetty, et al., 2015), cookies (Bassetto,
Samulak, Misugi, Barana, & Rosso, 2013), and gummy confections
(Hani, Romli, & Ahmad, 2015). Similarly to anthocyanins, processing
conditions such as temperature (Cejudo-Bastante, Hurtado, Mosquera,
& Heredia, 2014), water activity (Pitalua, Jimenez, Vernon-Carter, &
Beristain, 2010), light (Wong & Siow, 2015), and pH (Sanchez-
Gonzalez et al., 2013) can negatively impact the stability of betalains
and ultimately contribute to color loss (Woo, Ngou, Ngo, Soong, &
Fig. 1. General structure of betalains. The betalamic acid moiety is common to all Tang, 2011). However, betalains are not well studied in comparison to
compounds of this class, whereas R1 and R2 vary from hydrogen to aromatic anthocyanins and information regarding the effects of processing condi-
substituents in betacyanins and betaxanthins. tions on their physicochemical properties are scattered.
Adapted from Delgado-Vargas et al. (2000).
Thus, this review aims to present an overview of the recent research
on the extraction and processing of betalains from natural sources,
scavenging activity of betalains was shown to be highly affected by pH mostly covering the research that has been published in the last five
(increased activity was observed at pH N 5.5) and molecular structure years. Other reports that serve as a basis for the study of betalains and
(Gandía-Herrero, Escribano, & García-Carmona, 2010, 2012). Recently, that have been published since 2000 will also be included in this review.
betalains have been reported to help ameliorate obesity and insulin re- Firstly, the most common sources of betalains that could be used as raw
sistance in mice fed a high-fat diet (Song, Chu, Xu, Xu, & Zheng, 2016). material for the food industry are discussed. This is followed by a review
However, these and other health benefits associated with betalains of different strategies for the extraction of betalains and the effects of
still have to be confirmed in human trials. Even though this evidence processing on their physicochemical properties and stability. Finally,
is still missing in human trials, the use of betalains as natural colorants the colorant and relevant physicochemical properties of betalains are
is still favored over synthetic food dyes which are associated with detri- discussed and compared with anthocyanins, another important class
mental health effects (Swaroop, Roy, & Vijayakumar, 2011). of hydrophilic colorants that are relevant for the food industry.
It should be noted that little research is available on the pharmaco-
kinetics (i.e. absorption, distribution, metabolism, and excretion) of 1. Sources of betalains
betalains in humans. Researchers have indicated that the urinary excre-
tion of betalains accounts for approximately 0.28% of the administered A summary of various sources of betalains can be found in Table 1.
dose, which could indicate low bioavailability after oral administration Several biotic and abiotic factors can affect the accumulation of
or a different route of elimination (Frank et al., 2005). Clifford et al. betalains in plants (Hilou, Millogo-Rasolodimby, & Nacoulma, 2013;
(2016) recently evaluated the bioavailability after ingestion of commer- Sumaya-Martínez et al., 2011) and contribute to the discrepant values
cial beetroot products, and although the products were rich in betalains, reported in the literature, including differences among varieties
the authors did not detect the compounds in plasma up to 8 h after their (Niveyro, Mortensen, Fomsgaard, & Salvo, 2013) and cultivars (Yahia
consumption (Clifford et al., 2016). In contrast to that study, Tesoriere, & Mondragon-Jacobo, 2011), parts of the plant under consideration

Table 1
Summary of different betalain sources.

Source Total betalain content (mg/100 g)⁎ Reference

Yellow beetroot (Beta vulgaris L.) 568a Slatnar et al. (2015)

Red beetroot (B. vulgaris L.) 40–77b Sanchez-Gonzalez et al. (2013)
78.9–130.9b Wruss et al. (2015)
240–1260a Nemzer et al. (2011)
2935–3969a Slatnar et al. (2015)
Swiss chard (B. vulgaris L. spp. cicla) 5.7–6.5b Kugler, Stintzing, and Carle (2007)
Amaranth (Amaranthus sp.) 0.07–20.93a Li et al. (2015)
Prickly pear (O. joconostle F.A.C. Weber ex Diguet) 92.7b Sanchez-Gonzalez et al. (2013)
Yellow prickly pear (O. ficus-indica (L.) Mill.) 3.78b Khatabi, Hanine, Elothmani, and Hasib (2011)
Red prickly pear (Opuntia sp.) 3b de Souza, Santana, de Macedo, de Brito, and Correia (2015)
Red prickly pear (O. ficus-indica (L.) Mill.) 10.24b Khatabi et al. (2011)
Purple prickly pear (O. ficus-indica (L.) Mill.) 30b Robert et al. (2015)
Pitaya peel (Hylocereus sp.) 101a Mello et al. (2015)
Pitaya peel (H. polyrhizus (Weber) Britton) 73b Faridah et al. (2015)
Pigeon berry (Rivina humilis L.) 1700a Khan, Sri Harsha, Giridhar, and Ravishankar (2012)
Facheiro (Philosocereus pachycladus Ritter) 134b de Souza et al. (2015)
Waterleaf flower (Talinum triangulare (Jacq.) Willd.) 499.3b Swarna et al. (2013)
Malabar spinach (Basella rubra L.) 143.8b Kumar, Manoj, Shetty, et al. (2015)
Quinoa (Chenopodium quinoa Willd. var. Pasankalla) 0.1a Díaz-Rojas, Mendoza-Llamo, and Vidaurre-Ruiz (2015)
Quinoa (C. quinoa Willd. var. Collana) 0.13a Díaz-Rojas et al. (2015)
Epiphitic cactus flower and fruits (Epiphyllum sp.) 782.1a Erdelská and Stintzing (2011)
“Jiotilla” (Escontria chiotilla [Weber] Britton & Rose) 20.8b Soriano-Santos et al. (2007)
Garambullo fruit (Myrtillocactus geometrizans [Mart. ex Pfeiff.] Console) 214a Reynoso, Garcia, Morales, and Gonzalez de Mejia (1997)
⁎Total betalain content expressed as mg/100 g of material on a a dry weight (DW) or b fresh weight (FW) basis.
 G.B. Celli, M.S.-L. Brooks / Food Research International 100 (2017) 501–509 503

