SciELO - Scientific Electronic Library Online

 
vol.50 número8Productividad y calidad industrial de trigos harineros en relación a enfermedadesCalidad de la luz led y desarrollo in vitro de Oncidium tigrinum y Laelia autumnalis (orchidaceae) índice de autoresíndice de assuntospesquisa de artigos
Home Pagelista alfabética de periódicos  

Serviços Personalizados

Journal

Artigo

Indicadores

Links relacionados

  • Não possue artigos similaresSimilares em SciELO

Compartilhar


Agrociencia

versão On-line ISSN 2521-9766versão impressa ISSN 1405-3195

Agrociencia vol.50 no.8 Texcoco Nov./Dez. 2016

 

Food science

Nutraceutic aspects of pigmented maize: digestibility of carbohydrates and anthocyanins

L. Arturo Bello-Pérez1  * 

Gustavo A. Camelo-Mendez1 

Edith Agama-Acevedo1 

Rubí G. Utrilla-Coello2 

1 Instituto Politécnico Nacional, CEPROBI, Km. 8.5 carretera Yautepec-Jojutla, colonia San Isidro, 62731 .Yautepec, Morelos, México. labellop@ipn.mx.

2 Instituto Politécnico Nacional, CIIDIR-Oaxaca, Hornos No. 1003, Colonia Noche Buena, Santa Cruz Xoxocotlán, 71230. Oaxaca, México.


Abstract

Pigmented maize is traditionally used as food in various countries, particularly in Latin America. In Mexico its use is in nixtamalized products such as tortillas, snacks, toasted tortillas and tamales, among others. The main component of the maize grain is starch, which provides functional and nutritional properties to the products that are elaborated with this cereal. The anthocyanins give the characteristic color to these types of maize and have beneficial properties for human health. Anthocyanins are associated with disease prevention, such as cancer, due to its antioxidant properties, as they seize free radicals in the bloodstream that are associated with the development of these disorders. The interactions between bioactive compounds and carbohydrates are important because they could limit or boost bio-accessibility and reduce the digestibility of starch. The study of the interactions between carbohydrates and anthocyanins in pigmented maize is underdeveloped, but evidence indicates the nutraceutical function of both compounds, and as such it is necessary to carry out further research in this sense.

Key words maize; starch; anthocyanins; dietary fiber

Resumen

Los maíces pigmentados se usan tradicionalmente en la alimentación en diversos países, principalmente de América Latina. En México se usan en productos nixtamalizados como las tortillas, botanas, tostadas y tamales, entre otros. El principal componente del grano de maíz es el almidón, el cual imparte las propiedades funcionales y nutricionales a los productos elaborados con este cereal. Las antocianinas dan la coloración características a estos maíces y tienen propiedades benéficas para la salud de los humanos. Las antocianinas están asociadas con la prevención de padecimientos, como el cáncer, por sus propiedades antioxidantes, ya que secuestran radicales libres en el torrente sanguíneo, los cuales están asociados con el desarrollo de estas patologías. Las interacciones entre compuestos bioactivos y carbohidratos son importantes porque pudieran limitar o potenciar su bioaccesibilidad y disminuir la digestibilidad del almidón. El estudio de las interacciones entre carbohidratos y antocianinas en maíces pigmentados está poco desarrollado, pero las evidencias señalan la función nutracéutica de ambos compuestos, por lo cual es necesario realizar más investigación al respecto.

Palabras claves: maíz; almidón; antocianinas; fibra dietética

Introduction

Maize (Zea mays L.) is the staple food of the diet in Mexico and other cultures. Mexico is the center of origin for maize, whose nixtamalization provides an important nutritional contribution to this cereal. Nixtamalized maize products like tortillas and other snacks are consumed in countries as diverse as China and Australia.

White and yellow maize are the main varieties used in nixtamalized products, but in other regions, especially in central Mexico, other pigmented varieties like red, blue, purple, and black are used. These colors are due to the anthocyanins that are present, principally in the pericarp and the aleuronic layer. People in this region prefer to consume “tortillas”, “tamales” and “atoles” with these pigmented varieties of maize because they say that the taste and texture is different than those foods made with white and yellow maize. While studies with the starch of pigmented corn have shown similar physiochemical, molecular and structural characteristics (Agama-Acevedo et al., 2005, 2008), research has shown that tortillas elaborated with these pigmented maize varieties have less digestibility of starch (Hernández-Uribe et al., 2007), which could be an effect of the anthocyanins. There are studies of pigmented maize that focus on the isolation of the anthocyanins for its pharmaceutical and food use, while others focus on pigmented maize to elaborate food that have antioxidant properties.

This essay shows the importance of the interaction between anthocyanins and carbohydrates, the possible mechanisms to reduce the digestion and absorption of glycemic carbohydrates, as well as where future research should focus to advance the knowledge on this topic.

Generalities about maize

Maize is one of the plants with greater domestication and evolution, and moreover, its genetic diversity is concentrated in Mesoamerica, principally Mexico, which is the principal center of origin, domestication and diversification of this plant. The diversification is very extensive, and in the country there are 59 maize races described (Sánchez et al., 2000), which is a significant percentage of the 220 to 300 species that exist in the Americas (Kato et al., 2009). The race show pigmented grain varieties, with colors that range from black to light pink, with the most common being red and blue/purple (Salinas, 2010).

The annual world production of maize is greater than 1000 million Mg, with the principle producers being the United States, China, Brazil, the European Union, Argentina and Ukraine (FAO, 2015; Singh et al., 2011). In Mexico the production of maize in 2012 was 22,069,254 Mg (SIAP, 2013). However, there are no official statistics about the world or national production of pigmented maize and this data is only reported in the states of Chiapas (Salinas et al., 2012a), Sinaloa, Tlaxcala (Agama-Acevedo et al., 2011) and the Estado de Mexico (Salinas et al., 2010). This is due to the fact that pigmented maize is produced by subsistence farmers on small parcels and the majority of their production is for self-consumption. In the Estado de Mexico and state of Puebla, the cost-benefit relationship of the production of blue maize is 2.24, which is greater than the ratio 1.57 of commercial maize of white grain (Keleman y Hellin, 2009). The development and the cultivation of other pigmented varieties and hybrids have increased in Bolivia, Germany, China and the United States

In Mexico, the daily consumption of maize is 335 g, which is equivalent to 122 kg each year-1 (FAO, 2012), and comes in the form of tortillas, gorditas, pinoles, atoles, toasted tortillas, snacks, tamales, corn on the cob and many others (Figueroa et al., 2005). Maize is also used in various industries like textile, cosmetics, and food (Rooney y Serna-Saldivar, 2003), which make it economically important globally.

Pigmented maize and its products

Pigmented maize genotypes are common in the Peruvian Andes, as pigmented maize is understood as those that owe their color to pigments like carotenoid (yellows), as well as those that have anthocyanin pigments (reds, purples, pinks, among others) in the pericarp and the aleuronic layer or in both structures of the grain (Wellhausen et al., 1951; Salinas, 2010). There is a marginal presence (0.07 a 008 mg grano-1) of these polyphenols in the endosperm and the embryo (Cui et al., 2012). The accumulation of pigment in the grain structures determines the possible use of these varieties of maize. For example, if the pigment concentrates in the aleuronic layer, the grain can be used for the nixtamalization and produce products with blue tones. However, if the pigment concentrates in the pericarp the and amount is sufficient enough, the pigmented grain could be used for the extraction of pigments (Salinas et al., 1999; Salinas, 2009).

In the states of Chiapas, Oaxaca and the State of Mexico, the maize species are pigmented: Olotillo, Tehua, Olotón, Tepecintle, Vandeño, Zapalote Chico y Grande, Bolita, Cónico, Mushito and Tuxpeño (Salinas-Moreno et al., 2012a, 2013), but there are no statistics about their production. The diversity of pigmented maize, and its diverse uses, can be observed in its physical properties (Table 1), which is important to choose the variety of pigmented maize and the characteristics of texture and taste for the products that will be elaborated from these.

The consumption of pigmented maize increased in the United States, whereas in Mexico, pigmented maize is primarily used to elaborate tortillas for self-consumption, as well as on a small-scale, in commercial establishments to be used as traditional food. However of the total production of maize in Mexico, the pigmented maize only represents 10%, which indicates low achievement, since its nutritional content and nutraceutical properties represents a significant opportunity for the development of new products with new or better functional and nutritional characteristics.

The nutraceutical properties of pigmented maize are related to its high content of anthocyanins, which y Grande, Bolita, Cónico, Mushito and Tuxpeño (Salinas-Moreno et al., 2012a, 2013), but there are no statistics about their production. The diversity of pigmented maize, and its diverse uses, can be observed in its physical properties (Table 1), which is important to choose the variety of pigmented maize and the characteristics of texture and taste for the products that will be elaborated from these.