(Slatnar et al., 2015), ripening stage (Castellar, Solano, & Obón, and low pH value (on average 3.7), which can be beneficial for the sen-
2012; Cayupána, Ochoa, & Nazareno, 2011; Herrera-Hernández, sory properties of the product and against microbiological spoilage
Guevara-Lara, Reynoso-Camacho, & Guzmán-Maldonado, 2011), (Moussa-Ayoub, El-Samahy, Rohn, & Kroh, 2011). Researchers have
salinity (Jain & Gould, 2015; Mulry, Hanson, & Dudle, 2015), oxidative also investigated the propagation of plant tissue (Viñas, Fernández-
stress (Wang, Chen, & Wang, 2007), light (Cao et al., 2012), concentra- Brenes, Azofeifa, & Jiménez, 2012) and production of betalains in vitro
tion of micronutrients (Tyszka-Czochara et al., 2016), insects (Biswas, Das, & Dey, 2013; Lage, Tirado, Vanicore, Sabino, & Albarello,
(Casique-Arroyo, Martínez-Gallardo, de la Vara, & Délano-Frier, 2014), 2015) as alternative methods for enabling the large-scale production
drought (Marchesini, Yin, Colmer, & Veneklaas, 2014), growing temper- of betalains.
ature (Szopińska & Gawęda, 2013), and farming practice (Nizioł-
Łukaszewska & Gawęda, 2014). 2. Effect of extraction and processing conditions on betalain content
In comparison to the widespread anthocyanins (Fernandes, Faria,
Calhau, Freitas, & Mateus, 2014), betalains are limited to a number of The use of betalains as natural colorants can be beneficial due to
families of the order Caryophylalles (Brockington et al., 2015) and cer- their associated health benefits and innocuousness; however, the sub-
tain fungi (Girod & Zryd, 1991), and their tissues are not often edible stitution of synthetic food dyes can be very challenging. An important
(Vendramin & Brvar, 2014). Beetroot red (E 162) and dehydrated beet consideration for the broader application of betalains is their extraction
(or beet powder) are currently the only betalain-based colorants ap- from the plant matrix, which should be aimed at maximum yield in
proved for use in food products in Europe (EU, 2012) and the USA order to supply sufficient material for industrial applications. Another
(FDA, 2009), respectively, which restricts the spectrum of shades that challenge with colorant powdered extracts produced from fruits and
can be explored by the food industry. In addition, beetroot can negative- vegetables is the presence of compounds other than the pigment of in-
ly impact the sensory characteristics of food preparations by conferring terest, which can affect the quality of the food in which they are applied,
an earthy flavor and aroma (Bach, Mikkelsen, Kidmose, & Edelenbos, such as the case of beetroot (Freidig & Goldman, 2014). However, the
2015) due to geosmin (Freidig & Goldman, 2014) and pyrazines main issue related to the application of betalains as natural colorants
(Parliment, Kolor, & Maing, 1977). Another concern that has been raised is their limited stability during processing (Güneşer, 2016) and storage
regarding the use of beetroot juice as a food colorant is the elevated ni- (Kathiravan, Nadanasabapathi, & Kumar, 2014), which will ultimately
trate content (van Velzen, Sips, Schothorst, Lambers, & Meulenbelt, impact the color of the food product. For example, Güneşer (2016) re-
2008); however, this is an ongoing debate as supplementation with ni- cently reported that the thermal degradation of betroot betalains ap-
trates could have a positive effect on the control of blood pressure plied to milk follows a first-order reaction kinetics (at 70–90 °C), i.e.
(Ferguson et al., 2013). For this reason, a considerable body of research increased temperature is associated with higher degradation, in agree-
has been focused on identifying different sources of betalains that could ment with Fernández-López, Angosto, Giménez, and León (2013),
be used as a substitute for beetroot and would not interfere with the Mello et al. (2015), and Sánchez-Chávez, Cortez-Arredondo, Solano-
quality of the matrix in which they are applied. Cornejo, and Vidaurre-Ruiz (2015). This section will discuss different
The genus Amaranthus has been investigated as a potential source of strategies for the extraction of betalains and the effects of processing
betalain-based food colorants. It contains more than 60 species (Chan & on their physicochemical properties and content.
Sun, 1997), some of which are used as vegetables or herbal medicines
(Mahomoodally & Ramalingum, 2015). The major limitation with this 2.1. Extraction
genus is that in addition to the betalains, triterpenoid saponins are a
major bioactive constituent and these are associated with the unpalat- Betalains are commonly obtained from plant sources by convention-
ability of some species (Zehring et al., 2015), though the pattern and al solid–liquid extraction methods, such as maceration (Ramli, Ismail, &
profile of saponins can vary. In a study by Oleszek, Junkuszew, and Rahmat, 2014) and soxhlet extraction (Hilou et al., 2013). In a study by
Stochmal (1999), the concentration of saponins in amaranth seeds Sanchez-Gonzalez et al. (2013) the extraction of betalains from Opuntia
was shown to account for 0.09 to 0.1% of the dry matter. The authors in- jonocostle by maceration was optimized. According to these authors,
dicated that the toxicity due to saponins was minimal to non-existent aqueous extraction was more efficient than higher concentrations of
and no deleterious health effects would be expected with the consump- methanol or ethanol, resulting in a higher concentration of pigments
tion of amaranth (Oleszek et al., 1999). in the extracts. Taking into consideration the extraction solvent, tem-
Cactus (or prickly) pears (Opuntia spp.) and pitaya (e.g. Hylocereus perature, and time, the maximum betalain concentration would be ob-
spp.) are more promising edible sources of betalains (de Souza et al., tained with 20% methanol (v/v) in a water bath at 15 °C for 10 min (with
2015; Faridah et al., 2015). Studies have shown that these fruits have the pH of extract corrected to 5 with 1% citric acid). In another study also
health-promoting properties (Albano et al., 2015). An advantage of using water as the extraction solvent, Maran, Manikandan, and Mekala
using cactus pears is that the yellow and orange fruits can be a useful (2013) optimized the maceration procedure to obtain betalains from
source of yellow hydrophilic colorants, which are not obtained when prickle pears and found that the optimal conditions were different
using red beetroot (Moßhammer, Stintzing, & Carle, 2005a). Even than previously described for xonocostle: temperature of 42 °C for
though the red-purple pitaya has been widely investigated as a source 115 min at pH 6.9, which indicates that the extraction method can differ
of betalains, the yellow fruits (Selenicereus megalanthus [K. Schumann greatly depending on the plant matrix used.
ex Vaupel] Moran) could also be used as a source of natural colorants Recent reports have investigated the use of novel techniques as mild
(Cejudo-Bastante, Hurtado, Delgado, & Heredia, 2016). alternatives to conventional methods to increase the yield of betalains
Other interesting sources of betalains that are not commonly used extracted and include ultrasound (Ramli et al., 2014), microwave
include Epiphyllum plants (Erdelská & Stintzing, 2011), ulluco (Ellucus (Cardoso-Ugarte, Sosa-Morales, Ballard, Liceaga, & San Martín-
tuberosus Loz.) (Cejudo-Bastante et al., 2014), “jiotilla” (Escontria González, 2014), and pulsed electric field (PEF) extraction (Loginova,
chiotilla [Weber] Britton & Rose) (Soriano-Santos et al., 2007), Lebovka, & Vorobiev, 2011).
garambullo fruits (Myrtillocactus geometrizans [Mart. ex Pfeiff.] Console) The ultrasound-assisted extraction of betalains was investigated and
(Herrera-Hernández et al., 2011; Reynoso et al., 1997), “koubo” (Cereus optimized for Malabar spinach (Maran & Priya, 2015) and red beet
peruvianus [L.] Miller) (Mizrahi, 2014), and Celosia argentea L. (Cai, Sun, stalks (Maran & Priya, 2016). Optimal conditions were roughly similar:
Schliemann, & Corke, 2001). The red-purple cactus Opuntia macrorhiza for Malabar spinach, temperature of 54 °C, 94 W, 1:17 (w/v) solid to sol-
fruits are also a valuable source of betalains and offers several advan- vent ratio, for 32 min (Maran & Priya, 2015), whereas for beet stalks the
tages in comparison to the well-known O. ficus-indica fruits, such as conditions were 53 °C, 89 W, 1:19 (w/v) solid to solvent ratio, for 35 min
high concentration of vitamin C, total soluble solids around 10.5 °Brix, (Maran & Priya, 2016). However, Ramli et al. (2014) recently compared
504 G.B. Celli, M.S.-L. Brooks / Food Research International 100 (2017) 501–509

the extraction of betacyanin from pitaya by maceration and ultrasound- exhibiting significantly lower degradation rate constant (3.3–
assisted extraction. Maceration used water as the solvent, 1/25 and 1/55 4.3 × 103 day− 1) than betacyanins (7.2–8.2 × 103 day− 1) (Vergara
(w/v) solid to liquid ratio for flesh and peel, respectively, and a shaker at et al., 2014).
200 rpm for 120 min at 50 °C. The ultrasound-assisted extraction used Similarly to anthocyanins, the stability of betalains is highly affected
the same solid to solvent ratio and water as the extraction medium, by temperature and light during processing, whereas they are generally
and the mixture was sonicated at 50 kHz for 30 min at 25 °C. Both pro- stable at refrigerated storage (Woo et al., 2011). Ravichandran et al.
cedures were repeated with the residue obtained after filtration. In the (2013) evaluated the stability of betalain-rich extract from beetroot
case of the peel, the extraction yield was higher for maceration subjected to different thermal and non-thermal processes. They report-
(95.25%) than ultrasound-assisted extraction (47.07%); however for ed a reduction of betalain content in boiled (up to 51 and 33% of
the flesh, the yield was higher for ultrasound (90.08%) than maceration betacyanin and betaxanthin, respectively) and roasted samples (up to
(73.27%). For both parts of the fruit, maceration resulted in significantly 35% of betacyanin), whereas an increase of betaxanthin content was ob-
higher amounts of betacyanin in the final extract (Ramli et al., 2014). served after microwaving (up to 20%). Applying a vacuum resulted in an
On the other hand, Cardoso-Ugarte et al. (2014) compared macera- increase of betacyanins and betaxanthins by 20 and 12%, respectively, in
tion with microwave-assisted extraction of betalains from beetroot and comparison to a control, possibly due to low oxygen content in the sam-
found that the latter resulted in higher yields (N50% of maximum ex- ples and higher extractability (Ravichandran et al., 2013).
tractable pigment) than the former (10–20%). Extraction for longer Temperature during storage can also affect the stability of betalains.
time periods than 100–120 and 140–150 min resulted in a reduction Caldas-Cueva et al. (2015) compared the stability of betacyanin-rich ex-
of the yield of betanins and betaxanthins, respectively (Cardoso- tracts from ayrampo (Opuntia soehrensii Britton & Rose) and beetroot at
Ugarte et al., 2014), due to the high temperatures observed with micro- refrigerated conditions (4 °C), room temperature (25 °C) (both at
wave extraction (Gonçalves, Di Genova, Dörr, Pinto, & Bastos, 2013). The pH 4.5), and high temperature (80 °C up to 90 min, pH 3, 4, 5). The sta-
authors also evaluated the use of ascorbic acid (0.04 mol/L extraction bility of betacyanins was similar in both extracts subject to high temper-
solvent) on the extraction yield and showed that it can protect and re- atures at pH 4 and 5. Higher pHs were also associated with higher half-
generate betanins during thermal treatment, although a detrimental ef- life (e.g. 74.3 and 150.4 min for pH 3 and 5, respectively). The degrada-
fect was observed for betaxanthins (Cardoso-Ugarte et al., 2014). In tion of betacyanins followed a first-order kinetics reaction; however, at
another report, a higher extraction yield (83% of maximum extractable refrigerated and room temperature, the half-life of compounds from
pigment) was obtained from cactus pear using high pressure CO2- ayrampo were significantly higher (272 and 26 days, respectively)
assisted extraction, which is twice the yield obtained by maceration than from beetroot (95 and 13 days, respectively) (Caldas-Cueva et al.,
with water at room temperature (Nunes, Carmo, & Duarte, 2015) and 2015). In another study, García-Cruz, Valle-Guadarrama, Salinas-
significantly higher than the that obtained with the use microwave Moreno, and Luna-Morales (2016) showed that the total betalain
extraction. content in whole pitaya fruits remained unchanged during storage at
24 °C for 6 days.
2.2. Processing The degradation of betalains can occur by isomerization (Herbach,
Stintzing, & Carle, 2006a; Ravichandran et al., 2013), deglycosylation
A summary of various studies exploring the effect of processing con- (Dumbravă, Enache, Oprea, Georgescu, & Gîrţu, 2012), decarboxylation,
ditions on betalain content is given in Table 2, where products with both dehydrogenation (Herbach, Stintzing, & Carle, 2004a; Nemzer et al.,
naturally-present and added betalains are included. It is evident that for 2011), and hydrolysis (Herbach, Stintzing, & Carle, 2005; Vergara et
the diverse range of products and processing conditions considered, al., 2014), which will result in a gradual reduction of the red color and
betalain stability is affected by a wide range of factors. Indeed, the stabil- appearance of a brown shade (Chandran, Nisha, Singhal, & Pandit,
ity of betalains during processing is highly affected by a range of intrin- 2014; Khan & Giridhar, 2014). Different strategies have been proposed
sic (e.g. molecular structure) and extrinsic (e.g. temperature) factors, as to prevent or reduce the degradation of betalains, such as the use of
presented in Table 3. The reader is also referred to the article by ascorbic acid (Cardoso-Ugarte et al., 2014; Herbach et al., 2007; Khan
Herbach, Stintzing, & Carle (2006b), where the stability and degradation & Giridhar, 2014; Narkprasom et al., 2012; Wong & Siow, 2015), citric
of betacyanins is reviewed, for further discussion. acid (Durge et al., 2013), tetraethyl orthosilicate (TEOS) (Molina,
Even though pitaya fruits are an interesting source of betalains, their Hernández-Martínez, Cortez-Valadez, García-Hernández, & Estevez,
processing is often considered to be difficult due to the high levels of 2014), alternative solvent system (e.g. aqueous trifluoroethanol)
mucilagenous material (Stintzing & Carle, 2007), which can significantly (Bartoloni et al., 2013) and encapsulation techniques (Gandía-Herrero,
affect the juice or extract yield (Esquivel, Stintzing, & Carle, 2007). Cabanes, Escribano, García-Carmona, & Jimeńez-Atieńzar, 2013;
Schweiggert, Villalobos-Gutierrez, Esquivel, and Carle (2009) devel- Gandía-Herrero, Jiménez-Atiénzar, Cabanes, García-Carmona &
oped and optimized a liquefaction process for the preparation of juice Escribano, 2010; Janiszewska, 2014; Otálora, Carriazo, Iturriaga,
from purple pitaya using pectinolytic enzymes at low temperatures Nazareno, & Osorio, 2015; Otálora, Carriazo, Iturriaga, Osorio, &
(4–12 °C). This method reduced the viscosity by 50%, retained 80% of Nazareno, 2016; Ravichandran et al., 2014).
the betalains, and increased the juice yield from 25–39% to 48–60%. Thermal treatment can significantly affect the concentration of
Further thermal concentration of the juice resulted in the reduction of betacyanins. Herbach, Stintzing, and Carle (2004b) noted a shift from
betalain content (to 70%). Interestingly, the enzymatic treatment result- red-purple hues of red beet juice after thermal treatment (85 °C for up
ed in the shift of the juice colour to lower hues, contributing to blueish to 8 h) to yellow-orange ones, and the authors proposed a mechanism
tonalities that are not normally observed in pitaya products that involves bond cleavage, decarboxylation, isomerization, and dehy-
(Schweiggert et al., 2009). drogenation. Herbach et al. (2006) noted that the stability of pitaya
In terms of molecular structure, the study by Vergara et al. (2014) is betacyanins under thermal treatment depends on the pH of the
in agreement with Robert et al. (2015), indicating that the molecular samples, i.e. the concentration of these compounds was lower in ther-
structure plays a role in betalain stability. Vergara et al. (2014) evaluat- mally treated samples with a higher pH (pH 6) in comparison to a low
ed the microencapsulation of betalains from cactus pear by spray dry- pH (pH 4). Khan and Giridhar (2014) showed that ascorbic acid
ing, followed by accelerated stability at 60 °C up to 25 weeks. They (0.25 g/mL Rivina humilis L. berry juice) in combination with selenium
noted a higher recovery of betaxanthins (88.5–96.8%) than betacyanins (40 μg/mL) protected betacyanins from metal-induced bleaching and
(70.9–72.4%), possibly due to the better stability of the former at high regenerated the pigment after intermittent or continuous thermal treat-
temperatures. The degradation kinetics of both compounds was ment, corroborating the results by Herbach et al. (2006). The regenera-
shown to follow a pseudo-first order kinetics, with betaxanthins tion after thermal treatment is also dependent on the sample pH. In this
 G.B. Celli, M.S.-L. Brooks / Food Research International 100 (2017) 501–509 505