Table 1 Physical properties of pigmented maize. 

Maíz Peso de cien granos (g) Peso hectolítrico (kg hL-1) Índice de flotación Referencia
Azul-Rojo(Arrocillo amarillo) 26.8 75.6 27.1 Salinas-Moreno et al. (2003)
Azul-Rojo (Bolita) 36.8 74.9 57.1
Azul-Rojo (Elotes Chalqueños) 46.0 71.2 82.2
Azul-Rojo (Azul x Cristalino de Chihuahua) 33.3 75.2 80.3
Blanco (México) 34.9 Nd nd Del Pozo-Insfran et al. (2007)
Azul (México) 38.2
Azul(EE.UU.) 32.0
Azul/Rojo (Olotillo) 38.22 Nd 49 Salinas-Moreno et al. (2012a)
Azul (Olotón) 26.7 38
Azul, rojo, magenta (Tehua) 39.9 34
Azul (Tepecintle) 42.9 51
Azul, rojo, magenta (Tuxpeño) 37.3 31
Azul, rojo, magenta (Vandeño) 35.7 25
Azul (Zapalote grande) 31.3 38
Azul/Morado (Chalqueño) 25.1-46.8 Nd nd Salinas-Moreno et al. (2012b)
Azul/Morado (Elote cónico) 24.8-46.8
Azul/Morado (Bolita) 39.2-46.8
Azul/Morado (Tropicales) 27.2-33.7 75.1-79.9 16-73 Salinas-Moreno et al. (2013)
Azul/Morado (Subtropicales) 34.5-40.6 77.9-80.7 22-37
Azul/Morado (Bolita) 37.3-47.5 75.9-79.7 8-69
Azul/Rojo (Hibridos) Celaya 30.1-43.7 Nd 10-99.3 Urias-Peraldi et al. (2013)
Azul/Rojo (Híbrido) Morelia Azul/Rojo (Híbrido) Morelia 10-99.6

Nd; not determined.

The consumption of pigmented maize increased in the United States, whereas in Mexico, pigmented maize is primarily used to elaborate tortillas for self-consumption, as well as on a small-scale, in commercial establishments to be used as traditional food. However of the total production of maize in Mexico, the pigmented maize only represents 10%, which indicates low achievement, since its nutritional content and nutraceutical properties represents a significant opportunity for the development of new products with new or better functional and nutritional characteristics.

The nutraceutical properties of pigmented maize are related to its high content of anthocyanins, which possess beneficial biological activity (antioxidants), derived from its secondary metabolites (Ruiz et al., 2008; Mora-Rochin et al., 2010; Mendoza-Díaz et al., 2012). These compounds have a positive effect on health: their antioxidant activity reduces mutagenesis (López-Martínez et al., 2009; Zhao et al., 2009) and the proliferation of the growth of cancerous cells (Jing et al., 2008; Urias-Lugo et al., 2015), and anti-inflammatory cells (Li et al., 2012; Zhu et al., 2013). Besides, anthocyanins in the maize grain have a protecting action against nephropathy that develops in patients with type-2 diabetes (Li et al., 2012). However, these properties are lost during the boiling of the maize before its consumption. As such, the cooking method and the duration of the thermal treatment should be studied to see how these factors affect the properties of the anthocyanins in the human body.

Chemical composition

The chemical composition of the maize grain is affected by the genotype (variety), the environment and by the conditions during cultivation (Table 2).

Table 2 Chemical composition of pigmented maize (g 100 g -1 ) 

Maíz Humedad Proteínas Cenizas Lípidos Carbohidratos Referencia
Blanco 6.6 9.3 1.2 4.8 78.2 Agama-Acevedo et al. (2005)
Azul 9.8 8.2 1.1 3.7 77.2
Negro 8.4 9.4 1.6 4.0 76.2
Blanco 6.3 7.5 0.6 0.2 78.7 Utrilla et al. (2009)
Azul 7.4 8.3 0.3 0.5 84.1
Conejo ND 101 ND 4.7 ND Salinas-Moreno et al. (2013)
EO 102 4.4
Olotillo 102 4.3
Tepeantle 9.6 4.4
Tuxpeño 9.8 4.2
ZC 9.7 5
Chiquito 11 5
EC 10.5 4.6
EO 10 5.2
Bolita 10-11.6 5-5.6

x ND: not determined.

On average, makes up 10 % of maize and the majority of it is found in the endosperm of the grain. Pigmented maize (blue and black) has an 8.2 to 9.4 % composition of proteins (Agama-Acevedo et al., 2005; Utrilla-Coello et al., 2009), whereas in the state of Oaxaca, the species of pigmented maize that has adapted to tropical climates have 9.5 to 10.4 % protein makeup and a 10.1 to 10.6 % in subtropical climates, and in some segregating varieties of the species Bolita, there is a positive relationship between the hardness of the grain and the protein composition that is attributed to a greater presence of protein bodies (prolamins) that surround the starch granules (Salinas-Moreno et al., 2013). A vitreous endosperm relationship can be present in the maize grain: floury of 2:1, but it varies considerably according to the race (Inglett et al., 1970).

The lipid content of the maize grain is about 5 % and is principally located in the seed. In pigmented maize, the content varies between 3.7 to 5 % (Agama-Acevedo et al., 2004; Salinas-Moreno et al., 2013), but in the endosperm of blue maize, there is only 0.52 % (Utrilla-Coello et al., 2009). The ash content, that is the minerals present in pigmented maize, is ≈ 1 to 2 %, and the majority is in the seed of the grain.

Carbohydrates are the major component of the maize grain, and in pigmented maize they vary from 76 to 84 % (Agama-Acevedo et al., 2004). Starch is the main carbohydrate in maize and is formed by amylose, or linear component, and amylopectin, or branched component (Table 3). The starch in pigmented maize presents ≈20 % of amylose, but there are species with 13 % (De la Rosa-Millán et al., 2010), which indicates differences in the organization of these components inside the starch granule and as such, there are differences in the functional and nutritional properties. Despite the diversity in the species of pigmented maize, there are few studies about the characteristics of their starch, which is a topic that should be further investigated to strengthen its use and application.

Table 3 Starch and amylose content in pigmented maize (g 100 g -1 ). 

Maíz Almidón Amilosa Referencia
Blanco 60.21 27.2 Agama-Acevedo et al. (2004)
Negro 79.20 22.3
Azul 73.4 20.3
Blanco 78.7 26.3 Utrilla-Coello et al. (2009)
Azul 84.1 23.1
101 23.5
111 28
177 ND 13 De la Rosa Millán et al. (2010)
196 20.5
444 21
455 18
Blanco 70.9-76.2 20.5-32.8 Agama-Acevedo et al. (2013)
Azul 71.3-81.73 22.3-27.4

ND: not determined.

Anthocyanins

Anthocyanins are phenolic compounds from the flavonoid group (Escribano-Bailón et al., 2004) and in their formula there are two aromatic rings connected by a three-carbon structure (Gross, 1987). In their natural form, this structure is found esterified to one or two sugars, denominating them simple anthocyanins; however, if in addition to the sugar in the molecule, there is an acyl radical, then, these are called acrylate anthocyanins (Strack and Wray, 1989). The anthocyanin content varies between species (Table 4); maize with low anthocyanin content are yellow and pink maize; those with medium levels of anthocyanins are blue; and maize with the highest levels are those with purple and black grains (Salinas-Moreno et al., 2013).