Table 2
Effects of processing conditions on betalain content.

Source of betalain Product/process Effect on betalain content Reference

Betalains in their natural source

Beetroot (B. vulgaris L.) juice Microfiltration - Reduction of 5.91 and 13.04% of betacyanins and Amirasgari and Mirsaeedghazi
betaxanthins, respectively (2015)
Beetroot (B. vulgaris L.) slices High-hydrostatic pressure - Increase of betalain content in comparison to raw Paciulli, Medina-Meza, Chiavaro,
(HHP) (650 MPa) samples by 6-fold (up to 7 min) and Barbosa-Cánovas (2016)
- Treatment for 15 and 30 min decreased the betanin content
Beetroot (B. vulgaris L.) RTS juice - ~50% degradation of betalains at 96 °C for 720 s than 900 s Kathiravan et al. (2014)
- 65% reduction after 180 days of storage at room temperature
Beetroot (B. vulgaris L.) juice Fermentation (lactic) - All strains tested negatively affected the content of betanins. Chwastek, Klewicka, Klewicki,
Highest reduction (~42%) was observed for Lactobacillus brevis 944 and Sójka (2015)
Betroot (B. vulgaris L.) grated Fermentation (lactic) - More than 90% of betanin was retained up to 48 h Jagannath, Kumar, and Raju
- Content after 32 days under refrigerated storage was 27% (2015)
Beetroot (B. vulgaris L.) pulp Steam blanching - 35% reduction of betacyanin compared to untreated sample Gokhale and Lele (2014)
- Betaxanthin was comparable in treated and untreated samples
Beetroot (B. vulgaris L.) grated Steam cooking (34.4 kPa, 15 min) - Reduced betanin content by 40% Jagannath et al. (2015)
Beetroot (B. vulgaris L.) pulp Hot air drying (50–120 °C) - Samples dried at 50 and 65 °C had similar betacyanin content Gokhale and Lele (2014)
than control (freeze-dried powder)
- Increasing the temperature resulted in reduction of
betacyanin concentration
Betroot (B. vulgaris L.) Refrigerated storage (8–10 °C) - 50% reduction of betanin content in 10 days Jagannath et al. (2015)
- Vulgaxanthin I and II contents were not affected
Cactus pear (O. ficus-indica Fermentation (kombucha) - Increase of betacyanin content during fermentation Ayed and Hamdi (2015)
(L.) Mill.) juice
Cactus pear (O. ficus-indica High-hydrostatic pressure - No significant differences were observed at 400 MPa Jiménez-Aguilar et al. (2015)
(L.) Mill.) (HHP) (400 or 550 MPa) - 550 MPa for 2–4 min increased the concentration of betaxanthins
(6–8%) and betacyanin (4–7%)
Cactus pear (O. ficus-indica UHT (138 °C, 2 s) - Considerable reduction: 7 and 45% for betaxanthin and 18 and 26% Jiménez-Aguilar et al. (2015)
(L.) Mill.) for betacyanin for samples with or without additives, respectively
Cactus pear (O. ficus-indica Microfitration - Retention of 20.6% of the initial concentration in the permeate Vergara et al. (2015)
(L.) Mill.) juice
Cactus pear (O. ficus-indica Clarification and - Frozen fruits were peeled and the pulp was separated from the Moßhammer et al. (2005a)
(L.) Mill.) juice pasteurization seeds, fibers, and mucilageous material. This was followed by
enzymatic treatment and pasteurization (HTST, 92 °C)
- Thermal inactivation of the enzymes resulted in losses of
batacyanins and betaxanthins in comparison to unheated samples,
although it had no effects on the colour of the juice
- Betacyanins were more stable during pasteurization than
betaxanthins (loss of 2.3–6.3% vs. 6.0–12.6%)
- Light, chroma, and hue angle were similar for manually squeezed
juice and pasteurized samples
Pitaya (Hylocereus spp) Freeze drying - Visual color after rehydration was similar to the original color Liaotrakoon, De Clercq, Lewille,
- Up to 360 mg/100 g of betacyanins were obtained in the and Dewettinck (2012)
freeze-dried powder
Pitaya (Hylocereus polyrhizus Thermal treatment - Samples were heated at 85 °C for 1 h, followed by cooling in Herbach et al., 2006
[Weber] Britton & Rose) juice ice bath and cold storage at 10 °C for 24 h
- Addition of 1% ascorbic acid before thermal treatment resulted in
the retention of 91% of betacyanins (pH 4), which is twice as high
as the content of untreated samples
Malabar spinach Fermentation (alcoholic) - Marginal reduction of betalains (5 to 11% depending on the strain) Kumar, Manoj, & Giridhar
(Basella rubra L.) after 3 h compared to control (2015)
- Increase of betacyanin and reduction of betaxanthin contents
between 3 and 6 h of fermentation

Betalains added to an external food matrix

Beetroot (B. vulgaris L.) peel Baking (cookies) - Reduction of 58.05 and 63.84% of betacyanins for the preparation Bassetto et al. (2013)
of beet flour (100 °C, 2 h) and cookies (200 °C, 20 min), respectively
Betroot (B. vulgaris L.) Extrusion (16% moisture - Maximum retention of color Durge, Sarkar, Survase, and
content, 160 °C, 170 rpm) - Addition of citric acid reduced color requirement Singhal (2013)
- Better retention of color when stored in metallised polyethylene
Cactus pear (O. ficus-indica Extrusion cooking (screw - Retention of betalains intimately related to the residence time of Ruiz-Gutiérrez et al. (2015)
(L.) Mill.) speed 225–325 rpm, the mixture in the extruder
80–140 °C)
Pitaya (H. polyrizhus (Weber) Pasterurization (milk, 63 °C, - Betacyanin content was less affected by pasteurization than Gengatharan et al. (2016)
Britton) extract 30 min) control (beetroot)
- Loss during storage (4 °C, 7 days) was significantly lower than control
- Betacyanin possibly delayed the onset of microbial growth
(5 days compared to 3 days for plain milk)
Pigeon berry (R. humilis L.) Spread (banana-based) - 68% betalain content retained after 6 months at 5 °C Khan et al. (2015)
fruits
Pigeon berry (R. humilis L.) RTS beverage (banana-based) - Loss of betalain and color during pasteurization Khan et al. (2015)
fruits (85 °C for 15 min)
Malabar spinach Ice cream - Approximately 87% of color retained after storage for 6 months Kumar, Manoj, Shetty,
(Basela rubra L.) fruits at −20 °C et al. (2015)
- Good sensory qualities

Note: RTS — ready-to-serve.