Table 4 Anthocyanin content in pigmented maize 

Maíz Origen Antocianinas* CA Referencia
Azul Estado de México, México 291.5±14.4 Nd. Agama-Acevedo et al. (2004)
Negro 100.7±17.6
Azul Canadá 196.7±2.-322.7 Nd. Abdel-Aal et al. (2006)
Rosa 163.9
Morado 1277
Rojo escaralata 607.1
Rojo rubí 69.4
Rojo carmesí 50.9
Azul Querétaro, México 271.2±2.1 Nd. Cortés et al. (2006)
Blanco Toluca, México Nd 17.41 Del Pozo-Insfran et al. (2007)
Azul 342.2 29.61
Azul Nuevo México, EE.UU. 260.9 25.61
Rosa (JHY) 127.4.1 Nd.
Gris (BP) 292.2±8.6
Rojo carmesí (SZ) 1493±56.3 Zhao et al. (2008)
Morado (JHN) 2565±112.1
Negro (EZPC) 3045±163.2
Negro D.F., México 762±22 ~742 López-Martínez et al. (2009)
Morado 932±11 ~762
Rojo Puebla, México 852±22 ~752
Azul D.F., México 995±18 ~552
Naranja Oaxaca, México 306±9 ~352
Amarillo Veracruz, México 702±9 ~902
Blanco 154±9 ~262
Púrpura Estado de México, México 1269.4 Nd. Espinosa-Trujillo et al. (2009)
Rojo Puebla, México 57.0
Azul Tlaxcala, México 371.7
Morado Hidalgo, México 48.8
Azul D.F., México 631±14 ~542 López-Martínez et al. (2011)
Rojo 823±38 ~652
Morado Veracruz, México 3251±72 ~602
Morado Cajamarca, Perú 2870±40 20.51 Ramos-Escudero et al. (2012)
Rojos-Olotillo Chiapas, México 547.7 81.73 Salinas-Moreno et al. (2012a)
Rojos-Tehua 105.2-151.7 44.5-66.53
Rojos-Tuxpeño 71.6-126.0 32.0-89.53
Rojos-Vandeño 64.7-90.8 37.7-733
Azul/Morado Chalqueño D.F., México 720.9-1046.1 34.0-60.33 Salinas-Moreno et al. (2012b)
Azul/Morado Estado de México, México
Elote Cónico 997.8-1332.2 46.6-60.43
Azul/Morado
Bolita Oaxaca, México 304.1-528.0 21-39.53
Amarillo-Rojo EE.UU. 2.5±0.06 ~244 Zilic et al. (2012)
Rojo 15.43±1.64 ~264
Rojo oscuro Serbia 696.07±2.73 ~274
Azul claro 378.92±4.89 ~354
Azul oscuro EE.UU. 597.15±6.54 ~284
Multicolor Holanda 139.12±1.63 ~194
Híbridos (negros y rojos) Celaya, México 181.6-769.4 6.8-285
Morelia, México 307.2-796.2 Urias-Peraldí et al. (2013)

AC: Antioxidant capacity, *Values are expressed in mg equivalents of cyaniding-3-glucoside kg-1 of the sample. The antioxidant activity is expressed in:1 μM of equivalents of de trolox g-1 of the sample; 2Percentage of radical reduction; 3Percentage of DPPH radical reduction; 4mM of equivalent of trolox kg-1 of the sample; 5mM of equivalents of trolox 100 g-1 of the sample; Nd: not determined.

In maize, anthocyanins are peonidin (Aoki et al., 2002; Abdel-Aal et al., 2006; Montilla et al., 2011; Zilic et al., 2012; Salinas-Moreno, et al., 2012b), malvidin (Caldwel and Peterson, 1992), cyanidin, (Aoki et al., 2002; Abdel-Aal et al., 2006; Zilic et al., 2012) and pelargonidin (Aoki et al., 2002; Montilla et al., 2011; Zilic et al., 2012), and the anthocyanin glycosides are the anthocyanins. Salinas-Moreno et al. (1999) analyzed the anthocyanin in blue and red grain maize in four species, and found that in the blue grain maize, the anthocyanin are derived from cyanidin and malvidin, and are predominately derived from the former; red-grain maize is derived from pelargonidin, cyanidin, malvidin and an unidentified aglycone. The characterization of the type of anthocyanins in pigmented maize is important, but the effect associated with the consumption of pigmented maize after its processing (i. e. nixtamalization) is even more important. Urias-Lugo et al. (2015) evaluated anthocyanins from blue maize hybrid and native blue maize for the proliferation of cancer cells in breasts (MCF7), liver (HepG2), colon (Caco2 y HT29) and prostate (PC3); they found that acidified extracts presented greater anti-proliferative activity.

Antioxidant capacity and bioavailability

Pigmented maize has potential benefits beyond its nutritional value. For example, blue and red maize inhibit colorectal carcinogenesis in male rats (Hagiwara et al., 2001), they present anti-mutagen properties (Yoshimoto et al., 1999) and they capture free radicals (Del Pozo-Insfran et al., 2006, 2007); this last point is an accepted mechanism for antioxidant activity related to the inhibition of lipid peroxidation (Brand-Williams et al., 1995). The function of anthocyanins in plants is similar to the function of all of the flavonoids: antioxidants, light protection, defense mechanisms, as well as other ecological functions (Escribano-Bailón et al., 2004).

Because the interest in developing foods with blue maize for its antioxidant properties, the processing method is important in the conservation of bioactive prosperities. In this sense, the effect of the nixtamalization process on the phytochemical profiles (total phenols, anthocyanins, ferulic acid, carotenoids) has been studied, along with the antioxidant capacity of five types of maize processed into dough, tortillas and tortilla chips; the nixtamalization process was observed to significantly reduce the content of total phenols and the antioxidant capacity, in comparison to raw grains (De la Parra et al., 2007). Besides, Bello-Pérez et al. (2015) studied the effect of ecological nixtamalization (using calcium salts) on the content of total anthocyanins and the antioxidant capacity of blue maize tortillas; they found that the ecological method was not aggressive and conserved the antioxidant capacity in the tortillas, in comparison to lime, which is used in the traditional nixtamalization process.

To establish the final intake of anthocyanins and the antioxidant capacity of food, such as those elaborated with blue maize (Table 5), one must take into consideration pre-treatments, the type of cooking method, as well as the type of product used (whether it is to be mixed with other ingredients or used as raw material). The anthocyanin stability depends on the processing of the food and the formation of the food matrix, which can protect against factors such as light, temperature and humidity during the processing, and storage and consumption of the product (Escribano-Bailón et al., 2004). Phenolic compounds, with biological and chemical properties interact through non-covalent bonds with macromolecules (proteins, lipids and polysaccharides) in biological systems, (Bordenave et al., 2014), with a positive impact on the texture, nutritional and sensorial properties of the product, which has implications on its bioavailability. However, the studies on the use of blue maize for the development of functional food are limited and as such require more research.

Table 5 Antioxidant properties in foods elaborated with blue maize 

Producto Propiedades antioxidantes Referencia
Tortillas Presentó aproximadamente del 65-75 % de capacidad antioxidante referente a valores ORAC. Aguayo-Rojas et al. (2012)
Nejayote Presentó capacidad antioxidante significante representada por la metodología ORAC de compuestos libres y unidos (13.791 y 436.66 mM equivalentes trolox 100 g-1 de muestra respectivamente) Gutiérrez-Uribe et al. (2010)
Grano Presentó capacidad antioxidante como inhibición de radical libre DPPH (60 %) y ABTS (55 %) Lopez-Martínez et al. (2009)
Tortilla de harina nixtamalizada Presentó capacidad antioxidante significante por la metodología ORAC de compuestos libres y unidos (0.002 y 0.008 mol equivalentes trolox100 g-1 de muestra respectivamente) Mora-Rochin et al. (2010)
Tortilla de harina extruida Presentó capacidad antioxidante significante por la metodología ORAC de compuestos libres y unidos (0.0025 y 0.009 mol equivalentes trolox 100 g-1 de muestra, respectivamente) Mora-Rochin et al. (2010)
Tortillas y chips Presentaron capacidad antioxidante significante por la metodología ORAC (15, 12 y 14, 10 mmol ET g-1) elaboradas con maíz mexicano y americano, respectivamente Del Pozo-Insfran et al. (2006)
Tortilla tradicional y nixtamalizada con sal de calcio Presentaron capacidad antioxidante significante de los polifenoles extraíbles polifenoles hidrolizables y taninos condensados por las metodologías DPPH(0.5-2.0 mM Trolox/g-1), ABTS (0.1-0.5 mM Trolox/g) y FRAP (0.1-0.6 mM Trolox/g-1) respectivamente Bello-Pérez et al. (2015)

Carbohydrates

Carbohydrates, the main component of pigmented maize, are found in the cells of the endosperm, principally in the form of starch. Carbohydrates represent about 78% of the dry weight of the grain, while in some races, variants of blue maize (Table 2), this can reach up to 84%. There is a minimum amount of simple carbohydrates (monosaccharaides and disaccharides) known as sugars in the maize grain and these represent close to 2% of the dry weight of the grain. Starch is the principal carbohydrate in maize, and there is more starch in pigmented maize than in white maize (Table 3), which is related to the biosynthesis of the polysaccharide and requires further study. Starch, as the main component in the maize grain, is what most influences the functional (texture) and nutritional (caloric intake) properties of the products that are elaborated with this cereal, like tortillas, tamales, bread, cookies, etc. Starch is formed by macromolecules of glucose (amylose and amylopectin); amylose is an essential linear component while amylopectin is a branched component. The proportion of both components in the starch has implications in its functionality. In this sense, starches with 98-99% of amylopectin provide high viscosity, and starches with higher content of amylose form gels that harden (retrograde) more rapidly (Biliaderis, 1991). The maize used in the food industry has a proportion (%) of amylose: amylopectin of 30:70, denominated normal starches. According to De la Rosa-Millán et al. (2010), amylose varies between 13-28 % in blue maize.

Starch is organized in discreet particles known as granules, whose size and shape depends on the botanical source (cereal, tubers, legumes, fruit). Starch from maize has two populations: small granules of 1-10 mm, and large granules between 15-40 mm. Even though the two populations of granules are inside the same source, they have different amylose content and physicochemical properties. (Jane, 2006). In isolated starch of blue maize, granules between 20 y 40 μm were found (Agama-Acevedo et al., 2008). Utrilla-Coello et al. (2010) found a bimodal distribution in the starch of blue maize, where the highest point of the first spike was at 3 mm, which represented 24 % of the total volume; the highest point of the second spike was at 9 mm, which is related to the population of large granules and represents 76%. The starch of pigmented maize, like the starch of other cereals (wheat, rice, barley) presents A-type diffraction pattern (Agama-Acevedo et al., 2008; De la Rosa-Millan et al., 2010).

Agama-Acevedo et al. (2013) evaluated the characteristics of starch and its relation to the enzymes of its biosynthesis during the development of the grain of two maize varieties (white and blue); 50 days after the pollination (ddp), the blue maize accumulated a greater amount of starch and had less amylose content. Besides, they found two isoforms from the branched enzyme in the starch of the blue maize, which is related to the production of highly branched amylopectin molecules with short chains, leaving less available space inside the granular structure for amylose synthesis. In that study, the starch from the blue maize presented a higher temperature and enthalpy of gelatinization than the white maize, which is important during the cooking of maize and the other products made with this cereal. In other studies, there were no differences in temperature of gelatinization, only small changes in its enthalpy (Agama-Acevedo et al., 2008; De la Rosa-Millán et al., 2010; Utrilla-Coello et al., 2010). However, the organization and distribution of the chains of amylopectin inside the starch granule needs to be researched since this influences the physiochemical properties and digestibility.

Starch digestibility

Starch is the majority component of maize; thus, the products of this cereal represents an important supply of glucose in humans’ diets. In the early 1990s, a fraction of starch was found not to hydrolyze, for which it was called resistant starch (RS) (Englyst et al., 1992). The consumption of RS was related to various health benefits, for which a number of foods were analyzed in order to know the amount of RS (Muir et al., 1994; Kritchevsky, 1995; Cummings et al., 1996). One type of RS was formed when foods rich in starch were cooked and stored, which was due to the phenomenon of starch retrogradation that consists of a re-arrangement of its structure that is not recognized by the salivary and pancreatic a-amylases and cannot be hydrolyzed, following its course to the large intestine, where is then fermented by the bacteria found in the colon. In nixtamalized maize tortillas (white or yellow grain) the increase in RS was directly proportional to the storage time and was favored by a temperature of 4 °C (Agama-Acevedo et al., 2005). However, the properties of starch digestibility in tortillas elaborated with blue maize were not affected by time or temperature in storage. The available starch and the RS did not see a change after 48 hours of storage (Hernández-Uribe et al., 2007). This characteristic of blue maize tortillas was related to its thermal properties, due to a low tendency for retrogradation. It was unknown if the differences found in the digestibility of the starch in blue maize tortillas were due to the physical characteristics of the maize grain, the starch per se or the anthocyanins present in the grain.

In terms of the physical characteristics of the blue maize grain, it has a floury endosperm (Serna-Saldivar, 2010). Tortillas elaborated with white maize with a floury endosperm did not present an increase in RS content during the storage compared with the tortillas elaborated with white maize with an intermediate or vitreous endosperm (Osorio-Díaz et al., 2011). Because of this, it was thought that the type of endosperm in blue maize influences the enzymatic hydrolysis of starch.

The possibility that morphological characteristics and the molecular organization of the starch could be responsible for the differences in the velocity of enzymatic hydrolysis, led to carrying out the characterization of starch from the blue variety, which differ in anthocyanin content. The two varieties of blue maize had a greater starch granule size, lesser content of amylose, and required more energy to disorganize due to a greater percentage of crystallinity compared to maize grains of the white variety (Agama-Acevedo et al., 2005,2008). Due to this, the digestibility properties of the starch in tortillas are associated with the differences found in the starch present in each type of maize. However, when blue maize was analyzed with similar values of anthocyanins, no considerable differences were observed, especially in the molecular characteristics. (De la Rosa-Millan et al., 2010).

The interest in knowing the rate of starch hydrolysis and its repercussions began research that emulated conditions that occur during the digestive process in humans. The most used protocol is the one proposed by Englys et al. (1992), that is based on the rate of starch hydrolysis; it considers that rapidly digestible starch (RDS) is hydrolyzed during the first 20 min, that slowly digestible starch (SDS) is hydrolyzed between 20 and 120 min, and after 120 min the starch that does not hydrolyze, or the RS is found. Beyond the velocity at which the starch is digested, the most important implication is the physiological effect that is produced when it is consumed.

The RDS is hydrolyzed in the first fraction of the small intestine, increasing the glucose in the blood immediately after its consumption, which is associated with multiple risk factors related to problems such as obesity, coronary diseases and heart troubles (Ludwin, 2002; Brennan, 2005). Contrarily, SDS is digested slowly throughout the small intestine with the subsequent slow release of glucose, for which its consumption reduces the responses of postprandial and insulinemic glucose, as well as fatty acids (Seal et al., 2003, Ells et al., 2005); likewise, even though it isn’t completely clear, this increases the feeling of satiety. This classification of starch, and the benefits attributed to SDS, the research to increase the SDS content in food, whether it is used as raw material (principally cereals that possess the characteristics that their starch without cooking is slowly digested) or to add to the development of food starches modified with a slow hydrolysis rate. In nutritional bars elaborated with a mix of oatmeal, barley, wheat and blue maize, there is a larger content of SDS (10.8 %), but less RS content (3.6 %), compared to the bars elaborated where blue maize was exchanged for white maize (7.1 % SDS y 4.4 % AR) (Utrilla-Coello et al., 2011). The highest SDS content found in the bar where blue maize was used is attributed to the high content of lipids, proteins and indigestible soluble fraction, which form a matrix that causes slow starch hydrolysis. Carrera et al. (2015) report an SDS content of 39.8 and 24.6 % in the flour of raw and toasted blue maize, respectively, for the elaboration of pinol (a pre Hispanic drink); these values were higher than the ones obtained by white maize for the same process. These differences can be related to the anthocyanin content and its effect on the digestibility of carbohydrates, but it requires more research.

The effect that anthocyanins found in blue maize have on the digestibility of starch is still not known with clarity. Anthocyanins are classified as flavonoids that are part of the group of polyphenol. It has been suggested that polyphenols can: 1) “Interfere” with digestive enzymes, changing the digestive process of starch with the reduction in the response of postprandial glucose; 2) have an effect on the on the carriers of glucose in the small intestine, and 3) provoke structural changes in starch because of the union with flavonoids through non covalent bonds. Up until now, the type of bond between starch and polyphenols has not been defined, since the possibility of hydrophobic interaction is also speculated (Barros et al., 2012). Even though this last point is controversial, there are reportd that the presence of polyphenols (proanthocyanidin) reduces the digestibility of starch (Barros et al., 2012); others report that the presences of flavonoids modifies the starch structure, causing the amylose to be more susceptible to the attack by amylases (Liu et al., 2011). Besides the tannins increased the RS (Barros et al., 2012; Mkandawire et al., 2013), they reduced SDS (Barros et al., 2012). The latter information is unclear because the authors do not specify if the tannins are hydrolysable or condensed; the former are formed by malic acid, phenolic acids and free sugars polymerized heterogeneously, while the latter are polymerized flavonoids. These structural differences in the tannins impact functionality.

The effect that polyphenols can have on the digestibility of starch depends on the type and amount of polyphenols present, the elaboration process of the product and if they are found in their natural form or are added to the food. The polyphenols that are added to food (more than 10% based on the weight of the starch), will produce structural changes in the starch and subsequently, the reduction of their digestibility; whereas polyphenols that are found naturally in food act as enzyme inhibitors for a-amylase and amyloglucosidase (He et al., 2006).

Dietary fiber

In maize, dietary fiber is found in the pericarp and is primarily made up of arabinoxylans, heteroxylans, cellulose and phenolic acids, principally ferulic and diferulic acid (Carvajal-Millan et al., 2007). Ferulic acid is the predominant phenolic compound in maize bran and is found bound to the cell wall (Fry, 1986). In pigmented maize grains, pigments have been found in the pericarp and in the aleuronic layer. The aleuronic layer of blue maize contains anthocyanin pigments, which gives its characteristic color. (Escalante-Aburto et al., 2013). When wholegrain is used, the pigmented maize has the advantage of a material that can present antioxidant properties, which in recent years, has gained importance due to the effect that it can have on humans’ health (this depends on the process of the maize grain before its consumption).