506 G.B. Celli, M.S.-L. Brooks / Food Research International 100 (2017) 501–509

Table 3 An important difference between betalains and anthocyanins is that

Intrinsic and extrinsic factors that govern betalain stability. studies have shown that the betalains are able to regenerate after ther-
Factor Reference mal treatment, for example, and this is not observed for anthocyanins
Intrinsic
(Cardoso-Ugarte et al., 2014; Khan & Giridhar, 2014). The regeneration
Chemical structure Herbach, Stintzing, & Carle (2006a,b) can be achieved by the concomitant use of ascorbic acid (Khan &
Vergara, Saavedra, Sáenz, García, Giridhar, 2014), which is known to affect the stability of anthocyanins
and Robert (2014) contributing to their degradation (West & Mauer, 2013). In addition,
Pigment content Lee-Fong and Yen-Ming (2016)
betalains are stable at a broader pH range (between pH 3 and 7)
Extrinsic (Montes-Lora et al., 2016) compared to anthocyanins (b pH 4) (Sui,
Temperature Cejudo-Bastante et al. (2014) Dong, & Zhou, 2014), which makes them a good alternative for low-
Herbach, Maier, Stintzing, and
acidic to neutral products. A combination of betalains and anthocyanins
Carle (2007)
Water activity (aw) Pitalua et al. (2010) is also a good strategy to cover a broader range of pH and to obtain dif-
Enzymes (e.g. POD and PPO) Wybraniec and Michałowski (2011) ferent hues that would not be possible when using the compounds in
pH Cejudo-Bastante et al. (2016) isolation. In addition, a combination of betaxanthin and betacyanin mix-
Sanchez-Gonzalez et al. (2013) tures could be used to tailor different colorants to cover from yellow to
Cations Khan and Giridhar (2014)
purple-blue hues, as demonstrated by Moßhammer, Stintzing, and Carle
Chelating agents (e.g. ascorbate) Cardoso-Ugarte et al. (2014)
Herbach, Rohe, Stintzing & Carle (2006) (2005b).
Light Wybraniec, Stalica, Spórna, and
Mizrahi (2010) 4. Conclusion
Wong and Siow (2015)
Oxygen Correa-Betanzo, Jacob, Perez-Perez,
and Paliyath (2011) Evidence suggesting that synthetic colorants have deleterious health
Free radicals (e.g. •OH) Sumaya-Martínez et al. (2011) effects combined with the consumer's awareness and preference to-
Solvent system (e.g. ethanol-HCl García Barrera, Reynoso, and wards natural ingredients has contributed to the increased body of re-
vs. water) González de Mejía (1998)
search on natural pigments. The substitution of synthetic ingredients,
however, is not straight forward, as natural alternatives such as
betalains can have limited stability during processing and storage. Addi-
case, a higher pH can enhance betacyanin regeneration (Herbach et al., tionally, researchers have investigated alternative sources of betalains
2006). The use of ascorbic acid could also protect the pigments from the that could be used to address this need and would not interfere with
deleterious effects of light (Wong & Siow, 2015). The protective effects the quality attributes of products in which they are applied. Similarly
exhibited by ascorbic acid were also observed for betaxanthin-rich to anthocyanins, the stability of betalains is influenced by intrinsic and
juices subjected to thermal treatment (El Gharras, Hasib, Jaouad, El- extrinsic factors, including the source from which they are extracted. Al-
bouadili, & Schoefs, 2008). though limited to a number of genera in the Caryophylalles order,
Encapsulation can also promote the retention of betalains under ad- betalains are advantageous as natural colorants due to their stability in
verse conditions, provided that low relative humidity and temperature a broader range of pH and potential regeneration after thermal treat-
are maintained (Kaimainen, Laaksonen, Järvenpää, Sandell, & ment, which is not observed with anthocyanins. In combination, antho-
Huopalahti, 2015). For instance, Otálora et al. (2016) reported a signifi- cyanins and betalains could offer a variety of hues to be explored by the
cantly higher retention of betalains encapsulated in calcium-alginate food technologist that would not be observed when they are used in
particles in comparison to non-entrapped freeze-dried extract (con- isolation.
trol). Increasing the relative humidity and temperature resulted in a re-
duction of betalain content; however, the encapsulated compounds Acknowledgments
were less affected by variations in these extrinsic factors than the con-
trol sample (Otálora et al., 2016). Another advantage of encapsulation, The authors acknowledge the Natural Sciences and Engineering Re-
besides promoting stability, is the possibility of co-encapsulating puri- search Council (NSERC) of Canada (Grant number: 341213) for financial
fied betalains to produce a palette of colors that can be tailored as need- support.
ed. This was reported by Gandía-Herrero et al. (2013), who prepared
spray-dried powders with varying amounts of miraxanthin V (yellow) References
and betanidin (purple).
Albano, C., Negro, C., Tommasi, N., Gerardi, C., Mita, G., Miceli, A., et al. (2015). Betalains,
phenols and antioxidant capacity in cactus pear [Opuntia ficus-indica (L.) Mill.] fruits
from Apulia (South Italy) genotypes. Antioxidants, 4, 269–280.
3. Betalains as an alternative to anthocyanins as food colorants Amchova, P., Kotolova, H., & Ruda-Kucerova, J. (2015). Health safety issues of synthetic
food colorants. Regulatory Toxicology and Pharmacology, 73, 914–922.
Amirasgari, N., & Mirsaeedghazi, H. (2015). Microfiltration of red beet juice using mixed
Anthocyanins are ubiquitous in the plant kingdom (Davies, 2015) cellulose ester membrane. Journal of Food Processing and Preservation, 39, 614–623.
and commonly used as natural colorants by the food industry Ayed, L., & Hamdi, M. (2015). Manufacture of a beverage from cactus pear juice using “tea
(Tennant & Klingenberg, 2016). Similarly to betalains, the stability of fungus” fermentation. Annals of Microbiology, 65, 2293–2299.
Bach, V., Mikkelsen, L., Kidmose, U., & Edelenbos, M. (2015). Culinary preparation of beet-
anthocyanins is highly affected by processing and storage conditions root (Beta vulgaris L.): The impact on sensory quality and appropriateness. Journal of
(Fischer, Carle, & Kammerer, 2013; Kamiloglu, Pasli, Ozcelik, Camp, & the Science of Food and Agriculture, 95, 1852–1859.
Capanoglu, 2015; Reque et al., 2014). For instance, the content of antho- Bartoloni, F. H., Gonçalves, L. C. P., Rodrigues, A. C. B., Dörr, F. A., Pinto, E., & Bastos, E. L.
(2013). Photophysics and hydrolytic stability of betalains in aqueous trifluoroethanol.
cyanins can be negatively affected by factors such as pH and tempera-
Monatshefte für Chemie, 144, 567–571.
ture (when in solution) or by relative humidity (when in a powder Bassetto, R. Z., Samulak, R., Misugi, C., Barana, A., & Rosso, N. (2013). Produção de biscoitos
form) (West & Mauer, 2013), which will negatively impact the color. com resíduo do processamento de beterraba (Beta vulgaris L.). Revista Verde de
Agroecologia e Desenvolvimento Sustentável, 8, 139–145.
The pH and temperature also have an effect on betalain content
Biswas, M., Das, S. S., & Dey, S. (2013). Establishment of a stable Amaranthus tricolor callus
(Cejudo-Bastante et al., 2014). It is important to note that this is a gen- line for production of food colorant. Food Science and Biotechnology, 22, 1–8.
eralization as other factors can contribute to the stability of the com- Brockington, S. F., Walker, R. H., Glover, B. J., Soltis, P. S., & Soltis, D. E. (2011). Complex
pounds, such as the chemical structure, chemical composition of the pigment evolution in the Caryophyllales. New Phytologist, 190, 854–864.
Brockington, S. F., Yang, Y., Gandia-Herrero, F., Covshoff, S., Hibberd, J. M., Sage, R. F., et al.
plant source, among others, which should ultimately guide the selection (2015). Lineage-specific gene radiations underlie the evolution of novel betalain pig-
of the raw material. mentation in Caryophyllales. New Phytologist, 207, 1170–1180.
 G.B. Celli, M.S.-L. Brooks / Food Research International 100 (2017) 501–509 507