Arabinoxylans are principally found on the cell wall of the endosperm, on the aleuronic layer and in the pericarp of the maize (Carvajal-Millán et al., 2007). These compounds generate great interest due to their nutraceutical properties and the classification as a soluble fiber contributes to the control of diabetes and cardiovascular diseases. The effects of arabinoxylans on these illnesses are due to the increase in the absorption of minerals and the improvement of colon function; and they decreases the risk of colorectal cancer (Saedd et al., 2011). Furthermore, arabinoxylans contribute to transporting of phenolic compounds (ferulic and coumaric acid) and oligomers to the colon, presenting antioxidant characteristics with potential health benefits (Vitaglione et al., 2008).

In Mexico, nixtamalization is the principal way that maize is transformed for consumption. The alkaline cooking and the soaking that is involved in this process, provokes the dissolution and swelling of the pericarp layers. This makes the cell walls of the dietary fiber components of this part of the grain turn fragile, facilitating their soaking, which reduces the content of insoluble dietary fiber (Paredes-López et al., 2006). The nixtamalization process of pigmented maize affects anthocyanins, since it significantly reduces its content, which is because large quantities of these compounds degrade due to the alkaline pH and high temperature. Furthermore, other chemical structures derived from polyphenols are affected by the rupture of ester bonds and subsequently, phenols are liberated into the cooking solution. The majority of these compounds is found in the pericarp of the grain and is eliminated during the washing of the nixtamal (De la Parra et al., 2007; Escalante-Aburto et al., 2013). In this sense, new nixtamalization methods like fractioning and extrusion have been proposed, which in the case of pigmented maize has shown to retain a greater amount of anthocyanins (from 38 to 58 %) in products developed with these technologies. Additionally, during the processing, different compounds are formed or the content of the existing compounds is increased, which changes the profile of anthocyanins (Escalante-Aburto et al., 2013).

Interaction of carboydrates and anthocyanins: nutraceutical aspects

The use of pigmented maize has significantly increased for the development of foods with functional character like tortillas (Del Pozo-Insfran et al., 2006; de la Parra et al., 2007; Del Pozo-Insfran et al., 2007, Mora-Rochin et al., 2010; Aguayo-Rojas et al., 2012), cookies (Utrilla-Coello et al., 2011) and snacks (Del Pozo-Insfran et al., 2006, 2007), due to its content of anthocyanins and indigestible carbohydrates. However, there are very few studies that evaluate the interaction between carbohydrates (starch and non-starch polysaccharides) and anthocyanins in food, as well as their effect on the health of consumers.

Non-starch polysaccharides (dietary fiber) have an essential function in intestinal health and could be significantly associated with cholesterol reduction and a glycemic response. Additionally, phenolic compounds have antioxidant properties and free radical inhibitors that protect against oxidative damage to cells (Quiros-Sauceda et al., 2014). These properties are associated with the chemical structure of phenolic compounds, which determines their physiological and nutritional properties and should be considered during the development of nutraceutical foods. (Figure 1).

Figure 1 Effect of indigestible anthocyanins and carbohydrates for the development of nutracentical foods. 

Phenolic compounds, including anthocyanins, affect the digestibility of starch and the postprandial response of glucose by interfering with digestive enzymes (Lo Piparo et al., 2008; Barros et al., 2012, 2014; Miao et al., 2014) and the transportation of glucose in the wall of intestinal brush (Hanhineva et al., 2010), as well as in nutritional properties induced by the non-covalent interactions between flavonoids (polymeric or monomeric) and starch (Bordenave et al., 2014). In studies carried out with foods that contain phenolic compounds and carbohydrates, the content of the RS was observed to have increased when there was greater concentration of phenolic compounds (Barros et al., 2012). This increase in the RS content reduced the amount of starch digested as well as the rate with which it was digested, which means that the starch was digested slowly. Slow digestion of starch has been associated with beneficial health effects like the control of hunger and more evenly spaced consumption. Additionally, phenolic compounds had an effect on the in vitro digestibility of starch (Deshpande y Salunke, 2006; Barros et al., 2012) and in vivo (Yoon et al., 1983), as well as the reduction in the in vivo glycemic response (Kim et al., 2011; Liu et al., 2011; Rojo et al., 2012; Wedick et al., 2012).

The effect of slow digesting carbohydrates and the high dietary fiber content in the development of functional products has been reported (Ovando-Martínez et al., 2009, Gallegos-Infante et al., 2010a, 2010b; Khan et al., 2013; Sun-Waterhouse et al., 2013), as well as how phenolic compounds affect human health (Saura-Calixto, 2012; Wedick et al., 2012). However, the physiochemical, sensorial and nutritional aspects of the interaction between carbohydrates and anthocyanins and their effect on human health is still not completely clear. In the case of food elaborated with pigmented maize, the interaction between polysaccharides and anthocyanins is evaluated and its effect on the functional, sensorial and nutritional (beneficial effect on the health of its consumers) properties, requires more research.

Perspectives

The development of nutraceutical foods is a priority for the food industry, especially because of the interest in having healthy food that can help to prevent chronic-degenerative illnesses. Excess weight and obesity are two important risk factors for the development of those diseases, such as diabetes, high arterial pressure and cardiovascular diseases. Pigmented maize, which is cultivated around the world, has been underutilized, as white and yellow maize are more commonly consumed. The presences of anthocyanins in maize with shades ranging from black to red, makes maize a feasible raw material for the elaboration of nutraceutical foods like tortillas, breakfast cereals, snacks, and pastas. The interactions that are produced between anthocyanins and polysaccharides present in foods elaborated with pigmented maize and the impact on the digestion of starch, would help to understand the nutraceutical contribution of these products and advance the knowledge of the structural-functional relationship of said interactions.

Conclusions

Maize is a fundamental cereal in the diet of Mexico and in other countries. The use of pigmented maize in the development of food has been minimal when compared to white and yellow maize. Anthocyanins in pigmented maize have an antioxidant effect and can interact with polysaccharides (starch and dietary fiber), which limit the digestion of starch, and as such, the contribution of glucose into the bloodstream after consumption. Research has shown some beneficial effects on consumption of pigmented maize, but more studies must be done. Understanding the anthocyanin-polysaccharide interactions in foods elaborated with pigmented maize would aid in the development of nutraceutical foods, with a greater impact on the prevention of sicknesses like excess weight and obesity.

Literatura citada

Abdel-Aal, E-S. M., J. C. Young, and I. Rabalski. 2006. Anthocyanin composition in black, blue, pink, purple, and red cereal grains. J. Agric. Food Chem. 54:4696-4704. [ Links ]

Agama-Acevedo, E., M. A. Otthenhof, I. A. Farhat, O. Paredes López, J. Ortíz-Cereceres, and L. A. Bello-Pérez. 2004. Efecto de la nixtamalización sobre las características moleculares del almidón de variedades pigmentadas de maíz. Interciencia 29:643-649. [ Links ]

Agama-Acevedo, E., R. Rendón-Villalobos, J. Tovar, S. R. Trejo Estrada, and L. A. Bello-Pérez. 2005. Effect of storage time on in vitro digestion rate and resistant starch content of tortillas elaborated from commercial corn masas. Arch. Latinoam. Nutr. 55:86-92. [ Links ]

Agama-Acevedo, E., A.P. Barba D. L. R., G. Mendez-Montealvo., and L.A. Bello-Pérez. 2008. Physicochemical and biochemical characterization of starch granule isolated from pigmented maize hybrids. Starch/Starke 60: 433-441. [ Links ]

Agama-Acevedo, E., Y. Salinas-Moreno, G. Pacheco-Vargas, y L. A. Bello-Pérez. 2011. Características físicas y químicas de dos razas de maíz azul: morfología del almidón. Rev. Mex. Ciencias Agríc. 2:317-329. [ Links ]

Agama-Acevedo, E., E. Juárez-García, S. Evangelista-Lozano, O. L. Rosales-Reynoso, y L. A. Bello-Pérez. 2013. Características del almidón de maíz y relación con las enzimas de su biosíntesis. Agrociencia 47:1-12. [ Links ]

Aguayo-Rojas, J., S. Mora-Rochín, E. O. Cuevas-Rodríguez, S. O. Serna-Saldivar, J. A. Gutierrez-Uribe, C. Reyes-Moreno, and J. Milán-Carrillo. 2012. Phytochemicals and antioxidant capacity of tortillas obtained after lime-cooking extrusion process of whole pigmented Mexican maize. Plant Foods Human Nutr. 67:178-185. [ Links ]

Aoki, H., N. Kuze, and Y. Kato. 2002. Anthocyanins isolated from purple corn (Zea mays L.). Foods Food Ingred. J. Jpn. 199:41-45. [ Links ]

Barros, F., J.M. Awika, and L.W. Rooney. 2012. Interaction of tannins and other sorghum phenolic compounds with starch and effects on in vitro starch digestibility. J. Agric. Food Chem. 60: 11609-11617. [ Links ]

Bello-Perez, L.A., P.C. Flores-Silva, G. A. Camelo-Méndez, O, Paredes-López, and J. D. C. Figueroa. 2015. Effect of the nixtamalization process on the dietary fiber content, starch digestibility and antioxidant capacity of blue maize tortilla. Cereal Chem. 92: 265-270. [ Links ]

Biliaderis, C. G. 1991. The structure and interactions of starch with food constituents. Can. J. Physiol. Pharmacol. 69:60-78. [ Links ]

Bordenave, N., B. R. Hamaker, and M. G. Ferruzzi. 2014. Nature and consequences of non-covalent interactions between flavonoids and macronutrients in foods. Food Funct. 5: 1834. [ Links ]

Brand-Williams, W., M.E. Cuvelier, and C. Berset. 1995. Use of free radical method to evaluate antioxidant activity. Lebensm. Wiss. Technol. 28:25-30. [ Links ]

Brennan, C. S. 2005. Dietary fibre, glycaemic response, and diabetes. Mol. Nutr. Food Res. 49: 560-570. [ Links ]

Caldwell, E. E. O., and P. A. Peterson. 1992. HPLC identification of anthocyanins in maize endosperm. Maize Genet. Coop News 66: 2. [ Links ]

Carrera, Y., R. Utrilla-Coello, A. Bello-Pérez, J. Alvarez-Ramirez, and E. J. Vernon-Carter. 2015. In vitro digestibility, crystallinity, rheological, thermal, particle size and morphological characteristics of pinole, a traditional energy food obtained from toasted ground maize. Carbohydr. Polym. 123: 246-255. [ Links ]

Carvajal-Millan, E., A. Rascón-Chu, J. Márquez-Escalante, N. Ponce de León, V. Micard, and A. Gardea. 2007. Maize bran gum: Characterization and functional properties. Carbohydr. Polym. 69: 280-285. [ Links ]

Cortés, G. A., M. Y. Salinas, E. San Martín-Martínez, and F. Matínez-Bustos. 2006. Stability of anthocyanins of blue maize (Zea mays L.) after nixtamalization of separated periparp-germ tip cap and endosperm fractions. J. Cereal Sci. 43:57-62. [ Links ]

Cui, L., G. Rongqi, D. Shuting, J. Zhang, L. Peng, H. Zhang, J. Meng, and D. Shi. 2012. Effects of ear shading on the anthocyanin contents and quality of kernels in various genotypes of maize. Aust. J. Crop Sci. 4:704-710. [ Links ]

Cummings, J. H., E. R. Beatty, S. M. Kingman, S. A. Bingham, and H. N. Englyst. 1996. Digestion and physiological properties of resistant starch in the human large bowel. Br. J. Nutr. 75: 733-747. [ Links ]

De la Parra, C., S. O. Serna-Saldivar, and R. H. Liu. 2007. Effect of processing on the phytochemical profiles and antioxidant activity of corn for production of masa, tortillas, and tortilla chips. J. Agric. Food Chem. 55: 4177-4183 [ Links ]

De La Rosa-Millán, J., E. Agama-Acevedo, A.R. Jiménez-Aparicio, and L.A. Bello-Pérez. 2010. Starch characterization of different blue maize varieties. Starch-Starke 62: 549-557. [ Links ]

Del Pozo-Insfran, D., C.H. Brenes, S. O. Serna-Saldivar, and S. T. Talcott. 2006. Polyphenolic and antioxidant content of white and blue corn (Zea mays L.) products. Food Res. Int. 39: 696-703. [ Links ]

Del Pozo-Insfran D., S. O. Serna-Saldivar, C.H. Brenes, and S. T. Talcott. 2007. Polyphenolics and antioxidant capacity of white and blue corns processed into tortillas and chips. Cereal Chem. 84: 162-168. [ Links ]

Deshpande, S. S., and D. K. Salunke. 1982. Interactions of tannic acid and catechin with legume starches. J. Food Sci. 47: 2080-2081. [ Links ]

Ells, L. J., C. J. Seal., B. Kettliz, W. Bal and, J. C. Mathers. 2005. Postprandial glycaemic, lipaemic and haemostatic responses to ingestion of rapidly and slowly digested starches in healthy young women. Br. J. Nutr. 94: 948-955. [ Links ]

Englyst, H., S. Kigman, and J. Cummings. 1992. Classification and measurement of nutritionally important starch fractions. Eur. J. Clin. Nutr. 46: S33-S50. [ Links ]

Escalante-Aburto, A., B. Ramírez-Wong, P. Torres-Chávez, J. M. Barrón-Hoyos, J. D. Figueroa-Cárdenas, and J. López Cervantes. 2013. La nixtamalización y su efecto en el contenido de antocianinas maíces pigmentados, una revisión. Rev. Fitotec. Mex. 36:429-437. [ Links ]

Escribano-Bailón, M. T., C. Santos-Buelga., and J. C. Rivas Gonzalo. 2004. Anthocyanins in cereals. J. Chromatogr. A. 1054: 128-141. [ Links ]

Espinosa-Trujillo, E., M. C. Mendoza-Castillo, F. Castillo González, J. Ortiz-Cereceres, A. Delgado-Alvarado, and A. Carrillo-Salazar. 2009. Acumulación de antocianinas en pericarpio y aleurona del grano y sus efectos genéticos en poblaciones criollas de maíz pigmentado. Rev. Fitotec. Mex. 32:303-309. [ Links ]

FAO. 2012. Food and Agriculture Organization. FAOSTAT Base de Datos Estadísticos. El maíz en los trópicos. http://faostat.fao.org . (Acceded: February 2016). [ Links ]

FAO. 2015. Food and Agriculture Organization. FAOSTAT Base de Datos Estadísticos. El maíz en la nutrición humana. http://faostat.fao.org . (Acceded: February 2016). [ Links ]

Figueroa C. J. D., R. A. Mauricio, S. Taba, E. Morales, A. Mendoza-Gaytán, F. Rincón-Sánchez, L. M. Reyes, and J. J. Vélez. 2005. Kernel characteristics and tortilla making quality of maize accessions from Mexico, the Caribbean, and South and Central America. In: Proceedings of a Workshop held at CIMMYT, April 7-10 April. México, D.F. pp: 71. [ Links ]

Fry, S. C. 1986. Cross-linking of matrix polymers in the growing cell walls of angiosperms. Annu Rev. Plant Physiol. 37:165-186. [ Links ]

Gallegos-Infante, J. A., L. A. Bello-Perez, N. E. Rocha-Guzman, R. F. Gonzalez-Laredo, and M. Avila-Ontiveros. 2010a. Effect of the addition of common bean (Phaseolus vulgaris L.) flour on the in vitro digestibility of starch and undigestible carbohydrates in spaghetti. J. Food Sci. 75: 151-156. [ Links ]

Gallegos-Infante, J. A., N. E. Rocha-Guzman, F. R. Gonzalez Laredo, L. A. Ochoa-Martínez, N. Corzo, L. A. Bello-Perez, L. Medina-Torres, and L. E. Peralta-Alvarez. 2010b. Quality of spaghetti pasta containing Mexican common bean flour (Phaseolus vulgaris L.). Food Chem. 119: 1544-1549. [ Links ]

Gross, J. 1987. Pigments in Fruits. Academic Press. New York. 303 p. [ Links ]

Gutiérrez-Uribe, J. A., C. Rojas-García, S. García-Lara, and S. O. Serna-Saldivar. 2010. Phytochemical analysis of wastewater (nejayote) obtained after lime-cooking of different types of maize kernels processed into masa for tortillas. J. Cereal Sci. 52: 410-416. [ Links ]

Hagiwara, A., K. Miyashita, T. Nakanishi, M. Sano, S. Tamano, T, Kadota, T. Koda., M. Nakamura, K. Imaida, N. Ito, and T. Shirai. 2001. Pronounced inhibition by a natural anthocyanin, purple corn color, of 2-amino-1-methyl-6phenylimidazo[4,5-b]pyridine (PhIP)-associated colorectal carcinogenesis in male F344 rats pretreated with 1,2-dimethylhydrazine. Cancer Lett. 171: 17-25. [ Links ]

Hanhineva, K., R. Törrönen, I. Bondia-Pons, J. Pekkinen, M. Kolehmainen, H. Mykkänen, and K. Poutanen. 2010. Impact of dietary polyphenols on carbohydrate metabolism. Int. J. Mol. Sci. 11: 1365-402. [ Links ]

He, Q., Y. Lv, and K. Yao. 2006. Effects of tea polyphenols on activities of amylase, pepsin, trypsin and lipase. Food Chem. 101: 1178-1182. [ Links ]

Hernández-Uribe J. P., E. Agama-Acevedo, J. J. Islas-Hernández, J. Tovar, and L.A. Bello-Pérez. 2007. Chemical composition and in vitro starch digestibility of pigmented corn tortilla. J. Sci. Food Agric. 87: 2482-2487. [ Links ]