Cai, Y., Sun, M., Schliemann, W., & Corke, H. (2001). Chemical stability and colorant prop- FDA (US Food and Drug Administration) (2009). Code of Federal Regulations. Title 21.
erties of betaxanthin pigments from Celosia argentea. Journal of Agricultural and Food Cite: 21CFR73.40. Sec. 73.40 Vegetable juice, Vol. 1, (Revised as of May, 2015).
Chemistry, 49, 4429–4435. Ferguson, S. K., Hirai, D. M., Copp, S. W., Holdsworth, C. T., Allen, J. D., Jones, A. M., et al.
Caldas-Cueva, J. P., Morales, P., Ludeña, F., Betalleluz-Pallardel, I., Chirinos, R., Noratto, G., & (2013). Impact of dietary nitrate supplementation via beetroot juice on exercising
Campos, D. (2015). Stability of betacyanin pigments and antioxidants in ayrampo muscle vascular control in rats. Journal of Physiology, 591, 547–557.
(Opuntia soehrensii Britton and Rose) seed extracts and as a yogurt natural colorant. Fernandes, I., Faria, A., Calhau, C., Freitas, V., & Mateus, N. (2014). Bioavailability of antho-
Journal of Food Processing and Preservation. http://dx.doi.org/10.1111/jfpp.12633. cyanins and derivatives. Journal of Functional Foods, 7, 54–66.
Cao, S., Liu, T., Jiang, Y., He, S., Harrison, D. K., & Joyce, D. C. (2012). The effects of host de- Fernández-López, J. A., Angosto, J. M., Giménez, P. J., & León, G. (2013). Thermal stability of
fence elicitors on betacyanin accumulation in Amaranthus mangostanus seedlings. selected natural red extracts used as food colorants. Plant Foods for Human Nutrition,
Food Chemistry, 134, 1715–1718. 68, 11–17.
Cardoso-Ugarte, G. A., Sosa-Morales, M. E., Ballard, T., Liceaga, A., & San Martín-González, Fischer, U. A., Carle, R., & Kammerer, D. R. (2013). Thermal stability of anthocyanins and
M. F. (2014). Microwave-assisted extraction of betalains from red beet (Beta colourless phenolics in pomegranate (Punica granatum L.) juices and model solutions.
vulgaris). LWT - Food Science and Technology, 59, 276–282. Food Chemistry, 138, 1800–1809.
Casique-Arroyo, G., Martínez-Gallardo, N., de la Vara, L. G., & Délano-Frier, J. P. (2014). Frank, T., Stintzing, F. C., Carle, R., Bitsch, I., Quaas, D., Straß, G., et al. (2005). Urinary phar-
Betacyanin biosynthetic genes and enzymes are differentially induced by (a)biotic macokinetics of betalains following consumption of red beet juice in healthy humans.
stress in Amaranthus hypochondriacus. PLoS One, 9, e99012. Pharmacological Research, 52, 290–297.
Castellar, M. R., Solano, F., & Obón, J. M. (2012). Betacyanin and other antioxidants pro- Freidig, A. K., & Goldman, I. L. (2014). Geosmin (2β,6α-dimethylbicyclo[4.4.0]decan-1β-
duction during growth of Opuntia stricta (Haw.) fruits. Plant Foods for Human ol) production associated with Beta vulgaris ssp. vulgaris is cultivar specific. Journal
Nutrition, 67, 337–343. of Agricultural and Food Chemistry, 62, 2031–2036.
Cayupána, Y. S. C., Ochoa, M. J., & Nazareno, M. A. (2011). Health-promoting substances Gandía-Herrero, F., Cabanes, J., Escribano, J., García-Carmona, F., & Jimeńez-Atieńzar, M.
and antioxidant properties of Opuntia sp. fruits. Changes in bioactive-compound con- (2013). Encapsulation of the most potent antioxidant betalains in edible matrixes
tents during ripening process. Food Chemistry, 126, 514–519. as powders of different colors. Journal of Agricultural and Food Chemistry, 61,
Cejudo-Bastante, M. J., Hurtado, N., Delgado, A., & Heredia, F. J. (2016). Impact of pH and 4294–4302.
temperature on the colour and betalain content of Colombian yellow pitaya peel Gandía-Herrero, F., Escribano, J., & García-Carmona, F. (2010a). Structural implications on
(Selenicereus megalanthus). Journal of Food Science and Technology, 53, 2405–2413. color, fluorescence, and antiradical activity in betalains. Planta, 232, 449–460.
Cejudo-Bastante, M. J., Hurtado, N., Mosquera, N., & Heredia, F. J. (2014). Potential use of Gandía-Herrero, F., Escribano, J., & García-Carmona, F. (2012). Purification and antiradical
new Colombian sources of betalains. Color stability of ulluco (Ullucus tuberosus) ex- properties of the structural unit of betalains. Journal of Natural Products, 75,
tracts under different pH and thermal conditions. Food Research International, 64, 1030–1036.
465–471. Gandía-Herrero, F., Jiménez-Atiénzar, M., Cabanes, J., García-Carmona, F., & Escribano, J.
Chan, K. F., & Sun, M. (1997). Genetic diversity and relationships detected by isozyme and (2010b). Stabilization of the bioactive pigment of Opuntia fruits through maltodex-
RAPD analysis of crop and wild species of Amaranthus. Theoretical and Applied trin encapsulation. Journal of Agricultural and Food Chemistry, 58, 10646–10652.
Genetics, 95, 865–873. García Barrera, F. A., Reynoso, C. R., & González de Mejía, E. (1998). Estabilidad de las
Chandran, J., Nisha, P., Singhal, R. S., & Pandit, A. B. (2014). Degradation of colour in beet- betalaínas extraídas del garambullo (Myrtillocactus geometrizans). Food Science and
root (Beta vulgaris L.): A kinetics study. Journal of Food Science and Technology, 51, Technology International, 4, 115–120.
2678–2684. García-Cruz, L., Valle-Guadarrama, S., Salinas-Moreno, Y., & Luna-Morales, C. C. (2016).
Charron, C. S., Kurilich, A. C., Clevidence, B. A., Simon, P. W., Harrison, D. J., Britz, S. J., et al. Postharvest quality, soluble phenols, betalains content, and antioxidant activity of
(2009). Bioavailability of anthocyanins from purple carrot juice: Effects of acylation Stenocereus pruinosus and Stenocereus stellatus fruit. Postharvest Biology and
and plant matrix. Journal of Agricultural and Food Chemistry, 58, 1226–1230. Technology, 111, 69–76.
Chung, C., Rojanasasithara, T., Mutilangi, W., & McClements, D. J. (2016). Enhancement of Gengatharan, A., Dykes, G. A., & Choo, W. S. (2016). Stability of betacyanin from red
colour stability of anthocyanins in model beverages by gum arabic addition. Food pitahaya (Hylocereus polyrhizus) and its potential application as a natural colourant
Chemistry, 201, 14–22. in milk. International Journal of Food Science and Technology, 51, 427–434.
Chwastek, A., Klewicka, E., Klewicki, R., & Sójka, M. (2015). Lactic acid fermentation of red Girod, P. -A., & Zryd, J. -P. (1991). Biogenesis of betalains: Purification and partial charac-
beet juice supplemented with waste highbush blueberry–sucrose osmotic syrup as a terization of dopa 4,5-dioxygenase from Amanita muscaria. Phytochemistry, 30,
method of probiotic beverage production. Journal of Food Processing and Preservation. 169–174.
http://dx.doi.org/10.1111/jfpp.12659. Gokhale, S. V., & Lele, S. S. (2014). Betalain content and antioxidant activity of Beta
Clifford, T., Constantinou, C. M., Keane, K. M., West, D. J., Howatson, G., & Stevenson, E. J. vulgaris: Effect of hot air convective drying and storage. Journal of Food Processing
(2016). The plasma bioavailability of nitrate and betanin from Beta vulgaris rubra in and Preservation, 38, 585–590.
humans. European Journal of Nutrition. http://dx.doi.org/10.1007/s00394-016-1173-5. Gonçalves, L. C. P., Di Genova, B. M., Dörr, F. A., Pinto, E., & Bastos, E. L. (2013). Effect of
Correa-Betanzo, J., Jacob, J. K., Perez-Perez, C., & Paliyath, G. (2011). Effect of a sodium ca- dielectric microwave heating on the color and antiradical capacity of betanin.
seinate edible coating on berry cactus fruit (Myrtillocactus geometrizans) phytochem- Journal of Food Engineering, 118, 49–55.
icals. Food Research International, 44, 1897–1904. Güneşer, O. (2016). Pigment and color stability of beetroot betalains in cow milk during
Davies, K. M. (2015). Swapping one red pigment for another. Nature Genetics, 47, 5–6. thermal treatment. Food Chemistry, 196, 220–227.
Delgado-Vargas, F., Jiménez, A. R., & Paredes-López, O. (2000). Natural pigments: Caroten- Hani, N. M., Romli, S. R., & Ahmad, M. (2015). Influences of red pitaya fruit puree and gel-
oids, anthocyanins, and betalains — Characteristics, biosynthesis, processing, and sta- ling agents on the physico-mechanical properties and quality changes of gummy
bility. Critical Reviews in Food Science and Nutrition, 40, 173–289. confections. International Journal of Food Science & Technology, 50, 331–339.
Díaz-García, M. C., Castellar, M. R., Obón, J. M., Obón, C., Alcaraz, F., & Rivera, D. (2015). Harris, N. N., Javellana, J., Davies, K. M., Lewis, D. H., Jameson, P. E., Deroles, S. C.,
Production of an anthocyanin-rich food colourant from Thymus moroderi and its ap- et al. (2012). Betalain production is possible in anthocyanin-producing plant
plication in foods. Journal of the Science of Food and Agriculture, 95, 1283–1293. species given the presence of DOPA-dioxygenase and L-DOPA. BMC Plant
Díaz-Rojas, G. L., Mendoza-Llamo, E. J., & Vidaurre-Ruiz, J. M. (2015). Cinética de la Biology, 12, 34.
degradación de betalainas y fenoles totales durante la coccion de la quinua Herbach, K. M., Maier, C., Stintzing, F. C., & Carle, R. (2007). Effects of processing and stor-
(Chenopodium quinoa). Revista Científica Ingeniería: Ciencia, Tecnología e Innovación, age on juice colour and betacyanin stability of purple pitaya (Hylocereus polyrhizus)
2, 85–95. juice. European Food Research and Technology, 224, 649–658.
Dumbravă, A., Enache, I., Oprea, C. I., Georgescu, A., & Gîrţu, M. A. (2012). Toward a more Herbach, K. M., Rohe, M., Stintzing, F. C., & Carle, R. (2006a). Structural and chromatic sta-
efficient utilisation of betalains as pigments for dye-sensitized solar cells. Digest bility of purple pitaya (Hylocereus polyrhizus [Weber] Britton & Rose) betacyanins as
Journal of Nanomaterials and Biostructures, 7, 339–351. affected by the juice matrix and selected additives. Food Research International, 39,
Durge, A. V., Sarkar, S., Survase, S. A., & Singhal, R. S. (2013). Impact of extrusion on red 667–677.
beetroot colour used as pre-extrusion colouring of rice flour. Food and Bioprocess Herbach, K. M., Stintzing, F. C., & Carle, R. (2004a). Thermal degradation of betacyanins in
Technology, 6, 570–575. juices from purple pitaya [Hylocereus polyrhizus (Weber) Britton & Rose] monitored
El Gharras, H., Hasib, A., Jaouad, A., El-bouadili, A., & Schoefs, B. (2008). Stability of vacu- by high-performance liquid chromatography-tandem mass spectometric analyses.
olar betaxanthin pigments in juices from Moroccan yellow Opuntia ficus indica fruits. European Food Research and Technology, 219, 377–385.
International Journal of Food Science and Technology, 43, 351–356. Herbach, K. M., Stintzing, F. C., & Carle, R. (2004b). Impact of thermal treatment on color
El-Wahab, H. M., & Moram, G. S. (2013). Toxic effects of some synthetic food colorants and pigment pattern of red beet (Beta vulgaris L.) preparations. Journal of Food
and/or flavor additives on male rats. Toxicology and Industrial Health, 29, 224–232. Science, 69, C491–C498.
Erdelská, O., & Stintzing, F. (2011). Phytochemical and morphological evaluation of Herbach, K. M., Stintzing, F. C., & Carle, R. (2005). Identification of heat-induced degrada-
flowers and fruits from Epiphyllum hybrids during development. Biologia, 66, tion products from purified betanin, phyllocactin and hylocerenin by high-perfor-
821–827. mance liquid chromatography/electrospray ionization mass spectrometry. Rapid
Esquivel, P., Stintzing, F. C., & Carle, R. (2007). Comparison of morphological and chemical Communications in Mass Spectrometry, 19, 2603–2616.
fruit traits from different pitaya genotypes (Hylocereus sp.) grown in Costa Rica. Herbach, K. M., Stintzing, F. C., & Carle, R. (2006b). Stability and color changes of thermally
Journal of Applied Botany and Food Quality, 81, 7–14. treated betanin, phyllocactin, and hylocerenin solutions. Journal of Agricultural and
European Union (EU) (2012). Commission Regulation No. 231/2012 of 9 March 2012 lay- Food Chemistry, 54, 390–398.
ing down specifications for food additives listed in Annexes II and III to Regulation Herbach, K. M., Stintzing, F. C., & Carle, R. (2006c). Betalain stability and degradation —
(EC) No. 1333/2008 of the European Parliament and of the Council. OJ L 83, 22.3. Structural and chromatic aspects. Journal of Food Science, 71, R41–R50.
2012 (pp. 1–295). Herrera-Hernández, M. G., Guevara-Lara, F., Reynoso-Camacho, R., & Guzmán-
Faridah, A., Holinesti, R., & Syukri, D. (2015). Betalains from red pitaya peel (Hylocereus Maldonado, S. H. (2011). Effects of maturity stage and storage on cactus berry
polyrhizus): Extraction, spectrophotometric and HPLC-DAD identification, bioactivity (Myrtillocactus geometrizans) phenolics, vitamin C, betalains and their antioxidant
and toxicity screening. Pakistan Journal of Nutrition, 14, 976–982. properties. Food Chemistry, 129, 1744–1750.
508 G.B. Celli, M.S.-L. Brooks / Food Research International 100 (2017) 501–509