Inglett, E. 1970. Kernel structure, composition and quality. In: Inglett, E. G. (ed). Corn: Culture, Processing, Products. The Avi publishing Co., Inc,. USA. pp: 123-124. [ Links ]

Jane, J. L. 2006. Current understanding on starch granule structures. Jpn. Soc. Applied Glycosci. 53: 205-213. [ Links ]

Jing, P., J. A. Bomser, S. J. Schwartz, J. He, B. A. Magnuson, and M. M. Giusti. 2008. Structure−function relationships of anthocyanins from various anthocyanin-rich extracts on the inhibition of colon cancer cell growth. J. Agric. Food Chem. 56: 9391-9398. [ Links ]

Kato, T. A., C. Mapes, L. M. Mera, J. A. Serratos, and R. A. Bye. 2009. Origen y Diversificación del Maíz: Una Revisión Analítica. Universidad Nacional Autónoma de México, Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. México. D. F. 116 p. [ Links ]

Keleman, A., and J. Hellin. 2009. Specialty maize varieties in Mexico: A case study in market-driven agro-biodiversity conservation. J. Lat. Am. Geogr. 8:147-174. [ Links ]

Khan, I., A. Yousif, S. K. Johnson, and S. Gamlath. 2013. Effect of sorghum flour addition on resistant starch content, phenolic profile and antioxidant capacity of durum wheat pasta. Food Res. Int. 54: 578-586. [ Links ]

Kim, J. H., M. J. Kang, H. N. Choi, S. M. Jeong, Y. M. Lee, and J. I. Kim. 2011. Quercetin attenuates fasting and postprandial hyperglycemia in animal models of diabetes mellitus. Nutr. Res. Pract. 5: 107-111. [ Links ]

Kritchevsky, D. 1995. Epidemiology of fibre resistant starch and colorectal cancer. Eur. J. Cancer Prev. 4: 345-352. [ Links ]

Li, J., S.S. Lim, J.Y. Lee, J.K. Kim, S. W. Kang, J. L. Kim, and Y. H. Kang. 2012. Purple corn anthocyanins dampened high-glucose-induced mesangial fibrosis and inflammation: possible renoprotective role in diabetic nephropathy. J. Nutr. Biochem. 23: 320-331. [ Links ]

Liu, J., M. Wang, S. Peng, and G. Zhang. 2011. Effect of green tea catechins on the postprandial glycemic response to starches differing in amylose content. J. Agr. Food Chem. 59: 4582-4588. [ Links ]

Lo Piparo, E., H. Scheib, N. Frei, G. Williamson, M. Grigorov, and C. J. Chou. 2008. Flavonoids for controlling starch digestion: structural requirements for inhibiting human α-amylase. J. Med. Chem. 51: 3555-3561. [ Links ]

López-Martínez, L. X., K. L. Parkin, and H. S. García. 2011. Phase II-inducing, polyphenols content and antioxidant capacity of corn (Zea mays L.) from phenotypes of white, blue, red and purple colors processed into masa and tortillas. Plant Foods Hum. Nutr. 66: 41-47. [ Links ]

Lopez-Martinez, L. X., R. M. Oliart-Ros, G. Valerio-Alfaro, L. Chen-Hsien, K. L. Parkin, H. S. Garcia. 2009. Antioxidant activity, phenolic compounds and anthocyanins content of eighteen strains of Mexican maize. LWT-Food Sci. Tech. 42: 1187-1192. [ Links ]

Ludwin, D. S. 2002. The glycemic index: Physiological mechanisms relating to obesity, diabetes, and cardiovascular disease. JAMA 287: 2414-2423. [ Links ]

Mendoza-Díaz, S., M. C. Ortíz-Valerio, E. Castaño-Tostado, J. D. Figueroa Cárdenas, R. Reynoso-Camacho, M. Ramos Gómez, R. Campos-Vega, and G. F. Loarca-Piña. 2012. Antioxidant capacity and antimutagenic activity of anthocyanin and carotenoid extracts from nixtamalized pigmented creole maize races (Zea mays L.). Plant Food Hum. Nutr. 67:442-449. [ Links ]

Miao, M., H. Jiang, B. Jiang, T. Zhang, S. W. Cui, and Z. Jin. 2014. Phytonutrients for controlling starch digestion: Evaluation of grape skin extract. Food Chem. 145: 205-211. [ Links ]

Mkandawire, N. L., R. C. Kaufman, S. R. Bean, C. L. Weller, D. J. Jackson, and J. Rose. 2013. Effects of sorghum (Sorghum bicolor (L.) Moench) tannins on a amylase activity and in vitro digestibility of starch in raw and processed flours. J. Agric. Food Chem. 61: 4448-4454. [ Links ]

Montilla C. E., S. Hillebrand, A. Antezana, and P. Winterhalter. 2011. Soluble and bound phenolic compounds in different Bolivian purple corn (Zea mays L.) cultivars. J. Agric. Food Chem. 59: 7068-7074. [ Links ]

Mora-Rochin, S., J. A. Gutiérrez-Uribe, S. O. Serna-Saldivar, P. Sánchez-Peña, C. Reyes-Moreno, and J. Milán-Carrillo. 2010. Phenolic content and antioxidant activity of tortillas produced from pigmented maize processed by conventional nixtamalization or extrusion cooking. J. Cereal Sci. 52: 502-508. [ Links ]

Muir, J. G., G. P. Young, and K. O'Dea. 1994. Resistant starch impllications for health. Proc. Nutr. Soc. Austr. 18: 23-32. [ Links ]

Osorio-Díaz, P., E. Agama-Acevedo, L. A. Bello-Pérez, J. J. Islas Hernández, N. O. Gómez-Montiel, and O. Paredes-López. 2011. Effect of endosperm type on texture and in vitro starch digestibility of maize tortilla. LWT-Food Sci. Technol. 44: 611-615. [ Links ]

Ovando-Martinez, M., S. Sáyago-Ayerdi, E. Agama-Acevedo, I. Goñi, L. A. Bello-Pérez. 2009. Unripe banana flour as an ingredient to increase the undigestible carbohydrates of pasta. Food Chem. 113: 121-126. [ Links ]

Paredes-López, O., F. Guevara-Lara, and L. A. Bello-Pérez. 2006. Los Alimentos Mágicos de las Culturas Indígenas Mesoamericanas. Fondo de Cultura Económica, México. pp: 205. [ Links ]

Quirós-Sauceda, A. E., H. Palafox-Carlos, S. G. Sáyago-Ayerdi, J. F. Ayala-Zavala, L. A. Bello-Perez, E. Alvarez-Parrilla, L. A. de la Rosa, A. F González-Córdova, G. A. González-Aguilar. 2014. Dietary fiber and phenolic compounds as functional ingredients: interaction and possible effect after ingestion. Food Funct. 5:1063-1072. [ Links ]

Ramos-Escudero, F., A. M. Muñoz, C. Alvarado-Ortíz, A. Alvarado, and J. A. Yánez. 2012. Purple corn (Zea mays L.) phenolic compounds profile and its assessment as an agent against oxidative stress in isolated mouse organs. J. Med. Food 15:206-215. [ Links ]

Rojo, L. E., D. Ribnicky., S. Logendra, A. Poulev., P. Rojas-Silva, P. Kuhn, R. Dorn, M. H. Grace, M. A. Lila, and I. Raskin. 2012. In vitro and in vivo anti-diabetic effects of anthocyanins from Maqui Berry (Aristotelia chilensis). Food Chem. 131:387-96. [ Links ]

Rooney, L, and S. O. Serna-Saldívar. 2003. Food use of whole corn and dry milled fractions. In: White, J. P. and Johnson L. A (eds). Corn Chemistry and Technology. American Association of Cereal Chemists, Inc. 2nd Ed . St Paul, MN. USA. pp: 495-535. [ Links ]

Ruiz, N. A, F. Rincón Sánchez, V. M. Hernández-López, J. D. Figueroa Cárdenas, y M. G. F. Loarca Piña. 2008. Determinación de compuestos fenólicos y su actividad antioxidante en granos de maíz. Rev Fitotec Mex 31:29-31. [ Links ]

Saeed, F., I. Pasha, F. M. Anjum, and M. T. Sultan. 2011. Arabinoxylans and arabinogalactans: a comprehensive treatise. J. Food Sci. Nutr. 51:467-476. [ Links ]

Salinas, M. Y., M. Soto H, F, Martínez, B. V. González H, y R. Ortega P. 1999. Análisis de antocianinas en maíces de grano azul y rojo provenientes de cuatro razas. Rev. Fitotec. Mex. 22:161-174. [ Links ]