Hilou, A., Millogo-Rasolodimby, J., & Nacoulma, O. G. (2013). Betacyanins are the most rel- Marchesini, V. A., Yin, C., Colmer, T. D., & Veneklaas, E. J. (2014). Drought tolerances of
evant antioxidant molecules of Amaranthus spinosus and Boerhavia erecta. Journal of three stem-succulent halophyte species of an inland semiarid salt lake system.
Medicinal Plants Research, 7, 645–652. Functional Plant Biology, 41, 1230–1238.
Hobbs, D. A., Goulding, M. G., Nguyen, A., Malaver, T., Walker, C. F., George, T. W., et al. Martins, N., Roriz, C. L., Morales, P., Barros, L., & Ferreira, I. C. F. R. (2016). Food colorants:
(2013). Acute ingestion of beetroot bread increases endothelium-independent vaso- Challenges, opportunities and current desires of agroindustries to ensure consumer
dilation and lowers diastolic blood pressure in healthy men: A randomized controlled expectations and regulatory practices. Trends in Food Science & Technology, 52, 1–15.
trial. Journal of Nutrition, 143, 1399–1405. Mello, F. R., Bernardo, C., Dias, C. O., Gonzaga, L., Amante, E. R., Fett, R., & Candido, L. M. B.
Jagannath, A., Kumar, M., & Raju, P. S. (2015). Fermentative stabilization of betanin con- (2015). Antioxidant properties, quantification and stability of betalains from pitaya
tent in beetroot and its loss during processing and refrigerated storage. Journal of (Hylocereus undatus) peel. Ciência Rural, 45, 323–328.
Food Processing and Preservation, 39, 606–613. Mizrahi, Y. (2014). Cereus peruvianus (Koubo) new cactus fruit for the world. Revista
Jain, G., & Gould, K. S. (2015). Functional significance of betalain biosynthesis in leaves of Brasileira de Fruticultura, 36, 68–78.
Disphyma australe under salinity stress. Environmental and Experimental Botany, 109, Molina, G. A., Hernández-Martínez, A. R., Cortez-Valadez, M., García-Hernández, F., &
131–140. Estevez, M. (2014). Effects of tetraethyl orthosilicate (TEOS) on the light and temper-
Janiszewska, E. (2014). Microencapsulated beetroot juice as a potential source of betalain. ature stability of a pigment from Beta vulgaris and its potential food industry applica-
Powder Technology, 264, 190–196. tions. Molecules, 19, 17985–18002.
Jiménez-Aguilar, D. M., Escobedo-Avellaneda, Z., Martín-Belloso, O., Gutiérrez-Uribe, J., Montes-Lora, S., Hurtado, N., Mosquera, N., Heredia, F. J., & Cejudo-Bastante, M. J. (2016).
Valdez-Fragoso, A., García-García, R., et al. (2015). Effect of high hydrostatic pressure Effect of technological practices on individual betalains and antioxidant activity of Co-
on the content of phytochemical compounds and antioxidant activity of prickly pears lumbian betalain-rich raw materials. International Journal of Food Science and
(Opuntia ficus-indica) beverages. Food Engineering Reviews, 7, 198–208. Technology, 51, 1041–1047.
Kaimainen, M., Laaksonen, O., Järvenpää, E., Sandell, M., & Huopalahti, R. (2015). Consum- Moßhammer, M. R., Stintzing, F. C., & Carle, R. (2005a). Colour studies on fruit juice blends
er acceptance and stability of spray dried betanin in model juices. Food Chemistry, from Opuntia and Hylocereus cacti and betalain-containing model solutions derived
187, 398–406. therefrom. Food Research International, 38, 975–981.
Kamiloglu, S., Pasli, A. A., Ozcelik, B., Camp, J. V., & Capanoglu, E. (2015). Colour retention, Moßhammer, M. R., Stintzing, F. C., & Carle, R. (2005b). Development of a process for the
anthocyanin stability and antioxidant capacity in black carrot (Daucus carota) jams production of a betalain-based colouring foodstuff from cactus pear. Innovative Food
and marmalades: Effect of processing, storage conditions and in vitro gastrointestinal Science & Emerging Technologies, 6, 221–231.
digestion. Journal of Functional Foods, 13, 1–10. Moussa-Ayoub, T. E., El-Samahy, S. K., Rohn, S., & Kroh, L. W. (2011). Flavonols,
Kathiravan, T., Nadanasabapathi, S., & Kumar, R. (2014). Standardization of process condi- betacyanins content and antioxidant activity of cactus Opuntia macrorhiza fruits.
tion in batch thermal pasteurization and its effect on antioxidant, pigment and micro- Food Research International, 44, 2169–2174.
bial inactivation of Ready to Drink (RTD) beetroot (Beta vulgaris L.) juice. International Mulry, K. R., Hanson, B. A., & Dudle, D. A. (2015). Alternative strategies in response to sa-
Food Research Journal, 21, 1305–1312. line stress in two varieties of Portulaca oleracea (Purslane). PLoS One, 10, e0138723.
Khan, M. I., & Giridhar, P. (2014). Enhanced chemical stability, chromatic properties and Narkprasom, K., Su, W. -L., Cheng, M. -Y., Wang, S. -P., Hsiao, S. -M., & Tsai, P. -J. (2012).
regeneration of betalains in Rivina humilis L. berry juice. LWT - Food Science and Relative effects of alcohol and ph on betacyanin stability in aqueous Djulis extracts
Technology, 58, 649–657. and their color qualities after organic acid addition. Journal of Food Quality, 35,
Khan, M. I., Sri Harsha, P. S. C., Chauhan, A. S., Vijayendra, S. V. N., Asha, M. R., & Giridhar, P. 283–291.
(2015). Betalains rich Rivina humilis L. berry extract as natural colorant in product Naselli, F., Tesoriere, L., Caradonna, F., Bellavia, D., Attanzio, A., Gentile, C., & Livrea, M. A.
(fruit spread and RTS beverage) development. Journal of Food Science and (2014). Anti-proliferative and pro-apoptotic activity of whole extract and isolated
Technology, 52, 1808–1813. indicaxanthin from Opuntia ficus-indica associated with re-activation of the onco-
Khan, M. I., Sri Harsha, P. S. C., Giridhar, P., & Ravishankar, G. A. (2012). Pigment identifi- suppressor p16INK4a gene in human colorectal carcinoma (Caco-2) cells.
cation, nutritional composition, bioactivity, and in vitro cancer cell cytotoxicity of Biochemical and Biophysical Research Communications, 450, 652–658.
Rivina humilis L. berries, potential source of betalains. LWT - Food Science and Nemzer, B., Pietrzkowski, Z., Spórna, A., Stalica, P., Thresher, W., Michałowski, T., &
Technology, 47, 315–323. Wybraniec, S. (2011). Betalainic and nutritional profiles of pigment-enriched red
Khatabi, O., Hanine, H., Elothmani, D., & Hasib, A. (2011). Extraction and determination of beet root (Beta vulgaris L.) dried extracts. Food Chemistry, 127, 42–53.
polyphenols and betalain pigments in the Moroccan prickly pear fruits (Opuntia ficus Niveyro, S. L., Mortensen, A. G., Fomsgaard, I. S., & Salvo, A. (2013). Differences among five
indica). Arabian Journal of Chemistry. http://dx.doi.org/10.1016/j.arabjc.2011.04.001. amaranth varieties (Amaranthus spp.) regarding secondary metabolites and foliar
Kugler, F., Stintzing, F. C., & Carle, R. (2007). Evaluation of the antioxidant capacity of herbivory by chewing insects in the field. Arthropod-Plant Interactions, 7, 235–245.
betalainic fruits and vegetables. Journal of Applied Botany and Food Quality, 81, 69–76. Nizioł-Łukaszewska, Z., & Gawęda, M. (2014). Changes in quality of selected red beet
Kumar, S. S., Manoj, P., & Giridhar, P. (2015a). A method for red-violet pigments extrac- (Beta vulgaris L.) cultivars during the growing season. Folia Horticulturae, 26,
tion from fruits of Malabar spinach (Basella rubra) with enhanced antioxidant poten- 139–146.
tial under fermentation. Journal of Food Science and Technology, 52(5), 3037–3043. Nunes, A. N., Carmo, C. S., & Duarte, C. M. M. (2015). Production of a natural red pigment
Kumar, S. S., Manoj, P., Giridhar, P., Shrivastava, R., & Bharadwaj, M. (2015c). Fruit extracts derived from Opuntia spp. using a novel high pressure CO2 assisted-process. RSC
of Basella rubra that are rich in bioactives and betalains exhibit antioxidant activity Advances, 5, 83106–83114.
and cytotoxicity against human cervical carcinoma cells. Journal of Functional Foods, Oleszek, W., Junkuszew, M., & Stochmal, A. (1999). Determination and toxicity of sapo-
15, 509–515. nins from Amaranthus cruentus seeds. Journal of Agricultural and Food Chemistry, 47,
Kumar, S. S., Manoj, P., Shetty, N. P., Prakash, M., & Giridhar, P. (2015b). Characterization 3685–3687.
of major betalain pigments -gomphrenin, betanin and isobetanin from Basella rubra L. Otálora, M. C., Carriazo, J. G., Iturriaga, L., Nazareno, M. A., & Osorio, C. (2015). Microencap-
fruit and evaluation of efficacy as a natural colourant in product (ice cream) develop- sulation of betalains obtained from cactus fruit (Opuntia ficus-indica) by spray drying
ment. Journal of Food Science and Technology, 52, 4994–5002. using cactus cladode mucilage and maltodextrin as encapsulating agents. Food
Lage, D. A., Tirado, M. S., Vanicore, S. R., Sabino, K. C. C., & Albarello, N. (2015). Production of Chemistry, 187, 174–181.
betalains from callus and cell suspension cultures of Pereskia aculeata Miller, an uncon- Otálora, M. C., Carriazo, J. G., Iturriaga, L., Osorio, C., & Nazareno, M. A. (2016). Encapsulat-
ventional leafy vegetable. Plant Cell, Tissue and Organ Culture (PCTOC), 122, 341–350. ing betalains from Opuntia ficus-indica fruits by ionic gelation: Pigment chemical sta-
Lee-Fong, S., & Yen-Ming, W. (2016). Effect of juice concentration on storage stability, bility during storage of beads. Food Chemistry, 202, 373–382.
betacyanin degradation kinetics and sensory acceptance of red-fleshed dragon fruit Paciulli, M., Medina-Meza, I. G., Chiavaro, E., & Barbosa-Cánovas, G. V. (2016). Impact of
(Hylocereus polyrhizus) juice. International Journal of Food Properties. http://dx.doi. thermal and high pressure processing on quality parameters of beetroot (Beta
org/10.1080/10942912.2016.1172086. vulgaris L.). LWT - Food Science and Technology, 68, 98–104.
Li, H., Deng, Z., Liu, R., Zhu, H., Draves, J., Marcone, M., et al. (2015). Characterization of Parliment, T. H., Kolor, M. G., & Maing, I. Y. (1977). Identification of the major volatile
phenolics, betacyanins and antioxidant activities of the seed, leaf, sprout, flower components of cooked beets. Journal of Food Science, 42, 1592–1593.
and stalk extracts of three Amaranthus species. Journal of Food Composition and Piatelli, M. (1981). The betalains: Structure, biosynthesis and chemical taxonomy. In E.
Analysis, 37, 75–81. Conn (Ed.), The Biochemistry of Plants: A Comprehensive Treatise (pp. 557–575). New
Liaotrakoon, W., De Clercq, N., Lewille, B., & Dewettinck, K. (2012). Physicochemical prop- York: Academic Press.
erties, glass transition state diagram and colour stability of pulp and peel of two drag- Pitalua, E., Jimenez, M., Vernon-Carter, E. J., & Beristain, C. I. (2010). Antioxidative activity
on fruit varieties (Hylocereus spp.) as affected by freeze-drying. International Food of microcapsules with beetroot juice using gum Arabic as wall material. Food and
Research Journal, 19, 743–750. Bioproducts Processing, 88, 253–258.
Loginova, K. V., Lebovka, N. I., & Vorobiev, E. (2011). Pulsed electric field assisted aqueous Ramli, N. S., Ismail, P., & Rahmat, A. (2014). Influence of conventional and ultrasonic-
extraction of colorants from red beet. Journal of Food Engineering, 106, 127–133. assisted extraction on phenolic contents, betacyanin contents, and antioxidant capac-
Mahomoodally, M. F., & Ramalingum, N. (2015). An investigation into the consumption ity of red dragon fruit (Hylocereus polyrhizus). The Scientific World Journal, 2014,
patterns, attitude, and perception of Mauritians towards common medicinal food 964731.
plants. Journal of Herbal Medicine, 5, 99–112. Ravichandran, K., Palaniraj, R., Saw, N. M. M. T., Gabr, A. M. M., Ahmed, A. R., Knorr,
Maran, J. P., & Priya, B. (2015). Natural pigments extraction from Basella rubra L. fruits by D., & Smetanska, I. (2014). Effects of different encapsulation agents and drying
ultrasound-assisted extraction combined with Box–Behnken response surface de- process on stability of betalains extract. Journal of Food Science and Technology,
sign. Separation Science and Technology, 50, 1532–1540. 51, 2216–2221.
Maran, J. P., & Priya, B. (2016). Multivariate statistical analysis and optimization of ultra- Ravichandran, K., Saw, N. M. M. T., Mohdaly, A. A. A., Gabr, A. M. M., Kastell, A., Riedel, H.,
sound-assisted extraction of natural pigments from waste red beet stalks. Journal of et al. (2013). Impact of processing of red beet on betalain content and antioxidant ac-
Food Science and Technology, 53, 792–799. tivity. Food Research International, 50, 670–675.
Maran, J. P., Manikandan, S., & Mekala, V. (2013). Modeling and optimization of betalain Reque, P. M., Steffens, R. S., Jablonski, A., Flôres, S. H., Rios, A. O., & Jong, E. V. (2014). Cold
extraction from Opuntia ficus-indica using Box–Behnken design with desirability storage of blueberry (Vaccinium spp.) fruits and juice: Anthocyanin stability and an-
function. Industrial Crops and Products, 49, 304–311. tioxidant activity. Journal of Food Composition and Analysis, 33, 111–116.
 G.B. Celli, M.S.-L. Brooks / Food Research International 100 (2017) 501–509 509

Reynoso, R., Garcia, F. A., Morales, D., & Gonzalez de Mejia, E. (1997). Stability of betalain pig- Tesoriere, L., Gentile, C., Angileri, F., Attanzio, A., Tutone, M., Allegra, M., et al. (2013).
ments from a cactacea fruit. Journal of Agricultural and Food Chemistry, 45, 2884–2889. Trans-epithelial transport of the betalain pigments indicaxanthin and betanin across
Robert, P., Torres, V., García, P., Vergara, C., & Sáenz, C. (2015). The encapsulation of purple Caco-2 cell monolayers and influence of food matrix. European Journal of Nutrition, 52,
cactus pear (Opuntia ficus-indica) pulp by using polysaccharide-proteins as encapsu- 1077–1087.
lating agents. LWT - Food Science and Technology, 60, 1039–1045. Tyszka-Czochara, M., Pasko, P., Zagrodzki, P., Gajdzik, E., Wietecha-Posluszny, R., &
Ruiz-Gutiérrez, M. G., Amaya-Guerra, C. A., Quintero-Ramos, A., Pérez-Carrillo, E., Ruiz- Gorinstein, S. (2016). Selenium Supplementation of amaranth sprouts influences
Anchondo, T. J., Báez-González, J. G., & Meléndez-Pizarro, C. O. (2015). Effect of extru- betacyanin content and improves anti-inflammatory properties via NFκB in murine
sion cooking on bioactive compounds in encapsulated red cactus pear powder. RAW 264.7 macrophages. Biological Trace Element Research, 169, 320–330.
Molecules, 20, 8875–8892. van Velzen, A. G., Sips, A. J. A. M., Schothorst, R. C., Lambers, A. C., & Meulenbelt, J. (2008).
Sánchez-Chávez, W., Cortez-Arredondo, J., Solano-Cornejo, M., & Vidaurre-Ruiz, J. (2015). The oral bioavailability of nitrate from nitrate-rich vegetables in humans. Toxicology
Kinetics of thermal degradation of betacyanins, betaxantins and vitamin C in a juice- Letters, 181, 177–181.
based drink beet (Beta vulgaris L.) and honey. Scientia Agropecuaria, 6, 111–118. Vendramin, A., & Brvar, M. (2014). Amanita muscaria and Amanita pantherina poisoning:
Sanchez-Gonzalez, N., Jaime-Fonseca, M. R., San Martin-Martinez, E., & Zepeda, L. G. Two syndromes. Toxicon, 90, 269–272.
(2013). Extraction, stability, and separation of betalains from Opuntia joconostle cv. Vergara, C., Cancino-Madariaga, B., Ramírez-Salvo, A., Sáenz, C., Robert, P., & Lutz, M.
using response surface methodology. Journal of Agricultural and Food Chemistry, 61, (2015). Clarification of purple cactus pear juice using microfiltration membranes to
11995–12004. obtain a solution of betalain pigments. Brazilian Journal of Food Technology, 18,
Schweiggert, R. M., Villalobos-Gutierrez, M. G., Esquivel, P., & Carle, R. (2009). Develop- 220–230.
ment and optimization of low temperature enzyme-assisted liquefaction for the pro- Vergara, C., Saavedra, J., Sáenz, C., García, P., & Robert, P. (2014). Microencapsulation of
duction of colouring foodstuff from purple pitaya (Hylocereus sp. [Weber] Britton & pulp and ultrafiltered cactus pear (Opuntia ficus-indica) extracts and betanin stability
Rose). European Food Research and Technology, 230, 269–280. during storage. Food Chemistry, 157, 246–251.
Shahid, M., Islam, S., & Mohammad, F. (2013). Recent advancements in natural dye appli- Vidal, P. J., López-Nicolás, J. M., Gandía-Herrero, F., & García-Carmona, F. (2014). Inactiva-
cations: A review. Journal of Cleaner Production, 53, 310–331. tion of lipoxygenase and cyclooxygenase by natural betalains and semi-synthetic an-
Slatnar, A., Stampar, F., Veberic, R., & Jakopic, J. (2015). HPLC-MSn identification of betalain alogues. Food Chemistry, 154, 246–254.
profile of different beetroot (Beta vulgaris L. ssp. vulgaris) parts and cultivars. Journal Viñas, M., Fernández-Brenes, M., Azofeifa, A., & Jiménez, V. M. (2012). In vitro propagation
of Food Science, 80, C1952–C1958. of purple pitahaya (Hylocereus costaricensis [F.A.C. Weber] Britton & Rose) cv. Cebra.
Song, H., Chu, Q., Xu, D., Xu, Y., & Zheng, X. (2016). Purified betacyanins from Hylocereus Micropropagation, 48, 469–477.
undatus peel ameliorate obesity and insulin resistance in high-fat-diet-fed mice. Vulić, J. J., Ćebović, T. N., Čanadanović, V. M., Ćetković, G. S., Djilas, S. M., Čanadanović-
Journal of Agricultural and Food Chemistry, 64, 236–244. Brunet, J. M., et al. (2013). Antiradical, antimicrobial and cytotoxic activities of com-
Soriano-Santos, J., Franco-Zavaleta, M. E., Pelayo-Zaldívar, C., Armella-Villalpando, M. A., mercial beetroot pomace. Food & Function, 4, 713–721.
Yáñez-López, M. L., & Guerrero-Legarreta, I. (2007). Caracterizacion parcial del Wang, C. -Q., Chen, M., & Wang, B. -S. (2007). Betacyanin accumulation in the leaves of C3
pigmento rojo del fruto de la “jiotilla” (Escontria chiotilla [Weber] Britton & Rose). halophyte Suaeda salsa L. is induced by watering roots with H2O2. Plant Science, 172,
Revista Mexicana de Ingeniería Química, 6, 19–25. 1–7.
de Souza, R. L. A., Santana, M. F. S., de Macedo, E. M. S., de Brito, E. S., & Correia, R. T. P. West, M. E., & Mauer, L. J. (2013). Color and chemical stability of a variety of anthocyanins
(2015). Physicochemical, bioactive and functional evaluation of the exotic fruits and ascorbic acid in solution and powder forms. Journal of Agricultural and Food
Opuntia ficus-indica and Pilosocereus pachycladus Ritter from the Brazilian caatinga. Chemistry, 61, 4169–4179.
Journal of Food Science and Technology, 52, 7329–7336. Wong, Y. -M., & Siow, L. -F. (2015). Effects of heat, pH, antioxidant, agitation and light on
Stevens, L. J., Kuczek, T., Burgess, J. R., Stochelski, M. A., Arnold, L., & Galland, L. (2013). betacyanin stability using red-fleshed dragon fruit (Hylocereus polyrhizus) juice and
Mechanisms of behavioral, atopic, and other reactions to artificial food colors in chil- concentrate as models. Journal of Food Science and Technology, 52, 3086–3092.
dren. Nutrition Reviews, 71, 268–281. Woo, K. K., Ngou, F. H., Ngo, L. S., Soong, W. K., & Tang, P. Y. (2011). Stability of betalain
Stintzing, F. C., & Carle, R. (2007). Betalains — Emerging prospects for food scientists. pigment from red dragon fruit (Hylocereus polyrhizus). American Journal of Food
Trends in Food Science & Technology, 18, 514–552. Technology, 6, 140–148.
Strack, D., Vogt, T., & Schliemann, W. (2003). Recent advances in betalain research. Wruss, J., Waldenberger, G., Huemer, S., Uygun, P., Lanzerstorfer, P., Müller, U., et al.
Phytochemistry, 62, 247–269. (2015). Compositional characteristics of commercial beetroot products and beetroot
Sui, X., Dong, X., & Zhou, W. (2014). Combined effect of pH and high temperature on the juice prepared from seven beetroot varieties grown in Upper Austria. Journal of Food
stability and antioxidant capacity of two anthocyanins in aqueous solution. Food Composition and Analysis, 42, 46–55.
Chemistry, 163, 163–170. Wybraniec, S., & Michałowski, T. (2011). New pathways of betanidin and betanin enzy-
Sumaya-Martínez, M. T., Cruz-Jaime, S., Madrigal-Santillán, E., García-Paredes, J. D., matic oxidation. Journal of Agricultural and Food Chemistry, 59, 9612–9622.
Cariño-Cortés, R., Cruz-Cansino, N., et al. (2011). Betalain, acid ascorbic, phenolic con- Wybraniec, S., Stalica, P., Spórna, A., & Mizrahi, Y. (2010). Profiles of betacyanins in epi-
tents and antioxidant properties of purple, red, yellow and white cactus pears. dermal layers of grafted and light-stressed cacti studied by LC-DAD-ESI-MS/MS.
International Journal of Molecular Sciences, 12, 6452–6468. Journal of Agricultural and Food Chemistry, 58, 5347–5354.
Swarna, J., Lokeswari, T. S., Smita, M., & Ravindhran, R. (2013). Characterisation and deter- Yahia, E. M., & Mondragon-Jacobo, C. (2011). Nutritional components and anti-oxidant
mination of in vitro antioxidant potential of betalains from Talinum triangulare (Jacq.) capacity of ten cultivars and lines of cactus pear fruit (Opuntia spp.). Food Research
Willd. Food Chemistry, 141, 4382–4390. International, 44, 2311–2318.
Swaroop, V. R., Roy, D. D., & Vijayakumar, T. (2011). Genotoxicity of synthetic food color- Yu, Z. -H., Han, Y. -N., & Xiao, X. -G. (2015). A PPO promoter from betalain-producing red
ants. Journal of Food Science and Engineering, 1, 128–134. swiss chard, directs petiole- and root-preferential expression of foreign gene in an-
Szopińska, A. A., & Gawęda, M. (2013). Comparison of yield and quality of red beet roots thocyanins-producing plants. International Journal of Molecular Sciences, 16,
cultivated using conventional, integrated and organic method. Journal of Horticultural 27032–37043.
Research, 21, 107–114. Zehring, J., Reim, V., Schröter, D., Neugart, S., Schreiner, M., Rohn, S., & Maul, R. (2015).
Tennant, D. R., & Klingenberg, A. (2016). Consumer exposures to anthocyanins from col- Identification of novel saponins in vegetable amaranth and characterization of their
our additives, colouring foodstuffs and from natural occurrence in foods. Food hemolytic activity. Food Research International, 78, 361–368.
Additives & Contaminants: Part A. http://dx.doi.org/10.1080/19440049.2016.1179561. Žilić, S., Kocadağlı, T., Vančetović, J., & Gökmen, V. (2016). Effects of baking conditions and
Tesoriere, L., Allegra, M., Butera, D., & Livrea, M. A. (2004). Absorption, excretion, and dis- dough formulations on phenolic compound stability, antioxidant capacity and color
tribution of dietary antioxidant betalains in LDLs: Potential health effects of betalains of cookies made from anthocyanin-rich corn flour. LWT — Food Science and
in humans. American Journal of Clinical Nutrition, 80, 941–945. Technology, 65, 597–603.