Salinas-Moreno, Y., F. Martínez-Bustos, M. Soto-Hernández, R. Ortega-Paczka, y J. L. Arellano-Vázquez. 2003. Efecto de la nixtamalización sobre las antocianinas de granos pigmentados. Agrociencia 37:617-628. [ Links ]

Salinas, M. Y. 2009. Uso de maíces con pigmento tipo antociano. In: De Teresa-Ochoa, A. P., y G. Viniegra-González. (comps). Temas Selectos de la Cadena Maíz-Tortilla: Un Enfoque Multidisciplinario. Universidad Autónoma Metropolitana. pp: 177-202. [ Links ]

Salinas, M. Y., J. Soria R., y E. T. Espinosa. 2010. Aprovechamiento y distribución de maíz azul en el Estado de México. Folleto Técnico 42. Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias. SAGARPA, INIFAP. pp: 50. [ Links ]

Salinas-Moreno, Y., F. J. Cruz-Chávez, S. A. Díaz-Ortiz, y F. Castillo-González. 2012a. Granos de maíces pigmentados de Chiapas, características físicas, contenido de antocianinas y valor nutracéutico. Rev. Fitotec Mex. 35: 33-41. [ Links ]

Salinas-Moreno, Y., J. J. Pérez-Alonso, G. Vázquez-Carrillo, F. Aragón Cuevas, y G. A. Velázquez-Cardelas. 2012b. Antocianinas y actividad antioxidante en maíces (Zea mays L.) de las razas Chalqueño, Elotes Cónicos y Bolita. Agrociencia 47: 815-825. [ Links ]

Salinas-Moreno, Y., F. A. Cuevas, C. Y. Moncada, J. A. Villarreal, B.A. López, y Y. E. S. Montes. 2013. Caracterización física y composición química de razas de maíz de grano azul/morado de las regiones tropicales y subtropicales de Oaxaca. Rev. Fitotec Mex. 36(1): 23-31. [ Links ]

Salinas-Moreno, Y., C. García-Salinas, B. Coutiño-Estrada, y V. A. Vidal-Martínez. 2013. Variabilidad en contenido tipos de antocianinas en granos de color azul/morado de poblaciones mexicanas de maíz. Rev. Fitotec. Mex. 36:185-294. [ Links ]

Sánchez, J. J., M. M. Goodman, and C. W. Stuber. 2000 Isozymatic and morphological diversity in the races of maize of Mexico. Econ. Bot. 54: 43-59. [ Links ]

Saura-Calixto F. 2012. Concept and health-related properties of nonextractable polyphenols: the missing dietary polyphenols. J. Agric. Food Chem. 60: 11195-11200. [ Links ]

Seal, C. J., M. E. Daly, L. C. Thomas, W. Ball, A. M. Birkett, and R. Jeffcoat. 2003. Postprandial carbohydrates metabolism in healthy subjects and those with type 2 diabetes with a slow and rapid hydrolysis rate determined in vitro. Br. J. Nutr. 90: 853-864. [ Links ]

Serna-Saldivar, S.O. 2010. Physical properties, grading, and specialty grains: In: Cereal Grains Properties, Processing and Nutritional Attributes. CRC Press. Boca Raton FL. 752 p. [ Links ]

SIAP, Servicio de Información Agroalimentaria y Pesquera. 2013. Estadística Básica Agrícola, Anuario 2013. www.siap.gob.mx (Consulta: Agosto 2013). [ Links ]

Singh, N, S. Singh, and K. Shevkani. 2011. Maize: Composition, bioactive constituents,and unleavened bread. In: Preedy, V. J., W. R. Ross, and P. V. Patel (eds). Flour and Breads and Their Fortification in Health and Disease Prevention. Elsevier Inc. California, USA. pp: 89-95. [ Links ]

Strack, D, and V. Wray. 1989. Anthocyanins. In: Harbone H. B. (ed). Methods in Plant Biochemistry, Plant Phenolics. Academic Press, New York. pp: 325-356. [ Links ]

Sun-Waterhouse, D, D. Jin, and G. I. N. Waterhouse. 2013. Effect of adding elderberry juice concentrate on the quality attributes, polyphenol contents and antioxidant activity of three fibre-enriched pastas. Food. Res. Int. 54: 781-789. [ Links ]

Urias-Lugo. D. A., J. B. Heredia, M. D. Muy-Rangel, J. B. Valdez-Torres, S. O. Serna-Saldívar, and J.A. Gutiérrez-Uribe. 2015. Anthocyanins and phenolic acids of hybrid and native blue maize (Zea mays L.) extracts and their antiproliferative activity in mammary (MCF7), liver (HepG2), colon (Caco2 and HT29) and prostate (PC3) Cancer Cells. Plant Foods Hum. Nutr. 70:193-199. [ Links ]

Urias-Peraldí, M., J. A. Gutiérrez-Utibe, R. E. Preciado-Ortiz, A. S. Cruz-Morales, S. O. Serna-Saldívar, and S. García-Lara, S. 2013. Nutraceutical profiles of improved blue maize (Zea mays) hybrids for subtropical regions. Field Crops Res. 141: 69-76. [ Links ]

Vitaglione, P., A. Napolitano, V. and Fogliano. 2008. Cereal dietary fibre: A natural functional ingredient to deliver phenolic compounds into the gut. Trends Food Sci. Tech. 19: 451-463. [ Links ]

Utrilla-Coello, R. G., E. Agama-Acevedo, A. P. Barba de la Rosa, J. L. Martínez-Salgado, S. L. Rodríguez-Ambriz, and L. A. Bello-Pérez, 2009. Blue maize: Morphology and starch synthase characterization of starch granule. Plant Foods Hum. Nutr. 64: 18-24. [ Links ]

Utrilla-Coello, R. G., E. Agama-Acevedo, A. P. Barba de la Rosa, S. L. Rodriguez-Ambriz, and L. A. Bello-Pérez. 2010. Physicochemical and enzyme characterization of small and large starch granules isolated from two maize cultivars. Cereal Chem. 1:50-56. [ Links ]

Utrilla-Coello, R.G., E. Agama-Acevedo, P. Osorio-Díaz, J. Tovar, and L.A. Bello-Pérez. 2011. Composition and starch digestibility of whole grain bars containing maize or unripe banana flours. Starch - Stärke 63:416-423 [ Links ]

Wedick N.M., A. Pan, A. Cassidy, E. B. Rimm, L. Sampson, B. Rosner, W. Willett, F.B. Hu, Q. Sun, and R.M. van Dam. 2012. Dietary flavonoid intakes and risk of type 2 diabetes in US men and women. Am. J. Clin. Nutr. 95:925-933. [ Links ]

Wellhausen, E. J., L. M. Roberts, E. Hernández, y P. C. Mangelsdorf. 1951. Razas de maíz en México. Su origen, características y distribución. In: Xolocotzia. Obras de Efraín Hernández Xolocotzi. Revista de Geografía Agrícola. Tomo II Universidad Autónoma de Chapingo. pp: 609-732. [ Links ]

Yoon, J. H., L. U. Thompson, and D. J. A. Jenkins. 1983. The effect of phytic acid on in vitro rate of starch digestibility and blood glucose response. Am. J. Clin. Nutr. 38: 835-842. [ Links ]

Yoshimoto, M., S. Okuno, T. Kumagi, M. Yoshinaga, and O. Yamakawa,. 1999. Distribution of antimutagenic components in colored sweet potatoes. Jpn. Agr. Res. Q. 33: 143-148. [ Links ]

Zhao, X., M. Corrales, C. Zhang, X. Hu, Y. Ma, and B. Tauscher. 2008. Composition and thermal stability of anthocyanins from Chinese purple corn (Zea mays L.). J. Agric. Food Chem. 56: 10761-10766. [ Links ]

Zhao, X, C. Zhang, C. Guigas, Y. Ma, M. Corrales, B. Tauscher, and X. Hu. 2009. Composition, antimicrobial activity and antiproliferative capacity of anthocyanin extracts of purple corn (Zea mays L.) from China. Eur. Food Res. Technol. 228:759-765. [ Links ]

Zhu, Y, W. Ling, H. Guo, F. Song, Q. Ye, T. Zou, D. Li, Y. Zhang, G. Li, Y. Xiao, F. Liu, Z. Li, Z. Shi, and Y. Zhang 2013. Anti-inflammatory effect of purified dietary anthocyanins in adult with hypercholesterolemic: A randomized controlled trial. Nutr. Metab. Cardiovas 23:842-849. [ Links ]

Zilic, S., A. Serpen, G. Akilloglu, V. Gökmen, and J. Vancetovic. 2012. Phenolic compounds, carotenoids, anthocyanins, and antioxidant capacity of colored maize (Zea mays L.) kernels. J. Agric. Food Chem. 60:1224-1231. [ Links ]

Received: September 2015; Accepted: March 2016

Creative Commons License Este es un artículo publicado en acceso abierto bajo una licencia Creative Commons